Soluble factors from multipotent mesenchymal stromal cells have antinecrotic effect on cardiomyocytes in vitro and improve cardiac function in infarcted rat hearts

Cell Transplantation

Volumn 21, Issue 5, 2012, Pages 1011-1021

  Fidelis de Oliveira, P ^a,b   Werneck de Castro, J P S ^a   Pinho Ribeiro, V ^a   Shalom, B C M ^a   Nascimento Silva, J H ^a   Costa e Souza, R H ^a   Cruz, I S ^a   Rangel, R R ^a   Goldenberg, R C S ^a   Campos de Carvalho, A C ^a,c  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF UBERLÂNDIA   (Brazil)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis necrosis; Conditioned medium; Multipotent mesenchymal stromal cells (MSCs); Myocardial infarction; Paracrine effect

Indexed keywords

ANGIOPOIETIN 1; FIBROBLAST GROWTH FACTOR; INTERLEUKIN 1; INTERLEUKIN 6; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; VASCULOTROPIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANTINECROSIS EFFECT; APOPTOSIS; ARTICLE; CYTOKINE RELEASE; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAM; HEART CATHETERIZATION; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE; HEART MUSCLE CELL; HEART PROTECTION; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STROMA CELL; MULTIPOTENT STEM CELL; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; RAT; TREADMILL EXERCISE;

ANIMALS; APOPTOSIS; CELL HYPOXIA; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; CULTURE MEDIA, SERUM-FREE; ECHOCARDIOGRAPHY; HEART; MALE; MESENCHYMAL STROMAL CELLS; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; RATS; RATS, WISTAR; VENTRICULAR FUNCTION, LEFT;

EID: 84862550765     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X623916     Document Type: Article

References (59)

