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Characteristic adaptations of the extracellular matrix in dilated cardiomyopathy

  • Laura Louzao-Martinez
    Affiliations
    Department of Nephrology and Hypertension, Division of Internal Medicine and Dermatology, University Medical Center Utrecht, The Netherlands

    Netherlands Heart Institute, University Medical Center Utrecht, The Netherlands
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  • Aryan Vink
    Affiliations
    Department of Pathology, University Medical Center Utrecht, The Netherlands
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  • Magdalena Harakalova
    Affiliations
    Netherlands Heart Institute, University Medical Center Utrecht, The Netherlands

    Department of Pathology, University Medical Center Utrecht, The Netherlands

    Department of Cardiology, Division of Heart and Lungs, University Medical Center Utrecht, The Netherlands
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  • Folkert W. Asselbergs
    Affiliations
    Netherlands Heart Institute, University Medical Center Utrecht, The Netherlands

    Department of Cardiology, Division of Heart and Lungs, University Medical Center Utrecht, The Netherlands

    Institute of Cardiovascular Science, Faculty of Population Health Sciences, University College London, United Kingdom
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  • Marianne C. Verhaar
    Affiliations
    Department of Nephrology and Hypertension, Division of Internal Medicine and Dermatology, University Medical Center Utrecht, The Netherlands
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  • Caroline Cheng
    Correspondence
    Corresponding author at: Department of Nephrology and Hypertension, Division of Internal Medicine and Dermatology, University Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands.
    Affiliations
    Department of Nephrology and Hypertension, Division of Internal Medicine and Dermatology, University Medical Center Utrecht, The Netherlands

    Department of Cardiology, Thoraxcenter, Division of Experimental Cardiology, Erasmus University Medical Center Rotterdam, The Netherlands
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      Highlights

      • Dilated cardiomyopathy (DCM) involves extracellular matrix (ECM) adaptations.
      • GEO datasets analysis reveals a novel transcriptome-based catalogue of ECM genes associated with dilated cardiomyopathy.
      • ECM adaptations in DCM: 1) ECM synthesis and stabilization 2) fibroblast activity 3) collagens deposition 4) cell adhesion.

      Abstract

      Dilated cardiomyopathy (DCM) is a relatively common heart muscle disease characterized by the dilation and thinning of the left ventricle accompanied with left ventricular systolic dysfunction. Myocardial fibrosis is a major feature in DCM and therefore it is inevitable that corresponding extracellular matrix (ECM) changes are involved in DCM onset and progression. Increasing our understanding of how ECM adaptations are involved in DCM could be important for the development of future interventions. This review article discusses the molecular adaptations in ECM composition and structure that have been reported in both animal and human studies of DCM. Furthermore, we provide a transcriptome-based catalogue of ECM genes that are associated with DCM, generated by using NCBI Gene Expression Omnibus database sets for DCM. Based on this in silico analysis, many novel ECM components involved in DCM are identified and discussed in this review. With the information gathered, we propose putative pathways of ECM adaptations in onset and progression of DCM.

      Keywords

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      References

        • Maron B.J.
        • Towbin J.A.
        • Thiene G.
        • et al.
        Contemporary definitions and classification of the cardiomyopathies: an American Heart Association scientific statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention.
        Circulation. 2006; 113: 1807-1816
        • Wilkinson J.D.
        • Landy D.C.
        • Colan S.D.
        • et al.
        The pediatric cardiomyopathy registry and heart failure: key results from the first 15 years.
        Heart Fail. Clin. 2010; 6: 401-413
        • Elliott P.
        • Andersson B.
        • Arbustini E.
        • et al.
        Classification of the cardiomyopathies: a position statement from the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases.
        Eur. Heart J. 2008; 29: 270-276
        • Rubis P.
        The diagnostic work up of genetic and inflammatory dilated cardiomyopathy.
        Cardiol. Pract. 2015; 13
        • Gopal D.M.
        • Sam F.
        New and emerging biomarkers in left ventricular systolic dysfunction—insight into dilated cardiomyopathy.
        J. Cardiovasc. Transl. Res. 2013; 6: 516-527
        • Michels V.V.
        • Driscoll D.J.
        • Miller F.A.
        • et al.
        Progression of familial and non-familial dilated cardiomyopathy: long term follow up.
        Heart. 2003; 89: 757-761
        • Hershberger R.E.
        • Hedges D.J.
        • Morales A.
