The Cochlear Matrisome: Importance in Hearing and Deafness.

[en] The extracellular matrix (ECM) consists in a complex meshwork of collagens, glycoproteins, and proteoglycans, which serves a scaffolding function and provides viscoelastic properties to the tissues. ECM acts as a biomechanical support, and actively participates in cell signaling to induce tissular changes in response to environmental forces and soluble cues. Given the remarkable complexity of the inner ear architecture, its exquisite structure-function relationship, and the importance of vibration-induced stimulation of its sensory cells, ECM is instrumental to hearing. Many factors of the matrisome are involved in cochlea development, function and maintenance, as evidenced by the variety of ECM proteins associated with hereditary deafness. This review describes the structural and functional ECM components in the auditory organ and how they are modulated over time and following injury.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Pressé, Mary ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Developmental Neurobiology

Malgrange, Brigitte ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie

Delacroix, Laurence ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques

Language :

English

Title :

The Cochlear Matrisome: Importance in Hearing and Deafness.

Publication date :

07 December 2023

Journal title :

Matrix Biology: Journal of the International Society for Matrix Biology

ISSN :

0945-053X

eISSN :

1569-1802

Publisher :

Elsevier B.V., Netherlands

Volume :

125

Pages :

40 - 58

Peer reviewed :

Peer reviewed

Additional URL :

https://api.elsevier.com/content/article/PII:S0945053X23001257?httpAccept=text/xml

Funding text :

This work was supported by grants from the Belgian National Funds for Scientifc Research (FRS-FNRS, Belgium), the Fondation Léon Fredericq, and the Fonds spéciaux (ULiège, Belgium).

Available on ORBi :

since 30 January 2024

Statistics

Number of views

114 (9 by ULiège)

