Gene transfer in inner ear cells: a challenging race

[en] Recent advances in human genomics led to the identification of numerous defective genes causing deafness, which represent novel putative therapeutic targets. Future gene-based treatment of deafness resulting from genetic or acquired sensorineural hearing loss may include strategies ranging from gene therapy to antisense delivery. For successful development of gene therapies, a minimal requirement involves the engineering of appropriate gene carrier systems. Transfer of exogenous genetic material into the mammalian inner ear using viral or non-viral vectors has been characterized over the last decade. The nature of inner ear cells targeted, as well as the transgene expression level and duration, are highly dependent on the vector type, the route of administration and the strength of the promoter driving expression. This review summarizes and discusses recent advances in inner ear gene-transfer technologies aimed at examining gene function or identifying new treatment for inner ear disorders.

Disciplines :

Otolaryngology

Author, co-author :

Sacheli, Rosalie

Delacroix, Laurence ; Université de Liège - ULiège > Département des sciences cliniques > GIGA-R: Neurosciences

Van Den Ackerveken, Priscilla ; Université de Liège - ULiège > GIGA - Neurosciences

Nguyen, Laurent ; Université de Liège - ULiège > Département des sciences cliniques > Neurologie

Malgrange, Brigitte ; Université de Liège - ULiège > GIGA - Neurosciences

Language :

English

Title :

Gene transfer in inner ear cells: a challenging race

Publication date :

2013

Journal title :

Gene Therapy

ISSN :

0969-7128

eISSN :

1476-5462

Publisher :

Nature Publishing Group, London, United Kingdom

Volume :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 25 June 2012

Statistics

Number of views

128 (29 by ULiège)

