Journal of Molecular and Cellular Cardiology
Volume 43, Issue 2 , Pages 137-147 , August 2007

Stretch-induced MAP kinase activation in cardiac myocytes: Differential regulation through β1-integrin and focal adhesion kinase

Received 18 December 2006 ,Revised 8 May 2007 ,Accepted 14 May 2007.

References 

  1. Kudoh S, Komuro I, Hiroi Y, Zou Y, Harada K, Sugaya T, et al. Mechanical stretch induces hypertrophic responses in cardiac myocytes of angiotensin II type 1a receptor knockout mice. J. Biol. Chem. 1998;273:24037–24043
  2. Lammerding J, Kamm RD, Lee RT. Mechanotransduction in cardiac myocytes. Ann. N.Y. Acad. Sci. 2004;1015:53–70
  3. Sadoshima J, Izumo S. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu. Rev. Physiol. 1997;59:551–571
  4. Sadoshima J, Izumo S. Mechanical stretch rapidly activates multiple signal transduction pathways in cardiac myocytes: potential involvement of an autocrine/paracrine mechanism. EMBO J. 1993;12:1681–1692
  5. Yazaki Y, Komuro I. Role of protein kinase system in the signal transduction of stretch-mediated myocyte growth. Basic Res. Cardiol. 1992;87(Suppl. 2):11–18
  6. Laser M, Kasi VS, Hamawaki M, Cooper Gt, Kerr CM, Kuppuswamy D. Differential activation of p70 and p85 S6 kinase isoforms during cardiac hypertrophy in the adult mammal. J. Biol. Chem. 1998;273:24610–24619
  7. Aikawa R, Nagai T, Kudoh S, Zou Y, Tanaka M, Tamura M, et al. Integrins play a critical role in mechanical stress-induced p38-MAPK activation. Hypertension. 2002;39:233–238
  8. Komuro I, Kudo S, Yamazaki T, Zou Y, Shiojima I, Yazaki Y. Mechanical stretch activates the stress-activated protein kinases in cardiac myocytes. FASEB J. 1996;10:631–636
  9. Ruwhof C, van der Laarse A. Mechanical stress-induced cardiac hypertrophy: mechanisms and signal transduction pathways. Cardiovasc. Res. 2000;47:23–37
  10. Knoll R, Hoshijima M, Chien K. Cardiac mechanotransduction and implications for heart disease. J. Mol. Med. 2003;81:750–756
  11. Wernig F, Mayr M, Xu Q. Mechanical stretch-induced apoptosis in smooth muscle cells is mediated by beta1-integrin signaling pathways. Hypertension. 2003;41:903–911
  12. Brancaccio M, Hirsch E, Notte A, Selvetella G, Lembo G, Tarone G. Integrin signalling: the tug-of-war in heart hypertrophy. Cardiovasc. Res. 2006;70:422–433
  13. Ross RS, Pham C, Shai SY, Goldhaber JI, Fenczik C, Glembotski CC, et al. Beta1 integrins participate in the hypertrophic response of rat ventricular myocytes. Circ. Res. 1998;82:1160–1172
  14. Shai SY, Harpf AE, Babbitt CJ, Jordan MC, Fishbein MC, Chen J, et al. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res. 2002;90:458–464
  15. Jia N, Okamoto H, Shimizu T, Chiba S, Matsui Y, Sugawara T, et al. A newly developed angiotensin II type 1 receptor antagonist, CS866, promotes regression of cardiac hypertrophy by reducing integrin beta1 expression. Hypertens. Res. 2003;26:737–742
  16. Zou Y, Akazawa H, Qin Y, Sano M, Takano H, Minamino T, et al. Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat. Cell Biol. 2004;6:499–506
  17. Hanks SK, Calalb MB, Harper MC, Patel SK. Focal adhesion protein–tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc. Natl. Acad. Sci. U. S. A. 1992;89:8487–8491
  18. Wang HB, Dembo M, Hanks SK, Wang Y. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc. Natl. Acad. Sci. U. S. A. 2001;98:11295–11300
  19. Fonseca PM, Inoue RY, Kobarg CB, Crosara-Alberto DP, Kobarg J, Franchini KG. Targeting to C-terminal myosin heavy chain may explain mechanotransduction involving focal adhesion kinase in cardiac myocytes. Circ. Res. 2005;96:73–81
  20. Franchini KG, Torsoni AS, Soares PH, Saad MJ. Early activation of the multicomponent signaling complex associated with focal adhesion kinase induced by pressure overload in the rat heart. Circ. Res. 2000;87:558–565
  21. Laser M, Willey CD, Jiang W, Cooper Gt, Menick DR, Zile MR, et al. Integrin activation and focal complex formation in cardiac hypertrophy. J. Biol. Chem. 2000;275:35624–35630
  22. Domingos PP, Fonseca PM, Nadruz W, Franchini KG. Load-induced focal adhesion kinase activation in the myocardium: role of stretch and contractile activity. Am. J. Physiol., Heart Circ. Physiol. 2002;282:H556–H564
  23. Seko Y, Takahashi N, Tobe K, Kadowaki T, Yazaki Y. Pulsatile stretch activates mitogen-activated protein kinase (MAPK) family members and focal adhesion kinase (p125(FAK)) in cultured rat cardiac myocytes. Biochem. Biophys. Res. Commun. 1999;259:8–14
  24. Torsoni AS, Constancio SS, Nadruz W, Hanks SK, Franchini KG. Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ. Res. 2003;93:140–147
  25. Furuta Y, Ilic D, Kanazawa S, Takeda N, Yamamoto T, Aizawa S. Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene. 1995;11:1989–1995