Number of downloads

135 (7 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenAlex citations

Bibliography

Karamanos, N.K., Theocharis, A.D., Piperigkou, Z., Manou, D., Passi, A., Skandalis, S.S., Vynios, D.H., Orian-Rousseau, V., Ricard-Blum, S., Schmelzer, C.E.H., Duca, L., Durbeej, M., Afratis, N.A., Troeberg, L., Franchi, M., Masola, V., Onisto, M., A guide to the composition and functions of the extracellular matrix. FEBS J. 288 (2021), 6850–6912, 10.1111/febs.15776.
Kalluri, R., Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3 (2003), 422–433, 10.1038/nrc1094.
Kechagia, J.Z., Ivaska, J., Roca-Cusachs, P., Integrins as biomechanical sensors of the microenvironment. Nat. Rev. Mol. Cell Biol. 20 (2019), 457–473, 10.1038/s41580-019-0134-2.
Kanchanawong, P., Calderwood, D.A., Organization, dynamics and mechanoregulation of integrin-mediated cell–ECM adhesions. Nat. Rev. Mol. Cell Biol. 24 (2023), 142–161, 10.1038/s41580-022-00531-5.
Muncie, J.M., Weaver, V.M., The physical and biochemical properties of the extracellular matrix regulate cell fate. Current Topics in Developmental Biology, 2018, Elsevier, 1–37, 10.1016/bs.ctdb.2018.02.002.
Dzamba, B.J., DeSimone, D.W., Extracellular matrix (ECM) and the sculpting of embryonic tissues. Current Topics in Developmental Biology, 2018, Elsevier, 245–274, 10.1016/bs.ctdb.2018.03.006.
Sorokin, L., The impact of the extracellular matrix on inflammation. Nat. Rev. Immunol. 10 (2010), 712–723, 10.1038/nri2852.
Karampoga, A., Tzaferi, K., Koutsakis, C., Kyriakopoulou, K., Karamanos, N.K., Exosomes and the extracellular matrix: a dynamic interplay in cancer progression. Int. J. Dev. Biol. 66 (2022), 97–102, 10.1387/ijdb.210120nk.
Al Halawani, A., Mithieux, S.M., Yeo, G.C., Hosseini-Beheshti, E., Weiss, A.S., Extracellular vesicles: interplay with the extracellular matrix and modulated cell responses. Int. J. Mol. Sci., 23, 2022, 3389, 10.3390/ijms23063389.
Naba, A., Clauser, K.R., Hoersch, S., Liu, H., Carr, S.A., Hynes, R.O., The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol. Cell. Proteom., 11, 2012, M111.014647, 10.1074/mcp.M111.014647.
Naba, A., Clauser, K.R., Ding, H., Whittaker, C.A., Carr, S.A., Hynes, R.O., The extracellular matrix: tools and insights for the “omics” era. Matrix Biol. 49 (2016), 10–24, 10.1016/j.matbio.2015.06.003.
Basch, M.L., Brown, R.M., Jen, H.I., Groves, A.K., Where hearing starts: the development of the mammalian cochlea. J. Anat. 228 (2016), 233–254, 10.1111/joa.12314.
Delmaghani, S., El-Amraoui, A., Inner ear gene therapies take off: current promises and future challenges. JCM, 9, 2020, 2309, 10.3390/jcm9072309.
Santi, P.A., Johnson, S.B., Decellularized ear tissues as scaffolds for stem cell differentiation. JARO 14 (2013), 3–15, 10.1007/s10162-012-0355-y.
Santi, P.A., Aldaya, R., Brown, A., Johnson, S., Stromback, T., Cureoglu, S., Rask-Andersen, H., Scanning electron microscopic examination of the extracellular matrix in the decellularized mouse and human cochlea. JARO 17 (2016), 159–171, 10.1007/s10162-016-0562-z.
Liu, W., Atturo, F., Aldaya, R., Santi, P., Cureoglu, S., Obwegeser, S., Glueckert, R., Pfaller, K., Schrott-Fischer, A., Rask-Andersen, H., Macromolecular organization and fine structure of the human basilar membrane - RELEVANCE for cochlear implantation. Cell Tissue Res. 360 (2015), 245–262, 10.1007/s00441-014-2098-z.
Tsuprun, V., Santi, P., Proteoglycan arrays in the cochlear basement membrane. Hear. Res. 157 (2001), 65–76, 10.1016/S0378-5955(01)00278-7.
Ishiyama, A., Mowry, S.E., Lopez, I.A., Ishiyama, G., Immunohistochemical distribution of basement membrane proteins in the human inner ear from older subjects. Hear. Res. 254 (2009), 1–14, 10.1016/j.heares.2009.03.014.
Satoh, H., Kawasaki, K., Kihara, I., Nakano, Y., Importance of type IV collagen, laminin, and heparan sulfate proteoglycan in the regulation of labyrinthine fluid in the rat cochlear duct. Eur. Arch. Otorhinolaryngol. 255 (1998), 285–288, 10.1007/s004050050060.
Kwiatkowska, M., Reinhard, J., Roll, L., Kraft, N., Dazert, S., Faissner, A., Volkenstein, S., The expression pattern and inhibitory influence of Tenascin-C on the growth of spiral ganglion neurons suggest a regulatory role as boundary formation molecule in the postnatal mouse inner ear. Neuroscience 319 (2016), 46–58, 10.1016/j.neuroscience.2016.01.039.
Zhao, Y., Zhao, F., Zong, L., Zhang, P., Guan, L., Zhang, J., Wang, D., Wang, J., Chai, W., Lan, L., Li, Q., Han, B., Yang, L., Jin, X., Yang, W., Hu, X., Wang, X., Li, N., Li, Y., Petit, C., Wang, J., Wang, H.Y.J., Wang, Q., Exome sequencing and linkage analysis identified Tenascin-C (TNC) as a novel causative gene in nonsyndromic hearing loss. PLoS ONE, 8, 2013, e69549, 10.1371/journal.pone.0069549.
Imanaka-Yoshida, K., Tawara, I., Yoshida, T., Tenascin-C in cardiac disease: a sophisticated controller of inflammation, repair, and fibrosis. Am. J. Physiol. Cell Physiol. 319 (2020), C781–C796, 10.1152/ajpcell.00353.2020.
Warchol, M.E., Speck, J.D., Expression of GATA3 and tenascin in the avian vestibular maculae: normative patterns and changes during sensory regeneration. J. Comp. Neurol. 500 (2007), 646–657, 10.1002/cne.21153.
Thalmann, I., Collagen of accessory structures of organ of corti. Connect. Tissue Res. 29 (1993), 191–201, 10.3109/03008209309016826.
Tsuprun, V., Santi, P., Ultrastructure and immunohistochemical identification of the extracellular matrix of the chinchilla cochlea. Hear. Res. 129 (1999), 35–49, 10.1016/S0378-5955(98)00219-6.
Amma, L.L., Goodyear, R., Faris, J.S., Jones, I., Ng, L., Richardson, G., Forrest, D., An emilin family extracellular matrix protein identified in the cochlear basilar membrane. Mol. Cell. Neurosci. 23 (2003), 460–472, 10.1016/S1044-7431(03)00075-7.
Russell, I.J., Lukashkina, V.A., Levic, S., Cho, Y.W., Lukashkin, A.N., Ng, L., Forrest, D., Emilin 2 promotes the mechanical gradient of the cochlear basilar membrane and resolution of frequencies in sound. Sci. Adv., 6, 2020, eaba2634, 10.1126/sciadv.aba2634.
Sellon, J.B., Ghaffari, R., Freeman, D.M., The tectorial membrane: mechanical properties and functions. Cold Spring Harb. Perspect. Med., 9, 2019, a033514, 10.1101/cshperspect.a033514.
Hasko, J.A., Richardson, G.P., The ultrastructural organization and properties of the mouse tectorial membrane matrix. Hear. Res. 35 (1988), 21–38, 10.1016/0378-5955(88)90037-8.
Slepecky, N.B., Cefaratti, L.K., Yoo, T.J., Type II and Type IX collagen form heterotypic fibers in the tectorial membrane of the inner ear. Matrix 12 (1992), 80–86, 10.1016/S0934-8832(11)80108-3.
Richardson, G.P., Russell, I.J., Duance, V.C., Bailey, A.J., Polypeptide composition of the mammalian tectorial membrane. Hear. Res. 25 (1987), 45–60, 10.1016/0378-5955(87)90078-5.
Thalmann, I., Thallinger, G., Comegys, T.H., Thalmann, R., Collagen – the predominant protein of the tectorial membrane. ORL 48 (1986), 107–115, 10.1159/000275855.
Lim, D.J., Fine morphology of the tectorial membrane: its relationship to the organ of Corti. Arch. Otolaryngol. Head Neck Surg. 96 (1972), 199–215, 10.1001/archotol.1972.00770090321001.
Asamura, K., Abe, S., Imamura, Y., Aszodi, A., Suzuki, N., Hashimoto, S., Takumi, Y., Hayashi, T., Fässler, R., Nakamura, Y., Usami, S., Type IX collagen is crucial for normal hearing. Neuroscience 132 (2005), 493–500, 10.1016/j.neuroscience.2005.01.013.
McGuirt, W.T., Prasad, S.D., Griffith, A.J., Kunst, H.P.M., Green, G.E., Shpargel, K.B., Runge, C., Huybrechts, C., Mueller, R.F., Lynch, E., King, M.C., Brunner, H.G., Cremers, C.W.R.J., Takanosu, M., Li, S.W., Arita, M., Mayne, R., Prockop, D.J., Camp, G.V., Smith, R.J.H., Mutations in COL11A2 cause non-syndromic hearing loss (DFNA13). Nat. Genet. 23 (1999), 413–419, 10.1038/70516.
Masaki, K., Gu, J.W., Ghaffari, R., Chan, G., Smith, R.J.H., Freeman, D.M., Aranyosi, A.J., Col11a2 deletion reveals the molecular basis for tectorial membrane mechanical anisotropy. Biophys. J. 96 (2009), 4717–4724, 10.1016/j.bpj.2009.02.056.
Legan, P.K., Lukashkina, V.A., Goodyear, R.J., Kössl, M., Russell, I.J., Richardson, G.P., A targeted deletion in α-tectorin reveals that the tectorial membrane is required for the gain and timing of cochlear feedback. Neuron 28 (2000), 273–285, 10.1016/S0896-6273(00)00102-1.
Russell, I.J., Legan, P.K., Lukashkina, V.A., Lukashkin, A.N., Goodyear, R.J., Richardson, G.P., Sharpened cochlear tuning in a mouse with a genetically modified tectorial membrane. Nat. Neurosci. 10 (2007), 215–223, 10.1038/nn1828.
Cheatham, M.A., Goodyear, R.J., Homma, K., Legan, P.K., Korchagina, J., Naskar, S., Siegel, J.H., Dallos, P., Zheng, J., Richardson, G.P., Loss of the tectorial membrane protein CEACAM16 enhances spontaneous, stimulus-frequency, and transiently evoked otoacoustic emissions. J. Neurosci. 34 (2014), 10325–10338, 10.1523/JNEUROSCI.1256-14.2014.
Kim, D.K., Kim, J.A., Park, J., Niazi, A., Almishaal, A., Park, S., The release of surface-anchored α-tectorin, an apical extracellular matrix protein, mediates tectorial membrane organization. Sci. Adv., 5, 2019, eaay6300, 10.1126/sciadv.aay6300.
Jones, G.P., Elliott, S.J., Russell, I.J., Lukashkin, A.N., Modified protein expression in the tectorial membrane of the cochlea reveals roles for the striated sheet matrix. Biophys. J. 108 (2015), 203–210, 10.1016/j.bpj.2014.11.1854.
Jones, G.P., Lukashkina, V.A., Russell, I.J., Elliott, S.J., Lukashkin, A.N., Frequency-dependent properties of the tectorial membrane facilitate energy transmission and amplification in the cochlea. Biophys. J. 104 (2013), 1357–1366, 10.1016/j.bpj.2013.02.002.
Goodyear, R.J., Cheatham, M.A., Naskar, S., Zhou, Y., Osgood, R.T., Zheng, J., Richardson, G.P., Accelerated age-related degradation of the tectorial membrane in the ceacam16βgal/βgal null mutant mouse, a model for late-onset human hereditary deafness DFNB113. Front. Mol. Neurosci., 12, 2019, 147, 10.3389/fnmol.2019.00147.