        Dilated cardiomyopathy: the complexity of a diverse genetic architecture.
        Nat. Rev. Cardiol. 2013; 10: 531-547
        • McNally E.M.
        • Golbus J.R.
        • Puckelwartz M.J.
        Genetic mutations and mechanisms in dilated cardiomyopathy.
        J. Clin. Invest. 2013; 123: 19-26
        • Harakalova M.
        • Kummeling G.
        • Sammani A.
        • et al.
        A systematic analysis of genetic dilated cardiomyopathy reveals numerous ubiquitously expressed and muscle-specific genes.
        Eur. J. Heart Fail. 2015; 17: 484-493
        • Brooks A.
        • Schinde V.
        • Bateman A.C.
        • Gallagher P.J.
        Interstitial fibrosis in the dilated non-ischaemic myocardium.
        Heart. 2003; 89: 1255-1256
        • Heneghan M.A.
        • Malone D.
        • Dervan P.A.
        Myocardial collagen network in dilated cardiomyopathy. Morphometry and scanning electron microscopy study.
        Ir. J. Med. Sci. 1991; 160: 399-401
        • Unverferth D.V.
        • Baker P.B.
        • Swift S.E.
        • et al.
        Extent of myocardial fibrosis and cellular hypertrophy in dilated cardiomyopathy.
        Am. J. Cardiol. 1986; 57: 816-820
        • Weber K.T.
        • Pick R.
        • Silver M.A.
        • et al.
        Fibrillar collagen and remodeling of dilated canine left ventricle.
        Circulation. 1990; 82: 1387-1401
        • Caulfield J.B.
        • Wolkowicz P.E.
        Myocardial connective tissue alterations.
        Toxicol. Pathol. 1990; 18: 488-496
        • Jellis C.
        • Martin J.
        • Narula J.
        • Marwick T.H.
        Assessment of nonischemic myocardial fibrosis.
        J. Am. Coll. Cardiol. 2010; 56: 89-97
        • Okada H.
        • Kawaguchi H.
        • Kudo T.
        • et al.
        Alteration of extracellular matrix in dilated cardiomyopathic hamster heart.
        Mol. Cell. Biochem. 1996; 156: 9-15
        • Masutomo K.
        • Makino N.
        • Maruyama T.
        • Shimada T.
        • Yanaga T.
        Effects of enalapril on the collagen matrix in cardiomyopathic Syrian hamsters (bio 14.6 and 53.58).
        Jpn. Circ. J. 1996; 60: 50-61
        • Woodiwiss A.J.
        • Tsotetsi O.J.
        • Sprott S.
        • et al.
        Reduction in myocardial collagen cross-linking parallels left ventricular dilatation in rat models of systolic chamber dysfunction.
        Circulation. 2001; 103: 155-160
        • Kapelko V.I.
        Extracellular matrix alterations in cardiomyopathy: the possible crucial role in the dilative form.
        Exp. Clin. Cardiol. 2001; 6: 41-49
        • Tyagi S.C.
        • Kumar S.G.
        • Banks J.
        • Fortson W.
        Co-expression of tissue inhibitor and matrix metalloproteinase in myocardium.
        J. Mol. Cell. Cardiol. 1995; 27: 2177-2189
        • Coker M.L.
        • Thomas C.V.
        • Clair M.J.
        • et al.
        Myocardial matrix metalloproteinase activity and abundance with congestive heart failure.
        Am. J. Phys. 1998; 274: H1516-H1523
        • McElmurray 3rd, J.H.
        • Mukherjee R.
        • New R.B.
        • et al.
        Angiotensin-converting enzyme and matrix metalloproteinase inhibition with developing heart failure: comparative effects on left ventricular function and geometry.
        J. Pharmacol. Exp. Ther. 1999; 291: 799-811
        • Spinale F.G.
        • Coker M.L.
        • Krombach S.R.
        • et al.
        Matrix metalloproteinase inhibition during the development of congestive heart failure: effects on left ventricular dimensions and function.
        Circ. Res. 1999; 85: 364-376
        • Spinale F.G.
        • Coker M.L.
        • Thomas C.V.
        • Walker J.D.
        • Mukherjee R.
        • Hebbar L.
        Time-dependent changes in matrix metalloproteinase activity and expression during the progression of congestive heart failure: relation to ventricular and myocyte function.
        Circ. Res. 1998; 82: 482-495
        • Spinale F.G.
        • Tomita M.
        • Zellner J.L.
