Journal of Molecular and Cellular Cardiology
Volume 48, Issue 5 , Pages 817-823 , May 2010

Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width

  • Brenda Russell

      Affiliations

    • Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, IL, USA
    • Corresponding Author InformationCorresponding author. Department of Physiology and Biophysics, University of Illinois at Chicago, MC 901, 835 S. Wolcott Avenue, Chicago, IL 60612, USA. Tel.: +1 312 413 0407; fax: +1 312 996 1414.
    • ,
  • Matthew W. Curtis

      Affiliations

    • Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, IL, USA
    • ,
  • Yevgeniya E. Koshman

      Affiliations

    • The Cardiovascular Institute, Loyola University Medical Center, Maywood, IL, USA
    • ,
  • Allen M. Samarel

      Affiliations

    • The Cardiovascular Institute, Loyola University Medical Center, Maywood, IL, USA

Received 30 October 2009 ,Revised 15 February 2010 ,Accepted 17 February 2010.

References 

  1. Esposito G, Rapacciuolo A, Naga Prasad SV, Takaoka H, Thomas SA, Koch WJ, et al. Genetic alterations that inhibit in vivo pressure-overload hypertrophy prevent cardiac dysfunction despite increased wall stress. Circulation. 2002;105:85–92
  2. Russell B, Motlagh D, Ashley WW. Form follows function: how muscle shape is regulated by work. J Appl Physiol. 2000;88:1127–1132
  3. Gerdes AM, Kellerman SE, Moore JA, Muffly KE, Clark LC, Reaves PY, et al. Structural remodeling of cardiac myocytes in patients with ischemic cardiomyopathy. Circulation. 1992;86:426–430
  4. Gregorio CC, Antin PB. To the heart of myofibril assembly. Trends Cell Biol. 2000;10:355–362
  5. Ehler E, Horowits R, Zuppinger C, Price RL, Perriard E, Leu M, et al. Alterations at the intercalated disk associated with the absence of muscle LIM protein. J Cell Biol. 2001;153:763–772
  6. Clark KA, McElhinny AS, Beckerle MC, Gregorio CC. Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol. 2002;18:637–706
  7. Sanger JW, Chowrashi P, Shaner NC, Spalthoff S, Wang J, Freeman NL, et al. Myofibrillogenesis in skeletal muscle cells. Clin Orthop Relat Res. 2002;S153–S162
  8. Dabiri GA, Turnacioglu KK, Sanger JM, Sanger JW. Myofibrillogenesis visualized in living embryonic cardiomyocytes. Proc Natl Acad Sci USA. 1997;94:9493–9498
  9. Sanger JW, Wang J, Holloway B, Du A, Sanger JM. Myofibrillogenesis in skeletal muscle cells in zebrafish. Cell Motil Cytoskeleton. 2009;66:556–566
  10. Stout AL, Wang J, Sanger JM, Sanger JW. Tracking changes in Z-band organization during myofibrillogenesis with FRET imaging. Cell Motil Cytoskeleton. 2008;65:353–367
  11. Huang W, Zhang R, Xu X. Myofibrillogenesis in the developing zebrafish heart: A functional study of tnnt2. Dev Biol. 2009;331:237–249
  12. Dix DJ, Eisenberg BR. Myosin mRNA accumulation and myofibrillogenesis at the myotendinous junction of stretched muscle fibers. J Cell Biol. 1990;111:1885–1894
  13. Yu JG, Russell B. Cardiomyocyte remodeling and sarcomere addition after uniaxial static strain in vitro. J Histochem Cytochem. 2005;53:839–844
  14. Perriard JC, Hirschy A, Ehler E. Dilated cardiomyopathy: a disease of the intercalated disc?. Trends Cardiovasc Med. 2003;13:30–38
  15. Yu JG, Thornell LE. Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem Cell Biol. 2002;118:171–179
