Cardiac fibroblasts protect cardiomyocytes against lethal ischemia-reperfusion injury

Journal of Molecular and Cellular Cardiology

Volumn 68, Issue , 2014, Pages 56-65

  Abrial, Maryline ^a   Da Silva, Claire Crola ^a   Pillot, Bruno ^a   Augeul, Lionel ^a   Ivanes, Fabrice ^a,b   Teixeira, Geoffrey ^a   Cartier, Régine ^c   Angoulvant, Denis ^b   Ovize, Michel ^a,c   Ferrera, René ^a  

^a UNIVERSITÉ LYON 1   (France)

^b FHU SUPORT   (France)

^c LOUIS PRADEL HOSPITAL   (France)

Author keywords

Cardiomyocytes; Cytokines; Fibroblasts; Growth factors; Hypoxia; Ischemia reperfusion injury

Indexed keywords

CARDIOMYOCYTES; CYTOKINES; FIBROBLASTS; GROWTH FACTORS; HYPOXIA; ISCHEMIA-REPERFUSION INJURY;

ANIMALS; CELL SURVIVAL; CULTURE MEDIA, CONDITIONED; CYTOKINES; HEART VENTRICLES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; MYOFIBROBLASTS; RATS; RATS, WISTAR; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84894242540     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.01.005     Document Type: Article

References (46)

