The myosin mesa and a possible unifying hypothesis for the molecular basis of human hypertrophic cardiomyopathy

Biochemical Society Transactions

Volumn 43, Issue , 2015, Pages 64-72

  Spudich, James A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hypertrophic cardiomyopathy; Myosin

Indexed keywords

MOLECULAR MOTOR; MYOSIN; MYOSIN BINDING PROTEIN C; MYOSIN HEAVY CHAIN ALPHA; MYOSIN HEAVY CHAIN BETA; MYOSIN II; TROPONIN; CARRIER PROTEIN; MYOSIN-BINDING PROTEIN C; PROTEIN BINDING;

ACTIN FILAMENT; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; GENE MUTATION; HEART CONTRACTION; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; PRIORITY JOURNAL; PROTEIN DOMAIN; SARCOMERE; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CARDIOMYOPATHY, HYPERTROPHIC; CARRIER PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MYOSINS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84921826432     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140324     Document Type: Article

References (45)

1. Spudich, J.A. (1994) How molecular motors work. Nature 372, 515-518 CrossRef PubMed
2. Spudich, J.A. (2001) The myosin swinging cross-bridge model. Nat. Rev. Mol. Cell Biol. 2, 387-392 CrossRef PubMed
3. Spudich, J.A. (2011) Molecular motors: forty years of interdisciplinary research. Mol. Biol. Cell 22, 3936-3939 CrossRef PubMed
4. Spudich, J.A. (2012) One path to understanding energy transduction in biological systems. Nat. Med. 18, 1478-1482 CrossRef PubMed
5. Brown, S., Levinson, W. and Spudich, J.A. (1976) Cytoskeletal elements of chick embryo fibroblasts revealed by detergent extraction. J. Supramol. Struct. 5, 119-130 CrossRef PubMed
6. De Lozanne, A. and Spudich, J.A. (1987) Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236, 1086-1091 CrossRef PubMed
7. Pollard, T.D. (2002) Cellular motility powered by actin filament assembly and disassembly. Harvey Lect. 98, 1-17 PubMed
8. Pollard, T.D. and Cooper, J.A. (2009) Actin, a central player in cell shape and movement. Science 326, 1208-1212 CrossRef PubMed
9. Moores, S.L., Sabry, J.H. and Spudich, J.A. (1996) Myosin dynamics in live Dictyostelium cells. Proc. Natl. Acad. Sci. U.S.A. 93, 443-446 CrossRef PubMed
10. Zang, J.H., Cavet, G., Sabry, J.H., Wagner, P., Moores, S.L. and Spudich, J.A. (1997) On the role of myosin-II in cytokinesis: division of Dictyostelium cells under adhesive and nonadhesive conditions. Mol. Biol. Cell 8, 2617-2629 CrossRef PubMed
11. Ruppel, K.M. and Spudich, J.A. (1996) Structure-function analysis of the motor domain of myosin. Annu. Rev. Cell Dev. Biol. 12, 543-573 CrossRef PubMed
12. Spudich, J.A., Kron, S.J. and Sheetz, M.P. (1985) Movement of myosin-coated beads on oriented filaments reconstituted from purified actin. Nature 315, 584-586 CrossRef PubMed
13. Kron, S.J. and Spudich, J.A. (1986) Fluorescent actin filaments move on myosin fixed to a glass surface. Proc. Natl. Acad. Sci. U.S.A. 83, 6272-6276 CrossRef PubMed
14. Toyoshima, Y.Y., Kron, S.J., McNally, E.M., Niebling, K.R., Toyoshima, C. and Spudich, J.A. (1987) Myosin subfragment-1 is sufficient to move actin filaments in vitro. Nature 328, 536-539 CrossRef PubMed