  16. Yu JG, Furst DO, Thornell LE. The mode of myofibril remodelling in human skeletal muscle affected by DOMS induced by eccentric contractions. Histochem Cell Biol. 2003;119:383–393
  17. Senyo SE, Koshman YE, Russell B. Stimulus interval, rate and direction differentially regulate phosphorylation for mechanotransduction in neonatal cardiac myocytes. FEBS Lett. 2007;581:4241–4247
  18. Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol. 2005;289:H2291–H2301
  19. Wang N, Butler JP, Ingber DE. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 1993;260:1124–1127
  20. Street SF. Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. J Cell Physiol. 1983;114:346–364
  21. Bloch RJ, Gonzalez-Serratos H. Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev. 2003;31:73–78
  22. Vandenburgh H, Kaufman S. In vitro model for stretch-induced hypertrophy of skeletal muscle. Science. 1979;203:265–268
  23. Peterson MB, Lesch M. synthesis and amino acid transport in the isolated rabbit right ventricular papillary muscle. Effect of isometric tension development. Circ Res. 1972;31:317–327
  24. Takala T. Protein synthesis in the isolated perfused rat heart. Effects of mechanical work load, diastolic ventricular pressure and coronary pressure on amino acid incorporation and its transmural distribution into left ventricular protein. Basic Res Cardiol. 1981;76:44–61
  25. Samarel AM, Engelmann GL. Contractile activity modulates myosin heavy chain-β expression in neonatal rat heart cells. Am J Physiol. 1991;261:H1067–H1077
  26. Sharp WW, Terracio L, Borg TK, Samarel AM. Contractile activity modulates actin synthesis and turnover in cultured neonatal rat heart cells. Circ Res. 1993;73:172–183
  27. Simpson DG, Terracio L, Terracio M, Price RL, Turner DC, Borg TK. Modulation of cardiac myocyte phenotype in vitro by the composition and orientation of the extracellular matrix. J Cell Physiol. 1994;161:89–105
  28. Simpson DG, Majeski M, Borg TK, Terracio L. Regulation of cardiac myocyte protein turnover and myofibrillar structure in vitro by specific directions of stretch. Circ Res. 1999;85:e59–e69
  29. Gopalan SM, Flaim C, Bhatia SN, Hoshijima M, Knoell R, Chien KR, et al. Anisotropic stretch-induced hypertrophy in neonatal ventricular myocytes micropatterned on deformable elastomers. Biotechnol Bioeng. 2003;81:578–587
  30. Zile MR, Cowles MK, Buckley JM, Richardson K, Cowles BA, Baicu CF, et al. Gel stretch method: a new method to measure constitutive properties of cardiac muscle cells. Am J Physiol. 1998;274:H2188–H2202
  31. Mansour H, de Tombe PP, Samarel AM, Russell B. Restoration of resting sarcomere length after uniaxial static strain is regulated by protein kinase Cε and focal adhesion kinase. Circ Res. 2004;94:642–649
  32. Braga VM. Cell–cell adhesion and signalling. Curr Opin Cell Biol. 2002;14:546–556
  33. Sussman MA, McCulloch A, Borg TK. Dance band on the Titanic: biomechanical signaling in cardiac hypertrophy. Circ Res. 2002;91:888–898
  34. Deutsch J, Motlagh D, Russell B, Desai TA. Fabrication of microtextured membranes for cardiac myocyte attachment and orientation. J Biomed Mater Res. 2000;53:267–275
  35. Motlagh D, Hartman TJ, Desai TA, Russell B. Microfabricated grooves recapitulate neonatal myocyte connexin43 and N-cadherin expression and localization. J Biomed Mater Res A. 2003;67:148–157