1. Abbate, A.; Biondi-Zoccai, G. G. L.; Baldi, A. Pathophysiologic role of myocardial apoptosis in post-infarction left ventricular remodeling. J. Cell. Physiol. 193:145-153; 2002.
2. Alvarez-Dolado, M.; Pardal, R.; Garcia-Verdugo, J. M.; Fike, J. R.; Lee, H. O.; Pfeffer, K.; Lois, C.; Morrison, S. J.; Alvarez-Buylla, A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968-973; 2003.
3. Amado, L. C.; Saliaris, A. P.; Schuleri, K. H.; John, M. S.; Xie, J.-S.; Cattaneo, S.; Durand, D. J.; Fitton, T.; Kuang, J. Q.; Stewart, G.; Lehrke, S.; Baumgartner, W. W.; Martin, B. J.; Heldman, A. W.; Hare, J. M. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc. Natl. Acad. Sci. USA 102:11474-11479; 2005.
4. Beltrami, A. P.; Barlucchi, L.; Torella, D.; Baker, M.; Limana, F.; Chimenti, S.; Kasahara, H.; Rota, M.; Musso, E.; Urbanek, K.; Leri, A.; Kajstura, J.; Nadal-Ginard, B.; Anversa, P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763-776; 2003.
5. Berry, M. F.; Engler, A. J.; Woo, Y. J.; Pirolli, T. J.; Bish, L. T.; Jayasankar, V.; Morine, K. J.; Gardner, T. J.; Discher, D. E.; Sweeney, H. L. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol. 290: H2196-H2203; 2006.
6. Biondi-Zoccai, G. G. L.; Abbate, A.; Vasaturo, F.; Scarpa, S.; Santini, D.; Leone, A. M.; Parisi, Q.; Giorgio, F. D.; Bussani, R.; Silvestri, F.; Baldi, F.; Biasucci, L. M.; Baldi, A. Increased apoptosis in remote non-infarcted myocardium in multivessel coronary disease. Int. J. Cardiol. 94: 105-110; 2004.
7. Boomsma, R. A.; Swaminathan, P. D.; Geenen, D. L. Intravenously injected mesenchymal stem cells home to viable myocardium after coronary occlusion and preserve systolic function without altering infarct size. Int. J. Cardiol. 122:17-28; 2007.
8. Borlongan, C. V.; Hadman, M.; Sanberg, C. D.; Sanberg, P. R. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke 35:2385-2389; 2004.
9. Caplan, A. I. Mesenchymal stem cells. J. Orthop. Res. 9: 641-650; 1991.
10. Carvalho, A. B.; Quintanilha, L. F.; Dias, J. V.; Paredes, B. D.; Mannheimer, E. G.; Carvalho, F. G.; Asensi, K. D.; Gutfilen, B.; Fonseca, L. M. B.; Resende, C. M. C.; Rezende, G. F. M.; Takiya, C. M.; Campos-de-Carvalho, A. C.; Goldenberg, R. C. S. Bone marrow multipotent mesenchymal stromal cells do not reduce fibrosis or improve function in a rat model of severe chronic liver injury. Stem Cells 26:1307-1314; 2008.
11. Cheng, W.; Kajstura, J.; Nitahara, J. A.; Li, B.; Reiss, K.; Liu, Y.; Clark, W. A.; Krajewski, S.; Reed, J. C.; Olivetti, G.; Anversa, P. Programmed myocyte cell death affects the viable myocardium after infarction in rats. Exp. Cell Res. 226:316-327; 1996.
12. Friedenstein, A. J.; Chailakhyan, R. K.; Latsinik, N. V.; Panasyuk, A. F.; Keiliss-Borok, I. V. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17:331-340; 1974.
13. Gnecchi, M.; He, H.; Liang, O. D.; Melo, L. G.; Morello, F.; Mu, H.; Noiseux, N.; Zhang, L.; Pratt, R. E.; Ingwall, J. S.; Dzau, V. J. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11:367-368; 2005.
14. Hatzistergos, K. E.; Quevedo, H.; Oskouei, B. N.; Hu, Q.; Feigenbaum, G. S.; Margitich, I. S.; Mazhari, R.; Boyle, A. J.; Zambrano, J. P.; Rodriguez, J. E.; Dulce, R.; Pattany, P. M.; Valdes, D.; Revilla, C.; Heldman, A. W.; McNiece, I.; Hare, J. M. Bone marrow mesenchymal stem cells stimulate cardiac stem cell proliferation and differentiation. Circ. Res. 107:913-922; 2010.
15. Horwitz, E. M.; Blanc, K. L.; Dominici, M.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F. C.; Deans, R. J.; Krause, D. S.; Keating, A. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 7:393-395; 2005.
