The 133-kDa N-terminal domain enables myosin 15 to maintain mechanotransducing stereocilia and is essential for hearing

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages

  Fang, Qing ^a   Indzhykulian, Artur A ^b,e   Mustapha, Mirna ^a,f   Riordan, Gavin P ^c   Dolan, David F ^d   Friedman, Thomas B ^c   Belyantseva, Inna A ^c   Frolenkov, Gregory I ^b   Camper, Sally A ^a   Bird, Jonathan E ^c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN; ISOPROTEIN; MYO15 PROTEIN, MOUSE; PROTEIN BINDING;

133 KD AMINO TERMINAL SEQUENCE; ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DISEASE SEVERITY; EVOKED BRAIN STEM AUDITORY RESPONSE; GENE AMPLIFICATION; GENE MUTATION; GENE SEQUENCE; HAIR CELL; HEARING; HEARING IMPAIRMENT; IMMUNOFLUORESCENCE; IMMUNOGOLD ELECTRON MICROSCOPY; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PROTEIN INTERACTION; PROTEIN STRUCTURE; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SCANNING ELECTRON MICROSCOPY; STEREOCILIUM; TRANSMISSION ELECTRON MICROSCOPY; VESTIBULAR DISORDER; ANIMAL; COCHLEAR HAIR CELL; GENETICS; INNER EAR; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; EAR, INNER; HAIR CELLS, AUDITORY; HEARING; MICE; MICE, KNOCKOUT; MYOSINS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; STEREOCILIA;

EID: 84943763606     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08627     Document Type: Article

References (60)

1. Anderson DW, Probst FJ, Belyantseva IA, Fridell RA, Beyer L, Martin DM, Wu D, Kachar B, Friedman TB, Raphael Y, Camper SA. 2000. The motor and tail regions of myosin XV are critical for normal structure and function of auditory and vestibular hair cells. Human Molecular Genetics 9:1729–1738. doi: 10.1093/hmg/9.12.1729.
2. Barr-Gillespie PG. 2015. Assembly of hair bundles, an amazing problem for cell biology. Molecular Biology of the Cell 26:2727–2732. doi: 10.1091/mbc.E14-04-0940.
3. Bashir R, Fatima A, Naz S. 2012. Prioritized sequencing of the second exon of MYO15A reveals a new mutation segregating in a Pakistani family with moderate to severe hearing loss. European Journal of Medical Genetics 55: 99–102. doi: 10.1016/j.ejmg.2011.12.003.
4. Belyantseva IA, Boger ET, Friedman TB. 2003. Myosin XVa localizes to the tips of inner ear sensory cell stereocilia and is essential for staircase formation of the hair bundle. Proceedings of the National Academy of Sciences of USA 100:13958–13963. doi: 10.1073/pnas.2334417100.
5. Belyantseva IA, Boger ET, Naz S, Frolenkov GI, Sellers JR, Ahmed ZM, Griffith AJ, Friedman TB. 2005. Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nature Cell Biology 7: 148–156. doi: 10.1038/ncb1219.
6. Beurg M, Fettiplace R, Nam JH, Ricci AJ. 2009. Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging. Nature Neuroscience 12:553–558. doi: 10.1038/nn.2295.
7. Bird JE, Takagi Y, Billington N, Strub MP, Sellers JR, Friedman TB. 2014. Chaperone-enhanced purification of unconventional myosin 15, a molecular motor specialized for stereocilia protein trafficking. Proceedings of the National Academy of Sciences of USA 111:12390–12395. doi: 10.1073/pnas.1409459111.
8. Brawley CM, Rock RS. 2009. Unconventional myosin traffic in cells reveals a selective actin cytoskeleton. Proceedings of the National Academy of Sciences of USA 106:9685–9690. doi: 10.1073/pnas.0810451106.
9. Caberlotto E, Michel V, Foucher I, Bahloul A, Goodyear RJ, Pepermans E, Michalski N, Perfettini I, Alegria-Prevot O, Chardenoux S, Do Cruzeiro M, Hardelin JP, Richardson GP, Avan P, Weil D, Petit C. 2011. Usher type 1G protein sans is a critical component of the tip-link complex, a structure controlling actin polymerization in stereocilia. Proceedings of the National Academy of Sciences of USA 108:5825–5830. doi: 10.1073/pnas.1017114108.
