Cardiomyocyte contractile status is associated with differences in fibronectin and integrin interactions

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 298, Issue 6, 2010, Pages

  Wu, Xin ^a   Sun, Zhe ^b   Foskett, Andrea ^a   Trzeciakowski, Jerome P ^a   Meininger, Gerald A ^b   Muthuchamy, Mariappan ^a  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Atomic force microscopy; Cell mechanics; Extracellular matrix protein; Integrins; Mechanobiology

Indexed keywords

ACTIN; CALCIUM ION; CYTOCHALASIN D; CYTOSKELETON PROTEIN; DIACETYL OXIME; FIBRONECTIN; INTEGRIN; MONOCLONAL ANTIBODY; POTASSIUM; PROTEIN SUBUNIT; VERY LATE ACTIVATION ANTIGEN 3; VERY LATE ACTIVATION ANTIGEN 5;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL ADHESION; CELL ISOLATION; CONTROLLED STUDY; CYTOSKELETON; EXTRACELLULAR MATRIX; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILE FORCE; HEART MUSCLE RELAXATION; HYPOTHESIS; MALE; MOUSE; MUSCLE ISOTONIC CONTRACTION; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION;

ACTINS; ANIMALS; CELLS, CULTURED; CYTOSKELETON; EXTRACELLULAR MATRIX; FIBRONECTINS; INTEGRINS; MALE; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; MYOSINS;

EID: 77952629071     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01156.2009     Document Type: Article

References (85)