15. Uyeda, T.Q., Abramson, P.D. and Spudich, J.A. (1996) The neck region of the myosin motor domain acts as a lever arm to generate movement. Proc. Natl. Acad. Sci. 93, 4459-4464 CrossRef
16. Shih, W.M., Gryczynski, Z., Lakowicz, J.R. and Spudich, J.A. (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 CrossRef PubMed
17. Finer, J.T., Simmons, R.M. and Spudich, J.A. (1994) Single myosin molecule mechanics: piconewton forces and nanometre steps. Nature 368, 113-119 CrossRef PubMed
18. Geisterfer-Lowrance, A.A., Kass, S., Tanigawa, G., Vosberg, H.P., McKenna, W., Seidman, C.E. and Seidman, J.G. (1990) A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation. Cell 62, 999-1006 CrossRef PubMed
19. Seidman, C.E. and Seidman, J.G. (2000) Hypertrophic cardiomyopathy. In The Metabolic and Molecular Bases of Inherited Disease (Scriver, C.R., Beaudet, A.L., Valle, D., Sly, W.S., Childs, K.W. and Vogelstein, B., eds), pp. 5532-5452, McGraw-Hill
20. Harvey, P.A. and Leinwand, L.A. (2011) Cellular mechanisms of cardiomyopathy. J. Cell Biol. 194, 355-365 CrossRef PubMed
21. Maron, B.J. (2010) Hypertrophic cardiomyopathy. In Braunwald's Heart Disease, pp. 1582-1594, Elsevier Inc.
22. Maron, B.J., Gardin, J.M., Flack, J.M., Gidding, S.S., Kurosaki, T.T. and Bild, D.E. (1995) Prevalence of hypertrophic cardiomyopathy in a general population of young adults: echocardiographic analysis of 4111 subjects in the CARDIA study. Circulation 92, 785-789 CrossRef PubMed
23. Buvoli, M., Hamady, M., Leinwand, L.A. and Knight, R. (2008) Bioinformatics assessment of β-myosin mutations reveals myosin's high sensitivity to mutations. Trends Cardiovasc. Med. 18, 141-149 CrossRef PubMed
24. Seidman, C.E. and Seidman, J.G. (2011) Identifying sarcomere gene mutations in hypertrophic cardiomyopathy: a personal history. Circ. Res. 108, 743-750
25. Walsh, R., Rutland, C., Thomas, R. and Loughna, S. (2010) Cardiomyopathy: a systematic review of disease-causing mutations in myosin heavy chain 7 and their phenotypic manifestations. Cardiology 115, 49-60 CrossRef PubMed
26. Kensler, R.W., Shaffer, J.F. and Harris, S.P. (2011) Binding of the N-terminal fragment C0-C2 of cardiac MyBP-C to cardiac F-actin. J. Struct. Biol. 174, 44-51 CrossRef PubMed
27. van Dijk, S.J., Bezold, K.L. and Harris, S.P. (2014) Earning stripes: myosin binding protein-C interactions with actin. Pflugers Archiv. 466, 445-450 CrossRef
28. Chow, M.L., Shaffer, J.F., Harris, S.P. and Dawson, J.F. (2014) Altered interactions between cardiac myosin binding protein-C and alpha-cardiac actin variants associated with cardiomyopathies. Arch. Biochem. Biophys. 550-551, 28-32 CrossRef
29. Harris, S.P., Rostkova, E., Gautel, M. and Moss, R.L. (2004) Binding of myosin binding protein-C to myosin subfragment S2 affects contractility independent of a tether mechanism. Circ. Res. 95, 930-936 CrossRef PubMed
30. Kampourakis, T., Yan, Z., Gautel, M., Sun, Y.B. and Irving, M. (2014) Myosin binding protein-C activates thin filaments and inhibits thick filaments in heart muscle cells. Proc. Natl. Acad. Sci. U.S.A. 111, 18763-18768 CrossRef PubMed
31. Pfuhl, M. and Gautel, M. (2012) Structure, interactions and function of the N-terminus of cardiac myosin binding protein C (MyBP-C): who does what, with what, and to whom? J. Muscle Res. Cell Motil. 33, 83-94 CrossRef PubMed
