Fibulin-2 deficiency attenuates angiotensin II-induced cardiac hypertrophy by reducing transforming growth factor-β signalling

Clinical Science

Volumn 126, Issue 4, 2014, Pages 275-288

  Zhang, Hangxiang ^a,c   Wu, Jing ^b,c   Dong, Hailong ^c   Khan, Shaukat A ^c   Chu, Mon Li ^d   Tsuda, Takeshi ^a,c  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b XI'AN JIAOTONG UNIVERSITY   (China)

^c NEMOURS ALFRED I DUPONT HOSPITAL FOR CHILDREN   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Angiotensin II (angii); autoinduction; Cardiac hypertrophy; Extracellular matrix; Signalling; Transforming growth factor (TGF )

Indexed keywords

ANGIOTENSIN II; COLLAGEN TYPE 2; COLLAGEN TYPE 3; FIBULIN; FIBULIN 2; GELATINASE A; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE P38; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; HEART VENTRICLE HYPERTROPHY; HYPERTENSION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANGIOTENSIN II; ANIMALS; CALCIUM-BINDING PROTEINS; CARDIOMEGALY; EXTRACELLULAR MATRIX PROTEINS; FIBROSIS; HYPERTENSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCARDIUM; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; VASOCONSTRICTOR AGENTS;

EID: 84886690135     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120636     Document Type: Article

References (54)

