Focal adhesion kinase governs cardiac concentric hypertrophic growth by activating the AKT and mTOR pathways

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 2, 2012, Pages 493-501

  Clemente, C F M Z ^b   Xavier Neto, J ^b   Dalla Costa, A P ^a   Consonni, S R ^a   Antunes, J E ^a   Rocco, S A ^b   Pereira, M B ^a   Judice, C C ^a   Strauss, B ^c   Joazeiro, P P ^a   Matos Souza, J R ^a   Franchini, K G ^a,b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cardiac failure; Cardiac myocytes; Mechanotransduction; Signal transduction; Transgenic mice

Indexed keywords

ANP PROTEIN; FOCAL ADHESION KINASE; FOCAL ADHESION KINASE INHIBITOR; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOCHONDRIAL DNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN HEAVY CHAIN BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE P85 SUBUNIT; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN KINASE B; PROTEIN SERCA2A; RAPAMYCIN; RPS6 KINASE; S6 KINASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SRC PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BODY WEIGHT; CELL SIZE; CONCENTRIC LEFT VENTRICULAR HYPERTROPHY; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; ENZYME ACTIVITY; GENE OVEREXPRESSION; HEART AFTERLOAD; HEART LEFT VENTRICLE; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE; HEART MUSCLE CELL; HEART RATE; HEART SIZE; KIDNEY MASS; LEFT VENTRICULAR END DIASTOLIC DIAMETER; LUNG WEIGHT; MOUSE; MUSCLE FIBRIL; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE WEIGHT; SYSTOLIC BLOOD PRESSURE; TRANSGENE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; CARDIOMEGALY; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION; GENE ORDER; GENETIC VECTORS; MALE; MICE; MICE, TRANSGENIC; MYOCARDIUM; MYOCYTES, CARDIAC; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

MUS; MUS MUSCULUS;

EID: 84855984472     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.10.015     Document Type: Article

References (40)

