Comparison of human adipose-derived stem cells and bone marrow-derived stem cells in a myocardial infarction model

Cell Transplantation

Volumn 23, Issue 2, 2014, Pages 195-206

  Rasmussen, Jeppe Grøndahl ^a,b   Frøbert, Ole ^c   Holst Hansen, Claus ^d   Kastrup, Jens ^e   Baandrup, Ulrik ^b,f   Zachar, Vladimir ^b   Fink, Trine ^b   Simonsen, Ulf ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b AALBORG UNIVERSITY   (Denmark)

^c ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

^d AALBORG UNIVERSITY HOSPITAL   (Denmark)

^e University of Copenhagen   (Denmark)

^f NORTH DENMARK REGIONAL HOSPITAL   (Denmark)

Author keywords

Angiogenesis; Cell therapy; Left ventricular function; Myocardial infarction; Remodeling

Indexed keywords

5' NUCLEOTIDASE; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ENDOGLIN; MICROSOMAL AMINOPEPTIDASE; PHOSPHATE BUFFERED SALINE; THY 1 ANTIGEN;

ADIPOSE DERIVED STEM CELL; AGED; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL HYPOXIA; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPLASM; HEART FUNCTION; HEART INFARCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; HUMAN CELL; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADIPOSE TISSUE; ANIMALS; APOPTOSIS; BONE MARROW CELLS; ECHOCARDIOGRAPHY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; MALE; MESENCHYMAL STROMAL CELLS; MYOCARDIAL INFARCTION; RATS, SPRAGUE-DAWLEY; STEM CELLS;

EID: 84893324697     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X659871     Document Type: Article

References (45)