Number of downloads

4 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Tucci DL, Schulz K, Witsell DL. Building a national research network for clinical investigations in otology and neurotology. Otol Neurotol Am Otol Soc Am Neurotol Soc Eur Acad Otol Neurotol 2010; 31: 190-195.
Raphael Y, Altschuler RA. Structure and innervation of the cochlea. Brain Res Bull 2003; 60: 397-422.
Harris JP. Immunology of the inner ear: evidence of local antibody production. Annal Otol Rhinol Laryngol 1984; 93: 157-162.
Staecker H, Brough DE, Praetorius M, Baker K. Drug delivery to the inner ear using gene therapy. Otolaryngol Clin North Am 2004; 37: 1091-1108.
Staecker H, Praetorius M, Brough DE. Development of gene therapy for inner ear disease: Using bilateral vestibular hypofunction as a vehicle for translational research. Hear Res 2011; 276: 44-51.
Kootstra NA, Verma IM. Gene therapy with viral vectors. Annu Rev Pharmacol Toxicol 2003; 43: 413-439.
Breyer B, Jiang W, Cheng H, Zhou L, Paul R, Feng T et al. Adenoviral vectormediated gene transfer for human gene therapy. Curr Gene Ther 2001; 1: 149-162.
Raphael Y, Frisancho JC, Roessler BJ. Adenoviral-mediated gene transfer into guinea pig cochlear cells in vivo. Neurosci Lett 1996; 207: 137-141.
Weiss MA, Frisancho JC, Roessler BJ, Raphael Y. Viral-mediated gene transfer in the cochlea. Int J Dev Neurosci 1997; 15: 577-583.
Dazert S, Aletsee C, Brors D, Gravel C, Sendtner M, Ryan A. In vivo adenoviral transduction of the neonatal rat cochlea and middle ear. Hear Res 2001; 151: 30-40.
Dazert S, Battaglia A, Ryan AF. Transfection of neonatal rat cochlear cells in vitro with an adenovirus vector. Int J Dev Neurosci 1997; 15: 595-600.
Kanzaki S, Ogawa K, Camper SA, Raphael Y. Transgene expression in neonatal mouse inner ear explants mediated by first and advanced generation adenovirus vectors. Hear Res 2002; 169: 112-120.
Holt JR, Johns DC, Wang S, Chen ZY, Dunn RJ, Marban E et al. Functional expression of exogenous proteins in mammalian sensory hair cells infected with adenoviral vectors. J Neurophysiol 1999; 81: 1881-1888.
Ruan Q, Chen D, Wang Z, Chi F, He J, Wang J et al. Effects of Kir2.1 gene transfection in cochlear hair cells and application of neurotrophic factors on survival and neurite growth of co-cultured cochlear spiral ganglion neurons. Mol Cell Neurosci 2010; 43: 326-339.
Duan LM, Bordet T, Mezzina M, Kahn A, Ulfendahl M. Adenoviral and adenoassociated viral vector mediated gene transfer in the guinea pig cochlea. Neuroreport 2002; 13: 1295-1299.
Luebke AE, Foster PK, Muller CD, Peel AL. Cochlear function and transgene expression in the guinea pig cochlea, using adenovirus- and adeno-associated virus-directed gene transfer. Hum Gene Ther 2001; 12: 773-781.
Yamasoba T, Yagi M, Roessler BJ, Miller JM, Raphael Y. Inner ear transgene expression after adenoviral vector inoculation in the endolymphatic sac. Hum Gene Ther 1999; 10: 769-774.
Ishimoto S, Kawamoto K, Kanzaki S, Raphael Y. Gene transfer into supporting cells of the organ of Corti. Hear Res 2002; 173: 187-197.
Iizuka T, Kanzaki S, Mochizuki H, Inoshita A, Narui Y, Furukawa M et al. Noninvasive in vivo delivery of transgene via adeno-associated virus into supporting cells of the neonatal mouse cochlea. Hum Gene Ther 2008; 19: 384-390.
Yagi M, Magal E, Sheng Z, Ang KA, Raphael Y. Hair cell protection from aminoglycoside ototoxicity by adenovirus-mediated overexpression of glial cell linederived neurotrophic factor. Hum Gene Ther 1999; 10: 813-823.
Suzuki M, Yagi M, Brown JN, Miller AL, Miller JM, Raphael Y. Effect of transgenic GDNF expression on gentamicin-induced cochlear and vestibular toxicity. Gene Therapy 2000; 7: 1046-1054.
Kawamoto K, Yagi M, Stover T, Kanzaki S, Raphael Y. Hearing and hair cells are protected by adenoviral gene therapy with TGF-beta1 and GDNF. Mol Ther 2003; 7: 484-492.
Yagi M, Kanzaki S, Kawamoto K, Shin B, Shah PP, Magal E et al. Spiral ganglion neurons are protected from degeneration by GDNF gene therapy. J Assoc Res Otolaryngol 2000; 1: 315-325.
Hakuba N, Watabe K, Hyodo J, Ohashi T, Eto Y, Taniguchi M et al. Adenovirusmediated overexpression of a gene prevents hearing loss and progressive inner hair cell loss after transient cochlear ischemia in gerbils. Gene Therapy 2003; 10: 426-433.
