Unconventional myosins in inner-ear sensory epithelia

Journal of Cell Biology

Volumn 137, Issue 6, 1997, Pages 1287-1307

  Hasson, Tama ^a   Gillespie, Peter G ^b   Garcia, Jesus A ^c   MacDonald, Richard B ^c,d   Zhao, Yi Dong ^b   Yee, Ann G ^c   Mooseker, Mark S ^a   Corey, David P ^c,d,e  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; ISOENZYME; MYOSIN;

ACTIN FILAMENT; ADAPTATION; ANIMAL TISSUE; ARTICLE; BULLFROG; CELLULAR DISTRIBUTION; ENZYME LOCALIZATION; INNER EAR; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; STEREOCILIUM;

ANIMALS; DYNEIN ATPASE; EAR; EAR, INNER; EPITHELIUM; HUMANS; ISOENZYMES; MICE; MYOSIN HEAVY CHAINS; MYOSINS; RABBITS; RANA CATESBEIANA;

EID: 0030973305     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.6.1287     Document Type: Article

References (87)

1. Assad, J.A., and D.P. Corey. 1992. An active motor model for adaptation by vertebrate hair cells. J. Neurosci. 12:3291-3309.
2. Avraham, K.B., T. Hasson, K.P. Steel, D.M. Kingsley, L.B. Russell, M.S. Mooseker, N.G. Copeland, and N.A. Jenkins. 1995. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat. Genet. 11:369-375.
3. Bagshaw, C.R. 1993. Muscle Contraction. Second edition. Chapman and Hall. London. 155 pp.
4. Baines, I.C., H. Brzeska, and E.D. Korn. 1992. Differential localization of Acanthamoeba myosin 1 isoforms. J. Cell Biol. 5:1193-1203.
5. Baines, I.C., A. Corigliano-Murphy, and E.D. Korn. 1995. Quantification and localization of phosphorylated myosin I isoforms in Acanthamoeba castellanii. J. Cell Biol. 130:591-603.
6. Bearer, E.L., J.A. DeGiorgis, R.A. Bodner, A.W. Kao, and T.S. Reese. 1993. Evidence for myosin motors on organelles in squid axoplasm. Proc. Natl. Acad. Sci. USA. 90:11252-11256.
7. Bernent, W.M., and M.S. Mooseker. 1995. TEDS rule: a molecular rationale for differential regulation of myosins by phosphorylation of the heavy chain head. Cell Motil. Cytoskeleton. 31:87-92.
8. Bernent, W.M., T. Hasson, J.A. Wirth, R.E. Cheney, and M.S. Mooseker. 1994. Identification and overlapping expression of multiple unconventional myosin genes in vertebrate cell types. Proc. Natl. Acad. Sci. USA. 91:6549-6553.
9. Burlacu, A., W.D. Tap, E.A. Lumpkin, and A.J. Hudspeth. 1996. ATPase activity of myosin in hair bundles of the bullfrog's sacculus. Biophys. J. 72:262-271.
10. Chen, Z.-Y., T. Hasson, P.M. Kelley, B.J. Schwender, M.F. Schwartz, M. Ramakrishnan, W.J. Kimberling, M.S. Mooseker, and D.P. Corey. 1996. Molecular cloning and domain structure of myosin VIIa, the gene product defective in Usher Syndrome 1B. Genomics. 36:440-448.
11. Corey, D.P., and J.A. Assad. 1992. Transduction and adaptation in vertebrate hair cells: correlating structure with function. In Sensory Transduction. D.P. Corey and S. Roper, editors. Rockefeller University Press, New York. 336-342.
12. Corwin, J.T. 1985. Perpetual production of hair cells and maturational changes in hair cell ultrastructure accompany postembryonic growth in an amphibian ear. Proc. Natl. Acad. Sci. USA. 82:3911-3915.
13. Cotanche, D.A., and J.T. Corwin. 1991. Stereociliary bundles reorient during hair cell development and regeneration in the chick cochlea. Hearing Res. 52:379-402.
14. Denk, W., J.R. Holt, G.M.G. Shepherd, and D.P. Corey. 1995. Calcium imaging of single stereocilia in hair cells: localization of transduction channels at both ends of tip links. Neuron. 15:1311-1321.
15. Deol, M.S., and M.C. Green. 1966. Snell's waltzer, a new mutation affecting behavior and the inner ear in the mouse. Genet. Res. 8:339-345.
16. DeRosier, D.J., and L.G. Tilney. 1989. The structure of the cuticular plate, an in vivo actin gel. J. Cell Biol. 109:2853-2867.
17. Drenckhahn, D., J. Kellner, H.G. Mannherz, U. Gröschel-Stewart, J. Kendrick-Jones, and J. Scholey. 1982. Absence of myosin-like immunoreactivity in stereocilia of cochlear hair cells. Nature (Lond.). 300:531-532.
