Serine-910 phosphorylation of focal adhesion kinase is critical for sarcomere reorganization in cardiomyocyte hypertrophy

Cardiovascular Research

Volumn 92, Issue 3, 2011, Pages 409-419

  Chu, Miensheng ^a   Iyengar, Rekha ^a   Koshman, Yevgeniya E ^a   Kim, Taehoon ^a   Russell, Brenda ^b   Martin, Jody L ^a   Heroux, Alain L ^a   Robia, Seth L ^a   Samarel, Allen M ^a  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Costamere; Dilated cardiomyopathy; Protein kinase C; Signal transduction; Src

Indexed keywords

ENDOTHELIN 1; FOCAL ADHESION KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE 5; PAXILLIN; PROTEIN KINASE C DELTA; PROTEIN KINASE P60; RAF PROTEIN; SERINE; SERINE 910; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVIADENOVIRUS; CELL SPREADING; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; COSTAMERE; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HEART LEFT VENTRICLE; HEART MUSCLE; HEART MUSCLE CELL; HEART TRANSPLANTATION; HEART VENTRICLE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SARCOMERE; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

ANGIOTENSIN II; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CARDIOMYOPATHY, DILATED; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIN-1; ENZYME ACTIVATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FOCAL ADHESION KINASE 1; HEART FAILURE; HUMANS; IMMUNOPRECIPITATION; INSULIN-LIKE GROWTH FACTOR I; MICROSCOPY, FLUORESCENCE; MUTATION; MYOCYTES, CARDIAC; PAXILLIN; PHENYLEPHRINE; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SARCOMERES; SERINE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TIME FACTORS; TRANSFECTION;

EID: 81055143965     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvr247     Document Type: Article

References (46)