16. Hou, M.; Yang, K.-M.; Zhang, H.; Zhu, W.-Q.; Duan, F.-J.; Wang, H.; Song, Y.-H.; Wei, Y.-J.; Hu, S.-S. Transplantation of mesenchymal stem cells from human bone marrow improves damaged heart function in rats. Int. J. Cardiol. 115:220-228; 2007.
17. Hung, S.-C.; Chen, N.-J.; Hsieh, S.-L.; Li, H.; Ma, H.-L.; Lo, W.-H. Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells 20:249-258; 2002.
18. Jayasankar, V.; Woo, Y. J.; Pirolli, T. J.; Bish, L. T.; Berry, M. F.; Burdick, J.; Gardner, T. J.; Sweeney, H. L. Induction of angiogenesis and inhibition of apoptosis by hepatocyte growth factor effectively treats postischemic heart failure. J. Card. Surg. 20:93-101; 2005.
19. Jiang, L.; Huang, Y.; Hunyor, S.; dos Remedios, C. G. Cardiomyocyte apoptosis is associated with increased wall stress in chronic failing left ventricle. Eur. Heart J. 24: 742-751; 2003.
20. Kajstura, J.; Liu, Y.; Baldini, A.; Li, B.; Olivetti, G.; Leri, A.; Anversa, P. Coronary artery constriction in rats: Necrotic and apoptotic myocyte death. Am. J. Cardiol. 82: 30K-41K; 1998.
21. Kawada, H.; Fujita, J.; Kinjo, K.; Matsuzaki, Y.; Tsuma, M.; Miyatake, H.; Muguruma, Y.; Tsuboi, K.; Itabashi, Y.; Ikeda, Y.; Ogawa, S.; Okano, H.; Hotta, T.; Ando, K.; Fukuda, K. Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood 104:3581-3587; 2004.
22. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein, S. E. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ. Res. 94:678-685; 2004.
23. Kinnaird, T.; Stabile, E.; Burnett, M. S.; Shou, M.; Lee, C. W.; Barr, S.; Fuchs, S.; Epstein, S. E. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109: 1543-1549; 2004.
24. Makino, S.; Fukuda, K.; Miyoshi, S.; Konishi, F.; Kodama, H.; Pan, J.; Sano, M.; Takahashi, T.; Hori, S.; Abe, H.; Hata, J.; Umezawa, A.; Ogawa, S. Cardiomyocytes can be generated from marrow stromal cells in vitro. J. Clin. Invest. 103:697-705; 1999.
25. Mangi, A. A.; Noiseux, N.; Kong, D.; He, H.; Rezvani, M.; Ingwall, J. S.; Dzau, V. J. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9:1195-1201; 2003.
26. Melo, L. G.; Agrawal, R.; Zhang, L.; Rezvani, M.; Mangi, A. A.; Ehsan, A.; Griese, D. P.; Dell'Acqua, G.; Mann, M. J.; Oyama, J.; Yet, S.-F.; Layne, M. D.; Perrella, M. A.; Dzau, V. J. Gene therapy strategy for long-term myocardial protection using adeno-associated virus-mediated delivery of heme oxygenase gene. Circulation 105:602-607; 2002.
27. Miranda, A.; Costa-e-Sousa, R. H.; Werneck-de-Castro, J. P. S.; Mattos, E. C.; Olivares, E. L.; Ribeiro, V. P.; Silva, M. G.; Goldenberg, R. C. S.; Campos-de-Carvalho, A. C. Time course of echocardiographic and electrocardiographic parameters in myocardial infarct in rats. An. Acad. Bras. Cienc. 79:639-648; 2007.
28. Misao, J.; Hayakawa, Y.; Ohno, M.; Kato, S.; Fujiwara, T.; Fujiwara, H. Expression of bcl-2 protein, an inhibitor of apoptosis, and Bax, an accelerator of apoptosis, in ventricular myocytes of human hearts with myocardial infarction. Circulation 94:1506-1512; 1996.
29. Monceau, V.; Belikova, Y.; Kratassiouk, G.; Robidel, E.; Russo-Marie, F.; Charlemagne, D. Myocyte apoptosis during acute myocardial infarction in rats is related to early sarcolemmal translocation of annexin A5 in border zone. Am. J. Physiol. Heart Circ. 291:H965-H971; 2006.
30. Nagaya, N.; Fujii, T.; Iwase, T.; Ohgushi, H.; Itoh, T.; Uematsu, M.; Yamagishi, M.; Mori, H.; Kangawa, K.; Kitamura, S. Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am. J. Physiol. Heart Circ. Physiol. 287:H2670-H2676; 2004.