        • Cook J.C.
        • Crawford F.A.
        • Zile M.R.
        Collagen remodeling and changes in lv function during development and recovery from supraventricular tachycardia.
        Am. J. Phys. 1991; 261: H308-H318
        • Spinale F.G.
        • Zellner J.L.
        • Johnson W.S.
        • Eble D.M.
        • Munyer P.D.
        Cellular and extracellular remodeling with the development and recovery from tachycardia-induced cardiomyopathy: changes in fibrillar collagen, myocyte adhesion capacity and proteoglycans.
        J. Mol. Cell. Cardiol. 1996; 28: 1591-1608
        • Chancey A.L.
        • Brower G.L.
        • Peterson J.T.
        • Janicki J.S.
        Effects of matrix metalloproteinase inhibition on ventricular remodeling due to volume overload.
        Circulation. 2002; 105: 1983-1988
        • Peterson J.T.
        • Hallak H.
        • Johnson L.
        • et al.
        Matrix metalloproteinase inhibition attenuates left ventricular remodeling and dysfunction in a rat model of progressive heart failure.
        Circulation. 2001; 103: 2303-2309
        • Rohde L.E.
        • Ducharme A.
        • Arroyo L.H.
        • et al.
        Matrix metalloproteinase inhibition attenuates early left ventricular enlargement after experimental myocardial infarction in mice.
        Circulation. 1999; 99: 3063-3070
        • Fedak P.W.
        • Smookler D.S.
        • Kassiri Z.
        • et al.
        Timp-3 deficiency leads to dilated cardiomyopathy.
        Circulation. 2004; 110: 2401-2409
        • Nishikawa N.
        • Yamamoto K.
        • Sakata Y.
        • et al.
        Differential activation of matrix metalloproteinases in heart failure with and without ventricular dilatation.
        Cardiovasc. Res. 2003; 57: 766-774
        • Sivasubramanian N.
        • Coker M.L.
        • Kurrelmeyer K.M.
        • et al.
        Left ventricular remodeling in transgenic mice with cardiac restricted overexpression of tumor necrosis factor.
        Circulation. 2001; 104: 826-831
        • Li J.
        • Schwimmbeck P.L.
        • Tschope C.
        • et al.
        Collagen degradation in a murine myocarditis model: relevance of matrix metalloproteinase in association with inflammatory induction.
        Cardiovasc. Res. 2002; 56: 235-247
        • Cheung C.
        • Luo H.
        • Yanagawa B.
        • et al.
        Matrix metalloproteinases and tissue inhibitors of metalloproteinases in coxsackievirus-induced myocarditis.
        Cardiovasc. Pathol. 2006; 15: 63-74
        • Heymans S.
        • Pauschinger M.
        • De Palma A.
        • et al.
        Inhibition of urokinase-type plasminogen activator or matrix metalloproteinases prevents cardiac injury and dysfunction during viral myocarditis.
        Circulation. 2006; 114: 565-573
        • Szabo Z.
        • Magga J.
        • Alakoski T.
        • et al.
        Connective tissue growth factor inhibition attenuates left ventricular remodeling and dysfunction in pressure overload-induced heart failure.
        Hypertension. 2014; 63: 1235-1240
        • Hutchinson K.R.
        • Guggilam A.
        • Cismowski M.J.
        • et al.
        Temporal pattern of left ventricular structural and functional remodeling following reversal of volume overload heart failure.
        J. Appl. Physiol. 2011; 111: 1778-1788
        • Gunja-Smith Z.
        • Morales A.R.
        • Romanelli R.
        • Woessner Jr., J.F.
        Remodeling of human myocardial collagen in idiopathic dilated cardiomyopathy. Role of metalloproteinases and pyridinoline cross-links.
        Am. J. Pathol. 1996; 148: 1639-1648
        • Stetler-Stevenson W.G.
        Dynamics of matrix turnover during pathologic remodeling of the extracellular matrix.
        Am. J. Pathol. 1996; 148: 1345-1350
        • Bishop J.E.
        • Greenbaum R.
        • Gibson D.G.
        • Yacoub M.
        • Laurent G.J.
        Enhanced deposition of predominantly type I collagen in myocardial disease.
        J. Mol. Cell. Cardiol. 1990; 22: 1157-1165
        • Khan S.
        • Joyce J.
        • Margulies K.B.
        • Tsuda T.
        Enhanced bioactive myocardial transforming growth factor-beta in advanced human heart failure.
