Lever arms and necks: A common mechanistic theme across the myosin superfamily

Journal of Muscle Research and Cell Motility

Volumn 25, Issue 6, 2004, Pages 467-474

  Warshaw, David M ^a  

^a UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN;

ACTIN MYOSIN INTERACTION; ALPHA HELIX; ARM MUSCLE; CONFERENCE PAPER; ELECTRON MICROSCOPY; MUSCLE CELL; NECK MUSCLE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; SKELETAL MUSCLE; X RAY ANALYSIS;

ACTINS; ANIMALS; FORECASTING; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MYOSINS;

EID: 19944432301     PISSN: 01424319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10974-004-1767-z     Document Type: Conference Paper

References (71)

1. Ali MY, Homma K, Iwane AH, Adachi K, Itoh H, Kinosita K Jr, Yanagida T and Ikebe M (2004) Unconstrained steps of myosin vi appear longest among known molecular motors. Biophys J 86: 3804-3810.
2. Ali MY, Uemura S, Adachi K, Itoh H, Kinosita K Jr and Ishiwata S (2002) Myosin V is a left-handed spiral motor on the right-handed actin helix. Nat Struct Biol 9: 464-467.
3. Altman D, Sweeney HL and Spudich JA (2004) The mechanism of myosin VI translocation and its load-induced anchoring. Cell 116: 737-749.
4. Bahloul A, Chevreux G, Wells AL, Martin D, Nolt J, Yang Z, Chen LQ, Potier N, Van Dorsselaer A, Rosenfeld S, Houdusse A and Sweeney HL (2004) The unique insert in myosin VI is a structural calcium-calmodulin binding site. Proc Natl Acad Sci USA 101: 4787-4792.
5. Baker JE, Brosseau C, Joel PB and Warshaw DM (2002) The biochemical kinetics underlying actin movement generated by one and many skeletal muscle myosin molecules. Biophys J 82: 2134-2147.
6. Baker JE, Brust-Mascher I, Ramachandran S, LaConte LE and Thomas DD (1998) A large and distinct rotation of the myosin light chain domain occurs upon muscle contraction. Proc Natl Acad Sci USA 95: 2944-2949.
7. Berg JS, Pwell BC and Cheney RE (2001) A millennial myosin census. Mol Biol Cell 12: 780-794.
8. Block SM (1996) Fifty ways to love your lever: myosin motors. Cell 87: 151-157.
9. Block SM, Goldstein LS and Schnapp BJ (1990) Bead movement by single kinesin molecules studies with optical tweezers. Nature 348: 348-352.
10. Corrie JE, Brandmeier BD, Ferguson RE, Trentham DR, Kendrick-Jones J, Hopkins SC, van der Heide UA, Goldman YE, Sabido-David C, Dale RE, Criddle S and Irving M (1999) Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature 400: 425-430.
11. Cremo CR and Geeves MA (1998) Interaction of actin and ADP with the head domain of smooth muscle myosin: implications for strain-dependent ADP release in smooth muscle. Biochemistry 37: 1969-1978.
12. Dantzig JA, Barsotti RJ, Manz S, Sweeney HL and Goldman YE (1999) The ADP release step of the smooth muscle cross-bridge cycle is not directly associated with force generation. Biophys J 77: 386-397.
13. Dominguez R, Freyzon Y, Trybus KM and Cohen C (1998) Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the pre-power stroke state. Cell 94: 559-571.
14. -. Biochemistry 34: 8960-8972.
15. Forkey JN, Quinlan ME, Shaw MA, Corrie JE and Goldman YE (2003) Three-dimensional structural dynamics of myosin V by single-molecule .uorescence polarization. Nature 422: 399-404.
16. Galkin VE, VanLoock MS, Orlova A and Egelman EH (2002) A new internal mode in F-actin helps explain the remarkable evolutionary conservation of actin's sequence and structure. Curr Biol 12: 570-575.
17. Geeves MA and Holmes KC (1999) Structural mechanism of muscle contraction. Annu Rev Biochem 68: 687-728.
18. Herm-Gotz A, Weiss S, Stratmann R, Fujita-Becker S, Ruff C, Meyhofer E, Soldati T, Manstein DJ, Geeves MA and Soldati D (2002) Toxoplasma gondii myosin A and its light chain: a fast, single-headed, plus-end-directed motor. EMBO J 21: 2149-2158.
19. Hodge T and Cope MJ (2000) A myosin family tree. J Cell Sci 113: 3353-3354
20. Holmes KC (1997) The swinging lever-arm hypothesis of muscle contraction. Curr Biol 7: R112-R118.
