Syndecans in heart fibrosis

Cell and Tissue Research

Volumn 365, Issue 3, 2016, Pages 539-552

  Lunde, Ida G ^a,b   Herum, Kate M ^a,b   Carlson, Cathrine C ^a,b   Christensen, Geir ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Extracellular matrix; Infarction; Inflammation; Myofibroblast; Wound healing

Indexed keywords

CELL ADHESION MOLECULE; CELL ENZYME; COLLAGEN; CYTOKINE; EXTRACELLAR MATRIX ENZYME; GLYCOSAMINOGLYCAN; GROWTH FACTOR; MYOFIBROBLAST DIFFERENTIATION FACTOR; SYNDECAN; SYNDECAN 1; SYNDECAN 4; UNCLASSIFIED DRUG; PROTEOGLYCAN;

BINDING AFFINITY; BINDING SITE; CELL DIFFERENTIATION; DISEASE ACTIVITY; DISEASE ASSOCIATION; EXTRACELLULAR MATRIX; HEART MUSCLE FIBROSIS; HEART RUPTURE; HUMAN; MOLECULAR PATHOLOGY; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; ANIMAL; BIOLOGICAL MODEL; CARDIAC MUSCLE; FIBROSIS; METABOLISM; PATHOLOGY;

ANIMALS; EXTRACELLULAR MATRIX; FIBROSIS; HUMANS; MODELS, BIOLOGICAL; MYOCARDIUM; PROTEOGLYCANS; SYNDECANS;

EID: 84978174581     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-016-2454-2     Document Type: Review

References (99)