31. Nalivaiko, E.; Antunes, V. R.; Paton, J. F. R. Control of cardiac contractility in the rat working heart-brainstem preparation. Exp. Physiol. 95:107-119; 2010.
32. Napoli, P. D.; Taccardi, A. A.; Grilli, A.; Felaco, M.; Balbone, A.; Angelucci, D.; Gallina, S.; Calafiore, A. M.; Caterina, R. D.; Barsotti, A. Left ventricular wall stress as a direct correlate of cardiomyocyte apoptosis in patients with severe dilated cardiomyopathy. Am. Heart J. 146: 1105-1111; 2003.
33. Ohnishi, S.; Sumiyoshi, H.; Kitamura, S.; Nagaya, N. Mesenchymal stem cells attenuate cardiac fibroblast proliferation and collagen synthesis through paracrine actions. FEBS Lett. 581:3961-3966; 2007.
34. Olivares, E. L.; Ribeiro, V. P.; Werneck-de-Castro, J. P. S.; Ribeiro, K. C.; Mattos, E. C.; Goldenberg, R. C. S.; Mill, J. G.; Dohmann, H. F.; dos Santos, R. R.; Campos-de-Carvalho, A. C.; Masuda, M. O. Bone marrow stromal cells improve cardiac performance in healed infarcted rat hearts. Am. J. Physiol. Heart Circ. Physiol. 287:H464-H470; 2004.
35. Olivetti, G.; Quaini, F.; Sala, R.; Lagrasta, C.; Corradi, D.; Bonacina, E.; Gambert, S. R.; Cigola, E.; Anversa, P. Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J. Mol. Cell. Cardiol. 28: 2005-2016; 1996.
36. Pak, H.-N.; Qayyum, M.; Kim, D. T.; Hamabe, A.; Miyauchi, Y.; Lill, M. C.; Frantzen, M.; Takizawa, K.; Chen, L. S.; Fishbein, M. C.; Sharifi, B. G.; Chen, P.-S.; Makkar, R. Mesenchymal stem cell injection induces cardiac nerve sprouting and increased tenascin expression in a Swine model of myocardial infarction. J. Cardiovasc. Electrophysiol. 14:841-848; 2003.
37. Palojoki, E.; Saraste, A.; Eriksson, A.; Pulkki, K.; Kallajoki, M.; Voipio-Pulkki, L. M.; Tikkanen, I. Cardiomyocyte apoptosis and ventricular remodeling after myocardial infarction in rats. Am. J. Physiol. Heart Circ. Physiol. 280: H2726-H2731; 2001.
38. Park, H.-J.; Bang, G.; Lee, B. R.; Kim, H. O.; Lee, P. H. Neuroprotective effect of human mesenchymal stem cells in an animal model of double toxin-induced multiple system atrophy-parkinsonism. Cell Transplant. 20:827-835; 2011.
39. Pittenger, M. F.; Mackay, A. M.; Beck, S. C.; Jaiswal, R. K.; Douglas, R.; Mosca, J. D.; Moorman, M. A.; Simonetti, D. W.; Craig, S.; Marshak, D. R. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147; 1999.
40. Reis, R. A. M.; da Silva, M. C. C.; dos Santos, N. E. L.; Bampton, E.; Taylor, J. S. H.; de Mello, F. G.; Linden, R. Sympathetic neuronal survival induced by retinal trophic factors. J. Neurobiol. 50:13-23; 2002.
41. Santos, P. E.; Masuda, M. O. The electrocardiogram of rats with an old extensive myocardial infarction. Braz. J. Med. Biol. Res. 24:1173-1177; 1991.
42. Saraste, A.; Pulkki, K.; Kallajoki, M.; Henriksen, K.; Parvinen, M.; Voipio-Pulkki, L. M. Apoptosis in human acute myocardial infarction. Circulation 95:320-323; 1997.
43. Schittini, A. V.; Celedon, P. F.; Stimamiglio, M. A.; Krieger, M.; Hansen, P.; da Costa, F. D.; Goldenberg, S.; Dallagiovanna, B.; Correa, A. Human cardiac explantconditioned medium: Soluble factors and cardiomyogenic effect on mesenchymal stem cells. Exp. Biol. Med. 235: 1015-1024; 2010.
44. Shabbir, A.; Zisa, D.; Suzuki, G.; Lee, T. Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: A noninvasive therapeutic regimen. Am. J. Physiol. Heart Circ. Physiol. 296:H1888-H1897; 2009.
