Table of Contents
Journal of Signal Transduction
Volume 2011, Article ID 521742, 8 pages
http://dx.doi.org/10.1155/2011/521742
Review Article

Integrins Are the Necessary Links to Hypertrophic Growth in Cardiomyocytes

1Cardiology Division, Department of Medicine, Gazes Cardiac Research Institute, Medical University of South Carolina, Charleston, SC 29425-2221, USA
2Advanced BioScience Laboratories, Inc., 5510 Nicholson Lane, Kensington, MD 20895, USA

Received 21 October 2010; Accepted 15 December 2010

Academic Editor: Wan-Wan Lin

Copyright © 2011 Rebecca K. Harston and Dhandapani Kuppuswamy. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Frey and E. N. Olson, “Cardiac hypertrophy: the good, the bad, and the ugly,” Annual Review of Physiology, vol. 65, pp. 45–79, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Ruwhof and A. van der Laarse, “Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways,” Cardiovascular Research, vol. 47, no. 1, pp. 23–37, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. W. J. Tuxworth, H. Shiraishi, P. C. Moschella, K. Yamane, P. J. McDermott, and D. Kuppuswamy, “Translational activation of 5-TOP mRNA in pressure overload myocardium,” Basic Research in Cardiology, vol. 103, no. 1, pp. 41–53, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. H. E. Morgan and C. J. Beinlich, “Contributions of increased efficiency and capacity of protein synthesis to rapid cardiac growth,” Molecular and Cellular Biochemistry, vol. 176, no. 1-2, pp. 145–151, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. X. Wang, F. L. Chow, T. Oka et al., “Matrix metalloproteinase-7 and ADAM-12 (a disintegrin and metalloproteinase-12) define a signaling axis in agonist-induced hypertension and cardiac hypertrophy,” Circulation, vol. 119, no. 18, pp. 2480–2489, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Cooper, R. L. Kent, C. E. Uboh, E. W. Thompson, and T. A. Marino, “Hemodynamic versus adrenergic control of cat right ventricular hypertrophy,” Journal of Clinical Investigation, vol. 75, no. 5, pp. 1403–1414, 1985. View at Google Scholar · View at Scopus
  7. D. Kuppuswamy, C. Kerr, T. Narishige, V. S. Kasi, D. R. Menick, and G. Cooper, “Association of tyrosine-phosphorylated c-Src with the cytoskeleton of hypertrophying myocardium,” Journal of Biological Chemistry, vol. 272, no. 7, pp. 4500–4508, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. J. I. Sadoshima, L. Jahn, T. Takahashi, T. J. Kulik, and S. Izumo, “Molecular characterization of the stretch-induced adaptation of cultured cardiac cells. An in vitro model of load-induced cardiac hypertrophy,” Journal of Biological Chemistry, vol. 267, no. 15, pp. 10551–10560, 1992. View at Google Scholar · View at Scopus
  9. I. Komuro, T. Kaida, Y. Shibazaki et al., “Stretching cardiac myocytes stimulates protooncogene expression,” Journal of Biological Chemistry, vol. 265, no. 7, pp. 3595–3598, 1990. View at Google Scholar · View at Scopus
  10. Y. Kira, T. Nakaoka, E. Hashimoto, F. Okabe, S. Asano, and I. Sekine, “Effect of long-term cyclic mechanical load on protein synthesis and morphological changes in cultured myocardial cells from neonatal rat,” Cardiovascular Drugs and Therapy, vol. 8, no. 2, pp. 251–262, 1994. View at Publisher · View at Google Scholar · View at Scopus
  11. R. S. Ross and T. K. Borg, “Integrins and the myocardium,” Circulation Research, vol. 88, no. 11, pp. 1112–1119, 2001. View at Google Scholar · View at Scopus
