Thrombospondin-4, tumour necrosis factor-like weak inducer of apoptosis (TWEAK) and its receptor Fn14: Novel extracellular matrix modulating factors in cardiac remodelling

References

• Cohn JN, Ferrari R, Sharpe N. Cardiac remodeling—concepts and clinical implications: a consensus paper from an international forum on cardiac remodeling. Behalf of an International Forum on Cardiac Remodeling. J Am Coll Cardiol. 2000;35:569–82.
   PubMed Web of Science ®Google Scholar
• Hill JA, Olson EN. Cardiac plasticity. N Engl J Med. 2008; 358:1370–80.
   PubMed Web of Science ®Google Scholar
• Brown RD, Ambler SK, Mitchell MD, Long CS. The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol. 2005;45: 657–87.
   PubMed Web of Science ®Google Scholar
• Porter KE, Turner NA. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther. 2009;123: 255–78.
   PubMed Web of Science ®Google Scholar
• Eyden B. The myofibroblast: phenotypic characterization as a prerequisite to understanding its functions in translational medicine. J Cell Mol Med. 2008;12:22–37.
   PubMed Web of Science ®Google Scholar
• Baudino TA, Carver W, Giles W, Borg TK. Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol. 2006; 291:H1015–26.
   PubMed Web of Science ®Google Scholar
• Berk BC, Fujiwara K, Lehoux S. ECM remodeling in hypertensive heart disease. J Clin Invest. 2007;117:568–75.
   PubMed Web of Science ®Google Scholar
• Fedak PW, Verma S, Weisel RD, Li RK. Cardiac remodeling and failure: from molecules to man (Part II). Cardiovasc Pathol. 2005;14:49–60.
   PubMedGoogle Scholar
• Graham HK, Horn M, Trafford AW. Extracellular matrix profiles in the progression to heart failure. European Young Physiologists Symposium Keynote Lecture—Bratislava 2007. Acta Physiol (Oxf). 2008;194:3–21.
   PubMed Web of Science ®Google Scholar
• Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol. 2002; 14:608–16.
   PubMed Web of Science ®Google Scholar
• Fedak PW, Verma S, Weisel RD, Li RK. Cardiac remodeling and failure: from molecules to man (Part I). Cardiovasc Pathol. 2005;14:1–11.
   Google Scholar
• Dobaczewski M, Gonzalez-Quesada C, Frangogiannis NG. The extracellular matrix as a modulator of the inflammatory and reparative response following myocardial infarction. J Mol Cell Cardiol. 2010;48:504–11.
   PubMed Web of Science ®Google Scholar
• Jugdutt BI. Remodeling of the myocardium and potential targets in the collagen degradation and synthesis pathways. Curr Drug Targets Cardiovasc Haematol Disord. 2003;3: 1–30.
   Google Scholar
• Jane-Lise S, Corda S, Chassagne C, Rappaport L. The extracellular matrix and the cytoskeleton in heart hypertrophy and failure. Heart Fail Rev. 2000;5:239–50.
   Google Scholar
• Manabe I, Shindo T, Nagai R. Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circ Res. 2002;91:1103–13.
   PubMed Web of Science ®Google Scholar
• Corda S, Samuel JL, Rappaport L. Extracellular matrix and growth factors during heart growth. Heart Fail Rev. 2000; 5:119–30.
   Google Scholar
• Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285–342.
   PubMed Web of Science ®Google Scholar
• Li YY, McTiernan CF, Feldman AM. Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling. Cardiovasc Res. 2000;46:214–24.
   PubMed Web of Science ®Google Scholar
• Bernardo BC, Weeks KL, Pretorius L, McMullen JR. Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol Ther. 2010;128:191–227.
   PubMed Web of Science ®Google Scholar
• Brower GL, Gardner JD, Forman MF, Murray DB, Voloshenyuk T, Levick SP, . The relationship between myocardial extracellular matrix remodeling and ventricular function. Eur J Cardiothorac Surg. 2006;30:604–10.
   PubMed Web of Science ®Google Scholar
• Jugdutt BI. Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation. 2003;108:1395–403.
   PubMed Web of Science ®Google Scholar
• Janicki JS, Brower GL. The role of myocardial fibrillar collagen in ventricular remodeling and function. J Card Fail. 2002;8:S319–25.
   Google Scholar
• Lopez B, Gonzalez A, Hermida N, Valencia F, de Teresa E, Diez J. Role of lysyl oxidase in myocardial fibrosis: from basic science to clinical aspects. Am J Physiol Heart Circ Physiol. 2010;299:H1–9.