1. Adams, R. H.; Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell. Biol. 8(6):464-478; 2007.
2. Argaud, L.; Gateau-Roesch, O.; Muntean, D.; Chalabreysse, L.; Loufouat, J.; Robert, D.; Ovize, M. Specific inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury. J. Mol. Cell. Cardiol. 38(2):367-374; 2005.
3. Bartholomew, A.; Sturgeon, C.; Siatskas, M.; Ferrer, K.; McIntosh, K.; Patil, S.; Hardy, W.; Devine, S.; Ucker, D.; Deans, R.; Moseley, A.; Hoffman, R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30(1):42-48; 2002.
4. Brown, L.; Fenning, A.; Chan, V.; Loch, D.; Wilson, K.; Anderson, B.; Burstow, D. Echocardiographic assessment of cardiac structure and function in rats. Heart Lung Circ. 11(3):167-173; 2002.
5. Cai, L.; Johnstone, B. H.; Cook, T. G.; Tan, J.; Fishbein, M. C.; Chen, P. S.; March, K. L. IFATS collection: Human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. Stem Cells 27(1):230-237; 2009.
6. Djouad, F.; Plence, P.; Bony, C.; Tropel, P.; Apparailly, F.; Sany, J.; Noel, D.; Jorgensen, C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102(10):3837-3844; 2003.
7. Fan, M.; Chen, W.; Liu, W.; Du, G. Q.; Jiang, S. L.; Tian, W. C.; Sun, L.; Li, R. K.; Tian, H. The effect of age on the efficacy of human mesenchymal stem cell transplantation after a myocardial infarction. Rejuvenation Res. 13(4):429-438; 2010.
8. Fink, T.; Rasmussen, J. G.; Lund, P.; Pilgaard, L.; Soballe, K.; Zachar, V. Isolation and expansion of adipose-derived stem cells for tissue engineering. Front. Biosci. (Elite Ed.) 3:256-263; 2011.
9. Friis, T.; Haack-Sorensen, M.; Hansen, S. K.; Hansen, L.; Bindslev, L.; Kastrup, J. Comparison of mesenchymal stromal cells from young healthy donors and patients with severe chronic coronary artery disease. Scand. J. Clin. Lab. Invest. 71(3):193-202; 2011.
10. Friis, T.; Haack-Sorensen, M.; Mathiasen, A. B.; Ripa, R. S.; Kristoffersen, U. S.; Jorgensen, E.; Hansen, L.; Bindslev, L.; Kjaer, A.; Hesse, B.; Dickmeiss, E.; Kastrup, J. Mesenchymal stromal cell derived endothelial progenitor treatment in patients with refractory angina. Scand. Cardiovasc. J. 45(3):161-168; 2011.
11. 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(4):367-368; 2005.
12. Griffiths, E. J.; Halestrap, A. P. Protection by Cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J. Mol. Cell. Cardiol. 25(12):1461-1469; 1993.
13. Heeschen, C.; Lehmann, R.; Honold, J.; Assmus, B.; Aicher, A.; Walter, D. H.; Martin, H.; Zeiher, A. M.; Dimmeler, S. Profoundly reduced neovascularization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation 109(13):1615-1622; 2004.
14. Henning, R. J.; Shariff, M.; Eadula, U.; Alvarado, F.; Vasko, M.; Sanberg, P. R.; Sanberg, C. D.; Delostia, V. Human cord blood mononuclear cells decrease cytokines and inflammatory cells in acute myocardial infarction. Stem Cells Dev. 17(6):1207-1219; 2008.
15. 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(2):220-228; 2007.
16. Hu, X.; Yu, S. P.; Fraser, J. L.; Lu, Z.; Ogle, M. E.; Wang, J. A.; Wei, L. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J. Thorac. Cardiovasc. Surg. 135(4):799-808; 2008.
17. Hung, S. C.; Pochampally, R. R.; Hsu, S. C.; Sanchez, C.; Chen, S. C.; Spees, J.; Prockop, D. J. Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS One 2(5):e416; 2007.
18. Iwasaki, H.; Fukushima, K.; Kawamoto, A.; Umetani, K.; Oyamada, A.; Hayashi, S.; Matsumoto, T.; Ishikawa, M.; Shibata, T.; Nishimura, H.; Hirai, H.; Mifune, Y.; Horii, M.; Sugimura, K.; Suehiro, S.; Asahara, T. Synchrotron radiation coronary microangiography for morphometric and physiological evaluation of myocardial neovascularization induced by endothelial progenitor cell transplantation. Arterioscler. Thromb. Vasc. Biol. 27(6):1326-1333; 2007.
19. Janssens, S.; Dubois, C.; Bogaert, J.; Theunissen, K.; Deroose, C.; Desmet, W.; Kalantzi, M.; Herbots, L.; Sinnaeve, P.; Dens, J.; Maertens, J.; Rademakers, F.; Dymarkowski, S.; Gheysens, O.; Van Cleemput, J.; Bormans, G.; Nuyts, J.; Belmans, A.; Mortelmans, L.; Boogaerts, M.; Van de Werf, F. Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: Double-blind, randomised controlled trial. Lancet 367(9505): 113-121; 2006.
20. Kim, H. W.; Haider, H. K.; Jiang, S.; Ashraf, M. Ischemic preconditioning augments survival of stem cells via miR-210 expression by targeting caspase-8-associated protein 2. J. Biol. Chem. 284(48):33161-33168; 2009.
21. Kocher, A. A.; Schuster, M. D.; Szabolcs, M. J.; Takuma, S.; Burkhoff, D.; Wang, J.; Homma, S.; Edwards, N. M.; Itescu, S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat. Med. 7(4):430-436; 2001.
22. Mazo, M.; Planat-Benard, V.; Abizanda, G.; Pelacho, B.; Leobon, B.; Gavira, J. J.; Penuelas, I.; Cemborain, A.; Penicaud, L.; Laharrague, P.; Joffre, C.; Boisson, M.; Ecay, M.; Collantes, M.; Barba, J.; Casteilla, L.; Prosper, F. Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction. Eur. J. Heart Fail. 10(5):454-462; 2008.
23. Miyahara, Y.; Nagaya, N.; Kataoka, M.; Yanagawa, B.; Tanaka, K.; Hao, H.; Ishino, K.; Ishida, H.; Shimizu, T.; Kangawa, K.; Sano, S.; Okano, T.; Kitamura, S.; Mori, H. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 12(4):459-465; 2006.
