Intracellular distributions and putative functions of calcium-binding proteins in the bullfrog vestibular otolith organs

Hearing Research

Volumn 103, Issue 1-2, 1997, Pages 85-100

  Baird, R A ^a   Steyger, P S ^a   Schuff, N R ^a  

^a LEGACY GOOD SAMARITAN HOSPITAL   (United States)

Author keywords

calbindin; calmodulin; calretinin; parvalbumin; S 100; sacculus; utriculus

Indexed keywords

CALBINDIN; CALMODULIN; CALRETININ; MONOCLONAL ANTIBODY; PARVALBUMIN; POLYCLONAL ANTIBODY; PROTEIN S 100;

ANIMAL CELL; ARTICLE; FROG; IMMUNOCYTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; SACCULUS; UTRICLE;

NASA DISCIPLINE NEUROSCIENCE; NASA DISCIPLINE NUMBER 40-10; NASA PROGRAM SPACE BIOLOGY; NON-NASA CENTER;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CALCIUM; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CALCIUM-BINDING PROTEINS; CALMODULIN; HAIR CELLS, VESTIBULAR; IMMUNOHISTOCHEMISTRY; OTOLITHIC MEMBRANE; PARVALBUMINS; RANA CATESBEIANA; S100 PROTEINS; SUBCELLULAR FRACTIONS;

EID: 0031037441     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-5955(96)00167-0     Document Type: Article

References (96)