21. Houdusse A, Szent-Gyorgyi AG and Cohen C (2000) Three conformational states of scallop myosin S1. Proc Natl Acad Sci USA 97: 11238-11243.
22. Howard J and Spudich JA (1996) Is the lever arm of myosin a molecular elastic element? Proc Natl Acad Sci USA 93: 4462-4464.
23. Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7: 255-318.
24. Huxley HE (1969) The mechanism of muscular contraction. Science 164: 1356-1365.
25. Huxley AF (1974) Muscular contraction. J Physiol 243: 1-43.
26. Huxley HE (1990) Sliding filaments and molecular motile systems. J Biol Chem 265: 8347-8350.
27. Huxley H and Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173: 973-976.
28. Huxley AF and Niedergerke R (1954) Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173: 971-973.
29. Huxley AF and Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233: 533-538.
30. Irving M, St Claire Allen T, Sabido-David C, Craik JS, Brandmeier B, Kendrick-Jones J, Corrie JE, Trentham DR and Goldman YE (1995) Tilting of the light-chain region of myosin during step length changes and active force generation in skeletal muscle. Nature 375: 688-691.
31. Itakura S, Yamakawa H, Toyoshima YY, Ishijima A, Kojima T, Harada Y, Yanagida T, Wakabayashi T and Sutoh K (1993) Force-generating domain of myosin motor. Biochem Biophys Res Commun 196: 1504-1510.
32. Jontes JD, Wilson-Kubalek EM and Milligan RA (1995) A 32 degree tail swing in brush border myosin I on ADP release. Nature 378: 751-753.
33. Kad NM, Rovner AS, Fagnant PM, Joel PB, Kennedy G, Patlak JB, Warshaw D and Trybus KM (2003) A mutant heterodimeric myosin with one inactive head generates maximal displacement. J Cell Biol 162: 481-488.
34. Khromov AS, Somlyo AP and Somlyo AV (2001) Photolytic release of MgADP reduces rigor force in smooth muscle. Biophys J 80: 1905-1914.
35. Kitamura K, Tokunaga M, Iwane AH and Yanagida T (1999) A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature 397: 129-134.
36. Kohler D, Ruff C, Meyhofer E and Bahler M (2003) Different degrees of lever arm rotation control myosin step size. J Cell Biol 161: 237-241.
37. Lauzon AM, Fagnant PM, Warshaw DM and Trybus KM (2001) Coiled-coil unwinding at the smooth muscle myosin head-rod junction is required for optimal mechanical performance. Biophys J 80: 1900-1904.
38. Lister I, Schmitz S, Walker M, Trinick J, Buss F, Veigel C and Kendrick-Jones J (2004) A monomeric myosin VI with a large working stroke. EMBO J 23: 1729-1738.
39. Lowey S, Slayter HS, Weeds AG and Baker H (1969) Substructure of the myosin molecule. I. Subfragments of myosin by enzymic degradation. J Mol Biol 42: 1-29.
40. Lymn RW and Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10: 4617-4624.
41. McGough A, Pope B, Chiu W and Weeds A (1997) Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J Cell Biol 138: 771-781.
42. Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS and Cheney RE (1999) Myosin-V is a processive actin-based motor. Nature 400: 590-593.
43. Moore JR, Krementsova EB, Trybus KM and Warshaw DM (2001) Myosin V exhibits a high duty cycle and large unitary displacement. J Cell Biol 155: 625-635.
44. Moore JR, Krementsova EB, Trybus KM and Warshaw DM (2004) Does the myosin V neck region act as a lever? J Muscle Res Cell Motil 25: 29-35.
45. Nishikawa S, Homma K, Komori Y, Iwaki M, Wazawa T, Hikikoshi Iwane A, Saito J, Ikebe R, Katayama E, Yanagida T and Ikebe M (2002) Class VI myosin moves processively along actin filaments backward with large steps. Biochem Biophys Res Commun 290: 311-317.
46. Purcell TJ, Morris C, Spudich JA and Sweeney HL (2002) Role of the lever arm in the processive stepping of myosin V. Proc Natl Acad Sci USA 99: 14159-14164.
47. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G and Holden HM (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261: 50-58.
48. Reedy MK, Holmes KC and Tregear RT (1965) Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature 207: 1276-1280.