   PubMed Web of Science ®Google Scholar
• Zieman S, Kass D. Advanced glycation end product cross-linking: pathophysiologic role and therapeutic target in cardiovascular disease. Congest Heart Fail. 2004;10:144–9; quiz 150–1.
   PubMedGoogle Scholar
• Gunja-Smith Z, Morales AR, Romanelli R, Woessner JF Jr. Remodeling of human myocardial collagen in idiopathic dilated cardiomyopathy. Role of metalloproteinases and pyridinoline cross-links. Am J Pathol. 1996;148:1639–48.
   Google Scholar
• Woodiwiss AJ, Tsotetsi OJ, Sprott S, Lancaster EJ, Mela T, Chung ES, . Reduction in myocardial collagen cross-linking parallels left ventricular dilatation in rat models of systolic chamber dysfunction. Circulation. 2001;103: 155–60.
   PubMed Web of Science ®Google Scholar
• Frangogiannis NG. Targeting the inflammatory response in healing myocardial infarcts. Curr Med Chem. 2006;13: 1877–93.
   PubMed Web of Science ®Google Scholar
• Baumgarten G, Knuefermann P, Kalra D, Gao F, Taffet GE, Michael L, . Load-dependent and -independent regulation of proinflammatory cytokine and cytokine receptor gene expression in the adult mammalian heart. Circulation. 2002;105:2192–97.
   PubMed Web of Science ®Google Scholar
• Xia Y, Lee K, Li N, Corbett D, Mendoza L, Frangogiannis NG. Characterization of the inflammatory and fibrotic response in a mouse model of cardiac pressure overload. Histochem Cell Biol. 2009;131:471–81.
   PubMedGoogle Scholar
• Celis R, Torre-Martinez G, Torre-Amione G. Evidence for activation of immune system in heart failure: is there a role for anti-inflammatory therapy? Curr Opin Cardiol. 2008;23: 254–60.
   Google Scholar
• Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. N Engl J Med. 1990;323:236–41.
   PubMed Web of Science ®Google Scholar
• Seta Y, Shan K, Bozkurt B, Oral H, Mann DL. Basic mechanisms in heart failure: the cytokine hypothesis. J Card Fail. 1996;2:243–49.
   PubMedGoogle Scholar
• Mann DL. Stress-activated cytokines and the heart: from adaptation to maladaptation. Annu Rev Physiol. 2003;65: 81–101.
   PubMed Web of Science ®Google Scholar
• Frangogiannis NG. The immune system and cardiac repair. Pharmacol Res. 2008;58:88–111.
   PubMed Web of Science ®Google Scholar
• Dreyer WJ, Michael LH, Nguyen T, Smith CW, Anderson DC, Entman ML, . Kinetics of C5a release in cardiac lymph of dogs experiencing coronary artery ischemia-reperfusion injury. Circ Res. 1992;71:1518–24.
   PubMed Web of Science ®Google Scholar
• Schellings MW, Pinto YM, Heymans S. Matricellular proteins in the heart: possible role during stress and remodeling. Cardiovasc Res. 2004;64:24–31.
   PubMed Web of Science ®Google Scholar
• Schellings MW, van Almen GC, Sage EH, Heymans S. Thrombospondins in the heart: potential functions in cardiac remodeling. J Cell Commun Signal. 2009;3:201–13.
   PubMed Web of Science ®Google Scholar
• Adams JC. Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol. 2001;17:25–51.
   PubMedGoogle Scholar
• Adams JC, Lawler J. The thrombospondins. Int J Biochem Cell Biol. 2004;36:961–8.
   PubMed Web of Science ®Google Scholar
• Frangogiannis NG, Ren G, Dewald O, Zymek P, Haudek S, Koerting A, . Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation. 2005;111:2935–42.
   PubMed Web of Science ®Google Scholar
• Swinnen M, Vanhoutte D, Van Almen GC, Hamdani N, Schellings MW, D'hooge J, . Absence of thrombospondin-2 causes age-related dilated cardiomyopathy. Circulation. 2009;120:1585–97.
   Google Scholar
• Blankesteijn WM, Creemers E, Lutgens E, Cleutjens JP, Daemen MJ, Smits JF. Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice. Acta Physiol Scand. 2001;1731:75–82.
   Google Scholar
• Schroen B, Heymans S, Sharma U, Blankesteijn WM, Pokharel S, Cleutjens JP, . Thrombospondin-2 is essential for myocardial matrix integrity: increased expression identifies failure-prone cardiac hypertrophy. Circ Res. 2004;95: 515–22.
