Dispensability of tubulin acetylation for 15-protofilament microtubule formation in the mammalian cochlea.

Renauld, Justine; Thelen, Nicolas; Bartholomé, Odile; Malgrange, Brigitte; Thiry, Marc

doi:10.1247/csf.20057

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Dispensability of tubulin acetylation for 15-protofilament microtubule formation in the mammalian cochlea.

Renauld, Justine; Thelen, Nicolas; Bartholomé, Odile et al.

2021 • In Cell Structure and Function

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https://hdl.handle.net/2268/255969

DOI
10.1247/csf.20057

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33473065

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Keywords :

Acetylation; cytoskeleton; inner ear; microtubule; supporting cells

Abstract :

[en] The development of hearing in mammals requires the formation and maturation of a highly organized and specialized epithelium known as the organ of Corti. This epithelium contains two types of cells, the sensory cells, which are the true receptors of auditory information, and the surrounding supporting cells, which are composed of a highly developed cytoskeleton essential to the architecture of the mature organ of Corti. The supporting cells are the only mammalian cells reported to contain the unusual 15-protofilament microtubules. In this paper, we show that 15-protofilament microtubules appear between the second and fourth day after birth in the pillar cells of the organ of Corti in mice. We also show that contrary to what has been described in the nematode worm Caenorhabiditis. Elegans, microtubule acetylation is not essential for the formation of 15-protofilament microtubules in mice but is required for fine-tuning of their diameter. Key words: Acetylation, cytoskeleton, microtubule, inner ear, supporting cells.

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Renauld, Justine ; Université de Liège > Département des sciences de la vie > GIGA-R : Biologie cellulaire

Thelen, Nicolas ; Université de Liège - ULiège > Département des sciences de la vie > Biologie cellulaire

Bartholomé, Odile ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine

Malgrange, Brigitte ; Université de Liège - ULiège > Stem Cells-Developmental Neurobiology

Thiry, Marc ; Université de Liège - ULiège > Département des sciences de la vie > Biologie cellulaire

Language :

English

Title :

Dispensability of tubulin acetylation for 15-protofilament microtubule formation in the mammalian cochlea.

Publication date :

2021

Journal title :

Cell Structure and Function

ISSN :

0386-7196

eISSN :

1347-3700

Publisher :

