Temperature dependent measurements reveal similarities between muscle and non-muscle myosin motility

Journal of Muscle Research and Cell Motility

Volumn 33, Issue 6, 2012, Pages 385-394

  Yengo, Christopher M ^a   Takagi, Yasuharu ^b   Sellers, James R ^b  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Enzymatic activity; Motility; Muscle contraction; Myosin

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; MYOSIN; MYOSIN IIA;

ANIMAL; ARTICLE; CHICKEN; COMPARATIVE STUDY; KINETICS; METABOLISM; MOUSE; MOVEMENT (PHYSIOLOGY); RABBIT; TEMPERATURE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ANIMALS; CHICKENS; KINETICS; MICE; MOVEMENT; MYOSINS; NONMUSCLE MYOSIN TYPE IIA; RABBITS; SKELETAL MUSCLE MYOSINS; SMOOTH MUSCLE MYOSINS; TEMPERATURE;

EID: 84874468262     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-012-9316-7     Document Type: Article

References (67)

1. Barany M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50(6 Suppl):197-218
2. Bloemink MJ, Geeves MA (2011) Shaking the myosin family tree: biochemical kinetics defines four types of myosin motor. Semin Cell Dev Biol 22(9):961-967
3. Brenner B (2006) The stroke size of myosins: a reevaluation. J Muscle Res Cell Motil 27(2):173-187
4. Capitanio M, Canepari M, Cacciafesta P, Lombardi V, Cicchi R, Maffei M, Pavone FS, Bottinelli R (2006) Two independent mechanical events in the interaction cycle of skeletal muscle myosin with actin. Proc Natl Acad Sci USA 103(1):87-92
5. Cremo CR, Sellers JR, Facemyer KC (1995) Two heads are required for phosphorylation-dependent regulation of smooth muscle myosin. J Biol Chem 270(5):2171-2175
6. De La Cruz EM, Ostap EM (2004) Relating biochemistry and function in the myosin superfamily. Curr Opin Cell Biol 16(1):61-67
7. 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(24):13726-13731
8. De La Cruz EM, Sweeney HL, Ostap EM (2000) ADP inhibition of myosin V ATPase activity. Biophys J 79(3):1524-1529
9. Forgacs E, Cartwright S, Sakamoto T, Sellers JR, Corrie JE, Webb MR, White HD (2008) Kinetics of ADP dissociation from the trail and lead heads of actomyosin V following the power stroke. J Biol Chem 283(2):766-773
10. Furch M, Remmel B, Geeves MA, Manstein DJ (2000) Stabilization of the actomyosin complex by negative charges on myosin. Biochemistry 39(38):11602-11608
11. Goldman YE (1987) Kinetics of the actomyosin ATPase in muscle fibers. Annu Rev Physiol 49:637-654
12. Hannemann DE, Cao W, Olivares AO, Robblee JP, De La Cruz EM (2005) Magnesium, ADP, and actin binding linkage of myosin V: evidence for multiple myosin V-ADP and actomyosin V-ADP states. Biochemistry 44(24):8826-8840
13. Harris DE, Warshaw DM (1993) Smooth and skeletal muscle myosin both exhibit low duty cycles at zero load in vitro. J Biol Chem 268(20):14764-14768
14. Hooft AM, Maki EJ, Cox KK, Baker JE (2007) An accelerated state of myosin-based actin motility. Biochemistry 46(11):3513-3520. doi: 10.1021/bi0614840
15. Hu A, Wang F, Sellers JR (2002) Mutations in human nonmuscle myosin IIA found in patients with May-Hegglin anomaly and Fechtner syndrome result in impaired enzymatic function. J Biol Chem 277(48):46512-46517
16. Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255-318
17. Iorga B, Adamek N, Geeves MA (2007) The slow skeletal muscle isoform of myosin shows kinetic features common to smooth and non-muscle myosins. J Biol Chem 282(6):3559-3570
18. Jackson DR Jr, Baker JE (2009) The energetics of allosteric regulation of ADP release from myosin heads. Phys Chem Chem Phys 11(24):4808-4814
19. Jacobs DJ, Trivedi D, David C, Yengo CM (2011) Kinetics and thermodynamics of the rate-limiting conformational change in the actomyosin v mechanochemical cycle. J Mol Biol 407(5):716-730