18. Drenckhahn, D., K. Engel, D. Höfer, C. Merte, L. Tilney, and M. Tilney. 1991. Three different actin filament assemblies occur in every hair cell: each contains a specific actin crosslinking protein. J. Cell Biol. 112:641-651.
19. Espreafico, E.M., R.E. Cheney, M. Matteoli, A.A.C. Nascimento, P.V. De Camilli, R.E. Larson, and M.S. Mooseker. 1992. Primary structure and cellular localization of chicken brain myosin-V (p190). an unconventional myosin with calmodulin light chains. J. Cell Biol. 119:1541-1547.
20. Evans, L.L., and P.C. Bridgman. 1995. Particles move along actin filament bundles in nerve growth cones. Proc. Natl. Acad. Sci. USA. 92:1054-10958.
21. Fath, K.R., and D.R. Burgess. 1993. Golgi-derived vesicles from developing epithelial cells bind actin filaments and possess myosin-I as a cytoplasmically oriented peripheral membrane protein. J. Cell Biol. 120:117-127.
22. Flock, A., H.C. Cheung, B. Flock, and G. Utter. 1981. Three sets of actin filaments in sensory cells of the inner car. Identification and functional orientation determined by gel electrophoresis, immunofluorescence, and electron microscopy. J. Neurocytol. 10:133-147.
23. Frankel, S., R. Sohn, and L. Leinwand. 1991. The use of sarkosyl in generating soluble protein after bacterial expression. Proc. Natl. Acad. Sci. USA. 88: 1192-1196.
24. Furness, D.N. and C.M. Hackney. 1985. Cross-links between stereocilia in the guinea pig cochlea. Hearing Res. 18:177-188.
25. Furness, D.N., C.M. Hackney, and P.S. Steyger. 1990. Organization of microtubules in cochlear hair cells. J. Electron Microsc. Tech. 15:261-279.
26. Gibson, F., J. Walsh, P. Mburu, A. Varela, K.A. Brown, M. Antonio, K.W. Beisel, K.P. Steel, and S.D.M. Brown. 1995. A type VII myosin encoded by the mouse deafness gene shaker-1. Nature (Lond.). 374:62-64.
27. Gillespie, P.G., and A.J. Hudspeth. 1991. High-purity isolation of bullfrog hair bundles and subcellular and topological localization of constituent proteins. J. Cell Biol. 112:625-640.
28. Gillespie, P.G., and S.K.H. Gillespie. 1997. Improved electrophoresis and transfer of picogram amounts of protein with hemoglobin. Anal. Biochem. 246: 239-245.
29. Gillespie, P.G., M.C. Wagner, and A.J. Hudspeth. 1993. Identification of a 120-kD hair-bundle myosin I located near stereociliary tips. Neuron. 11:581-594.
30. Gillespie, P.G., T. Hasson, J.A. Garcia, and D.P. Corey. 1996. Multiple myosin isozymes and hair-cell function. Cold Spring Harbor Symp. Quant. Biol. LXI:309-318.
31. Govindan, B., R. Bowser, and P. Novick. 1995. The role of Myo2, a yeast class V myosin, in vesicular transport. J. Cell Biol. 128:1055-1068.
32. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory. Cold Spring Harbor. NY. 726 pp.
33. Hasson, T., and M.S. Mooseker. 1994. Porcine myosin-VI: characterization of a new mammalian unconventional myosin. J. Cell Biol. 127:425-400.
34. Hasson, T., M.B. Heintzelman, J. Santos-Sacchi, D.P. Corey, and M.S. Mooseker. 1995. 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.
35. Hasson, T., J.F. Skowron, D.J. Gilbert, K.B. Avraham, W.L. Perry, W.M. Bement, B.L. Anderson, E.H. Sherr, Z.-Y. Chen, L.A. Greene et al. 1996. Mapping of unconventional myosins in mouse and human. Genomics. 36:431-439.
36. Hata, Y., S. Butz, and T.C Sudhof. 1996. CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci. 16:2488-2494.
37. Heintzelman, M.B., T. Hasson, and M.S. Mooseker. 1994. Multiple unconventional myosin domains in the intestinal brush border cytoskeleton. J. Cell Sci. 107:3535-3543.
38. Heywood, P., T.R. van der Water, D.A. Hilding, and R.J. Ruben. 1975. Distribution of microtubules and microfilaments in developing vestibular sensory epithelium of mouse otocysts grown in vitro. J. Cell Sci. 17:171-189.
39. Hirokawa, N., and L.G. Tilney. 1982. Interactions between actin filaments and between actin filaments and membranes in quick-frozen and deeply etched hair cells of the chick ear. J. Cell Biol. 95:249-261.
40. Hudspeth, A.J. 1989. How the car's works work. Nature (Lond.). 341:397-404.
