A model of stereocilia adaptation based on single molecule mechanical studies of myosin I

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 359, Issue 1452, 2004, Pages 1895-1905

  Batters, Christopher ^a   Wallace, Mark I ^a   Coluccio, Lynne M ^b   Molloy, Justin E ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

Hearing; Molecular motors; Myolc; Optical tweezers; Sensory adaptation

Indexed keywords

MUSCLE;

EUKARYOTA;

EID: 13444256475     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2004.1559     Document Type: Conference Paper

References (44)

1. Balish, M. F., Moeller, E. F. & Coluccio, L. M. 1999 Overlapping distribution of the 130- and 110-kDa myosin I isoforms on rat liver membranes. Arch. Biochem. Biophys. 370, 285-293.
2. Batters, C., Arthur, C. P., Lin, A., Porter, J., Geeves, M. A., Milligan, R. A., Molloy, J. E. & Coluccio, L. M. 2004 Myo1c is designed for the adaptation response in the inner ear. EMBO J. 23, 1433-1440.
3. Bose, A., Guilherme, A., Robida, S. I., Nicoloro, S. M. C., Zhou, Q. L., Jiang, Z. Y., Pomerleau, D. P. & Czech, M. P. 2002 Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420, 821-824.
4. Brenner, B., Chalovich, J. M., Greene, L. E., Eisenberg, E. & Schoenberg, M. 1986 Stiffness of skinned rabbit psoas fibers in MgATP and MgPPi solution. Biophys. J. 50, 685-691.
5. Bustamante, C., Marko, J. F., Siggia, E. D. & Smith, S. 1994 Entropie elasticity of lambda-phage DNA. Science 265, 1599-1600.
6. Coluccio, L. M. & Conaty, C. 1993 Myosin-1 In mammalian liver. Cell Motil. Cytoskel. 24, 189-199.
7. Coluccio, L. R. & Geeves, M. A. 1999 Transient kinetic analysis of the 130-kDa myosin I (MYR-1 gene product) from rat liver - a myosin I designed for maintenance of tension? J. Biol. Chem. 130, 21 575-21 580.
8. Cordonnier, M. N., Dauzonne, D., Louvard, D. & Coudrier, E. 2001 Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell 12, 4013-4029.
9. Corey, D. P. & Hudspeth, A. J. 1983 Analysis of the microphonic potential of the bullfrogs sacculus. J. Neurosci. 3, 942-961.
10. Cremo, C. R. & Geeves, M. A. 1998 Interactions of actin with ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle. Biochemistry 37, 1969-1978.
11. Diefenbach, T. J., Latham, V. A., Yimlamai, D., Liu, C. A., Herman, I. M. & Jay, D. G. 2002 Myosin 1c and myosin IIB serve opposing roles in lamellipodial dynamics of the neuronal growth cone. J. Cell Biol. 158, 1207-1217.
12. Dupuis, D. E., Guilford, W. H., Wu, J. & Warshaw, D. M. 1997 Actin filament mechanics in the laser trap. J. Muscle Res. Cell Motil 18, 17-30.
13. Finer, J. T., Simmons, R. M. & Spudich, J. A. 1994 Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113-118.
14. Garcia, J. A., Yee, A. G., Gillespie, P. G. & Corey, D. P. 1998 Localization of myosin-1 beta near both ends of tip links in frog saccular hair cells. J. Neurosci. 18, 8637-8647.
15. Gillespie, P. G. 2004 Myosin-I and adaptation of mechanical transduction by the inner ear. Phil. Trans. R. Soc. B 359. 1945-1951.(doi:10.1098/rstb.2004. 1564.)
16. Gillespie, P. G. (and 27 others) 2001 Myosin-I nomenclature. J. Cell Biol. 155, 703-704.
17. Gillespie, P. G., Wagner, M. C. & Hudspeth, A. J. 1993 Identification of a 120 Kd hair-bundle myosin located near stereociliary tips. Neuron 11, 581-594.
18. Glowatzki, E. & Fuchs, P. A. 2002 Transmitter release at the hair cell ribbon synapse. Nature Neurosci, 5, 147-154.
19. Holt, J. R. & Corey, D. P. 2000 Two mechanisms for transducer adaptation in vertebrate hair cells. Proc. Natl Acad. Sci. USA 97, 11 730-11 735.
20. Holt, J. R., Gillespie, S. K., Provance, D. W., Shah, K., Shokat, K. M., Corey, D. P., Mercer, J. A. & Gillespie, P. G. 2002 A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108, 371-381.
21. Howard, J. & Hudspeth, A. J. 1987 Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrogs saccular hair cell. Proc. Natl Acad. Sci. USA 84, 3064-3068.