20. 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(5):2998-3003
21. Joel PB, Sweeney HL, Trybus KM (2003) Addition of lysines to the 50/20 kDa junction of myosin strengthens weak binding to actin without affecting the maximum ATPase activity. Biochemistry 42(30):9160-9166
22. Kojima S, Konishi K, Katoh K, Fujiwara K, Martinez HM, Morales MF, Onishi H (2001) Functional roles of ionic and hydrophobic surface loops in smooth muscle myosin: their interactions with actin. Biochemistry 40(3):657-664
23. Kovacs M, Wang F, Hu A, Zhang Y, Sellers JR (2003) Functional divergence of human cytoplasmic myosin II: kinetic characterization of the non-muscle IIA isoform. J Biol Chem 278(40):38132-38140
24. Kovacs M, Toth J, Nyitray L, Sellers JR (2004) Two-headed binding of the unphosphorylated nonmuscle heavy meromyosin. ADP complex to actin. Biochemistry 43(14):4219-4226
25. Kovacs M, Thirumurugan K, Knight PJ, Sellers JR (2007) Load-dependent mechanism of nonmuscle myosin 2. Proc Natl Acad Sci USA 104(24):9994-9999
26. Kron SJ, Toyoshima YY, Uyeda TQ, Spudich JA (1991) Assays for actin sliding movement over myosin-coated surfaces. Methods Enzymol 196:399-416
27. Lauzon AM, Tyska MJ, Rovner AS, Freyzon Y, Warshaw DM, Trybus KM (1998) A 7-amino-acid insert in the heavy chain nucleotide binding loop alters the kinetics of smooth muscle myosin in the laser trap. J Muscle Res Cell Motil 19(8):825-837
28. Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10(25):4617-4624
29. Malnasi-Csizmadia A, Kovacs M (2010) Emerging complex pathways of the actomyosin powerstroke. Trends Biochem Sci 35:684-690
30. Malnasi-Csizmadia A, Pearson DS, Kovacs M, Woolley RJ, Geeves MA, Bagshaw CR (2001) Kinetic resolution of a conformational transition and the ATP hydrolysis step using relaxation methods with a Dictyostelium myosin II mutant containing a single tryptophan residue. Biochemistry 40(42):12727-12737
31. Margossian SS, Lowey S (1982) Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol 85(Pt B):55-71
32. Marston SB, Taylor EW (1980) Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles. J Mol Biol 139(4):573-600
33. Mehta A (2001) Myosin learns to walk. J Cell Sci 114(Pt 11):1981-1998
34. Mehta AD, Rock RS, Rief M, Spudich JA, Mooseker MS, Cheney RE (1999) Myosin-V is a processive actin-based motor. Nature 400(6744):590-593
35. Meijering E, Dzyubachyk O, Smal I (2012) Methods for cell and particle tracking. Methods Enzymol 504:183-200
36. Moore JR, Krementsova EB, Trybus KM, Warshaw DM (2001) Myosin V exhibits a high duty cycle and large unitary displacement. J Cell Biol 155(4):625-635
37. Nyitrai M, Geeves MA (2004) Adenosine diphosphate and strain sensitivity in myosin motors. Philos Trans R Soc Lond B Biol Sci 359(1452):1867-1877
38. Nyitrai M, Rossi R, Adamek N, Pellegrino MA, Bottinelli R, Geeves MA (2006) What limits the velocity of fast-skeletal muscle contraction in mammals? J Mol Biol 355(3):432-442
39. Oguchi Y, Mikhailenko SV, Ohki T, Olivares AO, De La Cruz EM, Ishiwata S (2008) Load-dependent ADP binding to myosins V and VI: implications for subunit coordination and function. Proc Natl Acad Sci USA 105(22):7714-7719
40. Olivares AO, De La Cruz EM (2005) Holding the reins on myosin V. Proc Natl Acad Sci USA 102(39):13719-13720
41. Onishi H, Mikhailenko SV, Morales MF (2006) Toward understanding actin activation of myosin ATPase: the role of myosin surface loops. Proc Natl Acad Sci USA 103(16):6136-6141
42. Pardee JD, Spudich JA (1982) Purification of muscle actin. Methods Enzymol 85(Pt B):164-181