Zwaenepoel, I., Mustapha, M., Leibovici, M., Verpy, E., Goodyear, R., Liu, X.Z., Nouaille, S., Nance, W.E., Kanaan, M., Avraham, K.B., Tekaia, F., Loiselet, J., Lathrop, M., Richardson, G., Petit, C., Otoancorin, an inner ear protein restricted to the interface between the apical surface of sensory epithelia and their overlying acellular gels, is defective in autosomal recessive deafness DFNB22. Proc. Natl. Acad. Sci. USA 99 (2002), 6240–6245, 10.1073/pnas.082515999.
Lukashkin, A.N., Legan, P.K., Weddell, T.D., Lukashkina, V.A., Goodyear, R.J., Welstead, L.J., Petit, C., Russell, I.J., Richardson, G.P., A mouse model for human deafness DFNB22 reveals that hearing impairment is due to a loss of inner hair cell stimulation. Proc. Natl. Acad. Sci. USA 109 (2012), 19351–19356, 10.1073/pnas.1210159109.
Verpy, E., Masmoudi, S., Zwaenepoel, I., Leibovici, M., Hutchin, T.P., Del Castillo, I., Nouaille, S., Blanchard, S., Lainé, S., Popot, J.L., Moreno, F., Mueller, R.F., Petit, C., Mutations in a new gene encoding a protein of the hair bundle cause non-syndromic deafness at the DFNB16 locus. Nat. Genet. 29 (2001), 345–349, 10.1038/ng726.
Verpy, E., Weil, D., Leibovici, M., Goodyear, R.J., Hamard, G., Houdon, C., Lefèvre, G.M., Hardelin, J.P., Richardson, G.P., Avan, P., Petit, C., Stereocilin-deficient mice reveal the origin of cochlear waveform distortions. Nature 456 (2008), 255–258, 10.1038/nature07380.
Verpy, E., Leibovici, M., Michalski, N., Goodyear, R.J., Houdon, C., Weil, D., Richardson, G.P., Petit, C., Stereocilin connects outer hair cell stereocilia to one another and to the tectorial membrane. J. Comp. Neurol. 519 (2011), 194–210, 10.1002/cne.22509.
Avan, P., Gal, S.Le, Michel, V., Dupont, T., Hardelin, J.P., Petit, C., Verpy, E., Otogelin, otogelin-like, and stereocilin form links connecting outer hair cell stereocilia to each other and the tectorial membrane. Proc. Natl. Acad. Sci. USA 116 (2019), 25948–25957, 10.1073/pnas.1902781116.
El-Amraoui, A., Cohen-Salmon, M., Petit, C., Simmler, M.C., Spatiotemporal expression of otogelin in the developing and adult mouse inner ear. Hear. Res. 158 (2001), 151–159, 10.1016/S0378-5955(01)00312-4.
Cohen-Salmon, M., El-Amraoui, A., Leibovici, M., Petit, C., Otogelin: a glycoprotein specific to the acellular membranes of the inner ear. Proc. Natl. Acad. Sci. USA 94 (1997), 14450–14455, 10.1073/pnas.94.26.14450.
Simmler, M.C., Cohen-Salmon, M., El-Amraoui, A., Guillaud, L., Benichou, J.C., Petit, C., Panthier, J.J., Targeted disruption of Otog results in deafness and severe imbalance. Nat. Genet. 24 (2000), 139–143, 10.1038/72793.
Strimbu, C.E., Prasad, S., Hakizimana, P., Fridberger, A., Control of hearing sensitivity by tectorial membrane calcium. Proc. Natl. Acad. Sci. USA 116 (2019), 5756–5764, 10.1073/pnas.1805223116.
Ceriani, F., Mammano, F., Calcium signaling in the cochlea – molecular mechanisms and physiopathological implications. Cell Commun. Signal., 10, 2012, 20, 10.1186/1478-811X-10-20.
Sotomayor, M., Weihofen, W.A., Gaudet, R., Corey, D.P., Structural determinants of Cadherin-23 function in hearing and deafness. Neuron 66 (2010), 85–100, 10.1016/j.neuron.2010.03.028.
Jeng, J., Harasztosi, C., Carlton, A.J., Corns, L.F., Marchetta, P., Johnson, S.L., Goodyear, R.J., Legan, K.P., Rüttiger, L., Richardson, G.P., Marcotti, W., MET currents and otoacoustic emissions from mice with a detached tectorial membrane indicate the extracellular matrix regulates Ca 2+ near stereocilia. J. Physiol. 599 (2021), 2015–2036, 10.1113/JP280905.
Kammerer, R., Rüttiger, L., Riesenberg, R., Schäuble, C., Krupar, R., Kamp, A., Sunami, K., Eisenried, A., Hennenberg, M., Grunert, F., Bress, A., Battaglia, S., Schrewe, H., Knipper, M., Schneider, M.R., Zimmermann, W., Loss of mammal-specific tectorial membrane component carcinoembryonic antigen cell adhesion molecule 16 (CEACAM16) leads to hearing impairment at low and high frequencies. J. Biol. Chem. 287 (2012), 21584–21598, 10.1074/jbc.M111.320481.
Trowe, M.O., Maier, H., Schweizer, M., Kispert, A., Deafness in mice lacking the T-box transcription factor Tbx18 in otic fibrocytes. Development 135 (2008), 1725–1734, 10.1242/dev.014043.
Peeleman, N., Verdoodt, D., Ponsaerts, P., Van Rompaey, V., On the role of fibrocytes and the extracellular matrix in the physiology and pathophysiology of the spiral ligament. Front. Neurol., 11, 2020, 580639, 10.3389/fneur.2020.580639.
Slepecky, N.B., Savage, J.E., Yoo, T.J., Localization of Type II, IX and V collagen in the inner ear. Acta Otolaryngol. 112 (1992), 611–617, 10.3109/00016489209137449.
Sonntag, M., Blosa, M., Schmidt, S., Reimann, K., Blum, K., Eckrich, T., Seeger, G., Hecker, D., Schick, B., Arendt, T., Engel, J., Morawski, M., Synaptic coupling of inner ear sensory cells is controlled by brevican-based extracellular matrix baskets resembling perineuronal nets. BMC Biol., 16, 2018, 99, 10.1186/s12915-018-0566-8.
Ikezono, T., Omori, A., Ichinose, S., Pawankar, R., Watanabe, A., Yagi, T., Identification of the protein product of the Coch gene (hereditary deafness gene) as the major component of bovine inner ear protein. Biochim. Biophys. Acta (BBA) Mol. Basis Dis. 1535 (2001), 258–265, 10.1016/S0925-4439(00)00101-0.
Makishima, T., Rodriguez, C.I., Robertson, N.G., Morton, C.C., Stewart, C.L., Griffith, A.J., Targeted disruption of mouse Coch provides functional evidence that DFNA9 hearing loss is not a COCH haploinsufficiency disorder. Hum. Genet. 118 (2005), 29–34, 10.1007/s00439-005-0001-4.
Jung, J., Yoo, J.E., Choe, Y.H., Park, S.C., Lee, H.J., Lee, H.J., Noh, B., Kim, S.H., Kang, G.Y., Lee, K.M., Yoon, S.S., Jang, D.S., Yoon, J.H., Hyun, Y.M., Choi, J.Y., Cleaved cochlin sequesters pseudomonas aeruginosa and activates innate immunity in the inner ear. Cell Host Microbe 25 (2019), 513–525.e6, 10.1016/j.chom.2019.02.001.
Verdoodt, D., Van Camp, G., Ponsaerts, P., Van Rompaey, V., On the pathophysiology of DFNA9: effect of pathogenic variants in the COCH gene on inner ear functioning in human and transgenic mice. Hear. Res., 401, 2021, 108162, 10.1016/j.heares.2020.108162.
Mizuta, K., Ikezono, T., Iwasaki, S., Arai, M., Hashimoto, Y., Pawankar, R., Watanabe, T., Shindo, S., Mineta, H., Ultrastructural co-localization of cochlin and type II collagen in the rat semicircular canal. Neurosci. Lett. 434 (2008), 104–107, 10.1016/j.neulet.2008.01.036.
Nagy, I., Trexler, M., Patthy, L., The second von Willebrand type A domain of cochlin has high affinity for type I, type II and type IV collagens. FEBS Lett. 582 (2008), 4003–4007, 10.1016/j.febslet.2008.10.050.
Nyberg, S., Abbott, N.J., Shi, X., Steyger, P.S., Dabdoub, A., Delivery of therapeutics to the inner ear: the challenge of the blood-labyrinth barrier. Sci. Transl. Med., 11, 2019, eaao0935, 10.1126/scitranslmed.aao0935.
Kikuchi, K., Hilding, D.A., The development of the stria vascularis in the mouse. Acta Otolaryngol. 62 (1966), 277–291, 10.3109/00016486609119573.
Takahashi, M., Hokunan, K., Localization of Type IV collagen and laminin in the guinea pig inner ear. Ann. Otol. Rhinol. Laryngol. 101 (1992), 58–62, 10.1177/0003489492101S1012.
Yamashita, H., Bagger-Sjöbäck, D., Wersäll, J., The presence of laminin in the fetal human inner ear. Eur. Arch. Otorhinolaryngol. 248 (1991), 479–482, 10.1007/BF00627638.
Torihara, K., Suganuma, T., Ide, S., Morimitsu, T., Anionic sites in blood capillaries of the mouse cochlear duct. Hear. Res. 77 (1994), 69–74, 10.1016/0378-5955(94)90253-4.
Mochizuki, T., Lemmink, H.H., Mariyama, M., Antignac, C., Gubler, M.C., Pirson, Y., Verellen-Dumoulin, C., Chan, B., Schröder, C.H., Smeets, H.J., Reeders, S.T., Identification of mutations in the α3(IV) and α4(IV) collagen genes in autosomal recessive Alport syndrome. Nat. Genet. 8 (1994), 77–82, 10.1038/ng0994-77.
Barker, D.F., Hostikka, S.L., Zhou, J., Chow, L.T., Oliphant, A.R., Gerken, S.C., Gregory, M.C., Skolnick, M.H., Atkin, C.L., Tryggvason, K., Identification of mutations in the COL4A5 collagen gene in alport syndrome. Science 248 (1990), 1224–1227, 10.1126/science.2349482.
Cosgrove, D., Samuelson, G., Meehan, D.T., Miller, C., McGee, J., Walsh, E.J., Siegel, M., Ultrastructural, physiological, and molecular defects in the inner ear of a gene-knockout mouse model for autosomal Alport syndrome. Hear. Res. 121 (1998), 84–98, 10.1016/S0378-5955(98)00069-0.
Dufek, B., Meehan, D.T., Delimont, D., Wilhelm, K., Samuelson, G., Coenen, R., Madison, J., Doyle, E., Smyth, B., Phillips, G., Gratton, M.A., Cosgrove, D., RNA-seq analysis of gene expression profiles in isolated stria vascularis from wild-type and Alport mice reveals key pathways underling Alport strial pathogenesis. PLoS ONE, 15, 2020, e0237907, 10.1371/journal.pone.0237907.
Meehan, D.T., Delimont, D., Dufek, B., Zallocchi, M., Phillips, G., Gratton, M.A., Cosgrove, D., Endothelin-1 mediated induction of extracellular matrix genes in strial marginal cells underlies strial pathology in Alport mice. Hear. Res. 341 (2016), 100–108, 10.1016/j.heares.2016.08.003.
Liu, W., Edin, F., Atturo, F., Rieger, G., Löwenheim, H., Senn, P., Blumer, M., Schrott-Fischer, A., Rask-Andersen, H., Glueckert, R., The pre- and post-somatic segments of the human type I spiral ganglion neurons – structural and functional considerations related to cochlear implantation. Neuroscience 284 (2015), 470–482, 10.1016/j.neuroscience.2014.09.059.
Vitellaro-Zuccarello, L., De Biasi, S., Spreafico, R., One hundred years of Golgi's “perineuronal net”: history of a denied structure. Ital. J. Neurol. Sci. 19 (1998), 249–253, 10.1007/BF02427613.
Fawcett, J.W., Oohashi, T., Pizzorusso, T., The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function. Nat. Rev. Neurosci. 20 (2019), 451–465, 10.1038/s41583-019-0196-3.
Reichelt, A.C., Hare, D.J., Bussey, T.J., Saksida, L.M., Perineuronal nets: plasticity, protection, and therapeutic potential. Trends Neurosci. 42 (2019), 458–470, 10.1016/j.tins.2019.04.003.
Richardson, T.L., Ishiyama, E., Keels, E.W., Submicroscopic studies of the round window membrane. Acta Otolaryngol. 71 (1971), 9–21, 10.3109/00016487109125327.
Carpenter, A.M., Muchow, D., Goycoolea, M.V., Ultrastructural studies of the human round window membrane. Arch. Otolaryngol. Head Neck Surg. 115 (1989), 585–590, 10.1001/archotol.1989.01860290043012.
