Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for Stem Cells International, enter your email address in the box below.

Stem Cells International
Volume 2013, Article ID 178346, 10 pages
http://dx.doi.org/10.1155/2013/178346
Research Article

Comparison of the Direct Effects of Human Adipose- and Bone-Marrow-Derived Stem Cells on Postischemic Cardiomyoblasts in an In Vitro Simulated Ischemia-Reperfusion Model

Mónika Szepes,1 Zsolt Benkő,1 Attila Cselenyák,1 Kai Michael Kompisch,2 Udo Schumacher,2 Zsombor Lacza,1 and Levente Kiss1

1Institute of Human Physiology and Clinical Experimental Research, Semmelweis University, Tűzoltó Utca 37-47, Budapest 1094, Hungary
2Department of Anatomy and Experimental Morphology, Center for Experimental Medicine, University Hospital Hamburg-Eppendorf, Martinistraße 52, 20246 Hamburg, Germany

Received 1 April 2013; Accepted 31 May 2013

Academic Editor: Shinsuke Yuasa

Copyright © 2013 Mónika Szepes et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Bajada, I. Mazakova, J. B. Richardson, and N. Ashammakhi, “Updates on stem cells and their applications in regenerative medicine,” Journal of Tissue Engineering and Regenerative Medicine, vol. 2, no. 4, pp. 169–183, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. M. Wu and K. Hochedlinger, “Harnessing the potential of induced pluripotent stem cells for regenerative medicine,” Nature Cell Biology, vol. 13, no. 5, pp. 497–505, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Leeb, M. Jurga, C. Mcguckin et al., “New perspectives in stem cell research: beyond embryonic stem cells,” Cell Proliferation, vol. 44, supplement 1, pp. 9–14, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. A. C. Brignier and A. M. Gewirtz, “Embryonic and adult stem cell therapy,” Journal of Allergy and Clinical Immunology, vol. 125, supplement 2, no. 2, pp. S336–S344, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Sanz-Ruiz, E. Gutiérrez Ibañes, A. V. Arranz, M. E. Fernández Santos, P. L. S. Fernández, and F. Fernández-Avilés, “Phases I-III clinical trials using adult stem cells,” Stem Cells International, vol. 2010, Article ID 579142, 12 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. P. A. Zuk, M. Zhu, P. Ashjian et al., “Human adipose tissue is a source of multipotent stem cells,” Molecular Biology of the Cell, vol. 13, no. 12, pp. 4279–4295, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Wilson, P. E. Butler, and A. M. Seifalian, “Adipose-derived stem cells for clinical applications: a review,” Cell Proliferation, vol. 44, no. 1, pp. 86–98, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. F. Hildner, C. Albrecht, C. Gabriel, H. Redl, and M. van Griensven, “State of the art and future perspectives of articular cartilage regeneration: a focus on adipose-derived stem cells and platelet-derived products,” Journal of Tissue Engineering and Regenerative Medicine, vol. 5, no. 4, pp. e36–e51, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. J. M. Gimble, W. Grayson, F. Guilak, M. J. Lopez, and G. Vunjak-Novakovic, “Adipose tissue as a stem cell source for musculoskeletal regeneration,” Frontiers in Bioscience, vol. 3, pp. 69–81, 2011. View at Google Scholar · View at Scopus
  10. S. Lendeckel, A. Jödicke, P. Christophis et al., “Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report,” Journal of Cranio-Maxillofacial Surgery, vol. 32, no. 6, pp. 370–373, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. C. M. Cowan, Y.-Y. Shi, O. O. Aalami et al., “Adipose-derived adult stromal cells heal critical-size mouse calvarial defects,” Nature Biotechnology, vol. 22, no. 5, pp. 560–567, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Cherubino, J. P. Rubin, N. Miljkovic, A. Kelmendi-Doko, and K. G. Marra, “Adipose-derived stem cells for wound healing applications,” Annals of Plastic Surgery, vol. 66, no. 2, pp. 210–215, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Léobon, J. Roncalli, C. Joffre et al., “Adipose-derived cardiomyogenic cells: in vitro expansion and functional improvement in a mouse model of myocardial infarction,” Cardiovascular Research, vol. 83, no. 4, pp. 757–767, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Sanz-Ruiz, M. E. F. Santos, M. D. Muñoa et al., “Adipose tissue-derived stem cells: the friendly side of a classic cardiovascular foe,” Journal of cardiovascular translational research, vol. 1, no. 1, pp. 55–63, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. X. Bai, Y. Yan, Y.