41. Hudspeth, A.J., and P.G. Gillespie. 1994. Pulling springs to tune transduction: adaptation by hair cells. Neuron. 12:1-9.
42. Jacobs, R.A., and A.J. Hudspeth. 1990. Ultrastructural correlates of mechanoelectrical transduction in hair cells of the bullfrog's internal ear. Cold Spring Harbor Symp. Quant. Biol. 55:547-561.
43. Jaeger, R.G., J. Fex, and B. Kachar. 1994. Structural basis for mechanical transduction in the frog vestibular sensory apparatus: II. The role of microtubules in the organization of the cuticular plate. Hearing Res. 77:207-215.
44. Johnston, G.C., J.A. Prendergast, and R.A. Singer. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113:539-551.
45. + channels by interaction with a family of membrane-associated guanylate kinases. Nature (Lond.). 378:85-88.
46. Kornau, H.C., L.T. Schenker, M.B. Kennedy, and P.H. Seeburg. 1995. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science (Wash. DC). 269:1737-1740.
47. Kozminski, K.G., K.A. Johnson, P. Forscher, and J.L. Rosenbaum. 1993. A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA. 90:5519-5523.
48. Langford, G.M., S.A. Kuznetsov, D. Johnson, D.L. Cohen, and D.G. Weiss. 1994. Movement of axoplasmic organelles on actin filaments assembled on acrosomal processes: evidence for a barbed-end-directed organelle motor. J. Cell Sci. 107:2291-2298.
49. Lue, R.A., E. Brandin, E.P. Chan, and D. Branton. 1996. Two independent domains of hDlg are sufficient for subcellular targeting: The PDZ1-2 confermational unit and an alternatively spliced domain. J. Cell Biol. 135:125-1137.
50. Ma, Y.-Z., and E.W. Taylor. 1994. Kinetic mechanism of myofibril ATPase. Biophys. J. 66:1542-1553.
51. Macartney, J.C., S.D. Comis, and J.O. Pickles. 1980. Is myosin in the cochlea a basis for active motility? Nature (Lond.). 288:491-192.
52. Matsudaira, P. 1994. The fimbrin and alpha-actinin footprint on actin. J. Cell Biol. 126:285-287.
53. Mercer, J.A., P.K. Seperack, M.C. Strobel, N.G. Copeland, and N.A. Jenkins. 1991. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature (Lond.). 349:709-713.
54. Metcalf, A.B., Y. Chelliah, and A.J. Hudspeth. 1994. Molecular cloning of a myosin Iβ isozyme that may mediate adaptation by hair cells of the bullfrog's internal ear. Proc. Natl. Acad. Sci. USA. 91:11821-11825.
55. Mooseker, M.S., and R.E. Cheney. 1995. Unconventional myosins. Annu. Rev. Cell Dev. Biol. 11:633-675.
56. Morris, R.L., and P.J. Hollenbeck. 1995. Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J. Cell Biol. 131: 1315-1326.
57. Niethammer, M., E. Kim, and M. Sheng. 1996. Interaction between the C terminus of the NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J. Neurosci. 16:2157-2163.
58. Ostap, E.M., and T.D. Pollard. 1996. Biochemical kinetic characterization of Acanthamoeba myosin-I ATPase. J. Cell Biol. 132:1053-1060.
59. Pickles, J.O., and D.P. Corey. 1992. Mechanoelectrical transduction by hair cells. Trends Nettnisci. 15:254-259.
60. Presson, J.C. 1994. Immunocytochemical reactivities of precursor cells and their progeny in the ear of a cichlid fish. Hearing Res. 80:1-9.
61. Rayment, I., H.M. Holden, M. Whittaker, B.C. Yohn, M. Lorenz, K.C. Holmes, and R.A. Milligan. 1993a. Structure of the actin-myosin complex and its implications for muscle contraction. Science (Wash. DC). 261:58-65.
62. Rayment, I., R.W. Rypniewski, K. Schmidt-Base, R. Smith, D.R. Tomchick, M.M. Benning, D.A. Winkelmann, G. Wessenberg, and H.M. Hoiden. 1993b. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science (Wash. DC). 261:50-58.
63. Ross, M.D., T.E. Komorowski, C.M. Rogers, K.G. Pote, and K.M. Donovan. 1987. Macular suprastructure, stereociliary bonding, and kinociliary/stereociliary coupling in rat utricular maculae. Acta Oto-laryngol. 104:56-65.
64. Sans, A., P. Alger, C. Cavadore, and J.C. Cavadore. 1989. Immunocytochemical localization of myosin, tropomyosin, and actin in vestibular hair cells of human fetuses and cats. Hearing Res. 40:117-125.