1. Ahumada GG, Saffitz JE. Fibronectin in rat heart: a link between cardiac myocytes and collagen. J Histochem Cytochem 32: 383-388, 1984.
2. Belke DD, Dillmann WH. Altered cardiac calcium handling in diabetes. Curr Hypertens Rep 6: 424-429, 2004.
3. Benoit M, Gabriel D, Gerisch G, Gaub HE. Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nat Cell Biol 2: 313-317, 2000.
4. Brancaccio M, Hirsch E, Notte A, Selvetella G, Lembo G, Tarone G. Integrin signalling: the tug-of-war in heart hypertrophy. Cardiovasc Res 70: 422-433, 2006.
5. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54: 1615-1625, 2005. (Pubitemid 40770750)
6. Casscells W, Ferrans VJ. Growth factors in the heart. In: The Development and Regenerative Potential of Cardiac Muscle, edited by Oberpriller JO, Oberpriller JS, Mauro A. New York: Harvard, 1990, p. 8-21.
7. Chen H, Huang XN, Stewart AF, Sepulveda JL. Gene expression changes associated with fibronectin-induced cardiac myocyte hypertrophy. Physiol Genomics 18: 273-283, 2004. (Pubitemid 39319510)
8. Contard F, Koteliansky V, Marotte F, Dubus I, Rappaport L, Samuel JL. Specific alterations in the distribution of extracellular matrix components within rat myocardium during the development of pressure overload. Lab Invest 64: 65-75, 1991.
9. Craig SW, Pardo JV. Gamma actin, spectrin, and intermediate filament proteins colocalize with vinculin at costameres, myofibril-to-sarcolemma attachment sites. Cell Motil 3: 449-462, 1983.
10. Dalen H, Saetersdal T, Roli J, Larsen TH. Effect of collagenase on surface expression of immunoreactive fibronectin and laminin in freshly isolated cardiac myocytes. J Mol Cell Cardiol 30: 947-955, 1998. (Pubitemid 28279307)
11. Danen EH, Yamada KM. Fibronectin, integrins, and growth control. J Cell Physiol 189: 1-13, 2001.
12. Davis MJ, Wu X, Nurkiewicz TR, Kawasaki J, Davis GE, Hill MA, Meininger GA. Integrins and mechanotransduction of the vascular myogenic response. Am J Physiol Heart Circ Physiol 280: H1427-H1433, 2001. (Pubitemid 33775763)
13. Efron B, Tibshirani R. An Introduction to the Bootstrap. London: Chapman and Hall, 1993.
14. Epstein ND, Davis JS. Sensing stretch is fundamental. Cell 112: 147-150, 2003.
15. Ervasti JM. Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278: 13591-13594, 2003.
16. Farhadian F, Contard F, Sabri A, Samuel JL, Rappaport L. Fibronectin and basement membrane in cardiovascular organogenesis and disease pathogenesis. Cardiovasc Res 32: 433-442, 1996. (Pubitemid 26288591)
17. Fredersdorf S, Thumann C, Ulucan C, Griese DP, Luchner A, Riegger GA, Kromer EP, Weil J. Myocardial hypertrophy and enhanced left ventricular contractility in Zucker diabetic fatty rats. Cardiovasc Pathol 13: 11-19, 2004. (Pubitemid 38169461)
18. Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane crosstalk between the extracellular matrix and the cytoskeleton. Nat Rev Mol Cell Biol 2: 793-805, 2001.
19. Glukhova M, Koteliansky V. Integrins, cytoskeletal and extracellular matrix proteins in developing smooth muscle cells of human aorta. In: The Vascular Smooth Muscle Cell: Molecular and Biological Responses to the Extracellular Matrix, edited by Schwartz S, Mecham R. San Diego, CA: Academic, 1995, p. 37-79.
20. Grimm D, Huber M, Jabusch HC, Shakibaei M, Fredersdorf S, Paul M, Riegger GA, Kromer EP. Extracellular matrix proteins in cardiac fibroblasts derived from rat hearts with chronic pressure overload: effects of β-receptor blockade. J Mol Cell Cardiol 33: 487-501, 2001. (Pubitemid 32539005)
21. 1integrin-deficient embryonic stem cell-derived cardiac cells. J Mol Cell Cardiol 33: 521-532, 2001.
22. Gui P, Wu X, Ling S, Stotz SC, Winkfein RJ, Wilson E, Davis GE, Braun AP, Zamponi GW, Davis MJ. Integrin receptor activation triggers converging regulation of Cav1.2 calcium channels by c-Src and protein kinase A pathways. J Biol Chem 281: 14015-14025, 2006. (Pubitemid 43848328)
23. Gwathmey JK, Hajjar RJ, Solaro RJ. Contractile deactivation and uncoupling of crossbridges. Effects of 2,3-butanedione monoxime on mammalian myocardium. Circ Res 69: 1280-1292, 1991.
24. Helenius J, Heisenberg CP, Gaub HE, Muller DJ. Single-cell force spectroscopy. J Cell Sci 121: 1785-1791, 2008.
25. Hesterberg T, Moore DS, Monaghan S, Clipson A, Epstein R. Bootstrap methods and permutation tests. In: Introduction to the Practice of Statistics, edited by Moore DS, McCabe GP. New York: Freeman, 2005.
26. Hynes RO. Fibronectins. Sci Am 254: 42-51, 1986.
27. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25, 1992.
28. Ingber D. Integrins as mechanochemical transducers. Curr Opin Cell Biol 3: 841-848, 1991.
29. Izenman AJ. Recent developments in nonparametric density estimation. J Am Stat Assoc 86: 205-224, 1991.