Japan Society for Cell Biology, Japan

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 27 January 2021

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Bibliography

Akella, J.S., Wloga, D., Kim, J., Starostina, N.G., Lyons-Abbott, S., Morrissette, N.S., Dougan, S.T., Kipreos, E.T., and Gaertig, J. 2010. MEC-17 is an α-tubulin acetyltransferase. Nature, 467: 218–222.
Akhmanova, A. and Severin, F. 2004. Thirteen is the lucky number for doublecortin. Dev. Cell, 7: 5–6.
Andrade, L.R. 2015. Evidence for changes in beta-and gamma-actin pro-portions during inner ear hair cell life. Cytoskeleton, 72: 282–291.
Ayoub, A.T., Klobukowski, M., and Tuszynski, J.A. 2015. Detailed Per-residue Energetic Analysis Explains the Driving Force for Microtubule Disassembly. PLoS Comput. Biol., 11: 1–21.
Bounoutas, A., O’Hagan, R., and Chalfie, M. 2009. The Multipurpose 15-Protofilament Microtubules in C. elegans Have Specific Roles in Mechanosensation. Curr. Biol., 19: 1362–1367.
Chaaban, S. and Brouhard, G.J. 2017. A microtubule bestiary: Structural diversity in tubulin polymers. Mol. Biol. Cell, 28: 2924–2931.
Chalfie, M. and Thomson, J.N. 1982. Structural and functional diversity in the neuronal microtubules of Caenorhabditis elegans. J. Cell Biol., 93: 15–23.
Chen, S., Xie, L., Xu, K., Cao, H.-Y., Wu, X., Xu, X.-X., Sun, Y., and Kong, W.-J. 2018. Developmental abnormalities in supporting cell pha-langeal processes and cytoskeleton in the Gjb2 knockdown mouse model. Dis. Model. Mech., 11: dmm033019.
Cueva, J.G., Hsin, J., Huang, K.C., Goodman, M.B., and Cueva et al. 2012. Posttranslational Acetylation of α-Tubulin Constrains Protofila-ment Number in Native Microtubules. Curr. Biol., 22: 1066–1074.
Fukushige, T., Siddiqui, Z.K., Chou, M., Culotti, J.G., Gogonea, C.B., Siddiqui, S.S., and Hamelin, M. 1999. MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J. Cell Sci., 112 (Pt 3): 395– 403.
Gaertig, J., Cruz, M.A., Bowen, J., Gu, L., Pennock, D.G., and Gorovsky, M.A. 1995. Acetylation of lysine 40 in a-tubulin is not essential in Tet-rahymena thermophila. J. Cell Biol., 129: 1301–1310.
Hammer, Ø., Harper, D.A.T., and Paul D. Ryan. 2001. Past: Paleontologi-cal statistics software package for education and data analysis. Palaeon-tol. Electron., 4: 1–9.
Henderson, C.G., Tucker, J.B., Chaplin, M. a, Mackie, J.B., Maidment, S.N., Mogensen, M.M., and Paton, C.C. 1994. Reorganization of the centrosome and associated microtubules during the morphogenesis of a mouse cochlear epithelial cell. J. Cell Sci., 107 (Pt 2): 589–600.
Henderson, C.G., Tucker, J.B., Mogensen, M.M., Mackie, J.B., Chaplin, M.a, Slepecky, N.B., and Leckie, L.M. 1995. Three microtubule-organizing centres collaborate in a mouse cochlear epithelial cell during supracellularly coordinated control of microtubule positioning. J. Cell Sci., 108 (Pt 1): 37–50.
Howes, S.C., Alushin, G.M., Shida, T., Nachury, M.V., and Nogales, E. 2014. Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol. Biol. Cell, 25: 257–266.
Ito, M., Spicer, S.S., and Schulte, B.a. 1995. Cytological changes related to maturation of the organ of Corti and opening of Corti’s tunnel. Hear. Res., 88: 107–123.
Janke, C. 2014. The tubulin code: Molecular components, readout mecha-nisms, functions. J. Cell Biol., 206: 461–472.
Janke, C. and Montagnac, G. 2017. Causes and Consequences of Microtu‐ bule Acetylation. Curr. Biol., 27: R1287–R1292.
Kalebic, N., Sorrentino, S., Perlas, E., Bolasco, G., Martinez, C., and Heppenstall, P.A. 2013. αTAT1 is the major α-tubulin acetyltransferase in mice. Nat. Commun., 4: 1962.
Katsuki, M., Drummond, D.R., and Cross, R.A. 2014. Ectopic A-lattice seams destabilize microtubules. Nat. Commun., 5: 3094.
Kikuchi, T., Takasaka, T., Tonosaki, A., Katori, Y., and Shinkawa, H. 1991. Microtubules of guinea pig cochlear epithelial cells. Acta Otolar-yngol., 111: 286–290.
Kim, G.-W., Li, L., Gorbani, M., You, L., and Yang, X.-J. 2013. Mice Lacking α-Tubulin Acetyltransferase 1 Are Viable but Display α-Tubulin Acetylation Deficiency and Dentate Gyrus Distortion. J. Biol. Chem., 288: 20334–20350.
Kozminski, K.G., Diener, D.R., and Rosenbaum, J.L. 1993. High level expression of nonacetylatable alpha-tubulin in Chlamydomonas rein-hardtii. Cell Motil. Cytoskeleton, 25: 158–170.
