How myosin motors power cellular functions - An exciting journey from structure to function: Based on a lecture delivered at the 34th FEBS Congress in Prague, Czech Republic, July 2009

FEBS Journal

Volumn 279, Issue 4, 2012, Pages 551-562

  Llinas, Paola ^a   Pylypenko, Olena ^a   Isabet, Tatiana ^a   Mukherjea, Monalisa ^b   Sweeney, H Lee ^b   Houdusse, Anne M ^a  

^a INSTITUT CURIE   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

chemo mechanical transduction; dimerisation; directionality; force production; intra cellular transport; molecular motor; myosin

Indexed keywords

ACTIN; MOLECULAR MOTOR; MYOSIN; MYOSIN VI;

BINDING AFFINITY; BINDING SITE; CELL ACTIVATION; CELL FUNCTION; CONFORMATIONAL TRANSITION; DIMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

EID: 84856317221     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08449.x     Document Type: Review

References (60)

1. Kühne W, (1864) Untersuchungen über das Protoplasma und die Contractilitat. W. Engelmann, Leipzig.
2. Odronitz F, &, Kollmar M, (2007) Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol 8, R196.
3. Hartman MA, Finan D, Sivaramakrishnan S, &, Spudich JA, (2011) Principles of unconventional myosin function and targeting. Annu Rev Cell Dev Biol 27, 133-155.
4. Sweeney HL, &, Houdusse A, (2010) Myosin VI rewrites the rules for myosin motors. Cell 141, 573-582.
5. McConnell RE, &, Tyska MJ, (2010) Leveraging the membrane- cytoskeleton interface with myosin-1. Trends Cell Biol 20, 418-426.
6. Norstrom MF, Smithback PA, &, Rock RS, (2010) Unconventional processive mechanics of non-muscle myosin IIB. J Biol Chem 285, 26326-26334.
7. Woolner S, &, Bement WM, (2009) Unconventional myosins acting unconventionally. Trends Cell Biol 19, 245-252.
8. Walsh R, Rutland C, Thomas R, &, Loughna S, (2010) Cardiomyopathy: a systematic review of disease-causing mutations in myosin heavy chain 7 and their phenotypic manifestations. Cardiology 115, 49-60.
9. Ostap EM, Franzini-Armstrong C, Goldman YE, Pollard TD, Sellers JR, Sweeney HL, &, Szent-Gyorgyi AG, (2004) Fifty important papers in the history of muscle contraction and myosin motility. J Muscle Res Cell Motil 25, 483-487.
10. De La Cruz EM, &, Ostap EM, (2004) Relating biochemistry and function in the myosin superfamily. Curr Opin Cell Biol 16, 61-67. (Pubitemid 38368153)
11. Geeves MA, &, Holmes KC, (1999) Structural mechanism of muscle constraction. Annu Rev Biochem 68, 687-728.
12. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM, Hasson T, Carragher BO, Milligan RA, &, Sweeney HL, (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401, 505-508.
13. Reifenberger JG, Toprak E, Kim H, Safer D, Sweeney HL, &, Selvin PR, (2009) Myosin VI undergoes a 180 degrees power stroke implying an uncoupling of the front lever arm. Proc Natl Acad Sci USA 106, 18255-18260.
14. Huxley AF, &, Niedergerke R, (1954) Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173, 971-973.
15. Huxley H, &, Hanson J, (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173, 973-976.
16. Huxley HE, (1969) The mechanism of muscular contraction. Science 164, 1356-1365.
17. Lymn RW, &, Taylor EW, (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10, 4617-4624.
18. Bagshaw CR, &, Trentham DR, (1974) The characterization of myosin-product complexes and of product-release steps during the magnesium ion dependent adenosine triphosphatase reaction. Biochem J 141, 331-349.
19. Sleep JA, &, Hutton RL, (1980) Exchange between inorganic phosphate and adenosine 5¢-triphosphate in the medium by actomyosin subfragment 1. Biochemistry 19, 1276-1283.
20. Whittaker M, Wilson-Kubalek EM, Smith JE, Faust L, Milligan RA, &, Sweeney HL, (1995) A 35-Å movement of smooth muscle myosin on ADP release. Nature 378, 748-751.
21. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, &, Holden HM, (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50-58. (Pubitemid 23265379)
22. Dominguez R, Freyzon Y, Trybus KM, &, Cohen C, (1998) Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualization of the prepower stroke state. Cell 94, 559-571. (Pubitemid 28427575)
23. Houdusse A, Szent-Gyorgyi AG, &, Cohen C, (2000) Three conformational states of scallop myosin S1. Proc Natl Acad Sci USA 97, 11238-11243.
24. Houdusse A, Kalabokis VN, Himmel D, Szent-Györgyi AG, &, Cohen C, (1999) Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97, 459-470. (Pubitemid 29231169)
25. Coureux PD, Wells AL, Menetrey J, Yengo CM, Morris CA, Sweeney HL, &, Houdusse A, (2003) A structural state of the myosin V motor without bound nucleotide. Nature 425, 419-423. (Pubitemid 37187273)
26. Coureux PD, Sweeney HL, &, Houdusse A, (2004) Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J 23, 4527-4537. (Pubitemid 39657853)
27. Warshaw DM, (2004) Lever arms and necks: a common mechanistic theme across the myosin superfamily. J Muscle Res Cell Motil 25, 467-474.
28. Geeves MA, &, Conibear PB, (1995) The role of three-state docking of myosin S1 with actin in force generation. Biophys J 68, 194S-199S.
29. Furch M, Geeves MA, &, Manstein DJ, (1998) Modulation of actin affinity and actomyosin adenosine triphosphatase by charge changes in the myosin motor domain. Biochemistry 37, 6317-6326. (Pubitemid 28213649)
30. De La Cruz EM, Wells AL, Rosenfeld SS, Ostap EM, &, Sweeney HL, (1999) The kinetic mechanism of myosin V. Proc Natl Acad Sci USA 96, 13726-13731.
31. Joel PB, Trybus KM, &, Sweeney HL, (2001) Two conserved lysines at the 50/20-kDa junction of myosin are necessary for triggering actin activation. J Biol Chem 276, 2998-3003.
32. Dantzig JA, Goldman YE, Millar NC, Lacktis J, &, Homsher E, (1992) Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol 451, 247-278.
33. Takagi Y, Shuman H, &, Goldman YE, (2004) Coupling between phosphate release and force generation in muscle actomyosin. Philos Trans R Soc Lond B Biol Sci 359, 1913-1920. (Pubitemid 40199238)
34. Lorenz M, &, Holmes KC, (2010) The actin-myosin interface. Proc Natl Acad Sci USA 107, 12529-12534.
35. Koppole S, Smith JC, &, Fischer S, (2007) The structural coupling between ATPase activation and recovery stroke in the myosin II motor. Structure 15, 825-837. (Pubitemid 47042437)
36. Cecchini M, Houdusse A, &, Karplus M, (2008) Allosteric communication in myosin V: from small conformational changes to large directed movements. PLoS Comput Biol 4, e1000129.
37. Kühner S, &, Fischer S, (2011) Structural mechanism of the ATP-induced dissociation of rigor myosin from actin. Proc Natl Acad Sci USA 108, 7793-7798.
38. Ali MY, Homma K, Iwane AH, Adachi K, Itoh H, Kinosita K Jr, Yanagida T, &, Ikebe M, (2004) Unconstrained steps of myosin VI appear longest among known molecular motors. Biophys J 86, 3804-3810. (Pubitemid 38780257)
39. Yildiz A, Park H, Safer D, Yang Z, Chen LQ, Selvin PR, &, Sweeney HL, (2004) Myosin VI steps via a hand-over-hand mechanism with its lever arm undergoing fluctuations when attached to actin. J Biol Chem 279, 37223-37226. (Pubitemid 39195426)
40. Okten Z, Churchman LS, Rock RS, &, Spudich JA, (2004) Myosin VI walks hand-over-hand along actin. Nat Struct Mol Biol 11, 884-887. (Pubitemid 39128806)
41. Nishikawa S, Arimoto I, Ikezaki K, Sugawa M, Ueno H, Komori T, Iwane AH, &, Yanagida T, (2010) Switch between large hand-over-hand and small inchworm-like steps in myosin VI. Cell 142, 879-888.
42. Menetrey J, Bahloul A, Wells AL, Yengo CM, Morris CA, Sweeney HL, &, Houdusse A, (2005) The structure of the myosin VI motor reveals the mechanism of directionality reversal. Nature 435, 779-785. (Pubitemid 40839723)