1. Grossman W., Jones D., McLaurin L.P. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest 1975, 56:56-64.
2. Russell B., Curtis M.W., Koshman Y.E., Samarel A.M. Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width. J Mol Cell Cardiol 2010, 48:817-823.
3. Berenji K., Drazner M.H., Rothermel B.A., Hill J.A. Does load-induced ventricular hypertrophy progress to systolic heart failure?. Am J Physiol Heart Circ Physiol 2005, 289:H8-H16.
4. Gerdes A.M., Onodera T., Wang X., McCune S.A. Myocyte remodeling during the progression to failure in rats with hypertension. Hypertension 1996, 28:609-614.
5. Heineke J., Molkentin J.D. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006, 7:589-600.
6. Parsons J.T. Focal adhesion kinase: the first ten years. J Cell Sci 2003, 116:1409-1416.
7. Torsoni A.S., Constancio S.S., Nadruz W., Hanks S.K., Franchini K.G. Focal adhesion kinase is activated and mediates the early hypertrophic response to stretch in cardiac myocytes. Circ Res 2003, 93:140-147.
8. Marin T.M., Clemente C.F., Santos A.M., Picardi P.K., Pascoal V.D., Lopes-Cendes I., et al. Shp2 negatively regulates growth in cardiomyocytes by controlling focal adhesion kinase/Src and mTOR pathways. Circ Res 2008, 103:813-824.
9. Taylor J.M., Rovin J.D., Parsons J.T. A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes. J Biol Chem 2000, 275:19250-19257.
10. Eble D.M., Strait J.B., Govindarajan G., Lou J., Byron K.L., Samarel A.M. Endothelin-induced cardiac myocyte hypertrophy: role for focal adhesion kinase. Am J Physiol Heart Circ Physiol 2000, 278:H1695-H1707.
11. Lopes M.M., Ribeiro G.C., Tornatore T.F., Clemente C.F., Teixeira V.P., Franchini K.G. Increased expression and phosphorylation of focal adhesion kinase correlates with dysfunction in the volume-overloaded human heart. Clin Sci (Lond) 2007, 113:195-204.
12. Clemente C.F., Tornatore T.F., Theizen T.H., Deckmann A.C., Pereira T.C., Lopes-Cendes I., et al. Targeting focal adhesion kinase with small interfering RNA prevents and reverses load-induced cardiac hypertrophy in mice. Circ Res 2007, 101:1339-1348.
13. Bayer A.L., Heidkamp M.C., Patel N., Porter M.J., Engman S.J., Samarel A.M. PYK2 expression and phosphorylation increases in pressure overload-induced left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 2002, 283:H695-H706.
14. Peng X., Kraus M.S., Wei H., Shen T.L., 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.
15. DiMichele L.A., Doherty J.T., Rojas M., Beggs H.E., Reichardt L.F., Mack C.P., et al. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ Res 2006, 99:636-645.
16. Lois C., Hong E.J., Pease S., Brown E.J., Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 2002, 295:868-872.
17. Rindt H., Gulick J., Knotts S., Neumann J., Robbins J. In vivo analysis of the murine beta-myosin heavy chain gene promoter. J Biol Chem 1993, 268:5332-5338.
18. Zhao X., Peng X., Sun S., Park A.Y., Guan J.L. Role of kinase-independent and -dependent functions of FAK in endothelial cell survival and barrier function during embryonic development. J Cell Biol 2010, 189:955-965.
19. Slack-Davis J.K., Martin K.H., Tilghman R.W., Iwanicki M., Ung E.J., Autry C., et al. Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 2007, 282:14845-14852.
20. Calalb M.B., Polte T.R., Hanks S.K. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 1995, 15:954-963.
21. Schlaepfer D.D., Hunter T. Focal adhesion kinase overexpression enhances ras-dependent integrin signaling to ERK2/mitogen-activated protein kinase through interactions with and activation of c-Src. J Biol Chem 1997, 272:13189-13195.
22. Chen H.C., Guan J.L. Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc Natl Acad Sci U S A 1994, 91:10148-10152.
23. Shioi T., Kang P.M., Douglas P.S., Hampe J., Yballe C.M., Lawitts J., et al. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J 2000, 19:2537-2548.
24. McMullen J.R., Shioi T., Zhang L., Tarnavski O., Sherwood M.C., Kang P.M., et al. Phosphoinositide 3-kinase(p110alpha) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc Natl Acad Sci U S A 2003, 100:12355-12360.
25. Luo J., McMullen J.R., Sobkiw C.L., Zhang L., Dorfman A.L., Sherwood M.C., et al. Class IA phosphoinositide 3-kinase regulates heart size and physiological cardiac hypertrophy. Mol Cell Biol 2005, 25:9491-9502.
26. Ceci M., Ross J., Condorelli G. Molecular determinants of the physiological adaptation to stress in the cardiomyocyte: a focus on AKT. J Mol Cell Cardiol 2004, 37:905-912.
27. Inoki K., Li Y., Xu T., Guan K.L. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 2003, 17:1829-1834.
28. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
29. Ma X.M., Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 2009, 10:307-318.
30. Senyo S.E., Koshman Y.E., Russell B. Stimulus interval, rate and direction differentially regulate phosphorylation for mechanotransduction in neonatal cardiac myocytes. FEBS Lett 2007, 581:4241-4247.
31. Franchini K.G., Torsoni A.S., Soares P.H., Saad M.J. 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.
32. Fonseca P.M., Inoue R.Y., Kobarg C.B., Crosara-Alberto D.P., Kobarg J., Franchini K.G. Targeting to C-terminal myosin heavy chain may explain mechanotransduction involving focal adhesion kinase in cardiac myocytes. Circ Res 2005, 96:73-81.
33. Shai S.Y., Harpf A.E., Babbitt C.J., Jordan M.C., Fishbein M.C., 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.
34. Peng X., Wu X., Druso J.E., Wei H., Park A.Y., Kraus M.S., et al. Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc Natl Acad Sci U S A 2008, 105:6638-6643.
35. Hakim Z.S., DiMichele L.A., Doherty J.T., Homeister J.W., Beggs H.E., Reichardt L.F., 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.
36. Manning B.D., Tee A.R., Logsdon M.N., Blenis J., Cantley L.C. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 2002, 10:151-162.
37. Gan B., Yoo Y., Guan J.L. Association of focal adhesion kinase with tuberous sclerosis complex 2 in the regulation of s6 kinase activation and cell growth. J Biol Chem 2006, 281:37321-37329.
38. DeBosch B., Treskov I., Lupu T.S., Weinheimer C., Kovacs A., Courtois M., et al. Akt1 is required for physiological cardiac growth. Circulation 2006, 113:2097-2104.
39. Condorelli G., Drusco A., Stassi G., Bellacosa A., Roncarati R., Iaccarino G., et al. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc Natl Acad Sci U S A 2002, 99:12333-12338.
40. Oudit G.Y., Sun H., Kerfant B.G., Crackower M.A., Penninger J.M., Backx P.H. The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease. J Mol Cell Cardiol 2004, 37:449-471.