β3 Integrin-mediated ubiquitination activates survival signaling during myocardial hypertrophy

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2759-2771

  Johnston, Rebecca K ^a   Balasubramanian, Sundaravadivel ^a   Kasiganesan, Harinath ^a   Baicu, Catalin F ^a   Zile, Michael R ^a,b   Kuppuswamy, Dhandapani ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

cIAP1; NF B; Pressure overload

Indexed keywords

BETA3 INTEGRIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIGASE; ARGINYL-GLYCYL-ASPARTIC ACID; ARGINYLGLYCYLASPARTIC ACID; I KAPPA B; INHIBITOR OF APOPTOSIS PROTEIN; OLIGOPEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; GROWTH PERIOD; HEART MUSCLE CELL; HEART VENTRICLE FUNCTION; HEART VENTRICLE HYPERTROPHY; MECHANOTRANSDUCTION; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; UBIQUITINATION; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; C57BL MOUSE; CARDIOMEGALY; CAT; CELL CULTURE; DRUG EFFECT; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

MUS;

ANIMALS; CARDIOMEGALY; CATS; CELL SURVIVAL; CELLS, CULTURED; I-KAPPA B PROTEINS; INHIBITOR OF APOPTOSIS PROTEINS; INTEGRIN BETA3; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; NF-KAPPA B; OLIGOPEPTIDES; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; UBIQUITINATION;

EID: 68849083046     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-127480     Document Type: Article

References (49)

