CoChat
Sign Up
Cited by 814Cardiac Fibrosis and RemodelingCongenital heart defects researchLiver physiology and pathology

Cardiac fibroblasts, fibrosis and extracellular matrix remodeling in heart disease

Open access
Fan, Dong, Takawale, Abhijit, Lee, Jiwon, Kassiri, Zamaneh·2012·Fibrogenesis & Tissue Repair
DOI 10.1186/1755-1536-5-15PMC PMC3464725
Open this paper in CoChat — free accountOpen PDF

Abstract

Fibroblasts comprise the largest cell population in the myocardium. In heart disease, the number of fibroblasts is increased either by replication of the resident myocardial fibroblasts, migration and transformation of circulating bone marrow cells, or by transformation of endothelial/epithelial cells into fibroblasts and myofibroblasts. The primary function of fibroblasts is to produce structural proteins that comprise the extracellular matrix (ECM). This can be a constructive process; however, hyperactivity of cardiac fibroblasts can result in excess production and deposition of ECM proteins in the myocardium, known as fibrosis, with adverse effects on cardiac structure and function. In addition to being the primary source of ECM proteins, fibroblasts produce a number of cytokines, peptides, and enzymes among which matrix metalloproteinases (MMPs) and their inhibitors, tissue inhibitor of metalloproteinases (TIMPs), directly impact the ECM turnover and homeostasis. Function of fibroblasts can also in turn be regulated by MMPs and TIMPs. In this review article, we will focus on the function of cardiac fibroblasts in the context of ECM formation, homeostasis and remodeling in the heart. We will discuss the origins and multiple roles of cardiac fibroblasts in myocardial remodeling in different types of heart disease in patients and in animal models. We will further provide an overview of what we have learned from experimental animal models and genetically modified mice with altered expression of ECM regulatory proteins, MMPs and TIMPs.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/1755-1536-5-15

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 142

  1. Camelliti P Borg TK Kohl P Structural and functional characterisation of cardiac fibroblasts Cardiovasc Res 2005 65 40 51 15621032
  2. Souders CA Bowers SL Baudino TA Cardiac fibroblast: the renaissance cell Circ Res 2009 105 1164 1176 19959782 PMC3345531
  3. Hill JA Olson EN Cardiac plasticity N Engl J Med 2008 358 1370 1380 18367740
  4. Koitabashi N Kass DA Reverse remodeling in heart failure – mechanisms and therapeutic opportunities Nat Rev Cardiol 2012 9 147 157 22143079
  5. Kranias EG Hajjar RJ Modulation of cardiac contractility by the phopholamban/SERCA2a regulatome Circ Res 2012 110 1646 1660 22679139 PMC3392125
  6. Krenning G Zeisberg EM Kalluri R The origin of fibroblasts and mechanism of cardiac fibrosis J Cell Physiol 2010 225 631 637 20635395 PMC3098503
  7. Fries KM Blieden T Looney RJ Sempowski GD Silvera MR Willis RA Phipps RP Evidence of fibroblast heterogeneity and the role of fibroblast subpopulations in fibrosis Clin Immunol Immunopathol 1994 72 283 292 7914840
  8. Franke WW Schmid E Osborn M Weber K Intermediate-sized filaments of human endothelial cells J Cell Biol 1979 81 570 580 379021 PMC2110384
  9. Mork C van Deurs B Petersen OW Regulation of vimentin expression in cultured human mammary epithelial cells Differentiation 1990 43 146 156 2373288
  10. Camelliti P Green CR LeGrice I Kohl P Fibroblast network in rabbit sinoatrial node: structural and functional identification of homogeneous and heterogeneous cell coupling Circ Res 2004 94 828 835 14976125
  11. Goldsmith EC Hoffman A Morales MO Potts JD Price RL McFadden A Rice M Borg TK Organization of fibroblasts in the heart Dev Dyn 2004 230 787 794 15254913
  12. Shrivastava A Radziejewski C Campbell E Kovac L McGlynn M Ryan TE Davis S Goldfarb MP Glass DJ Lemke G Yancopoulos GD An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors Mol Cell 1997 1 25 34 9659900
  13. Schlessinger J Direct binding and activation of receptor tyrosine kinases by collagen Cell 1997 91 869 872 9428509
  14. Alves F Vogel W Mossie K Millauer B Hofler H Ullrich A Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer Oncogene 1995 10 609 618 7845687