1. Almaas VM, Haugaa KH, Strøm EH, Scott H, Dahl CP, Leren TP, Geiran OR, Endresen K, Edvardsen T, Aakhus S, Amlie JP (2013) Increased amount of interstitial fibrosis predicts ventricular arrhythmias, and is associated with reduced myocardial septal function in patients with obstructive hypertrophic cardiomyopathy. Europace 15:1319–1327
2. Aramburu J, Garcia-Cózar F, Raghavan A, Okamura H, Rao A, Hogan PG (1998) Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol Cell 1:627–637
3. Barry SP, Townsend PA (2010) What causes a broken heart-molecular insights into heart failure. Int Rev Cell Mol Biol 284:113–179
4. Bellin RM, Kubicek JD, Frigault MJ, Kamien AJ, Steward RLJ, Barnes HM, Digiacomo MB, Duncan LJ, Edgerly CK, Morse EM, Park CY, Fredberg JJ, Cheng CM, LeDuc PR (2009) Defining the role of syndecan-4 in mechanotransduction using surface-modification approaches. Proc Natl Acad Sci U S A 106:22102–22107
5. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ (1992) Biology of the syndecans: a family of transmembrane heparan sulphate proteoglycans. Annu Rev Cell Biol 8:365–393
6. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729–777
7. Berry JM, Le V, Rotter D, Battiprolu PK, Grinsfelder B, Tannous P, Burchfield JS, Czubryt M, Backs J, Olson EN, Rothermel BA, Hill JA (2011) Reversibility of adverse, calcineurin-dependent cardiac remodeling. Circ Res 109:407–417
8. Bielecka-Dabrowa A, Haehling S von, Aronow WS, Ahmed MI, Rysz J, Banach M (2013) Heart failure biomarkers in patients with dilated cardiomyopathy. Int J Cardiol 168:2404–2410
9. Bielecka-Dabrowa A, Gluba-Brzózka A, Michalska-Kasiczak M, Misztal M, Rysz J, Banach M (2015a) The multi-biomarker approach for heart failure in patients with hypertension. Int J Mol Sci 16:10715–10733
10. Bielecka-Dabrowa A, Michalska-Kasiczak M, Gluba A, Ahmed A, Gerdts E, Haehling S von, Rysz J, Banach M (2015b) Biomarkers and echocardiographic predictors of myocardial dysfunction in patients with hypertension. Sci Rep 5:8916
11. Bishop JR, Schuksz M, Esko JD (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446:1030–1037
12. Braunwald E, Bristow MR (2000) Congestive heart failure: fifty years of progress. Circulation 102:IV14–IV23
13. Bui AL, Horwich TB, Fonarow GC (2011) Epidemiology and risk profile of heart failure. Nat Rev Cardiol 8:30–41
14. Bujak M, Frangogiannis NG (2007) The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc Res 74:184–195
15. Charalambous BM, Stephens RC, Feavers IM, Montgomery HE (2007) Role of bacterial endotoxin in chronic heart failure: the gut of the matter. Shock 28:15–23
16. Chen QQ, Zhang W, Chen XF, Bao YJ, Wang J, Zhu WZ (2012) Electrical field stimulation induces cardiac fibroblast proliferation through the calcineurin-NFAT pathway. Can J Physiol Pharmacol 90:1611–1622
17. Clarke MS, Caldwell RW, Chiao H, Miyake K, McNeil PL (1995) Contraction-induced cell wounding and release of fibroblast growth factor in heart. Circ Res 76:927–934
18. Couchman JR (2010) Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 26:89–114
19. Darby I, Skalli O, Gabbiani G (1990) Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63:21–29
20. Davis J, Burr AR, Davis GF, Birnbaumer L, Molkentin JD (2012) A TRPC6-dependent pathway for myofibroblast transdifferentiation and wound healing in vivo. Dev Cell 23:705–715
21. Dobaczewski M, Chen W, Frangogiannis NG (2011) Transforming growth factor (TGF)-β signaling in cardiac remodeling. J Mol Cell Cardiol 51:600–606
22. Dovas A, Yoneda A, Couchman JR (2006) PKCbeta-dependent activation of RhoA by syndecan-4 during focal adhesion formation. J Cell Sci 119:2837–2846
23. Echtermeyer F, Harendza T, Hubrich S, Lorenz A, Herzog C, Mueller M, Schmitz M, Grund A, Larmann J, Stypmann J, Schieffer B, Lichtinghagen R, Hilfiker-Kleiner D, Wollert KC, Heineke J, Theilmeier G (2011) Syndecan-4 signalling inhibits apoptosis and controls NFAT activity during myocardial damage and remodelling. Cardiovasc Res 92:123–131
24. Edwards IJ (2012) Proteoglycans in prostate cancer. Nat Rev Urol 9:196–206
25. Engebretsen KV, Lunde IG, Strand ME, Waehre A, Sjaastad I, Marstein H, Skrbic B, Dahl CP, Askevold ET, Christensen G, Bjørnstad JL, Tønnessen T (2013) Lumican is increased in experimental and clinical heart failure, and its production by cardiac fibroblasts is induced by mechanical and pro-inflammatory stimuli. FEBS J 280:2382–2398
26. Filmus J, Capurro M, Rast J (2008) Glypicans. Genome Biol 9:224