Ahmed, M., More, Y.I., Basha, S.I., Bilateral oval and round window atresia on CT temporal bone: a rare anomaly clinically mimicking otosclerosis in an adult. Case Rep. Radiol., 2019, 2019, 7457603, 10.1155/2019/7457603.
Choo, Y.B., Microscopic characteristics of round window problems in otology. Laryngoscope 94 (1984), 1–9, 10.1002/lary.5540940101.
Benson, J.C., Diehn, F., Passe, T., Guerin, J., Silvera, V.M., Carlson, M.L., Lane, J., The forgotten second window: a pictorial review of round window pathologies. Am. J. Neuroradiol. 41 (2020), 192–199, 10.3174/ajnr.A6356.
Pillers, D.A.M., Kempton, J.B., Duncan, N.M., Pang, J., Dwinnell, S.J., Trune, D.R., Hearing loss in the laminin-deficient dy mouse model of congenital muscular dystrophy. Mol. Genet. Metab. 76 (2002), 217–224, 10.1016/S1096-7192(02)00039-2.
Meyer Zum Gottesberge, A.M., Gross, O., Becker-Lendzian, U., Massing, T., Vogel, W.F., Inner ear defects and hearing loss in mice lacking the collagen receptor DDR1. Lab. Investig. 88 (2008), 27–37, 10.1038/labinvest.3700692.
Chen, A.H., Ni, L., Fukushima, K., Marietta, J., O'Neill, M., Coucke, P., Willems, P., Smith, R.J.H., Linkage of a gene for dominant non-syndromic deafness to chromosome 19. Hum. Mol. Genet. 4 (1995), 1073–1076, 10.1093/hmg/4.6.1073.
Zheng, J., Miller, K.K., Yang, T., Hildebrand, M.S., Shearer, A.E., DeLuca, A.P., Scheetz, T.E., Drummond, J., Scherer, S.E., Legan, P.K., Goodyear, R.J., Richardson, G.P., Cheatham, M.A., Smith, R.J., Dallos, P., Carcinoembryonic antigen-related cell adhesion molecule 16 interacts with α-tectorin and is mutated in autosomal dominant hearing loss (DFNA4). Proc. Natl. Acad. Sci. USA 108 (2011), 4218–4223, 10.1073/pnas.1005842108.
Wang, H., Wang, X., He, C., Li, H., Qing, J., Grati, M., Hu, Z., Li, J., Hu, Y., Xia, K., Mei, L., Wang, X., Yu, J., Chen, H., Jiang, L., Liu, Y., Men, M., Zhang, H., Guan, L., Xiao, J., Zhang, J., Liu, X., Feng, Y., Exome sequencing identifies a novel CEACAM16 mutation associated with autosomal dominant nonsyndromic hearing loss DFNA4B in a Chinese family. J. Hum. Genet. 60 (2015), 119–126, 10.1038/jhg.2014.114.
Booth, K.T., Kahrizi, K., Najmabadi, H., Azaiez, H., Smith, R.J., Old gene, new phenotype: splice-altering variants in CEACAM16 cause recessive non-syndromic hearing impairment. J. Med. Genet. 55 (2018), 555–560, 10.1136/jmedgenet-2018-105349.
Dias, A.M.M., Lezirovitz, K., Nicastro, F.S., Mendes, B.C.A., Mingroni-Netto, R.C., Further evidence for loss-of-function mutations in the CEACAM16 gene causing nonsyndromic autosomal recessive hearing loss in humans. J. Hum. Genet. 64 (2019), 257–260, 10.1038/s10038-018-0546-4.
Robertson, N.G., Lu, L., Heller, S., Merchant, S.N., Eavey, R.D., McKenna, M., Nadol, J.B., Miyamoto, R.T., Linthicum, F.H., Lubianca Neto, J.F., Hudspeth, A.J., Seidman, C.E., Morton, C.C., Seidman, J.G., Mutations in a novel cochlear gene cause DFNA9, a human nonsyndromic deafness with vestibular dysfunction. Nat. Genet. 20 (1998), 299–303, 10.1038/3118.
Usami, S., Takahashi, K., Yuge, I., Ohtsuka, A., Namba, A., Abe, S., Fransen, E., Patthy, L., Otting, G., Van Camp, G., Mutations in the COCH gene are a frequent cause of autosomal dominant progressive cochleo-vestibular dysfunction, but not of Meniere's disease. Eur. J. Hum. Genet. 11 (2003), 744–748, 10.1038/sj.ejhg.5201043.
Street, V.A., Kallman, J.C., Robertson, N.G., Kuo, S.F., Morton, C.C., Phillips, J.O., A novel DFNA9 mutation in the vWFA2 domain of COCH alters a conserved cysteine residue and intrachain disulfide bond formation resulting in progressive hearing loss and site-specific vestibular and central oculomotor dysfunction. Am. J. Med. Genet. 139A (2005), 86–95, 10.1002/ajmg.a.30980.
Yuan, H., Han, D., Sun, Q., Yan, D., Sun, H., Tao, R., Cheng, J., Qin, W., Angeli, S., Ouyang, X., Yang, S., Feng, L., Cao, J., Feng, G., Wang, Y., Dai, P., Zhai, S., Yang, W., He, L., Liu, X., Novel mutations in the vWFA2 domain of COCH in two Chinese DFNA9 families. Clin. Genet. 73 (2008), 391–394, 10.1111/j.1399-0004.2008.00972.x.
Jung, J., Kim, H.S., Lee, M.G., Yang, E.J., Choi, J.Y., Novel COCH p.V123E mutation, causative of DFNA9 sensorineural hearing loss and vestibular disorder, shows impaired cochlin post-translational cleavage and secretion. Hum. Mutat. 36 (2015), 1168–1175, 10.1002/humu.22855.
Hildebrand, M.S., Tack, D., DeLuca, A., Hur, I.A., Van Rybroek, J.M., McMordie, S.J., Muilenburg, A., Hoskinson, D.P., Van Camp, G., Pensak, M.L., Storper, I.S., Huygen, P.L.M., Casavant, T.L., Smith, R.J.H., Mutation in the COCH gene is associated with superior semicircular canal dehiscence. Am. J. Med. Genet. 149A (2009), 280–285, 10.1002/ajmg.a.32618.
Fransen, E., Verstreken, M., Bom, S.J.H., Lemaire, F., Kemperman, M.H., De Kok, Y.J.M., Wuyts, F.L., Verhagen, W.I.M., Huygen, P.L.M., Mcguirt, W.T., Smith, R.J.H., Van Maldergem, L., Declau, F., Cremers, C.W.R.J., Van De Heyning, P.H., Cremers, F.P.M., Van Camp, G., A common ancestor for COCH related cochleovestibular (DFNA9) patients in Belgium and The Netherlands bearing the P51S mutation. J. Med. Genet. 38 (2001), 61–65, 10.1136/jmg.38.1.61.
Robertson, N.G., Jones, S.M., Sivakumaran, T.A., Giersch, A.B.S., Jurado, S.A., Call, L.M., Miller, C.E., Maison, S.F., Liberman, M.C., Morton, C.C., A targeted Coch missense mutation: a knock-in mouse model for DFNA9 late-onset hearing loss and vestibular dysfunction. Hum. Mol. Genet. 17 (2008), 3426–3434, 10.1093/hmg/ddn236.
Mehregan, H., Mohseni, M., Akbari, M., Jalalvand, K., Arzhangi, S., Nikzat, N., Kahrizi, K., Najmabadi, H., Novel Mutations in KCNQ4, LHFPL5 and COCH Genes in Iranian Families with Hearing Impairment. Arch. Iran. Med. 22 (2019), 189–197.
Booth, K.T., Ghaffar, A., Rashid, M., Hovey, L.T., Hussain, M., Frees, K., Renkes, E.M., Nishimura, C.J., Shahzad, M., Smith, R.J., Ahmed, Z., Azaiez, H., Riazuddin, S., Novel loss-of-function mutations in COCH cause autosomal recessive nonsyndromic hearing loss. Hum. Genet. 139 (2020), 1565–1574, 10.1007/s00439-020-02197-5.
Ballo, R., Beighton, P.H., Ramesar, R.S., Stickler-like syndrome due to a dominant negative mutation in the COL2A1 gene. Am. J. Med. Genet. 80 (1998), 6–11, 10.1002/(SICI)1096-8628(19981102)80:1<6::AID-AJMG2>3.0.CO;2-0.
Guo, L., Elcioglu, N.H., Wang, Z., Demirkol, Y.K., Isguven, P., Matsumoto, N., Nishimura, G., Miyake, N., Ikegawa, S., Novel and recurrent COL11A1 and COL2A1 mutations in the Marshall–Stickler syndrome spectrum. Hum. Genome Var., 4, 2017, 17040, 10.1038/hgv.2017.40.
Gratton, M.A., Rao, V.H., Meehan, D.T., Askew, C., Cosgrove, D., Matrix metalloproteinase dysregulation in the stria vascularis of mice with alport syndrome. Am. J. Pathol. 166 (2005), 1465–1474, 10.1016/S0002-9440(10)62363-2.
Rost, S., Bach, E., Neuner, C., Nanda, I., Dysek, S., Bittner, R.E., Keller, A., Bartsch, O., Mlynski, R., Haaf, T., Müller, C.R., Kunstmann, E., Novel form of X-linked nonsyndromic hearing loss with cochlear malformation caused by a mutation in the type IV collagen gene COL4A6. Eur. J. Hum. Genet. 22 (2014), 208–215, 10.1038/ejhg.2013.108.
Tang, S., Yonezawa, T., Maeda, Y., Ono, M., Maeba, T., Miyoshi, T., Momota, R., Tomono, Y., Oohashi, T., Lack of collagen α6(IV) chain in mice does not cause severe-to-profound hearing loss or cochlear malformation, a distinct phenotype from nonsyndromic hearing loss with COL4A6 missense mutation. PLoS ONE, 16, 2021, e0249909, 10.1371/journal.pone.0249909.
Van Camp, G., Snoeckx, R.L., Hilgert, N., Van Den Ende, J., Fukuoka, H., Wagatsuma, M., Suzuki, H., Erica Smets, R.M., Vanhoenacker, F., Declau, F., Van De Heyning, P., Usami, S., A new autosomal recessive form of stickler syndrome is caused by a mutation in the COL9A1 gene. Am. Hum. Genet. 79 (2006), 449–457, 10.1086/506478.
Nikopoulos, K., Schrauwen, I., Simon, M., Collin, R.W.J., Veckeneer, M., Keymolen, K., Van Camp, G., Cremers, F.P.M., Van Den Born, L.I., Autosomal recessive stickler syndrome in two families is caused by mutations in the COL9A1 gene. Investig. Ophthalmol. Vis. Sci., 52, 2011, 4774, 10.1167/iovs.10-7128.
Nixon, T.R.W., Alexander, P., Richards, A., McNinch, A., Bearcroft, P.W.P., Cobben, J., Snead, M.P., Homozygous Type IX collagen variants (COL9A1, COL9A2, and COL9A3) causing recessive stickler syndrome–expanding the phenotype. Am. J. Med. Genet., 2019, 10.1002/ajmg.a.61191 ajmg.a.61191.
Baker, S., Booth, C., Fillman, C., Shapiro, M., Blair, M.P., Hyland, J.C., Ala-Kokko, L., A loss of function mutation in the COL9A2 gene causes autosomal recessive Stickler syndrome. Am. J. Med. Genet. 155 (2011), 1668–1672, 10.1002/ajmg.a.34071.
Kjellström, U., Martell, S., Brobeck, C., Andréasson, S., Autosomal recessive Stickler syndrome associated with homozygous mutations in the COL9A2 gene. Ophthalmic Genet. 42 (2021), 161–169, 10.1080/13816810.2020.1861309.
Faletra, F., D'Adamo, A.P., Bruno, I., Athanasakis, E., Biskup, S., Esposito, L., Gasparini, P., Autosomal recessive stickler syndrome due to a loss of function mutation in the COL 9 A 3 gene. Am. J. Med. Genet. 164 (2014), 42–47, 10.1002/ajmg.a.36165.
Hanson-Kahn, A., Li, B., Cohn, D.H., Nickerson, D.A., Bamshad, M.J., University of Washington Center for Mendelian Genomics. Hudgins, L., Autosomal recessive Stickler syndrome resulting from a COL9A3 mutation. Am. J. Med. Genet. 176 (2018), 2887–2891, 10.1002/ajmg.a.40647.
Markova, T., Sparber, P., Borovikov, A., Nagornova, T., Dadali, E., Clinical and genetic characterization of autosomal recessive stickler syndrome caused by novel compound heterozygous mutations in the COL9A3 gene. Mol. Genet. Genom. Med., 9, 2021, 10.1002/mgg3.1620.
Rad, A., Najafi, M., Suri, F., Abedini, S., Loum, S., Karimiani, E.G., Daftarian, N., Murphy, D., Doosti, M., Moghaddasi, A., Ahmadieh, H., Sabbaghi, H., Rajati, M., Hashemi, N., Vona, B., Schmidts, M., Identification of three novel homozygous variants in COL9A3 causing autosomal recessive Stickler syndrome. Orphanet J. Rare Dis., 17, 2022, 97, 10.1186/s13023-022-02244-6.
