ATPase activity of myosin in hair bundles of the bullfrog's sacculus

Biophysical Journal

Volumn 72, Issue 1, 1997, Pages 263-271

  Burlacu, S ^a   Tap, W D ^a   Lumpkin, E A ^a   Hudspeth, A J ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BULLFROG; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; HAIR CELL; NONHUMAN; SACCULUS;

ANIMALIA; RANA CATESBEIANA;

EID: 0031038446     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78665-X     Document Type: Article

References (60)

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. Assad, J. A., N. Hacohen, and D. P. Corey. 1989. Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc. Natl. Acad. Sci. U.S.A. 86:2918-2922.
3. 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. Nature Genet. 11:369-375.
4. Barylko, B., M. C. Wagner, O. Reizes, and J. P. Albanesi. 1992. Purification and characterization of a mammalian myosin I. Proc. Natl. Acad. Sci. U.S.A. 89:490-494.
5. Borejdo, J., and S. Burlacu. 1992. Velocity of movement of actin filaments in in vitro motility assay. Measured by fluorescence correlation spectroscopy. Biophys. J. 61:1267-1280.
6. Burnham, J. A., and C. E. Stirling. 1984. Quantitative Na-K pump sites in the frog sacculus. J. Neurocytol. 13:617-638.
7. Carafoli, E. 1991. Calcium pump of the plasma membrane. Physiol. Rev. 71:129-153.
8. Corey, D. P., and A. J. Hudspeth. 1979. Ionic basis of the receptor potential in a vertebrate hair cell. Nature. 281:675-677.
9. Cox, J. A., M. Comte, A. Mamar-Bachi, M. Milos, and J.-J. Schaer. 1988. Cation binding to calmodulin and relation to function. In Calcium and Calcium Binding Proteins C. Gerday, R. Gilles, and L. Bolis, editors. Springer-Verlag, Berlin. 141-162.
10. DasGupta, G., and E. Reisler. 1991. Nucleotide-induced changes in the interaction of myosin subfragment 1 with actin: detection by antibodies against the N-terminal segment of actin. Biochemistry. 30:9961-9966.
11. 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.
12. Drenckhahn, D., K. 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. 300:531-532.
13. Dumont, R. A., E. N. Yamoah, E. A. Lumpkin, A. J. Hudspeth, and P. G. Gillespie. 1996. Plasma-membrane calcium ATPase maintains a very low stereociliary calcium concentration. Soc. Neurosci. Abstr. 22:1064.
14. Eatock, R. A., D. P. Corey, and A. J. Hudspeth. 1987. Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus. J. Neurosci. 7:2821-2836.
15. Elzinga, M., J. H. Collins, W. M. Kuehl, and R. S. Adelstein. 1973. Complete amino-acid sequence of actin of rabbit skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 70:2687-2691.
16. Ferenczi, M. A., Z.-H. He, R. K. Chillingworth, M. Brune, J. E. T. Corrie, D. R. Trentham, and M. R. Webb. 1995. A new method for the time-resolved measurement of phosphate release in permeabilized muscle fibers. Biophys. J. 68:191s-193s.
17. Funatsu, T., Y. Harada, M. Tokunaga, K. Saito, and T. Yanagida. 1995. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature. 374:555-559.
18. Furness, D. N., and C. M. Hackney. 1985. Cross-links between stereocilia in the guinea pig cochlea. Hearing Res. 18:177-188.
19. 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. 374:62-64.
20. 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.
21. Gillespie, P. G., and A. J. Hudspeth. 1993. Adenine nucleoside diphosphates block adaptation of mechanoelectrical transduction in hair cells. Proc. Natl. Acad. Sci. U.S.A. 90:2710-2714.
22. Gillespie, P. G., M. C. Wagner, and A. J. Hudspeth. 1993. Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron. 11:581-594.
23. Hacohen, N., J. A. Assad, W. J. Smith, and D. P. Corey. 1989. Regulation of tension on hair-cell transduction channels: displacement and calcium dependence. J. Neurosci. 9:3988-3997.
24. 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. U.S.A. 92:9815-9819.
25. Howard, J., and A. J. Hudspeth. 1987a. Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell. Proc. Natl. Acad. Sci. U.S.A. 84: 3064-3068.
26. Howard, J., and A. J. Hudspeth. 1987b. Adaptation of mechanoelectrical transduction in hair cells. In Sensory Transduction. A. J. Hudspeth, P. R. MacLeish, F. L. Margolis, and T. N. Wiesel, editors. Report of the 1987 FESN Study Group; Discussions in Neurosciences, Vol. IV, No. 3. Fondation pour l'Etude du Système Nerveux Central et Périphérique, Geneva. 138-145.
27. Hudspeth, A. J. 1982. Extracellular current flow and the site of transduction by vertebrate hair cells. J. Neurosci. 2:1-10.
28. Hudspeth, A. J. 1989. How the ear's works work. Nature. 341:397-404.
29. Hudspeth, A. J., and P. G. Gillespie. 1994. Pulling springs to tune transduction: adaptation by hair cells. Neuron. 12:1-9.
30. Jaramillo, F., and A. J. Hudspeth. 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.
31. Jaramillo, F., and A. J. Hudspeth. 1993. Displacement-clamp measurement of the forces exerted by gating springs in the hair bundle. Proc. Natl. Acad. Sci. U.S.A. 90:1330-1334.