24. Orlic, D.; Kajstura, J.; Chimenti, S.; Jakoniuk, I.; Anderson, S. M.; Li, B.; Pickel, J.; McKay, R.; Nadal-Ginard, B.; Bodine, D. M.; Leri, A.; Anversa, P. Bone marrow cells regenerate infarcted myocardium. Nature 410(6829):701-705; 2001.
25. Pilgaard, L.; Lund, P.; Rasmussen, J. G.; Fink, T.; Zachar, V. Comparative analysis of highly defined proteases for the isolation of adipose tissue-derived stem cells. Regen. Med. 3(5):705-715; 2008.
26. Rasmussen, J. G.; Frobert, O.; Pilgaard, L.; Kastrup, J.; Simonsen, U.; Zachar, V.; Fink, T. Prolonged hypoxic culture and trypsinization increase the pro-angiogenic potential of human adipose tissue-derived stem cells. Cytotherapy 13(3):318-328; 2011.
27. Rasmussen, J. G.; Riis, S. E.; Frøbert, O.; Yang, S.; Kastrup, J.; Zachar, V.; Simonsen, U.; Fink, T. Activation of protease-activated receptor 2 induces VEGF independently of HIF-1. PLos One 7(9):e46087; 2012.
28. Sadat, S.; Gehmert, S.; Song, Y. H.; Yen, Y.; Bai, X.; Gaiser, S.; Klein, H.; Alt, E. The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochem. Biophys. Res. Commun. 363(3):674-679; 2007.
29. Schachinger, V.; Erbs, S.; Elsasser, A.; Haberbosch, W.; Hambrecht, R.; Holschermann, H.; Yu, J.; Corti, R.; Mathey, D. G.; Hamm, C. W.; Suselbeck, T.; Assmus, B.; Tonn, T.; Dimmeler, S.; Zeiher, A. M.; REPAIR-AMI investigators. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N. Engl. J. Med. 355(12):1210-1221; 2006.
30. Shafy, A.; Fink, T.; Zachar, V.; Lila, N.; Carpentier, A.; Chachques, J. C. Development of cardiac support bioprostheses for ventricular restoration and myocardial regeneration. Eur. J. Cardiothorac. Surg. 43(6):1211-1219; 2013.
31. Simpson, D.; Liu, H.; Fan, T. H.; Nerem, R.; Dudley, Jr., S. C. A tissue engineering approach to progenitor cell delivery results in significant cell engraftment and improved myocardial remodeling. Stem Cells 25(9):2350-2357; 2007.
32. Song, S. W.; Chang, W.; Song, B. W.; Song, H.; Lim, S.; Kim, H. J.; Cha, M. J.; Choi, E.; Im, S. H.; Chang, B. C.; Chung, N.; Jang, Y.; Hwang, K. C. Integrin-linked kinase is required in hypoxic mesenchymal stem cells for strengthening cell adhesion to ischemic myocardium. Stem Cells 27(6):1358-1365; 2009.
33. Strem, B. M.; Zhu, M.; Alfonso, Z.; Daniels, E. J.; Schreiber, R.; Beygui, R.; MacLellan, W. R.; Hedrick, M. H.; Fraser, J. K. Expression of cardiomyocytic markers on adipose tissue-derived cells in a murine model of acute myocardial injury. Cytotherapy 7(3):282-291; 2005.
34. Strioga, M.; Viswanathan, S.; Darinskas, A.; Slaby, O.; Michalek, J. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev. 21(14):2724-2752; 2012.
35. Tang, Y. L.; Zhu, W.; Cheng, M.; Chen, L.; Zhang, J.; Sun, T.; Kishore, R.; Phillips, M. I.; Losordo, D. W.; Qin, G. Hypoxic preconditioning enhances the benefit of cardiac progenitor cell therapy for treatment of myocardial infarction by inducing CXCR4 expression. Circ. Res. 104(10):1209-1216; 2009.
36. Toma, C.; Pittenger, M. F.; Cahill, K. S.; Byrne, B. J.; Kessler, P. D. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105(1):93-98; 2002.
37. Tomita, S.; Li, R. K.; Weisel, R. D.; Mickle, D. A.; Kim, E. J.; Sakai, T.; Jia, Z. Q. Autologous transplantation of bone marrow cells improves damaged heart function. Circulation 100(19 Suppl):II247-256; 1999.
38. Tse, W. T.; Pendleton, J. D.; Beyer, W. M.; Egalka, M. C.; Guinan, E. C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: Implications in transplantation. Transplantation 75(3):389-397; 2003.
39. Tsuji, H.; Miyoshi, S.; Ikegami, Y.; Hida, N.; Asada, H.; Togashi, I.; Suzuki, J.; Satake, M.; Nakamizo, H.; Tanaka, M.; Mori, T.; Segawa, K.; Nishiyama, N.; Inoue, J.; Makino, H.; Miyado, K.; Ogawa, S.; Yoshimura, Y.; Umezawa, A. Xenografted human amniotic membranederived mesenchymal stem cells are immunologically tolerated and transdifferentiated into cardiomyocytes. Circ. Res. 106(10):1613-1623; 2010.
40. 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(11):1414-1421; 2006.
41. Vidal, M. A.; Walker, N. J.; Napoli, E.; Borjesson, D. L. Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue. Stem Cells Dev. 21(2):273-283; 2012.
42. Wasmeier, G. H.; Melnychenko, I.; Voigt, J. U.; Zimmermann, W. H.; Eschenhagen, T.; Schineis, N.; Reulbach, U.; Flachskampf, F. A.; Daniel, W. G.; Nixdorff, U. Reproducibility of transthoracic echocardiography in small animals using clinical equipment. Coron Artery Dis. 18(4):283-291; 2007.
43. Wollert, K. C.; Meyer, G. P.; Lotz, J.; Ringes-Lichtenberg, S.; Lippolt, P.; Breidenbach, C.; Fichtner, S.; Korte, T.; Hornig, B.; Messinger, D.; Arseniev, L.; Hertenstein, B.; Ganser, A.; Drexler, H. Intracoronary autologous bone-marrow cell transfer after myocardial infarction: The BOOST randomised controlled clinical trial. Lancet 364(9429):141-148; 2004.
44. Yoon, Y. S.; Wecker, A.; Heyd, L.; Park, J. S.; Tkebuchava, T.; Kusano, K.; Hanley, A.; Scadova, H.; Qin, G.; Cha, D. H.; Johnson, K. L.; Aikawa, R.; Asahara, T.; Losordo, D. W. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J. Clin. Invest. 115(2):326-338; 2005.
45. Zachar, V.; Duroux, M.; Emmersen, J.; Rasmussen, J. G.; Pennisi, C. P.; Yang, S.; Fink, T. Hypoxia and adipose-derived stem cell-based tissue regeneration and engineering. Expert Opin. Biol. Ther. 11(6):775-786; 2011.