Sarcomeres and the Biophysics of Heart Failure

  • Jillian N. Simon
  • Jil C. Tardiff
  • Beata M. Wolska
Chapter
Part of the Biological and Medical Physics, Biomedical Engineering book series (BIOMEDICAL)

Abstract

Changes in the function of the sarcomere play a significant role in the development of cardiac dysfunction underlying heart failure. These changes in sarcomeric properties are the result of either alterations in isoform expression, post-translational modification of the sarcomeric proteins, or gene mutations linked to hypertrophic or dilated cardiomyopathy. These alterations act to modulate the contractile state of the heart via direct effects on the biophysical properties of the cardiac sarcomere. Coupling a deeper understanding of the primary biophysical causes of changes in contractile function to a more complete understanding of the resultant pathogenic ventricular remodeling that occurs over time will allow for both significant advances in disease management and new points of therapeutic intervention.

Keywords

Hydrolysis Depression Acidity Serine Carbonylation 

References

  1. 1.
    Alpert, N. R., & Gordon, M. S. (1962). Myofibrillar adenosine triphosphatase activity in congestive heart failure. American Journal of Physiology, 202, 940–946.Google Scholar
  2. 2.
    Anderson, P. A., Malouf, N. N., Oakeley, A. E., Pagani, E. D., & Allen, P. D. (1991). Troponin T isoform expression in humans. A comparison among normal and failing adult heart, fetal heart, and adult and fetal skeletal muscle. Circulation Research, 69, 1226–1233.Google Scholar
  3. 3.
    Avner, B. S., Shioura, K. M., Scruggs, S. B., Grachoff, M., Geenen, D. L., Helseth, D. L., Jr., et al. (2012). Myocardial infarction in mice alters sarcomeric function via post-translational protein modification. Molecular and Cellular Biochemistry, 363, 203–215.Google Scholar
  4. 4.
    Barton, P. J., Felkin, L. E., Koban, M. U., Cullen, M. E., Brand, N. J., & Dhoot, G. K. (2004). The slow skeletal muscle troponin T gene is expressed in developing and diseased human heart. Molecular and Cellular Biochemistry, 263, 91–97.Google Scholar
  5. 5.
    Belin, R. J., Sumandea, M. P., Allen, E. J., Schoenfelt, K., Wang, H., Solaro, R. J., et al. (2007). Augmented protein kinase C-alpha-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circulation Research, 101, 195–204.Google Scholar
  6. 6.
    Boheler, K. R., Carrier, L., de la Bastie, D., Allen, P. D., Komajda, M., Mercadier, J. J., et al. (1991). Skeletal actin mRNA increases in the human heart during ontogenic development and is the major isoform of control and failing adult hearts. The Journal of Clinical Investigation, 88, 323–330.Google Scholar
  7. 7.
    Borbely, A., Falcao-Pires, I., van Heerebeek, L., Hamdani, N., Edes, I., Gavina, C., et al. (2009). Hypophosphorylation of the Stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circulation Research, 104, 780–786.Google Scholar
  8. 8.
    Bouvagnet, P., Mairhofer, H., Leger, J. O., Puech, P., & Leger, J. J. (1989). Distribution pattern of alpha and beta myosin in normal and diseased human ventricular myocardium. Basic Research in Cardiology, 84, 91–102.Google Scholar
  9. 9.
    Bowling, N., Walsh, R. A., Song, G., Estridge, T., Sandusky, G. E., Fouts, R. L., et al. (1999). Increased protein kinase C activity and expression of Ca2+-sensitive isoforms in the failing human heart. Circulation, 99, 384–391.Google Scholar
  10. 10.
    Bristow, M. R., Ginsburg, R., Minobe, W., Cubicciotti, R. S., Sageman, W. S., Lurie, K., et al. (1982). Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. The New England Journal of Medicine, 307, 205–211.Google Scholar
  11. 11.
    Bristow, M. R., Ginsburg, R., Umans, V., Fowler, M., Minobe, W., Rasmussen, R., et al. (1986). Beta 1- and beta 2-adrenergic-receptor subpopulations in nonfailing and failing human ventricular myocardium: Coupling of both receptor subtypes to muscle contraction and selective beta 1-receptor down-regulation in heart failure. Circulation Research, 59, 297–309.Google Scholar
  12. 12.
    Brodde, O. E., Schuler, S., Kretsch, R., Brinkmann, M., Borst, H. G., Hetzer, R., et al. (1986). Regional distribution of beta-adrenoceptors in the human heart: Coexistence of functional beta 1- and beta 2-adrenoceptors in both atria and ventricles in severe congestive cardiomyopathy. Journal of Cardiovascular Pharmacology, 8, 1235–1242.Google Scholar
  13. 13.
