Deletion of 1-43 amino acids in cardiac myosin essential light chain blunts length dependency of ca2+ sensitivity and cross-bridge detachment kinetics

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 2, 2013, Pages

  Michael, John Jeshurun ^a   Gollapudi, Sampath K ^a   Ford, Steven J ^a   Kazmierczak, Katarzyna ^a   Szczesna Cordary, Danuta ^a   Chandra, Murali ^b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Cross bridge detachment rate; Length dependent activation of the myofilament; Maximal tension

Indexed keywords

CALCIUM ION; MUTANT PROTEIN; MYOSIN ESSENTIAL LIGHT CHAIN; MYOSIN LIGHT CHAIN; UNCLASSIFIED DRUG;

AMINO ACID DELETION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; HEART MUSCLE CONTRACTILITY; HEART MUSCLE TENSION; MOUSE; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MODIFICATION; SARCOMERE LENGTH;

AMINO ACID SEQUENCE; ANIMALS; BIOMECHANICS; CALCIUM; EXCITATION CONTRACTION COUPLING; FEMALE; GENE DELETION; HUMANS; KINETICS; MICE; MICE, TRANSGENIC; MUSCLE STRENGTH; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; MYOFIBRILS; MYOSIN LIGHT CHAINS; SARCOMERES;

EID: 84872395459     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00572.2012     Document Type: Article

References (46)

