Targeted disruption of Smad4 in cardiomyocytes results in cardiac hypertrophy and heart failure

Circulation Research

Volumn 97, Issue 8, 2005, Pages 821-828

  Wang, Jian ^a   Xu, Ning ^b   Feng, Xinheng ^b   Hou, Ning ^a   Zhang, JiShuai ^a   Cheng, Xuan ^a   Chen, Yeguang ^c   Zhang, Youyi ^b   Yang, Xiao ^a  

^a BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^b PEKING UNIVERSITY THIRD HOSPITAL   (China)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

Cardiac hypertrophy; Cre LoxP system; Heart failure; Mitogen activated protein kinase; Smad4

Indexed keywords

CRE RECOMBINASE; CYTOKINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENZYME REGULATION; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION; HEART DEVELOPMENT; HEART DISEASE; HEART FAILURE; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEMODYNAMICS; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOMEGALY; CELL SIZE; ENZYME ACTIVATION; FIBROSIS; HEART FAILURE, CONGESTIVE; MICE; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 26844468478     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000185833.42544.06     Document Type: Article

References (51)

1. Braunwald E, Bristow MR. Congestive heart failure: fifty years of progress. Circulation. 2000;102:14-23.
2. Hunter JJ, Chien KR. Signaling pathways for cardiac hypertrophy and failure. N Engl J Med. 1999;341:1276-1283.
3. Ritter O, Neyses L. The molecular basis of myocardial hypertrophy and heart failure. Trends Mol Med. 2003;9:313-321.
4. Molkentin JD, Dorn GW II. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu Rev Physiol. 2001;63:391-426.
5. Azhar M, Schultz Jel J, Grupp I, Dorn GW II, Meneton P, Molin DG, Gittenberger-de Groot AC, Doetschman T. Transforming growth factor beta in cardiovascular development and function. Cytokine Growth Factor Rev. 2003;14:391-407.
6. Takahashi N, Calderone A, Izzo NJ Jr, Maki TM, Marsh JD, Colucci WS. Hypertrophic stimuli induce transforming growth factor-beta 1 expression in rat ventricular myocytes. J Clin Invest. 1994;94:1470-1476.
7. Boluyt MO, O'Neill L, Meredith AL, Bing OH, Brooks WW, Conrad CH, Crow MT, Lakatta EG. Alterations in cardiac gene expression during the transition from stable hypertrophy to heart failure. Marked upregulation of genes encoding extracellular matrix components. Circ Res. 1994;75: 23-32.
8. Nakajima H, Nakajima HO, Salcher O, Dittie AS, Dembowsky K, Jing S, Field LJ. Atrial but not ventricular fibrosis in mice expressing a mutant transforming growth factor-beta(1) transgene in the heart. Circ Res. 2000;86:571-579.
9. Brooks WW, Conrad CH. Myocardial fibrosis in transforming growth factor beta(1)heterozygous mice. J Mol Cell Cardiol. 2000;32:187-195.
10. Kuwahara F, Kai H, Tokuda K, Kai M, Takeshita A, Egashira K, Imaizumi T. Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation. 2002;106:130-135.
11. 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.
12. Schultz Jel J, Witt SA, Glascock BJ, Nieman ML, Reiser PJ, Nix SL, Kimball TR, Doetschman T. TGF-beta1 mediates the hypertrophic cardiomyocyte growth induced by angiotensin II. J Clin Invest. 2002;109: 787-796.
13. Roberts AB. The ever-increasing complexity of TGF-beta signaling. Cytokine Growth Factor Rev. 2002;13:3-5.
14. Yamazaki T, Komuro I, Kudoh S, Zou Y, Shiojima I, Mizuno T, Takano H, Hiroi Y, Ueki K, Tobe K, Kadowaki T, Nagai R, Yazaki Y. Mechanical stress activates protein kinase cascade of phosphorylation in neonatal rat cardiac myocytes. J Clin Invest. 1995;96:438-446.
15. Petrich BG, Wang Y. Stress-activated MAP kinases in cardiac remodeling and heart failure; new insights from transgenic studies. Trends Cardiovasc Med. 2004;14:50-55.
16. Massague J. TGF-beta signal transduction. Annu Rev Biochem. 1998;67: 753-791.
17. Dixon IM, Hao J, Reid NL, Roth JC. Effect of chronic AT(1) receptor blockade on cardiac Smad overexpression in hereditary cardiomyopathic hamsters. Cardiovasc Res. 2000;46:286-297.
18. Yang X, Li C, Xu X, Deng C. The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice. Proc Natl Acad Sci U S A. 1998;95:3667-3672.
19. Sirard C, de la Pompa JL, Elia A, Itie A, Mirtsos C, Cheung A, Hahn S, Wakeham A, Schwartz L, Kern SE, Rossant J, Mak TW. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 1998;12: 107-119.
20. Yang X, Li C, Herrera PL, Deng CX. Generation of Smad4/Dpc4 conditional knockout mice. Genesis. 2002;32:80-81.
21. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999;21:70-71.
22. Yang G, Cui F, Hou N, Cheng X, Zhang JS, Wang YL, Jiang N, Gao X, Yang X. Transgenic mice that express Cre recombinase in hypertrophic chondrocytes. Genesis. 2005;42:33-36.
23. Wang YL, Cui F, Lv YX, Li CL, Xu XL, Deng CX, Wang DP, Sun YX, Hu GX, Lang ZW, Huang CF, Yang X. HBsAg and HBx knocked into the p21 locus causes hepatocellular carcinoma in mice. Hepatology. 2004; 39:318-324.
24. Sun YX, Zhou J, Liao XD, Lu YX, Deng CX, Huang PT, Chen Q, Yang X. Disruption of Smad5 gene induces mitochondria-dependent apoptosis in cardiomyocytes. Exp Cell Res. 2005;306:85-93.