1. Terracio L, Simpson DG, Hilenski L, Carver W, Decker RS, Vinson N et al. Distribution of vinculin in the Z-disk of striated muscle: analysis by laser scanning confocal microscopy. J Cell Physiol 1990;145:78-87.
2. Decker ML, Simpson DG, Behnke M, Cook MG, Decker RS. Morphological analysis of contracting and quiescent adult rabbit cardiac myocytes in long-term culture. Anat Rec 1990;227:285-299. (Pubitemid 20205719)
3. Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol 2005;289:H2291-H2301. (Pubitemid 41698534)
4. Domingos PP, Fonseca PM, Nadruz W Jr, 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. (Pubitemid 34654979)
5. Seko Y, Takahashi N, Sabe H, Tobe K, Kadowaki T, Nagai R. Hypoxia induces activation and subcellular translocation of focal adhesion kinase (p125FAK) in cultured rat cardiac myocytes. Biochem Biophys Res Commun 1999;262:290-296. (Pubitemid 29412662)
6. 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. (Pubitemid 43121807)
7. 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. (Pubitemid 44401455)
8. Peng X, Wu X, Druso JE, Wei H, Park AY, Kraus MS et al. Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc Natl Acad Sci USA 2008;105:6638-6643. (Pubitemid 351754559)
9. Quach NL, Rando TA. Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Dev Biol 2006;293:38-52.
10. 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. (Pubitemid 30395584)
11. Grigera PR, Jeffery ED, Martin KH, Shabanowitz J, Hunt DF, Parsons JT. FAK phosphorylation sites mapped by mass spectrometry. J Cell Sci 2005;118:4931-4935. (Pubitemid 41672425)
12. 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. (Pubitemid 32060574)
13. 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. (Pubitemid 40064899)
14. 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. (Pubitemid 43846081)
15. Sadoshima J, Izumo S. Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ Res 1993;73:413-423. (Pubitemid 23238726)
16. 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.
17. Taylor JM, Rovin JD, Parsons JT. A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes. J Biol Chem 2000;275:19250-19257. (Pubitemid 30422897)
18. Sugden PH, Clerk A. Endothelin signalling in the cardiac myocyte and its pathophysiological relevance. Curr Vasc Pharmacol 2005;3:343-351. (Pubitemid 41264286)
19. Garcia-Paramio P, Cabrerizo Y, Bornancin F, Parker PJ. The broad specificity of dominant inhibitory protein kinase C mutants infers a common step in phosphorylation. Biochem J 1998;333:631-636. (Pubitemid 28398530)
20. Whelan RD, Parker PJ. Loss of protein kinase C function induces an apoptotic response. Oncogene 1998;16:1939-1944. (Pubitemid 28200605)
21. Hunger-Glaser I, Fan RS, Perez-Salazar E, Rozengurt E. PDGF and FGF induce focal adhesion kinase (FAK) phosphorylation at Ser-910: dissociation from Tyr-397 phosphorylation and requirement for ERK activation. J Cell Physiol 2004;200:213-222. (Pubitemid 38880205)
22. 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. (Pubitemid 36830321)
23. Iijima Y, Laser M, Shiraishi H, Willey CD, Sundaravadivel B, Xu L et al. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem 2002;277:23065-23075. (Pubitemid 34967293)
24. Kovacic B, Ilic D, Damsky CH, Gardner DG. c-Src activation plays a role in endothelin-dependent hypertrophy of the cardiac myocyte. J Biol Chem 1998;273: 35185-35193. (Pubitemid 29028223)
25. Villa-Moruzzi E. Targeting of FAK Ser910 by ERK5 and PP1d in non-stimulated and phorbol ester-stimulated cells. Biochem J 2007;408:7-18. (Pubitemid 350158398)
26. Sun W, Wei X, Kesavan K, Garrington TP, Fan R, Mei J et al. MEK kinase 2 and the adaptor protein Lad regulate extracellular signal-regulated kinase 5 activation by epidermal growth factor via Src. Mol Cell Biol 2003;23:2298-2308. (Pubitemid 36351013)
27. Chien KR, Knowlton KU, Zhu H, Chien S. Regulation of cardiac gene expression during myocardial growth and hypertrophy: molecular studies of an adaptive physiologic response. FASEB J 1991;5:3037-3046. (Pubitemid 21892863)
28. Pham CG, Harpf AE, Keller RS, Vu HT, Shai SY, Loftus JC et al. Striated musclespecific b1D-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am J Physiol Heart Circ Physiol 2000;279:H2916-H2926. (Pubitemid 32005882)
29. 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. (Pubitemid 36919701)
30. 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. (Pubitemid 36706083)
31. Hein S, Kostin S, Heling A, Maeno Y, Schaper J. The role of the cytoskeleton in heart failure. Cardiovasc Res 2000;45:273-278. (Pubitemid 30069492)
32. Ito H, Hiroe M, Hirata Y, Fujisaki H, Adachi S, Akimoto H et al. Endothelin ETA receptor antagonist blocks cardiac hypertrophy provoked by hemodynamic overload. Circulation 1994;89:2198-2203.
33. Chiloeches A, Paterson HF, Marais R, Clerk A, Marshall CJ, Sugden PH. Regulation of Ras.GTP loading and Ras-Raf association in neonatal rat ventricular myocytes by G protein-coupled receptor agonists and phorbol ester. Activation of the extracellular signal-regulated kinase cascade by phorbol ester is mediated by Ras. J Biol Chem 1999; 274:19762-19770.
34. Hall KJ, Jones ML, Poole AW. Coincident regulation of PKCd in human platelets by phosphorylation of Tyr311 and Tyr565 and phospholipase C signalling. Biochem J 2007;406:501-509. (Pubitemid 47425456)
35. Rybin VO, Guo J, Gertsberg Z, Elouardighi H, Steinberg SF. Protein kinase C1 (PKC1) and Src control PKCd activation loop phosphorylation in cardiomyocytes. J Biol Chem 2007;282:23631-23638. (Pubitemid 47311967)
36. Sumandea MP, Rybin VO, Hinken AC, Wang C, Kobayashi T, Harleton E et al. Tyrosine phosphorylation modifies protein kinase Cd-dependent phosphorylation of cardiac troponin I. J Biol Chem 2008;283:22680-22689.
37. Rybin VO, Guo J, Harleton E, Feinmark SJ, Steinberg SF. Regulatory autophosphorylation sites on protein kinase C-d at threonine-141 and threonine-295. Biochemistry 2009;48:4642-4651.
38. Brandt DT, Goerke A, Heuer M, Gimona M, Leitges M, Kremmer E et al. Protein kinase Cd induces Src kinase activity via activation of the protein tyrosine phosphatase PTPa. J Biol Chem 2003;278:34073-34078. (Pubitemid 37553245)
39. Amos S, Martin PM, Polar GA, Parsons SJ, Hussaini IM. Phorbol 12-myristate 13-acetate induces epidermal growth factor receptor transactivation via protein kinase Cd/c-Src pathways in glioblastoma cells. J Biol Chem 2005;280:7729-7738. (Pubitemid 40349666)
40. 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. (Pubitemid 32938559)
41. Kehat I, Davis J, Tiburcy M, Accornero F, Saba-El-Leil MK, Maillet M et al. Extracellular signal-regulated kinases 1 and 2 regulate the balance between eccentric and concentric cardiac growth. Circ Res 2011;108:176-183.
42. Kovacic-Milivojevic B, Roediger F, Almeida EA, Damsky CH, Gardner DG, Ilic D. Focal adhesion kinase and p130Cas mediate both sarcomeric organization and activation of genes associated with cardiac myocyte hypertrophy. Mol Biol Cell 2001;12: 2290-2307. (Pubitemid 33051957)
43. Mansour H, deTombe PP, Samarel AM, Russell B. Restoration of resting sarcomere length after uniaxial static strain is regulated by protein kinase C1 and focal adhesion kinase. Circ Res 2004;94:642-649. (Pubitemid 38387747)
44. Subauste MC, Pertz O, Adamson ED, Turner CE, Junger S, Hahn KM. Vinculin modulation of paxillin-FAK interactions regulates ERK to control survival and motility. J Cell Biol 2004;165:371-381. (Pubitemid 38649912)
45. Conti FJ, Monkley SJ, Wood MR, Critchley DR, Muller U. Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junctions. Development 2009;136:3597-3606.
46. Zemljic-Harpf AE, Miller JC, Henderson SA, Wright AT, Manso AM, Elsherif L et al. Cardiac-myocyte-specific excision of the vinculin gene disrupts cellular junctions, causing sudden death or dilated cardiomyopathy. Mol Cell Biol 2007;27:7522-7537. (Pubitemid 350033658)