        Circ. J. 2014; 78: 2711-2718
        • Klotz S.
        • Foronjy R.F.
        • Dickstein M.L.
        • et al.
        Mechanical unloading during left ventricular assist device support increases left ventricular collagen cross-linking and myocardial stiffness.
        Circulation. 2005; 112: 364-374
        • Marijianowski M.M.
        • Teeling P.
        • Mann J.
        • Becker A.E.
        Dilated cardiomyopathy is associated with an increase in the type I/type III collagen ratio: a quantitative assessment.
        J. Am. Coll. Cardiol. 1995; 25: 1263-1272
        • Pauschinger M.
        • Doerner A.
        • Remppis A.
        • Tannhauser R.
        • Kuhl U.
        • Schultheiss H.P.
        Differential myocardial abundance of collagen type I and type III mRNA in dilated cardiomyopathy: effects of myocardial inflammation.
        Cardiovasc. Res. 1998; 37: 123-129
        • Pauschinger M.
        • Knopf D.
        • Petschauer S.
        • et al.
        Dilated cardiomyopathy is associated with significant changes in collagen type I/III ratio.
        Circulation. 1999; 99: 2750-2756
        • Sivakumar P.
        • Gupta S.
        • Sarkar S.
        • Sen S.
        Upregulation of lysyl oxidase and MMPs during cardiac remodeling in human dilated cardiomyopathy.
        Mol. Cell. Biochem. 2008; 307: 159-167
        • Yoshikane H.
        • Honda M.
        • Goto Y.
        • Morioka S.
        • Ooshima A.
        • Moriyama K.
        Collagen in dilated cardiomyopathy—scanning electron microscopic and immunohistochemical observations.
        Jpn. Circ. J. 1992; 56: 899-910
        • Mollnau H.
        • Munkel B.
        • Schaper J.
        Collagen vi in the extracellular matrix of normal and failing human myocardium.
        Herz. 1995; 20: 89-94
        • Reddy H.K.
        • Tjahja I.E.
        • Campbell S.E.
        • Janicki J.S.
        • Hayden M.R.
        • Tyagi S.C.
        Expression of matrix metalloproteinase activity in idiopathic dilated cardiomyopathy: a marker of cardiac dilatation.
        Mol. Cell. Biochem. 2004; 264: 183-191
        • Tyagi S.C.
        • Campbell S.E.
        • Reddy H.K.
        • Tjahja E.
        • Voelker D.J.
        Matrix metalloproteinase activity expression in infarcted, noninfarcted and dilated cardiomyopathic human hearts.
        Mol. Cell. Biochem. 1996; 155: 13-21
        • Tyagi S.C.
        • Kumar S.
        • Voelker D.J.
        • Reddy H.K.
        • Janicki J.S.
        • Curtis J.J.
        Differential gene expression of extracellular matrix components in dilated cardiomyopathy.
        J. Cell. Biochem. 1996; 63: 185-198
        • Rouet-Benzineb P.
        • Buhler J.M.
        • Dreyfus P.
        • et al.
        Altered balance between matrix gelatinases (MMP-2 and MMP-9) and their tissue inhibitors in human dilated cardiomyopathy: potential role of MMP-9 in myosin-heavy chain degradation.
        Eur. J. Heart Fail. 1999; 1: 337-352
        • Spinale F.G.
        • Coker M.L.
        • Heung L.J.
        • et al.
        A matrix metalloproteinase induction/activation system exists in the human left ventricular myocardium and is upregulated in heart failure.
        Circulation. 2000; 102: 1944-1949
        • Thomas C.V.
        • Coker M.L.
        • Zellner J.L.
        • Handy J.R.
        • Crumbley 3rd, A.J.
        • Spinale F.G.
        Increased matrix metalloproteinase activity and selective upregulation in lv myocardium from patients with end-stage dilated cardiomyopathy.
        Circulation. 1998; 97: 1708-1715
        • Klappacher G.
        • Franzen P.
        • Haab D.
        • et al.
        Measuring extracellular matrix turnover in the serum of patients with idiopathic or ischemic dilated cardiomyopathy and impact on diagnosis and prognosis.
        Am. J. Cardiol. 1995; 75: 913-918
        • Schwartzkopff B.
        • Fassbach M.
        • Pelzer B.
        • Brehm M.
        • Strauer B.E.
        Elevated serum markers of collagen degradation in patients with mild to moderate dilated cardiomyopathy.
