Cardiomyocyte-specific expression of CRNK, the C-terminal domain of PYK2, maintains ventricular function and slows ventricular remodeling in a mouse model of dilated cardiomyopathy

Journal of Molecular and Cellular Cardiology

Volumn 72, Issue , 2014, Pages 281-291

  Koshman, Yevgeniya E ^a   Chu, Miensheng ^a   Kim, Taehoon ^a   Kalmanson, Olivia ^a   Farjah, Mariam ^b   Kumar, Mohit ^a   Lewis, William ^c   Geenen, David L ^b   De Tombe, Pieter ^a   Goldspink, Paul H ^d   Solaro, R John ^b   Samarel, Allen M ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Echocardiography; Focal adhesion kinase; Gene expression; Heart failure; Protein kinase C

Indexed keywords

FOCAL ADHESION KINASE; FOCAL ADHESION KINASE 2; MYOSIN HEAVY CHAIN ALPHA; PROCOLLAGEN; PROCOLLAGEN TYPE 1; PROCOLLAGEN TYPE 3; PROTEIN KINASE C EPSILON; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SERCA2 PROTEIN; TROPONIN I; UNCLASSIFIED DRUG; MYH6 PROTEIN, MOUSE; MYOSIN HEAVY CHAIN; PTK2B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; CRNK GENE; DOWN REGULATION; ENZYME PHOSPHORYLATION; GENE; GENE EXPRESSION; GENETICALLY ENGINEERED MOUSE STRAIN; HEART DILATATION; HEART FAILURE; HEART LEFT VENTRICLE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE REMODELING; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SURVIVAL TIME; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; HEART VENTRICLE; HEART VENTRICLE FUNCTION; LONGEVITY; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; TRANSGENE;

ANIMALS; CARDIOMYOPATHY, DILATED; FOCAL ADHESION KINASE 2; GENE EXPRESSION REGULATION; HEART VENTRICLES; LONGEVITY; MICE; MICE, TRANSGENIC; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C-EPSILON; PROTEIN STRUCTURE, TERTIARY; TRANSGENES; VENTRICULAR FUNCTION; VENTRICULAR REMODELING;

EID: 84901357258     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.03.021     Document Type: Article

References (43)