Richards, A., A family with Stickler syndrome type 2 has a mutation in the COL11A1 gene resulting in the substitution of glycine 97 by valine in alpha 1 (XI) collagen. Hum. Mol. Genet. 5 (1996), 1339–1343, 10.1093/hmg/5.9.1339.
Griffith, A.J., Sprunger, L.K., Sirko-Osadsa, D.A., Tiller, G.E., Meisler, M.H., Warman, M.L., Marshall syndrome associated with a splicing defect at the COL11A1 locus. Am. Hum. Genet. 62 (1998), 816–823, 10.1086/301789.
Annunen, S., Körkkö, J., Czarny, M., Warman, M.L., Brunner, H.G., Kääriäinen, H., Mulliken, J.B., Tranebjærg, L., Brooks, D.G., Cox, G.F., Cruysberg, J.R., Curtis, M.A., Davenport, S.L.H., Friedrich, C.A., Kaitila, I., Krawczynski, M.R., Latos-Bielenska, A., Mukai, S., Olsen, B.R., Shinno, N., Somer, M., Vikkula, M., Zlotogora, J., Prockop, D.J., Ala-Kokko, L., Splicing mutations of 54-bp exons in the COL11A1 gene cause marshall syndrome, but other mutations cause overlapping marshall/stickler phenotypes. Am. Hum. Genet. 65 (1999), 974–983, 10.1086/302585.
Richards, A.J., Fincham, G.S., McNinch, A., Hill, D., Poulson, A.V., Castle, B., Lees, M.M., Moore, A.T., Scott, J.D., Snead, M.P., Alternative splicing modifies the effect of mutations in COL11A1 and results in recessive type 2 Stickler syndrome with profound hearing loss. J. Med. Genet. 50 (2013), 765–771, 10.1136/jmedgenet-2012-101499.
Mladenova, M., Todorov, T., Grozdanova, L., Mitev, V., Todorova, A., Novel mutation in the COL11A1 gene causing Marshall-Stickler syndrome in three generations of a Bulgarian family. Balk. J. Med. Genet. 24 (2021), 95–98, 10.2478/bjmg-2021-0001.
Tompson, S.W., Bacino, C.A., Safina, N.P., Bober, M.B., Proud, V.K., Funari, T., Wangler, M.F., Nevarez, L., Ala-Kokko, L., Wilcox, W.R., Eyre, D.R., Krakow, D., Cohn, D.H., Fibrochondrogenesis results from mutations in the COL11A1 Type XI collagen gene. Am. Hum. Genet. 87 (2010), 708–712, 10.1016/j.ajhg.2010.10.009.
Booth, K.T., Askew, J.W., Talebizadeh, Z., Huygen, P.L.M., Eudy, J., Kenyon, J., Hoover, D., Hildebrand, M.S., Smith, K.R., Bahlo, M., Kimberling, W.J., Smith, R.J.H., Azaiez, H., Smith, S.D., Splice-altering variant in COL11A1 as a cause of nonsyndromic hearing loss DFNA37. Genet. Med. 21 (2019), 948–954, 10.1038/s41436-018-0285-0.
Brunner, H.G., Van Beersum, S.E.C., Warman, M.L., Olsen, B.R., Ropers, H.H., Mariman, E.C.M., A Stickler syndrome gene is linked to chromosome 6 near the COL11A2 gene. Hum. Mol. Genet. 3 (1994), 1561–1564, 10.1093/hmg/3.9.1561.
Vikkula, M., Madman, E.C.M., Lui, V.C.H., Zhidkova, N.I., Tiller, G.E., Goldring, M.B., Van Beersum, S.E.C., De Waal Malefijt, M.C., Van Den Hoogen, F.H.J., Ropers, H.H., Mayne, R., Cheah, K.S.E., Olsen, B.R., Warman, M.L., Brunner, H.G., Autosomal dominant and recessive osteochondrodysplasias associated with the COL11A2 locus. Cell 80 (1995), 431–437, 10.1016/0092-8674(95)90493-X.
Van Beelen, E., Leijendeckers, J.M., Huygen, P.L.M., Admiraal, R.J.C., Hoefsloot, L.H., Lichtenbelt, K.D., Stöbe, L., Pennings, R.J.E., Leuwer, R., Snik, A.F.M., Kunst, H.P.M., Audiometric characteristics of two Dutch families with non-ocular Stickler syndrome (COL11A2). Hear. Res. 291 (2012), 15–23, 10.1016/j.heares.2012.07.001.
Harel, T., Rabinowitz, R., Hendler, N., Galil, A., Flusser, H., Chemke, J., Gradstein, L., Lifshitz, T., Ofir, R., Elbedour, K., Birk, O.S., COL11A2 mutation associated with autosomal recessive Weissenbacher-Zweymuller syndrome: molecular and clinical overlap with otospondylomegaepiphyseal dysplasia (OSMED). Am. J. Med. Genet. 132A (2005), 33–35, 10.1002/ajmg.a.30371.
Temtamy, S.A., Männikkö, M., Abdel-Salam, G.M.H., Hassan, N.A., Ala-Kokko, L., Afifi, H.H., Oto-spondylo-megaepiphyseal dysplasia (OSMED): clinical and radiological findings in sibs homozygous for premature stop codon mutation in theCOL11A2 gene. Am. J. Med. Genet. 140A (2006), 1189–1195, 10.1002/ajmg.a.31205.
De Leenheer, E.M.R., Kunst, H.P.M., McGuirt, W.T., Prasad, S.D., Brown, M.R., Huygen, P.L.M., Smith, R.J.H., Cremers, C.W.R.J., Autosomal dominant inherited hearing impairment caused by a missense mutation in COL11A2 (DFNA13). Arch. Otolaryngol. Head Neck Surg., 127, 2001, 13, 10.1001/archotol.127.1.13.
De Leenheer, E.M.R., Bosman, A.J., Huygen, P.L.M., Kunst, H.P.M., Cremers, C.W.R.J., Audiological characteristics of some affected members of a Dutch DFNA13/COL11A2 family. Ann. Otol. Rhinol. Laryngol. 113 (2004), 922–929, 10.1177/000348940411301112.
Chen, W., Mutation of COL11A2 causes autosomal recessive non-syndromic hearing loss at the DFNB53 locus. J. Med. Genet., 42, 2005, 10.1136/jmg.2005.032615 e61–e61.
Chakchouk, I., Grati, M., Bademci, G., Bensaid, M., Ma, Q., Chakroun, A., Foster, J., Yan, D., Duman, D., Diaz-Horta, O., Ghorbel, A., Mittal, R., Farooq, A., Tekin, M., Masmoudi, S., Liu, X.Z., Novel mutations confirm that COL11A2 is responsible for autosomal recessive non-syndromic hearing loss DFNB53. Mol. Genet. Genom. 290 (2015), 1327–1334, 10.1007/s00438-015-0995-9.
Umugire, A., Lee, S., Lee, C.J., Choi, Y., Kim, T., Cho, H.H., Hyaluronan synthase 1: a novel candidate gene associated with late-onset non-syndromic hereditary hearing loss. Clin. Exp. Otorhinolaryngol. 15 (2022), 220–229, 10.21053/ceo.2022.00038.
Muggenthaler, M.M.A., Chowdhury, B., Hasan, S.N., Cross, H.E., Mark, B., Harlalka, G.V., Patton, M.A., Ishida, M., Behr, E.R., Sharma, S., Zahka, K., Faqeih, E., Blakley, B., Jackson, M., Lees, M., Dolinsky, V., Cross, L., Stanier, P., Salter, C., Baple, E.L., Alkuraya, F.S., Crosby, A.H., Triggs-Raine, B., Chioza, B.A., Mutations in HYAL2, encoding hyaluronidase 2, cause a syndrome of orofacial clefting and cor triatriatum sinister in humans and mice. PLos Genet., 13, 2017, e1006470, 10.1371/journal.pgen.1006470.
Shahin, H., Walsh, T., Rayyan, A.A., Lee, M.K., Higgins, J., Dickel, D., Lewis, K., Thompson, J., Baker, C., Nord, A.S., Stray, S., Gurwitz, D., Avraham, K.B., King, M.C., Kanaan, M., Five novel loci for inherited hearing loss mapped by SNP-based homozygosity profiles in Palestinian families. Eur. J. Hum. Genet. 18 (2010), 407–413, 10.1038/ejhg.2009.190.
Lee, K., Chiu, I., Santos-Cortez, R., Basit, S., Khan, S., Azeem, Z., Andrade, P., Kim, S., Ahmad, W., Leal, S., Novel OTOA mutations cause autosomal recessive non-syndromic hearing impairment in Pakistani families: letter to the editor. Clin. Genet. 84 (2013), 294–296, 10.1111/cge.12047.
Walsh, T., Rayan, A.A., Sa'ed, J.A., Shahin, H., Shepshelovich, J., Lee, M.K., Hirschberg, K., Tekin, M., Salhab, W., Avraham, K.B., King, M.C., Kanaan, M., Genomic analysis of a heterogeneous Mendelian phenotype: multiple novel alleles for inherited hearing loss in the Palestinian population. Hum. Genom., 2, 2006, 203, 10.1186/1479-7364-2-4-203.
Schraders, M., Ruiz-Palmero, L., Kalay, E., Oostrik, J., del Castillo, F.J., Sezgin, O., Beynon, A.J., Strom, T.M., Pennings, R.J.E., Zazo Seco, C., Oonk, A.M.M., Kunst, H.P.M., Domínguez-Ruiz, M., García-Arumi, A.M., del Campo, M., Villamar, M., Hoefsloot, L.H., Moreno, F., Admiraal, R.J.C., del Castillo, I., Kremer, H., Mutations of the gene encoding otogelin are a cause of autosomal-recessive nonsyndromic moderate hearing impairment. Am. Hum. Genet. 91 (2012), 883–889, 10.1016/j.ajhg.2012.09.012.
Oonk, A.M.M., Leijendeckers, J.M., Huygen, P.L.M., Schraders, M., Del Campo, M., Del Castillo, I., Tekin, M., Feenstra, I., Beynon, A.J., Kunst, H.P.M., Snik, A.F.M., Kremer, H., Admiraal, R.J.C., Pennings, R.J.E., Similar phenotypes caused by mutations in OTOG and OTOGL. Ear Hear. 35 (2014), e84–e91, 10.1097/AUD.0000000000000008.
Yu, S., Choi, H.J., Lee, J.S., Lee, H.J., Rim, J.H., Choi, J.Y., Gee, H.Y., Jung, J., A novel early truncation mutation in OTOG causes prelingual mild hearing loss without vestibular dysfunction. Eur. J. Med. Genet. 62 (2019), 81–84, 10.1016/j.ejmg.2018.05.018.
Simmler, M.C., Zwaenepoel, I., Verpy, E., Guillaud, L., Elbaz, C., Petit, C., Panthier, J.J., Twister mutant mice are defective for otogelin, a component specific to inner ear acellular membranes. Mamm. Genome 11 (2000), 961–966, 10.1007/s003350010197.
El Hakam Kamareddin, C., Magnol, L., Blanquet, V., A new Otogelin ENU mouse model for autosomal-recessive nonsyndromic moderate hearing impairment. SpringerPlus, 4, 2015, 730, 10.1186/s40064-015-1537-y.
Yariz, K.O., Duman, D., Zazo Seco, C., Dallman, J., Huang, M., Peters, T.A., Sirmaci, A., Lu, N., Schraders, M., Skromne, I., Oostrik, J., Diaz-Horta, O., Young, J.I., Tokgoz-Yilmaz, S., Konukseven, O., Shahin, H., Hetterschijt, L., Kanaan, M., Oonk, A.M.M., Edwards, Y.J.K., Li, H., Atalay, S., Blanton, S., DeSmidt, A.A., Liu, X.Z., Pennings, R.J.E., Lu, Z., Chen, Z.Y., Kremer, H., Tekin, M., Mutations in OTOGL, encoding the inner ear protein otogelin-like, cause moderate sensorineural hearing loss. Am. Hum. Genet. 91 (2012), 872–882, 10.1016/j.ajhg.2012.09.011.
Bonnet, C., Louha, M., Loundon, N., Michalski, N., Verpy, E., Smagghe, L., Hardelin, J.P., Rouillon, I., Jonard, L., Couderc, R., Gherbi, S., Garabedian, E.N., Denoyelle, F., Petit, C., Marlin, S., Biallelic nonsense mutations in the otogelin-like gene (OTOGL) in a child affected by mild to moderate hearing impairment. Gene 527 (2013), 537–540, 10.1016/j.gene.2013.06.044.
Gu, X., Sun, S., Guo, L., Lu, X., Mei, H., Lai, C., Li, H., Novel biallelic OTOGL mutations in a Chinese family with moderate non-syndromic sensorineural hearing loss. Int. J. Pediatr. Otorhinolaryngol. 79 (2015), 817–820, 10.1016/j.ijporl.2015.03.008.
Kim, N.K.D., Kim, A.R., Park, K.T., Kim, S.Y., Kim, M.Y., Nam, J.Y., Woo, S.J., Oh, S.H., Park, W.Y., Choi, B.Y., Whole-exome sequencing reveals diverse modes of inheritance in sporadic mild to moderate sensorineural hearing loss in a pediatric population. Genet. Med. 17 (2015), 901–911, 10.1038/gim.2014.213.
Barake, R., Abou-Rizk, S., Nemer, G., Bassim, M., The OTOGL p.Arg925* variant is associated with moderate hearing loss in a Syrian nonconsanguineous family. Genet. Test. Mol. Biomark. 21 (2017), 445–449, 10.1089/gtmb.2016.0406.