    Buck, S. H., Konyn, P. J., Palermo, J., Robbins, J., & Moss, R. L. (1999). Altered kinetics of contraction of mouse atrial myocytes expressing ventricular myosin regulatory light chain. American Journal of Physiology, 276, H1167–H1171.Google Scholar
  14. 14.
    Burkart, E. M., Sumandea, M. P., Kobayashi, T., Nili, M., Martin, A. F., Homsher, E., et al. (2003). Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. Journal of Biological Chemistry, 278, 11265–11272.Google Scholar
  15. 15.
    Canton, M., Menazza, S., Sheeran, F. L., Polverino de Laureto, P., Di Lisa, F., & Pepe, S. (2011). Oxidation of myofibrillar proteins in human heart failure. Journal of the American College of Cardiology, 57, 300–309.Google Scholar
  16. 16.
    Canton, M., Neverova, I., Menabo, R., Van Eyk, J., & Di Lisa, F. (2004). Evidence of myofibrillar protein oxidation induced by postischemic reperfusion in isolated rat hearts. American Journal of Physiology. Heart and Circulatory Physiology, 286, H870–H877.Google Scholar
  17. 17.
    Canton, M., Skyschally, A., Menabo, R., Boengler, K., Gres, P., Schulz, R., et al. (2006). Oxidative modification of tropomyosin and myocardial dysfunction following coronary microembolization. European Heart Journal, 27, 875–881.Google Scholar
  18. 18.
    Colantonio, D. A., Van Eyk, J. E., & Przyklenk, K. (2004). Stunned peri-infarct canine myocardium is characterized by degradation of troponin T, not troponin I. Cardiovascular Research, 63, 217–225.Google Scholar
  19. 19.
    Copeland, O., Nowak, K. J., Laing, N. G., Ravenscroft, G., Messer, A. E., Bayliss, C. R., et al. (2010). Investigation of changes in skeletal muscle alpha-actin expression in normal and pathological human and mouse hearts. Journal of Muscle Research and Cell Motility, 31, 207–214.Google Scholar
  20. 20.
    Copeland, O., Sadayappan, S., Messer, A. E., Steinen, G. J., van der Velden, J., & Marston, S. B. (2010). Analysis of cardiac myosin binding protein-C phosphorylation in human heart muscle. Journal of Molecular and Cellular Cardiology, 49, 1003–1011.Google Scholar
  21. 21.
    Craig, R., & Lehman, W. (2001). Crossbridge and tropomyosin positions observed in native, interacting thick and thin filaments. Journal of Molecular Biology, 311, 1027–1036.Google Scholar
  22. 22.
    Crosbie, R. H., Miller, C., Cheung, P., Goodnight, T., Muhlrad, A., & Reisler, E. (1994). Structural connectivity in actin: Effect of C-terminal modifications on the properties of actin. Biophysical Journal, 67, 1957–1964.ADSGoogle Scholar
  23. 23.
    Decker, R. S., Decker, M. L., Kulikovskaya, I., Nakamura, S., Lee, D. C., Harris, K., et al. (2005). Myosin-binding protein C phosphorylation, myofibril structure, and contractile function during low-flow ischemia. Circulation, 111, 906–912.Google Scholar
  24. 24.
    Denz, C. R., Narshi, A., Zajdel, R. W., & Dube, D. K. (2004). Expression of a novel cardiac-specific tropomyosin isoform in humans. Biochemical and Biophysical Research Communications, 320, 1291–1297.Google Scholar
  25. 25.
    Fitzsimons, D. P., Patel, J. R., & Moss, R. L. (1998). Role of myosin heavy chain composition in kinetics of force development and relaxation in rat myocardium. The Journal of Physiology, 513(Pt 1), 171–183.Google Scholar
  26. 26.
    Frey, N., Luedde, M., & Katus, H. A. (2012). Mechanisms of disease: Hypertrophic cardiomyopathy. Nature Reviews Cardiology, 9, 91–100.Google Scholar
  27. 27.
    Gomes, A. V., Guzman, G., Zhao, J., & Potter, J. D. (2002). Cardiac troponin T isoforms affect the Ca2+ sensitivity and inhibition of force development. Insights into the role of troponin T isoforms in the heart. Journal of Biological Chemistry, 277, 35341–35349.Google Scholar
  28. 28.
