Translational lessons from scarless healing of cutaneous wounds and regenerative repair of the myocardium

Journal of Molecular and Cellular Cardiology

Volumn 48, Issue 3, 2010, Pages 550-557

  Palatinus, Joseph A ^a   Rhett, J Matthew ^a   Gourdie, Robert G ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Connexin 43; Gap junction; Heart; Myocardial infarction; Regenerative healing; Skin; Stem cell; TGF ; Wound repair

Indexed keywords

CONNEXIN 43; TRANSFORMING GROWTH FACTOR BETA;

DIABETES MELLITUS; GAP JUNCTION; HEART INFARCTION; HEART INJURY; HEART MUSCLE; HEART MUSCLE FIBROSIS; HEART TRANSPLANTATION; HUMAN; INFLAMMATION; MUSCLE REGENERATION; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVASCULARIZATION; REVIEW; SCAR FORMATION; SIGNAL TRANSDUCTION; SKIN GRAFT; SKIN INJURY; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE REPAIR; WOUND HEALING;

ANIMALS; CICATRIX; HUMANS; MODELS, BIOLOGICAL; MYOCARDIAL INFARCTION; MYOCARDIUM; SKIN; WOUND HEALING;

MAMMALIA;

EID: 77649272755     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.06.013     Document Type: Review

References (78)