10. Cengiz FB, Duman D, Sirmaci A, Tokgoz-Yilmaz S, Erbek S, Ozturkmen-Akay H, Incesulu A, Edwards YJ, Ozdag H, Liu XZ, Tekin M. 2010. Recurrent and private MYO15A mutations are associated with deafness in the Turkish population. Genetic Testing and Molecular Biomarkers 14:543–550. doi: 10.1089/gtmb.2010.0039.
11. Chui D, Oh-Eda M, Liao YF, Panneerselvam K, Lal A, Marek KW, Freeze HH, Moremen KW, Fukuda MN, Marth JD. 1997. Alpha-mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 90:157–167. doi: 10.1016/S0092-8674(00)80322-0.
12. Delprat B, Michel V, Goodyear R, Yamasaki Y, Michalski N, El-Amraoui A, Perfettini I, Legrain P, Richardson G, Hardelin JP, Petit C. 2005. Myosin XVa and whirlin, two deafness gene products required for hair bundle growth, are located at the stereocilia tips and interact directly. Human Molecular Genetics 14:401–410. doi: 10.1093/hmg/ddi036.
13. DeRosier DJ, Tilney LG. 2000. F-actin bundles are derivatives of microvilli: what does this tell us about how bundles might form? The Journal of Cell Biology 148:1–6. doi: 10.1083/jcb.148.1.1.
14. Disanza A, Carlier MF, Stradal TE, Didry D, Frittoli E, Confalonieri S, Croce A, Wehland J, Di Fiore PP, Scita G. 2004. Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nature Cell Biology 6: 1180–1188. doi: 10.1038/ncb1199.
15. Dishinger JF, Kee HL, Jenkins PM, Fan S, Hurd TW, Hammond JW, Truong YN, Margolis B, Martens JR, Verhey KJ. 2010. Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-beta2 and RanGTP. Nature Cell Biology 12:703–710. doi: 10.1038/ncb2073.
16. Diz-Munoz A, Fletcher DA, Weiner OD. 2013. Use the force: membrane tension as an organizer of cell shape and motility. Trends in Cell Biology 23:47–53. doi: 10.1016/j.tcb.2012.09.006.
17. Drummond MC, Barzik M, Bird JE, Zhang DS, Lechene CP, Corey DP, Cunningham LL, Friedman TB. 2015. Live-cell imaging of actin dynamics reveals mechanisms of stereocilia length regulation in the inner ear. Nature Communications 6:6873. doi: 10.1038/ncomms7873.
18. Drummond MC, Belyantseva IA, Friderici KH, Friedman TB. 2012. Actin in hair cells and hearing loss. Hearing Research 288:89–99. doi: 10.1016/j.heares.2011.12.003.
19. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z. 2002. Intrinsic disorder and protein function. Biochemistry 41:6573–6582. doi: 10.1021/bi012159+.
20. Fattahi Z, Shearer AE, Babanejad M, Bazazzadegan N, Almadani SN, Nikzat N, Jalalvand K, Arzhangi S, Esteghamat F, Abtahi R, Azadeh B, Smith RJ, Kahrizi K, Najmabadi H. 2012. Screening for MYO15A gene mutations in autosomal recessive nonsyndromic, GJB2 negative Iranian deaf population. American Journal of Medical Genetics. Part A 158A:1857–1864. doi: 10.1002/ajmg.a.34411.
21. Francis SP, Krey JF, Krystofiak ES, Cui R, Nanda S, Xu W, Kachar B, Barr-Gillespie PG, Shin JB. 2015. A short splice form of Xin-actin binding repeat containing 2 (XIRP2) lacking the Xin repeats is required for maintenance of stereocilia morphology and hearing function. The Journal of Neuroscience 35:1999–2014. doi: 10.1523/JNEUROSCI.3449-14.2015.