    Gomes, A. V., Venkatraman, G., Davis, J. P., Tikunova, S. B., Engel, P., Solaro, R. J., et al. (2004). Cardiac troponin T isoforms affect the Ca2+ sensitivity of force development in the presence of slow skeletal troponin I—Insights into the role of troponin T isoforms in the fetal heart. Journal of Biological Chemistry, 279, 49579–49587.Google Scholar
  29. 29.
    Granzier, H., & Labeit, S. (2002). Cardiac titin: An adjustable multi-functional spring. The Journal of Physiology, 541, 335–342.Google Scholar
  30. 30.
    Granzier, H. L., & Labeit, S. (2004). The giant protein titin: A major player in myocardial mechanics, signaling, and disease. Circulation Research, 94, 284–295.Google Scholar
  31. 31.
    Gregorio, C. C., Granzier, H., Sorimachi, H., & Labeit, S. (1999). Muscle assembly: A titanic achievement? Current Opinion in Cell Biology, 11, 18–25.Google Scholar
  32. 32.
    Grutzner, A., Garcia-Manyes, S., Kotter, S., Badilla, C. L., Fernandez, J. M., & Linke, W. A. (2009). Modulation of titin-based stiffness by disulfide bonding in the cardiac titin N2-B unique sequence. Biophysical Journal, 97, 825–834.ADSGoogle Scholar
  33. 33.
    Hajjar, R. J., & Gwathmey, J. K. (1992). Cross-bridge dynamics in human ventricular myocardium. Regulation of contractility in the failing heart. Circulation, 86, 1819–1826.Google Scholar
  34. 34.
    Harding, S. E., Jones, S. M., Vescovo, G., Del Monte, F., & Poole-Wilson, P. A. (1992). Reduced contractile responses to forskolin and a cyclic AMP analogue in myocytes from failing human ventricle. European Journal of Pharmacology, 223, 39–48.Google Scholar
  35. 35.
    Harris, D. E., Work, S. S., Wright, R. K., Alpert, N. R., & Warshaw, D. M. (1994). Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. Journal of Muscle Research and Cell Motility, 15, 11–19.Google Scholar
  36. 36.
    Harris, S. P., Lyons, R. G., & Bezold, K. L. (2011). In the thick of it: HCM-causing mutations in myosin binding proteins of the thick filament. Circulation Research, 108, 751–764.Google Scholar
  37. 37.
    Head, J. G., Ritchie, M. D., & Geeves, M. A. (1995). Characterization of the equilibrium between blocked and closed states of muscle thin filaments. European Journal of Biochemistry, 227, 694–699.Google Scholar
  38. 38.
    Hernandez, O. M., Jones, M., Guzman, G., & Szczesna-Cordary, D. (2007). Myosin essential light chain in health and disease. American Journal of Physiology. Heart and Circulatory Physiology, 292, H1643–H1654.Google Scholar
  39. 39.
    Herron, T. J., Korte, F. S., & McDonald, K. S. (2001). Loaded shortening and power output in cardiac myocytes are dependent on myosin heavy chain isoform expression. American Journal of Physiology. Heart and Circulatory Physiology, 281, H1217–H1222.Google Scholar
  40. 40.
    Herron, T. J., & McDonald, K. S. (2002). Small amounts of alpha-myosin heavy chain isoform expression significantly increase power output of rat cardiac myocyte fragments. Circulation Research, 90, 1150–1152.Google Scholar
  41. 41.
    Heusch, P., Canton, M., Aker, S., van de Sand, A., Konietzka, I., Rassaf, T., et al. (2010). The contribution of reactive oxygen species and p38 mitogen-activated protein kinase to myofilament oxidation and progression of heart failure in rabbits. British Journal of Pharmacology, 160, 1408–1416.Google Scholar
  42. 42.
    Hill, M. F., & Singal, P. K. (1996). Antioxidant and oxidative stress changes during heart failure subsequent to myocardial infarction in rats. The American Journal of Pathology, 148, 291–300.Google Scholar
  43. 43.
    Hofmann, P. A., Hartzell, H. C., & Moss, R. L. (1991). Alterations in Ca2+ sensitive tension due to partial extraction of C-protein from rat skinned cardiac myocytes and rabbit skeletal muscle fibers. The Journal of General Physiology, 97, 1141–1163.Google Scholar
  44. 44.
    Huxley, H. E. (1990). Sliding filaments and molecular motile systems. Journal of Biological Chemistry, 265, 8347–8350.Google Scholar
  45. 45.