45. Shake, J. G.; Gruber, P. J.; Baumgartner, W. A.; Senechal, G.; Meyers, J.; Redmond, J. M.; Pittenger, M. F.; Martin, B. J. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional. Ann. Thorac. Surg. 73:1919-1926; 2002.
46. Shalaby, A.; Rinne, T.; Jrvinen, O.; Saraste, A.; Laurikka, J.; Porkkala, H.; Saukko, P.; Tarkka, M. Initial results of a clinical study: adenosine enhanced cardioprotection and its effect on cardiomyocytes apoptosis during coronary artery bypass grafting. Eur. J. Cardiothorac. Surg. 33:639-644; 2008.
47. Suadicani, S. O.; Vink, M. J.; Spray, D. C. Slow intercellular Ca(2+) signaling in wild-type and Cx43-null neonatal mouse cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 279:H3076-H3088; 2000.
48. Taylor, D. G.; Parilak, L. D.; LeWinter, M. M.; Knot, H. J. Quantification of the rat left ventricle force and Ca2+-frequency relationships: Similarities to dog and human. Cardiovasc. Res. 61:77-86; 2004.
49. Terada, N.; Hamazaki, T.; Oka, M.; Hoki, M.; Mastalerz, D. M.; Nakano, Y.; Meyer, E. M.; Morel, L.; Petersen, B. E.; Scott, E. W. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416: 542-545; 2002.
50. Torres, C. A. A.; Varian, K. D.; Janssen, P. M. L. Variability in interbeat duration influences myocardial contractility in rat cardiac trabeculae. Open Cardiovasc. Med. J. 2:100-104; 2008.
51. Uemura, R.; Xu, M.; Ahmad, N.; Ashraf, M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ. Res. 98: 1414-1421; 2006.
52. Vermes, I.; Haanen, C.; Steffens-Nakken, H.; Reutelingsperger, C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 184:39-51; 1995.
53. Werneck-de-Castro, J. P. S.; Costa-e-Sousa, R. H. C.; Oliveira, P. F.; Pinho-Ribeiro, V.; Mello, D. B.; Peanha, R.; Mattos, E.; Olivares, E. L.; Maia, A. C. V.; Mill, J. G.; Goldenberg, R. C. D. S.; Campos-de-Carvalho, A. C. G-CSF does not improve systolic function in a rat model of acute myocardial infarction. Basic Res. Cardiol. 101: 494-501; 2006.
54. Westrich, J.; Yaeger, P.; He, C.; Stewart, J.; Chen, R.; Seleznik, G.; Larson, S.; Wentworth, B.; O'Callaghan, M.; Wadsworth, S.; Akita, G.; Molnar, G. Factors affecting residence time of mesenchymal stromal cells (MSC) injected into the myocardium. Cell Transplant. 19:937-948; 2010.
55. Xu, M.; Uemura, R.; Dai, Y.; Wang, Y.; Pasha, Z.; Ashraf, M. In vitro and in vivo effects of bone marrow stem cells on cardiac structure and function. J. Mol. Cell. Cardiol. 42:441-448; 2007.
56. Xu, R.-X.; Chen, X.; Chen, J.-H.; Han, Y.; Han, B.-M. Mesenchymal stem cells promote cardiomyocyte hypertrophy in vitro through hypoxia-induced paracrine mechanisms. Clin. Exp. Pharmacol. Physiol. 36:176-180; 2009.
57. Yew, T.-L.; Hung, Y.-T.; Li, H.-Y.; Chen, H.-W.; Chen, L.-L.; Tsai, K.-S.; Chiou, S.-H.; Chao, K.-C.; Huang, T.-F.; Chen, H.-L.; Hung, S.-C. Enhancement of wound healing by human multipotent stromal cell conditioned medium: The paracrine factors and p38MAPK activation. Cell Transplant. 20:693-706; 2011.
58. Yokokawa, M.; Ohnishi, S.; Ishibashi-Ueda, H.; Obata, H.; Otani, K.; Miyahara, Y.; Tanaka, K.; Shimizu, W.; Nakazawa, K.; Kangawa, K.; Kamakura, S.; Kitamura, S.; Nagaya, N. Transplantation of mesenchymal stem cells improves atrioventricular conduction in a rat model of complete atrioventricular block. Cell Transplant. 17: 1145-1155; 2008.
59. Zigova, T.; Song, S.; Willing, A. E.; Hudson, J. E.; Newman, M. B.; Saporta, S.; Sanchez-Ramos, J.; Sanberg, P. R. Human umbilical cord blood cells express neural antigens after transplantation into the developing rat brain. Cell Transplant. 11:265-274; 2002.