  12. R. O. Hynes, “Integrins: bidirectional, allosteric signaling machines,” Cell, vol. 110, no. 6, pp. 673–687, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. J. Q. Zhang, B. Elzey, G. Williams, S. Lu, D. J. Law, and R. Horowits, “Ultrastructural and biochemical localization of N-RAP at the interface between myofibrils and intercalated disks in the mouse heart,” Biochemistry, vol. 40, no. 49, pp. 14898–14906, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. T. K. Borg, E. C. Goldsmith, R. Price, W. Carver, L. Terracio, and A. M. Samarel, “Specialization at the Z line of cardiac myocytes,” Cardiovascular Research, vol. 46, no. 2, pp. 277–285, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Brancaccio, S. Guazzone, N. Menini et al., “Melusin is a new muscle-specific interactor for β1 integrin cytoplasmic domain,” Journal of Biological Chemistry, vol. 274, no. 41, pp. 29282–29288, 1999. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Wehrle-Haller and B. A. Imhof, “Integrin-dependent pathologies,” Journal of Pathology, vol. 200, no. 4, pp. 481–487, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Matsushita, M. Oyamada, K. Fujimoto et al., “Remodeling of cell-cell and cell-extracellular matrix interactions at the border zone of rat myocardial infarcts,” Circulation Research, vol. 85, no. 11, pp. 1046–1055, 1999. View at Google Scholar · View at Scopus
  18. C. J. Babbitt, S. Y. Shai, A. E. Harpf, C. G. Pham, and R. S. Ross, “Modulation of integrins and integrin signaling molecules in the pressure-loaded murine ventricle,” Histochemistry and Cell Biology, vol. 118, no. 6, pp. 431–439, 2002. View at Google Scholar · View at Scopus
  19. C. D. Willey, S. Balasubramanian, M. C. Rodríguez Rosas, R. S. Ross, and D. Kuppuswamy, “Focal complex formation in adult cardiomyocytes is accompanied by the activation of β3 integrin and c-Src,” Journal of Molecular and Cellular Cardiology, vol. 35, no. 6, pp. 671–683, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. R. K. Johnston, S. Balasubramanian, H. Kasiganesan, C. F. Baicu, M. R. Zile, and D. Kuppuswamy, “β3 integrin-mediated ubiquitination activates survival signaling during myocardial hypertrophy,” FASEB Journal, vol. 23, no. 8, pp. 2759–2771, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Nagai, M. Laser, C. F. Baicu, M. R. Zile, G. Cooper, and D. Kuppuswamy, “β3-integrin-mediated focal adhesion complex formation: adult cardiocytes embedded in three-dimensional polymer matrices,” American Journal of Cardiology, vol. 83, no. 12A, pp. 38H–43H, 1999. View at Google Scholar · View at Scopus
  22. M. Laser, C. D. Willey, W. Jiang et al., “Integrin activation and focal complex formation in cardiac hypertrophy,” Journal of Biological Chemistry, vol. 275, no. 45, pp. 35624–35630, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. R. S. Ross, C. Pham, S. Y. Shai et al., “β1 Integrins participate in the hypertrophic response of rat ventricular myocytes,” Circulation Research, vol. 82, no. 11, pp. 1160–1172, 1998. View at Google Scholar · View at Scopus
  24. E. Ogawa, Y. Saito, M. Harada et al., “Outside-in signalling of fibronectin stimulates cardiomyocyte hypertrophy in cultured neonatal rat ventricular myocytes,” Journal of Molecular and Cellular Cardiology, vol. 32, no. 5, pp. 765–776, 2000. View at Publisher · View at Google Scholar · View at Scopus
  25. L. K. Hornberger, S. Singhroy, T. Cavalle-Garrido, W. Tsang, F. Keeley, and M. Rabinovitch, “Synthesis of extracellular matrix and adhesion through β1 integrins are critical for fetal ventricular myocyte proliferation,” Circulation Research, vol. 87, no. 6, pp. 508–515, 2000. View at Google Scholar · View at Scopus
  26. S. P. Blatti, D. N. Foster, G. Ranganathan, H. L. Moses, and M. J. Getz, “Induction of fibronectin gene transcription and mRNA is a primary response to growth-factor stimulation of AKR-2B cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 4, pp. 1119–1123, 1988. View at Google Scholar · View at Scopus
  27. R. P. Ryseck, H. MacDonald-Bravo, M. Zerial, and R. Bravo, “Coordinate induction of fibronectin, fibronectin receptor, tropomyosin, and actin genes in serum-stimulated fibroblasts,” Experimental Cell Research, vol. 180, no. 2, pp. 537–545, 1989. View at Google Scholar · View at Scopus
  28. L. Terracio, K. Rubin, D. Gullberg et al., “Expression of collagen binding integrins during cardiac development and hypertrophy,” Circulation Research, vol. 68, no. 3, pp. 734–744, 1991. View at Google Scholar · View at Scopus