Villamar, M., Del Castillo, I., Valle, N., Romero, L., Moreno, F., Deafness locus DFNB16 is located on chromosome 15q13-q21 within a 5-cM interval flanked by markers D15S994 and D15S132. Am. Hum. Genet. 64 (1999), 1238–1241, 10.1086/302321.
Verhoeven, K., Schatteman, I., Verstreken, M., Brown, M.R., A gene for autosomal dominant nonsyndromic hearing loss (DFNA12) maps to chromosome 11q22-24. Am. J. Hum. Genet. 60 (1997), 1168–1173.
Verhoeven, K., Laer, L.V., Kirschhofer, K., Legan, P.K., Hughes, D.C., Schatteman, I., Verstreken, M., Hauwe, P.V., Coucke, P., Chen, A., Smith, R.J.H., Somers, T., Offeciers, F.E., Heyning, P.V.D., Richardson, G.P., Wachtler, F., Kimberling, W.J., Willems, P.J., Govaerts, P.J., Camp, G.V., Mutations in the human α-tectorin gene cause autosomal dominant non-syndromic hearing impairment. Nat. Genet. 19 (1998), 60–62, 10.1038/ng0598-60.
Collin, R.W.J., De Heer, A.M.R., Oostrik, J., Pauw, R.J., Plantinga, R.F., Huygen, P.L., Admiraal, R., De Brouwer, A.P.M., Strom, T.M., Cremers, C.W.R.J., Kremer, H., Mid-frequency DFNA8/12 hearing loss caused by a synonymous TECTA mutation that affects an exonic splice enhancer. Eur. J. Hum. Genet. 16 (2008), 1430–1436, 10.1038/ejhg.2008.110.
Legan, P.K., Lukashkina, V.A., Goodyear, R.J., Lukashkin, A.N., Verhoeven, K., Van Camp, G., Russell, I.J., Richardson, G.P., A deafness mutation isolates a second role for the tectorial membrane in hearing. Nat. Neurosci. 8 (2005), 1035–1042, 10.1038/nn1496.
Xia, A., Gao, S.S., Yuan, T., Osborn, A., Bress, A., Pfister, M., Maricich, S.M., Pereira, F.A., Oghalai, J.S., Deficient forward transduction and enhanced reverse transduction in the alpha tectorin C1509G human hearing loss mutation. Dis. Models Mech. 3 (2010), 209–223, 10.1242/dmm.004135.
Legan, P.K., Goodyear, R.J., Morin, M., Mencia, A., Pollard, H., Olavarrieta, L., Korchagina, J., Modamio-Hoybjor, S., Mayo, F., Moreno, F., Moreno-Pelayo, M.A., Richardson, G.P., Three deaf mice: mouse models for TECTA-based human hereditary deafness reveal domain-specific structural phenotypes in the tectorial membrane. Hum. Mol. Genet. 23 (2014), 2551–2568, 10.1093/hmg/ddt646.
Mustapha, M., An alpha-tectorin gene defect causes a newly identified autosomal recessive form of sensorineural pre-lingual non-syndromic deafness, DFNB21. Hum. Mol. Genet. 8 (1999), 409–412, 10.1093/hmg/8.3.409.
Naz, S., Distinctive audiometric profile associated with DFNB21 alleles of TECTA. J. Med. Genet. 40 (2003), 360–363, 10.1136/jmg.40.5.360.
Meyer, N.C., Alasti, F., Nishimura, C.J., Imanirad, P., Kahrizi, K., Riazalhosseini, Y., Malekpour, M., Kochakian, N., Jamali, P., Van Camp, G., Smith, R.J.H., Najmabadi, H., Identification of three novel TECTA mutations in Iranian families with autosomal recessive nonsyndromic hearing impairment at the DFNB21 locus. Am. J. Med. Genet. 143A (2007), 1623–1629, 10.1002/ajmg.a.31718.
Gerchman, E., Hilfer, S.R., Brown, J.W., Involvement of extracellular matrix in the formation of the inner ear. Dev. Dyn. 202 (1995), 421–432, 10.1002/aja.1002020411.
Moro-Balbás, J.A., Gato, A., Alonso, M.I., Martín, P., De La Mano, A., Basal lamina heparan sulphate proteoglycan is involved in otic placode invagination in chick embryos. Anat. Embryol. (Berl.) 202 (2000), 333–343, 10.1007/s004290000119.
Visconti, R.P., Hilfer, S.R., Perturbation of extracellular matrix prevents association of the otic primordium with the posterior rhombencephalon and inhibits subsequent invagination. Dev. Dyn. 223 (2002), 48–58, 10.1002/dvdy.1237.
Wang, X., Harris, R.E., Bayston, L.J., Ashe, H.L., Type IV collagens regulate BMP signalling in Drosophila. Nature 455 (2008), 72–77, 10.1038/nature07214.
Capurro, M.I., Xu, P., Shi, W., Li, F., Jia, A., Filmus, J., Glypican-3 inhibits hedgehog signaling during development by competing with patched for hedgehog binding. Dev. Cell 14 (2008), 700–711, 10.1016/j.devcel.2008.03.006.
Ornitz, D.M., FGFs, heparan sulfate and FGFRs: complex interactions essential for development. Bioessays 22 (2000), 108–112, 10.1002/(SICI)1521-1878(200002)22:2<108::AID-BIES2>3.0.CO;2-M.
Li, X., Zhang, L., Yin, X., Gao, Z., Zhang, H., Liu, X., Pan, X., Li, N., Yu, Z., Retinoic acid remodels extracellular matrix (ECM) of cultured human fetal palate mesenchymal cells (hFPMCs) through down-regulation of TGF-β/Smad signaling. Toxicol. Lett. 225 (2014), 208–215, 10.1016/j.toxlet.2013.12.013.
Geng, F.S., Abbas, L., Baxendale, S., Holdsworth, C.J., Swanson, A.G., Slanchev, K., Hammerschmidt, M., Topczewski, J., Whitfield, T.T., Semicircular canal morphogenesis in the zebrafish inner ear requires the function of gpr126 (lauscher), an adhesion class G protein-coupled receptor gene. Development 140 (2013), 4362–4374, 10.1242/dev.098061.
Haddon, C.M., Lewis, J.H., Hyaluronan as a propellant for epithelial movement: the development of semicircular canals in the inner ear of Xenopus. Development 112 (1991), 541–550, 10.1242/dev.112.2.541.
Girish, K.S., Kemparaju, K., The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci. 80 (2007), 1921–1943, 10.1016/j.lfs.2007.02.037.
Munjal, A., Hannezo, E., Tsai, T.Y.C., Mitchison, T.J., Megason, S.G., Extracellular hyaluronate pressure shaped by cellular tethers drives tissue morphogenesis. Cell 184 (2021), 6313–6325.e18, 10.1016/j.cell.2021.11.025.
Jones, A.A., Diamantopoulou, E., Baxendale, S., Whitfield, T.T., Presence of chondroitin sulphate and requirement for heparan sulphate biosynthesis in the developing zebrafish inner ear, Front. Cell Dev. Biol., 10, 2022, 959624, 10.3389/fcell.2022.959624.
Chacko, L.Johnson, Lahlou, H., Steinacher, C., Assou, S., Messat, Y., Dudás, J., Edge, A., Crespo, B., Crosier, M., Sergi, C., Schrott-Fischer, A., Zine, A., Transcriptome-wide analysis reveals a role for extracellular matrix and integrin receptor genes in otic neurosensory differentiation from human iPSCs. Int. J. Mol. Sci., 22, 2021, 10849, 10.3390/ijms221910849.
Davies, D., Cell-extracellular matrix versus cell-cell interactions during the development of the cochlear-vestibular ganglion. J. Neurosci. Res. 89 (2011), 1375–1387, 10.1002/jnr.22664.
Matern, M.S., Durruthy-Durruthy, R., Birol, O., Darmanis, S., Scheibinger, M., Groves, A.K., Heller, S., Transcriptional dynamics of delaminating neuroblasts in the mouse otic vesicle. Cell Rep., 42, 2023, 112545, 10.1016/j.celrep.2023.112545.
Yan, W., Cao, Q.J., Arenas, R.B., Bentley, B., Shao, R., GATA3 inhibits breast cancer metastasis through the reversal of epithelial-mesenchymal transition. J. Biol. Chem. 285 (2010), 14042–14051, 10.1074/jbc.M110.105262.
Bonnans, C., Chou, J., Werb, Z., Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 15 (2014), 786–801, 10.1038/nrm3904.
Davies, D., Holley, M.C., Differential expression of ?3 and ?6 integrins in the developing mouse inner ear. J. Comp. Neurol. 445 (2002), 122–132, 10.1002/cne.10161.
Van den Ackerveken, P., Mounier, A., Huyghe, A., Sacheli, R., Vanlerberghe, P.B., Volvert, M.L., Delacroix, L., Nguyen, L., Malgrange, B., The miR-183/ItgA3 axis is a key regulator of prosensory area during early inner ear development. Cell Death Differ. 24 (2017), 2054–2065, 10.1038/cdd.2017.127.
Brunetta, I., Casalotti, S.O., Hart, I.R., Forge, A., Reynolds, L.E., β3-integrin is required for differentiation in OC-2 cells derived from mammalian embryonic inner ear. BMC Cell Biol., 13, 2012, 5, 10.1186/1471-2121-13-5.
Mellott, A.J., Shinogle, H.E., Nelson-Brantley, J.G., Detamore, M.S., Staecker, H., Exploiting decellularized cochleae as scaffolds for inner ear tissue engineering. Stem Cell Res. Ther., 8, 2017, 41, 10.1186/s13287-017-0505-6.
Ryan, A.F., Wittig, J., Evans, A., Dazert, S., Mullen, L., Environmental micropatterning for the study of spiral ganglion neurite guidance. Audiol. Neurotol. 11 (2006), 134–143, 10.1159/000090686.
Evans, A.R., Euteneuer, S., Chavez, E., Mullen, L.M., Hui, E.E., Bhatia, S.N., Ryan, A.F., Laminin and fibronectin modulate inner ear spiral ganglion neurite outgrowth in an in vitro alternate choice assay. Dev. Neurobiol. 67 (2007), 1721–1730, 10.1002/dneu.20540.
Volkenstein, S., Kirkwood, J.E., Lai, E., Dazert, S., Fuller, G.G., Heller, S., Oriented collagen as a potential cochlear implant electrode surface coating to achieve directed neurite outgrowth. Eur. Arch. Otorhinolaryngol. 269 (2012), 1111–1116, 10.1007/s00405-011-1775-8.
Brand, Y., Sung, M., Chavez, E., Wei, E., Pak, K.K., Housley, G.D., Bodmer, D., Ryan, A.F., Neural cell adhesion molecule L1 modulates type i but not type II inner ear spiral ganglion neurite outgrowth in an in vitro alternate choice assay. J. Mol. Neurosci. 51 (2013), 663–670, 10.1007/s12031-013-0040-6.
Whitlon, D.S., Zhang, X., Pecelunas, K., Greiner, M.A., A temporospatial map of adhesive molecules in the organ of Corti of the mouse cochlea. J. Neurocytol. 28 (1999), 955–968, 10.1023/A:1007038609456.
Ramekers, D., Versnel, H., Grolman, W., Klis, S.F.L., Neurotrophins and their role in the cochlea. Hear. Res. 288 (2012), 19–33, 10.1016/j.heares.2012.03.002.
Lee, R., Kermani, P., Teng, K.K., Hempstead, B.L., Regulation of cell survival by secreted proneurotrophins. Science 294 (2001), 1945–1948, 10.1126/science.1065057.
Hwang, J.J., Park, M.H., Choi, S.Y., Koh, J.Y., Activation of the trk signaling pathway by extracellular zinc. J. Biol. Chem. 280 (2005), 11995–12001, 10.1074/jbc.M403172200.
Rodgers, K.D., Barritt, L., Miner, J.H., Cosgrove, D., The laminins in the murine inner ear: developmental transitions and expression in cochlear basement membranes. Hear. Res. 158 (2001), 39–50, 10.1016/S0378-5955(01)00283-0.
Cosgrove, D., Kornak, J.M., Samuelson, G., Expression of basement membrane type IV collagen chains during postnatal development in the murine cochlea. Hear. Res. 100 (1996), 21–32, 10.1016/0378-5955(96)00114-1.
Tani, T., Koike-Tani, M., Tran, M.T., Shribak, M., Levic, S., Postnatal structural development of mammalian Basilar Membrane provides anatomical basis for the maturation of tonotopic maps and frequency tuning. Sci. Rep., 11, 2021, 7581, 10.1038/s41598-021-87150-w.
Lim, D.J., Development of the tectorial membrane. Hear. Res. 28 (1987), 9–21, 10.1016/0378-5955(87)90149-3.
