About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 151679, 14 pages
http://dx.doi.org/10.1155/2013/151679
Research Article

Human Mesenchymal Stem Cells Provide Protection against Radiation-Induced Liver Injury by Antioxidative Process, Vasculature Protection, Hepatocyte Differentiation, and Trophic Effects

1Laboratoire de Radiopathologie et de Thérapies Expérimentales (LRTE), Institut de Radioprotection et de Sûreté Nucléaire (IRSN), PRP-HOM/SRBE/LRTE, BP 17, F-92262 Fontenay-aux-Roses Cedex, France
2UMRS-938, Equipe Prolifération et Différenciation des Cellules Souches du Pr Luc Douay: Application à la Thérapie Cellulaire, Faculté de Médecine Saint-Antoine, Université Paris VI Pierre et Marie Curie, 27 rue de Chaligny, 75012 Paris, France
3Service d'Hématologie et de Thérapie Cellulaire, Hôpital Saint-Antoine, 75012 Paris, France

Received 6 July 2013; Revised 20 October 2013; Accepted 20 October 2013

Academic Editor: Ji Wu

Copyright © 2013 Sabine Francois 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. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Gao, J. E. Dennis, R. F. Muzic, M. Lundberg, and A. I. Caplan, “The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion,” Cells Tissues Organs, vol. 169, no. 1, pp. 12–20, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. S. M. Devine, C. Cobbs, M. Jennings, A. Bartholomew, and R. Hoffman, “Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates,” Blood, vol. 101, no. 8, pp. 2999–3001, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Chapel, J. M. Bertho, M. Bensidhoum et al., “Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome,” Journal of Gene Medicine, vol. 5, no. 12, pp. 1028–1038, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Bensidhoum, A. Chapel, S. Francois et al., “Homing of in vitro expanded Stro-1- or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34 cell engraftment,” Blood, vol. 103, no. 9, pp. 3313–3319, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Allers, W. D. Sierralta, S. Neubauer, F. Rivera, J. J. Minguell, and P. A. Conget, “Dynamic of distribution of human bone marrow-derived mesenchymal stem cells after transplantation into adult unconditioned mice,” Transplantation, vol. 78, no. 4, pp. 503–508, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. S. François, M. Bensidhoum, M. Mouiseddine et al., “Local irradiation not only induces homing of human mesenchymal stem cells at exposed sites but promotes their widespread engraftment to multiple organs: a study of their quantitative distribution after irradiation damage,” Stem Cells, vol. 24, no. 4, pp. 1020–1029, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. S. François, M. Mouiseddine, N. Mathieu et al., “Human mesenchymal stem cells favour healing of the cutaneous radiation syndrome in a xenogenic transplant model,” Annals of Hematology, vol. 86, no. 1, pp. 1–8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Bey, M. Prat, P. Duhamel et al., “Emerging therapy for improving wound repair of severe radiation burns using local bone marrow-derived stem cell administrations,” Wound Repair and Regeneration, vol. 18, no. 1, pp. 50–58, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Horie, I. Sekiya, T. Muneta et al., “Intra-articular injected synovial stem cells differentiate into meniscal cells directly and promote meniscal regeneration without mobilization to distant organs in rat massive meniscal defect,” Stem Cells, vol. 27, no. 4, pp. 878–887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. X. Wu, L. Huang, Q. Zhou et al., “Mesenchymal stem cells participating in ex vivo endothelium repair and its effect on vascular smooth muscle cells growth,” International Journal of Cardiology, vol. 105, no. 3, pp. 274–282, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. M. F. Coronel, P. L. Musolino, and M. J. Villar, “Selective migration and engraftment of bone marrow mesenchymal stem cells in rat lumbar dorsal root ganglia after sciatic nerve constriction,” Neuroscience Letters, vol. 405, no. 1-2, pp. 5–9, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Natsu, M. Ochi, Y. Mochizuki, H. Hachisuka, S. Yanada, and Y. Yasunaga, “Allogeneic bone marrow-derived mesenchymal stromal cells promote the regeneration of injured skeletal muscle without differentiation into myofibers,” Tissue Engineering, vol. 10, no. 7-8, pp. 1093–1112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. X. Y. Wang, B. Liu, C. H. Yuan, H. Y. Yao, and N. Mao, “Effect of bone marrow mesenchymal stem cells on hematopoietic differentiation of murine embryonic stem cells,” Zhongguo Shi Yan Xue Ye Xue Za Zhi, vol. 11, no. 4, pp. 329–334, 2003. View at Scopus
  15. Y. Sato, H. Araki, J. Kato et al., “Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion,” Blood, vol. 106, no. 2, pp. 756–763, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. I. Aurich, L. P. Mueller, H. Aurich et al., “Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers,” Gut, vol. 56, no. 3, pp. 405–415, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Ringe, C. Kaps, G. Burmester, and M. Sittinger, “Stem cells for regenerative medicine: advances in the engineering of tissues and organs,” Naturwissenschaften, vol. 89, no. 8, pp. 338–351, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. R. S. Tuan, G. Boland, and R. Tuli, “Adult mesenchymal stem cells and cell-based tissue engineering,” Arthritis Research and Therapy, vol. 5, no. 1, pp. 32–45, 2003. View at Scopus