49. Rief M, Rock RS, Mehta AD, Mooseker MS, Cheney RE and Spudich JA (2000) Myosin-V stepping kinetics: a molecular model for processivity. Proc Natl Acad Sci USA 97: 9482-9486.
50. Rock RS, Rice SE, Wells AL, Purcell TJ, Spudich JA and Sweeney HL (2001) Myosin VI is a processive motor with a large step size. Proc Natl Acad Sci USA 98: 13655-13659.
51. Ruff C, Furch M, Brenner B, Manstein DJ and Meyhofer E (2001) Single-molecule tracking of myosins with genetically engineered amplifier domains. Nat Struct Biol 8: 226-229.
52. Sakamoto T, Amitani I, Yokota E and Ando T (2000) Direct observation of processive movement by individual myosin V molecules. Biochem Biophys Res Commun 272: 586-590.
53. Sakamoto T, Wang F, Schmitz S, Xu Y, Molloy JE, Veigel C and Sellers JR (2003) Neck length and processivity of myosin V. J Biol Chem 278: 29201-29207.
54. Schott DH, Collins RN and Bretscher A (2002) Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J Cell Biol 156: 35-39.
55. Shih WM, Gryczynski Z, Lakowicz JR and Spudich JA (2000) A FRET-based sensor reveals large ATP hydrolysis-induced conformational changes and three distinct states of the molecular motor myosin. Cell 102: 683-694.
56. Smith CA and Rayment I (1996) X-ray structure of the magnesium(II).ADP. vanadate complex of the Dictyostelium discoideum myosin motor domain to 1.9 A resolution. Biochemistry 35: 5404-5417.
57. Suzuki Y, Yasunaga T, Ohkura R, Wakabayashi T and Sutoh K (1998) Swing of the lever arm of a myosin motor at the isomerization and phosphate-release steps. Nature 396: 380-383.
58. Tanaka H, Homma K, Iwane AH, Katayama E, Ikebe R, Saito J, Yanagida T and Ikebe M (2002) The motor domain determines the large step of myosin-V. Nature 415: 192-195.
59. Tyska MJ and Warshaw DM (2002) The myosin power stroke. Cell Motil Cytoskeleton 51: 1-15.
60. Tyska MJ, Dupuis DE, Guilford WH, Patlak JB, Waller GS, Trybus KM, Warshaw DM and Lowey S (1999) Two heads of myosin are better than one for generating force and motion. Proc Natl Acad Sci USA 96: 4402-4407.
61. Uyeda TQ, Abramson PD and Spudich JA (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc Natl Acad Sci USA 93: 4459-4464.
62. Veigel C, Coluccio LM, Jontes JD, Sparrow JC, Milligan RA and Molloy JE (1999) The motor protein myosin-I produces its working stroke in two steps. Nature 398: 530-533.
63. Veigel C, Molloy JE, Schmitz S and Kendrick-Jones J (2003) Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers. Nat Cell Biol 5: 980-986.
64. Veigel C, Wang F, Bartoo ML, Sellers JR and Molloy JE (2002) The gated gait of the processive molecular motor, myosin V. Nat Cell Biol 4: 59-65.
65. Walker ML, Burgess SA, Sellers JR, Wang F, Hammer JA, III, Trinick J and Knight PJ (2000) Two-headed binding of a processive myosin to F-actin. Nature 405: 804-807.
66. Warshaw DM, Guilford WH, Freyzon Y, Krementsova E, Palmiter KA, Tyska MJ, Baker JE and Trybus KM (2000) The light chain binding domain of expressed smooth muscle heavy meromyosin acts as a mechanical lever. J Biol Chem 275: 37167-37172.
67. Watanabe TM, Tanaka H, Iwane AH, Maki-Yonekura S, Homma K, Inoue A, Ikebe R, Yanagida T and Ikebe M (2004) A one-headed class V myosin molecule develops multiple large (∼32 nm) steps successively. Proc Natl Acad Sci USA 101: 9630-9635.
68. Weeds AG and Lowey S (1971) Substructure of the myosin molecule. II. The light chains of myosin. J Mol Biol 61: 701-725.
69. Whittaker M, Wilson-Kubalek EM, Smith JE, Faust L, Milligan RA, Sweeney HL (1995) A 35-A movement of smooth muscle myosin on ADP release. Nature 378: 748-751.
70. Yanagida T, Kitamura K, Tanaka H, Hikikoshi Iwane A and Esaki S (2000) Single molecule analysis of the actomyosin motor. Curr Opin Cell Biol 12: 20-25.
71. Xie X, Harrison DH, Schlichting I, Sweet RM, Kalabokis VN, Szent-Gyorgyi AG and Cohen C (1994) Structure of the regulatory domain of scallop myosin at 2.8 A resolution. Nature 368: 306-312.