1. Adhikari BB, Regnier M, Rivera AJ, Kreutziger KL, Martyn DA. Cardiac length dependence of force and force redevelopment kinetics with altered cross-bridge cycling. Biophys J 87: 1784-1794, 2004.
2. Allen DG, Kentish JC. The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 17: 821-840, 1985.
3. Bottinelli R, Betto R, Schiaffino S, Reggiani C. Unloaded shortening velocity and myosin heavy chain and alkali light chain isoform composition in rat skeletal muscle fibres. J Physiol 478: 341-349, 1994.
4. 2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci USA 85: 3265-3269, 1988.
5. Brenner B, Eisenberg E. Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc Natl Acad Sci USA 83: 3542-3546, 1986.
6. Campbell KB, Chandra M, Kirkpatrick RD, Slinker BK, Hunter WC. Interpreting cardiac muscle force-length dynamics using a novel functional model. Am J Physiol Heart Circ Physiol 286: H1535-H1545, 2004.
7. 2+ activation of myofilaments from transgenic mouse hearts expressing R92Q mutant cardiac troponin T. Am J Physiol Heart Circ Physiol 280: H705-H713, 2001.
8. Chandra M, Tschirgi ML, Ford SJ, Slinker BK, Campbell KB. Interaction between myosin heavy chain and troponin isoforms modulate cardiac myofiber contractile dynamics. Am J Physiol Regul Integr Comp Physiol 293: R1595-R1607, 2007.
9. Chandra M, Tschirgi ML, Rajapakse I, Campbell KB. Troponin T modulates sarcomere length-dependent recruitment of cross-bridges in cardiac muscle. Biophys J 90: 2867-2876, 2006.
10. Fabiato A, Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75: 463-505, 1979.
11. Farman GP, Gore D, Allen E, Schoenfelt K, Irving TC, de Tombe PP. Myosin head orientation: a structural determinant for the Frank-Starling relationship. Am J Physiol Heart Circ Physiol 300: H2155-H2160, 2011.
12. 2+ activation of rat ventricular myocytes. Circ Res 83: 602-607, 1998.
13. Ford SJ, Chandra M, Mamidi R, Dong W, Campbell KB. Model representation of the nonlinear step response in cardiac muscle. J Gen Physiol 136: 159-177, 2010.
14. 2+ activation in cardiac muscle: some remaining questions. J Muscle Res Cell Motil 26: 199-212, 2005.
15. Fukuda N, Kajiwara H, Ishiwata S, Kurihara S. Effects of MgADP on length dependence of tension generation in skinned rat cardiac muscle. Circ Res 86: E1-E6, 2000.
16. Gordon AM, Homsher E, Regnier M. Regulation of contraction in striated muscle. Physiol Rev 80: 853-924, 2000.
17. Greaser ML, Moss RL, Reiser PJ. Variations in contractile properties of rabbit single muscle fibres in relation to troponin T isoforms and myosin light chains. J Physiol 406: 85-98, 1988.
18. Henry GD, Winstanley MA, Dalgarno DC, Scott GM, Levine BA, Trayer IP. Characterization of the actin-binding site on the alkali light chain of myosin. Biochim Biophys Acta 830: 233-243, 1985.
19. Hernandez OM, Jones M, Guzman G, Szczesna-Cordary D. Myosin essential light chain in health and disease. Am J Physiol Heart Circ Physiol 292: H1643-H1654, 2007.
20. Hill AV. The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond B Biol Sci 126: 136-195, 1938.
21. 2+ binding to cardiac troponin C. Am J Physiol Cell Physiol 253: C90-C96, 1987.
22. Huxley AF. Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7: 255-318, 1957.
23. Kazmierczak K, Xu Y, Jones M, Guzman G, Hernandez OM, Kerrick WG, Szczesna-Cordary D. The role of the N-terminus of the myosin essential light chain in cardiac muscle contraction. J Mol Biol 387: 706-725, 2009.
24. Konhilas JP, Irving TC, de Tombe PP. Frank-Starling law of the heart and the cellular mechanisms of length-dependent activation. Pflügers Arch 445: 305-310, 2002.
25. Lowey S, Waller GS, Trybus KM. Function of skeletal muscle myosin heavy and light chain isoforms by an in vitro motility assay. J Biol Chem 268: 20414-20418, 1993.
26. Lu X, Heeley DH, Smillie LB, Kawai M. The role of tropomyosin isoforms and phosphorylation in force generation in thin-filament reconstituted bovine cardiac muscle fibres. J Muscle Res Cell Motil 31: 93-109, 2010.
27. 2+ activation in cardiac muscle. Biophys J 92: 4379-4390, 2007.
28. Metzger JM. Myosin binding-induced cooperative activation of the thin filament in cardiac myocytes and skeletal muscle fibers. Biophys J 68: 1430-1442, 1995.
29. Miller MS, Palmer BM, Ruch S, Martin LA, Farman GP, Wang Y, Robbins J, Irving TC, Maughan DW. The essential light chain N-terminal extension alters force and fiber kinetics in mouse cardiac muscle. J Biol Chem 280: 34427-34434, 2005.
30. Milligan RA, Whittaker M, Safer D. Molecular structure of F-actin and location of surface binding sites. Nature 348: 217-221, 1990.
31. Miyanishi T, Ishikawa T, Hayashibara T, Maita T, Wakabayashi T. The two actin-binding regions on the myosin heads of cardiac muscle. Biochemistry 41: 5429-5438, 2002.
32. Morano I. Tuning the human heart molecular motors by myosin light chains. J Mol Med (Berl) 77: 544-555, 1999.
33. Morano I, Ritter O, Bonz A, Timek T, Vahl CF, Michel G. Myosin light chain-actin interaction regulates cardiac contractility. Circ Res 76: 720-725, 1995.
34. Muthu P, Wang L, Yuan CC, Kazmierczak K, Huang W, Hernandez OM, Kawai M, Irving TC, Szczesna-Cordary D. Structural and functional aspects of the myosin essential light chain in cardiac muscle contraction. FASEB J 25: 4394-4405 2011.
35. Rarick HM, Opgenorth TJ, von Geldern TW, Wu-Wong JR, Solaro RJ. An essential myosin light chain peptide induces supramaximal stimulation of cardiac myofibrillar ATPase activity. J Biol Chem 271: 27039-27043, 1996.
36. Rayment I, Rypniewski WR, Schmidt-Base K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261: 50-58, 1993.
37. Regnier M, Martin H, Barsotti RJ, Rivera AJ, Martyn DA, Clemmens E. Cross-bridge versus thin filament contributions to the level and rate of force development in cardiac muscle. Biophys J 87: 1815-1824, 2004.
38. Sanbe A, Gulick J, Fewell J, Robbins J. Examining the in vivo role of the amino terminus of the essential myosin light chain. J Biol Chem 276: 32682-32686, 2001.
39. Smith L, Tainter C, Regnier M, Martyn DA. Cooperative cross-bridge activation of thin filaments contributes to the Frank-Starling mechanism in cardiac muscle. Biophys J 96: 3692-3702, 2009.
40. Stepkowski D, Efimova N, Paczynska A, Moczarska A, Nieznanska H, Kakol I. The possible role of myosin A1 light chain in the weakening of actin-myosin interaction. Biochim Biophys Acta 1340: 105-114, 1997.
41. Sutoh K. Identification of myosin-binding sites on the actin sequence. Biochemistry 21: 3654-3661, 1982.
42. Sweeney HL. Function of the N terminus of the myosin essential light chain of vertebrate striated muscle. Biophys J 68: 112S-119S, 1995.
43. Timson DJ. Fine tuning the myosin motor: the role of the essential light chain in striated muscle myosin. Biochimie 85: 639-645, 2003.
44. Timson DJ, Trayer HR, Smith KJ, Trayer IP. Size and charge requirements for kinetic modulation and actin binding by alkali 1-type myosin essential light chains. J Biol Chem 274: 18271-18277, 1999.
45. Trayer IP, Trayer HR, Levine BA. Evidence that the N-terminal region of A1-light chain of myosin interacts directly with the C-terminal region of actin. A proton magnetic resonance study. Eur J Biochem 164: 259- 266, 1987.
46. 2+ binding in skinned bovine cardiac muscle. J Muscle Res Cell Motil 22: 251-257, 2001.