    Jacques, A. M., Copeland, O., Messer, A. E., Gallon, C. E., King, K., McKenna, W. J., et al. (2008). Myosin binding protein C phosphorylation in normal, hypertrophic and failing human heart muscle. Journal of Molecular and Cellular Cardiology, 45, 209–216.Google Scholar
  46. 46.
    Katz, A. M. (2011). Physiology of the heart. Philadelphia, PA: Wolters Kluwer Health/Lippincott Williams & Wilkins Health. p. xv, 576p.Google Scholar
  47. 47.
    Knoll, R. (2012). Myosin binding protein C: Implications for signal-transduction. Journal of Muscle Research and Cell Motility, 33, 31–42.Google Scholar
  48. 48.
    Kooij, V., Boontje, N., Zaremba, R., Jaquet, K., dos Remedios, C., Stienen, G. J., et al. (2010). Protein kinase C alpha and epsilon phosphorylation of troponin and myosin binding protein C reduce Ca2+ sensitivity in human myocardium. Basic Research in Cardiology, 105, 289–300.Google Scholar
  49. 49.
    Korte, F. S., Herron, T. J., Rovetto, M. J., & McDonald, K. S. (2005). Power output is linearly related to MyHC content in rat skinned myocytes and isolated working hearts. American Journal of Physiology. Heart and Circulatory Physiology, 289, H801–H812.Google Scholar
  50. 50.
    Korte, F. S., McDonald, K. S., Harris, S. P., & Moss, R. L. (2003). Loaded shortening, power output, and rate of force redevelopment are increased with knockout of cardiac myosin binding protein-C. Circulation Research, 93, 752–758.Google Scholar
  51. 51.
    Kruger, M., Kotter, S., Grutzner, A., Lang, P., Andresen, C., Redfield, M. M., et al. (2009). Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circulation Research, 104, 87–94.Google Scholar
  52. 52.
    Lehman, W., Rosol, M., Tobacman, L. S., & Craig, R. (2001). Troponin organization on relaxed and activated thin filaments revealed by electron microscopy and three-dimensional reconstruction. Journal of Molecular Biology, 307, 739–744.Google Scholar
  53. 53.
    Levine, R. J., Kensler, R. W., Yang, Z., Stull, J. T., & Sweeney, H. L. (1996). Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments. Biophysical Journal, 71, 898–907.ADSGoogle Scholar
  54. 54.
    Li, Y., Wu, G., Tang, Q., Huang, C., Jiang, H., Shi, L., et al. (2011). Slow cardiac myosin regulatory light chain 2 (MYL2) was down-expressed in chronic heart failure patients. Clinical Cardiology, 34, 30–34.Google Scholar
  55. 55.
    Litten, R. Z., III, Martin, B. J., Low, R. B., & Alpert, N. R. (1982). Altered myosin isozyme patterns from pressure-overloaded and thyrotoxic hypertrophied rabbit hearts. Circulation Research, 50, 856–864.Google Scholar
  56. 56.
    Manning, E. P., Tardiff, J. C., & Schwartz, S. D. (2011). A model of calcium activation of the cardiac thin filament. Biochemistry, 50, 7405–7413.Google Scholar
  57. 57.
    Margossian, S. S., White, H. D., Caulfield, J. B., Norton, P., Taylor, S., & Slayter, H. S. (1992). Light chain 2 profile and activity of human ventricular myosin during dilated cardiomyopathy. Identification of a causal agent for impaired myocardial function. Circulation, 85, 1720–1733.Google Scholar
  58. 58.
    Martin, A. F., Ball, K., Gao, L. Z., Kumar, P., & Solaro, R. J. (1991). Identification and functional significance of troponin I isoforms in neonatal rat heart myofibrils. Circulation Research, 69, 1244–1252.Google Scholar
  59. 59.
    Martos, R., Baugh, J., Ledwidge, M., O’Loughlin, C., Conlon, C., Patle, A., et al. (2007). Diastolic heart failure: Evidence of increased myocardial collagen turnover linked to diastolic dysfunction. Circulation, 115, 888–895.Google Scholar
  60. 60.
    Maughan, D. W. (2005). Kinetics and energetics of the crossbridge cycle. Heart Failure Reviews, 10, 175–185.Google Scholar
  61. 61.
    Maytum, R., Lehrer, S. S., & Geeves, M. A. (1999). Cooperativity and switching within the three-state model of muscle regulation. Biochemistry, 38, 1102–1110.Google Scholar
  62. 62.
    McClellan, G., Kulikovskaya, I., Flavigny, J., Carrier, L., & Winegrad, S. (2004). Effect of cardiac myosin-binding protein C on stability of the thick filament. Journal of Molecular and Cellular Cardiology, 37, 823–835.Google Scholar
  63. 63.