  15. Lai C Lemke G An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system Neuron 1991 6 691 704 2025425
  16. Ebihara Y Masuya M Larue AC Fleming PA Visconti RP Minamiguchi H Drake CJ Ogawa M Hematopoietic origins of fibroblasts: II. In vitro studies of fibroblasts, CFU-F, and fibrocytes Exp Hematol 2006 34 219 229 16459190
  17. Shyu KG Chao YM Wang BW Kuan P Regulation of discoidin domain receptor 2 by cyclic mechanical stretch in cultured rat vascular smooth muscle cells Hypertension 2005 46 614 621 16087782
  18. Ferri N Carragher NO Raines EW Role of discoidin domain receptors 1 and 2 in human smooth muscle cell-mediated collagen remodeling: potential implications in atherosclerosis and lymphangioleiomyomatosis Am J Pathol 2004 164 1575 1585 15111304 PMC1615659
  19. Mohan RR Wilson SE Discoidin domain receptor (DDR) 1 and 2: collagen-activated tyrosine kinase receptors in the cornea Exp Eye Res 2001 72 87 92 11133186
  20. Strutz F Okada H Lo CW Danoff T Carone RL Tomaszewski JE Neilson EG Identification and characterization of a fibroblast marker: FSP1 J Cell Biol 1995 130 393 405 7615639 PMC2199940
  21. Mazzucchelli L Protein S100A4: too long overlooked by pathologists? Am J Pathol 2002 160 7 13 11786392 PMC1867142
  22. Petrov VV Fagard RH Lijnen PJ Stimulation of collagen production by transforming growth factor-beta1 during differentiation of cardiac fibroblasts to myofibroblasts Hypertension 2002 39 258 263 11847194
  23. Baum J Duffy HS Fibroblasts and myofibroblasts: what are we talking about? J Cardiovasc Pharmacol 2011 57 376 379 21297493 PMC3077448
  24. Santiago JJ Dangerfield AL Rattan SG Bathe KL Cunnington RH Raizman JE Bedosky KM Freed DH Kardami E Dixon IM Cardiac fibroblast to myofibroblast differentiation in vivo and in vitro: expression of focal adhesion components in neonatal and adult rat ventricular myofibroblasts Dev Dyn 2010 239 1573 1584 20503355
  25. Gabbiani G The myofibroblast in wound healing and fibrocontractive diseases J Pathol 2003 200 500 503 12845617
  26. Calderone A Bel-Hadj S Drapeau J El-Helou V Gosselin H Clement R Villeneuve L Scar myofibroblasts of the infarcted rat heart express natriuretic peptides J Cell Physiol 2006 207 165 173 16270351
  27. Tamaoki M Imanaka-Yoshida K Yokoyama K Nishioka T Inada H Hiroe M Sakakura T Yoshida T Tenascin-C regulates recruitment of myofibroblasts during tissue repair after myocardial injury Am J Pathol 2005 167 71 80 15972953 PMC1603439
  28. Walker GA Masters KS Shah DN Anseth KS Leinwand LA Valvular myofibroblast activation by transforming growth factor-beta: implications for pathological extracellular matrix remodeling in heart valve disease Circ Res 2004 95 253 260 15217906
  29. Lie-Venema H van den Akker NM Bax NA Winter EM Maas S Kekarainen T Hoeben RC de Ruiter MC Poelmann RE Gittenberger-de Groot AC Origin, fate, and function of epicardium-derived cells (EPDCs) in normal and abnormal cardiac development ScientificWorldJournal 2007 7 1777 1798 18040540 PMC5901302
  30. Norris RA Borg TK Butcher JT Baudino TA Banerjee I Markwald RR Neonatal and adult cardiovascular pathophysiological remodeling and repair: developmental role of periostin Ann N Y Acad Sci 2008 1123 30 40 18375575
  31. Olivey HE Mundell NA Austin AF Barnett JV Transforming growth factor-beta stimulates epithelial–mesenchymal transformation in the proepicardium Dev Dyn 2006 235 50 59 16245329 PMC3160345
  32. Gittenberger-de Groot AC Vrancken Peeters MP Mentink MM Gourdie RG Poelmann RE Epicardium-derived cells contribute a novel population to the myocardial wall and the atrioventricular cushions Circ Res 1998 82 1043 1052 9622157
  33. Kolditz DP Wijffels MC Blom NA van der Laarse A Hahurij ND Lie-Venema H Markwald RR Poelmann RE Schalij MJ Gittenberger-de Groot AC Epicardium-derived cells in development of annulus fibrosis and persistence of accessory pathways Circulation 2008 117 1508 1517 18332266
  34. Zhou B von Gise A Ma Q Hu YW Pu WT Genetic fate mapping demonstrates contribution of epicardium-derived cells to the annulus fibrosis of the mammalian heart Dev Biol 2010 338 251 261 20025864 PMC2815244
  35. de Lange FJ Moorman AF Anderson RH Manner J Soufan AT de Gier-de Vries C Schneider MD Webb S van den Hoff MJ Christoffels VM Lineage and morphogenetic analysis of the cardiac valves Circ Res 2004 95 645 654 15297379