30. Jane-Lise S, Corda S, Chassagne C, Rappaport L. The extracellular matrix and the cytoskeleton in heart hypertrophy and failure. Heart Fail Rev 5: 239-250, 2000.
31. Kaur H, Chen S, Xin X, Chiu J, Khan ZA, Chakrabarti S. Diabetes-induced extracellular matrix protein expression is mediated by transcription coactivator p300. Diabetes 55: 3104-3111, 2006. (Pubitemid 44923649)
32. Knowlton AA, Connelly CM, Romo GM, Mamuya W, Apstein CS, Brecher P. Rapid expression of fibronectin in the rabbit heart after myocardial infarction with and without reperfusion. J Clin Invest 89: 1060-1068, 1992.
33. Kuppuswamy D, Kerr C, Narishige T, Kasi VS, Menick DR, Cooper GT. Association of tyrosine-phosphorylated c-Src with the cytoskeleton of hypertrophying myocardium. J Biol Chem 272: 4500-4508, 1997. (Pubitemid 27078529)
34. Lehenkari PP, Horton MA. Single integrin molecule adhesion forces in intact cells measured by atomic force microscopy. Biochem Biophys Res Commun 259: 645-650, 1999.
35. Li F, Redick SD, Erickson HP, Moy VT. Force measurements of the α5β1 integrin-fibronectin interaction. Biophys J 84: 1252-1262, 2003.
36. Lundgren E, Gullberg D, Rubin K, Borg TK, Terracio MJ, Terracio L. In vitro studies on adult cardiac myocytes: attachment and biosynthesis of collagen type IV and laminin. J Cell Physiol 136: 43-53, 1988.
37. Magnusson M, Mosher D. Fibronectin: structure, assembly, and cardio-vascular implications. Arterioscler Thromb Vasc Biol 18: 1363-1370, 1998.
38. Mamuya WS, Brecher P. Fibronectin expression in the normal and hypertrophic rat heart. J Clin Invest 89: 392-401, 1992.
39. Martin GR, Timpl R. Laminin and other basement membrane components. Annu Rev Cell Biol 3: 57-85, 1987.
40. McCrossan ZA, Billeter R, White E. Transmural changes in size, contractile and electrical properties of SHR left ventricular myocytes during compensated hypertrophy. Cardiovasc Res 63: 283-292, 2004. (Pubitemid 38900842)
41. McNamee HP, Ingber DE, Schwartz MA. Adhesion to fibronectin stimulates inositol lipid synthesis and enhances PDGF-induced inositol lipid breakdown. J Cell Biol 121: 673-678, 1993.
42. Miyamoto S, Akiyama SK, Yamada KM. Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function. Science 267: 883-885, 1995.
43. Miyamoto S, Teramoto H, Coso OA, Gutkind JS, Burbelo PD, Akiyama SK, Yamada KM. Integrin function: molecular hierarchies of cytoskeletal and signaling molecules. J Cell Biol 131: 791-805, 1995.
44. Moss RL, Fitzsimons DP. Frank-Starling relationship: long on importance, short on mechanism. Circ Res 90: 11-13, 2002.
45. Muller DJ, Helenius J, Alsteens D, Dufrene YF. Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5: 383-390, 2009.
46. Nagai T, Laser M, Baicu CF, Zile MR, Cooper Gt, Kuppuswamy D. β3-Integrin-mediated focal adhesion complex formation: adult cardiocytes embedded in three-dimensional polymer matrices. Am J Cardiol 83: 38H-43H, 1999. (Pubitemid 29330926)
47. Pardo JV, Siliciano JD, Craig SW. A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ("costameres") mark sites of attachment between myofibrils and sarcolemma. Proc Natl Acad Sci USA 80: 1008-1012, 1983.
48. Parzen E. On the estimation of a probability density and mode. Ann Math Stat 33: 1065-1076, 1962.
49. Ross RS. Molecular and mechanical synergy: cross-talk between integrins and growth factor receptors. Cardiovasc Res 63: 381-390, 2004.
50. Ross RS, Borg TK. Integrins and the myocardium. Circ Res 88: 1112-1119, 2001.
51. Rotsch C, Braet F, Wisse E, Radmacher M. AFM imaging and elasticity measurements on living rat liver macrophages. Cell Biol Int 21: 685-696, 1997. (Pubitemid 28454226)
52. Roy S, Sala R, Cagliero E, Lorenzi M. Overexpression of fibronectin induced by diabetes or high glucose: phenomenon with a memory. Proc Natl Acad Sci USA 87: 404-408, 1990. (Pubitemid 20033079)
53. 2+ currents in adherent guinea-pig cardiomyocytes. J Physiol 560: 403-411, 2004.
54. Ruwhof C, van der Laarse A. Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways. Cardiovasc Res 47: 23-37, 2000. (Pubitemid 30408547)
55. Sachs F. Mechanical transduction by ion channels: how forces reach the channel. Soc Gen Physiol Series 52: 209-218, 1997.
56. Sadoshima J, Izumo S. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev Physiol 59: 551-571, 1997. (Pubitemid 27142455)
57. Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechano-transduction. Am J Physiol Heart Circ Physiol 289: H2291-H2301, 2005.
58. Samuel JL, Barrieux A, Dufour S, Dubus I, Contard F, Koteliansky V, Farhadian F, Marotte F, Thiery JP, Rappaport L. Accumulation of fetal fibronectin mRNAs during the development of rat cardiac hypertrophy induced by pressure overload. J Clin Invest 88: 1737-1746, 1991.
59. Sarin V, Gaffin RD, Meininger GA, Muthuchamy M. Arginine-glycine- aspartic acid (RGD)-containing peptides inhibit the force production of mouse papillary muscle bundles via α5β1 integrin. J Physiol 564: 603-617, 2005. (Pubitemid 40585057)