    McClellan, G., Weisberg, A., & Winegrad, S. (1994). cAMP can raise or lower cardiac actomyosin ATPase activity depending on alpha-adrenergic activity. American Journal of Physiology, 267, H431–H442.Google Scholar
  64. 64.
    McDonough, J. L., Arrell, D. K., & Van Eyk, J. E. (1999). Troponin I degradation and covalent complex formation accompanies myocardial ischemia/reperfusion injury. Circulation Research, 84, 9–20.Google Scholar
  65. 65.
    McKillop, D. F., & Geeves, M. A. (1991). Regulation of the acto.myosin subfragment 1 interaction by troponin/tropomyosin. Evidence for control of a specific isomerization between two acto.myosin subfragment 1 states. Biochemical Journal, 279(Pt 3), 711–718.Google Scholar
  66. 66.
    McKillop, D. F., & Geeves, M. A. (1993). Regulation of the interaction between actin and myosin subfragment 1: Evidence for three states of the thin filament. Biophysical Journal, 65, 693–701.ADSGoogle Scholar
  67. 67.
    McNally, E. M., Kraft, R., Bravo-Zehnder, M., Taylor, D. A., & Leinwand, L. A. (1989). Full-length rat alpha and beta cardiac myosin heavy chain sequences. Comparisons suggest a molecular basis for functional differences. Journal of Molecular Biology, 210, 665–671.Google Scholar
  68. 68.
    Mercadier, J. J., Bouveret, P., Gorza, L., Schiaffino, S., Clark, W. A., Zak, R., et al. (1983). Myosin isoenzymes in normal and hypertrophied human ventricular myocardium. Circulation Research, 53, 52–62.Google Scholar
  69. 69.
    Mesnard-Rouiller, L., Mercadier, J. J., Butler-Browne, G., Heimburger, M., Logeart, D., Allen, P. D., et al. (1997). Troponin T mRNA and protein isoforms in the human left ventricle: Pattern of expression in failing and control hearts. Journal of Molecular and Cellular Cardiology, 29, 3043–3055.Google Scholar
  70. 70.
    Miyata, S., Minobe, W., Bristow, M. R., & Leinwand, L. A. (2000). Myosin heavy chain isoform expression in the failing and nonfailing human heart. Circulation Research, 86, 386–390.Google Scholar
  71. 71.
    Morano, I. (1992). Effects of different expression and posttranslational modifications of myosin light chains on contractility of skinned human cardiac fibers. Basic Research in Cardiology, 87(Suppl. 1), 129–141.Google Scholar
  72. 72.
    Morano, I. (1999). Tuning the human heart molecular motors by myosin light chains. Journal of Molecular Medicine, 77, 544–555.Google Scholar
  73. 73.
    Morano, I., & Haase, H. (1997). Different actin affinities of human cardiac essential myosin light chain isoforms. FEBS Letters, 408, 71–74.Google Scholar
  74. 74.
    Morano, I., Hadicke, K., Grom, S., Koch, A., Schwinger, R. H., Bohm, M., et al. (1994). Titin, myosin light chains and C-protein in the developing and failing human heart. Journal of Molecular and Cellular Cardiology, 26, 361–368.Google Scholar
  75. 75.
    Morano, I., Hadicke, K., Haase, H., Bohm, M., Erdmann, E., & Schaub, M. C. (1997). Changes in essential myosin light chain isoform expression provide a molecular basis for isometric force regulation in the failing human heart. Journal of Molecular and Cellular Cardiology, 29, 1177–1187.Google Scholar
  76. 76.
    Morano, M., Zacharzowski, U., Maier, M., Lange, P. E., Alexi-Meskishvili, V., Haase, H., et al. (1996). Regulation of human heart contractility by essential myosin light chain isoforms. The Journal of Clinical Investigation, 98, 467–473.Google Scholar
  77. 77.
    Neumann, J., Eschenhagen, T., Jones, L. R., Linck, B., Schmitz, W., Scholz, H., et al. (1997). Increased expression of cardiac phosphatases in patients with end-stage heart failure. Journal of Molecular and Cellular Cardiology, 29, 265–272.Google Scholar
  78. 78.
    Noguchi, T., Hunlich, M., Camp, P. C., Begin, K. J., El-Zaru, M., Patten, R., et al. (2004). Thin-filament-based modulation of contractile performance in human heart failure. Circulation, 110, 982–987.Google Scholar
  79. 79.