  29. P. Krishnamurthy, V. Subramanian, M. Singh, and K. Singh, “β1 integrins modulate β-adrenergic receptor-stimulated cardiac myocyte apoptosis and myocardial remodeling,” Hypertension, vol. 49, no. 4, pp. 865–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Menon, J. N. Johnson, R. S. Ross, M. Singh, and K. Singh, “Glycogen synthase kinase-3β plays a pro-apoptotic role in β-adrenergic receptor-stimulated apoptosis in adult rat ventricular myocytes: role of β1 integrins,” Journal of Molecular and Cellular Cardiology, vol. 42, no. 3, pp. 653–661, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. X. Yutao, W. Geru, B. Xiaojun, G. Tao, and M. Aiqun, “Mechanical stretch-induced hypertrophy of neonatal rat ventricular myocytes is mediated by β1-integrin-microtubule signaling pathways,” European Journal of Heart Failure, vol. 8, no. 1, pp. 16–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Balasubramanian and D. Kuppuswamy, “RGD-containing peptides activate S6K1 through β3 integrin in adult cardiac muscle cells,” Journal of Biological Chemistry, vol. 278, no. 43, pp. 42214–42224, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. R. K. Johnston, S. Balasubramanian, H. Kasiganesan, C. F. Baicu, M. R. Zile, and D. Kuppuswamy, “β3 integrin-mediated ubiquitination activates survival signaling during myocardial hypertrophy,” FASEB Journal, vol. 23, no. 8, pp. 2759–2771, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Singh, M. Roginskaya, S. Dalal et al., “Extracellular ubiquitin inhibits β-AR-stimulated apoptosis in cardiac myocytes: role of GSK-3β and mitochondrial pathways,” Cardiovascular Research, vol. 86, no. 1, pp. 20–28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Iijima, M. Laser, H. Shiraishi et al., “c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells,” Journal of Biological Chemistry, vol. 277, no. 25, pp. 23065–23075, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. K. von Wnuck Lipinski, P. Keul, N. Ferri et al., “Integrin-mediated transcriptional activation of inhibitor of apoptosis proteins protects smooth muscle cells against apoptosis induced by degraded collagen,” Circulation Research, vol. 98, no. 12, pp. 1490–1497, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. S. K. Sastry and K. Burridge, “Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics,” Experimental Cell Research, vol. 261, no. 1, pp. 25–36, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. H. C. Chen, P. A. Appeddu, H. Isoda, and J. L. Guan, “Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase,” Journal of Biological Chemistry, vol. 271, no. 42, pp. 26329–26334, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. M. C. Heidkamp, A. L. Bayer, B. T. Scully, D. M. Eble, and A. M. Samarel, “Activation of focal adhesion kinase by protein kinase Cε in neonatal rat ventricular myocytes,” American Journal of Physiology, vol. 285, no. 4, pp. H1684–H1696, 2003. View at Google Scholar · View at Scopus
  40. J. L. Guan, J. E. Trevithick, and R. O. Hynes, “Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein,” Cell Regulation, vol. 2, no. 11, pp. 951–964, 1991. View at Google Scholar · View at Scopus
  41. M. D. Schaller, J. D. Hildebrand, J. D. Shannon, J. W. Fox, R. R. Vines, and J. T. Parsons, “Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src,” Molecular and Cellular Biology, vol. 14, no. 3, pp. 1680–1688, 1994. View at Google Scholar · View at Scopus
  42. G. G. Choudhury, F. Marra, and H. E. Abboud, “Thrombin stimulates association of src homology domain containing adaptor protein Nek with pp125,” American Journal of Physiology, vol. 270, no. 2, pp. F295–F300, 1996. View at Google Scholar · View at Scopus
  43. K. G. Franchini, A. S. Torsoni, P. H. A. Soares, and M. J. A. Saad, “Early activation of the multicomponent signaling complex associated with focal adhesion kinase induced by pressure overload in the rat heart,” Circulation Research, vol. 87, no. 7, pp. 558–565, 2000. View at Google Scholar · View at Scopus
