Underestimated Sensitivity of Mammalian Cochlear Hair Cells Due to Splay between Stereociliary Columns

Biophysical Journal

Volumn 108, Issue 11, 2015, Pages 2633-2647

  Nam, Jong Hoon ^a   Peng, Anthony W ^b   Ricci, Anthony J ^b  

^a University of Rochester   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

ANIMAL; ARTIFACT; BIOLOGICAL MODEL; BIOMECHANICS; CYTOLOGY; ELECTROPHYSIOLOGY; FINITE ELEMENT ANALYSIS; INNER HAIR CELL; MECHANOTRANSDUCTION; METABOLISM; MICROSCOPY; OUTER HAIR CELL; RAT; STEREOCILIUM;

ANIMALS; ARTIFACTS; BIOMECHANICAL PHENOMENA; ELECTROPHYSIOLOGICAL PHENOMENA; FINITE ELEMENT ANALYSIS; HAIR CELLS, AUDITORY, INNER; HAIR CELLS, AUDITORY, OUTER; MECHANOTRANSDUCTION, CELLULAR; MICROSCOPY; MODELS, BIOLOGICAL; RATS; STEREOCILIA;

EID: 84930617187     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2015.04.028     Document Type: Article

References (65)

1. R. Fettiplace, and K.X. Kim The physiology of mechanoelectrical transduction channels in hearing Physiol. Rev. 94 2014 951 986
2. A.J. Hudspeth Integrating the active process of hair cells with cochlear function Nat. Rev. Neurosci. 15 2014 600 614
3. R.J. Goodyear, and W. Marcotti G.P. Richardson Development and properties of stereociliary link types in hair cells of the mouse cochlea J. Comp. Neurol. 485 2005 75 85
4. C.M. Hackney, and D.N. Furness The composition and role of cross links in mechanoelectrical transduction in vertebrate sensory hair cells J. Cell Sci. 126 2013 1721 1731
5. M. Beurg, and R. Fettiplace A.J. Ricci Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging Nat. Neurosci. 12 2009 553 558
6. E. Verpy, and M. Leibovici C. Petit Stereocilin connects outer hair cell stereocilia to one another and to the tectorial membrane J. Comp. Neurol. 519 2011 194 210
7. D.J. Lim Cochlear anatomy related to cochlear micromechanics. A review J. Acoust. Soc. Am. 67 1980 1686 1695
8. M. Billone, and S. Raynor Transmission of radial shear forces to cochlear hair cells J. Acoust. Soc. Am. 54 1973 1143 1156
9. D.M. Freeman, and T.F. Weiss The role of fluid inertia in mechanical stimulation of hair cells Hear. Res. 35 1988 201 207
10. R. Ghaffari, A.J. Aranyosi, and D.M. Freeman Longitudinally propagating traveling waves of the mammalian tectorial membrane Proc. Natl. Acad. Sci. USA 104 2007 16510 16515
11. J. Howard, and A.J. Hudspeth Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell Neuron 1 1988 189 199
12. J. Ashmore, and P. Avan B. Canlon The remarkable cochlear amplifier Hear. Res. 266 2010 1 17
13. A.J. Ricci, A.C. Crawford, and R. Fettiplace Active hair bundle motion linked to fast transducer adaptation in auditory hair cells J. Neurosci. 20 2000 7131 7142
14. H.J. Kennedy, A.C. Crawford, and R. Fettiplace Force generation by mammalian hair bundles supports a role in cochlear amplification Nature 433 2005 880 883
15. L. Robles, and M.A. Ruggero Mechanics of the mammalian cochlea Physiol. Rev. 81 2001 1305 1352
16. E.A. Stauffer, and J.R. Holt Sensory transduction and adaptation in inner and outer hair cells of the mouse auditory system J. Neurophysiol. 98 2007 3360 3369
17. A. Lelli, and Y. Asai G.S. Géléoc Tonotopic gradient in the developmental acquisition of sensory transduction in outer hair cells of the mouse cochlea J. Neurophysiol. 101 2009 2961 2973
18. A.W. Peng, T. Effertz, and A.J. Ricci Adaptation of mammalian auditory hair cell mechanotransduction is independent of calcium entry Neuron 80 2013 960 972
19. S.L. Johnson, and M. Beurg R. Fettiplace Prestin-driven cochlear amplification is not limited by the outer hair cell time constant Neuron 70 2011 1143 1154