    Noland, T. A., Jr., & Kuo, J. F. (1992). Protein kinase C phosphorylation of cardiac troponin T decreases Ca(2+)-dependent actomyosin MgATPase activity and troponin T binding to tropomyosin-F-actin complex. Biochemical Journal, 288(Pt 1), 123–129.Google Scholar
  80. 80.
    Noland, T. A., Jr., Raynor, R. L., Jideama, N. M., Guo, X., Kazanietz, M. G., Blumberg, P. M., et al. (1996). Differential regulation of cardiac actomyosin S-1 MgATPase by protein kinase C isozyme-specific phosphorylation of specific sites in cardiac troponin I and its phosphorylation site mutants. Biochemistry, 35, 14923–14931.Google Scholar
  81. 81.
    Palmiter, K. A., Tyska, M. J., Dupuis, D. E., Alpert, N. R., & Warshaw, D. M. (1999). Kinetic differences at the single molecule level account for the functional diversity of rabbit cardiac myosin isoforms. The Journal of Physiology, 519(Pt 3), 669–678.Google Scholar
  82. 82.
    Pan, B. S., & Solaro, R. J. (1987). Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. Journal of Biological Chemistry, 262, 7839–7849.Google Scholar
  83. 83.
    Passarelli, C., Petrini, S., Pastore, A., Bonetto, V., Sale, P., Gaeta, L. M., et al. (2008). Myosin as a potential redox-sensor: An in vitro study. Journal of Muscle Research and Cell Motility, 29, 119–126.Google Scholar
  84. 84.
    Pawloski-Dahm, C. M., Song, G., Kirkpatrick, D. L., Palermo, J., Gulick, J., Dorn, G. W., II, et al. (1998). Effects of total replacement of atrial myosin light chain-2 with the ventricular isoform in atrial myocytes of transgenic mice. Circulation, 97, 1508–1513.Google Scholar
  85. 85.
    Potter, J. D., Sheng, Z., Pan, B. S., & Zhao, J. (1995). A direct regulatory role for troponin T and a dual role for troponin C in the Ca2+ regulation of muscle contraction. Journal of Biological Chemistry, 270, 2557–2562.Google Scholar
  86. 86.
    Purcell, I. F., Bing, W., & Marston, S. B. (1999). Functional analysis of human cardiac troponin by the in vitro motility assay: Comparison of adult, foetal and failing hearts. Cardiovascular Research, 43, 884–891.Google Scholar
  87. 87.
    Rajan, S., Jagatheesan, G., Karam, C. N., Alves, M. L., Bodi, I., Schwartz, A., et al. (2010). Molecular and functional characterization of a novel cardiac-specific human tropomyosin isoform. Circulation, 121, 410–418.Google Scholar
  88. 88.
    Randhawa, A. K., & Singal, P. K. (1992). Pressure overload-induced cardiac hypertrophy with and without dilation. Journal of the American College of Cardiology, 20, 1569–1575.Google Scholar
  89. 89.
    Rao, V. S., La Bonte, L. R., Xu, Y., Yang, Z., French, B. A., & Guilford, W. H. (2007). Alterations to myofibrillar protein function in nonischemic regions of the heart early after myocardial infarction. American Journal of Physiology. Heart and Circulatory Physiology, 293, H654–H659.Google Scholar
  90. 90.
    Rayment, I., Rypniewski, W. R., Schmidt-Base, K., Smith, R., Tomchick, D. R., Benning, M. M., et al. (1993). Three-dimensional structure of myosin subfragment-1: A molecular motor. Science, 261, 50–58.ADSGoogle Scholar
  91. 91.
    Reiser, P. J., Portman, M. A., Ning, X. H., & Schomisch Moravec, C. (2001). Human cardiac myosin heavy chain isoforms in fetal and failing adult atria and ventricles. American Journal of Physiology. Heart and Circulatory Physiology, 280, H1814–H1820.Google Scholar
  92. 92.
    Revera, M., Van der Merwe, L., Heradien, M., Goosen, A., Corfield, V. A., Brink, P. A., et al. (2007). Long-term follow-up of R403WMYH7 and R92WTNNT2 HCM families: Mutations determine left ventricular dimensions but not wall thickness during disease progression. Cardiovascular Journal of Africa, 18, 146–153.Google Scholar
  93. 93.
    Rundell, V. L., Manaves, V., Martin, A. F., & de Tombe, P. P. (2005). Impact of beta-myosin heavy chain isoform expression on cross-bridge cycling kinetics. American Journal of Physiology. Heart and Circulatory Physiology, 288, H896–H903.Google Scholar
  94. 94.