-H. Song et al., “Both cultured and freshly isolated adipose tissue-derived stem cells enhance cardiac function after acute myocardial infarction,” European Heart Journal, vol. 31, no. 4, pp. 489–501, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Mazo, J. J. Gavira, B. Pelacho, and F. Prosper, “Adipose-derived stem cells for myocardial infarction,” Journal of Cardiovascular Translational Research, vol. 4, no. 2, pp. 145–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Schenke-Layland, B. M. Strem, M. C. Jordan et al., “Adipose tissue-derived cells improve cardiac function following myocardial infarction,” Journal of Surgical Research, vol. 153, no. 2, pp. 217–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. N. N. Hoke, F. N. Salloum, K. E. Loesser-Casey, and R. C. Kukreja, “Cardiac regenerative potential of adipose tissue-derived stem cells,” Acta Physiologica Hungarica, vol. 96, no. 3, pp. 251–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Valina, K. Pinkernell, Y.-H. Song et al., “Intracoronary administration of autologous adipose tissue-derived stem cells improves left ventricular function, perfusion, and remodelling after acute myocardial infarction,” European Heart Journal, vol. 28, no. 21, pp. 2667–2677, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Abdel-Latif, R. Bolli, I. M. Tleyjeh et al., “Adult bone marrow-derived cells for cardiac repair: a systematic review and meta-analysis,” Archives of Internal Medicine, vol. 167, no. 10, pp. 989–997, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. M. J. Lipinski, G. G. L. Biondi-Zoccai, A. Abbate et al., “Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction. A collaborative systematic review and meta-analysis of controlled clinical trials,” Journal of the American College of Cardiology, vol. 50, no. 18, pp. 1761–1767, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Chavakis, M. Koyanagi, and S. Dimmeler, “Enhancing the outcome of cell therapy for cardiac repair: progress from bench to bedside and back,” Circulation, vol. 121, no. 2, pp. 325–335, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Mazo, M. Araña, B. Pelacho, and F. Prosper, “Mesenchymal stem cells and cardiovascular disease: a bench to bedside roadmap,” Stem Cells International, vol. 2012, Article ID 175979, 11 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. M. T. Elnakish, F. Hassan, D. Dakhlallah et al., “Mesenchymal stem cells for cardiac regeneration: translation to bedside reality,” Stem Cells International, vol. 2012, Article ID 646038, 14 pages, 2012. View at Publisher · View at Google Scholar
  25. M. Mazo, V. Planat-Bénard, G. Abizanda et al., “Transplantation of adipose derived stromal cells is associated with functional improvement in a rat model of chronic myocardial infarction,” European Journal of Heart Failure, vol. 10, no. 5, pp. 454–462, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. J. G. Rasmussen, O. Frobert, C. Holst-Hansen et al., “Comparison of human adipose-derived stem cells and bone marrow-derived stem cells in a myocardial infarction model,” Cell Transplantation. In press.
  27. M. Alvarez-Dolado, R. Pardal, J. M. Garcia-Verdugo et al., “Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes,” Nature, vol. 425, no. 6961, pp. 968–973, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Kajstura, M. Rota, B. Whang et al., “Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion,” Circulation Research, vol. 96, no. 1, pp. 127–137, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. C. E. Murry, M. H. Soonpaa, H. Reinecke et al., “Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts,” Nature, vol. 428, no. 6983, pp. 664–668, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Nygren, S. Jovinge, M. Breitbach et al., “Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation,” Nature Medicine, vol. 10, no. 5, pp. 494–501, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Rehman, D. Traktuev, J. Li et al., “Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells,” Circulation, vol. 109, no. 10, pp. 1292–1298, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. T. P. Lozito and R. S. Tuan, “Mesenchymal stem cells inhibit both endogenous and exogenous MMPs via secreted TIMPs,” Journal of Cellular Physiology, vol. 226, no. 2, pp. 385–396, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Sadat, S. Gehmert, Y.