20. A.C. Crawford, and R. Fettiplace The mechanical properties of ciliary bundles of turtle cochlear hair cells J. Physiol. 364 1985 359 379
21. A.J. Ricci, and R. Fettiplace The effects of calcium buffering and cyclic AMP on mechano-electrical transduction in turtle auditory hair cells J. Physiol. 501 1997 111 124
22. A.J. Ricci, and R. Fettiplace Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph J. Physiol. 506 1998 159 173
23. A.J. Ricci, A.C. Crawford, and R. Fettiplace Tonotopic variation in the conductance of the hair cell mechanotransducer channel Neuron 40 2003 983 990
24. J.R. Cotton, and J.W. Grant A finite element method for mechanical response of hair cell ciliary bundles J. Biomech. Eng. 122 2000 44 50
25. J.H. Nam, J.R. Cotton, and W. Grant A virtual hair cell, I: addition of gating spring theory into a 3-D bundle mechanical model Biophys. J. 92 2007 1918 1928
26. J.H. Nam, J.R. Cotton, and W. Grant A virtual hair cell, II: evaluation of mechanoelectric transduction parameters Biophys. J. 92 2007 1929 1937
27. J.H. Nam, and R. Fettiplace Theoretical conditions for high-frequency hair bundle oscillations in auditory hair cells Biophys. J. 95 2008 4948 4962
28. M. Beurg, and J.H. Nam R. Fettiplace The actions of calcium on hair bundle mechanics in mammalian cochlear hair cells Biophys. J. 94 2008 2639 2653
29. B. Roth, and V. Bruns Postnatal development of the rat organ of Corti. II. Hair cell receptors and their supporting elements Anat. Embryol. (Berl.) 185 1992 571 581
30. P.A. Santi, and C.B. Anderson A newly identified surface coat on cochlear hair cells Hear. Res. 27 1987 47 65
31. S.G. Dolgobrodov, A.N. Lukashkin, and I.J. Russell Electrostatic interaction between stereocilia: II. Influence on the mechanical properties of the hair bundle Hear. Res. 150 2000 94 103
32. M. Sun, and J.S. Graham M. Grandbois Multiple membrane tethers probed by atomic force microscopy Biophys. J. 89 2005 4320 4329
33. A.A. Indzhykulian, and R. Stepanyan G.I. Frolenkov Molecular remodeling of tip links underlies mechanosensory regeneration in auditory hair cells PLoS Biol. 11 2013 e1001583
34. C. Söllner, and G.J. Rauch T. Nicolson Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells Nature 428 2004 955 959
35. L.F. Corns, and S.L. Johnson W. Marcotti Calcium entry into stereocilia drives adaptation of the mechanoelectrical transducer current of mammalian cochlear hair cells Proc. Natl. Acad. Sci. USA 111 2014 14918 14923
36. G.M. Shepherd, and D.P. Corey The extent of adaptation in bullfrog saccular hair cells J. Neurosci. 14 1994 6217 6229
37. J. Cotton, and W. Grant Computational models of hair cell bundle mechanics: II. Simplified bundle models Hear. Res. 197 2004 105 111
38. J. Silber, and J. Cotton W. Grant Computational models of hair cell bundle mechanics: III. 3-D utricular bundles Hear. Res. 197 2004 112 130
39. J.H. Nam, and J.R. Cotton W. Grant Mechanical properties and consequences of stereocilia and extracellular links in vestibular hair bundles Biophys. J. 90 2006 2786 2795
40. A.S. Kozlov, T. Risler, and A.J. Hudspeth Coherent motion of stereocilia assures the concerted gating of hair-cell transduction channels Nat. Neurosci. 10 2007 87 92
41. K.D. Karavitaki, and D.P. Corey Sliding adhesion confers coherent motion to hair cell stereocilia and parallel gating to transduction channels J. Neurosci. 30 2010 9051 9063
42. M.G. Langer, and S. Fink J.P. Ruppersberg Lateral mechanical coupling of stereocilia in cochlear hair bundles Biophys. J. 80 2001 2608 2621
