Common threads in cardiac fibrosis, infarct scar formation, and wound healing

Fibrogenesis and Tissue Repair

Volumn 5, Issue 1, 2012, Pages

  Czubryt, Michael P ^a  

^a St Boniface Research Centre   (Canada)

Author keywords

Cardiac infarct scar; Collagen; Fibrosis; Wound healing

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 3; CONNECTIVE TISSUE GROWTH FACTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MATRIX METALLOPROTEINASE; SMAD3 PROTEIN; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA;

BLOOD CLOTTING; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL REGENERATION; CELL TYPE; COLLAGEN SYNTHESIS; EPITHELIZATION; EXTRACELLULAR MATRIX; FIBROBLAST; GENE DELETION; GENE EXPRESSION; HEART ARRHYTHMIA; HEART CONTRACTION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE FIBROSIS; HEART MUSCLE RELAXATION; HEMOSTASIS; HUMAN; KELOID; LYMPHOCYTE; MACROPHAGE; MONOCYTE; MYOFIBROBLAST; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SCAR FORMATION; THROMBOCYTE ACTIVATION; UPREGULATION; WOUND HEALING; WOUND HEALING IMPAIRMENT;

EID: 84871869933     PISSN: None     EISSN: 17551536     Source Type: Journal    
DOI: 10.1186/1755-1536-5-19     Document Type: Review

References (83)