    Sadayappan, S., Osinska, H., Klevitsky, R., Lorenz, J. N., Sargent, M., Molkentin, J. D., et al. (2006). Cardiac myosin binding protein C phosphorylation is cardioprotective. Proceedings of the National Academy of Sciences of the United States of America, 103, 16918–16923.ADSGoogle Scholar
  95. 95.
    Sanbe, A., Fewell, J. G., Gulick, J., Osinska, H., Lorenz, J., Hall, D. G., et al. (1999). Abnormal cardiac structure and function in mice expressing nonphosphorylatable cardiac regulatory myosin light chain 2. Journal of Biological Chemistry, 274, 21085–21094.Google Scholar
  96. 96.
    Schiaffino, S., Gorza, L., Saggin, L., Valfre, C., & Sartore, S. (1984). Myosin changes in hypertrophied human atrial and ventricular myocardium. A correlated immunofluorescence and quantitative immunochemical study on serial cryosections. European Heart Journal, 5(Suppl. F), 95–102.Google Scholar
  97. 97.
    Schwartz, K., Carrier, L., Lompre, A. M., Mercadier, J. J., & Boheler, K. R. (1992). Contractile proteins and sarcoplasmic reticulum calcium-ATPase gene expression in the hypertrophied and failing heart. Basic Research in Cardiology, 87(Suppl. 1), 285–290.Google Scholar
  98. 98.
    Scruggs, S. B., Hinken, A. C., Thawornkaiwong, A., Robbins, J., Walker, L. A., de Tombe, P. P., et al. (2009). Ablation of ventricular myosin regulatory light chain phosphorylation in mice causes cardiac dysfunction in situ and affects neighboring myofilament protein phosphorylation. Journal of Biological Chemistry, 284, 5097–5106.Google Scholar
  99. 99.
    Scruggs, S. B., Reisdorph, R., Armstrong, M. L., Warren, C. M., Reisdorph, N., Solaro, R. J., et al. (2010). A novel, in-solution separation of endogenous cardiac sarcomeric proteins and identification of distinct charged variants of regulatory light chain. Molecular & Cellular Proteomics, 9, 1804–1818.Google Scholar
  100. 100.
    Simpson, P. C. (1999). Beta-protein kinase C and hypertrophic signaling in human heart failure. Circulation, 99, 334–337.Google Scholar
  101. 101.
    Sobotka, P. A., Brottman, M. D., Weitz, Z., Birnbaum, A. J., Skosey, J. L., & Zarling, E. J. (1993). Elevated breath pentane in heart failure reduced by free radical scavenger. Free Radical Biology & Medicine, 14, 643–647.Google Scholar
  102. 102.
    Solaro, R. J., & Rarick, H. M. (1998). Troponin and tropomyosin: Proteins that switch on and tune in the activity of cardiac myofilaments. Circulation Research, 83, 471–480.Google Scholar
  103. 103.
    Stelzer, J. E., Dunning, S. B., & Moss, R. L. (2006). Ablation of cardiac myosin-binding protein-C accelerates stretch activation in murine skinned myocardium. Circulation Research, 98, 1212–1218.Google Scholar
  104. 104.
    Stelzer, J. E., Fitzsimons, D. P., & Moss, R. L. (2006). Ablation of myosin-binding protein-C accelerates force development in mouse myocardium. Biophysical Journal, 90, 4119–4127.ADSGoogle Scholar
  105. 105.
    Sugiura, S., Kobayakawa, N., Fujita, H., Yamashita, H., Momomura, S., Chaen, S., et al. (1998). Comparison of unitary displacements and forces between 2 cardiac myosin isoforms by the optical trap technique: Molecular basis for cardiac adaptation. Circulation Research, 82, 1029–1034.Google Scholar
  106. 106.
    Sugiura, S., & Yamashita, H. (1998). Functional characterization of cardiac myosin isoforms. The Japanese Journal of Physiology, 48, 173–179.Google Scholar
  107. 107.
    Sumandea, M. P., Pyle, W. G., Kobayashi, T., de Tombe, P. P., & Solaro, R. J. (2003). Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin T. Journal of Biological Chemistry, 278, 35135–35144.Google Scholar
  108. 108.
    Suurmeijer, A. J., Clement, S., Francesconi, A., Bocchi, L., Angelini, A., Van Veldhuisen, D. J., et al. (2003). Alpha-actin isoform distribution in normal and failing human heart: A morphological, morphometric, and biochemical study. The Journal of Pathology, 199, 387–397.Google Scholar
  109. 109.