1. Longaker M.T., Whitby D.J., Ferguson M.W., Lorenz H.P., Harrison M.R., Adzick N.S. Adult skin wounds in the fetal environment heal with scar formation. Ann. Surg. 1994 Jan, 219(1):65-72.
2. Clark R. Wound repair overview and general considerations. The Molecular and Cellular Biology of Wound Repair 1996, 3-50. Plenum Press, New York. R. Clark (Ed.).
3. Bertalanffy F.D. Comparison of mitotic rates in normal renewing and neoplastic cell populations. Proc. Can. Cancer Conf. 1967, 7:65-83.
4. Sun Y., Weber K.T. Infarct scar: a dynamic tissue. Cardiovasc. Res. 2000 May, 46(2):250-256.
5. Aarabi S., Bhatt K.A., Shi Y., Paterno J., Chang E.I., Loh S.A., et al. Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis. Faseb J. 2007 Oct, 21(12):3250-3261.
6. Rhett J.M., Ghatnekar G.S., Palatinus J.A., O'Quinn M., Yost M.J., Gourdie R.G. Novel therapies for scar reduction and regenerative healing of skin wounds. Trends Biotechnol. 2008 Apr, 26(4):173-180.
7. Prasertsung I., Kanokpanont S., Bunaprasert T., Thanakit V., Damrongsakkul S. Development of acellular dermis from porcine skin using periodic pressurized technique. J. Biomed. Mater. Res., B. Appl. Biomater. 2008 Apr, 85(1):210-219.
8. Dovi J.V., He L.K., DiPietro L.A. Accelerated wound closure in neutrophil-depleted mice. J. Leukoc. Biol. 2003 Apr, 73(4):448-455.
9. Romson J.L., Hook B.G., Kunkel S.L., Abrams G.D., Schork M.A., Lucchesi B.R. Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 1983 May, 67(5):1016-1023.
10. Wang J., Jiao H., Stewart T., Lyons M.V., Shankosky H.A., Scott P.G., et al. Accelerated wound healing in leukocyte-specific, protein 1-deficient mouse is associated with increased infiltration of leukocytes and fibrocytes. J. Leukoc. Biol. 2007 Sep 4.
11. Bodi V., Sanchis J., Nunez J., Mainar L., Minana G., Benet I., et al. Uncontrolled immune response in acute myocardial infarction: unraveling the thread. Am. Heart J. 2008 Dec, 156(6):1065-1073.
12. Neuman R.B., Bloom H.L., Shukrullah I., Darrow L.A., Kleinbaum D., Jones D.P., et al. Oxidative stress markers are associated with persistent atrial fibrillation. Clin. Chem. 2007 Sep, 53(9):1652-1657.
13. Amadeu T., Braune A., Mandarim-de-Lacerda C., Porto L.C., Desmouliere A., Costa A. Vascularization pattern in hypertrophic scars and keloids: a stereological analysis. Pathol. Res. Pract. 2003, 199(7):469-473.
14. Molin D., Post M.J. Therapeutic angiogenesis in the heart: protect and serve. Curr. Opin. Pharmacol. 2007 Apr, 7(2):158-163.
15. Annex B.H., Simons M. Growth factor-induced therapeutic angiogenesis in the heart: protein therapy. Cardiovasc. Res. 2005 Feb 15, 65(3):649-655.
16. Yoshioka J., Lee R.T. Vascularization as a potential enemy in valvular heart disease. Circulation 2008 Oct. 21, 118(17):1694-1696.
17. Shah M., Foreman D.M., Ferguson M.W. Neutralisation of TGF-beta 1 and TGF-beta 2 or exogenous addition of TGF-beta 3 to cutaneous rat wounds reduces scarring. J. Cell. Sci. 1995 Mar, 108(Pt 3):985-1002.
18. Ferguson M.W., Duncan J., Bond J., Bush J., Durani P., So K., et al. Prophylactic administration of avotermin for improvement of skin scarring: three double-blind, placebo-controlled, phase I/II studies. Lancet 2009 Apr 11, 373(9671):1264-1274.
19. Ellmers L.J., Scott N.J., Medicherla S., Pilbrow A.P., Bridgman P.G., Yandle T.G., et al. Transforming growth factor-beta blockade down-regulates the renin-angiotensin system and modifies cardiac remodeling after myocardial infarction. Endocrinology 2008 Nov, 149(11):5828-5834.
20. Pfeffer M.A., Braunwald E., Moye L.A., Basta L., Brown E.J., Cuddy T.E., et al. Effect of captopril on mortality and morbidity in patients with left ventricular dysfunction after myocardial infarction. Results of the survival and ventricular enlargement trial. The SAVE Investigators. N. Engl. J. Med. 1992 Sep 3, 327(10):669-677.
21. Zhang C.H., Lu J., Yu X.J., Sun L., Zang W.J. Ameliorative effect of Captopril and Valsartan on an animal model of diabetic cardiomyopathy. Biol. Pharm. Bull. 2008 Nov, 31(11):2045-2049.
22. Cohn R.D., van Erp C., Habashi J.P., Soleimani A.A., Klein E.C., Lisi M.T., et al. Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat. Med. 2007 Feb, 13(2):204-210.
23. Spinale F.G. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol. Rev. 2007 Oct, 87(4):1285-1342.
24. Wolk R., Cobbe S.M., Hicks M.N., Kane K.A. Functional, structural, and dynamic basis of electrical heterogeneity in healthy and diseased cardiac muscle: implications for arrhythmogenesis and anti-arrhythmic drug therapy. Pharmacol. Ther. 1999 Nov, 84(2):207-231.
25. Ehrlich H.P., Diez T. Role for gap junctional intercellular communications in wound repair. Wound Repair Regen 2003 Nov-Dec, 11(6):481-489.