27. Finsen AV, Woldbaek PR, Li J, Wu J, Lyberg T, Tønnessen T, Christensen G (2004) Increased syndecan expression following myocardial infarction indicates a role in cardiac remodeling. Physiol Genomics 16:301–308
28. Finsen AV, Lunde IG, Sjaastad I, Østli EK, Lyngra M, Jarstadmarken HO, Hasic A, Nygård S, Wilcox-Adelman SA, Goetinck PF, Lyberg T, Skrbic B, Florholmen G, Tønnessen T, Louch WE, Djurovic S, Carlson CR, Christensen G (2011) Syndecan-4 is essential for development of concentric myocardial hypertrophy via stretch-induced activation of the calcineurin-NFAT pathway. PLoS One 6:e28302
29. Frangogiannis NG (2010) Syndecan-1: a critical mediator in cardiac fibrosis. Hypertension 55:233–235
30. Goffin JM, Pittet P, Csucs G, Lussi JW, Meister JJ, Hinz B (2006) Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J Cell Biol 172:259–268
31. Gopal S, Søgaard P, Multhaupt HA, Pataki C, Okina E, Xian X, Pedersen ME, Stevens T, Griesbeck O, Park PW, Pocock R, Couchman JR (2015) Transmembrane proteoglycans control stretch-activated channels to set cytosolic calcium levels. J Cell Biol 210:1199–1211
32. Götte M (2003) Syndecans in inflammation. FASEB J 17:575–591
33. Gullestad L, Kjekshus J, Damås JK, Ueland T, Yndestad A, Aukrust P (2006) Agents targeting inflammation in heart failure. Expert Opin Investig Drugs 14:557–566
34. Hartmann S, Ridley AJ, Lutz S (2015) The function of Rho-associated kinases ROCK1 and ROCK2 in the pathogenesis of cardiovascular disease. Front Pharmacol 6:276
35. Hartupee J, Mann DL (2016) Role of inflammatory cells in fibroblast activation. J Mol Cell Cardiol 93:143–148. doi:10.1016/j.yjmcc.2015.11.016
36. Herum KM, Lunde IG, Skrbic B, Florholmen G, Behmen D, Sjaastad I, Carlson CR, Gomez MF, Christensen G (2013) Syndecan-4 signaling via NFAT regulates extracellular matrix production and cardiac myofibroblast differentiation in response to mechanical stress. J Mol Cell Cardiol 54:73–81
37. Herum KM, Lunde IG, Skrbic B, Louch WE, Hasic A, Boye S, Unger A, Brorson SH, Sjaastad I, Tønnessen T, Linke WA, Gomez MF, Christensen G (2015) Syndecan-4 is a key determinant of collagen cross-linking and passive myocardial stiffness in the pressure-overloaded heart. Cardiovasc Res 106:217–226
38. Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand JL, Cohen-Tervaert JW, Drexler H, Filippatos G, Felix SB, Gullestad L, Hilfiker-Kleiner D, Janssens S, Latini R, Neubauer G, Paulus WJ, Pieske B, Ponikowski P, Schroen B, Schultheiss HP, Tschöpe C, Van Bilsen M, Zannad F, McMurray J, Shah AM (2009) 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 11:119–129
39. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G (2007) The myofibroblast: one function, multiple origins. Am J Pathol 170:1807–1816
40. Ho CY, López B, Coelho-Filho OR, Lakdawala NK, Cirino AL, Jarolim P, Kwong R, González A, Colan SD, Seidman JG, Díez J, Seidman CE (2010) Myocardial fibrosis as an early manifestation of hypertrophic cardiomyopathy. N Engl J Med 363:552–563
41. Ho KK, Pinsky JL, Kannel WB, Levy D (1993) The epidemiology of heart failure: the Framingham Study. J Am Coll Cardiol 22:6A–13A
42. Horowitz A, Simons M (1998) Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Calpha. J Biol Chem 273:25548–25551
43. Iozzo RV, Schaefer L (2010) Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J 277:3864–3875
44. Itoh N, Ohta H (2013) Pathophysiological roles of FGF signaling in the heart. Front Physiol 4:247
45. Kasner M, Westermann D, Lopez B, Gaub R, Escher F, Kühl U, Schultheiss HP, Tschöpe C (2011) Diastolic tissue Doppler indexes correlate with the degree of collagen expression and cross-linking in heart failure and normal ejection fraction. J Am Coll Cardiol 57:977–985
46. Kaye DM, Krum H (2007) Drug discovery for heart failure: a new era or the end of the pipeline? Nat Rev Drug Discov 6:127–139
47. Kehat I, Molkentin JD (2010) Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 122:2727–2735
48. Keum E, Kim Y, Kim J, Kwon S, Lim Y, Han I, Oh ES (2004) Syndecan-4 regulates localization, activity and stability of protein kinase C-alpha. Biochem J 378:1007–1014
49. Kjellén L, Pettersson I, Höök M (1981) Cell-surface heparan sulfate: an intercalated membrane proteoglycan. Proc Natl Acad Sci U S A 78:5371–5375
50. Kliment CR, Englert JM, Gochuico BR, Yu G, Kaminski N, Rosas I, Oury TD (2009) Oxidative stress alters syndecan-1 distribution in lungs with pulmonary fibrosis. J Biol Chem 284:3537–3545