43. Homma K, Yoshimura M, Saito J, Ikebe R, &, Ikebe M, (2001) The core of the motor domain determines the direction of myosin movement. Nature 412, 831-834. (Pubitemid 32801466)
44. Rock RS, Ramamurthy B, Dunn AR, Beccafico S, Rami BR, Morris C, Spink BJ, Franzini-Armstrong C, Spudich JA, &, Sweeney HL, (2005) A flexible domain is essential for the large step size and processivity of myosin VI. Mol Cell 17, 603-609. (Pubitemid 40269124)
45. Ménétrey J, Llinas P, Mukherjea M, Sweeney HL, &, Houdusse A, (2007) The structural basis for the large powerstroke of myosin VI. Cell 131, 300-308. (Pubitemid 47592918)
46. Ménétrey J, Llinas P, Cicolari J, Squires G, Liu X, Li A, Sweeney HL, &, Houdusse A, (2008) The post-rigor structure of myosin VI and implications for the recovery stroke. EMBO J 27, 244-252.
47. Sweeney HL, Park H, Zong AB, Yang Z, Selvin PR, &, Rosenfeld SS, (2007) How myosin VI coordinates its heads during processive movement. EMBO J 26, 2682-2692. (Pubitemid 46884286)
48. Pylypenko O, Song L, Squires G, Liu X, Zong AB, Houdusse A, &, Sweeney HL, (2011) Role of insert-1 of myosin VI in modulating nucleotide affinity. J Biol Chem. 286, 11716-11723.
49. Lister I, Schmitz S, Walker M, Trinick J, Buss F, Veigel C, &, Kendrick-Jones J, (2004) A monomeric myosin VI with a large working stroke. EMBO J 23, 1729-1738. (Pubitemid 38649636)
50. Park H, Ramamurthy B, Travaglia M, Safer D, Chen LQ, Franzini-Armstrong C, Selvin PR, &, Sweeney HL, (2006) Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering. Mol Cell 21, 331-336. (Pubitemid 43163528)
51. Yu C, Feng W, Wei Z, Miyanoiri Y, Wen W, Zhao Y, &, Zhang M, (2009) Myosin VI undergoes cargo-mediated dimerization. Cell 138, 537-548.
52. Rock RS, Rice SE, Wells AL, Purcell TJ, Spudich JA, &, Sweeney HL, (2001) Myosin VI is a processive motor with a large step size. Proc Natl Acad Sci USA 98, 13655-13659. (Pubitemid 33115953)
53. Nishikawa S, Homma K, Komori Y, Iwaki M, Wazawa T, Hikikoshi Iwane A, Saito J, Ikebe R, Katayama E, Yanagida T, et al. (2002) Class VI myosin moves processively along actin filaments backward with large steps. Biochem Biophys Res Commun 290, 311-317. (Pubitemid 34694501)
54. Spink BJ, Sivaramakrishnan S, Lipfert J, Doniach S, &, Spudich JA, (2008) Long single alpha-helical tail domains bridge the gap between structure and function of myosin VI. Nat Struct Mol Biol 15, 591-597. (Pubitemid 351799136)
55. Knight PJ, Thirumurugan K, Xu Y, Wang F, Kalverda AP, Stafford WF III, Sellers JR, &, Peckham M, (2005) The predicted coiled-coil domain of myosin 10 forms a novel elongated domain that lengthens the head. J Biol Chem 280, 34702-34708. (Pubitemid 41504602)
56. Mukherjea M, Llinas P, Kim H, Travaglia M, Safer D, Méné trey J, Franzini-Armstrong C, Selvin PR, Houdusse A, &, Sweeney HL, (2009) Myosin VI dimerization triggers an unfolding of a three-helix bundle in order to extend its reach. Mol Cell 35, 305-315.
57. Phichith D, Travaglia M, Yang Z, Liu X, Zong AB, Safer D, &, Sweeney HL, (2009) Cargo binding induces dimerization of myosin VI. Proc Natl Acad Sci USA 106, 17320-17324.
58. Kim H, Hsin J, Liu Y, Selvin PR, &, Schulten K, (2010) Formation of salt bridges mediates internal dimerization of myosin VI medial tail domain. Structure 18, 1443-1449.
59. Finan D, Hartman MA, &, Spudich JA, (2011) Proteomics approach to study the functions of Drosophila myosin VI through identification of multiple cargo-binding proteins. Proc Natl Acad Sci USA 108, 5566-5571.
60. Iwaki M, Iwane AH, Shimokawa T, Cooke R, &, Yanagida T, (2009) Brownian search-and-catch mechanism for myosin-VI steps. Nat Chem Biol 5, 403-405.