32. Johara, M., Y. Y. Toyoshima, A. Ishijima, H. Kojima, T. Yanagida, and K. Sutoh. 1993. Charge-reversion mutagenesis of Dictyostelium actin to map the surface recognized by myosin during ATP-driven sliding motion. Proc. Natl. Acad. Sci. U.S.A. 90:2127-2131.
33. Kellerman, K. A., and K. G. Miller. 1992. An unconventional myosin heavy chain gene from Drosophila melanogaster. J. Cell Biol. 119: 823-834.
34. Kögler, H., A. J. G. Moir, I. P. Trayer, and J. C. Rüegg. 1991. Peptide competition of actin activation of myosin-subfragment 1 ATPase by an amino terminal actin fragment. FEBS Lett. 294:31-34.
35. Korn, E. D., J. H. Collins, and H. Maruta. 1982. Myosins from Acanthamoeba castellanii. Meth. Enzymol. 85:357-363.
36. Lin, C. H., E. M. Espreafico, M. S. Mooseker, and P. Forscher. 1996. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron. 16:769-782.
37. 2+ entry through mechanosensitive channels localizes the site of mechanoelectrical transduction in hair cells. Proc. Natl. Acad. Sci. U.S.A. 92: 10297-10301.
38. Marks, P. W., and F. R. Maxfield. 1991. Preparation of solutions with free calcium concentration in the nanomolar range using 1,2-bis(o-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid. Anal. Biochem. 193: 61-71.
39. 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. U.S.A. 91:11821-11825.
40. Mornet, D., R. Bertrand, P. Pantel, E. Audemard, and R. Kassab. 1981. Structure of the actin-myosin interface. Nature. 292:301-306.
41. Narins, P. M., and E. R. Lewis. 1984. The vertebrate ear as an exquisite seismic sensor. J. Acoust. Soc. Am. 76:1384-1387.
42. Ohmori, H. 1985. Mechano-electrical transduction currents in isolated vestibular hair cells of the chick. J. Physiol. 359:189-217.
43. Ohno, T., and T. Kodama. 1991. Kinetics of adenosine triphosphate hydrolysis by shortening myofibrils from rabbit psoas muscle. J. Physiol. 441:685-702.
44. Pemrick, S., and A. Weber. 1976. Mechanism of inhibition of relaxation by N-ethylmaleimide treatment of myosin. Biochemistry. 15:5193-5198.
45. Pickles, J. O., S. D. Comis, and S. D. Osborne. 1984. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hearing Res. 15:103-112.
46. Rayment, I., H. M. Holden, M. Whittaker, C. B. Yohn, M. Lorenz, K. C. Holmes, and R. A. Milligan. 1993. Structure of the actin-myosin complex and its implications for muscle contraction. Science. 261:58-65.
47. Reizes, O., B. Barylko, C. Li, T. C. Südhof, and J. P. Albanesi. 1994. Domain structure of a mammalian myosin Iβ. Proc. Natl. Acad. Sci. U.S.A. 91:6349-6353.
48. Richards, D. E., A. F. Rega, and P. J. Garrahan. 1977. ATPase and phosphatase activities from human red cell membranes: I. The effects of N-ethylmaleimide. J. Membr. Biol. 35:113-124.
49. 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. U.S.A. 86:4973-4977.
50. Solc, C. K., B. H. Derfler, G. M. Duyk, and D. P. Corey. 1994. Molecular cloning of myosins from the bullfrog saccular macula: a candidate for the hair cell adaptation motor. Auditory Neurosci. 1:63-75.
51. Sowerby, A. J., C. K. Seehra, M. Lee, and C. R. Bagshaw. 1993. Turnover of fluorescent nucleoside triphosphates by isolated immobilized myosin filaments. Transient kinetics on the zeptomole scale. J. Mol. Biol. 234:114-123.
52. Takemura, H., A. R. Hughes, O. Thastrup, and J. W. Putney, Jr. 1989. Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool, and not an inositol phosphate, regulates calcium fluxes at the plasma membrane. J. Biol. Chem. 264:12266-12271.
53. Wagner, M. C., K. K. Pfister, G. S. Bloom, and S. T. Brady. 1989. Copurification of kinesin polypeptides with microtubule-stimulated Mg-ATPase activity and kinetic analysis of enzymatic properties. Cell Motil. Cytoskeleton. 12:195-215.
54. 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. U.S.A. 93:2203-2207.
55. Walker, R. G., A. J. Hudspeth, and P. G. Gillespie. 1993. Calmodulin and calmodulin-binding proteins in hair bundles. Proc. Natl. Acad. Sci. U.S.A. 90:2807-2811
56. Weil, D., S. Blanchard, J. Kaplan, P. Guilford, F. Gibson, J. Walsh, P. Mburu, A. Varela, J. Levilliers, M. D. Weston, P. M. Kelley, W. J. Kimberling, M. Wagenaar, F. Levi-Acobas, D. Larget-Piet, A. Munnich, K. P. Steel, S. D. M. Brown, and C. Petit. 1995. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature. 374:60-61.
57. Wolenski, J. S., S. M. Hayden, P. Forscher, and M. S. Mooseker. 1993. Calcium-calmodulin and regulation of brush border myosin-I MgATPase and mechanochemistry. J. Cell Biol. 122:613-621.
58. 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.
59. Zhu, T., M. Sata, and M. Ikebe. 1996. Functional expression of mammalian myosin Iβ: analysis of its motor activity. Biochemistry. 35:513-522.
60. Zot, H. G., S. K. Doberstein, and T. D. Pollard. 1992. Myosin-I moves actin filaments on a phospholipid substrate: implications for membrane targeting. J. Cell Biol. 116:367-376.