  36. Lucas JA Zhang Y Li P Gong K Miller AP Hassan E Hage F Xing D Wells B Oparil S Chen YF Inhibition of transforming growth factor-beta signaling induces left ventricular dilation and dysfunction in the pressure-overloaded heart Am J Physiol Heart Circ Physiol 2010 298 H424 H432 19933419 PMC2822586
  37. Zeisberg EM Tarnavski O Zeisberg M Dorfman AL McMullen JR Gustafsson E Chandraker A Yuan X Pu WT Roberts AB Neilson EG Sayegh MH Isumo S Kalluri R Endothelial-to-mesenchymal transition contributes to cardiac fibrosis Nat Med 2007 13 952 961 17660828
  38. Wynn TA Ramalingam TR Mechanisms of fibrosis: therapeutic translation for fibrotic disease Nat Med 2012 18 1028 1040 22772564 PMC3405917
  39. Garcia J Sandi MJ Cordelier P Binetruy B Pouyssegur J Iovanna JL Tournaire R Tie1 deficiency induces endothelial–mesenchymal transition EMBO Rep 2012 13 431 439 22421998 PMC3343349
  40. Russell JL Goetsch SC Gaiano NR Hill JA Olson EN Schneider JW A dynamic notch injury response activates epicardium and contributes to fibrosis repair Circ Res 2011 108 51 59 21106942 PMC3042596
  41. Haudek SB Xia Y Huebener P Lee JM Carlson S Crawford JR Pilling D Gomer RH Trial J Frangogiannis NG Entman ML Bone marrow-derived fibroblast precursors mediate ischemic cardiomyopathy in mice Proc Natl Acad Sci U S A 2006 103 18284 18289 17114286 PMC1643845
  42. van Amerongen MJ Bou-Gharios G Popa E van Ark J Petersen AH van Dam GM van Luyn MJ Harmsen MC Bone marrow-derived myofibroblasts contribute functionally to scar formation after myocardial infarction J Pathol 2008 214 377 386 18095257
  43. van Amerongen MJ Harmsen MC van Rooijen N Petersen AH van Luyn MJ Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice Am J Pathol 2007 170 818 829 17322368 PMC1864893
  44. Ogawa M LaRue AC Drake CJ Hematopoietic origin of fibroblasts/myofibroblasts: Its pathophysiologic implications Blood 2006 108 2893 2896 16840726
  45. Mollmann H Nef HM Kostin S von Kalle C Pilz I Weber M Schaper J Hamm CW Elsasser A Bone marrow-derived cells contribute to infarct remodelling Cardiovasc Res 2006 71 661 671 16854401
  46. Kania G Blyszczuk P Stein S Valaperti A Germano D Dirnhofer S Hunziker L Matter CM Eriksson U Heart-infiltrating prominin-1+/CD133+ progenitor cells represent the cellular source of transforming growth factor beta-mediated cardiac fibrosis in experimental autoimmune myocarditis Circ Res 2009 105 462 470 19628793
  47. Xu J Lin SC Chen J Miao Y Taffet GE Entman ML Wang Y CCR2 mediates the uptake of bone marrow-derived fibroblast precursors in angiotensin II-induced cardiac fibrosis Am J Physiol Heart Circ Physiol 2011 301 H538 H547 21572015 PMC3154672
  48. Humphreys BD Lin SL Kobayashi A Hudson TE Nowlin BT Bonventre JV Valerius MT McMahon AP Duffield JS Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis Am J Pathol 2010 176 85 97 20008127 PMC2797872
  49. Tapscott SJ Davis RL Thayer MJ Cheng PF Weintraub H Lassar AB MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts Science 1988 242 405 411 3175662
  50. Song K Nam YJ Luo X Qi X Tan W Huang GN Acharya A Smith CL Tallquist MD Neilson EG Hill JA Bassel-Duby R Olson EN Heart repair by reprogramming non-myocytes with cardiac transcription factors Nature 2012 485 599 604 22660318 PMC3367390
  51. Ieda M Fu JD Delgado-Olguin P Vedantham V Hayashi Y Bruneau BG Srivastava D Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors Cell 2010 142 375 386 20691899 PMC2919844
  52. Jayawardena TM Egemnazarov B Finch EA Zhang L Payne JA Pandya K Zhang Z Rosenberg P Mirotsou M Dzau VJ MicroRNA-mediated in vitro and in vivo direct reprogramming of cardiac fibroblasts to cardiomyocytes Circ Res 2012 110 1465 1473 22539765 PMC3380624
  53. Kohl P Heterogeneous cell coupling in the heart: an electrophysiological role for fibroblasts Circ Res 2003 93 381 383 12958139
  54. Gaudesius G Miragoli M Thomas SP Rohr S Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin Circ Res 2003 93 421 428 12893743
  55. Porter KE Turner NA Cardiac fibroblasts: at the heart of myocardial remodeling Pharmacol Ther 2009 123 255 278 19460403
  56. Eghbali M Cardiac fibroblasts: function, regulation of gene expression, and phenotypic modulation Basic Res Cardiol 1992 87 Suppl 2 183 189 1299209