1. Wencker, D., Chandra, M., Nguyen, K., Miao, W., Garantziotis, S., Factor, S. M., Shirani, J., Armstrong, R. C., and Kitsis, R. N. (2003) A mechanistic role for cardiac myocyte apoptosis in heart failure. J. Clin. Invest. 111, 1497-1504 (Pubitemid 38063282)
2. Sarkar, S., Chawla-Sarkar, M., Young, D., Nishiyama, K., Rayborn, M. E., Hollyfield, J. G., and Sen, S. (2004) Myocardial cell death and regeneration during progression of cardiac hypertrophy to heart failure. J. Biol. Chem. 279, 52630-52642 (Pubitemid 39656639)
3. Narula, J., Haider, N., Virmani, R., DiSalvo, T. G., Kolodgie, F. D., Hajjar, R. J., Schmidt, U., Semigran, M. J., Dec, G. W., and Khaw, B. A. (1996) Apoptosis in myocytes in end-stage heart failure. N. Engl. J. Med. 335, 1182-1189 (Pubitemid 26339772)
4. Olivetti, G., Abbi, R., Quaini, F., Kajstura, J., Cheng, W., Nitahara, J. A., Quaini, E., Di Loreto, C., Beltrami, C. A., Krajewski, S., Reed, J. C., and Anversa, P. (1997) Apoptosis in the failing human heart. N. Engl. J. Med. 336, 1131-1141
5. Hedhli, N., Pelat, M., and Depre, C. (2005) Protein turnover in cardiac cell growth and survival. Cardiovasc. Res. 68, 186-196 (Pubitemid 41428415)
6. Depre, C., Wang, Q., Yan, L., Hedhli, N., Peter, P., Chen, L., Hong, C., Hittinger, L., Ghaleh, B., Sadoshima, J., Vatner, D. E., Vatner, S. F., and Madura, K. (2006) Activation of the cardiac proteasome during pressure overload promotes ventricular hypertrophy. Circulation 114, 1821-1828 (Pubitemid 44673357)
7. Weekes, J., Morrison, K., Mullen, A., Wait, R., Barton, P., and Dunn, M. J. (2003) Hyperubiquitination of proteins in dilated cardiomyopathy. Proteomics 3, 208-216
8. Kostin, S., Pool, L., Elsasser, A., Hein, S., Drexler, H. C., Arnon, E., Hayakawa, Y., Zimmermann, R., Bauer, E., Klovekorn, W. P., and Schaper, J. (2003) Myocytes die by multiple mechanisms in failing human hearts. Circ. Res. 92, 715-724 (Pubitemid 36457635)
9. Tsukamoto, O., Minamino, T., Okada, K., Shintani, Y., Takashima, S., Kato, H., Liao, Y., Okazaki, H., Asai, M., Hirata, A., Fujita, M., Asano, Y., Yamazaki, S., Asanuma, H., Hori, M., and Kitakaze, M. (2006) Depression of proteasome activities during the progression of cardiac dysfunction in pressureoverloaded heart of mice. Biochem. Biophys. Res. Commun. 340, 1125-1133 (Pubitemid 43083395)
10. Hu, S., and Yang, X. (2003) Cellular inhibitor of apoptosis 1 and 2 are ubiquitin ligases for the apoptosis inducer Smac/DIABLO. J. Biol. Chem. 278, 10055-10060 (Pubitemid 36800260)
11. Bertrand, M. J., Milutinovic, S., Dickson, K. M., Ho, W. C., Boudreault, A., Durkin, J., Gillard, J. W., Jaquith, J. B., Morris, S. J., and Barker, P. A. (2008) cIAP1 and cIAP2 facilitate cancer cell survival by functioning as E3 ligases that promote RIP1 ubiquitination. Mol. Cell. 30, 689-700 (Pubitemid 351818251)
12. Fang, S., Jensen, J. P., Ludwig, R. L., Vousden, K. H., and Weissman, A. M. (2000) Mdm2 is a RING finger-dependent ubiquitin protein ligase for itself and p53. J. Biol. Chem. 275, 8945-8951 (Pubitemid 30180252)
13. Balasubramanian, S., Mani, S., Shiraishi, H., Johnston, R. K., Yamane, K., Willey, C. D., Cooper 4th, G., Tuxworth, W. J., and Kuppuswamy, D. (2006) Enhanced ubiquitination of cytoskeletal proteins in pressure overloaded myocardium is accompanied by changes in specific E3 ligases. J. Mol. Cell. Cardiol. 41, 669-679
14. Spruill, L. S., Baicu, C. F., Zile, M. R., and McDermott, P. J. (2008) Selective translation of mRNAs in the left ventricular myocardium of the mouse in response to acute pressure overload. J. Mol. Cell. Cardiol. 44, 69-75
15. Brown, K., Gerstberger, S., Carlson, L., Franzoso, G., and Siebenlist, U. (1995) Control of I κB-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267, 1485-1488
16. Sanlioglu, S., Williams, C. M., Samavati, L., Butler, N. S., Wang, G., McCray, P. B. Jr., Ritchie, T. C., Hunninghake, G. W., Zandi, E., and Engelhardt, J. F. (2001) Lipopolysaccharide induces Rac1-dependent reactive oxygen species formation and coordinates tumor necrosis factor-alpha secretion through IKK regulation of NF-κB. J. Biol. Chem. 276, 30188-30198 (Pubitemid 37385100)
