The actin-binding proteins Eps8 and gelsolin have complementary roles in regulating the growth and stability of mechanosensory hair bundles of mammalian cochlear outer hair cells

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Olt, Jennifer ^a   Mburu, Philomena ^b   Johnson, Stuart L ^a   Parker, Andy ^b   Kuhn, Stephanie ^a,c   Bowl, Mike ^b   Marcotti, Walter ^a   Brown, Steve D M ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN BINDING PROTEIN; GELSOLIN; MUTANT PROTEIN; PROTEIN EPS8; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; COCHLEA; CONTROLLED STUDY; DEVELOPMENTAL STAGE; GROWTH REGULATION; HAIR CELL; HEARING; KNOCKOUT MOUSE; MAMMAL CELL; MECHANOTRANSDUCTION; MEMBRANE CURRENT; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; SENSORY RECEPTOR; STEREOCILIUM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CYTOSKELETAL PROTEINS; GELSOLIN; HAIR CELLS, AUDITORY, OUTER; IMMUNOHISTOCHEMISTRY; MECHANORECEPTORS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, SCANNING; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS;

EID: 84900321950     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087331     Document Type: Article

References (35)

1. Fettiplace R, Hackney CM (2006) The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7: 19-29. (Pubitemid 41828928)
2. Beurg M, Fettiplace R, Nam JH, Ricci AJ (2009) Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging. Nat Neurosci 12: 553-558.
3. Tinley LG, Tinley MS, DeRosier D (1992) Actin filaments, stereocilia, and hair cells: how cells count and measure. Ann Rev Cell Biol 8: 257-274.
4. Bartles JR (2000) Parallel actin bundles and their multiple actin-bundling proteins. Curr Opin Cell Biol 12: 72-78.
5. Petit C, Richardson GP (2009) Linking genes underlying deafness to hair-bundle development and function. Nature Neurosci Rev 12: 703-710.
6. Manor U, Kachar B (2008) Dynamic length regulation of sensory stereocilia. Semin Cell Dev Biol 19: 502-510.
7. Zheng L, Sekerkova G, Vranich K, Tinley LG, Mugnaini E, et al. (2000) The deaf jerker mouse has a mutation in the gene encoding the espin actin-bundling protein of hair cell stereocilia and lacks espin. Cell 102: 377-385.
8. Sekerková G, Richter CP, Bartles JR (2011) Roles of the espin actin-bundling proteins in the morphogenesis and stabilization of hair cell stereocilia revealed in CBA/CaJ congenic jerker mice. PLoS Genet 7:e1002032.
9. Peng AW, Belyantseva IA, Hsu PD, Friedman TB, Heller S (2009) Twinfilin 2 regulates actin filament lengths in cochlear stereocilia. J Neurosci 29: 15083-15088.
10. Mburu P, Romero MR, Hilton H, Parker A, Townsend S, et al. (2010) Gelsolin plays a role in the actin polymerization complex of hair cell stereocilia. PLoS One 5:e11627.
11. Manor U, Disanza A, Grati M, Andrade L, Lin H, et al. (2011) Regulation of stereocilia length by myosin XVa and Whirlin depends on the actin-regulatiry protein Eps8. Current Biol 21: 167-172.
12. Zampini V, Rüttiger L, Johnson SL, Franz C, Furness DN, et al. (2011) Eps8 regulates hair bundle length and functional maturation of mammalian auditory hair cells. PLoS Biol 9:e1001048.
13. Furness ND, Johnson SL, Manor U, Rüttiger L, Tochhetti A, et al. (2013) Progressive hearing loss and gradual deterioration of sensory hair bundles in the ears of mice lacking the actin-binding protein Eps8L2. Proc Natl Acad Sci USA 110:13898-13903.
14. Mburu P, Mustapha M, Varela A, Weil D, El-Amraoui A, et al. (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. (Pubitemid 36935335)
15. Belyantseva IA, Boger ET, Naz S, Frolenkov GI, Sellers JR, et al. (2005) Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 7: 148-156. (Pubitemid 40268129)