22. Friedman TB, Liang Y, Weber JL, Hinnant JT, Barber TD, Winata S, Arhya IN, Asher JH Jr. 1995. A gene for congenital, recessive deafness DFNB3 maps to the pericentromeric region of chromosome 17. Nature Genetics 9:86–91. doi: 10.1038/ng0195-86.
23. Furness DN, Johnson SL, Manor U, Ruttiger L, Tocchetti A, Offenhauser N, Olt J, Goodyear RJ, Vijayakumar S, Dai Y, Hackney CM, Franz C, Di Fiore PP, Masetto S, Jones SM, Knipper M, Holley MC, Richardson GP, Kachar B, Marcotti W. 2013. Progressive hearing loss and gradual deterioration of sensory hair bundles in the ears of mice lacking the actin-binding protein Eps8L2. Proceedings of the National Academy of Sciences of USA 110: 13898–13903. doi: 10.1073/pnas.1304644110.
24. Hartman MA, Finan D, Sivaramakrishnan S, Spudich JA. 2011. Principles of unconventional myosin function and targeting. Annual Review of Cell and Developmental Biology 27:133–155. doi: 10.1146/annurev-cellbio-100809-151502.
25. Howard J, Hudspeth AJ. 1987. Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog’s saccular hair cell. Proceedings of the National Academy of Sciences of USA 84: 3064–3068. doi: 10.1073/pnas.84.9.3064.
26. Hu Q, Milenkovic L, Jin H, Scott MP, Nachury MV, Spiliotis ET, Nelson WJ. 2010. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329:436–439. doi: 10.1126/science.1191054.
27. Karolyi IJ, Dootz GA, Halsey K, Beyer L, Probst FJ, Johnson KR, Parlow AF, Raphael Y, Dolan DF, Camper SA. 2007. Dietary thyroid hormone replacement ameliorates hearing deficits in hypothyroid mice. Mammalian Genome 18:596–608. doi: 10.1007/s00335-007-9038-0.
28. Kawashima Y, Geleoc GS, Kurima K, Labay V, Lelli A, Asai Y, Makishima T, Wu DK, Della Santina CC, Holt JR, Griffith AJ. 2011. Mechanotransduction in mouse inner ear hair cells requires transmembrane channel-like genes. The Journal of Clinical Investigation 121:4796–4809. doi: 10.1172/JCI60405.
29. Kitajiri S, Sakamoto T, Belyantseva IA, Goodyear RJ, Stepanyan R, Fujiwara I, Bird JE, Riazuddin S, Ahmed ZM, Hinshaw JE, Sellers J, Bartles JR, Hammer JA, Richardson GP, Griffith AJ, Frolenkov GI, Friedman TB. 2010. Actin-bundling protein TRIOBP forms resilient rootlets of hair cell stereocilia essential for hearing. Cell 141: 786–798. doi: 10.1016/j.cell.2010.03.049.
30. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H. 1996. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proceedings of the National Academy of Sciences of USA 93:5860–5865. doi: 10.1073/pnas.93.12.5860.
31. Liang Y, Wang A, Belyantseva IA, Anderson DW, Probst FJ, Barber TD, Miller W, Touchman JW, Jin L, Sullivan SL, Sellers JR, Camper SA, Lloyd RV, Kachar B, Friedman TB, Fridell RA. 1999. Characterization of the human and mouse unconventional myosin XV genes responsible for hereditary deafness DFNB3 and shaker 2. Genomics 61: 243–258. doi: 10.1006/geno.1999.5976.
32. Linke WA, Ivemeyer M, Mundel P, Stockmeier MR, Kolmerer B. 1998. Nature of PEVK-titin elasticity in skeletal muscle. Proceedings of the National Academy of Sciences of USA 95:8052–8057. doi: 10.1073/pnas.95.14.8052.
33. Ma K, Forbes JG, Gutierrez-Cruz G, Wang K. 2006. Titin as a giant scaffold for integrating stress and Src homology domain 3-mediated signaling pathways: the clustering of novel overlap ligand motifs in the elastic PEVK segment. The Journal of Biological Chemistry 281:27539–27556. doi: 10.1074/jbc.M604525200.