51. Kojima T, Takagi A, Maeda M, Segawa T, Shimizu A, Yamamoto K, Matsushita T, Saito H (2001) Plasma levels of syndecan-4 (ryudocan) are elevated in patients with acute myocardial infarction. Thromb Haemost 85:793–799
52. Koo BK, Jung YS, Shin J, Han I, Mortier E, Zimmermann P, Whiteford JR, Couchman JR, Oh ES, Lee W (2006) Structural basis of syndecan-4 phosphorylation as a molecular switch to regulate signaling. J Mol Biol 355:651–663
53. Lambaerts K, Wilcox-Adelman SA, Zimmermann P (2009) The signaling mechanisms of syndecan heparan sulfate proteoglycans. Curr Opin Cell Biol 21:662–669
54. Lei J, Xue SN, Wu W, Zhou SX, Zhang YL, Yuan GY, Wang JF (2012) Increased level of soluble syndecan-1 in serum correlates with myocardial expression in a rat model of myocardial infarction. Mol Cell Biochem 359:177–182
55. Levy D, Kenchaiah S, Larson MG, Benjamin EJ, Kupka MJ, Ho KK, Murabito JM, Vasan RS (2002) Long-term trends in the incidence of and survival with heart failure. N Engl J Med 347:1397–1402
56. Li J, Brown LF, Laham RJ, Volk R, Simons M (1997) Macrophage-dependent regulation of syndecan gene expression. Circ Res 81:785–796
57. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Roger VL, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J, Subcommittee AHASCaSS (2010) Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 121:e46–e215
58. López B, Querejeta R, González A, Larman M, Díez J (2012) Collagen cross-linking but not collagen amount associates with elevated filling pressures in hypertensive patients with stage C heart failure: potential role of lysyl oxidase. Hypertension 60:677–683
59. Lund O, Emmertsen K, Dørup I, Jensen FT, Flø C (2003) Regression of left ventricular hypertrophy during 10 years after valve replacement for aortic stenosis is related to the preoperative risk profile. Eur Heart J 24:1437–1446
60. Mack CP, Somlyo AV, Hautmann M, Somlyo AP, Owens GK (2001) Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization. J Biol Chem 276:341–347
61. Mann DL, Zipes DP, Libby P, Bonow RO (2014) Braunwald’s heart disease: a textbook of cardiovascular medicine, 10th edn. Elsevier Saunders, Philadelphia
62. Manon-Jensen T, Itoh Y, Couchman JR (2010) Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J 277:3876–3889
63. Matsui Y, Ikesue M, Danzaki K, Morimoto J, Sato M, Tanaka S, Kojima T, Tsutsui H, Uede T (2011) Syndecan-4 prevents cardiac rupture and dysfunction after myocardial infarction. Circ Res 108:1328–1339
64. McCullough PA, Philbin EF, Spertus JA, Kaatz S, Sandberg KR, Weaver WD, Study RUACHFR (2002) Confirmation of a heart failure epidemic: findings from the Resource Utilization Among Congestive Heart Failure (REACH) study. J Am Coll Cardiol 39:60–69
65. Molkentin JD (2004) Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovasc Res 63:467–475
66. Molkentin JD (2013) Parsing good versus bad signaling pathways in the heart: role of calcineurin-nuclear factor of activated T-cells. Circ Res 113:16–19
67. Mudd JO, Kass DA (2008) Tackling heart failure in the twenty-first century. Nature 451:919–928
68. O’Connell JB, Bristow MR (1994) Economic impact of heart failure in the United States; time for a different approach. J Heart Lung Transpl 13:S107–S112
69. Oh ES, Woods A, Couchman JR (1997) Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem 272:8133–8136
70. Parish CR (2006) The role of heparan sulphate in inflammation. Nat Rev Immunol 6:633–643
71. Petrov VV, Fagard RH, Lijnen PJ (2002) Stimulation of collagen production by transforming growth factor-beta1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension 39:258–263
72. Porter KE, Turner NA (2009) Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther 123:255–278
73. Ramos G, Hofmann U, Frantz S (2016) Myocardial fibrosis seen through the lenses of T-cell biology. J Mol Cell Cardiol 92:41–45
74. Rapraeger AC, Krufka A, Olwin BB (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252:1705–1708
75. Rienks M, Papageorgiou AP, Frangogiannis NG, Heymans S (2014) Myocardial extracellular matrix: an ever-changing and diverse entity. Circ Res 114:872–888
76. Samarel AM (2013) Syndecan-4: a component of the mechanosensory apparatus of cardiac fibroblasts. J Mol Cell Cardiol 56:19–21
77. Schellings MW, Vanhoutte D, Almen GC van, Swinnen M, Leenders JJ, Kubben N, Leeuwen RE van, Hofstra L, Heymans S, Pinto YM (2010) Syndecan-1 amplifies angiotensin II-induced cardiac fibrosis. Hypertension 55:249–256