1. Melendez J., Welch S., Schaefer E., Moravec C.S., Avraham S., Avraham H., et al. Activation of Pyk2/related focal adhesion tyrosine kinase and focal adhesion kinase in cardiac remodeling. J Biol Chem 2002, 277:45203-45210.
2. 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.
3. Bayer A.L., Ferguson A.G., Lucchesi P.A., Samarel A.M. Pyk2 expression and phosphorylation in neonatal and adult cardiomyocytes. J Mol Cell Cardiol 2001, 33:1017-1030.
4. Menashi E.B., Loftus J.C. Differential effects of Pyk2 and FAK on the hypertrophic response of cardiac myocytes. Cell Tissue Res 2009, 337:243-255.
5. Bayer A.L., Heidkamp M.C., Howes A.L., Heller Brown J., Byron K.L., Samarel A.M. Protein kinase Cε-dependent activation of proline-rich tyrosine kinase 2 in neonatal rat ventricular myocytes. J Mol Cell Cardiol 2003, 35:1121-1133.
6. 2+/calmodulin to FERM F2 α2 helix and thus forming its dimer. Biochem J 2008, 410:513-523.
7. Park S.Y., Avraham H.K., Avraham S. RAFTK/Pyk2 activation is mediated by trans-acting autophosphorylation in a Src-independent manner. J Biol Chem 2004, 279:33315-33322.
8. Blaukat A., Ivankovic-Dikic I., Gronroos E., Dolfi F., Tokiwa G., Vuori K., et al. Adaptor proteins Grb2 and Crk couple Pyk2 with activation of specific mitogen-activated protein kinase cascades. J Biol Chem 1999, 274:14893-14901.
9. Pandey P., Avraham S., Kumar S., Nakazawa A., Place A., Ghanem L., et al. Activation of p38 mitogen-activated protein kinase by PYK2/related adhesion focal tyrosine kinase-dependent mechanism. J Biol Chem 1999, 274:10140-10144.
10. Taniyama Y., Weber D.S., Rocic P., Hilenski L., Akers M.L., Park J., et al. Pyk2- and Src-dependent tyrosine phosphorylation of PDK1 regulates focal adhesions. Mol Cell Biol 2003, 23:8019-8029.
11. 1-Adrenergic receptors activate AKT via a Pyk2/PDK-1 pathway that is tonically inhibited by novel protein kinase C isoforms in cardiomyocytes. Circ Res 2006, 99:1367-1375.
12. Lang D., Glukhov A.V., Efimova T., Efimov I.R. Role of Pyk2 in cardiac arrhythmogenesis. Am J Physiol Heart Circ Physiol 2011, 301:H975-H983.
13. i production in cardiomyocytes via a FAK-dependent signaling pathway. J Signal Transduct 2012, 2012:473410.
14. 2+-ATPase gene expression in cultured neonatal rat heart cells. Am J Physiol 1996, 271:H1031-H1039.
15. Porter M.J., Heidkamp M.C., Scully B.T., Patel N., Martin J.L., Samarel A.M. Isoenzyme-selective regulation of SERCA2 gene expression by protein kinase C in neonatal rat ventricular myocytes. Am J Physiol Cell Physiol 2003, 285:C39-C47.
16. Heidkamp M.C., Scully B.T., Vijayan K., Engman S.J., Szotek E.L., Samarel A.M. PYK2 regulates SERCA2 gene expression in neonatal rat ventricular myocytes. Am J Physiol Cell Physiol 2005, 289:C471-C482.
17. Xiong W.C., Macklem M., Parsons J.T. Expression and characterization of splice variants of PYK2, a focal adhesion kinase-related protein. J Cell Sci 1998, 111:1981-1991.
18. Li X., Dy R.C., Cance W.G., Graves L.M., Earp H.S. Interactions between two cytoskeleton-associated tyrosine kinases: calcium-dependent tyrosine kinase and focal adhesion tyrosine kinase. J Biol Chem 1999, 274:8917-8924.
19. 11 signaling to GLUT4 glucose transporters. J Biol Chem 2001, 276:47751-47754.
20. MAPK activation in glomerular mesangial cells. J Biol Chem 2001, 276:21521-21528.
21. Watson J.M., Harding T.W., Golubovskaya V., Morris J.S., Hunter D., Li X., et al. Inhibition of the calcium-dependent tyrosine kinase (CADTK) blocks monocyte spreading and motility. J Biol Chem 2001, 276:3536-3542.
22. van Buul J.D., Anthony E.C., Fernandez-Borja M., Burridge K., Hordijk P.L. Proline-rich tyrosine kinase 2 (Pyk2) mediates vascular endothelial-cadherin-based cell-cell adhesion by regulating beta-catenin tyrosine phosphorylation. J Biol Chem 2005, 280:21129-21136.
23. Hart D.L., Heidkamp M.C., Iyengar R., Vijayan K., Szotek E.L., Barakat J.A., et al. CRNK gene transfer improves function and reverses the myosin heavy chain isoenzyme switch during post-myocardial infarction left ventricular remodeling. J Mol Cell Cardiol 2008, 45:93-105.