1. Olson, E. N. (2004) A decade of discoveries in cardiac biology. Nat. Med. 10, 467-474
2. Sutton, M. G. and Sharpe, N. (2000) Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 101, 2981-2988
3. Mann, D. L. (2004) Heart failure as a progressive disease. In Heart Failure 123-128, W.B. Saunders, Philadelphia.
4. Higuchi, S, Ohtsu, H, Suzuki, H, Shirai, H, Frank, G. D. and Eguchi, S. (2007) Angiotensin II signal transduction through the AT1 receptor: novel insights into mechanisms and pathophysiology. Clin. Sci. 112, 417-428
5. Weber, K. T. (1997) Extracellular matrix remodeling in heart failure: a role for de novo angiotensin II generation. Circulation 96, 4065-4082
6. Pfeffer, J. M., Fischer, T. A. and Pfeffer, M. A. (1995) Angiotensin-converting enzyme inhibition and ventricular remodeling after myocardial infarction. Ann. Rev. Physiol. 57, 805-826
7. Pfeffer, M. A., Braunwald, E., Moye, L. A., Basta, L., Brown, Jr, E. J., Cuddy, T. E., Davis, B. R., Geltman, E. M., Goldman, S., Flaker, G. C. et al. (1992) Effect of captopril on mortality and morbidity in patients with left ventricular dysfunction after myocardial infarction. Results of the survival and ventricular enlargement trial. The SAVE Investigators. N. Engl. J. Med. 327, 669-677
8. Schieffer, B., Wirger, A., Meybrunn, M., Seitz, S., Holtz, J., Riede, U. N. and Drexler, H. (1994) Comparative effects of chronic angiotensin-converting enzyme inhibition and angiotensin II type 1 receptor blockade on cardiac remodeling after myocardial infarction in the rat. Circulation 89, 2273-2282
9. Harada, K., Sugaya, T., Murakami, K., Yazaki, Y. and Komuro, I. (1999) Angiotensin II type 1A receptor knockout mice display less left ventricular remodeling and improved survival after myocardial infarction. Circulation 100, 2093-2099
10. Jain, M., Liao, R., Ngoy, S., Whittaker, P., Apstein, C. S. and Eberli, F. R. (2000) Angiotensin II receptor blockade attenuates the deleterious effects of exercise training on post-MI ventricular remodelling in rats. Cardiovasc. Res. 46, 66-72
11. Selvetella, G., Hirsch, E., Notte, A., Tarone, G. and Lembo, G. (2004) Adaptive and maladaptive hypertrophic pathways: points of convergence and divergence. Cardiovasc. Res. 63, 373-380
12. Opie, L. H., Commerford, P. J., Gersh, B. J. and Pfeffer, M. A. (2006) Controversies in ventricular remodeling. Lancet 367, 356-367
13. Manabe, I., Shindo, T. and Nagai, R. (2002) Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circ. Res. 91, 1103-1113
14. Cleutjens, J. P. and Creemers, E. E. (2002) Integration of concepts: cardiac extracellular matrix remodeling after myocardial infarction. J. Card. Failure 8, S344-S348
15. Blobe, G. C., Schiemann, W. P. and Lodish, H. F. (2000) Role of transforming growth factor β in human disease. N. Engl. J. Med. 342, 1350-1358
16. Lijnen, P. J., Petrov, V. V. and Fagard, R. H. (2000) Induction of cardiac fibrosis by transforming growth factor-β1. Mol. Genet. Metab. 71, 418-435
17. Hao, J., Ju, H., Zhao, S., Junaid, A., Scammell-La Fleur, T. and Dixon, I. M. (1999) Elevation of expression of Smads 2, 3, and 4, decorin and TGF-β in the chronic phase of myocardial infarct scar healing. J. Mol. Cell. Cardiol. 31, 667-678
18. Campbell, S. E. and Katwa, L. C. (1997) Angiotensin II stimulated expression of transforming growth factor-β1 in cardiac fibroblasts and myofibroblasts. J. Mol. Cell. Cardiol. 29, 1947-1958
19. Lee, A. A., Dillmann, W. H., McCulloch, A. D. and Villarreal, F. J. (1995) Angiotensin II stimulates the autocrine production of transforming growth factor-β1 in adult rat cardiac fibroblasts. J. Mol. Cell. Cardiol. 27, 2347-2357
20. Sadoshima, J. and Izumo, S. (1993) Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ. Res. 73, 413-423
21. Schorb, W., Booz, G. W., Dostal, D. E., Conrad, K. M., Chang, K. C. and Baker, K. M. (1993) Angiotensin II is mitogenic in neonatal rat cardiac fibroblasts. Circ. Res. 72, 1245-1254