22. Howard, J. & Hudspeth, A. J. 1988 Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrogs saccular hair cell. Neuron 1, 189-199.
23. Huxley, A. F. & Simmons, R. M. 1971 Proposed mechanism of force generation in muscle. Nature 233, 533-538.
24. Jacobs, R. A. & Hudspeth, A. J. 1990 Ultrastructural correlates of mechanoelectrical transduction in hair cells of the bullfrogs internal ear. Cold Spring Harbor Symp. Quant. Biol. 55, 547-561.
25. Kishino, A. & Yanagida, T. 1988 Force measurements by micromanipulation of a single actin filament by glass needles. Nature 334, 74-76.
26. Kron, S. J. & Spudich, J. A. 1986 Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl Acad. Sci. USA 83, 6272-6276.
27. Kros, C. J., Marcotti, W., van Netten, S. M., Self, T. J., Libby, R. T., Brown, S. D. M., Richardson, G. P. & Steel, K. P. 2002 Reduced climbing and increased slipping adaptation in cochlear hair cells of mice with Myo7a mutations. Nature Neurosci. 5, 41-47.
28. Marquis, R. E. & Hudspeth, A. J. 1997 Effects of extracellular Ca2+ concentration on hair-bundle stiffness and gating-spring integrity in hair cells. Proc. Natl Acad. Sci. USA 94, 11 923-11928.
29. Martin, P., Mehta, A. D. & Hudspeth, A. J. 2000 Negative hair-bundle stiffness betrays a mechanism for mechanical amplification by the hair cell. Proc. Natl Acad. Sci. USA 97, 12026-12031.
30. Molloy, J. E. 1998 Optical chopsticks: digital synthesis of multiple optical traps. Meth. Cell Biol. 55, 205-216.
31. Molloy, J. E., Burns, J. E., Kendrick Jones, J., Tregear, R. T. & White, D. C. S. 1995 Movement and force produced by a single myosin head. Nature 378, 209-212.
32. Pardee, J. D. & Spudich, J. A. 1982 Purification of muscle actin Meth. Enzymol. 85, 164-181.
33. Rayment, I., Rypniewski, W. R., Schmidtbase, K., Smith, R., Tomchick, D. R., Benning, M. M., Winkelmann, D. A., Wesenberg, G. & Holden, H. M. 1993 Three-dimensional structure of myosin subfragment-1 - a molecular motor. Science 261, 50-58.
34. Ruppert, C., Kroschewski, R. & Bahler, M. 1993 Identification, characterization and cloning of Myr-1, a mammalian myosin-I. J. Cell Biol. 120, 1393-1403.
35. Siemens, J., Lillo, C., Dumont, R. A., Reynolds, A., Williams, D. S., Gillespie, P. G. & Muller, U. 2004 Cadherin 23 is a component of the tip link in hair cell stereocilia. Nature 428, 950-955.
36. Sleep, J. A. & Hutton, R. L. 1978 Actin mediated release of ATP from a myosin-ATP complex. Biochemistry 17, 5423-5430.
37. Sollner, C., Rauch, G. J., Siemens, J., Geisler, R., Schuster, S. C., Tubingen 2000 Screen Consortium, t., Muller, U. & Nicolson, T. 2004 Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428, 955-959.
38. Steffen, W., Smith, D. & Sleep, J. 2003 The working stroke upon myosin-nucleotide complexes binding to actin. Proc. Natl Acad. Sci. USA 100, 6434-6439.
39. Tang, N. Y., Lin, T. M. & Ostap, E. M. 2002 Dynamics of Myo1c (myosin-I beta) lipid binding and dissociation. J. Biol. Chem. 277, 42 763-42 768.
40. Trentham, D. R. 1977 The ATPase reactions of myosin and actomyosin and their relation to energy transduction in muscle Biochem. J. 5, 5-22.
41. Veigel, C., Bartoo, M. L., White, D. C. S., Sparrow, J. C. & Molloy, J. E. 1998 The stiffness of rabbit skeletal actomyosin cross-bridges determined with an optical tweezers transducer Biophys. J. 75, 1424-1438.
42. Veigel, C., Coluccio, L. M., Jontes, J. D., Sparrow, J. C., Milligan, R. A. & Molloy, J. E. 1999 The motor protein myosin-I produces its working stroke in two steps. Nature 398, 530-533.
43. Weil, D., Blanchard, S., Kaplan, J., Guilford, P., Gibson, F., Walsh, J., Mburu, P., Valera, A., Levillers, J. & Weston, M. D. 1995 Defective myosin VIIA gene responsible for usher syndrome typeB. Nature 374, 60-61.
44. Wu, Y. C., Ricci, A. J. & Fettiplace, R. 1999 Two components of transducer adaptation in auditory hair cells. J. Neurophysiol. 82, 2171-2181.