Luebke AE, Steiger JD, Hodges BL, Amalfitano A. A modified adenovirus can transfect cochlear hair cells in vivo without compromising cochlear function. Gene Therapy 2001; 8: 789-794.
Brough DE, Lizonova A, Hsu C, Kulesa VA, Kovesdi I. A gene transfer vector-cell line system for complete functional complementation of adenovirus early regions E1 and E4. J Virol 1996; 70: 6497-6501.
Holt Jr. Viral-mediated gene transfer to study the molecular physiology of the mammalian inner ear. Audiol Neurootol 2002; 7: 157-160.
Sheffield AM, Gubbels SP, Hildebrand MS, Newton SS, Chiorini JA, Di Pasquale G et al. Viral vector tropism for supporting cells in the developing murine cochlea. Hear Res 2011; 277: 28-36.
Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 2003; 23: 4395-4400.
Izumikawa M, Minoda R, Kawamoto K, Abrashkin KA, Swiderski DL, Dolan DF et al. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 2005; 11: 271-276.
Kawamoto K, Sha SH, Minoda R, Izumikawa M, Kuriyama H, Schacht J et al. Antioxidant gene therapy can protect hearing and hair cells from ototoxicity. Mol Ther 2004; 9: 173-181.
Wise AK, Tu T, Atkinson PJ, Flynn BO, Sgro BE, Hume C et al. The effect of deafness duration on neurotrophin gene therapy for spiral ganglion neuron protection. Hear Res 2011; 278: 69-76.
Schlecker C, Praetorius M, Brough DE, Presler Jr RG, Hsu C, Plinkert PK et al. Selective atonal gene delivery improves balance function in a mouse model of vestibular disease. Gene Therapy 2011; 18: 884-890.
Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993; 73: 309-319.
Venail F, Wang J, Ruel J, Ballana E, Rebillard G, Eybalin M et al. Coxsackie adenovirus receptor and alpha nu beta3/alpha nu beta5 integrins in adenovirus gene transfer of rat cochlea. Gene Therapy 2007; 14: 30-37.
Praetorius M, Brough DE, Hsu C, Plinkert PK, Pfannenstiel SC, Staecker H. Adenoviral vectors for improved gene delivery to the inner ear. Hear Res 2009; 248: 31-38.
Taura A, Taura K, Choung YH, Masuda M, Pak K, Chavez E et al. Histone deacetylase inhibition enhances adenoviral vector transduction in inner ear tissue. Neuroscience 2010; 166: 1185-1193.
Sugiyama A, Hattori S, Tanaka S, Isoda F, Kleopoulos S, Rosenfeld M et al. Defective adenoassociated viral-mediated transfection of insulin gene by direct injection into liver parenchyma decreases blood glucose of diabetic mice. Horm Metab Res 1997; 29: 599-603.
Champion HC, Georgakopoulos D, Haldar S, Wang L, Wang Y, Kass DA. Robust adenoviral and adeno-associated viral gene transfer to the in vivo murine heart: application to study of phospholamban physiology. Circulation 2003; 108: 2790-2797.
Peel AL, Klein RL. Adeno-associated virus vectors: activity and applications in the CNS. J Neurosci Methods 2000; 98: 95-104.
Stone IM, Lurie DI, Kelley MW, Poulsen DJ. Adeno-associated virus-mediated gene transfer to hair cells and support cells of the murine cochlea. Mol Ther 2005; 11: 843-848.
Jero J, Mhatre AN, Tseng CJ, Stern RE, Coling DE, Goldstein JA et al. Cochlear gene delivery through an intact round window membrane in mouse. Hum Gene Ther 2001; 12: 539-548.
Li Duan M, Bordet T, Mezzina M, Kahn A, Ulfendahl M. Adenoviral and adenoassociated viral vector mediated gene transfer in the guinea pig cochlea. Neuroreport 2002; 13: 1295-1299.
Liu Y, Okada T, Sheykholeslami K, Shimazaki K, Nomoto T, Muramatsu S et al. Specific and efficient transduction of Cochlear inner hair cells with recombinant adeno-associated virus type 3 vector. Mol Ther 2005; 12: 725-733.
Ballana E, Wang J, Venail F, Estivill X, Puel JL, Arbones ML et al. Efficient and specific transduction of cochlear supporting cells by adeno-associated virus serotype 5. Neurosci Lett 2008; 442: 134-139.
Konishi M, Kawamoto K, Izumikawa M, Kuriyama H, Yamashita T. Gene transfer into guinea pig cochlea using adeno-associated virus vectors. J Gene Med 2008; 10: 610-618.
Bedrosian JC, Gratton MA, Brigande JV, Tang W, Landau J, Bennett J. In vivo delivery of recombinant viruses to the fetal murine cochlea: transduction characteristics and long-term effects on auditory function. Mol Ther 2006; 14: 328-335.
Lalwani A, Walsh B, Reilly P, Carvalho G, Zolotukhin S, Muzyczka N et al. Long-term in vivo cochlear transgene expression mediated by recombinant adeno-associated virus. Gene Therapy 1998; 5: 277-281.