1. Espira L, Czubryt MP. Emerging concepts in cardiac matrix biology. Can J Physiol Pharmacol 2009, 87:996-1008. 10.1139/Y09-105, 20029536.
2. Weber KT, Sun Y, Katwa LC. Wound healing following myocardial infarction. Clin Cardiol 1996, 19:447-455. 10.1002/clc.4960190602, 8790947.
3. Enoch S, Leaper DJ. Basic science of wound healing. Surgery 2005, 23:37-42.
4. Undas A, Ariens RA. Fibrin clot structure and function: a role in the pathophysiology of arterial and venous thromboembolic diseases. Arterioscler Thromb Vasc Biol 2011, 31:e88-e99. 10.1161/ATVBAHA.111.230631, 21836064.
5. Brass LF, Wannemacher KM, Ma P, Stalker TJ. Regulating thrombus growth and stability to achieve an optimal response to injury. J Thromb Haemost 2011, 9(Suppl 1):66-75. 3422128, 21781243.
6. Crawford JR, Haudek SB, Cieslik KA, Trial J, Entman ML. Origin of developmental precursors dictates the pathophysiologic role of cardiac fibroblasts. J Cardiovasc Transl Res 2012,
7. Ehrlich HP, Rajaratnam JB. Cell locomotion forces versus cell contraction forces for collagen lattice contraction: an in vitro model of wound contraction. Tissue Cell 1990, 22:407-417. 10.1016/0040-8166(90)90070-P, 2260082.
8. Harris AK, Stopak D, Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 1981, 290:249-251. 10.1038/290249a0, 7207616.
9. Gabbiani G, Ryan GB, Majne G. Presence of modified fibroblasts in granulation tissue and their possible role in wound contraction. Experientia 1971, 27:549-550. 10.1007/BF02147594, 5132594.
10. Porter S. The role of the fibroblast in wound contraction and healing. Wounds UK 2007, 3:33-40.
11. Desmouliere A, Redard M, Darby I, Gabbiani G. Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 1995, 146:56-66. 1870783, 7856739.
12. Bakker K, Schaper NC. The development of global consensus guidelines on the management and prevention of the diabetic foot 2011. Diabetes Metab Res Rev 2012, 28(Suppl 1):116-118.
13. Wall IB, Moseley R, Baird DM, Kipling D, Giles P, Laffafian I, Price PE, Thomas DW, Stephens P. Fibroblast dysfunction is a key factor in the non-healing of chronic venous leg ulcers. J Invest Dermatol 2008, 128:2526-2540. 10.1038/jid.2008.114, 18449211.
14. Ramelet AA, Hirt-Burri N, Raffoul W, Scaletta C, Pioletti DP, Offord E, Mansourian R, Applegate LA. Chronic wound healing by fetal cell therapy may be explained by differential gene profiling observed in fetal versus old skin cells. Exp Gerontol 2009, 44:208-218. 10.1016/j.exger.2008.11.004, 19049860.
15. Jun JI, Lau LF. The matricellular protein CCN1 induces fibroblast senescence and restricts fibrosis in cutaneous wound healing. Nat Cell Biol 2010, 12:676-685. 10.1038/ncb2070, 2919364, 20526329.
16. Berman B, Bieley HC. Adjunct therapies to surgical management of keloids. Dermatol Surg 1996, 22:126-130.
17. Shockman S, Paghdal KV, Cohen G. Medical and surgical management of keloids: a review. J Drugs Dermatol 2010, 9:1249-1257.
18. Parsonage G, Filer AD, Haworth O, Nash GB, Rainger GE, Salmon M, Buckley CD. A stromal address code defined by fibroblasts. Trends Immunol 2005, 26:150-156. 10.1016/j.it.2004.11.014, 3121558, 15745857.
19. Flavell SJ, Hou TZ, Lax S, Filer AD, Salmon M, Buckley CD. Fibroblasts as novel therapeutic targets in chronic inflammation. Br J Pharmacol 2008, 153(Suppl 1):S241-S246. 2268075, 17965753.
20. Murphy KE, McCue SW, McElwain DL. Clinical strategies for the alleviation of contractures from a predictive mathematical model of dermal repair. Wound Repair Regen 2012, 20:194-202. 10.1111/j.1524-475X.2012.00775.x, 22313453.
21. 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. 10.1002/dvdy.22280, 20503355.