  36. Motlagh D, Senyo SE, Desai TA, Russell B. Microtextured substrata alter gene expression, protein localization and the shape of cardiac myocytes. Biomaterials. 2003;24:2463–2476
  37. Boateng SY, Hartman TJ, Ahluwalia N, Vidula H, Desai TA, Russell B. Inhibition of fibroblast proliferation in cardiac myocyte cultures by surface microtopography. Am J Physiol Cell Physiol. 2003;285:C171–C182
  38. Kumar A, Chaudhry I, Reid MB, Boriek AM. Distinct signaling pathways are activated in response to mechanical stress applied axially and transversely to skeletal muscle fibers. J Biol Chem. 2002;277:46493–46503
  39. Kaunas R, Nguyen P, Usami S, Chien S. Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proc Natl Acad Sci USA. 2005;102:15895–15900
  40. Pyle WG, Solaro RJ. At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ Res. 2004;94:296–305
  41. Miller MK, Granzier H, Ehler E, Gregorio CC. The sensitive giant: the role of titin-based stretch sensing complexes in the heart. Trends Cell Biol. 2004;14:119–126
  42. Knoll R, Hoshijima M, Hoffman HM, Person V, Lorenzen-Schmidt I, Bang ML, et al. The cardiac mechanical stretch sensor machinery involves a Z disc complex that is defective in a subset of human dilated cardiomyopathy. Cell. 2002;111:943–955
  43. Boateng SY, Belin RJ, Geenen DL, Margulies KB, Martin JL, Hoshijima M, et al. Cardiac dysfunction and heart failure are associated with abnormalities in the subcellular distribution and amounts of oligomeric muscle LIM protein. Am J Physiol Heart Circ Physiol. 2007;292:H259–H269
  44. Boateng SY, Senyo SE, Qi L, Goldspink PH, Russell B. Myocyte remodeling in response to hypertrophic stimuli requires nucleocytoplasmic shuttling of muscle LIM protein. J Mol Cell Cardiol. 2009;47:426–435
  45. Wixler V, Geerts D, Laplantine E, Westhoff D, Smyth N, Aumailley M, et al. The LIM-only protein DRAL/FHL2 binds to the cytoplasmic domain of several α and β integrin chains and is recruited to adhesion complexes. J Biol Chem. 2000;275:33669–33678
  46. Robinson PA, Brown S, McGrath MJ, Coghill ID, Gurung R, Mitchell CA. Skeletal muscle LIM protein 1 regulates integrin-mediated myoblast adhesion, spreading, and migration. Am J Physiol Cell Physiol. 2003;284:C681–C695
  47. Heineke J, Kempf T, Kraft T, Hilfiker A, Morawietz H, Scheubel RJ, et al. Downregulation of cytoskeletal muscle LIM protein by nitric oxide: impact on cardiac myocyte hypertrophy. Circulation. 2003;107:1424–1432
  48. Yi XP, Wang X, Gerdes AM, Li F. Subcellular redistribution of focal adhesion kinase and its related nonkinase in hypertrophic myocardium. Hypertension. 2003;41:1317–1323
  49. Yi XP, Zhou J, Huber L, Qu J, Wang X, Gerdes AM, et al. Nuclear compartmentalization of FAK and FRNK in cardiac myocytes. Am J Physiol Heart Circ Physiol. 2006;290:H2509–H2515
  50. Kuwahara K, Teg Pipes GC, McAnally J, Richardson JA, Hill JA, Bassel-Duby R, et al. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J Clin Invest. 2007;117:1324–1334
  51. Gautel M. The sarcomere and the nucleus: functional links to hypertrophy, atrophy and sarcopenia. Adv Exp Med Biol. 2008;642:176–191
  52. Koshman Y.E., Piano M.R., Russell B., Schwertz D.W. Signaling responses after exposure to 5α-dihydrotestosterone or 17β-estradiol in norepinephrine-induced hypertrophy of neonatal rat ventricular myocytes. J Appl Physiol; in press.