   PubMed Web of Science ®Google Scholar
• Adolph KW. Relative abundance of thrombospondin 2 and thrombospondin 3 mRNAs in human tissues. Biochem Biophys Res Commun. 1999;258:792–6.
   PubMedGoogle Scholar
• Tan FL, Moravec CS, Li J, Apperson-Hansen C, McCarthy PM, Young JB, . The gene expression fingerprint of human heart failure. Proc Natl Acad Sci U S A. 2002;99: 11387–92.
   PubMed Web of Science ®Google Scholar
• Gabrielsen A, Lawler PR, Yongzhong W, Steinbruchel D, Blagoja D, Paulsson-Berne G, . Gene expression signals involved in ischemic injury, extracellular matrix composition and fibrosis defined by global mRNA profiling of the human left ventricular myocardium. J Mol Cell Cardiol. 2007;42: 870–83.
   PubMed Web of Science ®Google Scholar
• Rysä J, Leskinen H, Ilves M, Ruskoaho H. Distinct upregulation of extracellular matrix genes in transition from hypertrophy to hypertensive heart failure. Hypertension. 2005;45: 927–33.
   PubMed Web of Science ®Google Scholar
• Moens AL, Cingolani O, Spinale FS, Kass DA. Exacerbated cardiac remodeling to pressure-overload in mice lacking thrombospondin-4. Hypertension. 2008;52:747–75.
   Google Scholar
• Frolova E, Sopko N, Penn M, Stenina O, Plow E. Heart hypertrophy in response to pressure overload in TSP4 knockout mice. FASEB J. 2009;23(Meeting Abstracts):642. 5–642.5.
   Google Scholar
• Narouz-Ott L, Maurer P, Nitsche DP, Smyth N, Paulsson M. Thrombospondin-4 binds specifically to both collagenous and non-collagenous extracellular matrix proteins via its C-terminal domains. J Biol Chem. 2000;275:37110–7.
   PubMed Web of Science ®Google Scholar
• Sodersten F, Ekman S, Niehoff A, Zaucke F, Heinegard D, Hultenby K. Ultrastructural immunolocalization of cartilage oligomeric matrix protein, thrombospondin-4, and collagen fibril size in rodent achilles tendon in relation to exercise. Connect Tissue Res. 2007;48:254–62.
   PubMed Web of Science ®Google Scholar
• Halasz K, Kassner A, Morgelin M, Heinegard D. COMP acts as a catalyst in collagen fibrillogenesis. J Biol Chem. 2007;282:31166–73.
   PubMed Web of Science ®Google Scholar
• Mustonen E, Aro J, Puhakka J, Ilves M, Soini Y, Leskinen H, . Thrombospondin-4 expression is rapidly upregulated by cardiac overload. Biochem Biophys Res Commun. 2008;373:186–91.
   PubMed Web of Science ®Google Scholar
• Stenina OI, Desai SY, Krukovets I, Kight K, Janigro D, Topol EJ, . Thrombospondin-4 and its variants: expression and differential effects on endothelial cells. Circulation. 2003;108:1514–9.
   Google Scholar
• Zhao XM, Hu Y, Miller GG, Mitchell RN, Libby P. Association of thrombospondin-1 and cardiac allograft vasculopathy in human cardiac allografts. Circulation. 2001;103: 525–31.
   Google Scholar
• Sezaki S, Hirohata S, Iwabu A, Nakamura K, Toeda K, Miyoshi T, . Thrombospondin-1 is induced in rat myocardial infarction and its induction is accelerated by ischemia/reperfusion. Exp Biol Med (Maywood). 2005;230:621–30.
   Google Scholar
• Mustonen E, Leskinen H, Aro J, Luodonpää M, Vuolteenaho O, Ruskoaho H, . Metoprolol treatment lowers thrombospondin-4 expression in rats with myocardial infarction and left ventricular hypertrophy. Basic Clin Pharmacol Toxicol. 2010;107:709–17.
   Google Scholar
• Fang C, Carlson CS, Leslie MP, Tulli H, Stolerman E, Perris R, . Molecular cloning, sequencing, and tissue and developmental expression of mouse cartilage oligomeric matrix protein (COMP). J Orthop Res. 2000;18:593–603.
   Google Scholar
• Kipnes JR, Xu L, Han F, Rallapalli R, Jimenez S, Hall DJ, . Molecular cloning and expression patterns of mouse cartilage oligomeric matrix protein gene. Osteoarthritis Cartilage. 2000;8:236–9.