Johnen, N., Francart, M.E., Thelen, N., Cloes, M., Thiry, M., Evidence for a partial epithelial–mesenchymal transition in postnatal stages of rat auditory organ morphogenesis. Histochem. Cell Biol. 138 (2012), 477–488, 10.1007/s00418-012-0969-5.
Mendus, D., Sundaresan, S., Grillet, N., Wangsawihardja, F., Leu, R., Müller, U., Jones, S.M., Mustapha, M., Thrombospondins 1 and 2 are important for afferent synapse formation and function in the inner ear. Eur. J. Neurosci. 39 (2014), 1256–1267, 10.1111/ejn.12486.
Morioka, S., Sakaguchi, H., Mohri, H., Taniguchi-Ikeda, M., Kanagawa, M., Suzuki, T., Miyagoe-Suzuki, Y., Toda, T., Saito, N., Ueyama, T., Congenital hearing impairment associated with peripheral cochlear nerve dysmyelination in glycosylation-deficient muscular dystrophy. PLos Genet., 16, 2020, e1008826, 10.1371/journal.pgen.1008826.
Heaney, D.L., Schulte, B.A., Niedzielski, A.S., Dystroglycan expression in the developing and senescent gerbil cochlea. Hear. Res. 174 (2002), 9–18, 10.1016/S0378-5955(02)00611-1.
Haydont, V., Bernard, B.A., Fortunel, N.O., Age-related evolutions of the dermis: clinical signs, fibroblast and extracellular matrix dynamics. Mech. Ageing Dev. 177 (2019), 150–156, 10.1016/j.mad.2018.03.006.
Zakusilo, F.T., Kerry O'Banion, M., Gelbard, H.A., Seluanov, A., Gorbunova, V., Matters of size: roles of hyaluronan in CNS aging and disease. Ageing Res. Rev., 72, 2021, 101485, 10.1016/j.arr.2021.101485.
Amargant, F., Manuel, S.L., Tu, Q., Parkes, W.S., Rivas, F., Zhou, L.T., Rowley, J.E., Villanueva, C.E., Hornick, J.E., Shekhawat, G.S., Wei, J., Pavone, M.E., Hall, A.R., Pritchard, M.T., Duncan, F.E., Ovarian stiffness increases with age in the mammalian ovary and depends on collagen and hyaluronan matrices. Aging Cell, 19, 2020, 10.1111/acel.13259.
Bhatt, K.A., Liberman, M.C., Nadol, J.B., Morphometric analysis of age-related changes in the human basilar membrane. Ann. Otol. Rhinol. Laryngol. 110 (2001), 1147–1153, 10.1177/000348940111001212.
Gong, T.W.L., Karolyi, I.J., MacDonald, J., Beyer, L., Raphael, Y., Kohrman, D.C., Camper, S.A., Lomax, M.I., Age-related changes in cochlear gene expression in normal and shaker 2 mice. JARO 7 (2006), 317–328, 10.1007/s10162-006-0046-7.
Thomopoulos, G.N., Spicer, S.S., Gratton, M.A., Schulte, B.A., Age-related thickening of basement membrane in stria vascularis capillaries. Hear. Res. 111 (1997), 31–41, 10.1016/S0378-5955(97)00080-4.
Sakaguchi, N., Spicer, S.S., Thomopoulos, G.N., Schulte, B.A., Increased laminin deposition in capillaries of the stria vascularis of quiet-aged gerbils. Hear. Res. 105 (1997), 44–56, 10.1016/S0378-5955(96)00180-3.
Jorgensen, M.B., Changes of aging in the inner ear: histological studies. Arch. Otolaryngol. Head Neck Surg. 74 (1961), 164–170, 10.1001/archotol.1961.00740030169007.
Wu, P., O'Malley, J.T., De Gruttola, V., Liberman, M.C., Age-related hearing loss is dominated by damage to inner ear sensory cells, not the cellular battery that powers them. J. Neurosci. 40 (2020), 6357–6366, 10.1523/JNEUROSCI.0937-20.2020.
Buckiova, D., Popelar, J., Syka, J., Collagen changes in the cochlea of aged Fischer 344 rats. Exp. Gerontol. 41 (2006), 296–302, 10.1016/j.exger.2005.11.010.
Zhao, T., Liu, X., Sun, Z., Zhang, J., Zhang, X., Wang, C., Geng, R., Zheng, T., Li, B., Zheng, Q.Y., RNA-seq analysis of potential lncRNAs for age-related hearing loss in a mouse model. Aging 12 (2020), 7491–7510, 10.18632/aging.103103.
Liu, W., Johansson, Å., Rask-Andersen, H., Rask-Andersen, M., A combined genome-wide association and molecular study of age-related hearing loss in H. sapiens. BMC Med., 19, 2021, 302, 10.1186/s12916-021-02169-0.
Bullen, A., Forge, A., Wright, A., Richardson, G.P., Goodyear, R.J., Taylor, R., Ultrastructural defects in stereocilia and tectorial membrane in aging mouse and human cochleae. J Neurosci. Res. 98 (2020), 1745–1763, 10.1002/jnr.24556.
Rau, A., Legan, P.K., Richardson, G.P., Tectorin mRNA expression is spatially and temporally restricted during mouse inner ear development. J. Comp. Neurol. 405 (1999), 271–280, 10.1002/(SICI)1096-9861(19990308)405:2<271::AID-CNE10>3.0.CO;2-2.
Knipper, M., Richardson, G., Mack, A., Müller, M., Goodyear, R., Limberger, A., Rohbock, K., Köpschall, I., Zenner, H.P., Zimmermann, U., Thyroid hormone-deficient period prior to the onset of hearing is associated with reduced levels of β-tectorin protein in the tectorial membrane: implication for hearing loss*. J. Biol. Chem. 276 (2001), 39046–39052, 10.1074/jbc.M103385200.
Mansour, A., Sellon, J.B., Filizzola, D., Ghaffari, R., Cheatham, M.A., Freeman, D.M., Age-related degradation of tectorial membrane dynamics with loss of CEACAM16. Biophys. J. 120 (2021), 4777–4785, 10.1016/j.bpj.2021.09.029.
Ma, P., Wang, S., Geng, R., Gong, Y., Li, M., Xie, D., Dong, Y., Zheng, T., Li, B., Zhao, T., Zheng, Q., MiR-29a-deficiency causes thickening of the basilar membrane and age-related hearing loss by upregulating collagen IV and laminin, Front. Cell. Neurosci., 17, 2023, 1191740, 10.3389/fncel.2023.1191740.
Liberman, M.C., Kujawa, S.G., Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms. Hear. Res. 349 (2017), 138–147, 10.1016/j.heares.2017.01.003.
Ruan, Q., Ao, H., He, J., Chen, Z., Yu, Z., Zhang, R., Wang, J., Yin, S., Topographic and quantitative evaluation of gentamicin-induced damage to peripheral innervation of mouse cochleae. Neurotoxicology 40 (2014), 86–96, 10.1016/j.neuro.2013.11.002.
Kujawa, S.G., Liberman, M.C., Adding insult to injury: cochlear nerve degeneration after “temporary” noise-induced hearing loss. J. Neurosci. 29 (2009), 14077–14085, 10.1523/JNEUROSCI.2845-09.2009.
Sergeyenko, Y., Lall, K., Liberman, M.C., Kujawa, S.G., Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J. Neurosci. 33 (2013), 13686–13694, 10.1523/JNEUROSCI.1783-13.2013.
Kujawa, S.G., Liberman, M.C., Acceleration of age-related hearing loss by early noise exposure: evidence of a misspent youth. J. Neurosci. 26 (2006), 2115–2123, 10.1523/JNEUROSCI.4985-05.2006.
Hickman, T.T., Hashimoto, K., Liberman, L.D., Liberman, M.C., Synaptic migration and reorganization after noise exposure suggests regeneration in a mature mammalian cochlea. Sci. Rep., 10, 2020, 19945, 10.1038/s41598-020-76553-w.
Wan, G., Gómez-Casati, M.E., Gigliello, A.R., Liberman, M.C., Corfas, G., Neurotrophin-3 regulates ribbon synapse density in the cochlea and induces synapse regeneration after acoustic trauma. eLife, 3, 2014, e03564, 10.7554/eLife.03564.
Shi, L., Liu, K., Wang, H., Zhang, Y., Hong, Z., Wang, M., Wang, X., Jiang, X., Yang, S., Noise induced reversible changes of cochlear ribbon synapses contribute to temporary hearing loss in mice. Acta Otolaryngol. 135 (2015), 1093–1102, 10.3109/00016489.2015.1061699.
Kim, K.X., Payne, S., Yang-Hood, A., Li, S.Z., Davis, B., Carlquist, J., V-Ghaffari, B., Gantz, J.A., Kallogjeri, D., Fitzpatrick, J.A.J., Ohlemiller, K.K., Hirose, K., Rutherford, M.A., Vesicular glutamatergic transmission in noise-induced loss and repair of cochlear ribbon synapses. J. Neurosci., 2019, 10.1523/JNEUROSCI.2228-18.2019.
Manrique, M., Ramos, Á., de Paula Vernetta, C., Gil-Carcedo, E., Lassaletta, L., Sanchez-Cuadrado, I., Espinosa, J.M., Batuecas, Á., Cenjor, C., Lavilla, M.J., Núñez, F., Cavalle, L., Huarte, A., Guideline on cochlear implants. Acta Otorrinolaringol. (Engl. Ed.) 70 (2019), 47–54, 10.1016/j.otoeng.2017.10.012.
Zhang, G., Gao, Y., Zhao, Z., Pyykko, I., Zou, J., Low-molecular-weight hyaluronic acid contributes to noise-induced cochlear inflammation. Audiol. Neurotol., 2023, 1–14, 10.1159/000530280.
Jongkamonwiwat, N., Ramirez, M.A., Edassery, S., Wong, A.C.Y., Yu, J., Abbott, T., Pak, K., Ryan, A.F., Savas, J.N., Noise exposures causing hearing loss generate proteotoxic stress and activate the proteostasis network. Cell Rep., 33, 2020, 108431, 10.1016/j.celrep.2020.108431.
Hu, B.H., Cai, Q., Hu, Z., Patel, M., Bard, J., Jamison, J., Coling, D., Metalloproteinases and their associated genes contribute to the functional integrity and noise-induced damage in the cochlear sensory epithelium. J. Neurosci. 32 (2012), 14927–14941, 10.1523/JNEUROSCI.1588-12.2012.
Somdas, M.A., Li, P.M.M.C., Whiten, D.M., Eddington, D.K. Jr., Nadol Joseph, B, Quantitative evaluation of new bone and fibrous tissue in the cochlea following cochlear implantation in the human. Audiol. Neurotol. 12 (2007), 277–284, 10.1159/000103208.
Cai, Q., Patel, M., Coling, D., Hu, B.H., Transcriptional changes in adhesion-related genes are site-specific during noise-induced cochlear pathogenesis. Neurobiol. Dis. 45 (2012), 723–732, 10.1016/j.nbd.2011.10.018.
Shi, M., Cao, L., Ding, D., Shi, L., Hu, Y., Qi, G., Zhan, L., Zhu, Y., Yu, W., Lv, P., Yu, N., Acute noise causes down-regulation of ECM protein expression in guinea pig cochlea. Mol. Biotechnol. 65 (2023), 774–785, 10.1007/s12033-022-00557-2.
Milon, B., Shulman, E.D., So, K.S., Cederroth, C.R., Lipford, E.L., Sperber, M., Sellon, J.B., Sarlus, H., Pregernig, G., Shuster, B., Song, Y., Mitra, S., Orvis, J., Margulies, Z., Ogawa, Y., Shults, C., Depireux, D.A., Palermo, A.T., Canlon, B., Burns, J., Elkon, R., Hertzano, R., A cell-type-specific atlas of the inner ear transcriptional response to acoustic trauma. Cell Rep., 36, 2021, 109758, 10.1016/j.celrep.2021.109758.
Smeriglio, P., Wangsawihardja, F.V., Leu, R., Mustapha, M., TSP1 and TSP2 have unique and overlapping roles in protecting against noise-induced auditory synaptopathy. Neuroscience 408 (2019), 68–80, 10.1016/j.neuroscience.2019.03.036.
Marzeda, A.M., Midwood, K.S., Internal affairs: tenascin-c as a clinically relevant, endogenous driver of innate immunity. J. Histochem. Cytochem. 66 (2018), 289–304, 10.1369/0022155418757443.
Wu, J., Han, W., Chen, X., Guo, W., Liu, K., Wang, R., Zhang, J., Sai, N., Matrix metalloproteinase-2 and −9 contribute to functional integrity and noise-induced damage to the blood-labyrinth-barrier. Mol. Med. Rep. 16 (2017), 1731–1738, 10.3892/mmr.2017.6784.