  44. A. S. Torsoni, S. S. Constancio, W. Nadruz, S. K. Hanks, and K. G. Franchini, “Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes,” Circulation Research, vol. 93, no. 2, pp. 140–147, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Ussar, H. V. Wang, S. Linder, R. Fässler, and M. Moser, “The Kindlins: subcellular localization and expression during murine development,” Experimental Cell Research, vol. 312, no. 16, pp. 3142–3151, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Tu, S. Wu, X. Shi, KA. Chen, and C. Wu, “Migfilin and Mig-2 link focal adhesions to filamin and the actin cytoskeleton and function in cell shape modulation,” Cell, vol. 113, no. 1, pp. 37–47, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. J. J. Dowling, E. Gibbs, M. Russell et al., “Kindlin-2 is an essential component of intercalated discs and is required for vertebrate cardiac structure and function,” Circulation Research, vol. 102, no. 4, pp. 423–431, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. C. J. Hatcher and C. T. Basson, “Disrupted intercalated discs: is kindlin-2 required?” Circulation Research, vol. 102, no. 4, pp. 392–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. G. E. Hannigan, J. G. Coles, and S. Dedhar, “Integrin-linked kinase at the heart of cardiac contractility, repair, and disease,” Circulation Research, vol. 100, no. 10, pp. 1408–1414, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Brancaccio, L. Fratta, A. Notte et al., “Melusin, a muscle-specific integrin β-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload,” Nature Medicine, vol. 9, no. 1, pp. 68–75, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Menon, M. Singh, R. S. Ross, J. N. Johnson, and K. Singh, “β-adrenergic receptor-stimulated apoptosis in adult cardiac myocytes involves MMP-2-mediated disruption of β integrin signaling and mitochondrial pathway,” American Journal of Physiology, vol. 290, no. 1, pp. C254–C261, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. J. T. Peterson, H. Hallak, L. Johnson et al., “Matrix metalloproteinase inhibition attenuates left ventricular remodeling and dysfunction in a rat model of progressive heart failure,” Circulation, vol. 103, no. 18, pp. 2303–2309, 2001. View at Google Scholar · View at Scopus
  53. M. De Acetis, A. Notte, F. Accornero et al., “Cardiac overexpression of melusin protects from dilated cardiomyopathy due to long-standing pressure overload,” Circulation Research, vol. 96, no. 10, pp. 1087–1094, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. D. P. Crosara-Alberto, R. Y. Inoue, and C. R. C. Costa, “FAK signalling mediates NF-κB activation by mechanical stress in cardiac myocytes,” Clinica Chimica Acta, vol. 403, no. 1-2, pp. 81–86, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Li, T. Ha, X. Gao et al., “NF-κ activation is required for the development of cardiac hypertrophy in vivo,” American Journal of Physiology, vol. 287, no. 4, pp. H1712–H1720, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. E. Choi, M. Butterworth, S. Malladi, C. S. Duckett, G. M. Cohen, and S. B. Bratton, “The E3 ubiquitin ligase cIAP1 binds and ubiquitinates caspase-3 and -7 via unique mechanisms at distinct steps in their processing,” Journal of Biological Chemistry, vol. 284, no. 19, pp. 12772–12782, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Balasubramanian, S. Mani, H. Shiraishi et al., “Enhanced ubiquitination of cytoskeletal proteins in pressure overloaded myocardium is accompanied by changes in specific E3 ligases,” Journal of Molecular and Cellular Cardiology, vol. 41, no. 4, pp. 669–679, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. C. A. P. Joazeiro, S. S. Wing, H. K. Huang, J. D. Leverson, T. Hunter, and Y. C. Liu, “The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase,” Science, vol. 286, no. 5438, pp. 309–312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  59. R. J. Lefkowitz, “G protein-coupled receptors: III. New roles for receptor kinases and β-arrestins in receptor signaling and desensitization,” Journal of Biological Chemistry, vol. 273, no. 30, pp. 18677–18680, 1998. View at Publisher · View at Google Scholar · View at Scopus