17. Toruner, M., Fernandez-Zapico, M., Sha, J. J., Pham, L., Urrutia, R., and Egan, L. J. (2006) Antianoikis effect of nuclear factor-κB through up-regulated expression of osteoprotegerin, BCL-2, and IAP-1. J. Biol. Chem. 281, 8686-8696 (Pubitemid 43847973)
18. Von Wnuck Lipinski, K., Keul, P., Ferri, N., Lucke, S., Heusch, G., Fischer, J. W., and Levkau, B. (2006) Integrin-mediated transcriptional activation of inhibitor of apoptosis proteins protects smooth muscle cells against apoptosis induced by degraded collagen. Circ. Res. 98, 1490-1497 (Pubitemid 44297071)
19. Li, Y., Ha, T., Gao, X., Kelley, J., Williams, D. L., Browder, I. W., Kao, R. L., and Li, C. (2004) NF-κB activation is required for the development of cardiac hypertrophy in vivo. Am. J. Physiol. Heart. Circ. Physiol. 287, H1712-H1720 (Pubitemid 39313278)
20. Ha, T., Li, Y., Gao, X., McMullen, J. R., Shioi, T., Izumo, S., Kelley, J. L., Zhao, A., Haddad, G. E., Williams, D. L., Browder, I. W., Kao, R. L., and Li, C. (2005) Attenuation of cardiac hypertrophy by inhibiting both mTOR and NFκB activation in vivo. Free Radic. Biol. Med. 39, 1570-1580 (Pubitemid 41642588)
21. Zhang, J. Q., Elzey, B., Williams, G., Lu, S., Law, D. J., and Horowits, R. (2001) Ultrastructural and biochemical localization of N-RAP at the interface between myofibrils and intercalated disks in the mouse heart. Biochemistry 40, 14898-14906 (Pubitemid 33136111)
22. Laser, M., Willey, C. D., Jiang, W., Cooper 4th, G., Menick, D. R., Zile, M. R., and Kuppuswamy, D. (2000) Integrin activation and focal complex formation in cardiac hypertrophy. J. Biol. Chem. 275, 35624-35630
23. Willey, C. D., Balasubramanian, S., Rodriguez Rosas, M. C., Ross, R. S., and Kuppuswamy, D. (2003) Focal complex formation in adult cardiomyocytes is accompanied by the activation of beta3 integrin and c-Src. J. Mol. Cell. Cardiol. 35, 671-683 (Pubitemid 36677451)
24. Balasubramanian, S., and Kuppuswamy, D. (2003) RGD-containing peptides activate S6K1 through beta3 integrin in adult cardiac muscle cells. J. Biol. Chem. 278, 42214-42224 (Pubitemid 37310488)
25. Ross, R. S., Pham, C., Shai, S. Y., Goldhaber, J. I., Fenczik, C., Glembotski, C. C., Ginsberg, M. H., and Loftus, J. C. (1998) Beta1 integrins participate in the hypertrophic response of rat ventricular myocytes. Circ. Res. 82, 1160-1172 (Pubitemid 28311124)
26. Yutao, X., Geru, W., Xiaojun, B., Tao, G., and Aiqun, M. (2006) Mechanical stretch-induced hypertrophy of neonatal rat ventricular myocytes is mediated by beta(1)-integrin-microtubule signaling pathways. Eur. J. Heart. Fail. 8, 16-22 (Pubitemid 43012096)
27. Ogawa, E., Saito, Y., Harada, M., Kamitani, S., Kuwahara, K., Miyamoto, Y., Ishikawa, M., Hamanaka, I., Kajiyama, N., Takahashi, N., Nakagawa, O., Masuda, I., Kishimoto, I., and Nakao, K. (2000) Outside-in signalling of fibronectin stimulates cardiomyocyte hypertrophy in cultured neonatal rat ventricular myocytes. J. Mol. Cell. Cardiol. 32, 765-776 (Pubitemid 30658914)
28. Iijima, Y., Laser, M., Shiraishi, H., Willey, C. D., Sundaravadivel, B., Xu, L., McDermott, P. J., and Kuppuswamy, D. (2002) c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J. Biol. Chem. 277, 23065-23075 (Pubitemid 34967293)
29. Cheng, G., Zile, M. R., Takahashi, M., Baicu, C. F., Bonnema, D. D., Cabral, F., Menick, D. R., and Cooper 4th, G. (2008) A direct test of the hypothesis that increased microtubule network density contributes to contractile dysfunction of the hypertrophied heart. Am. J. Physiol. Heart Circ. Physiol. 294, H2231-H2241
30. Sahn, D. J., DeMaria, A., Kisslo, J., and Weyman, A. (1978) Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58, 1072-1083 (Pubitemid 9091990)
31. DeGroff, C. G., Shandas, R., Kwon, J., and Valdes-Cruz, L. (2000) Accuracy of the Bernoulli equation for estimation of pressure gradient across stenotic Blalock-Taussig shunts: an in vitro and numerical study. Pediatr. Cardiol. 21, 439-447 (Pubitemid 30676878)