34. Manley GA. 2000. Cochlear mechanisms from a phylogenetic viewpoint. Proceedings of the National Academy of Sciences of USA 97:11736–11743. doi: 10.1073/pnas.97.22.11736.
35. Manor U, Disanza A, Grati M, Andrade L, Lin H, Di Fiore PP, Scita G, Kachar B. 2011. Regulation of stereocilia length by myosin XVa and whirlin depends on the actin-regulatory protein Eps8. Current Biology 21:167–172. doi: 10.1016/j.cub.2010.12.046.
36. Manor U, Kachar B. 2008. Dynamic length regulation of sensory stereocilia. Seminars in Cell & Developmental Biology 19:502–510. doi: 10.1016/j.semcdb.2008.07.006.
37. Mburu P, Mustapha M, Varela A, Weil D, El-Amraoui A, Holme RH, Rump A, Hardisty RE, Blanchard S, Coimbra RS, Perfettini I, Parkinson N, Mallon AM, Glenister P, Rogers MJ, Paige AJ, Moir L, Clay J, Rosenthal A, Liu XZ, Blanco G, Steel KP, Petit C, Brown SD. 2003. Defects in whirlin, a PDZ domain molecule involved in stereocilia elongation, cause deafness in the whirler mouse and families with DFNB31. Nature Genetics 34:421–428. doi: 10.1038/ng1208.
38. Nal N, Ahmed ZM, Erkal E, Alper OM, Luleci G, Dinc¸ O, Waryah AM, Ain Q, Tasneem S, Husnain T, Chattaraj P, Riazuddin S, Boger E, Ghosh M, Kabra M, Riazuddin S, Morell RJ, Friedman TB. 2007. Mutational spectrum of MYO15A: the large N-terminal extension of myosin XVA is required for hearing. Human Mutation 28:1014–1019. doi: 10.1002/humu.20556.
39. Narayanan P, Chatterton P, Ikeda A, Ikeda S, Corey DP, Ervasti JM, Perrin BJ. 2015. Length regulation of mechanosensitive stereocilia depends on very slow actin dynamics and filament-severing proteins. Nature Communications 6:6855. doi: 10.1038/ncomms7855.
40. Peng AW, Salles FT, Pan B, Ricci AJ. 2011. Integrating the biophysical and molecular mechanisms of auditory hair cell mechanotransduction. Nature Communications 2:523. doi: 10.1038/ncomms1533.
41. Perrin BJ, Strandjord DM, Narayanan P, Henderson DM, Johnson KR, Ervasti JM. 2013. beta-Actin and fascin-2 cooperate to maintain stereocilia length. The Journal of Neuroscience 33:8114–8121. doi: 10.1523/JNEUROSCI.0238-13.2013.
42. Petralia RS, Wenthold RJ. 1999. Immunocytochemistry of NMDA receptors. Methods in Molecular Biology 128: 73–92. doi: 10.1385/1-59259-683-5:73.
43. Pickles JO, Comis SD, Osborne MP. 1984. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hearing Research 15:103–112. doi: 10.1016/0378-5955(84)90041-8.
44. Probst FJ, Fridell RA, Raphael Y, Saunders TL, Wang A, Liang Y, Morell RJ, Touchman JW, Lyons RH, Noben- Trauth K, Friedman TB, Camper SA. 1998. Correction of deafness in shaker-2 mice by an unconventional myosin in a BAC transgene. Science 280:1444–1447. doi: 10.1126/science.280.5368.1444.
45. Rzadzinska AK, Schneider ME, Davies C, Riordan GP, Kachar B. 2004. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. The Journal of Cell Biology 164:887–897. doi: 10.1083/jcb.200310055.
46. Scheffer DI, Zhang DS, Shen J, Indzhykulian A, Karavitaki KD, Xu YJ, Wang Q, Lin JJ, Chen ZY, Corey DP. 2015. XIRP2, an actin-binding protein essential for inner ear hair-cell stereocilia. Cell Reports 10:1811–1818. doi: 10.1016/j.celrep.2015.02.042.
47. Schneider ME, Belyantseva IA, Azevedo RB, Kachar B. 2002. Rapid renewal of auditory hair bundles. Nature 418: 837–838. doi: 10.1038/418837a.
