Myoblasts and embryonic stem cells differentially engraft in a mouse model of genetic dilated cardiomyopathy

Molecular Therapy

Volumn 21, Issue 5, 2013, Pages 1064-1075

  Catelain, Cyril ^a   Riveron, Stéphanie ^a   Papadopoulos, Aurélie ^a   Mougenot, Nathalie ^a,b   Jacquet, Adeline ^a,b   Vauchez, Karine ^a   Yada, Erica ^a   Pucéat, Michel ^b   Fiszman, Marc ^a   Butler Browne, Gillian ^a   Bonne, Gisèle ^a   Vilquin, Jean Thomas ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CARDIOVASCULAR PARAMETERS; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CONFERENCE PAPER; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE COURSE; EMBRYONIC STEM CELL; ENGRAFTMENT; GENETIC DISORDER; LAMINOPATHY; LEFT VENTRICULAR FRACTIONAL SHORTENING; MALE; MOUSE; MYOBLAST; NONHUMAN; SCAR; TERATOMA; THERAPY EFFECT;

ANIMALIA; MUS;

EID: 84877030605     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.15     Document Type: Conference Paper

References (52)

1. Durrani, S, Konoplyannikov, M, Ashraf, M and Haider, KH (2010). Skeletal myoblasts for cardiac repair. Regen Med 5: 919-932.
2. Okada, M, Payne, TR, Drowley, L, Jankowski, RJ, Momoi, N, Beckman, S et al. (2012). Human skeletal muscle cells with a slow adhesion rate after isolation and an enhanced stress resistance improve function of ischemic hearts. Mol Ther 20: 138-145.
3. Léobon, B, Roncalli, J, Joffre, C, Mazo, M, Boisson, M, Barreau, C et al. (2009). Adipose-derived cardiomyogenic cells: in vitro expansion and functional improvement in a mouse model of myocardial infarction. Cardiovasc Res 83: 757-767.
4. Ghodsizad, A, Niehaus, M, Kögler, G, Martin, U, Wernet, P, Bara, C et al. (2009). Transplanted human cord blood-derived unrestricted somatic stem cells improve leftventricular function and prevent left-ventricular dilation and scar formation after acute myocardial infarction. Heart 95: 27-35.
5. Ohnishi, S, Yanagawa, B, Tanaka, K, Miyahara, Y, Obata, H, Kataoka, M et al. (2007). Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis. J Mol Cell Cardiol 42: 88-97.
6. Bolli, R, Chugh, AR, D'Amario, D, Loughran, JH, Stoddard, MF, Ikram, S et al. (2011). Cardiac stem cells in patients with ischaemic cardiomyopathy (SCIPIO): initial results of a randomised phase 1 trial. Lancet 378: 1847-1857.
7. Liu, J, Zhang, Z, Liu, Y, Guo, C, Gong, Y, Yang, S et al. (2012). Generation, characterization, and potential therapeutic applications of cardiomyocytes from various stem cells. Stem Cells Dev 21: 2095-2110.
8. Menasché, P (2012). Embryonic stem cells for severe heart failure: why and how J Cardiovasc Transl Res 5: 555-565.
9. Perez-Ilzarbe, M, Agbulut, O, Pelacho, B, Ciorba, C, San Jose-Eneriz, E, Desnos, M et al. (2008). Characterization of the paracrine effects of human skeletal myoblasts transplanted in infarcted myocardium. Eur J Heart Fail 10: 1065-1072.
10. den Haan, MC, Grauss, RW, Smits, AM, Winter, EM, van Tuyn, J, Pijnappels, DA et al. (2012). Cardiomyogenic differentiation-independent improvement of cardiac function by human cardiomyocyte progenitor cell injection in ischaemic mouse hearts. J Cell Mol Med 16: 1508-1521.
11. Ebelt, H, Jungblut, M, Zhang, Y, Kubin, T, Kostin, S, Technau, A et al. (2007). Cellular cardiomyoplasty: improvement of left ventricular function correlates with the release of cardioactive cytokines. Stem Cells 25: 236-244.
12. Menasché, P, Alfieri, O, Janssens, S, McKenna, W, Reichenspurner, H, Trinquart, L et al. (2008). The Myoblast Autologous Grafting in Ischemic Cardiomyopathy (MAGIC) trial: first randomized placebo-controlled study of myoblast transplantation. Circulation 117: 1189-1200.
13. Jiang, M, He, B, Zhang, Q, Ge, H, Zang, MH, Han, ZH et al. (2010). Randomized controlled trials on the therapeutic effects of adult progenitor cells for myocardial infarction: meta-analysis. Expert Opin Biol Ther 10: 667-680.