Kilpatrick LA, Li Q, Yang J, Goddard JC, Fekete DM, Lang H. Adeno-associated virus-mediated gene delivery into the scala media of the normal and deafened adult mouse ear. Gene Therapy 2011; 18: 569-578.
Alexopoulou AN, Couchman JR, Whiteford Jr. The CMV early enhancer/chicken beta actin (CAG) promoter can be used to drive transgene expression during the differentiation of murine embryonic stem cells into vascular progenitors. BMC Cell Biol 2008; 9: 2.
Liu Y, Okada T, Nomoto T, Ke X, Kume A, Ozawa K et al. Promoter effects of adenoassociated viral vector for transgene expression in the cochlea in vivo. Exp Mol Med 2007; 39: 170-175.
Luchsinger E, Strobbe R, Wellemans G, Dekegel D, Sprecher-Goldberger S. [Haemagglutinating adeno-associated virus (AAV) in association with bovine adenovirus type 1. Brief report]. Arch Gesamte Virusforsch 1970; 31: 390-392.
Di Pasquale G, Rzadzinska A, Schneider ME, Bossis I, Chiorini JA, Kachar B. A novel bovine virus efficiently transduces inner ear neuroepithelial cells. Mol Ther 2005; 11: 849-855.
Shibata SB, Di Pasquale G, Cortez SR, Chiorini JA, Raphael Y. Gene transfer using bovine adeno-associated virus in the guinea pig cochlea. Gene Therapy 2009; 16: 990-997.
Liu Y, Okada T, Shimazaki K, Sheykholeslami K, Nomoto T, Muramatsu S et al. Protection against aminoglycoside-induced ototoxicity by regulated AAV vectormediated GDNF gene transfer into the cochlea. Mol Ther 2008; 16: 474-480.
Shibata SB, Cortez SR, Beyer LA, Wiler JA, Di Polo A, Pfingst BE et al. Transgenic BDNF induces nerve fiber regrowth into the auditory epithelium in deaf cochleae. Exp Neurol 2010; 223: 464-472.
Crispino G, Di Pasquale G, Scimemi P, Rodriguez L, Galindo Ramirez F, De Siati RD et al. BAAV mediated GJB2 gene transfer restores gap junction coupling in cochlear organotypic cultures from deaf Cx26Sox10Cre mice. PLoS One 2011; 6: e23279.
Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998; 72: 9873-9880.
Han JJ, Mhatre AN, Wareing M, Pettis R, Gao WQ, Zufferey RN et al. Transgene expression in the guinea pig cochlea mediated by a lentivirus-derived gene transfer vector. Hum Gene Ther 1999; 10: 1867-1873.
Pietola L, Aarnisalo AA, Joensuu J, Pellinen R, Wahlfors J, Jero J. HOX-GFP and WOX-GFP lentivirus vectors for inner ear gene transfer. Acta Otolaryngol 2008; 128: 613-620.
Lei L, Han D. Efficient transduction of spiral ganglion cells using adenovirus type 5 vector in the rat. Acta Otolaryngol 2010; 130: 810-814.
Epstein AL. Progress and prospects: biological properties and technological advances of herpes simplex virus type 1-based amplicon vectors. Gene Therapy 2009; 16: 709-715.
Chen X, Frisina RD, Bowers WJ, Frisina DR, Federoff HJ. HSV amplicon-mediated neurotrophin-3 expression protects murine spiral ganglion neurons from cisplatin- induced damage. Mol Ther 2001; 3: 958-963.
Staecker H, Liu W, Malgrange B, Lefebvre PP, Van De Water TR. Vector-mediated delivery of bcl-2 prevents degeneration of auditory hair cells and neurons after injury. ORL J Otorhinolaryngol Relat Spec 2007; 69: 43-50.
Geschwind MD, Hartnick CJ, Liu W, Amat J, Van De Water TR, Federoff HJ. Defective HSV-1 vector expressing BDNF in auditory ganglia elicits neurite outgrowth: model for treatment of neuron loss following cochlear degeneration. Hum Gene Ther 1996; 7: 173-182.
Bowers WJ, Chen X, Guo H, Frisina DR, Federoff HJ, Frisina RD. Neurotrophin-3 transduction attenuates cisplatin spiral ganglion neuron ototoxicity in the cochlea. Mol Ther 2002; 6: 12-18.
Staecker H, Li D, O'Malley Jr. BW, Van De Water TR. Gene expression in the mammalian cochlea: a study of multiple vector systems. Acta Otolaryngol 2001; 121: 157-163.
Staecker H, Gabaizadeh R, Federoff H, Van De Water TR. Brain-derived neurotrophic factor gene therapy prevents spiral ganglion degeneration after hair cell loss. Otolaryngol Head Neck Surg 1998; 119: 7-13.
Derby ML, Sena-Esteves M, Breakefield XO, Corey DP. Gene transfer into the mammalian inner ear using HSV-1 and vaccinia virus vectors. Hear Res 1999; 134: 1-8.
Bitzer M, Armeanu S, Lauer UM, Neubert WJ. Sendai virus vectors as an emerging negative-strand RNA viral vector system. J Gene Med 2003; 5: 543-553.