26. Qiu C., Coutinho P., Frank S., Franke S., Law L.Y., Martin P., et al. Targeting connexin43 expression accelerates the rate of wound repair. Curr. Biol. 2003 Sep 30, 13(19):1697-1703.
27. Chanson M., Derouette J.P., Roth I., Foglia B., Scerri I., Dudez T., et al. Gap junctional communication in tissue inflammation and repair. Biochim. Biophys. Acta 2005 Jun 10, 1711(2):197-207.
28. Kostin S., Rieger M., Dammer S., Hein S., Richter M., Klovekorn W.P., et al. Gap junction remodeling and altered connexin43 expression in the failing human heart. Mol. Cell. Biochem. 2003 Jan, 242(1-2):135-144.
29. Kanno S., Kovacs A., Yamada K.A., Saffitz JE Connexin43 as a determinant of myocardial infarct size following coronary occlusion in mice. J Am Coll Cardiol 2003 Feb. 19., 41(4):681-686.
30. Asazuma-Nakamura Y., Dai P., Harada Y., Jiang Y., Hamaoka K., Takamatsu T. Cx43 contributes to TGF-beta signaling to regulate differentiation of cardiac fibroblasts into myofibroblasts. Exp. Cell. Res. 2009 Apr 15, 315(7):1190-1199.
31. Ghatnekar G.S., O'Quinn M.P., Jourdan L.J., Gurjarpadhye A.A., Draughn R.L., Gourdie R.G. Connexin43 carboxyl-terminal peptides reduce scar progenitor and promote regenerative healing following skin wounding. Regen. Med. 2009 Mar, 4(2):205-223.
32. Lindsey M.L., Escobar G.P., Mukherjee R., Goshorn D.K., Sheats N.J., Bruce J.A., et al. Matrix metalloproteinase-7 affects connexin-43 levels, electrical conduction, and survival after myocardial infarction. Circulation 2006 Jun 27, 113(25):2919-2928.
33. Lerner D.L., Yamada K.A., Schuessler R.B., Saffitz J.E. Accelerated onset and increased incidence of ventricular arrhythmias induced by ischemia in Cx43-deficient mice. Circulation 2000 2000/02/08/, 101(5):547-552.
34. Gutstein D.E., Morley G.E., Vaidya D., Liu F., Chen F.L., Stuhlmann H., et al. Heterogeneous expression of gap junction channels in the heart leads to conduction defects and ventricular dysfunction. Circulation 2001, 104:1194-1199.
35. O'Quinn M., Harris B., Hewett K., Gourdie R. A Peptide containing the carboxy-terminal domain of connexin43 reduces arrhythmias and improves cardiac function after myocardial injury. Circulation 2009, 118.
36. Hunter A.W., Barker R.J., Zhu C., Gourdie R.G. Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion. Mol. Biol. Cell. 2005 Dec, 16(12):5686-5698.
37. Boengler K., Stahlhofen S., van de Sand A., Gres P., Ruiz-Meana M., Garcia-Dorado D., et al. Presence of connexin 43 in subsarcolemmal, but not in interfibrillar cardiomyocyte mitochondria. Basic Res. Cardiol. 2009 Mar, 104(2):141-147.
38. Camelliti P., Borg T.K., Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc. Res. 2005 Jan 1, 65(1):40-51.
39. Spinale F.G. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ. Res. 2002 Mar 22, 90(5):520-530.
40. van Zuijlen P.P., Ruurda J.J., van Veen H.A., van Marle J., van Trier A.J., Groenevelt F., et al. Collagen morphology in human skin and scar tissue: no adaptations in response to mechanical loading at joints. Burns 2003 Aug, 29(5):423-431.
41. Stramer B.M., Mori R., Martin P. The inflammation-fibrosis link? A Jekyll and Hyde role for blood cells during wound repair. J. Invest. Dermatol. 2007 May, 127(5):1009-1017.
42. Mollmann H., Nef H.M., Kostin S., von Kalle C., Pilz I., Weber M., et al. Bone marrow-derived cells contribute to infarct remodelling. Cardiovasc. Res. 2006 Sep 1, 71(4):661-671.
43. Wang J., Chen H., Shankowsky H.A., Scott P.G., Tredget E.E. Improved scar in postburn patients following interferon-alpha2b treatment is associated with decreased angiogenesis mediated by vascular endothelial cell growth factor. J. Interferon Cytokine Res. 2008 Jul, 28(7):423-434.
44. Desmouliere A., Chaponnier C., Gabbiani G. Tissue repair, contraction, and the myofibroblast. Wound Repair Regen. 2005 Jan-Feb, 13(1):7-12.
45. Miragoli M., Salvarani N., Rohr S. Myofibroblasts induce ectopic activity in cardiac tissue. Circ. Res. 2007 Oct 12, 101(8):755-758.
46. Poss K.D., Wilson L.G., Keating M.T. Heart regeneration in zebrafish. Science 2002 Dec 13, 298(5601):2188-2190.
47. Lepilina A., Coon A.N., Kikuchi K., Holdway J.E., Roberts R.W., Burns C.G., et al. A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 2006 Nov 3, 127(3):607-619.
48. Ausoni S., Sartore S. From fish to amphibians to mammals: in search of novel strategies to optimize cardiac regeneration. J. Cell Biol. 2009 Feb 9, 184(3):357-364.
49. Stoick-Cooper C.L., Moon R.T., Weidinger G. Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev. 2007 Jun 1, 21(11):1292-1315.
50. Heber-Katz E., Leferovich J., Bedelbaeva K., Gourevitch D., Clark L. The scarless heart and the MRL mouse. Philos. Trans. R. Soc. Lond., B. Biol. Sci. 2004 May 29, 359(1445):785-793.
51. Colwell A.S., Krummel T.M., Kong W., Longaker M.T., Lorenz H.P. Skin wounds in the MRL/MPJ mouse heal with scar. Wound Repair Regen. 2006 Jan-Feb, 14(1):81-90.