24. Goldspink P.H., Montgomery D.E., Walker L.A., Urboniene D., McKinney R.D., Geenen D.L., et al. Protein kinase Cε overexpression alters myofilament properties and composition during the progression of heart failure. Circ Res 2004, 95:424-432.
25. Schlaepfer D.D., Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol Cell Biol 1996, 16:5623-5633.
26. Koshman Y.E., Patel N., Chu M., Iyengar R., Kim T., Ersahin C., et al. Regulation of connective tissue growth factor gene expression and fibrosis in human heart failure. J Card Fail 2013, 19:283-294.
27. Melendez J., Turner C., Avraham H., Steinberg S.F., Schaefer E., Sussman M.A. Cardiomyocyte apoptosis triggered by RAFTK/Pyk2 via Src kinase is antagonized by paxillin. J Biol Chem 2004, 279:53516-53523.
28. Hinken A.C., Hanft L.M., Scruggs S.B., Sadayappan S., Robbins J., Solaro R.J., et al. Protein kinase C depresses cardiac myocyte power output and attenuates myofilament responses induced by protein kinase A. J Muscle Res Cell Motil 2012, 33:439-448.
29. Scruggs S.B., Walker L.A., Lyu T., Geenen D.L., Solaro R.J., Buttrick P.M., et al. Partial replacement of cardiac troponin I with a non-phosphorylatable mutant at serines 43/45 attenuates the contractile dysfunction associated with PKCε phosphorylation. J Mol Cell Cardiol 2006, 40:465-473.
30. Ping P., Zhang J., Pierce W.M., Bolli R. Functional proteomic analysis of protein kinase Cε signaling complexes in the normal heart and during cardioprotection. Circ Res 2001, 88:59-62.
31. Bayer A.L., Heidkamp M.C., Patel N., Porter M., Engman S., Samarel A.M. Alterations in protein kinase C isoenzyme expression and autophosphorylation during the progression of pressure overload-induced left ventricular hypertrophy. Mol Cell Biochem 2003, 242:145-152.
32. Montgomery D.E., Rundell V.L., Goldspink P.H., Urboniene D., Geenen D.L., de Tombe P.P., et al. Protein kinase Cε induces systolic cardiac failure marked by exhausted inotropic reserve and intact Frank-Starling mechanism. Am J Physiol Heart Circ Physiol 2005, 289:H1881-H1888.
33. Hankiewicz J.H., Goldspink P.H., Buttrick P.M., Lewandowski E.D. Principal strain changes precede ventricular wall thinning during transition to heart failure in a mouse model of dilated cardiomyopathy. Am J Physiol Heart Circ Physiol 2008, 294:H330-H336.
34. 2+-activated tension development in single adult cardiac myocytes. Circ Res 1999, 84:1310-1317.
35. Perez N.G., Hashimoto K., McCune S., Altschuld R.A., Marban E. Origin of contractile dysfunction in heart failure: calcium cycling versus myofilaments. Circulation 1999, 99:1077-1083.
36. Rundell V.L., Manaves V., Martin A.F., de Tombe P.P. Impact of β-myosin heavy chain isoform expression on cross-bridge cycling kinetics. Am J Physiol Heart Circ Physiol 2005, 288:H896-H903.
37. 2+-ATPase and calsequestrin gene expression in the heart. Can J Physiol Pharmacol 2012, 90:1017-1028.
38. 2+ homeostasis and cardiomyocyte function. J Biol Chem 2000, 275:38073-38080.
39. 2+-ATPase isoform 2 (SERCA2) gene. J Biol Chem 1999, 274:2556-2562.
40. Pena J.R., Szkudlarek A.C., Warren C.M., Heinrich L.S., Gaffin R.D., Jagatheesan G., et al. Neonatal gene transfer of SERCA2a delays onset of hypertrophic remodeling and improves function in familial hypertrophic cardiomyopathy. J Mol Cell Cardiol 2010, 49:993-1002.
41. Kawase Y., Ly H.Q., Prunier F., Lebeche D., Shi Y., Jin H., et al. Reversal of cardiac dysfunction after long-term expression of SERCA2a by gene transfer in a pre-clinical model of heart failure. J Am Coll Cardiol 2008, 51:1112-1119.
42. McDonough P.M., Stella S.L., Glembotski C.C. Involvement of cytoplasmic calcium and protein kinases in the regulation of atrial natriuretic factor secretion by contraction rate and endothelin. J Biol Chem 1994, 269:9466-9472.
43. 2+-sensitive tyrosine kinase Pyk2/CAKβ-dependent signaling is essential for G-protein-coupled receptor agonist-induced hypertrophy. J Mol Cell Cardiol 2004, 36:799-807.