22. Carlson S, Trial J, Soeller C, Entman ML. Cardiac mesenchymal stem cells contribute to scar formation after myocardial infarction. Cardiovasc Res 2011, 91:99-107. 10.1093/cvr/cvr061, 3112022, 21357194.
23. Zhou B, Pu WT. Epicardial epithelial-to-mesenchymal transition in injured heart. J Cell Mol Med 2011, 15:2781-2783. 10.1111/j.1582-4934.2011.01450.x, 3226901, 21914126.
24. Willems IE, Havenith MG, De Mey JG, Daemen MJ. The alpha-smooth muscle actin-positive cells in healing human myocardial scars. Am J Pathol 1994, 145:868-875. 1887334, 7943177.
25. Miragoli M, Salvarani N, Rohr S. Myofibroblasts induce ectopic activity in cardiac tissue. Circ Res 2007, 101:755-758.
26. Vasquez C, Benamer N, Morley GE. The cardiac fibroblast: functional and electrophysiological considerations in healthy and diseased hearts. J Cardiovasc Pharmacol 2011, 57:380-388. 10.1097/FJC.0b013e31820cda19, 3077441, 21242811.
27. Creemers EE, Pinto YM. Molecular mechanisms that control interstitial fibrosis in the pressure-overloaded heart. Cardiovasc Res 2011, 89:265-272. 10.1093/cvr/cvq308, 20880837.
28. Katwa LC, Shashikant CS. Cardiac remodeling and fibrosis: Role of myofibroblasts. The Cardiac Fibroblast 2011, 29-52. Research Signpost, Trivandrum, Turner NA.
29. Gramley F, Lorenzen J, Pezzella F, Kettering K, Himmrich E, Plumhans C, Koellensperger E, Munzel T. Hypoxia and myocardial remodeling in human cardiac allografts: a time-course study. J Heart Lung Transplant 2009, 28:1119-1126. 10.1016/j.healun.2009.05.038, 19782587.
30. Lokmic Z, Musyoka J, Hewitson TD, Darby IA. Hypoxia and hypoxia signaling in tissue repair and fibrosis. Int Rev Cell Mol Biol 2012, 296:139-185.
31. Deschene K, Celeste C, Boerboom D, Theoret CL. Hypoxia regulates the expression of extracellular matrix associated proteins in equine dermal fibroblasts via HIF1. J Dermatol Sci 2012, 65:12-18. 10.1016/j.jdermsci.2011.09.006, 21999945.
32. Ohtani K, Yutani C, Nagata S, Koretsune Y, Hori M, Kamada T. High prevalence of atrial fibrosis in patients with dilated cardiomyopathy. J Am Coll Cardiol 1995, 25:1162-1169. 10.1016/0735-1097(94)00529-Y, 7897130.
33. Cieslik KA, Taffet GE, Carlson S, Hermosillo J, Trial J, Entman ML. Immune-inflammatory dysregulation modulates the incidence of progressive fibrosis and diastolic stiffness in the aging heart. J Mol Cell Cardiol 2011, 50:248-256. 10.1016/j.yjmcc.2010.10.019, 3019252, 20974150.
34. Ramirez F, Tanaka S, Bou-Gharios G. Transcriptional regulation of the human alpha2(I) collagen gene (COL1A2), an informative model system to study fibrotic diseases. Matrix Biol 2006, 25:365-372. 10.1016/j.matbio.2006.05.002, 16815696.
35. Chen SJ, Yuan W, Lo S, Trojanowska M, Varga J. Interaction of smad3 with a proximal smad-binding element of the human alpha2(I) procollagen gene promoter required for transcriptional activation by TGF-beta. J Cell Physiol 2000, 183:381-392. 10.1002/(SICI)1097-4652(200006)183:3<381::AID-JCP11>3.0.CO;2-O, 10797313.
36. Dobaczewski M, Bujak M, Li N, Gonzalez-Quesada C, Mendoza LH, Wang XF, Frangogiannis NG. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ Res 2010, 107:418-428. 10.1161/CIRCRESAHA.109.216101, 2917472, 20522804.
37. Kenyon NJ, Ward RW, McGrew G, Last JA. TGF-beta1 causes airway fibrosis and increased collagen I and III mRNA in mice. Thorax 2003, 58:772-777. 10.1136/thorax.58.9.772, 1746790, 12947136.
38. Gressner AM, Weiskirchen R. Modern pathogenetic concepts of liver fibrosis suggest stellate cells and TGF-beta as major players and therapeutic targets. J Cell Mol Med 2006, 10:76-99. 10.1111/j.1582-4934.2006.tb00292.x, 16563223.