43. K.D. Karavitaki, P.D. Niksch, and D.P. Corey Weak lateral coupling between stereocilia of mammalian hair cells requires new stimulus methods to study the biomechanics of hearing J. Acoust. Soc. Am. 133 2013 3509
44. A.S. Kozlov, and J. Baumgart A.J. Hudspeth Forces between clustered stereocilia minimize friction in the ear on a subnanometer scale Nature 474 2011 376 379
45. D.N. Furness, and S. Mahendrasingam C.M. Hackney The dimensions and composition of stereociliary rootlets in mammalian cochlear hair cells: comparison between high- and low-frequency cells and evidence for a connection to the lateral membrane J. Neurosci. 28 2008 6342 6353
46. D.P. Corey, and A.J. Hudspeth Kinetics of the receptor current in bullfrog saccular hair cells J. Neurosci. 3 1983 962 976
47. A. Lelli, and P. Kazmierczak J.R. Holt Development and regeneration of sensory transduction in auditory hair cells requires functional interaction between cadherin-23 and protocadherin-15 J. Neurosci. 30 2010 11259 11269
48. H.J. Kennedy, and M.G. Evans R. Fettiplace Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells Nat. Neurosci. 6 2003 832 836
49. R.A. Eatock, D.P. Corey, and A.J. Hudspeth Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus J. Neurosci. 7 1987 2821 2836
50. J.A. Assad, N. Hacohen, and D.P. Corey Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells Proc. Natl. Acad. Sci. USA 86 1989 2918 2922
51. J.A. Assad, and D.P. Corey An active motor model for adaptation by vertebrate hair cells J. Neurosci. 12 1992 3291 3309
52. E.A. Stauffer, and J.D. Scarborough P.G. Gillespie Fast adaptation in vestibular hair cells requires myosin-1c activity Neuron 47 2005 541 553
53. B. Nadrowski, P. Martin, and F. Jülicher Active hair-bundle motility harnesses noise to operate near an optimum of mechanosensitivity Proc. Natl. Acad. Sci. USA 101 2004 12195 12200
54. J.Y. Tinevez, F. Jülicher, and P. Martin Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell Biophys. J. 93 2007 4053 4067
55. S.S. Gao, and R. Wang J.S. Oghalai Vibration of the organ of Corti within the cochlear apex in mice J. Neurophysiol. 112 2014 1192 1204
56. W.S. Rhode, and C.D. Geisler Model of the displacement between opposing points on the tectorial membrane and reticular lamina J. Acoust. Soc. Am. 42 1967 185 190
57. P. Dallos Organ of Corti kinematics J. Assoc. Res. Otolaryngol. 4 2003 416 421
58. J.H. Nam, and R. Fettiplace Force transmission in the organ of Corti micromachine Biophys. J. 98 2010 2813 2821
59. F. Chen, and D. Zha A.L. Nuttall A differentially amplified motion in the ear for near-threshold sound detection Nat. Neurosci. 14 2011 770 774
60. D.Z. He, S. Jia, and P. Dallos Mechanoelectrical transduction of adult outer hair cells studied in a gerbil hemicochlea Nature 429 2004 766 770
61. S. Jia, P. Dallos, and D.Z. He Mechanoelectric transduction of adult inner hair cells J. Neurosci. 27 2007 1006 1014
62. A.J. Hudspeth, and Y. Choe P. Martin Putting ion channels to work: mechanoelectrical transduction, adaptation, and amplification by hair cells Proc. Natl. Acad. Sci. USA 97 2000 11765 11772
63. B. Pan, and J. Waguespack A.J. Ricci Permeation properties of the hair cell mechanotransducer channel provide insight into its molecular structure J. Neurophysiol. 107 2012 2408 2420
64. J. Xue, and E.H. Peterson Hair bundle heights in the utricle: differences between macular locations and hair cell types J. Neurophysiol. 95 2006 171 186
65. C. Spoon, and W.J. Moravec E.H. Peterson Steady-state stiffness of utricular hair cells depends on macular location and hair bundle structure J. Neurophysiol. 106 2011 2950 2963