Hosoya N, Miura T, Kawana-Tachikawa A, Koibuchi T, Shioda T, Odawara T et al. Comparison between Sendai virus and adenovirus vectors to transduce HIV-1 genes into human dendritic cells. J Med Virol 2008; 80: 373-382.
Kanzaki S, Shiotani A, Inoue M, Hasegawa M, Ogawa K. Sendai virus vectormediated transgene expression in the cochlea in vivo. Audiol Neurootol 2007; 12: 119-126.
Wrobel I, Collins D. Fusion of cationic liposomes with mammalian cells occurs after endocytosis. Biochim Biophys Acta 1995; 1235: 296-304.
Zhang W, Zhang Y, Sood R, Ranjan S, Surovtseva E, Ahmad A et al. Visualization of intracellular trafficking of Math1 protein in different cell types with a newlyconstructed nonviral gene delivery plasmid. J Gene Med 2011; 13: 134-144.
Zine A, Van De Water TR, de Ribaupierre F. Notch signaling regulates the pattern of auditory hair cell differentiation in mammals. Development 2000; 127: 3373-3383.
Wareing M, Mhatre AN, Pettis R, Han JJ, Haut T, Pfister MH et al. Cationic liposome mediated transgene expression in the guinea pig cochlea. Hear Res 1999; 128: 61-69.
Jero J, Tseng CJ, Mhatre AN, Lalwani AK. A surgical approach appropriate for targeted cochlear gene therapy in the mouse. Hear Res 2001; 151: 106-114.
Zou J, Saulnier P, Perrier T, Zhang Y, Manninen T, Toppila E et al. Distribution of lipid nanocapsules in different cochlear cell populations after round window membrane permeation. J Biomed Mater Res B Appl Biomater 2008; 87: 10-18.
Gao X, Kim KS, Liu D. Nonviral gene delivery: what we know and what is next. Aaps J 2007; 9: E92-104.
Zhang W, Zhang Y, Lobler M, Schmitz KP, Ahmad A, Pyykko I et al. Nuclear entry of hyperbranched polylysine nanoparticles into cochlear cells. Int J Nanomed 2011; 6: 535-546.
Tan BT, Foong KH, Lee MM, Ruan R. Polyethylenimine-mediated cochlear gene transfer in guinea pigs. Arch Otolaryngol Head Neck Surg 2008; 134: 884-891.
Tamura T, Kita T, Nakagawa T, Endo T, Kim TS, Ishihara T et al. Drug delivery to the cochlea using PLGA nanoparticles. Laryngoscope 2005; 115: 2000-2005.
Heller LC, Ugen K, Heller R. Electroporation for targeted gene transfer. Expert Opin Drug Deliv 2005; 2: 255-268.
Favard C, Dean DS, Rols MP. Electrotransfer as a non viral method of gene delivery. Curr Gene Ther 2007; 7: 67-77.
Zheng JL, Gao WQ. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 2000; 3: 580-586.
Ono K, Nakagawa T, Kojima K, Matsumoto M, Kawauchi T, Hoshino M et al. Silencing p27 reverses post-mitotic state of supporting cells in neonatal mouse cochleae. Mol Cell Neurosci 2009; 42: 391-398.
Jones JM, Montcouquiol M, Dabdoub A, Woods C, Kelley MW. Inhibitors of differentiation and DNA binding (Ids) regulate Math1 and hair cell formation during the development of the organ of Corti. J Neurosci 2006; 26: 550-558.
Driver EC, Kelley MW. Transfection of mouse cochlear explants by electroporation. Current Protocols in Neuroscience, 2010; Chapter 4, Unit 4.34 1-10.
Puligilla C, Dabdoub A, Brenowitz SD, Kelley MW. Sox2 induces neuronal formation in the developing mammalian cochlea. J Neurosci 2010; 30: 714-722.
Hayashi T, Lamba DA, Slowik A, Reh TA, Bermingham-McDonogh O. A method for stabilizing RNA for transfection that allows control of expression duration. Dev Dyn 2010; 239: 2034-2040.
Gubbels SP, Woessner DW, Mitchell JC, Ricci AJ, Brigande JV. Functional auditory hair cells produced in the mammalian cochlea by in utero gene transfer. Nature 2008; 455: 537-541.
Belyantseva IA. Helios Gene Gun-mediated transfection of the inner ear sensory epithelium. Methods Mol Biol 2009; 493: 103-123.
Belyantseva IA, Boger ET, Friedman TB. Myosin XVa localizes to the tips of inner ear sensory cell stereocilia and is essential for staircase formation of the hair bundle. Proc Natl Acad Sci USA 2003; 100: 13958-13963.
Belyantseva IA, Boger ET, Naz S, Frolenkov GI, Sellers JR, Ahmed ZM et al. Myosin- XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 2005; 7: 148-156.
Toyama K, Ozeki M, Hamajima Y, Lin J. Expression of the integrin genes in the developing cochlea of rats. Hear Res 2005; 201: 21-26.
Woods C, Montcouquiol M, Kelley MW. Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 2004; 7: 1310-1318.
Brigande JV, Gubbels SP, Woessner DW, Jungwirth JJ, Bresee CS. Electroporationmediated gene transfer to the developing mouse inner ear. Methods Mol Biol 2009; 493: 125-139.