32. Ratti, J., Rostkova, E., Gautel, M. and Pfuhl, M. (2011) Structure and interactions of myosin-binding protein C domain C0: cardiac-specific regulation of myosin at its neck? J. Biol. Chem. 286, 12650-12658
33. Rayment, I., Rypniewski, W.R., Schmidt-Base, K., Smith, R., Tomchick, D.R., Benning, M.M., Winkelmann, D.A., Wesenberg, G. and Holden, H.M. (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261, 50-58 CrossRef PubMed
34. Dominguez, R., Freyzon, Y., Trybus, K.M. 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 CrossRef PubMed
35. Houdusse, A., Kalabokis, V.N., Himmel, D., Szent-Gyorgyi, A.G. and Cohen, C. (1999) Atomic structure of scallop myosin subfragment S1 complexed with MgADP: a novel conformation of the myosin head. Cell 97, 459-470 CrossRef PubMed
36. Houdusse, A., Szent-Gyorgyi, A.G. and Cohen, C. (2000) Three conformational states of scallop myosin S1. Proc. Natl. Acad. Sci. U.S.A. 97, 11238-11243 CrossRef PubMed
37. Coureux, P.D., Sweeney, H.L. and Houdusse, A. (2004) Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J. 23, 4527-4537 CrossRef PubMed
38. Holmes, K.C. (2005) The molecular basis of cross-bridge function. Adv. Exp. Med. Biol. 565, 13-22, discussion 23, 359-369 CrossRef PubMed
39. Geeves, M.A. and Holmes, K.C. (2005) The molecular mechanism of muscle contraction. Adv. Protein Chem. 71, 161-193 CrossRef PubMed
40. Sweeney, H.L. and Houdusse, A. (2010) Structural and functional insights into the myosin motor mechanism. Annu. Rev. Biophys. 39, 539-557 CrossRef PubMed
41. Pan, S., Caleshu, C.A., Dunn, K.E., Foti, M.J., Moran, M.K., Soyinka, O. and Ashley, E.A. (2012) Cardiac structural and sarcomere genes associated with cardiomyopathy exhibit marked intolerance of genetic variation. Circ. Cardiovasc. Genet. 5, 602-610 CrossRef PubMed
42. Spudich, J.A. (2014) Hypertrophic and dilated cardiomyopathy: four decades of basic research on muscle lead to potential therapeutic approaches to these devastating genetic diseases. Biophys. J. 106, 1236-1249 CrossRef PubMed
43. Moss, R.L., Fitzsimons, D.P. and Ralphe, J.C. (2015) Cardiac MyBP-C Regulates the Rate and Force of Contraction in Mammalian Myocardium. Circ. Res. 116, 183-192 CrossRef PubMed
44. Malik, F.I., Hartman, J.J., Elias, K.A., Morgan, B.P., Rodriguez, H., Brejc, K., Anderson, R.L., Sueoka, S.H., Lee, K.H., Finer, J.T., Sakowicz, R., Baliga, R., Cox, D.R., Garard, M., Godinez, G., Kawas, R., Kraynack, E., Lenzi, D., Lu, P.P., Muci, A., Niu, C., Qian, X., Pierce, D.W., Pokrovskii, M., Suehiro, I., Sylvester, S., Tochimoto, T., Valdez, C., Wang, W., Katori, T., Kass, D.A., Shen, Y.T., Vatner, S.F. and Morgans, D.J. (2011) Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science 331, 1439-1443 CrossRef PubMed
45. Pugh, T.J., Kelly, M.A., Gowrisankar, S., Hynes, E., Seidman, M.A., Baxter, S.M., Bowser, M., Harrison, B., Aaron, D., Mahanta, L.M., Lakdawala, N.K., McDermott, G., White, E.T., Rehm, H.L., Lebo, M. and Funke, B.H. (2014) The landscape of genetic variation in dilated cardiomyopathy as surveyed by clinical DNA sequencing. Genet. Med. 16, 601-608 CrossRef PubMed