  57. Butt RP Laurent GJ Bishop JE Collagen production and replication by cardiac fibroblasts is enhanced in response to diverse classes of growth factors Eur J Cell Biol 1995 68 330 335 8603686
  58. Moore L Fan D Basu R Kandalam V Kassiri Z Tissue inhibitor of metalloproteinases (TIMPs) in heart failure Heart Fail Rev 2012 17 693 706 21717224
  59. Spinale FG Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function Physiol Rev 2007 87 1285 1342 17928585
  60. Mann DL Spinale FG Activation of matrix metalloproteinases in the failing human heart: breaking the tie that binds Circulation 1998 98 1699 1702 9788821
  61. Spinale FG Wilbur NM Matrix metalloproteinase therapy in heart failure Curr Treat Options Cardiovasc Med 2009 11 339 346 19627666 PMC2745890
  62. Kelly D Khan S Cockerill G Ng LL Thompson M Samani NJ Squire IB Circulating stromelysin-1 (MMP-3): a novel predictor of LV dysfunction, remodelling and all-cause mortality after acute myocardial infarction Eur J Heart Fail 2008 10 133 139 18234553 PMC2635532
  63. Ma Y Chiao YA Zhang J Manicone AM Jin YF Lindsey ML Matrix metalloproteinase-28 deletion amplifies inflammatory and extracellular matrix responses to cardiac aging Microsc Microanal 2012 18 81 90 22153350 PMC3972008
  64. Manso AM Elsherif L Kang SM Ross RS Integrins, membrane-type matrix metalloproteinases and ADAMs: potential implications for cardiac remodeling Cardiovasc Res 2006 69 574 584 16253214
  65. Barbolina MV Stack MS Membrane type 1-matrix metalloproteinase: substrate diversity in pericellular proteolysis Semin Cell Dev Biol 2008 19 24 33 17702616 PMC2685078
  66. Takino T Saeki H Miyamori H Kudo T Sato H Inhibition of membrane-type 1 matrix metalloproteinase at cell-matrix adhesions Cancer Res 2007 67 11621 11629 18089791
  67. Shen XM Wu YP Feng YB Luo ML Du XL Zhang Y Cai Y Xu X Han YL Zhang X Zhan QM Wang MR Interaction of MT1-MMP and laminin-5γ2 chain correlates with metastasis and invasiveness in human esophageal squamous cell carcinoma Clin Exp Metastasis 2007 24 541 550 17668281
  68. Steffensen B Wallon UM Overall CM Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affinity binding to native type I collagen but not native type IV collagen J Biol Chem 1995 270 11555 11566 7744795
  69. Vincenti MP Coon CI Mengshol JA Yocum S Mitchell P Brinckerhoff CE Cloning of the gene for interstitial collagenase-3 (matrix metalloproteinase-13) from rabbit synovial fibroblasts: differential expression with collagenase-1 (matrix metalloproteinase-1) Biochem J 1998 331 Pt 1 341 346 9512498 PMC1219357
  70. Nuttall RK Sampieri CL Pennington CJ Gill SE Schultz GA Edwards DR Expression analysis of the entire MMP and TIMP gene families during mouse tissue development FEBS Lett 2004 563 129 134 15063736
  71. Visse R Nagase H Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry Circ Res 2003 92 827 839 12730128
  72. Kandalam V Basu R Abraham T Wang X Soloway PD Jaworski DM Oudit GY Kassiri Z TIMP2 deficiency accelerates adverse post-myocardial infarction remodeling because of enhanced MT1-MMP activity despite lack of MMP2 activation Circ Res 2010 106 796 808 20056917
  73. Li YY Feng Y McTiernan CF Pei W Moravec CS Wang P Rosenblum W Kormos RL Feldman AM Downregulation of matrix metalloproteinases and reduction in collagen damage in the failing human heart after support with left ventricular assist devices Circulation 2001 104 1147 1152 11535571
  74. Heymans S Schroen B Vermeersch P Milting H Gao F Kassner A Gillijns H Herijgers P Flameng W Carmeliet P Van de Werf F Pinto YM Janssens S Increased cardiac expression of tissue inhibitor of metalloproteinase-1 and tissue inhibitor of metalloproteinase-2 is related to cardiac fibrosis and dysfunction in the chronic pressure-overloaded human heart Circulation 2005 112 1136 1144 16103240
  75. Moore L Fan D Basu R Kandalam V Kassiri Z Tissue inhibitor of metalloproteinases (TIMPs) in heart failure Heart Fail Rev 2012 17 693706 21717224
  76. Vanhoutte D Heymans S TIMPs and cardiac remodeling: ‘Embracing the MMP-independent-side of the family’ J Mol Cell Cardiol 2010 48 445 453 19799912
  77. Page-McCaw A Ewald AJ Werb Z Matrix metalloproteinases and the regulation of tissue remodelling Nat Rev Mol Cell Biol 2007 8 221 233 17318226 PMC2760082