14. Ohno, N, Fedak, PW, Weisel, RD, Mickle, DA, Fujii, T and Li, RK (2003). Transplantation of cryopreserved muscle cells in dilated cardiomyopathy: effects on left ventricular geometry and function. J Thorac Cardiovasc Surg 126: 1537-1548.
15. Pouly, J, Hagège, AA, Vilquin, JT, Bissery, A, Rouche, A, Bruneval, P et al. (2004). Does the functional efficacy of skeletal myoblast transplantation extend to nonischemic cardiomyopathy Circulation 110: 1626-1631.
16. Yoo, KJ, Li, RK, Weisel, RD, Mickle, DA, Tomita, S, Ohno, N et al. (2002). Smooth muscle cells transplantation is better than heart cells transplantation for improvement of heart function in dilated cardiomyopathy. Yonsei Med J 43: 296-303.
17. Chen, M, Fan, ZC, Liu, XJ, Deng, JL, Zhang, L, Rao, L et al. (2006). Effects of autologous stem cell transplantation on ventricular electrophysiology in doxorubicininduced heart failure. Cell Biol Int 30: 576-582.
18. Guarita-Souza, LC, Francisco, JC, Simeoni, R, Faria-Neto, JR and de Carvalho, KA (2011). Benefit of stem cells and skeletal myoblast cells in dilated cardiomyopathies. World J Cardiol 3: 93-97.
19. Ishida, M, Tomita, S, Nakatani, T, Fukuhara, S, Hamamoto, M, Nagaya, N et al. (2004). Bone marrow mononuclear cell transplantation had beneficial effects on doxorubicin-induced cardiomyopathy. J Heart Lung Transplant 23: 436-445.
20. Laflamme, MA, Gold, J, Xu, C, Hassanipour, M, Rosler, E, Police, S et al. (2005). Formation of human myocardium in the rat heart from human embryonic stem cells. Am J Pathol 167: 663-671.
21. Singla, DK, Hacker, TA, Ma, L, Douglas, PS, Sullivan, R, Lyons, GE et al. (2006). Transplantation of embryonic stem cells into the infarcted mouse heart: formation of multiple cell types. J Mol Cell Cardiol 40: 195-200.
22. Blin, G, Nury, D, Stefanovic, S, Neri, T, Guillevic, O, Brinon, B et al. (2010). A purified population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates. J Clin Invest 120: 1125-1139.
23. Behfar, A, Zingman, LV, Hodgson, DM, Rauzier, JM, Kane, GC, Terzic, A et al. (2002). Stem cell differentiation requires a paracrine pathway in the heart. FASEB J 16: 1558-1566.
24. Behfar, A, Perez-Terzic, C, Faustino, RS, Arrell, DK, Hodgson, DM, Yamada, S et al. (2007). Cardiopoietic programming of embryonic stem cells for tumor-free heart repair. J Exp Med 204: 405-420.
25. Ménard, C, Hagège, AA, Agbulut, O, Barro, M, Morichetti, MC, Brasselet, C et al. (2005). Transplantation of cardiac-committed mouse embryonic stem cells to infarcted sheep myocardium: a preclinical study. Lancet 366: 1005-1012.
26. Laflamme, MA, Chen, KY, Naumova, AV, Muskheli, V, Fugate, JA, Dupras, SK et al. (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024.
27. Nussbaum, J, Minami, E, Laflamme, MA, Virag, JA, Ware, CB, Masino, A et al. (2007). Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J 21: 1345-1357.
28. Arimura, T, Helbling-Leclerc, A, Massart, C, Varnous, S, Niel, F, Lacène, E et al. (2005). Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet 14: 155-169.
29. Pucéat, M (2008). Protocols for cardiac differentiation of embryonic stem cells. Methods 45: 168-171.
30. Pucéat, M (2007). TGFbeta in the differentiation of embryonic stem cells. Cardiovasc Res 74: 256-261.
31. Yaffe, D and Saxel, O (1977). Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727.
32. Vilquin, JT, Guérette, B, Puymirat, J, Yaffe, D, Tomé, FM, Fardeau, M et al. (1999). Myoblast transplantations lead to the expression of the laminin alpha 2 chain in normal and dystrophic (dy/dy) mouse muscles. Gene Ther 6: 792-800.
33. Simpson, EM, Linder, CC, Sargent, EE, Davisson, MT, Mobraaten, LE and Sharp, JJ (1997). Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat Genet 16: 19-27.
34. Swijnenburg, RJ, Schrepfer, S, Cao, F, Pearl, JI, Xie, X, Connolly, AJ et al. (2008). In vivo imaging of embryonic stem cells reveals patterns of survival and immune rejection following transplantation. Stem Cells Dev 17: 1023-1029.