65. Sawada, H., and M. Esaki. 1994. Use of nanogold followed by silver enhancement and gold toning for preembedding immunolocalization in osmium-fixed, epon-embedded tissues. J. Electron Microsc. 43:361-366.
66. Scarfone, E., D. Dememes, D. Perrin, D. Aunis, and A. Sans. 1988. α-Fodrin (brain spectin) immunocytochemical localization in rat vestibular hair cells. Neurosci. Lett. 93:13-18.
67. Sheng, M. 1996. PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron. 17:575-578.
68. Shepherd, G.M.G., B.A. Barres, and D.P. Corey. 1989. "Bundle-blot" purification and initial protein characterization of hair cell stereocilia. Proc. Natl. Acad. Sci. USA. 86:4973-4977.
69. Shepherd, G.M.G., D.P. Corey, and S.M. Block. 1990. Actin cores of hair-cell stereocilia support myosin motility. Proc. Natl. Acad. Sci. USA. 87:8627-8631.
70. 2+ channel by INAD in Drosophila photoreceptors. Neuron. 16:991-998.
71. Siegel, J.H., and W.E. Brownell. 1986. Synaptic and Golgi membrane recycling in cochlear hair cells. J. Neurocytol. 15:311-328.
72. Silvers, W.K., editor. 1979. Dilute and Leaden, the p-locus. Ruby-Eye, and Ruby-Eye-2. In Coat Colors of Mice: A Model for Mammalian Gene Action and Interaction. Springer Verlag, New York. 83-89.
73. Slepecky, N.B., and S.C. Chamberlain. 1985. Immunoelectron microscopic and immunofluorescent localization of cytoskeletal and muscle-like contractile proteins in inner ear sensory hair cells. Hearing Res. 20:245-260.
74. Slepecky, N.B., and M. Ulfendahl. 1992. Actin-binding and microtubule-associated proteins in the organ of Corti. Hearing Res. 57:201-215.
75. Sobin, A., and A. Flock. 1983. Immunohistochemical identification and localization of actin and fimbrin in vestibular hair cells in the normal guinea pig and in a strain of the waltzing guinea pig. Acta Oto-laryngol. 96:407-412.
76. Solc, C.K., B.H. Derfler, G.M. Duyk, and D.P. Corey. 1994. Molecular cloning of myosins from bullfrog saccular macula: a candidate for the hair cell adaptation motor. Auditory Neurosci. 1:63-75.
77. Steel, K.P., and S.D.M. Brown. 1996. Genetics of deafness. Curr. Opin. Neurobiol. 6:520-525.
78. Steyger, P.S., D.N. Furness, C.M. Hackney, and G.P. Richardson. 1989. Tubulin and microtubules in cochlear hair cells: comparative immunocytochemistry and ultrastructure. Hearing Res. 42:1-16.
79. Tilney, L.G., D.J. DeRosier, and M.J. Mulroy. 1980. The organization of actin filaments in the stereocilia of cochlear hair cells. J. Cell Biol. 86:244-259.
80. Tilney, L.G., M.S. Tilney, and D.J. DeRosier. 1992. Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu. Rev. Cell Biol. 8:257-274.
81. Troutt, L.L., W.R.A. van Heumen, and J.O. Pickles. 1994. The changing microtubule arrangements in developing hair cells of the chick cochlea. Hearing Res. 81:100-108.
82. Wagner, M.C., B. Barylko, and J.P. Albanesi. 1992. Tissue distribution and subcellular localization of mammalian myosin I. J. Cell Biol. 119:163-170.
83. Walker, R.G., and A.J. Hudspeth. 1996. Calmodulin controls adaptation of mechanoelectrical transduction by hair cells of the bullfrog's sacculus. Proc. Natl. Acad. Sci. USA. 93:2203-2207.
84. Weil, D., S. Blanchard, J. Kaplan, P. Guilford, F. Gibson, J. Walsh, P. Mburu, A. Varela, J. Levilliers, M.D. Weston, P.M. Kelley et al. 1995. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature (Lond.). 374:60-61.
85. Weil, D., G. Levy, I. Sahly, F. Levi-Acobas, S. Blanchard, A. El-Amraoui, F. Crozet, H. Philippe, M. Abitbol, and C. Petit. 1996. Human myosin VIIA responsible for the Usher 1B syndrome: a predicted membrane-associated motor protein expressed in developing sensory epithelia. Proc. Natl. Acad. Sci. USA. 92:3232-3237.
86. Yamoah, E.N., and P.G. Gillespie. 1996. Phosphate analogs block adaptation in hair cells by inhibiting adaptation-motor force production. Neuron. 17:523-533.
87. Zhao, L.-P., J.S. Koslovsky, J. Reinhard, M. Bähler, A.E. Witt, D.W. Provance, and J.A. Mercer. 1996. Cloning and characterization of myr 6, an unconventional myosin of the dilute-myosin-V family. Proc. Natl. Acad. Sci. USA. 93: 10826-10831.