22. Schultz, Jel, J., Witt, S. A., Glascock, B. J., Nieman, M. L., Reiser, P. J., Nix, S. L., Kimball, T. R. and Doetschman, T. (2002) TGF-β1 mediates the hypertrophic cardiomyocyte growth induced by angiotensin II. J. Clin. Invest. 109, 787-796
23. Bujak, M. and Frangogiannis, N. G. (2007) The role of TGF-β signaling in myocardial infarction and cardiac remodeling. Cardiovasc. Res. 74, 184-195
24. Okada, H., Takemura, G., Kosai, K., Li, Y., Takahashi, T., Esaki, M., Yuge, K., Miyata, S., Maruyama, R., Mikami, A. et al. (2005) Postinfarction gene therapy against transforming growth factor-β signal modulates infarct tissue dynamics and attenuates left ventricular remodeling and heart failure. Circulation 111, 2430-2437
25. Tsuda, T., Wang, H., Timpl, R. and Chu, M. L. (2001) Fibulin-2 expression marks transformed mesenchymal cells in developing cardiac valves, aortic arch vessels, and coronary vessels. Dev. Dyn. 222, 89-100
26. Strom, A., Olin, A. I., Aspberg, A. and Hultgardh-Nilsson, A. (2006) Fibulin-2 is present in murine vascular lesions and is important for smooth muscle cell migration. Cardiovasc. Res. 69, 755-763
27. Fassler, R., Sasaki, T., Timpl, R., Chu, M. L. and Werner, S. (1996) Differential regulation of fibulin, tenascin-C, and nidogen expression during wound healing of normal and glucocorticoid-treated mice. Exp. Cell Res. 222, 111-116
28. Sicot, F. X., Tsuda, T., Markova, D., Klement, J. F., Arita, M., Zhang, R. Z., Pan, T. C., Mecham, R. P., Birk, D. E. and Chu, M. L. (2008) Fibulin-2 is dispensable for mouse development and elastic fiber formation. Mol. Cell. Biol. 28, 1061-1067
29. Tsuda, T., Wu, J., Gao, E., Joyce, J., Markova, D., Dong, H., Liu, Y., Zhang, H., Zou, Y., Gao, F. et al. (2012) Loss of fibulin-2 protects against progressive ventricular dysfunction after myocardial infarction. J. Mol. Cell. Cardiol. 52, 273-282
30. Susic, D., Nunez, E., Frohlich, E. D. and Prakash, O. (1996) Angiotensin II increases left ventricular mass without affecting myosin isoform mRNAs. Hypertension 28, 265-268
31. Rosenkranz, S. (2004) TGF-β1 and angiotensin networking in cardiac remodeling. Cardiovasc. Res. 63, 423-432
32. Deten, A., Holzl, A., Leicht, M., Barth, W. and Zimmer, H. G. (2001) Changes in extracellular matrix and in transforming growth factor β isoforms after coronary artery ligation in rats. J. Mol. Cell. Cardiol. 33, 1191-1207
33. Meulmeester, E. and Ten Dijke, P. (2011) The dynamic roles of TGF-β in cancer. J. Pathol. 223, 205-218
34. Chaudhry, S. S., Cain, S. A., Morgan, A., Dallas, S. L., Shuttleworth, C. A. and Kielty, C. M. (2007) Fibrillin-1 regulates the bioavailability of TGFβ1. J. Cell. Biol. 176, 355-367
35. Crawford, S. E., Stellmach, V., Murphy-Ullrich, J. E., Ribeiro, S. M., Lawler, J., Hynes, R. O., Boivin, G. P. and Bouck, N. (1998) Thrombospondin-1 is a major activator of TGF-β1 in vivo. Cell 93, 1159-1170
36. Frangogiannis, N. G., Ren, G., Dewald, O., Zymek, P., Haudek, S., Koerting, A., Winkelmann, K., Michael, L. H., Lawler, J. and Entman, M. L. (2005) Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation 111, 2935-2942
37. Schellings, M. W., Pinto, Y. M. and Heymans, S. (2004) Matricellular proteins in the heart: possible role during stress and remodeling. Cardiovasc. Res. 64, 24-31
38. Kehat, I. and Molkentin, J. D. (2010) Extracellular signal-regulated kinase 1/2 (ERK1/2) signaling in cardiac hypertrophy. Ann. N. Y. Acad. Sci. 1188, 96-102
39. Purcell, N. H., Wilkins, B. J, York, A., Saba-El-Leil, M. K., Meloche, S., Robbins, J. and Molkentin, J. D. (2007) Genetic inhibition of cardiac ERK1/2 promotes stress-induced apoptosis and heart failure but has no effect on hypertrophy in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 14074-14079