    Tardiff, J. C. (2005). Sarcomeric proteins and familial hypertrophic cardiomyopathy: Linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Failure Reviews, 10, 237–248.Google Scholar
  110. 110.
    Tardiff, J. C. (2011). Thin filament mutations: Developing an integrative approach to a complex disorder. Circulation Research, 108, 765–782.Google Scholar
  111. 111.
    Tobacman, L. S., Nihli, M., Butters, C., Heller, M., Hatch, V., Craig, R., et al. (2002). The troponin tail domain promotes a conformational state of the thin filament that suppresses myosin activity. Journal of Biological Chemistry, 277, 27636–27642.Google Scholar
  112. 112.
    Tyska, M. J., & Warshaw, D. M. (2002). The myosin power stroke. Cell Motility and the Cytoskeleton, 51, 1–15.Google Scholar
  113. 113.
    van der Velden, J., Klein, L. J., van der Bijl, M., Huybregts, M. A., Stooker, W., Witkop, J., et al. (1999). Isometric tension development and its calcium sensitivity in skinned myocyte-sized preparations from different regions of the human heart. Cardiovascular Research, 42, 706–719.Google Scholar
  114. 114.
    van der Velden, J., Papp, Z., Boontje, N. M., Zaremba, R., de Jong, J. W., Janssen, P. M., et al. (2003). The effect of myosin light chain 2 dephosphorylation on Ca2+-sensitivity of force is enhanced in failing human hearts. Cardiovascular Research, 57, 505–514.Google Scholar
  115. 115.
    van der Velden, J., Papp, Z., Zaremba, R., Boontje, N. M., de Jong, J. W., Owen, V. J., et al. (2003). Increased Ca2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovascular Research, 57, 37–47.Google Scholar
  116. 116.
    van Heerebeek, L., Hamdani, N., Handoko, M. L., Falcao-Pires, I., Musters, R. J., Kupreishvili, K., et al. (2008). Diastolic stiffness of the failing diabetic heart: Importance of fibrosis, advanced glycation end products, and myocyte resting tension. Circulation, 117, 43–51.Google Scholar
  117. 117.
    Vandekerckhove, J., Bugaisky, G., & Buckingham, M. (1986). Simultaneous expression of skeletal muscle and heart actin proteins in various striated muscle tissues and cells. A quantitative determination of the two actin isoforms. Journal of Biological Chemistry, 261, 1838–1843.Google Scholar
  118. 118.
    Vandekerckhove, J., & Weber, K. (1979). The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle, and rabbit slow skeletal muscle. A protein-chemical analysis of muscle actin differentiation. Differentiation, 14, 123–133.Google Scholar
  119. 119.
    Weisberg, A., & Winegrad, S. (1996). Alteration of myosin cross bridges by phosphorylation of myosin-binding protein C in cardiac muscle. Proceedings of the National Academy of Sciences of the United States of America, 93, 8999–9003.ADSGoogle Scholar
  120. 120.
    Weith, A., Sadayappan, S., Gulick, J., Previs, M. J., Vanburen, P., Robbins, J., et al. (2012). Unique single molecule binding of cardiac myosin binding protein-C to actin and phosphorylation-dependent inhibition of actomyosin motility requires 17 amino acids of the motif domain. Journal of Molecular and Cellular Cardiology, 52, 219–227.Google Scholar
  121. 121.
    Wolff, M. R., Buck, S. H., Stoker, S. W., Greaser, M. L., & Mentzer, R. M. (1996). Myofibrillar calcium sensitivity of isometric tension is increased in human dilated cardiomyopathies: Role of altered beta-adrenergically mediated protein phosphorylation. The Journal of Clinical Investigation, 98, 167–176.Google Scholar
  122. 122.
    Xiao, L., Zhao, Q., Du, Y., Yuan, C., Solaro, R. J., & Buttrick, P. M. (2007). PKCepsilon increases phosphorylation of the cardiac myosin binding protein C at serine 302 both in vitro and in vivo. Biochemistry, 46, 7054–7061.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2013

Authors and Affiliations

  • Jillian N. Simon
    • 1
  • Jil C. Tardiff
    • 2
  • Beata M. Wolska
    • 3
  1. 1.Department of Physiology and BiophysicsUniversity of Illinois at ChicagoChicagoUSA
  2. 2.University of ArizonaTucsonUSA
  3. 3.Department of Medicine, Section of Cardiology and Department of Physiology and Biophysics, Center for Cardiovascular ResearchUniversity of IllinoisChicagoUSA

Personalised recommendations