Li, H., DeRosier, D.J., Nicholson, W.V., Nogales, E., and Downing, K.H. 2002. Microtubule structure at 8 A resolution. Structure, 10: 1317– 1328.
Li, L. and Yang, X.-J. 2015. Tubulin acetylation: responsible enzymes, biological functions and human diseases. Cell. Mol. Life Sci., 72: 4237– 4255.
Liew, K.M., Xiang, P., and Zhang, L.W. 2015. Mechanical properties and characteristics of microtubules: A review. Compos. Struct., 123: 98– 108.
Liu, W., Wang, C., Yu, H., Liu, S., and Yang, J. 2018. Expression of ace-tylated tubulin in the postnatal developing mouse cochlea. Eur. J. Histo-chem., 62: 2942.
Meurer-Grob, P., Kasparian, J., and Wade, R.H. 2001. Microtubule structure at improved resolution. Biochemistry, 40: 8000–8008.
Moores, C. a, Perderiset, M., Francis, F., Chelly, J., Houdusse, A., and Milligan, R.a. 2004. Mechanism of microtubule stabilization by dou-blecortin. Mol. Cell, 14: 833–839.
Pickles, J.O. 2015. Auditory pathways: Anatomy and physiology, 1st ed.
Raff, E.C. 1997. Microtubule Architecture Specified by a beta-Tubulin Isoform. Science (80-.)., 275: 70–73.
Renauld, J., Johnen, N., Thelen, N., Cloes, M., and Thiry, M. 2015. Spatio-temporal dynamics of β-tubulin isotypes during the development of the sensory auditory organ in rat. Histochem. Cell Biol., 144: 403– 416.
Reynolds, E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol., 17: 208–212.
Roth, B. and Bruns, V. 1992. Postnatal development of the rat organ of Corti II. Hair cell receptors and their supporting elements. Anat. Embryol. (Berl)., 185: 571–581.
Savage, C., Hamelin, M., Culotti, J.G., Coulson, a, Albertson, D.G., and Chalfie, M. 1989. mec-7 is a beta-tubulin gene required for the produc-tion of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev., 3: 870–881.
Shida, T., Cueva, J.G., Xu, Z., Goodman, M.B., and Nachury, M.V. 2010. The major α-tubulin K40 acetyltransferase αTAT1 promotes rapid cilio-genesis and efficient mechanosensation. Proc. Natl. Acad. Sci. USA, 107: 21517–21522.
Sui, H. and Downing, K.H. 2010. Structural basis of interprotofilament interaction and lateral deformation of microtubules. Structure, 18: 1022–1031.
Szarama, K.B., Gavara, N., Petralia, R.S., Kelley, M.W., and Chadwick, R.S. 2012. Cytoskeletal changes in actin and microtubules underlie the developing surface mechanical properties of sensory and supporting cells in the mouse cochlea. Development, 139: 2187–2197.
Tannenbaum, J. and Slepecky, N.B. 1997. Localization of microtubules containing posttranslationally modified tubulin in cochlear epithelial cells during development. Cell Motil. Cytoskeleton, 38: 146–162.
Ti, S.C., Alushin, G.M., and Kapoor, T.M. 2018. Human β-Tubulin Iso-types Can Regulate Microtubule Protofilament Number and Stability. Dev. Cell, 47: 175-190.e5.
Tilney, L.G., Bryan, J., Bush, D.J., Fujiwara, K., Mooseker, M.S., Murphy, D.B., and Snyder, D.H. 1973. Microtubules: evidence for 13 protofila-ments. J. Cell Biol., 59: 267–275.
Tolomeo, J.A. and Holley, M.C. 1997. Mechanics of microtubule bundles in pillar cells from the inner ear. Biophys. J., 73: 2241–2247.
Topalidou, I., Keller, C., Kalebic, N., Nguyen, K.C.Q., Somhegyi, H., Politi, K.A., Heppenstall, P., Hall, D.H., and Chalfie, M. 2012. Geneti-cally separable functions of the MEC-17 tubulin acetyltransferase affect microtubule organization. Curr. Biol., 22: 1057–1065.
Tucker, J.B., Paton, C.C., Richardson, G.P., Mogensen, M.M., and Russell, I.J. 1992. A cell surface-associated centrosomal layer of microtubule-organizing material in the inner pillar cell of the mouse cochlea. J. Cell Sci., 102 (Pt 2): 215–226.
Wade, R.H. 2009. On and around microtubules: an overview. Mol. Bio-technol., 43: 177–191.
Zetes, D.E., Tolomeo, J.a., and Holley, M.C. 2012. Structure and Mechanics of Supporting Cells in the Guinea Pig Organ of Corti. PLoS One, 7: e49338.
Zhang, Y., Kwon, S., Yamaguchi, T., Cubizolles, F., Rousseaux, S., Kneissel, M., Cao, C., Li, N., Cheng, H.-L., Chua, K., Lombard, D., Mizeracki, A., Matthias, G., Alt, F.W., Khochbin, S., and Matthias, P. 2008. Mice Lacking Histone Deacetylase 6 Have Hyperacetylated Tubulin but Are Viable and Develop Normally. Mol. Cell. Biol., 28: 1688–1701.