  78. Shi Q Liu X Bai Y Cui C Li J Li Y Hu S Wei Y In vitro effects of pirfenidone on cardiac fibroblasts: proliferation, myofibroblast differentiation, migration and cytokine secretion PLoS One 2011 6 e28134 22132230 PMC3223242
  79. Tyagi SC Kumar SG Banks J Fortson W Co-expression of tissue inhibitor and matrix metalloproteinase in myocardium J Mol Cell Cardiol 1995 27 2177 2189 8576934
  80. Awad AE Kandalam V Chakrabarti S Wang X Penninger JM Davidge ST Oudit GY Kassiri Z Tumor necrosis factor induces matrix metalloproteinases in cardiomyocytes and cardiofibroblasts differentially via superoxide production in a PI3Kγ-dependent manner Am J Physiol Cell Physiol 2010 298 C679 C692 20007453
  81. Deschamps AM Spinale FG Pathways of matrix metalloproteinase induction in heart failure: bioactive molecules and transcriptional regulation Cardiovasc Res 2006 69 666 676 16426590
  82. Tsuruda T Boerrigter G Huntley BK Noser JA Cataliotti A Costello-Boerrigter LC Chen HH Burnett JC Brain natriuretic Peptide is produced in cardiac fibroblasts and induces matrix metalloproteinases Circ Res 2002 91 1127 1134 12480813
  83. Sabeh F Li XY Saunders TL Rowe RG Weiss SJ Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion J Biol Chem 2009 284 23001 23011 19542530 PMC2755707
  84. Zavadzkas JA Mukherjee R Rivers WT Patel RK Meyer EC Black LE McKinney RA Oelsen JM Stroud RE Spinale FG Direct regulation of membrane type 1 matrix metalloproteinase following myocardial infarction causes changes in survival, cardiac function, and remodeling Am J Physiol Heart Circ Physiol 2011 301 H1656 H1666 21666120 PMC3197432
  85. Spinale FG Escobar GP Mukherjee R Zavadzkas JA Saunders SM Jeffords LB Leone AM Beck C Bouges S Stroud RE Cardiac-restricted overexpression of membrane type-1 matrix metalloproteinase in mice: effects on myocardial remodeling with aging Circ Heart Fail 2009 2 351 360 19808359 PMC2743030
  86. Yu Q Stamenkovic I Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis Genes Dev 2000 14 163 176 10652271 PMC316345
  87. Bergman MR Teerlink JR Mahimkar R Li L Zhu BQ Nguyen A Dahi S Karliner JS Lovett DH Cardiac matrix metalloproteinase-2 expression independently induces marked ventricular remodeling and systolic dysfunction Am J Physiol Heart Circ Physiol 2007 292 H1847 H1860 17158653
  88. Lovelock JD Baker AH Gao F Dong JF Bergeron AL McPheat W Sivasubramanian N Mann DL Heterogeneous effects of tissue inhibitors of matrix metalloproteinases on cardiac fibroblasts Am J Physiol Heart Circ Physiol 2005 288 H461 H468 15650153
  89. Diez J Querejeta R Lopez B Gonzalez A Larman M Martinez Ubago JL Losartan-dependent regression of myocardial fibrosis is associated with reduction of left ventricular chamber stiffness in hypertensive patients Circulation 2002 105 2512 2517 12034658
  90. Zannad F Rossignol P Iraqi W Extracellular matrix fibrotic markers in heart failure Heart Fail Rev 2010 15 319 329 19404737
  91. Laviades C Varo N Fernandez J Mayor G Gil MJ Monreal I Diez J Abnormalities of the extracellular degradation of collagen type I in essential hypertension Circulation 1998 98 535 540 9714110
  92. Lindsay MM Maxwell P Dunn FG TIMP-1: a marker of left ventricular diastolic dysfunction and fibrosis in hypertension Hypertension 2002 40 136 141 12154103
  93. Querejeta R Varo N Lopez B Larman M Artinano E Etayo JC Martinez Ubago JL Gutierrez-Stampa M Emparanza JI Gil MJ Monreal I Mindan JP Diez J Serum carboxy-terminal propeptide of procollagen type I is a marker of myocardial fibrosis in hypertensive heart disease Circulation 2000 101 1729 1735 10758057
  94. Lin YH Chiu YW Shiau YC Yen RF Tsai IJ Ho YL Huang PJ The relation between serum level of amioterminal propeptide of type I procollagen and diastolic dysfunction in hypertensive patients without diabetes mellitus: a pilot study J Hum Hypertens 2006 20 964 967 17024136
  95. Zannad F Alla F Dousset B Perez A Pitt B Limitation of excessive extracellular matrix turnover may contribute to survival benefit of spironolactone therapy in patients with congestive heart failure: insights from the randomized aldactone evaluation study (RALES) Rales Investigators. Circulation 2000 102 2700 2706 11094035