1. Art, J.J., Crawford, A.C. and Fettiplace, R. (1986) Electrical resonance and membrane currents in turtle cochlear hair cells. Hear. Res. 22, 31-36.
2. Assad, J.A., Hacohen, N. and Corey, D.P. (1989) Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc. Natl. Acad. Sci. USA 86, 2918-2922.
3. Baimbridge, K.G., Miller, J.J. and Parkes, C.O. (1982) Calcium-binding protein distribution in the rat brain. Brain Res. 239, 519-525.
4. Baimbridge, K.G., Celio, M.R. and Rogers, J.H. (1992) Calcium-binding proteins in the nervous system. TINS 15, 303-308.
5. Baird, R.A. (1992) Morphological and electrophysiological properties of hair cells in the bullfrog utriculus. Ann. NY Acad. Sci. 626, 12-26.
6. Baird, R.A. (1994a) Comparative transduction and tuning mechanisms of hair cells in the bullfrog utriculus. I. Responses to intracellular current. J. Neurophysiol. 71, 666-684.
7. Baird, R.A. (1994b) Comparative transduction and tuning mechanisms of hair cells in the bullfrog utriculus. II. Sensitivity and response dynamics to mechanical displacement in the bullfrog utriculus. J. Neurophysiol. 71, 685-705.
8. Baird, R.A. and Schuff, N.R. (1994) Peripheral innervation patterns of vestibular nerve afferents in the bullfrog utriculus. J. Comp. Neurol. 342, 279-298.
9. Baird, R.A., Bale S., Fiorillo, C. and Schuff, N.R. (1996a) Hair cell regeneration in the vestibular otolith organs does not require cell proliferation. Auditory Neurosci. (submitted).
10. Baird, R.A., Steyger, P.S., and Schuff, N.R. (1996b) Mitotic and non- mitotic mechanisms of hair cell regeneration in the bullfrog. Ann. NY Acad. Sci. 781, 59-70.
11. Baird, R.A., Torres, M.A. and Schuff, N.R. (1996c) Ongoing and gentamicin-induced hair cell regeneration in the bullfrog vestibular otolith organs. I. Relationship to cell proliferation. J. Comp. Neurol. (submitted).
12. Baird, R.A., Torres, M.A. and Schuff, N.R. (1996d) Ongoing and gentamicin-induced hair cell regeneration in the bullfrog vestibular otolith organs. II. Contribution of non-mitotic mechanisms. J. Comp. Neurol. (submitted).
13. Barylko, B., Wagner, M.C., Reizes, O. and Albanesi, J.P. (1992) Purification and characterization of a mammalian myosin I. Proc. Natl. Acad. Sci. USA 89, 490-494.
14. 2+-ATPase. Ann. NY Acad. Sci. 671, 11-18.
15. 14C-2-deoxyglucose uptake in the brain of the zebra finch. II. Visual system. Cell Tiss. Res. 240, 117-127.
16. Canlon, B. (1996) The effects of sound conditioning on the cochlea. In: R. Salvi, D. Henderson, F. Fiorino, and V. Collietti (Eds.), Auditory System Plasticity and Regeneration. Thieme Medical Publ., New York, in press.
17. Celio, M.R. (1984) Parvalbumin as a marker of fast-firing neurons. Neurosci. Lett. (Suppl. 18), 822.
18. Celio, M.R. (1987) Parvalbumin in most gamma-amino-butyric acid-containing neurons of the rat cerebral cortex. Science 231, 995-997.
19. Celio, M.R. and Heizmann, C.W. (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature (Lond.) 293, 300-302.
20. Chacko, S., Jacob, S.S. and Horiuchi, K.Y. (1994) Myosin I from mammalian smooth muscle is regulated by caldesmon-calmodulin. J. Biol. Chem. 269, 15803-15807.
21. Cheney, R.E. and Mooseker, M.S. (1992) Unconventional myosins. Curr. Opin. Cell Biol. 4, 27-35.
22. Cheung, E.J. (1980) Calmodulin plays a pivotal role in cellular regulation. Science 207, 19-27.
23. Coluccio, L.M. (1994) Differential calmodulin binding to three myosin-1 isoforms from liver. J. Cell Sci. 107, 2279-2284.
24. Corey, D.P., Smith, W.J., Barres, B.A. and Koroshetz, W.J. (1987) Calmodulin inhibitors block adaptation in vestibular hair cells. Soc. Neurosci Abstr. 13, 538.
25. 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.
26. Crawford, A.C. and Fettiplace, R. (1981) An electrical tuning mechanism in turtle cochlear hair cells. J. Physiol. (Lond.) 312, 377-412.
27. Crawford, A.C., Evans, M.G. and Fettiplace, R. (1989) Activation and adaptation of transducer currents in turtle hair cells. J. Physiol. (Lond.) 419, 405-434.