78. Seidman CE, Seidman JG (2011) Identifying sarcomere gene mutations in hypertrophic cardiomyopathy: a personal history. Circ Res 108:743–750
79. Small EM, Thatcher JE, Sutherland LB, Kinoshita H, Gerard RD, Richardson JA, Dimaio JM, Sadek H, Kuwahara K, Olson EN (2010) Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ Res 107:294–304
80. Strand ME, Herum KM, Rana ZA, Skrbic B, Askevold ET, Dahl CP, Vistnes M, Hasic A, Kvaløy H, Sjaastad I, Carlson CR, Tønnessen T, Gullestad L, Christensen G, Lunde IG (2013) Innate immune signaling induces expression and shedding of the heparan sulfate proteoglycan syndecan-4 in cardiac fibroblasts and myocytes, affecting inflammation in the pressure-overloaded heart. FEBS J 280:2228–2247
81. Strand ME, Aronsen JM, Braathen B, Sjaastad I, Kvaløy H, Tønnessen T, Christensen G, Lunde IG (2015) Shedding of syndecan-4 promotes immune cell recruitment and mitigates cardiac dysfunction after lipopolysaccharide challenge in mice. J Mol Cell Cardiol 88:133–144
82. Strunz CM, Matsuda M, Salemi VM, Nogueira A, Mansur AP, Cestari IN, Marquezini MV (2011) Changes in cardiac heparan sulfate proteoglycan expression and streptozotocin-induced diastolic dysfunction in rats. Cardiovasc Diabetol 10:35
83. Takahashi R, Negishi K, Watanabe A, Arai M, Naganuma F, Ohyama Y, Kurabayash M (2011) Serum syndecan-4 is a novel biomarker for patients with chronic heart failure. J Cardiol 57:325–332
84. Tromp J, Pol A van der, Klip IT, Boer RA de, Jaarsma T, Gilst WH van, Voors AA, Veldhuisen DJ van, Meer P van der (2014) The fibrosis marker syndecan-1 and outcome in heart failure patients with reduced and preserved ejection fraction. Circ Heart Fail 7:457–462
85. Vanhoutte D, Schellings MW, Götte M, Swinnen M, Herias V, Wild MK, Vestweber D, Chorianopoulos E, Cortés V, Rigotti A, Stepp MA, Van de Werf F, Carmeliet P, Pinto YM, Heymans S (2007) Increased expression of syndecan-1 protects against cardiac dilatation and dysfunction after myocardial infarction. Circulation 115:475–482
86. Velasquez LS, Sutherland LB, Liu Z, Grinnell F, Kamm KE, Schneider JW, Olson EN, Small EM (2013) Activation of MRTF-A-dependent gene expression with a small molecule promotes myofibroblast differentiation and wound healing. Proc Natl Acad Sci U S A 110:16850–16855
87. Vistnes M, Aronsen JM, Lunde IG, Sjaastad I, Carlson CR, Christensen G (2014) Pentosan polysulfate decreases myocardial expression of the extracellular matrix enzyme ADAMTS4 and improves cardiac function in vivo in rats subjected to pressure overload by aortic banding. PLoS One 9:e89621
88. Vizzardi E, Regazzoni V, Caretta G, Gavazzoni M, Sciatti E, Bonadei I, Trichaki E, Raddino R, Metra M (2014) Mineralcorticoid receptor antagonist in heart failure. Past, present and future perspectives. IJC Heart Vessels 3:6–14
89. Wang L, Fuster M, Sriramarao P, Esko JD (2005) Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol 6:902–910
90. Wang J, Wang Y, Zhang W, Zhao X, Chen X, Xiao W, Zhang L, Chen Y, Zhu WZ (2016) Phenylephrine promotes cardiac fibroblast proliferation through calcineurin-NFAT pathway. Front Biosci 21:502–513
91. Wei L (2011) Immunological aspect of cardiac remodeling: T lymphocyte subsets in inflammation-mediated cardiac fibrosis. Exp Mol Pathol 90:74–78
92. Whiteford JR, Ko S, Lee W, Couchman JR (2008) Structural and cell adhesion properties of zebrafish syndecan-4 are shared with higher vertebrates. J Biol Chem 283:29322–29330
93. Woods A, Longley RL, Tumova S, Couchman JR (2000) Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 374:66–72
94. Xie J, Wang J, Li R, Dai Q, Yong Y, Zong B, Xu Y, Li E, Ferro A, Xu B (2012) Syndecan-4 over-expression preserves cardiac function in a rat model of myocardial infarction. J Mol Cell Cardiol 53:250–258
95. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64:841–848
96. Yndestad A, Damås JK, Øie E, Ueland T, Gullestad L, Aukrust P (2007) Role of inflammation in the progression of heart failure. Curr Cardiol Rep 9:236–241
97. Yu Q, Vazquez R, Zabadi S, Watson RR, Larson DF (2010) T-lymphocytes mediate left ventricular fibrillar collagen cross-linking and diastolic dysfunction in mice. Matrix Biol 29:511–518
98. Yusuf S, Reddy S, Ounpuu S, Anand S (2001) Global burden of cardiovascular diseases. Part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization. Circulation 104:2746–2753
99. Zhang Y, Li J, Partovian C, Sellke FW, Simons M (2003) Syndecan-4 modulates basic fibroblast growth factor 2 signaling in vivo. Am J Physiol Heart Circ Physiol 284:H2078–H2082