25. Shioi T, Kang PM, Douglas PS, Hampe J, Yballe CM, Lawitts J, Cantley LC, Izumo S. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J. 2000;19:2537-2548.
26. Schultz JE, Witt SA, Nieman ML, Reiser PJ, Engle SJ, Zhou M, Pawlowski SA, Lorenz JN, Kimball TR, Doetschman T. Fibroblast growth factor-2 mediates pressure-induced hypertrophic response. J Clin Invest. 1999;104:709-719.
27. Yue J, Mulder KM. Requirement of Ras/MAPK pathway activation by transforming growth factor beta for transforming growth factor beta 1 production in a Smad-dependent pathway. J Biol Chem. 2000;275: 30765-30773.
28. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003;113:685-700.
29. Schlange T, Andree B, Arnold HH, Brand T. BMP2 is required for early heart development during a distinct time period. Mech Dev. 2000;91: 259-270.
30. Pelton RW, Saxena B, Jones M, Moses HL, Gold LI. Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J Cell Biol. 1991;115:1091-1105.
31. Zhang H, Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 1996; 122:2977-2986.
32. Letterio JJ, Geiser AG, Kulkarni AB, Roche NS, Sporn MB, Roberts AB. Maternal rescue of transforming growth factor-beta 1 null mice. Science. 1994;264:1936-1938.
33. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development. 1997;124:2659-2670.
34. Bartram U, Molin DG, Wisse LJ, Mohamad A, Sanford LP, Doetschman T, Speer CP, Poelmann RE, Gittenberger-de Groot AC. Double-outlet right ventricle and overriding Bicuspid valve reflect disturbances of looping, myocardialization, endocardial cushion differentiation, and apoptosis in TGF-beta(2)-knockout mice. Circulation. 2001;103:2745-2752.
35. Solloway MJ, Robertson EJ. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development. 1999;126:1753-1768.
36. Gaussin V, Van de Putte T, Mishina Y, Hanks MC, Zwijsen A, Huylebroeck D, Behringer RR, Schneider MD. Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proc Natl Acad Sci U S A. 2002;99:2878-2883.
37. Yang X, Castilla LH, Xu X, Li C, Gotay J, Weinstein M, Liu PP, Deng CX. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development. 1999;126:1571-1580.
38. Chu GC, Dunn NR, Anderson DC, Oxburgh L, Robertson EJ. Differential requirements for Smad4 in TGFbeta-dependent patterning of the early mouse embryo. Development. 2004;131:3501-3512.
39. Rosenkranz S. TGF-beta1 and angiotensin networking in cardiac remodeling. Cardiovasc Res. 2004;63:423-432.
40. Li RK, Li G, Mickle DA, Weisel RD, Merante F, Luss H, Rao V, Christakis GT, Williams WG. Overexpression of transforming growth factor-beta 1 and insulin-like growth factor-I in patients with idiopathic hypertrophic cardiomyopathy. Circulation. 1997;96:874-881.
41. Rosenkranz S, Flesch M, Amann K, Haeuseler C, Kilter H, Seeland U, Schlüter KD, Böhm M. Alterations of β-adrenergic signaling and cardiac hypertrophy in transgenic mice overexpressing TGF-β1 Am J Physiol Heart Circ Physiol. 2002;283:1253-1262.
42. Engel ME, McDonnell MA, Law BK, Moses HL. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J Biol Chem. 1999;274:37413-37420.
43. Ramirez MT, Sah VP, Zhao XL, Hunter JJ, Chien KR, Brown JH. The MEKK-JNK pathway is stimulated by alpha1-adrenergic receptor and ras activation and is associated with in vitro and in vivo cardiac hypertrophy. J Biol Chem. 1997;272:14057-14061.
44. Zechner D, Thuerauf DJ, Hanford DS, McDonough PM, Glembotski CC. A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J Cell Biol. 1997;139:115-127.
45. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, Klevitsky R, Hewett TE, Jones SP, Lefer DJ, Peng CF, Kitsis RN, Molkentin JD. The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J. 2000;19:6341-6350.
46. Yamazaki T, Tobe K, Hoh E, Maemura K, Kaida T, Komuro I, Tamemoto H, Kadowaki T, Nagai R, Yazaki Y. Mechanical loading activates mitogen-activated protein kinase and S6 peptide kinase in cultured rat cardiac myocytes. J Biol Chem. 1993;268:12069-12076.
47. 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.
48. Zou Y, Komuro I, Yamazaki T, Aikawa R, Kudoh S, Shiojima I, Hiroi Y, Mizuno T, Yazaki Y. Protein kinase C, but not tyrosine kinases or Ras, plays a critical role in angiotensin II-induced activation of Raf-1 kinase and extracellular signal-regulated protein kinases in cardiac myocytes. J Biol Chem. 1996;271:33592-33597.
49. Bueno OF, Molkentin JD. Involvement of extracellular signal-regulated kinases 1/2 in cardiac hypertrophy and cell death. Circ Res. 2002;91: 776-781.
50. Shibata R, Ouchi N, Ito M, Kihara S, Shiojima I, Pimentel DR, Kumada M, Sato K, Schiekofer S, Ohashi K, Funahashi T, Colucci WS, Walsh K. Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat Med. 2004;10:1384-1389.
51. Sanna B, Bueno OF, Dai YS, Wilkins BJ, Molkentin JD. Direct and indirect interactions between calcineurin-NFAT and MEK1-extracellular signal-regulated kinase 1/2 signaling pathways regulate cardiac gene expression and cellular growth. Mol Cell Biol. 2005;25:865-878.