1. Ieda M., Tsuchihashi T., Ivey K.N., Ross R.S., Hong T.-T., Shaw R.M., et al. Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev Cell 2009, 16:233-244.
2. Dell'Era P., Ronca R., Coco L., Nicoli S., Metra M., Presta M. Fibroblast growth factor receptor-1 is essential for in vitro cardiomyocyte development. Circ Res 2003, 93:414-420.
3. Bowers S.L.K., Banerjee I., Baudino T.A. The extracellular matrix: at the center of it all. J Mol Cell Cardiol 2009, 48:474-482.
4. Kakkar R., Lee R.T. Intramyocardial fibroblast myocyte communication. Circ Res 2010, 106:47-57.
5. Leask A. TGFbeta, cardiac fibroblasts, and the fibrotic response. Cardiovasc Res 2007, 74:207-212.
6. Fredj S., Bescond J., Louault C., Delwail A., Lecron J.-C., Potreau D. Role of interleukin-6 in cardiomyocyte/cardiac fibroblast interactions during myocyte hypertrophy and fibroblast proliferation. J Cell Physiol 2005, 204:428-436.
7. Takeda N., Manabe I., Uchino Y., Eguchi K., Matsumoto S., Nishimura S., et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest 2010, 120:254-265.
8. Seki K., Sanada S., Kudinova A.Y., Steinhauser M.L., Handa V., Gannon J., et al. Interleukin-33 prevents apoptosis and improves survival after experimental myocardial infarction through ST2 signaling. Circ Heart Fail 2009, 2:684-691.
9. Jiang Z.-S., Wen G.-B., Tang Z.-H., Srisakuldee W., Fandrich R.R., Kardami E. High molecular weight FGF-2 promotes postconditioning-like cardioprotection linked to activation of the protein kinase C isoforms Akt and p70 S6 kinase. Can J Physiol Pharmacol 2009, 87:798-804.
10. Liu X.-W., Margarida Bernado M., Fridman R., Kim H.-R.C. Tissue inhibitor of metalloproteinase-1 protects human breast epithelial cells against intrinsic apoptotic cell death via the focal adhesion kinase/phosphatidylinositol 3-kinase and MAPK signaling pathway. J Biol Chem 2003, 278:40364-40372.
11. Liu X.-W., Taube M.E., Jung K.-K. Tissue inhibitor of metalloproteinase-1 protects human breast epithelial cells from extrinsic cell death: a potential oncogenic activity of tissue inhibitor of metalloproteinase-1. Cancer Res 2005, 65:898-906.
12. Li G., Fridman R., Kim H.R. Tissue inhibitor of metalloproteinase-1 inhibits apoptosis of human breast epithelial cells. Cancer Res 1999, 59:6267-6275.
13. Ikonomidis J.S., Hendrick J.W., Parkhurst A.M., Herron A.R., Escobar P.G., Dowdy K.B., et al. Accelerated LV remodeling after myocardial infarction in TIMP-1-deficient mice: effects of exogenous MMP inhibition. Am J Physiol Heart Circ Physiol 2005, 288:H149-H158.
14. Creemers E.E.J.M., Davis J.N., Parkhurst A.M., Leenders P., Dowdy K.B., Hapke E., et al. Deficiency of TIMP-1 exacerbates LV remodeling after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 2003, 284:H364-H371.
15. Roten L., Nemoto S., Simsic J., Coker M.L., Rao V., Baicu S., et al. Effects of gene deletion of the tissue inhibitor of the matrix metalloproteinase-type 1 (TIMP-1) on left ventricular geometry and function in mice. J Mol Cell Cardiol 2000, 32:109-120.
16. Angoulvant D., Fazel S., Weisel R.D., Lai T.Y.Y., Fedak P.W., Chen L., et al. Cell-based gene therapy modifies matrix remodeling after a myocardial infarction in tissue inhibitor of matrix metalloproteinase-3-deficient mice. J Thorac Cardiovasc Surg 2009, 137:471-480.
17. Angoulvant D., Ivanes F., Ferrera R., Matthews P.G., Nataf S., Ovize M. Mesenchymal stem cell conditioned media attenuates in vitro and ex vivo myocardial reperfusion injury. J Heart Lung Transplant 2011, 30:95-102.
18. Gomez L., Paillard M., Thibault H., Derumeaux G., Ovize M. Inhibition of GSK3beta by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion. Circulation 2008, 117:2761-2768.
19. Vivaldi M.T., Kloner R.A., Schoen F.J. Triphenyltetrazolium staining of irreversible ischemic injury following coronary artery occlusion in rats. Am J Pathol 1985, 121:522-530.
20. Ovize M., Kloner R.A., Przyklenk K. Stretch preconditions canine myocardium. Am J Physiol 1994, 266:H137-H146.
21. Jung K.-K., Liu X.-W., Chirco R., Fridman R., Kim H.-R.C. Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. EMBO J 2006, 25:3934-3942.
22. Toricelli M., Melo F.H., Peres G.B., Silva D.C., Jasiulionis M.G. Timp1 interacts with beta-1 integrin and CD63 along melanoma genesis and confers anoikis resistance by activating PI3-K signaling pathway independently of Akt phosphorylation. Mol Cancer 2013, 12:22.
23. Kawaguchi M., Takahashi M., Hata T., Kashima Y., Usui F., Morimoto H., et al. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation 2011, 123:594-604.