-H. Song et al., “The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF,” Biochemical and Biophysical Research Communications, vol. 363, no. 3, pp. 674–679, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Kinnaird, E. Stabile, M. S. Burnett et al., “Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms,” Circulation Research, vol. 94, no. 5, pp. 678–685, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. H. K. Haider and M. Ashraf, “Strategies to promote donor cell survival: combining preconditioning approach with stem cell transplantation,” Journal of Molecular and Cellular Cardiology, vol. 45, no. 4, pp. 554–566, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. I. B. Copland and J. Galipeau, “Death and inflammation following somatic cell transplantation,” Seminars in Immunopathology, vol. 33, no. 6, pp. 535–550, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. P. A. Zuk, M. Zhu, H. Mizuno et al., “Multilineage cells from human adipose tissue: implications for cell-based therapies,” Tissue Engineering, vol. 7, no. 2, pp. 211–228, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. K. M. Kompisch, C. Lange, D. Steinemann et al., “Neurogenic transdifferentiation of human adipose-derived stem cells? A critical protocol reevaluation with special emphasis on cell proliferation and cell cycle alterations,” Histochemistry and Cell Biology, vol. 134, no. 5, pp. 453–468, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. M. A. Vidal, N. J. Walker, E. Napoli, and D. L. Borjesson, “Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue,” Stem Cells and Development, vol. 21, no. 2, pp. 273–283, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Cselenyák, E. Pankotai, E. M. Horváth, L. Kiss, and Z. Lacza, “Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections,” BMC Cell Biology, vol. 11, article 29, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Cselenyák, Z. Benko, M. Szepes, L. Kiss, and Z. Lacza, “Stem cell transplantation in an in vitro simulated ischemia/reperfusion model,” Journal of Visualized Experiments, no. 57, Article ID e3575, 2011. View at Google Scholar · View at Scopus
  42. M. Szepes, Z. Janicsek, Z. Benko et al., “Pretreatment of therapeutic cells with poly(ADP-ribose) polymerase inhibitor enhances their efficacy in an in vitro model of cell-based therapy in myocardial infarct,” International Journal of Molecular Medicine, vol. 31, no. 1, pp. 26–32, 2013. View at Google Scholar
  43. M. A. King, “Detection of dead cells and measurement of cell killing by flow cytometry,” Journal of Immunological Methods, vol. 243, no. 1-2, pp. 155–166, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. R. de La Fuente, J. L. Abad, J. García-Castro et al., “Dedifferentiated adult articular chondrocytes: a population of human multipotent primitive cells,” Experimental Cell Research, vol. 297, no. 2, pp. 313–328, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Oswald, S. Boxberger, B. Jørgensen et al., “Mesenchymal stem cells can be differentiated into endothelial cells in vitro,” Stem Cells, vol. 22, no. 3, pp. 377–384, 2004. View at Google Scholar · View at Scopus
  46. X. Liu, Z. Wang, R. Wang et al., “Direct comparison of the potency of human mesenchymal stem cells derived from amnion tissue, bone marrow and adipose tissue at inducing dermal fibroblast responses to cutaneous wounds,” International Journal of Molecular Medicine, vol. 31, no. 2, pp. 407–415, 2013. View at Google Scholar
  47. Z. Zhou, Y. Chen, H. Zhang et al., “Comparison of mesenchymal stromal cells from human bone marrow and adipose tissue for the treatment of spinal cord injury,” Cytotherapy, vol. 15, no. 4, pp. 434–448, 2013. View at Google Scholar
  48. Z. Xishan, H. Baoxin, Z. Xinna et al., “Comparison of the effects of human adipose and bone marrow mesenchymal stem cells on T lymphocytes,” Cell Biology International, vol. 37, no. 1, pp. 11–18, 2013. View at Google Scholar