39. Wang B, Komers R, Carew R, Winbanks CE, Xu B, Herman-Edelstein M, Koh P, Thomas M, Jandeleit-Dahm K, Gregorevic P, et al. Suppression of microRNA-29 expression by TGF-beta1 promotes collagen expression and renal fibrosis. J Am Soc Nephrol 2012, 23:252-265. 10.1681/ASN.2011010055, 22095944.
40. Massague J. TGFbeta in cancer. Cell 2008, 134:215-230. 10.1016/j.cell.2008.07.001, 3512574, 18662538.
41. Ashcroft GS, Yang X, Glick AB, Weinstein M, Letterio JL, Mizel DE, Anzano M, Greenwell-Wild T, Wahl SM, Deng C, Roberts AB. Mice lacking Smad3 show accelerated wound healing and an impaired local inflammatory response. Nat Cell Biol 1999, 1:260-266. 10.1038/12971, 10559937.
42. Tsuboi R, Shi CM, Sato C, Cox GN, Ogawa H. Co-administration of insulin-like growth factor (IGF)-I and IGF-binding protein-1 stimulates wound healing in animal models. J Invest Dermatol 1995, 104:199-203. 10.1111/1523-1747.ep12612755, 7530269.
43. Brown DL, Kane CD, Chernausek SD, Greenhalgh DG. Differential expression and localization of insulin-like growth factors I and II in cutaneous wounds of diabetic and nondiabetic mice. Am J Pathol 1997, 151:715-724. 1857837, 9284820.
44. Ghahary A, Shen YJ, Wang R, Scott PG, Tredget EE. Expression and localization of insulin-like growth factor-1 in normal and post-burn hypertrophic scar tissue in human. Mol Cell Biochem 1998, 183:1-9. 10.1023/A:1006890212478, 9655173.
45. Blakytny R, Jude EB, Martin Gibson J, Boulton AJ, Ferguson MW. Lack of insulin-like growth factor 1 (IGF1) in the basal keratinocyte layer of diabetic skin and diabetic foot ulcers. J Pathol 2000, 190:589-594. 10.1002/(SICI)1096-9896(200004)190:5<589::AID-PATH553>3.0.CO;2-T, 10727985.
46. Bitar MS, Al-Mulla F. ROS constitute a convergence nexus in the development of IGF1 resistance and impaired wound healing in a rat model of type 2 diabetes. Dis Model Mech 2012, 5:375-388. 10.1242/dmm.007872, 3339831, 22362362.
47. Cambrey AD, Kwon OJ, Gray AJ, Harrison NK, Yacoub M, Barnes PJ, Laurent GJ, Chung KF. Insulin-like growth factor I is a major fibroblast mitogen produced by primary cultures of human airway epithelial cells. Clin Sci (Lond) 1995, 89:611-617.
48. Wynes MW, Frankel SK, Riches DW. IL-4-induced macrophage-derived IGF-I protects myofibroblasts from apoptosis following growth factor withdrawal. J Leukoc Biol 2004, 76:1019-1027. 10.1189/jlb.0504288, 15316031.
49. Butt RP, Laurent GJ, Bishop JE. Mechanical load and polypeptide growth factors stimulate cardiac fibroblast activity. Ann N Y Acad Sci 1995, 752:387-393. 10.1111/j.1749-6632.1995.tb17446.x, 7755282.
50. Kanellakis P, Ditiatkovski M, Kostolias G, Bobik A. A pro-fibrotic role for interleukin-4 in cardiac pressure overload. Cardiovasc Res 2012, 95:77-85. 10.1093/cvr/cvs142, 22492684.
51. Vivar R, Humeres C, Varela M, Ayala P, Guzman N, Olmedo I, Catalan M, Boza P, Munoz C, Diaz Araya G. Cardiac fibroblast death by ischemia/reperfusion is partially inhibited by IGF-1 through both PI3K/Akt and MEK-ERK pathways. Exp Mol Pathol 2012, 93:1-7. 10.1016/j.yexmp.2012.01.010, 22537549.
52. Ito M, Kodama M, Tsumanuma I, Ramadan MM, Hirayama S, Kamimura T, Kashimura T, Fuse K, Hirono S, Okura Y, Aizawa Y. Relationship between insulin-like growth factor-I and brain natriuretic peptide in patients with acromegaly after surgery. Circ J 2007, 71:1955-1957. 10.1253/circj.71.1955, 18037753.
53. Delaughter MC, Taffet GE, Fiorotto ML, Entman ML, Schwartz RJ. Local insulin-like growth factor I expression induces physiologic, then pathologic, cardiac hypertrophy in transgenic mice. FASEB J 1999, 13:1923-1929.