48. Schwander M, Kachar B, Muller U. 2010. Review series: the cell biology of hearing. The Journal of Cell Biology 190: 9–20. doi: 10.1083/jcb.201001138.
49. Sellers JR, Knight PJ. 2007. Folding and regulation in myosins II and V. Journal of Muscle Research and Cell Motility 28:363–370. doi: 10.1007/s10974-008-9134-0.
50. Shen J, Scheffer DI, Kwan KY, Corey DP. 2015. SHIELD: an integrative gene expression database for inner ear research. Database 2015:bav071. doi: 10.1093/database/bav071.
51. Shin JB, Krey JF, Hassan A, Metlagel Z, Tauscher AN, Pagana JM, Sherman NE, Jeffery ED, Spinelli KJ, Zhao H, Wilmarth PA, Choi D, David LL, Auer M, Barr-Gillespie PG. 2013. Molecular architecture of the chick vestibular hair bundle. Nature Neuroscience 16:365–374. doi: 10.1038/nn.3312.
52. Stepanyan R, Frolenkov GI. 2009. Fast adaptation and Ca2+ sensitivity of the mechanotransducer require myosin- XVa in inner but not outer cochlear hair cells. The Journal of Neuroscience 29:4023–4034. doi: 10.1523/JNEUROSCI.4566-08.2009.
53. Taylor R, Bullen A, Johnson SL, Grimm-Gunter EM, Rivero F, Marcotti W, Forge A, Daudet N. 2015. Absence of plastin 1 causes abnormal maintenance of hair cell stereocilia and a moderate form of hearing loss in mice. Human Molecular Genetics 24:37–49. doi: 10.1093/hmg/ddu417.
54. Tilney LG, Egelman EH, DeRosier DJ, Saunder JC. 1983. Actin filaments, stereocilia, and hair cells of the bird cochlea. II. Packing of actin filaments in the stereocilia and in the cuticular plate and what happens to the organization when the stereocilia are bent. The Journal of Cell Biology 96:822–834. doi: 10.1083/jcb.96.3.822.
55. Tilney LG, Tilney MS, Cotanche DA. 1988. Actin filaments, stereocilia, and hair cells of the bird cochlea. V. How the staircase pattern of stereociliary lengths is generated. The Journal of Cell Biology 106:355–365. doi: 10.1083/jcb.106.2.355.
56. Wang A, Liang Y, Fridell RA, Probst FJ, Wilcox ER, Touchman JW, Morton CC, Morell RJ, Noben-Trauth K, Camper SA, Friedman TB. 1998. Association of unconventional myosin MYO15 mutations with human nonsyndromic deafness DFNB3. Science 280:1447–1451. doi: 10.1126/science.280.5368.1447.
57. Watanabe K, Nair P, Labeit D, Kellermayer MS, Greaser M, Labeit S, Granzier H. 2002. Molecular mechanics of cardiac titin’s PEVK and N2B spring elements. The Journal of Biological Chemistry 277:11549–11558. doi: 10.1074/jbc.M200356200.
58. Xiong W, Grillet N, Elledge HM, Wagner TF, Zhao B, Johnson KR, Kazmierczak P, Muller U. 2012. TMHS is an integral component of the mechanotransduction machinery of cochlear hair cells. Cell 151:1283–1295. doi: 10.1016/j.cell.2012.10.041.
59. Zampini V, Ruttiger L, Johnson SL, Franz C, Furness DN, Waldhaus J, Xiong H, Hackney CM, Holley MC, Offenhauser N, Di Fiore PP, Knipper M, Masetto S, Marcotti W. 2011. Eps8 regulates hair bundle length and functional maturation of mammalian auditory hair cells. PLOS Biology 9:e1001048. doi: 10.1371/journal.pbio.1001048.
60. Zhang DS, Piazza V, Perrin BJ, Rzadzinska AK, Poczatek JC, Wang M, Prosser HM, Ervasti JM, Corey DP, Lechene CP. 2012. Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 481:520–524. doi: 10.1038/nature10745.