   Google Scholar
• Svensson L, Aszódi A, Heinegård D, Hunziker EB, Reinholt FB, Fässler R, . Cartilage oligomeric matrix protein-deficient mice have normal skeletal development. Mol Cell Biol. 2002;22:4366–71.
   PubMed Web of Science ®Google Scholar
• Bornstein P, Agah A, Kyriakides TR. The role of thrombospondins 1 and 2 in the regulation of cell–matrix interactions, collagen fibril formation, and the response to injury. Int J Biochem Cell Biol. 2004;36:1115–25.
   PubMed Web of Science ®Google Scholar
• Frolova E, Pluskota E, Krukovets I, Burke T, Drumm C, Smith JD, . Thrombospondin-4 regulates vascular inflammation and atherogenesis. Circ Res. 2010;107: 1313–25.
   PubMed Web of Science ®Google Scholar
• Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, . TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem. 1997;272;51:32401–10.
   Google Scholar
• Brown SA, Ghosh A, Winkles JA. Full-length, membrane-anchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-kappaB pathway. J Biol Chem. 2010;285:17432–41.
   Google Scholar
• Meighan-Mantha RL, Hsu DK, Guo Y, Brown SA, Feng SL, Peifley KA, . The mitogen-inducible Fn14 gene encodes a type I transmembrane protein that modulates fibroblast adhesion and migration. J Biol Chem. 1999;274: 33166–76.
   PubMed Web of Science ®Google Scholar
• Wiley SR, Cassiano L, Lofton T, Davis-Smith T, Winkles JA, Lindner V, . A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity. 2001;155:837–46.
   Google Scholar
• Chorianopoulos E, Heger T, Lutz M, Frank D, Bea F, Katus HA, . FGF-inducible 14-kDa protein (Fn14) is regulated via the RhoA/ROCK kinase pathway in cardiomyocytes and mediates nuclear factor-kappaB activation by TWEAK. Basic Res Cardiol. 2010;105:301–13.
   PubMed Web of Science ®Google Scholar
• Jain M, Jakubowski A, Cui L, Shi J, Su L, Bauer M, . A novel role for tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in the development of cardiac dysfunction and failure. Circulation. 2009;119:2058–68.
   PubMed Web of Science ®Google Scholar
• Feng SL, Guo Y, Factor VM, Thorgeirsson SS, Bell DW, Testa JR, . The Fn14 immediate-early response gene is induced during liver regeneration and highly expressed in both human and murine hepatocellular carcinomas. Am J Pathol. 2000;156:1253–61.
   PubMed Web of Science ®Google Scholar
• Winkles JA. The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nat Rev Drug Discov. 2008;75:411–25.
   Google Scholar
• Burkly LC, Michaelson JS, Hahm K, Jakubowski A, Zheng TS. TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine. 2007;40:1–16.
   PubMed Web of Science ®Google Scholar
• Mustonen E, Säkkinen H, Tokola H, Isopoussu E, Aro J, Leskinen H, . Tumour necrosis factor-like weak inducer of apoptosis (TWEAK) and its receptor Fn14 during cardiac remodelling in rats. Acta Physiol (Oxf). 2010;199: 11–22.
   Google Scholar
• Chorianopoulos E, Rosenberg M, Zugck C, Wolf J, Katus HA, Frey N. Decreased soluble TWEAK levels predict an adverse prognosis in patients with chronic stable heart failure. Eur J Heart Fail. 2009;11:1050–6.
   PubMed Web of Science ®Google Scholar
• Richter B, Rychli K, Hohensinner PJ, Berger R, Mortl D, Neuhold S, . Differences in the predictive value of tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in advanced ischemic and non-ischemic heart failure. Atherosclerosis. 2010;213:545–8.
   PubMed Web of Science ®Google Scholar
• Chorianopoulos E, Jarr K, Steen H, Giannitsis E, Frey N, Katus HA. Soluble TWEAK is markedly upregulated in patients with ST-elevation myocardial infarction and related to an adverse short-term outcome. Atherosclerosis. 2010;211: 322–26.
   Google Scholar
• Meyer T, Amaya M, Desai H, Robles-Carrillo L, Hatfield M, Francis JL, . Human platelets contain and release TWEAK. Platelets. 2010;21:571–4.
   PubMed Web of Science ®Google Scholar
• Maecker H, Varfolomeev E, Kischkel F, Lawrence D, LeBlanc H, Lee W, . TWEAK attenuates the transition from innate to adaptive immunity. Cell. 2005;123:931–44.
   PubMed Web of Science ®Google Scholar
• Jakubowski A, Ambrose C, Parr M, Lincecum JM, Wang MZ, Zheng TS, . TWEAK induces liver progenitor cell proliferation. J Clin Invest. 2005;115:2330–40.