28. Crawford, A.C., Evans, M.G. and Fettiplace, R. (1991) The actions of calcium on the mechanoelectric transducer current of turtle hair cells. J. Physiol. (Lond.) 434, 369-398.
29. Dechesne, C.J. and Thomasset, M. (1988) Calbindin (CaBP-28kDa) appearance and distribution during development of the mouse inner ear. Dev. Brain Res. 40, 233-242.
30. Dechesne, C.J., Thomasset, M., Brehier, A. and Sans, A. (1988) Calbindin (CaBP 28 kDa) localization in the peripheral vestibular system of various vertebrates. Hear. Res. 33, 273-278.
31. Dechesne, C.J., Winsky, L., Kim, H.N., Going, G., Vu, T.D., Wenthold, R.J. and Jacobowitz, D.M. (1991) Identification and ultrastructural localization of a calretinin-like calcium-binding protein (protein 10) in the guinea pig and rat inner ear. Brain Res. 560, 139-148.
32. 2+ binding on the profile structure of the sarcoplasmic reticulum membrane using time-resolved X-ray diffraction. Biophys. J. 64, 1750-1759.
33. Dememes, D., Eybalin, M. and Renard, N. (1993) Cellular distribution of parvalbumin immunoreactivity in the peripheral vestibular system of three rodents. Cell Tiss. Res. 274, 487-492.
34. Dememes, D., Moniot, B., Lomri, N., Thomasset, M. and Sans, A. (1991) Detection of calbindin-28k mRNA in rat vestibular ganglion neurones by in situ hybridization. Mol. Brain Res. 9, 153-156.
35. Due, C., Barakat-Walter, I. and Droz, B. (1994) Innervation of putative rapidly adapting mechanoreceptors by calbindin- and calretinin-immunoreactive primary sensory neurons in the rat. Eur. J. Neurosci. 6, 264-271.
36. Eatock, R.A., Corey, D.P. and Hudspeth, A.J. (1988) Adaptation of mechanoelectric transduction in hair cells of the bullfrog's sacculus. J. Neurosci. 7, 2821-2836.
37. Eatock, R.A., M. Saeki, and M.J. Hutzler (1993) Electrical resonance of isolated hair cells does not account for acoustic tuning in the free-standing region of the alligator lizard's cochlea. J. Neurosci. 13, 1767-1783.
38. Fernández, C. and Goldberg, J.M. (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static, tilts and to long-duration centrifugal force. J. Neurophysiol. 39, 970-984.
39. Fernández, C., Goldberg, J.M. and Baird, R.A. (1990) The vestibular nerve of the chinchilla. III. Peripheral innervation patterns in the utricular macula. J. Neurophysiol. 63, 767-780.
40. Fuchs, P.A., Nagai, T. and Evans, M.G. (1988) Electrical tuning in hair cells isolated from chick cochlea. J. Neurosci. 8, 2460-2467.
41. Gillespie, P.G. and Hudspeth, A.J. (1991) High-purity isolation of bullfrog hair bundles and subcellular and topological localization of constituent proteins. J. Cell Biol. 112, 625-640.
42. Gillespie, P.G., Wagner, M.C. and Hudspeth, A.J. (1993) Identification of a 120 kDa hair-bundle myosin located near stereociliary tips. Neuron 11, 581-594.
43. Gottmann, K. and Lux, H.D. (1995) Growth cone calcium ion channels: properties, clustering, and functional roles. Pers. Dev. Neurobiol. 2, 371-377.
44. Hawkins, J.S., Steyger, P.S., Burton, M.D., Schuff, N.R. and Baird, R.A. (1996) Calcium-binding proteins may be early markers of non-mitotically regenerating hair cells in the vestibular otolith organs. ARO Midwinter Meeting Abstr. 19, 7.
45. Hacohen, N., Assad, J.A., Smith, W.J. and Corey, D.P. (1989) Regulation of tension on hair-cell transduction channels: displacement and calcium dependence. J. Neurosci. 9, 3988-3997.
46. 2+-binding proteins in humans neurodegenerative disorders. TINS 15, 259-264.
47. Heizmann, C.W. and Hunziker, W. (1991) Intracellular calcium-binding proteins: more sites than insights. TIBS 16, 97-103.
48. 2+ dissociation rates from parvalbumin of frog muscle fibres. J. Physiol. 449, 399-410.
49. Hou, T.T., Johnson, J.D. and Rall, J.A. (1993) Role of parvalbumin in relaxation of frog skeletal muscle. Adv. Exp. Med. Biol. 332, 141-151
50. Howard, J. and Hudspeth, A.J. (1987) Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bull-frog's saccular hair cell. Proc. Natl. Acad. Sci. USA 84, 3064-3068.
