Tonotopic gradient in the developmental acquisition of sensory transduction in outer hair cells of the mouse cochlea

Journal of Neurophysiology

Volumn 101, Issue 6, 2009, Pages 2961-2973

  Lelli, Andrea ^a   Asai, Yukako ^a   Forge, Andrew ^b   Holt, Jeffrey R ^a   Géléoc, Gwenaëlle S G ^a,c  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CADHERIN; CADHERIN 23; FLUORESCENT DYE; FM 143; MESSENGER RNA; MYOSIN; MYOSIN 15A; MYOSIN 3A; MYOSIN VIIA; PMCA2 ENZYME; PROTOCADHERIN 15; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; COCHLEA; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GENE EXPRESSION; HAIR CELL; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TONOTOPY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; COCHLEA; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY, OUTER; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE POTENTIALS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MYOSINS; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RNA, MESSENGER;

EID: 66349126903     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00136.2009     Document Type: Article

References (45)

1. Ahmed ZM, Goodyear R, Riazuddin S, Lagziel A, Legan PK, Behra M, Burgess SM, Lilley KS, Wilcox ER, Riazuddin S, Griffith AJ, Frolenkov GI, Belyantseva IA, Richardson GP, Friedman TB. The tip-link antigen, a protein associated with the transduction complex of sensory hair cells, is protocadherin-15. J Neurosci 26: 7022-7034, 2006. (Pubitemid 44309870)
2. Alagramam KN, Miller ND, Adappa ND, Pitts DR, Heaphy JC, Yuan H, Smith RJ. Promoter, alternative splice forms, and genomic structure of protocadherin 15. Genomics 90: 482-492, 2007. (Pubitemid 47404799)
3. Assad JA, Corey DP. An active motor model for adaptation by vertebrate hair cells. J Neurosci 12: 3291-3309, 1992.
4. Belyantseva IA, Adler HJ, Curi R, Frolenkov GI, Kachar B. Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J Neurosci 20:RC116, 2000.
5. 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 100: 13958-13963, 2003. (Pubitemid 37499173)
6. Belyantseva IA, Boger ET, Naz S, Frolenkov GI, Sellers JR, Ahmed ZM, Griffith AJ, Friedman TB. Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 7: 148-156, 2005. (Pubitemid 40268129)
7. Beurg M, Evans MG, Hackney CM, Fettiplace R. A large-conductance calcium-selective mechanotransducer channel in mammalian cochlear hair cells. J Neurosci 26: 10992-11000, 2006. (Pubitemid 44772189)
8. Chen P, Johnson JE, Zoghbi HY, Segil N. The role of Math1 in inner ear development: Uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129: 2495-2505, 2002.
9. Corey DP, Hudspeth AJ. Ionic basis of the receptor potential in a vertebrate hair cell. Nature 281: 675-677, 1979. (Pubitemid 10249043)
10. Corey DP, Hudspeth AJ. Kinetics of the receptor current in bullfrog saccular hair cells. J Neurosci 3: 962-976, 1983. (Pubitemid 13135421)
11. Crawford AC, Evans MG, Fettiplace R. Activation and adaptation of transducer currents in turtle hair cells. J Physiol 419: 405-434, 1989. (Pubitemid 20012026)
12. Crawford AC, Evans MG, Fettiplace R. The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J Physiol 434: 369-398, 1991.
13. Davies S, Forge A. Preparation of the mammalian organ of Corti for scanning electron microscopy. J Microsc 147: 89-101, 1987.
14. 2+-ATPase isoform 2a is the PMCA of hair bundles. J Neurosci 21: 5066-5078, 2001.
15. Dumont RA, Zhao YD, Holt JR, Bahler M, Gillespie PG. Myosin-I isozymes in neonatal rodent auditory and vestibular epithelia. J Assoc Res Otolaryngol 3: 375-389, 2002. (Pubitemid 36077388)
16. Eatock RA, Corey DP, Hudspeth AJ. Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus. J Neurosci 7: 2821-2836, 1987.
17. Ficarella R, Di Leva F, Bortolozzi M, Ortolano S, Donaudy F, Petrillo M, Melchionda S, Lelli A, Domi T, Fedrizzi L, Lim D, Shull GE, Gasparini P, Brini M, Mammano F, Carafoli E. A functional study of plasma-membrane calcium-pump isoform 2 mutants causing digenic deafness. Proc Natl Acad Sci USA 104: 1516-1521, 2007. (Pubitemid 46214622)
18. Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21: 7013-7025, 2001. (Pubitemid 32846949)
19. Géléoc GS, Holt JR. Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat Neurosci 6: 1019-1020, 2003. (Pubitemid 37186191)
20. Gibson F, Walsh J, Mburu P, Varela A, Brown KA, Antonio M, Beisel KW, Steel KP, Brown SD. A type VII myosin encoded by the mouse deafness gene shaker-1. Nature 374: 62-64, 1995.
21. Goodyear RJ, Marcotti W, Kros CJ, Richardson GP. Development and properties of stereociliary link types in hair cells of the mouse cochlea. J Comp Neurol 485: 75-85, 2005. (Pubitemid 40488087)