Park, J.S., Kang, S.J., Seo, M., Jou, I., Woo, H.G., Park, S.M., Role of cysteinyl leukotriene signaling in a mouse model of noise-induced cochlear injury. Proc. Natl. Acad. Sci. USA 111 (2014), 9911–9916, 10.1073/pnas.1402261111.
Dzyubenko, E., Manrique-Castano, D., Kleinschnitz, C., Faissner, A., Hermann, D.M., Topological remodeling of cortical perineuronal nets in focal cerebral ischemia and mild hypoperfusion. Matrix Biol. 74 (2018), 121–132, 10.1016/j.matbio.2018.08.001.
Yutsudo, N., Kitagawa, H., Involvement of chondroitin 6-sulfation in temporal lobe epilepsy. Exp. Neurol. 274 (2015), 126–133, 10.1016/j.expneurol.2015.07.009.
Revuelta, J., Bastida, A., Aminoglycoside antibiotics. Antibiotics - Therapeutic Spectrum and Limitations, 2023, Elsevier, 123–153, 10.1016/B978-0-323-95388-7.00018-8.
Romani, A.M.P., Cisplatin in cancer treatment. Biochem. Pharmacol., 206, 2022, 115323, 10.1016/j.bcp.2022.115323.
Hinojosa, R., Lerner, S.A., Cochlear neural degeneration without hair cell loss in two patients with aminoglycoside ototoxicity. J. Infect. Dis. 156 (1987), 449–455, 10.1093/infdis/156.3.449.
Setz, C., Brand, Y., Radojevic, V., Hanusek, C., Mullen, P.J., Levano, S., Listyo, A., Bodmer, D., Matrix metalloproteinases 2 and 9 in the cochlea: expression and activity after aminoglycoside exposition. Neuroscience 181 (2011), 28–39, 10.1016/j.neuroscience.2011.02.043.
Gabaizadeh, R., Staecker, H., Liu, W., Van De Water, T.R., BDNF protection of auditory neurons from cisplatin involves changes in intracellular levels of both reactive oxygen species and glutathione. Mol. Brain Res. 50 (1997), 71–78, 10.1016/S0169-328X(97)00173-3.
Gabaizadeh, R., Staecker, H., Liu, W., Kopke, R., Malgrange, B., Lefebvre, P.P., Van De Water, T.R., Protection of both auditory hair cells and auditory neurons from cisplatin induced damage. Acta Otolaryngol. 117 (1997), 232–238, 10.3109/00016489709117778.
Meen, E., Blakley, B., Quddusi, T., Brain-derived nerve growth factor in the treatment of sensorineural hearing loss. Laryngoscope 119 (2009), 1590–1593, 10.1002/lary.20515.
Ding, D., Zhang, J., Jiang, H., Xuan, W., Qi, W., Salvi, R., Some ototoxic drugs destroy cochlear support cells before damaging sensory hair cells. Neurotox. Res. 37 (2020), 743–752, 10.1007/s12640-020-00170-8.
Wang, J., Ladrech, S., Pujol, R., Brabet, P., Van De Water, T.R., Puel, J.L., Caspase inhibitors, but not c-Jun NH2-terminal kinase inhibitor treatment, prevent cisplatin-induced hearing loss. Cancer Res. 64 (2004), 9217–9224, 10.1158/0008-5472.CAN-04-1581.
Ruhl, D., Du, T.T., Wagner, E.L., Choi, J.H., Li, S., Reed, R., Kim, K., Freeman, M., Hashisaki, G., Lukens, J.R., Shin, J.B., Necroptosis and apoptosis contribute to cisplatin and aminoglycoside ototoxicity. J. Neurosci. 39 (2019), 2951–2964, 10.1523/JNEUROSCI.1384-18.2019.
Rilla, K., Mustonen, A.M., Arasu, U.T., Härkönen, K., Matilainen, J., Nieminen, P., Extracellular vesicles are integral and functional components of the extracellular matrix. Matrix Biol. 75–76 (2019), 201–219, 10.1016/j.matbio.2017.10.003.
Zhuang, P., Phung, S., Warnecke, A., Arambula, A., St. Peter, M., He, M., Staecker, H., Isolation of sensory hair cell specific exosomes in human perilymph. Neurosci. Lett., 764, 2021, 136282, 10.1016/j.neulet.2021.136282.
Breglio, A.M., May, L.A., Barzik, M., Welsh, N.C., Francis, S.P., Costain, T.Q., Wang, L., Anderson, D.E., Petralia, R.S., Wang, Y.X., Friedman, T.B., Wood, M.J.A., Cunningham, L.L., Exosomes mediate sensory hair cell protection in the inner ear. J. Clin. Investig. 130 (2020), 2657–2672, 10.1172/JCI128867.
Park, D.J., Park, J.E., Lee, S.H., Eliceiri, B.P., Choi, J.S., Seo, Y.J., Protective effect of MSC-derived exosomes against cisplatin-induced apoptosis via heat shock protein 70 in auditory explant model. Nanomed. Nanotechnol. Biol. Med., 38, 2021, 102447, 10.1016/j.nano.2021.102447.
Yang, T., Li, W., Peng, A., Wang, Q., Exosomes derived from heat shock preconditioned bone marrow mesenchymal stem cells alleviate cisplatin-induced ototoxicity in mice. J. Biol. Eng., 16, 2022, 24, 10.1186/s13036-022-00304-w.
Warnecke, A., Harre, J., Staecker, H., Prenzler, N., Strunk, D., Couillard-Despres, S., Romanelli, P., Hollerweger, J., Lassacher, T., Auer, D., Pachler, K., Wietzorrek, G., Köhl, U., Lenarz, T., Schallmoser, K., Laner-Plamberger, S., Falk, C.S., Rohde, E., Gimona, M., Extracellular vesicles from human multipotent stromal cells protect against hearing loss after noise trauma in vivo. Clin. Transl. Med., 10, 2020, 10.1002/ctm2.262.
Ladrech, S., Eybalin, M., Puel, J.L., Lenoir, M., Epithelial–mesenchymal transition, and collective and individual cell migration regulate epithelial changes in the amikacin-damaged organ of Corti. Histochem. Cell Biol. 148 (2017), 129–142, 10.1007/s00418-017-1548-6.
Schvartz-Leyzac, K.C., Colesa, D.J., Swiderski, D.L., Raphael, Y., Pfingst, B.E., Cochlear health and cochlear-implant function. JARO 24 (2023), 5–29, 10.1007/s10162-022-00882-y.
Tarabichi, O., Jensen, M., Hansen, M.R., Advances in hearing preservation in cochlear implant surgery. Curr. Opin. Otolaryngol. Head Neck Surg. 29 (2021), 385–390, 10.1097/MOO.0000000000000742.
Rahman, M.T., Chari, D.A., Ishiyama, G., Lopez, I., Quesnel, A.M., Ishiyama, A., Nadol, J.B., Hansen, M.R., Cochlear implants: causes, effects and mitigation strategies for the foreign body response and inflammation. Hear. Res., 422, 2022, 108536, 10.1016/j.heares.2022.108536.
Shaul, C., Bester, C.W., Weder, S., Choi, J., Eastwood, H., Padmavathi, K.V., Collins, A., O'Leary, S.J., Electrical impedance as a biomarker for inner ear pathology following lateral wall and peri-modiolar cochlear implantation. Otol. Neurotol. 40 (2019), e518–e526, 10.1097/MAO.0000000000002227.
Choong, J.K., Hampson, A.J., Brody, K.M., Lo, J., Bester, C.W., Gummer, A.W., Reynolds, N.P., O'Leary, S.J., Nanomechanical mapping reveals localized stiffening of the basilar membrane after cochlear implantation. Hear. Res., 385, 2020, 107846, 10.1016/j.heares.2019.107846.
Shepherd, R.K., Matsushima, J., Millard, R.E., Clark, G.M., Cochlear pathology following chronic electrical stimulation using non charge balanced stimuli. Acta Otolaryngol. 111 (1991), 848–860, 10.3109/00016489109138421.
O'Leary, S.J., Monksfield, P., Kel, G., Connolly, T., Souter, M.A., Chang, A., Marovic, P., O'Leary, J.S., Richardson, R., Eastwood, H., Relations between cochlear histopathology and hearing loss in experimental cochlear implantation. Hear. Res. 298 (2013), 27–35, 10.1016/j.heares.2013.01.012.
Kamakura, T., O'Malley, J.T., Nadol, J.B., Preservation of cells of the organ of corti and innervating dendritic processes following cochlear implantation in the human: an immunohistochemical study. Otol. Neurotol. 39 (2018), 284–293, 10.1097/MAO.0000000000001686.
Zhang, H., Stark, G., Reiss, L., Changes in gene expression and hearing thresholds after cochlear implantation. Otol. Neurotol. 36 (2015), 1157–1165, 10.1097/MAO.0000000000000787.
Claussen, A.D., Quevedo, R.V., Kirk, J.R., Higgins, T., Mostaert, B., Rahman, M.T., Oleson, J., Hernandez, R., Hirose, K., Hansen, M.R., Chronic cochlear implantation with and without electric stimulation in a mouse model induces robust cochlear influx of CX3CR1+/GFP macrophages. Hear. Res., 426, 2022, 108510, 10.1016/j.heares.2022.108510.
Bas, E., Goncalves, S., Adams, M., Dinh, C.T., Bas, J.M., Van De Water, T.R., Eshraghi, A.A., Spiral ganglion cells and macrophages initiate neuro-inflammation and scarring following cochlear implantation. Front. Cell. Neurosci., 9, 2015, 10.3389/fncel.2015.00303.
O'Malley, J.T., Burgess, B.J., Galler, D., Nadol, J.B., Foreign body response to silicone in cochlear implant electrodes in the human. Otol. Neurotol. 38 (2017), 970–977, 10.1097/MAO.0000000000001454.
Parker, M.W., Rossi, D., Peterson, M., Smith, K., Sikström, K., White, E.S., Connett, J.E., Henke, C.A., Larsson, O., Bitterman, P.B., Fibrotic extracellular matrix activates a profibrotic positive feedback loop. J. Clin. Investig. 124 (2014), 1622–1635, 10.1172/JCI71386.
Haak, A.J., Tan, Q., Tschumperlin, D.J., Matrix biomechanics and dynamics in pulmonary fibrosis. Matrix Biol. 73 (2018), 64–76, 10.1016/j.matbio.2017.12.004.
Abi Zeid Daou, C., Bassim, M., Hyaluronic acid in otology: its uses, advantages and drawbacks - a review. Am. J. Otolaryngol., 41, 2020, 102375, 10.1016/j.amjoto.2019.102375.
Bas, E., Anwar, M.R., Goncalves, S., Dinh, C.T., Bracho, O.R., Chiossone, J.A., Van De Water, T.R., Laminin-coated electrodes improve cochlear implant function and post-insertion neuronal survival. Neuroscience 410 (2019), 97–107, 10.1016/j.neuroscience.2019.04.048.
Truong, K., Leigh, B., Vecchi, J.T., Bartholomew, R., Xu, L., Guymon, C.A., Hansen, M.R., Interaction of micropatterned topographical and biochemical cues to direct neurite growth from spiral ganglion neurons. Hear. Res., 409, 2021, 108315, 10.1016/j.heares.2021.108315.
Warnecke, A., Prenzler, N., Harre, J., Köhl, U., Gärtner, L., Lenarz, T., Laner-Plamberger, S., Wietzorrek, G., Staecker, H., Lassacher, T., Hollerweger, J., Gimona, M., Rohde, E., First-in-human intracochlear application of human stromal cell-derived extracellular vesicles. J. Extracell. Vesicles, 10, 2021, 10.1002/jev2.12094.
Matusiak, M., Oziębło, D., Obrycka, A., Ołdak, M., Kaczmarek, L., Skarżyński, P., Skarżyński, H., Functional polymorphism of MMP9 and BDNF as potential biomarker of auditory neuroplasticity in prelingual deafness treatment with cochlear implantation–a retrospective cohort analysis. Trends Hear., 25, 2021, 233121652110021, 10.1177/23312165211002140.
Matusiak, M., Oziębło, D., Ołdak, M., Rejmak, E., Kaczmarek, L., Skarżyński, P.H., Skarżyński, H., Prospective cohort study reveals MMP-9, a neuroplasticity regulator, as a prediction marker of cochlear implantation outcome in prelingual deafness treatment. Mol. Neurobiol. 59 (2022), 2190–2203, 10.1007/s12035-022-02732-7.
Naba, A., Ten years of extracellular matrix proteomics: accomplishments, challenges, and future perspectives. Mol. Cell. Proteom., 22, 2023, 100528, 10.1016/j.mcpro.2023.100528.