  53. Fatkin D, Graham RM. Molecular mechanisms of inherited cardiomyopathies. Physiol Rev. 2002;82:945–980
  54. Sharp WW, Simpson DG, Borg TK, Samarel AM, Terracio L. Mechanical forces regulate focal adhesion and costamere assembly in cardiac myocytes. Am J Physiol. 1997;273:H546–H556
  55. Fluck M, Ziemiecki A, Billeter R, Muntener M. Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration. J Exp Biol. 2002;205:2337–2348
  56. Wang SM, Tsai YJ, Jiang MJ, Tseng YZ. Studies on the function of Rho A protein in cardiac myofibrillogenesis. J Cell Biochem. 1997;66:43–53
  57. VanWinkle WB, Snuggs MB, De Hostos EL, Buja LM, Woods A, Couchman JR. Localization of the transmembrane proteoglycan syndecan-4 and its regulatory kinases in costameres of rat cardiomyocytes: a deconvolution microscopic study. Anat Rec. 2002;268:38–46
  58. Ehler E, Fowler VM, Perriard JC. Myofibrillogenesis in the developing chicken heart: role of actin isoforms and of the pointed end actin capping protein tropomodulin during thin filament assembly. Dev Dyn. 2004;229:745–755
  59. Littlefield RS, Fowler VM. Thin filament length regulation in striated muscle sarcomeres: pointed-end dynamics go beyond a nebulin ruler. Semin Cell Dev Biol. 2008;19:511–519
  60. Cooper JA, Sept D. New insights into mechanism and regulation of actin capping protein. Int Rev Cell Mol Biol. 2008;267:183–206
  61. Willis MS, Schisler JC, Portbury AL, Patterson C. Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res. 2009;81:439–448
  62. Hart MC, Cooper JA. Vertebrate isoforms of actin capping protein β have distinct functions In vivo. J Cell Biol. 1999;147:1287–1298
  63. Wang J, Shaner N, Mittal B, Zhou Q, Chen J, Sanger JM, et al. Dynamics of Z-band based proteins in developing skeletal muscle cells. Cell Motil Cytoskeleton. 2005;61:34–48
  64. Schafer DA, Korshunova YO, Schroer TA, Cooper JA. Differential localization and sequence analysis of capping protein β-subunit isoforms of vertebrates. J Cell Biol. 1994;127:453–465
  65. Kim K, Yamashita A, Wear MA, Maeda Y, Cooper JA. Capping protein binding to actin in yeast: biochemical mechanism and physiological relevance. J Cell Biol. 2004;164:567–580
  66. Yamashita A, Maeda K, Maeda Y. Crystal structure of CapZ: structural basis for actin filament barbed end capping. EMBO J. 2003;22:1529–1538
  67. Wear MA, Yamashita A, Kim K, Maeda Y, Cooper JA. How capping protein binds the barbed end of the actin filament. Curr Biol. 2003;13:1531–1537
  68. Wear MA, Cooper JA. Capping protein: new insights into mechanism and regulation. Trends Biochem Sci. 2004;29:418–428
  69. Narita A, Maeda Y. Molecular determination by electron microscopy of the actin filament end structure. J Mol Biol. 2007;365:480–501
  70. Narita A, Takeda S, Yamashita A, Maeda Y. Structural basis of actin filament capping at the barbed-end: a cryo-electron microscopy study. EMBO J. 2006;25:5626–5633
  71. Wakasaki H, Koya D, Schoen FJ, Jirousek MR, Ways DK, Hoit BD, et al. Targeted overexpression of protein kinase C ß2 isoform in myocardium causes cardiomyopathy. Proc Natl Acad Sci USA. 1997;94:9320–9325
  72. Schafer DA, Jennings PB, Cooper JA. Dynamics of capping protein and actin assembly in vitro: uncapping barbed ends by polyphosphoinositides. J Cell Biol. 1996;135:169–179