  96. Lin YH Ho YL Wang TD Liu CP Kao HL Chao CL Chien KL Hung CS Wu VC Tsai IJ Yen RF Shiau YC Chen WJ The relation of amino-terminal propeptide of type III procollagen and severity of coronary artery disease in patients without myocardial infarction or hibernation Clin Biochem 2006 39 861 866 16919252
  97. Poulsen SH Host NB Jensen SE Egstrup K Relationship between serum amino-terminal propeptide of type III procollagen and changes of left ventricular function after acute myocardial infarction Circulation 2000 101 1527 1532 10747345
  98. Host NB Jensen LT Bendixen PM Jensen SE Koldkjaer OG Simonsen EE The aminoterminal propeptide of type III procollagen provides new information on prognosis after acute myocardial infarction Am J Cardiol 1995 76 869 873 7484822
  99. Manhenke C Orn S Squire I Radauceanu A Alla F Zannad F Dickstein K The prognostic value of circulating markers of collagen turnover after acute myocardial infarction Int J Cardiol 2011 150 277 282 20493567
  100. Thomas CV Coker ML Zellner JL Handy JR Crumbley AJ Spinale FG Increased matrix metalloproteinase activity and selective upregulation in LV myocardium from patients with end-stage dilated cardiomyopathy Circulation 1998 97 1708 1715 9591765
  101. Picard F Brehm M Fassbach M Pelzer B Scheuring S Kury P Strauer BE Schwartzkopff B Increased cardiac mRNA expression of matrix metalloproteinase-1 (MMP-1) and its inhibitor (TIMP-1) in DCM patients Clin Res Cardiol 2006 95 261 269 16598395
  102. Zervoudaki A Economou E Stefanadis C Pitsavos C Tsioufis K Aggeli C Vasiliadou K Toutouza M Toutouzas P Plasma levels of active extracellular matrix metalloproteinases 2 and 9 in patients with essential hypertension before and after antihypertensive treatment J Hum Hypertens 2003 17 119 124 12574790
  103. Tziakas DN Chalikias GK Parissis JT Hatzinikolaou EI Papadopoulos ED Tripsiannis GA Papadopoulou EG Tentes IK Karas SM Chatseras DI Serum profiles of matrix metalloproteinases and their tissue inhibitor in patients with acute coronary syndromes. The effects of short-term atorvastatin administration Int J Cardiol 2004 94 269 277 15093992
  104. Webb CS Bonnema DD Ahmed SH Leonardi AH McClure CD Clark LL Stroud RE Corn WC Finklea L Zile MR Spinale FG Specific temporal profile of matrix metalloproteinase release occurs in patients after myocardial infarction: relation to left ventricular remodeling Circulation 2006 114 1020 1027 16923753
  105. Kelly D Cockerill G Ng LL Thompson M Khan S Samani NJ Squire IB Plasma matrix metalloproteinase-9 and left ventricular remodelling after acute myocardial infarction in man: a prospective cohort study Eur Heart J 2007 28 711 718 17339265 PMC2202923
  106. Wagner DR Delagardelle C Ernens I Rouy D Vaillant M Beissel J Matrix metalloproteinase-9 is a marker of heart failure after acute myocardial infarction J Card Fail 2006 12 66 72 16500583
  107. Vandervelde S van Amerongen MJ Tio RA Petersen AH van Luyn MJ Harmsen MC Increased inflammatory response and neovascularization in reperfused vs. non-reperfused murine myocardial infarction Cardiovasc Pathol 2006 15 83 90 16533696
  108. Kobayashi K Luo M Zhang Y Wilkes DC Ge G Grieskamp T Yamada C Liu TC Huang G Basson CT Kisprt A Geenspan DS Sato TN Secreted Frizzled-related protein 2 is a procollagen C proteinase enhancer with a role in fibrosis associated with myocardial infarction Nat Cell Biol 2009 11 46 55 19079247 PMC2722759
  109. Duan J Gherghe C Liu D Hamlett E Srikantha L Rodgers L Regan JN Rojas M Willis M Leask A Majesky M Deb A Wnt1/betacatenin injury response activates the epicardium and cardiac fibroblasts to promote cardiac repair EMBO J 2012 31 429 442 22085926 PMC3261567
  110. Jugdutt BI Limiting fibrosis after myocardial infarction N Engl J Med 2009 360 1567 1569 19357414
  111. Van Lint P Libert C Matrix metalloproteinase-8: cleavage can be decisive Cytokine Growth Factor Rev 2006 17 217 223 16820317
  112. Cuadrado E Ortega L Hernandez-Guillamon M Penalba A Fernandez-Cadenas I Rosell A Montaner J Tissue plasminogen activator (t-PA) promotes neutrophil degranulation and MMP-9 release J Leukoc Biol 2008 84 207 214 18390930
  113. Matsuda A Itoh Y Koshikawa N Akizawa T Yana I Seiki M Clusterin, an abundant serum factor, is a possible negative regulator of MT6-MMP/MMP-25 produced by neutrophils J Biol Chem 2003 278 36350 36357 12860995