22. Gross J, Machulik A, Amarjargal N, Fuchs J, Mazurek B. Expression of prestin mRNA in the organotypic culture of rat cochlea. Hear Res 204: 183-190, 2005. (Pubitemid 40733215)
23. Hackney CM, Mahendrasingam S, Penn A, Fettiplace R. The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J Neurosci 25: 7867-7875, 2005. (Pubitemid 41208659)
24. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci USA 92: 9815-9819, 1995.
25. Haywood-Watson RJ, 2nd, Ahmed ZM, Kjellstrom S, Bush RA, Takada Y, Hampton LL, Battey JF, Sieving PA, Friedman TB. Ames Waltzer deaf mice have reduced electroretinogram amplitudes and complex alternative splicing of Pcdh15 transcripts. Invest Ophthalmol Vis Sci 47: 3074-3084, 2006.
26. Holt JR, Gillespie SK, Provance DW, Shah K, Shokat KM, Corey DP, Mercer JA, Gillespie PG. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108: 371-381, 2002. (Pubitemid 34178401)
27. Kazmierczak P, Sakaguchi H, Tokita J, Wilson-Kubalek EM, Milligan RA, Muller U, Kachar B. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 449: 87-91, 2007. (Pubitemid 47373771)
28. Kennedy HJ, Evans MG, Crawford AC, Fettiplace R. Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells. Nat Neurosci 6: 832-836, 2003. (Pubitemid 36929704)
29. Lagziel A, Ahmed ZM, Schultz JM, Morell RJ, Belyantseva IA, Friedman TB. Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev Biol 280: 295-306, 2005. (Pubitemid 40692133)
30. 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. Characterization of the human and mouse unconventional myosin XV genes responsible for hereditary deafness DFNB3 and shaker 2. Genomics 61: 243-258, 1999.
31. Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, Corwin JT, Corey DP. Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23: 4054-4065, 2003. (Pubitemid 36958424)
32. Nayak GD, Ratnayaka HS, Goodyear RJ, Richardson GP. Development of the hair bundle and mechanotransduction. Int J Dev Biol 51: 597-608, 2007. (Pubitemid 350084414)
33. Ricci AJ, Fettiplace R. Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph. J Physiol 506: 159-173, 1998. (Pubitemid 28046044)
34. Roth B, Bruns V. Postnatal development of the rat organ of Corti. II. Hair cell receptors and their supporting elements. Anat Embryol (Berlin) 185: 571-581, 1992.
35. Schneider ME, Dose AC, Salles FT, Chang W, Erickson FL, Burnside B, Kachar B. A new compartment at stereocilia tips defined by spatial and temporal patterns of myosin IIIa expression. J Neurosci 26: 10243-10252, 2006. (Pubitemid 44527418)
36. Self T, Mahony M, Fleming J, Walsh J, Brown SD, Steel KP. Shaker-1 mutations reveal roles for myosin VIIA in both development and function of cochlear hair cells. Development 125: 557-566, 1998. (Pubitemid 28108081)
37. Si F, Brodie H, Gillespie PG, Vazquez AE, Yamoah EN. Developmental assembly of transduction apparatus in chick basilar papilla. J Neurosci 23: 10815-10826, 2003. (Pubitemid 37499688)
38. Stauffer EA, Holt JR. Sensory transduction and adaptation in inner and outer hair cells of the mouse auditory system. J Neurophysiol 98: 3360-3369, 2007.
39. Stauffer EA, Scarborough JD, Hirono M, Miller ED, Shah K, Mercer JA, Holt JR, Gillespie PG. Fast adaptation in vestibular hair cells requires myosin-1c activity. Neuron 47: 541-553, 2005. (Pubitemid 41139212)
40. Waguespack J, Salles FT, Kachar B, Ricci AJ. Stepwise morphological and functional maturation of mechanotransduction in rat outer hair cells. J Neurosci 27: 13890-13902, 2007. (Pubitemid 350278258)
41. Walsh T, Walsh V, Vreugde S, Hertzano R, Shahin H, Haika S, Lee MK, Kanaan M, King MC, Avraham KB. From flies' eyes to our ears: mutations in a human class III myosin cause progressive nonsyndromic hearing loss DFNB30. Proc Natl Acad Sci USA 99: 7518-7523, 2002. (Pubitemid 34568723)
42. Wang A, Liang Y, Fridell RA, Probst FJ, Wilcox ER, Touchman JW, Morton CC, Morell RJ, Noben-Trauth K, Camper SA, Friedman TB. Association of unconventional myosin MYO15 mutations with human nonsyndromic deafness DFNB3. Science 280: 1447-1451, 1998. (Pubitemid 28264840)
43. Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J, Mburu P, Varela A, Levilliers J, Weston MD, et al. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 374: 60-61, 1995.
44. Weil D, Küssel P, Blanchard S, Levy G, Levi-Acobas F, Drira M, Ayadi H, Petit C. The autosomal recessive isolated deafness, DFNB2, and the Usher 1B syndrome are allelic defects of the myosin-VIIA gene. Nat Genet 16: 191-193, 1997. (Pubitemid 27240620)
45. Wu YC, Ricci AJ, Fettiplace R. Two components of transducer adaptation in auditory hair cells. J Neurophysiol 82: 2171-2181, 1999.