51. Hsu, S.-M., Raine, L. and Fanger, H. (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. A comparison between ABC and unlabelled antibody (PAP) procedures. J. Histochem. Cytochem. 29, 577-580.
52. Hudspeth, A.J. and Lewis, R.S. (1988) Kinetic analysis of voltage- and ion-dependent conductances in saccular hair cells of the bull-frog, Rana catesbeiana. J. Physiol. (Lond.) 400, 237-274.
53. Hudspeth, A.J. and Gillespie, P.G. (1994) Pulling strings to tune transduction: adaptation by hair cells. Neuron 12, 1-9.
54. Hussy, N. (1991) Developmental change in calcium-activated chloride current during the differentiation of Xenopus spinal neurons in culture. Dev. Biol. 147, 225-238.
55. + channels at fluorescently labeled presynaptic active zones of hair cells. Proc. Natl. Acad. Sci. USA 91, 7578-7582.
56. Jaramillo, F. and Hudspeth, A.J. (1991) Localization of the hair cell's transduction channels at the hair bundle's top by iontophoretic application of a channel blocker. Neuron 7, 409-420.
57. Kelley, M.W., Ochiai, C.K. and Corwin, J.T. (1992) Maturation of kinocilia in amphibian hair cells: growth and shortening related to the kinociliary bulb formation. Hear. Res. 59, 108-115.
58. Kerschbaum, H.H. and Hermann, A. (1993) Calcium-binding proteins in the inner ear of Xenopus laevis (Daudin). Brain Res. 617, 43-49.
59. Lewis, E.R. (1987) Speculations about noise and the evolution of vertebrate hearing. Hear. Res. 25, 83-90.
60. Lewis, E.R. (1988) Tuning in the bullfrog inner ear. Biophys. J. 53, 441-447.
61. Lewis, E.R. and Li, C.W. (1973) Evidence concerning the morphogenesis of saccular receptors in the bullfrog (Rana catesbeiana). J. Morphol. 139, 351-362.
62. Lewis, E.R. and Li, C.W. (1975) Hair cell types and distributions in the otolithic and auditory organs of the bullfrog. Brain Res. 83, 35-50.
63. Lewis, E.R., Baird, R.A., Leverenz, E.L. and Koyama, H. (1982) Inner ear: dye injection reveals peripheral origins of specific sensitivities. Science 215, 1641-1643.
64. Lewis, R.S. and Hudspeth, A.J. (1983) Voltage and ion-dependent conductances in solitary vertebrate hair cells. Nature 304, 538-541.
65. Li, C.W. and Lewis, E.R. (1979) Structure and development of vestibular hair cells in the larval bullfrog. Ann. Otol. Rhinol. Laryngol. 88, 427-437.
66. Maler, L., Jande, S.S. and Lawson, D.E.M. (1984) Localization of vitamin D-dependent calcium-binding protein in the electrosensory and electromotor system of high-frequency gymnotid fish. Brain Res. 301, 166-170.
67. Means, A.R., Van Berkum, M.F.A., Bagchi, I., Lu, K.P. and Rasmussen, C.D. (1991) Regulatory functions of calmodulin. Pharmacol. Ther. 50, 255-270.
68. Oberholtzer, J.C., Buettger, C., Summers, M.C. and Matschinsky, F.M. (1988) The 28-kDa calbindin-D is a major calcium-binding protein in the basilar papilla of the chick. Proc. Natl. Acad. Sci. USA 85, 3387-3390.
69. Pack, A.K. and Slepecky, N.B. (1995) Cytoskeletal and calcium-binding proteins in the mammalian organ of Corti: cell type-specific proteins displaying longitudinal and radial gradients. Hear. Res. 91, 119-135.
70. Pitchford, S. and Ashmore, J.F. (1987) An electrical resonance in hair cells of the amphibian papilla of the frog Rana temporaria. Hear. Res. 27, 75-84.
71. Platt, C. and Popper, A.N. (1981) Fine structure and function of the inner ear. In: W. Tavolga, A.N. Popper and R.R. Fay (Eds.), Hearing and Sound Communication in Fishes. Springer, New York, pp. 3-38.
72. Rabie, A., Thomasset, M. and Legrand, Ch. (1983) Immunocytochemical detection of calcium-binding protein in the cochlear and vestibular hair cells of the rat. Cell Tiss. Res. 233, 691-696.
73. Reizes, O., Barylko, B., Li, C., Sudhof, T.C. and Albanesi, J.P. (1994) Domain structure of a mammalian myosin I. Proc. Natl. Acad. Sci. USA 91, 6349-6353.
74. Roberts, W.M. (1993) Spatial calcium buffering in saccular hair cells. Nature (Lond.) 363, 74-76.