        Eur. J. Heart Fail. 2002; 4 (439-434)
        • Yan A.T.
        • Yan R.T.
        • Spinale F.G.
        • et al.
        Plasma matrix metalloproteinase-9 level is correlated with left ventricular volumes and ejection fraction in patients with heart failure.
        J. Card. Fail. 2006; 12: 514-519
        • Jordan A.
        • Roldan V.
        • Garcia M.
        • et al.
        Matrix metalloproteinase-1 and its inhibitor, TIMP-1, in systolic heart failure: relation to functional data and prognosis.
        J. Intern. Med. 2007; 262: 385-392
        • Naito Y.
        • Tsujino T.
        • Lee-Kawabata M.
        • et al.
        Matrix metalloproteinase-1 and -2 levels are differently regulated in acute exacerbation of heart failure in patients with and without left ventricular systolic dysfunction.
        Heart Vessel. 2009; 24: 181-186
        • Terasaki F.
        • Okamoto H.
        • Onishi K.
        • et al.
        Higher serum tenascin-C levels reflect the severity of heart failure, left ventricular dysfunction and remodeling in patients with dilated cardiomyopathy.
        Circ. J. 2007; 71: 327-330
        • Tamura A.
        • Kusachi S.
        • Nogami K.
        • et al.
        Tenascin expression in endomyocardial biopsy specimens in patients with dilated cardiomyopathy: distribution along margin of fibrotic lesions.
        Heart. 1996; 75: 291-294
        • Herpel E.
        • Singer S.
        • Flechtenmacher C.
        • et al.
        Extracellular matrix proteins and matrix metalloproteinases differ between various right and left ventricular sites in end-stage cardiomyopathies.
        Virchows Arch. 2005; 446: 369-378
        • Nogami K.
        • Kusachi S.
        • Nunoyama H.
        • et al.
        Extracellular matrix components in dilated cardiomyopathy. Immunohistochemical study of endomyocardial biopsy specimens.
        Jpn. Heart J. 1996; 37: 483-494
        • Hsia T.Y.
        • Ringewald J.M.
        • Stroud R.E.
        • et al.
        Determinants of extracellular matrix remodelling are differentially expressed in paediatric and adult dilated cardiomyopathy.
        Eur. J. Heart Fail. 2011; 13: 271-277
        • Naba A.
        • Clauser K.R.
        • Hoersch S.
        • Liu H.
        • Carr S.A.
        • Hynes R.O.
        The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices.
        Mol. Cell. Proteomics. 2012; 11: 9
        • Naba A.
        • Clauser K.R.
        • Ding H.
        • Whittaker C.A.
        • Carr S.A.
        • Hynes R.O.
        The extracellular matrix: tools and insights for the “omics” era.
        Matrix Biol. 2015; 8: 00121-00123
        • Clausen T.
        • Kaiser M.
        • Huber R.
        • Ehrmann M.
        HTRA proteases: regulated proteolysis in protein quality control.
        Nat. Rev. Mol. Cell Biol. 2011; 12: 152-162
        • Yana I.
        • Weiss S.J.
        Regulation of membrane type-1 matrix metalloproteinase activation by proprotein convertases.
        Mol. Biol. Cell. 2000; 11: 2387-2401
        • Pihlajaniemi T.
        • Myllyla R.
        • Kivirikko K.I.
        Prolyl 4-hydroxylase and its role in collagen synthesis.
        J. Hepatol. 1991; 13: S2-S7
        • Bader H.L.
        • Wang L.W.
        • Ho J.C.
        • et al.
        A disintegrin-like and metalloprotease domain containing thrombospondin type 1 motif-like 5 (ADAMTSL5) is a novel fibrillin-1-, fibrillin-2-, and heparin-binding member of the adamts superfamily containing a netrin-like module.
        Matrix Biol. 2012; 31: 398-411
        • Tsutsui K.
        • Manabe R.
        • Yamada T.
        • et al.
        ADAMTSL-6 is a novel extracellular matrix protein that binds to fibrillin-1 and promotes fibrillin-1 fibril formation.
        J. Biol. Chem. 2010; 285: 4870-4882
        • Bost F.
        • Diarra-Mehrpour M.
        • Martin J.P.
        Inter-alpha-trypsin inhibitor proteoglycan family—a group of proteins binding and stabilizing the extracellular matrix.
        Eur. J. Biochem. 1998; 252: 339-346
        • Bergqvist D.
        • Nilsson I.M.
        Hereditary alpha 2-macroglobulin deficiency.