   PubMed Web of Science ®Google Scholar
• Mittal A, Bhatnagar S, Kumar A, Lach-Trifilieff E, Wauters S, Li H, . The TWEAK-Fn14 system is a critical regulator of denervation-induced skeletal muscle atrophy in mice. J Cell Biol. 2010;188:833–49.
   PubMedGoogle Scholar
• Ortiz A, Sanz AB, Munoz Garcia B, Moreno JA, Sanchez Nino MD, Martin-Ventura JL, . Considering TWEAK as a target for therapy in renal and vascular injury. Cytokine Growth Factor Rev. 2009;20:251–8.
   PubMed Web of Science ®Google Scholar
• Hotta K, Sho M, Yamato I, Shimada K, Harada H, Akahori T, . Direct targeting of fibroblast growth factor-inducible 14 protein protects against renal ischemia reperfusion injury. Kidney Int. 2011;79:179–88.
   PubMed Web of Science ®Google Scholar
• Li H, Mittal A, Paul PK, Kumar M, Srivastava DS, Tyagi SC, . Tumor necrosis factor-related weak inducer of apoptosis augments matrix metalloproteinase 9 (MMP-9) production in skeletal muscle through the activation of nuclear factor-κB-inducing kinase and p38 mitogen-activated protein kinase: a potential role of MMP-9 in myopathy. J Biol Chem. 2009;284:4439–50.
   PubMedGoogle Scholar
• Dogra C, Hall SL, Wedhas N, Linkhart TA, Kumar A. Fibroblast growth factor inducible 14 (Fn14) is required for the expression of myogenic regulatory factors and differentiation of myoblasts into myotubes. Evidence for TWEAK-independent functions of Fn14 during myogenesis. J Biol Chem. 2007;282:15000–10.
   Google Scholar
• Bover LC, Cardo-Vila M, Kuniyasu A, Sun J, Rangel R, Takeya M, . A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. J Immunol. 2007;178:8183–94.
   PubMed Web of Science ®Google Scholar
• Polek TC, Talpaz M, Darnay BG, Spivak-Kroizman T. TWEAK mediates signal transduction and differentiation of RAW264.7 cells in the absence of Fn14/TweakR. Evidence for a second TWEAK receptor. J Biol Chem. 2003;278:32317–23.
   PubMed Web of Science ®Google Scholar
• De Ketelaere A, Vermeulen L, Vialard J, Van De Weyer I, Van Wauwe J, Haegeman G, . Involvement of GSK-3beta in TWEAK-mediated NF-kappaB activation. FEBS Lett. 2004;566:60–4.
   PubMed Web of Science ®Google Scholar
• Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand JL, Cohen-Tervaert JW, . Inflammation as a therapeutic target in heart failure? A scientific statement from the Translational Research Committee of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail. 2009;112:119–29.
   Google Scholar
• Bornstein P. Thrombospondins function as regulators of angiogenesis. J Cell Commun Signal. 2009;3:189–200.
   PubMed Web of Science ®Google Scholar
• Carlson CB, Lawler J, Mosher DF. Structures of thrombospondins. Cell Mol Life Sci. 2008;65:672–86.
   PubMed Web of Science ®Google Scholar
• Wiley SR, Winkles JA. TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev. 2003; 14:241–9.
   PubMed Web of Science ®Google Scholar
• Lawler J, Duquette M, Whittaker CA, Adams JC, McHenry K, DeSimone DW. Identification and characterization of thrombospondin-4, a new member of the thrombospondin gene family. J Cell Biol. 1993:120;1059–67.
   PubMed Web of Science ®Google Scholar
• Wang D, Oparil S, Feng JA, Li P, Perry G, Chen LB, . Effects of pressure overload on extracellular matrix expression in the heart of the atrial natriuretic peptide-null mouse. Hypertension. 2003;42:88–95.
   PubMed Web of Science ®Google Scholar
• Zhang XM, Shen F, Xv ZY, Yan ZY, Han S. Expression changes of thrombospondin-1 and neuropeptide Y in myocardium of STZ-induced rats. Int J Cardiol. 2005;105: 192–7.
   PubMed Web of Science ®Google Scholar
• van Almen GC, Swinnen M, Carai P, Verhesen W, Cleutjens JP, D'hooge J, . Absence of thrombospondin-2 increases cardiomyocyte damage and matrix disruption in doxorubicin-induced cardiomyopathy. J Mol Cell Cardiol. 2011;51:318–28.
   Google Scholar