24. Fidelis-de-Oliveira P., Werneck-de-Castro J.P.S., Pinho-Ribeiro V., Shalom B.C.M., Nascimento-Silva J.H., Costa e Souza R.H., et al. Soluble factors from multipotent mesenchymal stromal cells have antinecrotic effect on cardiomyocytes in vitro and improve cardiac function in infarcted rat hearts. Cell Transplant 2012, 21:1011-1021.
25. Timmers L., Lim S.K., Arslan F., Armstrong J.S., Hoefer I.E., Doevendans P.A., et al. Reduction of myocardial infarct size by human mesenchymal stem cell conditioned medium. Stem Cell Res 2008, 1:129-137.
26. Chanyshev B., Shainberg A., Isak A., Chepurko Y., Porat E., Hochhauser E. Conditioned medium from hypoxic cells protects cardiomyocytes against ischemia. Mol Cell Biochem 2012, 363:167-178.
27. Frangogiannis N.G., Smith C.W., Entman M.L. The inflammatory response in myocardial infarction. Cardiovasc Res 2002, 53:31-47.
28. Frangogiannis N.G. The immune system and cardiac repair. Pharmacol Res 2008, 58:88-111.
29. Lindsey M.L. MMP induction and inhibition in myocardial infarction. Heart Fail Rev 2004, 9:7-19.
30. Jayasankar V. Inhibition of matrix metalloproteinase activity by TIMP-1 gene transfer effectively treats ischemic cardiomyopathy. Circulation 2004, 110:II-180-II-186.
31. Singla D.K., McDonald D.E. Factors released from embryonic stem cells inhibit apoptosis of H9c2 cells. Am J Physiol Heart Circ Physiol 2007, 293:H1590-H1595.
32. Chirco R., Liu X.-W., Jung K.-K., Kim H.-R.C. Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev 2006, 25:99-113.
33. Akahane T., Akahane M., Shah A., Thorgeirsson U.P. TIMP-1 stimulates proliferation of human aortic smooth muscle cells and Ras effector pathways. Biochem Biophys Res Commun 2004, 324:440-445.
34. Guedez L., Stetler-Stevenson W.G. In vitro suppression of programmed cell death of B cells by tissue inhibitor of metalloproteinases-1. J Clin Invest 1998, 102:1-9.
35. Hayakawa T., Yamashita K., Tanzawa K., Uchijima E., Iwata K. Growth-promoting activity of tissue inhibitor of metalloproteinases-1 (TIMP-1) for a wide range of cells. A possible new growth factor in serum. FEBS Lett 1992, 298:29-32.
36. Lambert E., Bridoux L., Devy J., Dassé E., Sowa M.-L., Duca L., et al. TIMP-1 binding to proMMP-9/CD44 complex localized at the cell surface promotes erythroid cell survival. Int J Biochem Cell Biol 2009, 41:1102-1115.
37. Tsang A., Hausenloy D.J., Mocanu M.M., Yellon D.M. Postconditioning: a form of "modified reperfusion" protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway. Circ Res 2004, 95:230-232.
38. Sivaraman V., Mudalagiri N.R., Di Salvo C., Kolvekar S., Hayward M., Yap J., et al. Postconditioning protects human atrial muscle through the activation of the RISK pathway. Basic Res Cardiol 2007, 102:453-459.
39. Kadri Z., Petitfrère E., Boudot C., Freyssinier J.M., Fichelson S., Mayeux P., et al. Erythropoietin induction of tissue inhibitors of metalloproteinase-1 expression and secretion is mediated by mitogen-activated protein kinase and phosphatidylinositol 3-kinase pathways. Cell Growth Differ 2000, 11:573-580.
40. Lambert E., Boudot C., Kadri Z., Soula-Rothhut M., Sowa M.-L., Mayeux P., et al. Tissue inhibitor of metalloproteinases-1 signalling pathway leading to erythroid cell survival. Biochem J 2003, 372:767-774.
41. Haviernik P., Lahoda C., Bradley H.L., Hawley T.S., Ramezani A., Hawley R.G., et al. Tissue inhibitor of matrix metalloproteinase-1 overexpression in M1 myeloblasts impairs IL-6-induced differentiation. Oncogene 2004, 23:9212-9219.
42. Lalu M.M., Pasini E., Schulze C.J., Ferrari-Vivaldi M., Ferrari-Vivaldi G., Bachetti T., et al. Ischaemia-reperfusion injury activates matrix metalloproteinases in the human heart. Eur Heart J 2005, 26:27-35.
43. Vanhoutte D., Schellings M., Pinto Y., Heymans S. Relevance of matrix metalloproteinases and their inhibitors after myocardial infarction: a temporal and spatial window. Cardiovasc Res 2006, 69:604-613.
44. Bencsik P., Kupai K., Giricz Z., Görbe A., Pipis J., Murlasits Z., et al. Role of iNOS and peroxynitrite-matrix metalloproteinase-2 signaling in myocardial late preconditioning in rats. Am J Physiol Heart Circ Physiol 2010, 299:H512-H518.
45. Wang Z.-F., Wang N.-P., Harmouche S., Philip T., Pang X.-F., Bai F., et al. Postconditioning promotes the cardiac repair through balancing collagen degradation and synthesis after myocardial infarction in rats. Basic Res Cardiol 2013, 108:318.
46. Lalu M.M., Csonka C., Giricz Z., Csont T., Schulz R., Ferdinandy P. Preconditioning decreases ischemia/reperfusion-induced release and activation of matrix metalloproteinase-2. Biochem Biophys Res Commun 2002, 296:937-941.