32. Spinale, F. G., Coker, M. L., Thomas, C. V., Walker, J. D., Mukherjee, R., and Hebbar, L. (1998) Time-dependent changes in matrix metalloproteinase activity and expression during the progression of congestive heart failure: relation to ventricular and myocyte function. Circ. Res. 82, 482-495 (Pubitemid 28117330)
33. Kent, R. L., Mann, D. L., Urabe, Y., Hisano, R., Hewett, K. W., Loughnane, M., and Cooper 4th, G. (1989) Contractile function of isolated feline cardiocytes in response to viscous loading. Am. J. Physiol. Heart Circ. Physiol. 257, H1717-H1727
34. Sambrano, G. R., Fraser, I., Han, H., Ni, Y., O'Connell, T., Yan, Z., and Stull, J. T. (2002) Navigating the signalling network in mouse cardiac myocytes. Nature 420, 712-714 (Pubitemid 36764508)
35. Kuppuswamy, D., Kerr, C., Narishige, T., Kasi, V. S., Menick, D. R., and Cooper, G. (1997) Association of tyrosine-phosphorylated c-Src with the cytoskeleton of hypertrophying myocardium. J. Biol. Chem. 272, 4500-4508 (Pubitemid 27078529)
36. Willey, C. D., Palanisamy, A. P., Johnston, R. K., Mani, S. K., Shiraishi, H., Tuxworth, W. J., Zile, M. R., Balasubramanian, S., and Kuppuswamy, D. (2008) STAT3 activation in pressureoverloaded feline myocardium: role for integrins and the tyrosine kinase BMX. Int. J. Biol. Sci. 4, 184-199 (Pubitemid 351956719)
37. Tuxworth, W. J., Jr., Saghir, A. N., Spruill, L. S., Menick, D. R., and McDermott, P. J. (2004) Regulation of protein synthesis by eIF4E phosphorylation in adult cardiocytes: the consequence of secondary structure in the 5′-untranslated region of mRNA. Biochem. J. 378, 73-82
38. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408 (Pubitemid 34164012)
39. Sadoshima, J., and Izumo, S. (1997) The cellular and molecular response of cardiac myocytes to mechanical stress. Annu. Rev. Physiol. 59, 551-571 (Pubitemid 27142455)
40. Birks, E. J., Latif, N., Enesa, K., Folkvang, T., Luong le, A., Sarathchandra, P., Khan, M., Ovaa, H., Terracciano, C. M., Barton, P. J., Yacoub, M. H., and Evans, P. C. (2008) Elevated p53 expression is associated with dysregulation of the ubiquitinproteasome system in dilated cardiomyopathy. Cardiovasc. Res. 79, 472-480
41. Lindsey, M. L., Goshorn, D. K., Comte-Walters, S., Hendrick, J. W., Hapke, E., Zile, M. R., and Schey, K. (2006) A multidimensional proteomic approach to identify hypertrophy-associated proteins. Proteomics 6, 2225-2235
42. Chen, Z., Hagler, J., Palombella, V. J., Melandri, F., Scherer, D., Ballard, D., and Maniatis, T. (1995) Signal-induced site-specific phosphorylation targets I κB alpha to the ubiquitin-proteasome pathway. Genes Dev. 9, 1586-1597
43. Traenckner, E. B., Wilk, S., and Baeuerle, P. A. (1994) A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of I κB-α that is still bound to NF-κB. EMBO J. 13, 5433-5441 (Pubitemid 24351822)
44. Scatena, M., Almeida, M., Chaisson, M. L., Fausto, N., Nicosia, R. F., and Giachelli, C. M. (1998) NF-κB mediates αvβ3 integrininduced endothelial cell survival. J. Cell Biol. 141, 1083-1093 (Pubitemid 28243974)
45. Courter, D. L., Lomas, L., Scatena, M., and Giachelli, C. M. (2005) Src kinase activity is required for integrin αVβ3-mediated activation of nuclear factor-κB. J. Biol. Chem. 280, 12145-12151 (Pubitemid 40491025)
46. Ren, J., Avery, J., Zhao, H., Schneider, J. G., Ross, F. P., and Muslin, A. J. (2007) β3 integrin deficiency promotes cardiac hypertrophy and inflammation. J. Mol. Cell. Cardiol. 42, 367-377 (Pubitemid 46135609)
47. Acharyya, S., Ladner, K. J., Nelsen, L. L., Damrauer, J., Reiser, P. J., Swoap, S., and Guttridge, D. C. (2004) Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J. Clin. Invest. 114, 370-378 (Pubitemid 39071609)
48. Li, H. H., Willis, M. S., Lockyer, P., Miller, N., McDonough, H., Glass, D. J., and Patterson, C. (2007) Atrogin-1 inhibits Aktdependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of Forkhead proteins. J. Clin. Invest. 117, 3211-3223 (Pubitemid 350096979)
49. Lemler, M. S., Bies, R. D., Frid, M. G., Sastravaha, A., Zisman, L. S., Bohlmeyer, T., Gerdes, A. M., Reeves, J. T., and Stenmark, K. R. (2000) Myocyte cytoskeletal disorganization and right heart failure in hypoxia-induced neonatal pulmonary hypertension. Am. J. Physiol. Heart Circ. Physiol. 279, H1365-H1376