54. Wang L, Ma W, Markovich R, Chen JW, Wang PH. Regulation of cardiomyocyte apoptotic signaling by insulin-like growth factor I. Circ Res 1998, 83:516-522. 10.1161/01.RES.83.5.516, 9734474.
55. Buerke M, Murohara T, Skurk C, Nuss C, Tomaselli K, Lefer AM. Cardioprotective effect of insulin-like growth factor I in myocardial ischemia followed by reperfusion. Proc Natl Acad Sci U S A 1995, 92:8031-8035. 10.1073/pnas.92.17.8031, 41280, 7644533.
56. Huang G, Brigstock DR. Regulation of hepatic stellate cells by connective tissue growth factor. Front Biosci 2012, 17:2495-2507. 10.2741/4067, 22652794.
57. Detillieux KA, Sheikh F, Kardami E, Cattini PA. Biological activities of fibroblast growth factor-2 in the adult myocardium. Cardiovasc Res 2003, 57:8-19. 10.1016/S0008-6363(02)00708-3, 12504809.
58. Abe M, Yokoyama Y, Ishikawa O. A possible mechanism of basic fibroblast growth factor-promoted scarless wound healing: the induction of myofibroblast apoptosis. Eur J Dermatol 2012, 22:46-53.
59. Yahata Y, Shirakata Y, Tokumaru S, Yang L, Dai X, Tohyama M, Tsuda T, Sayama K, Iwai M, Horiuchi M, Hashimoto K. A novel function of angiotensin II in skin wound healing. Induction of fibroblast and keratinocyte migration by angiotensin II via heparin-binding epidermal growth factor (EGF)-like growth factor-mediated EGF receptor transactivation. J Biol Chem 2006, 281:13209-13216. 10.1074/jbc.M509771200, 16543233.
60. Ivkovic S, Yoon BS, Popoff SN, Safadi FF, Libuda DE, Stephenson RC, Daluiski A, Lyons KM. Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 2003, 130:2779-2791. 10.1242/dev.00505, 3360973, 12736220.
61. Hall-Glenn F, De Young RA, Huang BL, van Handel B, Hofmann JJ, Chen TT, Choi A, Ong JR, Benya PD, Mikkola H, et al. CCN2/connective tissue growth factor is essential for pericyte adhesion and endothelial basement membrane formation during angiogenesis. PLoS One 2012, 7:e30562. 10.1371/journal.pone.0030562, 3282727, 22363445.
62. Pi L, Shenoy AK, Liu J, Kim S, Nelson N, Xia H, Hauswirth WW, Petersen BE, Schultz GS, Scott EW. CCN2/CTGF regulates neovessel formation via targeting structurally conserved cystine knot motifs in multiple angiogenic regulators. FASEB J 2012, 6:3365-79.
63. House SL, Bolte C, Zhou M, Doetschman T, Klevitsky R, Newman G, Schultz Jel J. Cardiac-specific overexpression of fibroblast growth factor-2 protects against myocardial dysfunction and infarction in a murine model of low-flow ischemia. Circulation 2003, 108:3140-3148. 10.1161/01.CIR.0000105723.91637.1C, 14656920.
64. Padua RR, Sethi R, Dhalla NS, Kardami E. Basic fibroblast growth factor is cardioprotective in ischemia-reperfusion injury. Mol Cell Biochem 1995, 143:129-135. 10.1007/BF01816946, 7596347.
65. Luo K, Stroschein SL, Wang W, Chen D, Martens E, Zhou S, Zhou Q. The Ski oncoprotein interacts with the Smad proteins to repress TGFbeta signaling. Genes Dev 1999, 13:2196-2206. 10.1101/gad.13.17.2196, 316985, 10485843.
66. Liu X, Zhang E, Li P, Liu J, Zhou P, Gu DY, Chen X, Cheng T, Zhou Y. Expression and possible mechanism of c-ski, a novel tissue repair-related gene during normal and radiation-impaired wound healing. Wound Repair Regen 2006, 14:162-171. 10.1111/j.1743-6109.2006.00106.x, 16630105.
67. Liu X, Li P, Liu P, Xiong R, Zhang E, Chen X, Gu D, Zhao Y, Wang Z, Zhou Y. The essential role for c-Ski in mediating TGF-beta1-induced bi-directional effects on skin fibroblast proliferation through a feedback loop. Biochem J 2008, 409:289-297. 10.1042/BJ20070545, 17725545.