  73. Strait JB, Martin JL, Bayer A, Mestril R, Eble DM, Samarel AM. Role of protein kinase C-ε in hypertrophy of cultured neonatal rat ventricular myocytes. Am J Physiol Heart Circ Physiol. 2001;280:H756–H766
  74. Heidkamp MC, Bayer AL, Scully BT, Eble DM, Samarel AM. Activation of focal adhesion kinase by protein kinase Cε in neonatal rat ventricular myocytes. Am J Physiol Heart Circ Physiol. 2003;285:H1684–H1696
  75. Nicol RL, Frey N, Pearson G, Cobb M, Richardson J, Olson EN. Activated MEK5 induces serial assembly of sarcomeres and eccentric cardiac hypertrophy. EMBO J. 2001;20:2757–2767
  76. Heidkamp MC, Iyengar R, Szotek EL, Cribbs LL, Samarel AM. Protein kinase Cε-dependent MARCKS phosphorylation in neonatal and adult rat ventricular myocytes. J Mol Cell Cardiol. 2007;42:422–431
  77. Heidkamp MC, Bayer AL, Kalina JA, Eble DM, Samarel AM. GFP-FRNK disrupts focal adhesions and induces anoikis in neonatal rat ventricular myocytes. Circ Res. 2002;90:1282–1289
  78. Heidkamp MC, Bayer AL, Martin JL, Samarel AM. Differential activation of mitogen-activated protein kinase cascades and apoptosis by protein kinase C ε and δ in neonatal rat ventricular myocytes. Circ Res. 2001;89:882–890
  79. Clerk A, Pham FH, Fuller SJ, Sahai E, Aktories K, Marais R, et al. Regulation of mitogen-activated protein kinases in cardiac myocytes through the small G protein Rac1. Mol Cell Biol. 2001;21:1173–1184
  80. Torsoni AS, Fonseca PM, Crosara-Alberto DP, Franchini KG. Early activation of p160ROCK by pressure overload in rat heart. Am J Physiol Cell Physiol. 2003;284:C1411–C1419
  81. Torsoni AS, Marin TM, Velloso LA, Franchini KG. RhoA/ROCK signaling is critical to FAK activation by cyclic stretch in cardiac myocytes. Am J Physiol Heart Circ Physiol. 2005;289:H1488–H1496
  82. Hoshijima M, Sah VP, Wang Y, Chien KR, Brown JH. The low molecular weight GTPase Rho regulates myofibril formation and organization in neonatal rat ventricular myocytes. Involvement of Rho kinase. J Biol Chem. 1998;273:7725–7730
  83. Aoki H, Izumo S, Sadoshima J. Angiotensin II activates RhoA in cardiac myocytes: a critical role of RhoA in angiotensin II-induced premyofibril formation. Circ Res. 1998;82:666–676
  84. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005;6:56–68
  85. Ilic D, Kovacic B, McDonagh S, Jin F, Baumbusch C, Gardner DG, et al. Focal adhesion kinase is required for blood vessel morphogenesis. Circ Res. 2003;92:300–307
  86. Peng X, Kraus MS, Wei H, Shen TL, Pariaut R, Alcaraz A, et al. Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J Clin Invest. 2006;116:217–227
  87. DiMichele LA, Doherty JT, Rojas M, Beggs HE, Reichardt LF, Mack CP, et al. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ Res. 2006;99:636–645
  88. Hakim ZS, DiMichele LA, Doherty JT, Homeister JW, Beggs HE, Reichardt LF, et al. Conditional deletion of focal adhesion kinase leads to defects in ventricular septation and outflow tract alignment. Mol Cell Biol. 2007;27:5352–5364
  89. Yamakita Y, Totsukawa G, Yamashiro S, Fry D, Zhang X, Hanks SK, et al. Dissociation of FAK/p130CAS/c-Src complex during mitosis: role of mitosis-specific serine phosphorylation of FAK. J Cell Biol. 1999;144:315–324
  90. Ma A, Richardson A, Schaefer EM, Parsons JT. Serine phosphorylation of focal adhesion kinase in interphase and mitosis: a possible role in modulating binding to p130Cas. Mol Biol Cell. 2001;12:1–12