  114. Lambert JM Lopez EF Lindsey ML Macrophage roles following myocardial infarction Int J Cardiol 2008 130 147 158 18656272 PMC2857604
  115. Ammarguellat F Larouche I Schiffrin EL Myocardial fibrosis in DOCA-salt hypertensive rats: effect of endothelin ET(A) receptor antagonism Circulation 2001 103 319 324 11208696
  116. Ammarguellat FZ Gannon PO Amiri F Schiffrin EL Fibrosis, matrix metalloproteinases, and inflammation in the heart of DOCA-salt hypertensive rats: role of ET(A) receptors Hypertension 2002 39 679 684 11882630
  117. Koitabashi N Danner T Zaiman AL Pinto YM Rowell J Mankowski J Zhang D Nakamura T Takimoto E Kass DA Pivotal role of cardiomyocyte TGF-beta signaling in the murine pathological response to sustained pressure overload J Clin Invest 2011 121 2301 2312 21537080 PMC3104748
  118. Cao L Gardner DG Natriuretic peptides inhibit DNA synthesis in cardiac fibroblasts Hypertension 1995 25 227 234 7843772
  119. Tsuruda T Burnett JC Adrenomedullin: an autocrine/paracrine factor for cardiorenal protection Circ Res 2002 90 625 627 11934826
  120. Kapoun AM Liang F O’Young G Damm DL Quon D White RT Munson K Lam A Schreiner GF Protter AA B-type natriuretic peptide exerts broad functional opposition to transforming growth factor-beta in primary human cardiac fibroblasts: fibrosis, myofibroblast conversion, proliferation, and inflammation Circ Res 2004 94 453 461 14726474
  121. Watson CJ Phelan D Xu M Collier P Neary R Smolenski A Ledwidge M McDonald K Baugh J Mechanical stretch up-regulates the B-type natriuretic peptide system in human cardiac fibroblasts: a possible defense against transforming growth factor-ss mediated fibrosis Fibrogenesis Tissue Repair 2012 5 9 22768849 PMC3411484
  122. Knowles JW Esposito G Mao L Hagaman JR Fox JE Smithies O Rockman HA Maeda N Pressure-independent enhancement of cardiac hypertrophy in natriuretic peptide receptor A-deficient mice J Clin Invest 2001 107 975 984 11306601 PMC199554
  123. Kishimoto I Rossi K Garbers DL A genetic model provides evidence that the receptor for atrial natriuretic peptide (guanylyl cyclase-A) inhibits cardiac ventricular myocyte hypertrophy Proc Natl Acad Sci U S A 2001 98 2703 2706 11226303 PMC30202
  124. Vellaichamy E Khurana ML Fink J Pandey KN Involvement of the NF-κB/matrix metalloproteinase pathway in cardiac fibrosis of mice lacking guanylyl cyclase/natriuretic peptide receptor A J Biol Chem 2005 280 19230 19242 15710627
  125. Morita E Yasue H Yoshimura M Ogawa H Jougasaki M Matsumura T Mukoyama M Nakao K Increased plasma levels of brain natriuretic peptide in patients with acute myocardial infarction Circulation 1993 88 82 91 8319360
  126. Saremi A Gopal D Maisel AS Brain natriuretic peptide-guided therapy in the inpatient management of decompensated heart failure Expert Rev Cardiovasc Ther 2012 10 191 203 22292875
  127. Kandalam V Basu R Abraham T Wang X Awad A Wang W Lopaschuk GD Maeda N Oudit GY Kassiri Z Early activation of matrix metalloproteinases underlies the exacerbated systolic and diastolic dysfunction in mice lacking TIMP3 following myocardial infarction Am J Physiol Heart Circ Physiol 2010 299 H1012 H1023 20675565 PMC4116393
  128. Kandalam V Basu R Moore L Fan D Wang X Jaworski DM Oudit GY Kassiri Z Lack of tissue inhibitor of metalloproteinases 2 leads to exacerbated left ventricular dysfunction and adverse extracellular matrix remodeling in response to biomechanical stress Circulation 2011 124 2094 2105 21986284
  129. Thireau J Karam S Fauconnier J Roberge S Cassan C Cazorla O Aimond F Lacampagne A Babuty D Richard S Functional evidence for an active role of B-type natriuretic peptide in cardiac remodeling and pro-arrhythmogenicity Cardiovasc Res 2012 95 59 68 22617407
  130. Matsumura S Iwanaga S Mochizuki S Okamoto H Ogawa S Okada Y Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice J Clin Invest 2005 115 599 609 15711638 PMC548314
  131. Lindsey ML Escobar GP Mukherjee R Goshorn DK Sheats NJ Bruce JA Mains IM Hendrick JK Hewett KW Gourdie RG Matisian LM Spinale FG Matrix metalloproteinase-7 affects connexin-43 levels, electrical conduction, and survival after myocardial infarction Circulation 2006 113 2919 2928 16769909