68. Liu X, Li P, Chen XY, Zhou YG. c-Ski promotes skin fibroblast proliferation but decreases type I collagen: implications for wound healing and scar formation. Clin Exp Dermatol 2010, 35:417-424. 10.1111/j.1365-2230.2009.03606.x, 19874315.
69. Cunnington RH, Wang B, Ghavami S, Bathe KL, Rattan SG, Dixon IM. Antifibrotic properties of c-Ski and its regulation of cardiac myofibroblast phenotype and contractility. Am J Physiol Cell Physiol 2011, 300:C176-C186. 10.1152/ajpcell.00050.2010, 20943957.
70. Miyazono K, Koinuma D. Arkadia-beyond the TGF-beta pathway. J Biochem 2011, 149:1-3. 10.1093/jb/mvq133, 21109559.
71. Cserjesi P, Brown D, Ligon KL, Lyons GE, Copeland NG, Gilbert DJ, Jenkins NA, Olson EN. Scleraxis: a basic helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 1995, 121:1099-1110.
72. Murchison ND, Price BA, Conner DA, Keene DR, Olson EN, Tabin CJ, Schweitzer R. Regulation of tendon differentiation by scleraxis distinguishes force-transmitting tendons from muscle-anchoring tendons. Development 2007, 134:2697-2708. 10.1242/dev.001933, 17567668.
73. Espira L, Lamoureux L, Jones SC, Gerard RD, Dixon IM, Czubryt MP. The basic helix-loop-helix transcription factor scleraxis regulates fibroblast collagen synthesis. J Mol Cell Cardiol 2009, 47:188-195. 10.1016/j.yjmcc.2009.03.024, 19362560.
74. Lejard V, Brideau G, Blais F, Salingcarnboriboon R, Wagner G, Roehrl MH, Noda M, Duprez D, Houillier P, Rossert J. Scleraxis and NFATc regulate the expression of the pro-alpha1(I) collagen gene in tendon fibroblasts. J Biol Chem 2007, 282:17665-17675. 10.1074/jbc.M610113200, 17430895.
75. Bagchi RA, Czubryt MP. Synergistic roles of scleraxis and Smads in the regulation of collagen 1alpha2 gene expression. Biochim Biophys Acta 2012, 1823:1936-1944. 10.1016/j.bbamcr.2012.07.002, 22796342.
76. Mendias CL, Gumucio JP, Davis ME, Bromley CW, Davis CS, Brooks SV. Transforming growth factor-beta induces skeletal muscle atrophy and fibrosis through the induction of atrogin-1 and scleraxis. Muscle Nerve 2012, 45:55-59. 10.1002/mus.22232, 22190307.
77. Alberton P, Popov C, Pragert M, Kohler J, Shukunami C, Schieker M, Docheva D. Conversion of human bone marrow-derived mesenchymal stem cells into tendon progenitor cells by ectopic expression of scleraxis. Stem Cells Dev 2012, 21:846-858. 10.1089/scd.2011.0150, 21988170.
78. Naitoh M, Kubota H, Ikeda M, Tanaka T, Shirane H, Suzuki S, Nagata K. Gene expression in human keloids is altered from dermal to chondrocytic and osteogenic lineage. Genes Cells 2005, 10:1081-1091. 10.1111/j.1365-2443.2005.00902.x, 16236136.
79. Scott A, Sampaio A, Abraham T, Duronio C, Underhill TM. Scleraxis expression is coordinately regulated in a murine model of patellar tendon injury. J Orthop Res 2011, 29:289-296. 10.1002/jor.21220, 20740671.
80. Moellering RE, Cornejo M, Davis TN, Del Bianco C, Aster JC, Blacklow SC, Kung AL, Gilliland DG, Verdine GL, Bradner JE. Direct inhibition of the NOTCH transcription factor complex. Nature 2009, 462:182-188. 10.1038/nature08543, 2951323, 19907488.
81. Bishop JE, Laurent GJ. Collagen turnover and its regulation in the normal and hypertrophying heart. Eur Heart J 1995, 16(Suppl C):38-44. 10.1093/eurheartj/16.suppl_C.38, 8542880.
82. McAnulty RJ, Laurent GJ. Collagen synthesis and degradation in vivo. Evidence for rapid rates of collagen turnover with extensive degradation of newly synthesized collagen in tissues of the adult rat. Coll Relat Res 1987, 7:93-104.
83. Gulotta LV, Rodeo SA. Emerging ideas: evaluation of stem cells genetically modified with scleraxis to improve rotator cuff healing. Clin Orthop Relat Res 2011, 469:2977-2980. 10.1007/s11999-010-1727-4, 3171546, 21132407.