        Scand. J. Haematol. 1979; 23: 433-436
        • Somerville R.P.
        • Longpre J.M.
        • Jungers K.A.
        • et al.
        Characterization of ADAMTS-9 and ADAMTS-20 as a distinct ADAMTS subfamily related to Caenorhabditis elegans GON-1.
        J. Biol. Chem. 2003; 278: 9503-9513
        • Bizet A.A.
        • Liu K.
        • Tran-Khanh N.
        • et al.
        The TGF-beta co-receptor, CD109, promotes internalization and degradation of TGF-beta receptors.
        Biochim. Biophys. Acta. 2011; 5: 742-753
        • Bonnefoy A.
        • Legrand C.
        Proteolysis of subendothelial adhesive glycoproteins (fibronectin, thrombospondin, and von Willebrand factor) by plasmin, leukocyte cathepsin G, and elastase.
        Thromb. Res. 2000; 98: 323-332
        • Carmeliet P.
        • Moons L.
        • Lijnen R.
        • et al.
        Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation.
        Nat. Genet. 1997; 17: 439-444
        • Leask A.
        TGFbeta, cardiac fibroblasts, and the fibrotic response.
        Cardiovasc. Res. 2007; 74: 207-212
        • Gospodarowicz D.
        Localisation of a fibroblast growth factor and its effect alone and with hydrocortisone on 3T3 cell growth.
        Nature. 1974; 249: 123-127
        • Bouleau S.
        • Grimal H.
        • Rincheval V.
        • et al.
        FGF1 inhibits p53-dependent apoptosis and cell cycle arrest via an intracrine pathway.
        Oncogene. 2005; 24: 7839-7849
        • Powers C.J.
        • McLeskey S.W.
        • Wellstein A.
        Fibroblast growth factors, their receptors and signaling.
        Endocr. Relat. Cancer. 2000; 7: 165-197
        • Li Y.S.
        • Milner P.G.
        • Chauhan A.K.
        • et al.
        Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity.
        Science. 1990; 250: 1690-1694
        • Bowden E.T.
        • Stoica G.E.
        • Wellstein A.
        Anti-apoptotic signaling of pleiotrophin through its receptor, anaplastic lymphoma kinase.
        J. Biol. Chem. 2002; 277: 35862-35868
        • Panse K.D.
        • Felkin L.E.
        • Lopez-Olaneta M.M.
        • et al.
        Follistatin-like 3 mediates paracrine fibroblast activation by cardiomyocytes.
        J. Cardiovasc. Transl. Res. 2012; 5: 814-826
        • Elson G.C.
        • Graber P.
        • Losberger C.
        • et al.
        Cytokine-like factor-1, a novel soluble protein, shares homology with members of the cytokine type i receptor family.
        J. Immunol. 1998; 161: 1371-1379
        • Sciaky D.
        • Brazer W.
        • Center D.M.
        • Cruikshank W.W.
        • Smith T.J.
        Cultured human fibroblasts express constitutive IL-16 mRNA: cytokine induction of active IL-16 protein synthesis through a caspase-3-dependent mechanism.
        J. Immunol. 2000; 164: 3806-3814
        • Liu X.
        • Das A.M.
        • Seideman J.
        • et al.
        The CC chemokine ligand 2 (CCL2) mediates fibroblast survival through IL-6.
        Am. J. Respir. Cell Mol. Biol. 2007; 37: 121-128
        • Orlandini M.
        • Marconcini L.
        • Ferruzzi R.
        • Oliviero S.
        Identification of a c-fos-induced gene that is related to the platelet-derived growth factor/vascular endothelial growth factor family.
        Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 11675-11680
        • Puxeddu I.
        • Bader R.
        • Piliponsky A.M.
        • Reich R.
        • Levi-Schaffer F.
        • Berkman N.
        The CC chemokine eotaxin/CCL11 has a selective profibrogenic effect on human lung fibroblasts.
        J. Allergy Clin. Immunol. 2006; 117: 103-110
        • Iwabu A.
        • Smith K.
        • Allen F.D.
        • Lauffenburger D.A.
        • Wells A.
        Epidermal growth factor induces fibroblast contractility and motility via a protein kinase C delta-dependent pathway.
        J. Biol. Chem. 2004; 279: 14551-14560
        • Lembach K.J.
        Induction of human fibroblast proliferation by epidermal growth factor (EGF): enhancement by an EGF-binding arginine esterase and by ascorbate.