  49. E. Y. Plotnikov, T. G. Khryapenkova, A. K. Vasileva et al., “Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture,” Journal of Cellular and Molecular Medicine, vol. 12, no. 5A, pp. 1622–1631, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Ishikawa, H. Shimazu, L. D. Shultz et al., “Purified human hematopoietic stem cells contribute to the generation of cardiomyocytes through cell fusion,” The FASEB journal, vol. 20, no. 7, pp. 950–952, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. Z. Lacza, E. Horváth, and D. W. Busija, “Neural stem cell transplantation in cold lesion: a novel approach for the investigation of brain trauma and repair,” Brain Research Protocols, vol. 11, no. 3, pp. 145–154, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Garbade, A. Schubert, A. J. Rastan et al., “Fusion of bone marrow-derived stem cells with cardiomyocytes in a heterologous in vitro model,” European Journal of Cardio-Thoracic Surgery, vol. 28, no. 5, pp. 685–691, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Menasché, “You can't judge a book by its cover,” Circulation, vol. 113, no. 10, pp. 1275–1277, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. N. A. Kouris, J. A. Schaefer, M. Hatta et al., “Directed fusion of mesenchymal stem cells with cardiomyocytes via VSV-G facilitates stem cell programming,” Stem Cells International, vol. 2012, Article ID 414038, 13 pages, 2012. View at Publisher · View at Google Scholar
  55. L. Timmers, S. K. Lim, I. E. Hoefer et al., “Human mesenchymal stem cell-conditioned medium improves cardiac function following myocardial infarction,” Stem Cell Research, vol. 6, no. 3, pp. 206–214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. A. Wilson and A. Trumpp, “Bone-marrow haematopoietic-stem-cell niches,” Nature Reviews Immunology, vol. 6, no. 2, pp. 93–106, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. G.-Q. Huang, J.-N. Wang, J.-M. Tang et al., “The combined transduction of copper, zinc-superoxide dismutase and catalase mediated by cell-penetrating peptide, PEP-1, to protect myocardium from ischemia-reperfusion injury,” Journal of Translational Medicine, vol. 9, article no. 73, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. K. T. Keyes, Y. Ye, Y. Lin et al., “Resolvin E1 protects the rat heart against reperfusion injury,” The American Journal of Physiology, vol. 299, no. 1, pp. H153–H164, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. D. K. Singla and D. E. McDonald, “Factors released from embryonic stem cells inhibit apoptosis of H9c2 cells,” The American Journal of Physiology, vol. 293, no. 3, pp. H1590–H1595, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. D. Yang, W. Wang, L. Li et al., “The relative contribution of paracine effect versus direct differentiation on adipose-derived stem cell transplantation mediated cardiac repair,” PLoS One, vol. 8, no. 3, Article ID e59020, 2013. View at Google Scholar
  61. S. Alshammary, S. Fukushima, S. Miyagawa et al., “Impact of cardiac stem cell sheet transplantation on myocardial infarction,” Surgery Today, 2013. View at Publisher · View at Google Scholar
  62. A. R. Williams, K. E. Hatzistergos, B. Addicott et al., “Enhanced effect of combining human cardiac stem cells and bone marrow mesenchymal stem cells to reduce infarct size and to restore cardiac function after myocardial infarction,” Circulation, vol. 127, no. 2, pp. 213–223, 2013. View at Google Scholar
  63. J. K. Fraser, I. Wulur, Z. Alfonso, and M. H. Hedrick, “Fat tissue: an underappreciated source of stem cells for biotechnology,” Trends in Biotechnology, vol. 24, no. 4, pp. 150–154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Peng, Z. Jia, X. Yin et al., “Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue,” Stem Cells and Development, vol. 17, no. 4, pp. 761–773, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Diez Villanueva, R. Sanz-Ruiz, A. Nunez Garcia et al., “Functional multipotency of stem cells: what do we need from them in the heart?” Stem Cells International, vol. 2012, Article ID 817364, 12 pages, 2012. View at Publisher · View at Google Scholar