43. Putkey JA, Donnelly PV, Means AR (1987) Bacterial expression vectors for calmodulin. Methods Enzymol 139:303-317
44. 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(24):13655-13659
45. Rosenfeld SS, Sweeney HL (2004) A model of myosin V processivity. J Biol Chem 279(38):40100-40111
46. Rosenfeld SS, Houdusse A, Sweeney HL (2005) Magnesium regulates ADP dissociation from myosin V. J Biol Chem 280(7):6072-6079
47. Sakamoto T, Wang F, Schmitz S, Xu Y, Xu Q, Molloy JE, Veigel C, Sellers JR (2003) Neck length and processivity of myosin V. J Biol Chem 278(31):29201-29207
48. Sakamoto T, Yildez A, Selvin PR, Sellers JR (2005) Step-size is determined by neck length in myosin V. Biochemistry 44(49):16203-16210
49. Sellers JR (1981) Phosphorylation-dependent regulation of Limulus myosin. J Biol Chem 256(17):9274-9278
50. Sellers JR (1999) Myosins, 2nd edn. Oxford University Press, Oxford, UK
51. Sellers JR (2000) Myosins: a diverse superfamily. Biochim Biophys Acta 1496(1):3-22
52. Sellers JR, Veigel C (2010) Direct observation of the myosin-Va power stroke and its reversal. Nat Struct Mol Biol 17(5):590-595
53. Siemankowski RF, Wiseman MO, White HD (1985) ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unloaded shortening velocity in vertebrate muscle. Proc Natl Acad Sci USA 82(3):658-662
54. Sun M, Oakes JL, Ananthanarayanan SK, Hawley KH, Tsien RY, Adams SR, Yengo CM (2006) Dynamics of the upper 50-kDa domain of myosin V examined with fluorescence resonance energy transfer. J Biol Chem 281(9):5711-5717
55. Sun M, Rose MB, Ananthanarayanan SK, Jacobs DJ, Yengo CM (2008) Characterization of the pre-force-generation state in the actomyosin cross-bridge cycle. Proc Natl Acad Sci USA 105(25):8631-8636
56. Sweeney HL, Houdusse A (2010) Structural and functional insights into the myosin motor mechanism. Annu Rev Biophys 39:539-557
57. Sweeney HL, Rosenfeld SS, Brown F, Faust L, Smith J, Xing J, Stein LA, Sellers JR (1998) Kinetic tuning of myosin via a flexible loop adjacent to the nucleotide binding pocket. J Biol Chem 273(11):6262-6270
58. Szent-Gyorgyi AG, Kalabokis VN, Perreault-Micale CL (1999) Regulation by molluscan myosins. Mol Cell Biochem 190(1-2):55-62
59. Tyska MJ, Mooseker MS (2003) Myosin-V motility: these levers were made for walking. Trends Cell Biol 13(9):447-451
60. Tyska MJ, Warshaw DM (2002) The myosin power stroke. Cell Motil Cytoskeleton 51(1):1-15
61. Urbanke C, Wray J (2001) A fluorescence temperature-jump study of conformational transitions in myosin subfragment 1. Biochem J 358(Pt 1):165-173
62. Uyeda TQ, Kron SJ, Spudich JA (1990) Myosin step size. Estimation from slow sliding movement of actin over low densities of heavy meromyosin. J Mol Biol 214(3):699-710
63. Varkuti BH, Yang Z, Kintses B, Erdelyi P, Bardos-Nagy I, Kovacs AL, Hari P, Kellermayer M, Vellai T, Malnasi-Csizmadia A (2012) A novel actin binding site of myosin required for effective muscle contraction. Nat Struct Mol Biol 19(3):299-306
64. Veigel C, Wang F, Bartoo ML, Sellers JR, Molloy JE (2002) The gated gait of the processive molecular motor, myosin V. Nat Cell Biol 4(1):59-65
65. Weber A, Winicur S (1961) The role of calcium in the superprecipitation of actomyosin. J Biol Chem 236:3198-3202
66. Weiss S, Chizhov I, Geeves MA (2000) A flash photolysis fluorescence/light scattering apparatus for use with sub microgram quantities of muscle proteins. J Muscle Res Cell Motil 21(5):423-432
67. Weiss S, Rossi R, Pellegrino MA, Bottinelli R, Geeves MA (2001) Differing ADP release rates from myosin heavy chain isoforms define the shortening velocity of skeletal muscle fibers. J Biol Chem 276(49):45902-45908