        Proc. Natl. Acad. Sci. U. S. A. 1976; 73: 183-187
        • Westermark B.
        • Blomquist E.
        Stimulation of fibroblast migration by epidermal growth factor.
        Cell Biol. Int. Rep. 1980; 4: 649-654
        • You D.H.
        • Nam M.J.
        Effects of human epidermal growth factor gene-transfected mesenchymal stem cells on fibroblast migration and proliferation.
        Cell Prolif. 2013; 46: 408-415
        • Kajanne R.
        • Miettinen P.
        • Mehlem A.
        • et al.
        EGF-R regulates MMP function in fibroblasts through MAPK and AP-1 pathways.
        J. Cell. Physiol. 2007; 212: 489-497
        • Yamane K.
        • Asano Y.
        • Tamaki K.
        • Ihn H.
        Epidermal growth factor up-regulates transforming growth factor-beta receptor type II in human dermal fibroblasts via p38 mitogen-activated protein kinase pathway.
        Biochem. Biophys. Res. Commun. 2007; 352: 69-77
        • LeRoy E.C.
        • Trojanowska M.I.
        • Smith E.A.
        Cytokines and human fibrosis.
        Eur. Cytokine Netw. 1990; 1: 215-219
        • Struyf S.
        • Proost P.
        • Vandercappellen J.
        • et al.
        Synergistic up-regulation of MCP-2/CCL8 activity is counteracted by chemokine cleavage, limiting its inflammatory and anti-tumoral effects.
        Eur. J. Immunol. 2009; 39: 843-857
        • Heino J.
        The collagen family members as cell adhesion proteins.
        BioEssays. 2007; 29: 1001-1010
        • Wenstrup R.J.
        • Florer J.B.
        • Brunskill E.W.
        • Bell S.M.
        • Chervoneva I.
        • Birk D.E.
        Type v collagen controls the initiation of collagen fibril assembly.
        J. Biol. Chem. 2004; 279: 53331-53337
        • Monroe G.R.
        • Harakalova M.
        • van der Crabben S.N.
        • et al.
        Familial Ehlers–Danlos syndrome with lethal arterial events caused by a mutation in COL5A1.
        Am. J. Med. Genet. A. 2015; 167: 1196-1203
        • van der Rest M.
        • Garrone R.
        Collagen family of proteins.
        FASEB J. 1991; 5: 2814-2823
        • Walchli C.
        • Koch M.
        • Chiquet M.
        • Odermatt B.F.
        • Trueb B.
        Tissue-specific expression of the fibril-associated collagens XII and XIV.
        J. Cell Sci. 1994; 107: 669-681
        • Fitzgerald J.
        • Bateman J.F.
        A new facit of the collagen family: COL21A1.
        FEBS Lett. 2001; 505: 275-280
        • Tao G.
        • Levay A.K.
        • Peacock J.D.
        • et al.
        Collagen XIV is important for growth and structural integrity of the myocardium.
        J. Mol. Cell. Cardiol. 2012; 53: 626-638
        • Van Agtmael T.
        • Bailey M.A.
        • Schlotzer-Schrehardt U.
        • et al.
        COL4A1 mutation in mice causes defects in vascular function and low blood pressure associated with reduced red blood cell volume.
        Hum. Mol. Genet. 2010; 19: 1119-1128
        • Gould D.B.
        • Phalan F.C.
        • van Mil S.E.
        • et al.
        Role of COL4A1 in small-vessel disease and hemorrhagic stroke.
        N. Engl. J. Med. 2006; 354: 1489-1496
        • Verbeek E.
        • Meuwissen M.E.
        • Verheijen F.W.
        • et al.
        COL4A2 mutation associated with familial porencephaly and small-vessel disease.
        Eur. J. Hum. Genet. 2012; 20: 844-851
        • Adiguzel E.
        • Hou G.
        • Mulholland D.
        • et al.
        Migration and growth are attenuated in vascular smooth muscle cells with type VIII collagen-null alleles.
        Arterioscler. Thromb. Vasc. Biol. 2006; 26: 56-61
        • Pankov R.
        • Yamada K.M.
        Fibronectin at a glance.
        J. Cell Sci. 2002; 115: 3861-3863
        • Hyytiainen M.
        • Penttinen C.
        • Keski-Oja J.
        Latent TGF-beta binding proteins: extracellular matrix association and roles in TGF-beta activation.
        Crit. Rev. Clin. Lab. Sci. 2004; 41: 233-264
        • Dallas S.L.