  132. Heymans S Luttun A Nuyens D Theilmeier G Creemers E Moons L Dyspersin GD Cleutjens JP Shipley M Angellilo A Levi M Nube O Aker A Keshet E Lupu F Herbert JM Smits JF Shapio SD Baes M Borgers M Collen D Daemen MJ Carmeliet P Inhibition of plasminogen activators or matrix metalloproteinases prevents cardiac rupture but impairs therapeutic angiogenesis and causes cardiac failure Nat Med 1999 5 1135 1142 10502816
  133. Ducharme A Frantz S Aikawa M Rabkin E Lindsey M Rohde LE Schoen FJ Kelly RA Werb Z Libby P Lee RT Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction J Clin Invest 2000 106 55 62 10880048 PMC517910
  134. Creemers EE Davis JN Parkhurst AM Leenders P Dowdy KB Hapke E Hauet AM Escobar PG Cleutjens JP Smits JF Daemen MJ Zile MR Spinale FG Deficiency of TIMP-1 exacerbates LV remodeling after myocardial infarction in mice Am J Physiol Heart Circ Physiol 2003 284 H364 H371 12388239
  135. Koskivirta I Kassiri Z Rahkonen O Kiviranta R Oudit GY McKee TD Kyto V Saraste A Jokinen E Liu PP Vuoio E Khokha R Mice with tissue inhibitor of metalloproteinases 4 (Timp4) deletion succumb to induced myocardial infarction but not to cardiac pressure overload J Biol Chem 2010 285 24487 24493 20516072 PMC2915685
  136. Glass C Singla DK Overexpression of TIMP-1 in embryonic stem cells attenuates adverse cardiac remodeling following myocardial infarction Cell Transplant 2012 Epub ahead of print, PMID:22449760 22449760
  137. Jayasankar V Woo YJ Bish LT Pirolli TJ Berry MF Burdick J Bhalla RC Sharma RV Gardner TJ Sweeney HL Inhibition of matrix metalloproteinase activity by TIMP-1 gene transfer effectively treats ischemic cardiomyopathy Circulation 2004 110 II180 II186 15364860
  138. Ramani R Nilles K Gibson G Burkhead B Mathier M McNamara D McTiernan CF Tissue inhibitor of metalloproteinase-2 gene delivery ameliorates postinfarction cardiac remodeling Clin Transl Sci 2011 4 24 31 21348952 PMC3079205
  139. Matsusaka H Ide T Matsushima S Ikeuchi M Kubota T Sunagawa K Kinugawa S Tsutsui H Targeted deletion of matrix metalloproteinase 2 ameliorates myocardial remodeling in mice with chronic pressure overload Hypertension 2006 47 711 717 16505197
  140. Heymans S Lupu F Terclavers S Vanwetswinkel B Herbert JM Baker A Collen D Carmeliet P Moons L Loss or inhibition of uPA or MMP-9 attenuates LV remodeling and dysfunction after acute pressure overload in mice Am J Pathol 2005 166 15 25 15631996 PMC1602291
  141. Kassiri Z Oudit GY Sanchez O Dawood F Mohammed FF Nuttall RK Edwards DR Liu PP Backx PH Khokha R Combination of tumor necrosis factor-alpha ablation and matrix metalloproteinase inhibition prevents heart failure after pressure overload in tissue inhibitor of metalloproteinase-3 knock-out mice Circ Res 2005 97 380 390 16037568
  142. Kassiri Z Defamie V Hariri M Oudit GY Anthwal S Dawood F Liu P Khokha R Simultaneous transforming growth factor beta-tumor necrosis factor activation and cross-talk cause aberrant remodeling response and myocardial fibrosis in Timp3-deficient heart J Biol Chem 2009 284 29893 29904 19625257 PMC2785619

Cited by

Sorted by citations

Authors
Fan, D., Takawale, A., Lee, J., & Kassiri, Z.
Affiliations
University of Alberta (CA)
Corresponding author
Kassiri, Zamaneh
ORCID
Kassiri, Zamaneh
Venue
Fibrogenesis & Tissue Repair
Publisher
Springer Science and Business Media LLC
Published
2012-09-03
Volume
5
Issue
1
Pages
15-15
ISSN
1755-1536 (ISSN-L)
DOI
10.1186/1755-1536-5-15
PMC
PMC3464725
OpenAlex
W2132250523
Cited by
814
References
6
Citations by year
2026: 30 · 2025: 57 · 2024: 41 · 2023: 70 · 2022: 71 · 2021: 78 · 2020: 84 · 2019: 74 · 2018: 85 · 2017: 71 · 2016: 59 · 2015: 48 · 2014: 27 · 2013: 17 · 2012: 2
FWCI
19.34
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Fibrogenesis & Tissue Repair (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Heart and Stroke Foundation of Canada
  • Alberta Innovates
  • Canadian Institutes of Health Research
Topics
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
  • Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Keywords
cardiac fibroblasts, myocardial fibrosis, extracellular matrix remodeling, extracellular matrix homeostasis, matrix metalloproteinases, tissue inhibitors of metalloproteinases, myofibroblast transformation, bone marrow-derived fibroblasts, endothelial-to-mesenchymal transition, heart disease, genetically modified mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review