  26. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature. 1995;377:539–544
  27. 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
  28. Pham CG, Harpf AE, Keller RS, Vu HT, Shai SY, Loftus JC, et al. Striated muscle-specific beta(1D)-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am. J. Physiol., Heart Circ. Physiol. 2000;279:H2916–H2926
  29. Fukuzawa J, Booz GW, Hunt RA, Shimizu N, Karoor V, Baker KM, et al. Cardiotrophin-1 increases angiotensinogen mRNA in rat cardiac myocytes through STAT3: an autocrine loop for hypertrophy. Hypertension. 2000;35:1191–1196
  30. Dostal DE, Booz GW, Baker KM. Regulation of angiotensinogen gene expression and protein in neonatal rat cardiac fibroblasts by glucocorticoid and beta-adrenergic stimulation. Basic Res. Cardiol. 2000;95:485–490
  31. Yano M, Kim S, Izumi Y, Yamanaka S, Iwao H. Differential activation of cardiac c-jun amino-terminal kinase and extracellular signal-regulated kinase in angiotensin II-mediated hypertension. Circ. Res. 1998;83:752–760
  32. Schlaepfer DD, Broome MA, Hunter T. Fibronectin-stimulated signaling from a focal adhesion kinase–c-Src complex: involvement of the Grb2, p130cas, and Nck adaptor proteins. Mol. Cell Biol. 1997;17:1702–1713
  33. Eble DM, Strait JB, Govindarajan G, Lou J, Byron KL, Samarel AM. Endothelin-induced cardiac myocyte hypertrophy: role for focal adhesion kinase. Am. J. Physiol., Heart Circ. Physiol. 2000;278:H1695–H1707
  34. Lin TH, Aplin AE, Shen Y, Chen Q, Schaller M, Romer L, et al. Integrin-mediated activation of MAP kinase is independent of FAK: evidence for dual integrin signaling pathways in fibroblasts. J. Cell Biol. 1997;136:1385–1395
  35. 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
  36. Sundberg LJ, Galante LM, Bill HM, Mack CP, Taylor JM. An endogenous inhibitor of focal adhesion kinase blocks Rac1/JNK but not Ras/ERK-dependent signaling in vascular smooth muscle cells. J. Biol. Chem. 2003;278:29783–29791
  37. Sawhney RS, Cookson MM, Omar Y, Hauser J, Brattain MG. Integrin alpha2-mediated ERK and calpain activation play a critical role in cell adhesion and motility via focal adhesion kinase signaling: identification of a novel signaling pathway. J. Biol. Chem. 2006;281:8497–8510
  38. Ueyama T, Kawashima S, Sakoda T, Rikitake Y, Ishida T, Kawai M, et al. Requirement of activation of the extracellular signal-regulated kinase cascade in myocardial cell hypertrophy. J. Mol. Cell Cardiol. 2000;32:947–960
  39. Clerk A, Sugden PH. Activation of protein kinase cascades in the heart by hypertrophic G protein-coupled receptor agonists. Am. J. Cardiol. 1999;83:64H–69H
  40. 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
  41. Ross RS. The extracellular connections: the role of integrins in myocardial remodeling. J. Card. Fail. 2002;8:S326–S331
  42. Wary KK, Mainiero F, Isakoff SJ, Marcantonio EE, Giancotti FG. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell. 1996;87:733–743
  43. Wary KK, Mariotti A, Zurzolo C, Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell. 1998;94:625–634
  44. Woodman SE, Park DS, Cohen AW, Cheung MW, Chandra M, Shirani J, et al. Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAPK cascade. J. Biol. Chem. 2002;277:38988–38997
  45. 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(4):H1488–H1496
  46. Qin J, Liu ZX. FAK-related nonkinase attenuates hypertrophy induced by angiotensin-II in cultured neonatal rat cardiac myocytes. Acta Pharmacol. Sin. 2006;27(9):1159–1164
  47. Lim Y, Han I, Jeon J, Park H, Bahk YY, Oh ES. Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J. Biol. Chem. 2004;279(28):29060–29065
  48. Boutahar N, Guignandon A, Vico L, Lafage-Proust MH. Mechanical strain on osteoblasts activates autophosphorylation of focal adhesion kinase and proline-rich tyrosine kinase 2 tyrosine sites involved in ERK activation. J. Biol. Chem. 2004;279(29):30588–30599
  49. Yamazaki T, Komuro I, Kudoh S, Zou Y, Shiojima I, Hiroi Y, et al Endothelin-1 is involved in mechanical stress-induced cardiomyocyte hypertrophy. J. Biol. Chem. 1996;271:3221–3228
  50. Yamada K, Green KG, Samarel AM, Saffitz JE. distinct pathways regulate expression of cardiac electrical and mechanical junction proteins in response to stretch. Circ. Res. 2005;97(4):346–353
  51. Lal H, Guleria RS, Foster DM, Lu G, Watson LE, Sanghi S, et al. Intergins: novel therapeutic targets for cardiovascular diseases. Cardiovasc. Hematol. Agents Med. Chem. 2007;5:109–132

PII: S0022-2828(07)01051-6

doi: 10.1016/j.yjmcc.2007.05.012

Journal of Molecular and Cellular Cardiology
Volume 43, Issue 2 , Pages 137-147 , August 2007