35. Huard, J, Roy, R, Guérette, B, Verreault, S, Tremblay, G and Tremblay, JP (1994). Human myoblast transplantation in immunodeficient and immunosuppressed mice: evidence of rejection. Muscle Nerve 17: 224-234.
36. Kinoshita, I, Vilquin, JT, Guérette, B, Asselin, I, Roy, R and Tremblay, JP (1994). Very efficient myoblast allotransplantation in mice under FK506 immunosuppression. Muscle Nerve 17: 1407-1415.
37. Baldwin, KM and Haddad, F (2001). Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90: 345-357.
38. Tezuka, A, Kawada, T, Nakazawa, M, Masui, F, Konno, S, Nitta, S et al. (2008). Which skeletal myoblasts and how to be transplanted for cardiac repair Biochem Biophys Res Commun 369: 270-276.
39. Charron, P, Arad, M, Arbustini, E, Basso, C, Bilinska, Z, Elliott, P et al.; European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. (2010). Genetic counselling and testing in cardiomyopathies: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 31: 2715-2726.
40. Wu, DC, Boyd, AS and Wood, KJ (2008). Embryonic stem cells and their differentiated derivatives have a fragile immune privilege but still represent novel targets of immune attack. Stem Cells 26: 1939-1950.
41. Suzuki, K, Murtuza, B, Suzuki, N, Smolenski, RT and Yacoub, MH (2001). Intracoronary infusion of skeletal myoblasts improves cardiac function in doxorubicininduced heart failure. Circulation 104: I213-217.
42. Kirillov, AM, Fatkhudinov, TKh, Dyachkov, AV, Koroteev, AV, Goldshtein, DV and Bochkov, NP (2007). Transplantation of allogenic cells in the therapy of patients with dilated cardiomyopathy. Bull Exp Biol Med 144: 635-639.
43. Leobon, B, Garcin, I, Menasche, P, Vilquin, JT, Audinat, E and Charpak, S (2003). Myoblasts transplanted into rat infarcted myocardium are functionally isolated from their host. Proc Natl Acad Sci USA 100: 7808-7811.
44. Hagège, AA, Carrion, C, Menasché, P, Vilquin, JT, Duboc, D, Marolleau, JP et al. (2003). Viability and differentiation of autologous skeletal myoblast grafts in ischaemic cardiomyopathy. Lancet 361: 491-492.
45. Chuva de Sousa Lopes, SM, Feijen, A, Korving, J, Korchynskyi, O, Larsson, J, Karlsson S et al. (2004). Connective tissue growth factor expression and Smad signaling during mouse heart development and myocardial infarction. Dev Dyn 231: 542-550.
46. Zhao, T, Zhao, W, Chen, Y, Ahokas, RA and Sun, Y (2011). Acidic and basic fibroblast growth factors involved in cardiac angiogenesis following infarction. Int J Cardiol 152: 307-313.
47. Baba, S, Heike, T, Yoshimoto, M, Umeda, K, Doi, H, Iwasa, T et al. (2007). Flk1(+) cardiac stem/progenitor cells derived from embryonic stem cells improve cardiac function in a dilated cardiomyopathy mouse model. Cardiovasc Res 76: 119-131.
48. Yamada, S, Nelson, TJ, Crespo-Diaz, RJ, Perez-Terzic, C, Liu, XK, Miki, T et al. (2008). Embryonic stem cell therapy of heart failure in genetic cardiomyopathy. Stem Cells 26: 2644-2653.
49. Zlatkovic-Lindor, J, Arrell, DK, Yamada, S, Nelson, TJ and Terzic, A (2010). ATPsensitive K(+) channel-deficient dilated cardiomyopathy proteome remodeled by embryonic stem cell therapy. Stem Cells 28: 1355-1367.
50. Qu, Z, Balkir, L, van Deutekom, JC, Robbins, PD, Pruchnic, R and Huard, J (1998). Development of approaches to improve cell survival in myoblast transfer therapy. J Cell Biol 142: 1257-1267.
51. Habib, M, Shapira-Schweitzer, K, Caspi, O, Gepstein, A, Arbel, G, Aronson, D et al. (2011). A combined cell therapy and in-situ tissue-engineering approach for myocardial repair. Biomaterials 32: 7514-7523.
52. Hata, H, Matsumiya, G, Miyagawa, S, Kondoh, H, Kawaguchi, N, Matsuura, N et al. (2006). Grafted skeletal myoblast sheets attenuate myocardial remodeling in pacinginduced canine heart failure model. J Thorac Cardiovasc Surg 132: 918-924.