60. Schmidt C, Pommerenke H, Durr F, Nebe B, Rychly J. Mechanical stressing of integrin receptors induces enhanced tyrosine phosphorylation of cytoskeletally anchored protein. J Biol Chem 273: 5081-5085, 1998. (Pubitemid 28108667)
61. Schwarzbauer JE. Fibronectin: from gene to protein. Curr Opin Cell Biol 3: 786-791, 1991.
62. Shroff SG, Saner DR, Lal R. Dynamic micromechanical properties of cultured rat atrial myocytes measured by atomic force microscopy. Am J Physiol Cell Physiol 269: C286-C292, 1995.
63. Siperstein MD, Unger RH, Madison LL. Studies of muscle capillary basement membranes in normal subjects, diabetic, and prediabetic patients. J Clin Invest 47: 1973-1999, 1968.
64. Smoak IW. Hyperglycemia-induced TGFβ and fibronectin expression in embryonic mouse heart. Dev Dyn 231: 179-189, 2004.
65. Sun M, Graham JS, Hegedus B, Marga F, Zhang Y, Forgacs G, Grandbois M. Multiple membrane tethers probed by atomic force microscopy. Biophys J 89: 4320-4329, 2005. (Pubitemid 41725650)
66. Sun M, Opavsky MA, Stewart DJ, Rabinovitch M, Dawood F, Wen WH, Liu PP. Temporal response and localization of integrins beta1 and beta3 in the heart after myocardial infarction: regulation by cytokines. Circulation 107: 1046-1052, 2003.
67. Sun Z, Martinez-Lemus LA, Hill MA, Meininger GA. Extracellular matrix-specific focal adhesions in vascular smooth muscle produce mechanically active adhesion sites. Am J Physiol Cell Physiol 295: C268-C278, 2008.
68. 1-integrin on vascular smooth muscle cells studied using atomic force microscopy. Am J Physiol Heart Circ Physiol 289: H2526-H2535, 2005.
69. Tagawa H, Wang N, Narishige T, Ingber DE, Zile MR, Cooper GT. Cytoskeletal mechanics in pressure-overload cardiac hypertrophy. Circ Res 80: 281-289, 1997. (Pubitemid 27058701)
70. Takagi J, Erickson HP, Springer TA. C-terminal opening mimics "inside-out" activation of integrin α5β1. Nat Struct Biol 8: 412-416, 2001.
71. Tavi P, Laine M, Weckstrom M, Ruskoaho H. Cardiac mechanotransduction: from sensing to disease and treatment. Trends Pharmacol Sci 22: 254-260, 2001. (Pubitemid 32411527)
72. Tong CW, Kolomenskii A, Lioubimov VA, Schuessler HA, Trache A, Granger HJ, Muthuchamy M. Measurements of the cross-bridge attachment/detachment process within intact sarcomeres by surface plasmon resonance. Biochemistry 40: 13915-13924, 2001. (Pubitemid 33078860)
73. Trache A, Trzeciakowski JP, Gardiner L, Sun Z, Muthuchamy M, Guo M, Yuan SY, Meininger GA. Histamine effects on endothelial cell fibronectin interaction studied by atomic force microscopy. Biophys J 89: 2888-2898, 2005. (Pubitemid 41401074)
74. Trial J, Rossen RD, Rubio J, Knowlton AA. Inflammation and ischemia: macrophages activated by fibronectin fragments enhance the survival of injured cardiac myocytes. Exp Biol Med (Maywood) 229: 538-545, 2004. (Pubitemid 38736323)
75. Ulrich MM, Janssen AM, Daemen MJ, Rappaport L, Samuel JL, Contard F, Smits JF, Cleutjens JP. Increased expression of fibronectin isoforms after myocardial infarction in rats. J Mol Cell Cardiol 29: 2533-2543, 1997. (Pubitemid 27404445)
76. Valencik ML, Zhang D, Punske B, Hu P, McDonald JA, Litwin SE. Integrin activation in the heart: a link between electrical and contractile dysfunction? Circ Res 99: 1403-1410, 2006. (Pubitemid 44949676)
77. Venables WN, Ripley BD. Modern Applied Statistics with S. New York: Springer, 2002.
78. Villarreal FJ, Dillmann WH. Cardiac hypertrophy-induced changes in mRNA levels for TGF-β1, fibronectin, and collagen. Am J Physiol Heart Circ Physiol 262: H1861-H1866, 1992.
79. Wang N, Butler JP, Ingber DE. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124-1127, 1993. (Pubitemid 23186787)
80. Weber K. Extracellular matrix remodeling in heart failure: a role for de novo angiotensin II generation. Circulation 96: 4065-4082, 1997. (Pubitemid 27506067)
81. Willems IE, Arends JW, Daemen MJ. Tenascin and fibronectin expression in healing human myocardial scars. J Pathol 179: 321-325, 1996. (Pubitemid 26266413)
82. Wolska BM, Solaro RJ. Methood for isolation of adult mouse cardiac myocytes for studies of contraction and microfluorimetry. Am J Physiol Heart Circ Physiol 271: H1250-H1255, 1996. (Pubitemid 126832345)
83. Wu X, Davis GE, Meininger GA, Wilson E, Davis MJ. Regulation of the L-type calcium channel by α5β1 integrin requires signaling between focal adhesion proteins. J Biol Chem 276: 30285-30292, 2001. (Pubitemid 37385111)
84. Wu X, Mogford JE, Platts SH, Davis GE, Meininger GA, Davis MJ. Modulation of calcium current in arteriolar smooth muscle by αvβ3 and α5β1 integrin ligands. J Cell Biol 143: 241-252, 1998.
85. + (BK) channels by α5β1 integrin activation in arteriolar smooth muscle. J Physiol 586: 1699-1713, 2008.