52. Tucker B., Klassen H., Yang L., Chen D.F., Young M.J. Elevated MMP expression in the MRL mouse retina creates a permissive environment for retinal regeneration. Invest. Ophthalmol. Vis. Sci. 2008 Apr, 49(4):1686-1695.
53. Grisel P., Meinhardt A., Lehr H.A., Kappenberger L., Barrandon Y., Vassalli G. The MRL mouse repairs both cryogenic and ischemic myocardial infarcts with scar. Cardiovasc. Pathol. 2008 Jan-Feb, 17(1):14-22.
54. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005 Nov 12, 366(9498):1736-1743.
55. Galkowska H., Wojewodzka U., Olszewski W.L. Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers. Wound Repair Regen. 2006 Sep-Oct, 14(5):558-565.
56. Asbun J., Villarreal F.J. The pathogenesis of myocardial fibrosis in the setting of diabetic cardiomyopathy. J. Am. Coll. Cardiol. 2006 Feb 21, 47(4):693-700.
57. Acosta J.B., del Barco D.G., Vera D.C., Savigne W., Lopez-Saura P., Guillen Nieto G., et al. The pro-inflammatory environment in recalcitrant diabetic foot wounds. Int. Wound J. 2008 Oct, 5(4):530-539.
58. Hatanaka E., Monteagudo P.T., Marrocos M.S., Campa A. Neutrophils and monocytes as potentially important sources of proinflammatory cytokines in diabetes. Clin. Exp. Immunol. 2006 Dec, 146(3):443-447.
59. Pradhan L., Nabzdyk C., Andersen N.D., LoGerfo F.W., Veves A. Inflammation and neuropeptides: the connection in diabetic wound healing. Expert. Rev. Mol. Med. 2009, 11:e2.
60. Liu Z.J., Velazquez O.C. Hyperoxia, endothelial progenitor cell mobilization, and diabetic wound healing. Antioxid. Redox Signal 2008 Nov, 10(11):1869-1882.
61. Lobmann R., Ambrosch A., Schultz G., Waldmann K., Schiweck S., Lehnert H. Expression of matrix-metalloproteinases and their inhibitors in the wounds of diabetic and non-diabetic patients. Diabetologia 2002 Jul, 45(7):1011-1016.
62. Wang C.M., Lincoln J., Cook J.E., Becker D.L. Abnormal connexin expression underlies delayed wound healing in diabetic skin. Diabetes 2007 Nov, 56(11):2809-2817.
63. Marfella R., D'Amico M., Di Filippo C., Piegari E., Nappo F., Esposito K., et al. Myocardial infarction in diabetic rats: role of hyperglycaemia on infarct size and early expression of hypoxia-inducible factor 1. Diabetologia 2002 Aug, 45(8):1172-1181.
64. McDonagh P.F., Hokama J.Y. Microvascular perfusion and transport in the diabetic heart. Microcirculation 2000 Jun, 7(3):163-181.
65. Kranke P., Bennett M., Roeckl-Wiedmann I., Debus S. Hyperbaric oxygen therapy for chronic wounds. Cochrane Database Syst. Rev. 2004, (2):CD004123.
66. Khan M., Meduru S., Mohan I.K., Kuppusamy M.L., Wisel S., Kulkarni A., et al. Hyperbaric oxygenation enhances transplanted cell graft and functional recovery in the infarct heart. J. Mol. Cell Cardiol. 2009 Apr 17.
67. Fujimoto K.L., Tobita K., Merryman W.D., Guan J., Momoi N., Stolz D.B., et al. An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. J. Am. Coll. Cardiol. 2007 Jun 12, 49(23):2292-2300.
68. Ott H.C., Matthiesen T.S., Goh S.K., Black L.D., Kren S.M., Netoff T.I., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 2008 Jan 13.
69. Eschenhagen T., Zimmermann W.H. Engineering myocardial tissue. Circ. Res. 2005 Dec 9, 97(12):1220-1231.
70. Seo Y.K., Song K.Y., Kim Y.J., Park J.K. Wound healing effect of acellular artificial dermis containing extracellular matrix secreted by human skin fibroblasts. Artif. Organs 2007 Jul, 31(7):509-520.
71. Black L.D., Meyers J.D., Weinbaum J.S., Shvelidze Y.A., Tranquillo R.T. Cell-induced alignment augments twitch force in fibrin gel-based engineered myocardium via gap junction modification. Tissue Eng. Part A. 2009 Apr 1.
72. Quaini F., Urbanek K., Beltrami A.P., Finato N., Beltrami C.A., Nadal-Ginard B., et al. Chimerism of the transplanted heart. N. Engl. J. Med. 2002 Jan 3, 346(1):5-15.
73. Bergmann O., Bhardwaj R.D., Bernard S., Zdunek S., Barnabe-Heider F., Walsh S., et al. Evidence for cardiomyocyte renewal in humans. Science 2009 Apr 3, 324(5923):98-102.
74. Kajstura J., Urbanek K., Rota M., Bearzi C., Hosoda T., Bolli R., et al. Cardiac stem cells and myocardial disease. J. Mol. Cell. Cardiol. 2008 Oct, 45(4):505-513.
75. Rubart M., Field L.J. Stem cell differentiation: cardiac repair. Cells Tissues Organs 2008, 188(1-2):202-211.
76. Martin-Puig S., Wang Z., Chien K.R. Lives of a heart cell: tracing the origins of cardiac progenitors. Cell Stem Cell 2008 Apr 10, 2(4):320-331.
77. Liu P., Deng Z., Han S., Liu T., Wen N., Lu W., et al. Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif. Organs 2008 Dec, 32(12):925-931.
78. Akasha A.A., Sotiriadou I., Doss M.X., Halbach M., Winkler J., Baunach J.J., et al. Entrapment of embryonic stem cells-derived cardiomyocytes in macroporous biodegradable microspheres: preparation and characterization. Cell Physiol. Biochem. 2008, 22(5-6):665-672.