40. Ono, R. N., Sengle, G., Charbonneau, N. L., Carlberg, V., Bachinger, H. P., Sasaki, T., Lee-Arteaga, S., Zilberberg, L., Rifkin, D. B., Ramirez, F. et al. (2009) Latent transforming growth factor β-binding proteins and fibulins compete for fibrillin-1 and exhibit exquisite specificities in binding sites. J. Biol. Chem. 284, 16872-16881
41. Ji, Y., Prasad, N. B., Novotny, E. A., Kaur, S., Elkahloun, A., Chen, Y., Zhang, R. Z., Chu, M. L., Agarwal, S. K., Marx, S. J. et al. (2007) Mouse embryo fibroblasts lacking the tumor suppressor menin show altered expression of extracellular matrix protein genes. Mol. Cancer Res. 5, 1041-1051
42. Van Obberghen-Schilling, E., Roche, N. S., Flanders, K. C., Sporn, M. B. and Roberts, A. B. (1988) Transforming growth factor β 1 positively regulates its own expression in normal and transformed cells. J. Biol. Chem. 263, 7741-7746
43. Bascom, C. C., Wolfshohl, J. R., Coffey, Jr, R. J., Madisen, L., Webb, N. R., Purchio, A. R., Derynck, R. and Moses, H. L. (1989) Complex regulation of transforming growth factor β1, β2, and β3 mRNA expression in mouse fibroblasts and keratinocytes by transforming growth factors β1 and β2. Mol. Cell. Biol. 9, 5508-5515
44. Huang, X. R., Chung, A. C., Yang, F., Yue, W., Deng, C., Lau, C. P., Tse, H. F. and Lan, H. Y. (2010) Smad3 mediates cardiac inflammation and fibrosis in angiotensin II-induced hypertensive cardiac remodeling. Hypertension 55, 1165-1171
45. Watkins, S. J., Borthwick, G. K., Oakenfull, R., Robson, A. and Authur, H. M. (2012) Angiotensin II-induced cardiomyocyte hypertrophy in vitro is TAK1-dependent and Smad2/3-independent. Hypertens. Res. 35, 393-398
46. Matsumoto-Ida, M., Takimoto, Y., Aoyama, T., Akao, M., Takeda, T. and Kita, T. (2006) Activation of TGF-β1-TAK1-p38 MAPK pathway in spared cardiomyocytes is involved in left ventricular remodeling after myocardial infarction in rats. Am. J. Physiol. Heart Circ. Physiol. 290, H709-H715
47. Brezniceanu, M. L., Wei, C. C., Zhang, S. L., Hsieh, T. J., Guo, D. F., Hebert, M. J., Ingelfinger, J. R., Filep, J. G. and Chan, J. S. (2006) Transforming growth factor-β 1 stimulates angiotensinogen gene expression in kidney proximal tubular cells. Kidney Int. 69, 1977-1985
48. Zhang, M., Fraser, D. and Phillips, A. (2006) ERK, p38, and Smad signaling pathways differentially regulate transforming growth factor-β1 autoinduction in proximal tubular epithelial cells. Am. J. Pathol. 169, 1282-1293
49. Seo, J. Y., Park, J., Yu, M. R., Kim, Y. S., Ha, H. and Lee, H,B. (2009) Positive feedback loop between plasminogen activator inhibitor-1 and transforming growth factor-β1 during renal fibrosis in diabetes. Am. J. Nephrol. 30, 481-490
50. Ellmers, L. J., Scott, N. J., Medicherla, S., Pilbrow, A. P., Bridgman, P. G., Yandle, T. G., Richards, A. M., Protter, A. A. and Cameron, V. A. (2008) Transforming growth factor-β blockade down-regulates the renin-angiotensin system and modifies cardiac remodeling after myocardial infarction. Endocrinology 149, 5828-5834
51. Frantz, S., Hu, K., Adamek, A., Wolf, J., Sallam, A., Maier, S. K., Lonning, S., Ling, H., Ertl, G. and Bauersachs, J. (2008) Transforming growth factor β inhibition increases mortality and left ventricular dilatation after myocardial infarction. Basic Res. Cardiol. 103, 485-492
52. Lucas, J. A., Zhang, Y., Li, P., Gong, K., Miller, A. P., Hassan, E., Hage, F., Xing, D., Wells, B., Oparil, S. and Chen, Y. F. (2010) Inhibition of transforming growth factor-β signaling induces left ventricular dilation and dysfunction in the pressureoverloaded heart. Am. J. Physiol. Heart Circ. Physiol. 298, H424-H432
53. Karakikes, I., Chaanine, A. H., Kang, S., Mukete, B. N., Jeong, D., Hajjar, R. J. and Lebeche, D (2013) Therapeutic cardiac-targeted delivery of miR-1 reverses pressure overload-induced cardiac hypertrophy and attenuates pathological remodeling. J. Am. Heart Assoc. 2, e000078
54. Ruiz-Ortega, M., Rodriguez-Vita, J., Sanchez-Lopez, E., Carvajal, G. and Egido, J. (2007) TGF-β signaling in vascular fibrosis. Cardiovasc. Res. 74, 196-206