        • Sivakumar P.
        • Jones C.J.
        • et al.
        Fibronectin regulates latent transforming growth factor-beta (TGF beta) by controlling matrix assembly of latent TGF beta-binding protein-1.
        J. Biol. Chem. 2005; 280: 18871-18880
        • Kanzaki T.
        • Shiina R.
        • Saito Y.
        • Oohashi H.
        • Morisaki N.
        Role of latent TGF-beta 1 binding protein in vascular remodeling.
        Biochem. Biophys. Res. Commun. 1998; 246: 26-30
        • Zilberberg L.
        • Todorovic V.
        • Dabovic B.
        • et al.
        Specificity of latent TGF-beta binding protein (LTBP) incorporation into matrix: role of fibrillins and fibronectin.
        J. Cell. Physiol. 2012; 227: 3828-3836
        • Konstandin M.H.
        • Toko H.
        • Gastelum G.M.
        • et al.
        Fibronectin is essential for reparative cardiac progenitor cell response after myocardial infarction.
        Circ. Res. 2013; 113: 115-125
        • van Dijk A.
        • Niessen H.W.
        • Ursem W.
        • Twisk J.W.
        • Visser F.C.
        • van Milligen F.J.
        Accumulation of fibronectin in the heart after myocardial infarction: a putative stimulator of adhesion and proliferation of adipose-derived stem cells.
        Cell Tissue Res. 2008; 332: 289-298
        • Chen M.M.
        • Lam A.
        • Abraham J.A.
        • Schreiner G.F.
        • Joly A.H.
        CTGF expression is induced by TGF-beta in cardiac fibroblasts and cardiac myocytes: a potential role in heart fibrosis.
        J. Mol. Cell. Cardiol. 2000; 32: 1805-1819
        • Frazier K.
        • Williams S.
        • Kothapalli D.
        • Klapper H.
        • Grotendorst G.R.
        Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor.
        J. Invest. Dermatol. 1996; 107: 404-411
        • Kato A.
        • Okamoto O.
        • Ishikawa K.
        • et al.
        Dermatopontin interacts with fibronectin, promotes fibronectin fibril formation, and enhances cell adhesion.
        J. Biol. Chem. 2011; 286: 14861-14869
        • Liu X.
        • Meng L.
        • Shi Q.
        • et al.
        Dermatopontin promotes adhesion, spreading and migration of cardiac fibroblasts in vitro.
        Matrix Biol. 2013; 32: 23-31
        • Tanaka K.
        • Arao T.
        • Maegawa M.
        • et al.
        SRPX2 is overexpressed in gastric cancer and promotes cellular migration and adhesion.
        Int. J. Cancer. 2009; 124: 1072-1080
        • Ohashi K.
        • Enomoto T.
        • Joki Y.
        • et al.
        Neuron-derived neurotrophic factor functions as a novel modulator that enhances endothelial cell function and revascularization processes.
        J. Biol. Chem. 2014; 289: 14132-14144
        • Bornstein P.
        • Devarayalu S.
        • Li P.
        • Disteche C.M.
        • Framson P.
        A second thrombospondin gene in the mouse is similar in organization to thrombospondin 1 but does not respond to serum.
        Proc. Natl. Acad. Sci. U. S. A. 1991; 88: 8636-8640
        • Murphy-Ullrich J.E.
        • Gurusiddappa S.
        • Frazier W.A.
        • Hook M.
        Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity.
        J. Biol. Chem. 1993; 268: 26784-26789
        • Yang Z.
        • Kyriakides T.R.
        • Bornstein P.
        Matricellular proteins as modulators of cell-matrix interactions: adhesive defect in thrombospondin 2-null fibroblasts is a consequence of increased levels of matrix metalloproteinase-2.
        Mol. Biol. Cell. 2000; 11: 3353-3364
        • Beattie J.
        • Kreiner M.
        • Allan G.J.
        • Flint D.J.
        • Domingues D.
        • van der Walle C.F.
        IGFBP-3 and IGFBP-5 associate with the cell binding domain (CBD) of fibronectin.
        Biochem. Biophys. Res. Commun. 2009; 381: 572-576
        • Zeng H.
        • Zhang Y.
        • Yi Q.
        • Wu Y.
        • Wan R.
        • Tang L.
        CRIM1, a newfound cancer-related player, regulates the adhesion and migration of lung cancer cells.
        Growth Factors. 2015; 33: 384-392