16. Salles FT, Merritt RC Jr, Manor U, Dougherty GW, Sousa AD, et al. (2009) Myosin IIIa boosts elongation of stereocilia by transporting espin 1 to the plus ends of actin filaments. Nat Cell Biol 11: 443-450.
17. Johnson SL, Beurg M, Marcotti W, Fettiplace R (2011) Prestin-driven cochlear amplification is not limited by the outer hair cell membrane time constant. Neuron 70: 1143-1154.
18. Johnson SL, Kennedy H, Fettiplace R, Marcotti W (2012) The resting transducer current drives spontaneous activity in pre-hearing mammalian cochlear inner hair cells. J Neurosci 32: 10479-10483.
19. Crawford AC, Evans MG, Fettiplace R (1989) Activation and adaptation of transducer currents in turtle hair cells. J Physiol 419: 405-434. (Pubitemid 20012026)
20. Kennedy HJ, Evans MG, Crawford AC, Fettiplace R (2003) Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells. Nat Neurosci 6: 832-836. (Pubitemid 36929704)
21. Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP (2001) FM1-43 dye behaves as a permeant blocker of the hair-cell's mechanotransducer channel. J Neurosci 21: 7013-7025. (Pubitemid 32846949)
22. Kros CJ, Marcotti W, van Netten SM, Self TJ, Libby RT, et al. (2002) Reduced climbing and increased slipping adaptation in cochlear hair cells of mice with Myo7a mutations. Nat Neurosci 5: 41-47. (Pubitemid 34038781)
23. Heidrych P, Zimmermann U, Kuhn S, Franz C, Engel J, et al. (2009) Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum Mol Genet 18: 2779-2790.
24. Marcotti W, Kros CJ (1999) Developmental expression of the potassium current IK,n contributes to maturation of mouse outer hair cells. J Physiol 520: 653-660. (Pubitemid 29533025)
25. Mburu P, Kikkawa Y, Townsend S, Romero R, Yonekawa H, et al. (2006) Whirlin complexes with p55 at the stereocilia tip during hair cell development. Proc Natl Acad Sci USA 103: 10973-10978. (Pubitemid 44148403)
26. 2+ sensitivity of the mechanotransducer require myosin-XVa in inner but not outer cochlear hair cells. J Neurosci 29: 4023-4034.
27. Peng AW, Belyantseva IA, Hsu PD, Friedman TB, Heller S (2009) Twinfilin 2 regulates actin filament lengths in cochlear stereocilia. J Neurosci 29: 15083-15088.
28. Tinley LG, Tinley MS, DeRosier D (1992) Actin filaments, stereocilia, and hair cells: how cells count and measure. Ann Rev Cell Biol 8: 257-274.
29. Rzadzinska AK, Schneider ME, Davies C, Riordan GP, Kachar B (2004) An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J Cell Biol 164: 887-897. (Pubitemid 38366900)
30. Zhang DS, Piazza V, Perrin BJ, Rzadzinska AK, Poczatek JC, et al. (2012) Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 481:520-524.
31. Schwander M, Kachar B, Müller U (2010) The cell biology of hearing. J Cell Biol 190: 9-20.
32. Offenhäuser N, Borgonovo A, Disanza A, Romano P, Ponzanelli I, et al. (2004) The Eps8 family of proteins links growth factor stimulation to actin reorganization generating functional redundancy in the Ras/Rac pathway. Mol Biol Cell 15:91-98. (Pubitemid 38044946)
33. Goodyear RJ, Marcotti W, Kros CJ, Richardson GP (2005) Development and properties of stereociliary link types in hair cells of the mouse cochlea. J Comp Neurol 485: 75-85. (Pubitemid 40488087)
34. Géléoc GS, Lennan GW, Richardson GP, Kros CJ (1997) A quantitative comparison of mechanoelectrical transduction in vestibular and auditory hair cells of neonatal mice. Proc Biol Sci 264: 611-621. (Pubitemid 27196846)
35. Kikkawa Y, Mburu P, Morse S, Kominami R, Townsend S, et al. (2005) Mutant analysis reveals whirlin as a dynamic organizer in the growing hair cell stereocilium. Hum Mol Genet 14: 391-400. (Pubitemid 40220656)