75. Roberts, W.M., Jacobs, R.A. and Hudspeth, A.J. (1990) Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10, 3664-3684.
76. Rogers, J.H. (1987) Calretinin: a gene for a novel calcium-binding protein expressed principally in neurons. J. Cell Biol. 105, 1343-1353.
77. Rogers, J.H. (1989a) Calcium-binding proteins, the search for functions. Nature 339, 661-662.
78. Rogers, J.H. (1989b) Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31, 697-709.
79. Ruppert, C., Kroschewski, R. and Bahler, M. (1993) Identification, characterization and cloning of myr 1, a mammalian myosin-I. J. Cell Biol. 120, 1393-1403.
80. Sacks, D.B., Porter, S.E., Ladenson, J.H. and McDonald, J.M. (1991) Monoclonal antibody to calmodulin: development, characterization, and comparison with polyclonal anti-calmodulin antibodies. Anal. Biochem. 194, 369-377.
81. Saidel, W.M., Presson, J.C. and Chang, J.S. (1990) S-100 immunoreactivity identifies a subset of hair cells in the utricle and saccule of a fish. Hear. Res. 47, 139-146.
82. Sans, A., Etchecopar, B., Brehier, A. and Thomasset, M. (1986) Immunocytochemical detection of vitamin D-dependent calcium-binding protein (CaBP-28K) in vestibular sensory hair cells and vestibular ganglion neurones of the cat. Brain Res. 364, 190-194.
83. Sans, A., Brehier, A., Moniot, B. and Thomasset, M. (1987) Immunoelectronmicroscopic localization of 'vitamin D-dependent' calcium-binding protein (CaBP-28k) in the vestibular hair cells of the cat. Brain Res. 435, 293-304.
84. Shepherd, G.M.G., Barres, B.A. and Corey, D.P. (1989) 'Bundle blot' purification and initial protein characterization of hair cell stereocilia. Proc. Natl. Acad. Sci. USA 86, 4973-4977.
85. Solbach, S. and Celio, M.R. (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat. Embryol. 184, 103-124.
86. Speksnijder, J.E., Miller, A.L., Weisenseel, M.H., Chen, T.-H. and Jaffe, L.F. (1989). Calcium buffer injections block fucoid egg development by calcium diffusion. Proc. Natl. Acad. Sci. USA 86, 6607-6611.
87. Steyger, P.S., Dumont, R.A., Gillespie, P.G. and Baird, R.A. (1996a) Myosin Iβ immunolabeling in hair bundles of adapting and non-adapting vestibular hair cells. ARO Midwinter Abstr. 19, 743.
88. Steyger, P.S., Burton, M.D., Hawkins, J.S., Schuff, N.R., and Baird, R.A. (1996b) Calcium-binding proteins may be early markers of non-mitotically regenerating hair cells in the vestibular otolith organs. Inter. J. Dev. Neurosci., in press.
89. 2+ translocation. Biochem. Biophys. Res. Commun. 199, 56-62.
90. Warrick, H.M., Simmons, R.M., Finer, J.T., Uyeda, T.Q., Chu, S. and Spudich, J.A. (1993) In vitro methods for measuring force and velocity of the actin-myosin interaction using purified proteins. Meth. Cell Biol. 39, 1-21.
91. Walker, R.G., Hudspeth, A.J. and Gillespie, P.G. (1993) Calmodulin and calmodulin-binding proteins in hair bundles. Proc. Natl. Acad. Sci. USA 90, 2807-2811.
92. Wasserman, R.H., Chandler, J.S., Meyer, S.A., Smith, C.A., Brindak, M.E., Fullmer, C.S., Penniston, J.T. and Kumar, R. (1992) Intestinal calcium transport and calcium extrusion processes at the basolateral membrane. J. Nutr. 122 (Suppl.), 662-671.
93. Weiss, T.F. and Rose, C. (1988) Stages of degradation of timing information in the cochlea: a comparison of hair-cell and nerve-fiber responses in the alligator lizard. Hear. Res. 33, 167-174.
94. Wersäll, J. and Bägger-Sjöbäck, D. (1974) Morphology of the vestibular apparatus. In: H.H. Kornhuber (Ed.), Handbook of Sensory Physiology. Vol. VI/1. Springer, New York, pp. 123-170.
95. Williams, R. and Coluccio, L.M. (1995) Phosphorylation of myosin-I from rat liver by protein kinase C reduces calmodulin binding. Biochem. Biophys. Res. Comm. 216, 90-102.
96. Yamaguchi, T., Winsky, L. and Jacobowitz, D.M. (1991) Calretinin, a neuronal calcium binding protein inhibits phosphorylation of a 39 kDa synaptic membrane protein from rat cerebral cortex. Neurosci. Lett. 131, 79-82.