  91. Hunger-Glaser I, Salazar EP, Sinnett-Smith J, Rozengurt E. Bombesin, lysophosphatidic acid, and epidermal growth factor rapidly stimulate focal adhesion kinase phosphorylation at Ser-910: requirement for ERK activation. J Biol Chem. 2003;278:22631–22643
  92. Chu M, Iyengar R, Samarel AM. Biomechanical and neurohumoral stimulation of neonatal rat ventricular myocytes induces focal adhesion kinase phosphorylation at S910. FASEB J. 2009;23:LB56;abstract
  93. Schlaepfer DD, Mitra SK, Ilic D. Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta. 2004;1692:77–102
  94. Samarel AM. In vivo measurements of protein turnover during muscle growth and atrophy. FASEB J. 1991;5:2020–2028
  95. Eble DM, Spragia ML, Ferguson AG, Samarel AM. Sarcomeric myosin heavy chain is degraded by the proteasome. Cell Tissue Res. 1999;296:541–548
  96. Hartman TJ, Martin JL, Solaro RJ, Samarel AM, Russell B. CapZ dynamics are altered by endothelin-1 and phenylephrine via PIP2- and PKC-dependent mechanisms. Am J Physiol Cell Physiol. 2009;296:C1034–C1039
  97. Clerk A, Bogoyevitch MA, Anderson MB, Sugden PH. Differential activation of protein kinase C isoforms by endothelin-1 and phenylephrine and subsequent stimulation of p42 and p44 mitogen-activated protein kinases in ventricular myocytes cultured from neonatal rat hearts. J Biol Chem. 1994;269:32848–32857
  98. Pyle WG, Hart MC, Cooper JA, Sumandea MP, de Tombe PP, Solaro RJ. Actin capping protein: an essential element in protein kinase signaling to the myofilaments. Circ Res. 2002;90:1299–1306
  99. Pyle WG, La Rotta G, de Tombe PP, Sumandea MP, Solaro RJ. Control of cardiac myofilament activation and PKC-ßII signaling through the actin capping protein, CapZ. J Mol Cell Cardiol. 2006;41:537–543
  100. Suh BC, Hille B. Electrostatic interaction of internal Mg2+ with membrane PIP2 seen with KCNQ K+ channels. J Gen Physiol. 2007;130:241–256
  101. Suh BC, Hille B. PIP2 is a necessary cofactor for ion channel function: how and why?. Annu Rev Biophys. 2008;37:175–195
  102. Mao YS, Yin HL. Regulation of the actin cytoskeleton by phosphatidylinositol 4-phosphate 5 kinases. Pflugers Arch. 2007;455:5–18
  103. Smith J, Diez G, Klemm AH, Schewkunow V, Goldmann WH. CapZ–lipid membrane interactions: a computer analysis. Theor Biol Med Model. 2006;3:30
  104. Kim K, McCully ME, Bhattacharya N, Butler B, Sept D, Cooper JA. Structure/function analysis of the interaction of phosphatidylinositol 4, 5-bisphosphate with actin-capping protein: implications for how capping protein binds the actin filament. J Biol Chem. 2007;282:5871–5879
  105. Fraley TS, Pereira CB, Tran TC, Singleton C, Greenwood JA. Phosphoinositide binding regulates α-actinin dynamics: mechanism for modulating cytoskeletal remodeling. J Biol Chem. 2005;280:15479–15482
  106. Fukami K, Endo T, Imamura M, Takenawa T. α-Actinin and vinculin are PIP2-binding proteins involved in signaling by tyrosine kinase. J Biol Chem. 1994;269:1518–1522
  107. Young P, Gautel M. The interaction of titin and alpha-actinin is controlled by a phospholipid-regulated intramolecular pseudoligand mechanism. EMBO J. 2000;19:6331–6340

PII: S0022-2828(10)00077-5

doi: 10.1016/j.yjmcc.2010.02.016

Journal of Molecular and Cellular Cardiology
Volume 48, Issue 5 , Pages 817-823 , May 2010

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