  19. G. Pelled, G. Turgeman, H. Aslan, Z. Gazit, and D. Gazit, “Mesenchymal stem cells for bone gene therapy and tissue engineering,” Current Pharmaceutical Design, vol. 8, no. 21, pp. 1917–1928, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Muguruma, T. Yahata, H. Miyatake et al., “Reconstitution of the functional human hematopoietic microenvironment derived from human mesenchymal stem cells in the murine bone marrow compartment,” Blood, vol. 107, no. 5, pp. 1878–1887, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. O. N. Koç, S. L. Gerson, B. W. Cooper et al., “Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy,” Journal of Clinical Oncology, vol. 18, no. 2, pp. 307–316, 2000. View at Scopus
  22. L. Fouillard, M. Bensidhoum, D. Bories et al., “Engraftment of allogeneic mesenchymal stem cells in the bone marrow of a patient with severe idiopathic aplastic anemia improves stroma,” Leukemia, vol. 17, no. 2, pp. 474–476, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Le Blanc and O. Ringdén, “Mesenchymal stem cells: properties and role in clinical bone marrow transplantation,” Current Opinion in Immunology, vol. 18, no. 5, pp. 586–591, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. O. Ringdén, M. Uzunel, I. Rasmusson et al., “Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease,” Transplantation, vol. 81, no. 10, pp. 1390–1397, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. A. I. Caplan, “Osteogenesis imperfecta, rehabilitation medicine, fundamental research and mesenchymal stem cells,” Connective Tissue Research, vol. 31, no. 4, pp. S9–S14, 1995. View at Scopus
  26. E. M. Horwitz, D. J. Prockop, L. A. Fitzpatrick et al., “Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta,” Nature Medicine, vol. 5, no. 3, pp. 309–313, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. O. N. Koç, J. Day, M. Nieder, S. L. Gerson, H. M. Lazarus, and W. Krivit, “Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH),” Bone Marrow Transplantation, vol. 30, no. 4, pp. 215–222, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Ayatollahi, M. Soleimani, S. Z. Tabei, and M. K. Salmani, “Hepatogenic differentiation of mesenchymal stem cells induced by insulin like growth factor-I,” World Journal of Stem Cells, vol. 3, no. 12, pp. 113–121, 2011. View at Publisher · View at Google Scholar
  29. W. Zhao, J. J. Li, D. Y. Cao et al., “Intravenous injection of mesenchymal stem cells is effective in treating liver fibrosis,” World Journal of Gastroenterology, vol. 18, no. 10, pp. 1048–1058, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. S. M. Fouraschen, Q. Pan, P. E. de Ruiter et al., “Secreted factors of human liver-derived mesenchymal stem cells promote liver regeneration early after partial hepatectomy,” Stem Cells and Development, vol. 21, no. 13, pp. 2410–2419, 2012. View at Publisher · View at Google Scholar
  31. L. Zhao, Z. Feng, B. Hu, X. Chi, and S. Jiao, “Ex vivo-expanded bone marrow mesenchymal stem cells facilitate recovery from chemically induced acute liver damage,” Hepatogastroenterology, vol. 59, no. 120, pp. 2389–2394, 2012.
  32. M. Mouiseddine, S. François, M. Souidi, and A. Chapel, “Intravenous human mesenchymal stem cells transplantation in NOD/SCID mice preserve liver integrity of irradiation damage,” Methods in Molecular Biology, vol. 826, pp. 179–188, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. A. I. Caplan, “Adult mesenchymal stem cells and the NO pathways,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 8, pp. 2695–2696, 2013. View at Publisher · View at Google Scholar
  34. K. A. Cho, S. Y. Woo, J. Y. Seoh, H. S. Han, and K. H. Ryu, “Mesenchymal stem cells restore CCl4-induced liver injury by an antioxidative process,” Cell Biology International, vol. 36, no. 12, pp. 1267–1274, 2012. View at Publisher · View at Google Scholar
  35. M. Muscaritoli, G. Grieco, S. Capria, A. P. Iori, and F. R. Fenelli, “Nutritional and metabolic support in patients undergoing bone marrow transplantation,” The American Journal of Clinical Nutrition, vol. 75, no. 2, pp. 183–190, 2002. View at Scopus
  36. M. H. Bourguignon, “The use of ionising radiations in medicine. A new era?” Quarterly Journal of Nuclear Medicine, vol. 44, no. 4, pp. 299–300, 2000. View at Scopus
  37. S. A. Lorimore and E. G. Wright, “Radiation-induced genomic instability and bystander effects: related inflammatory-type responses to radiation-induced stress and injury? A review,” International Journal of Radiation Biology, vol. 79, no. 1, pp. 15–25, 2003. View at Scopus
  38. M. H. El-Sayed, A. El-Haddad, O. A. Fahmy, I. I. Salama, and H. K. Mahmoud, “Liver disease is a major cause of mortality following allogeneic bone-marrow transplantation,” European Journal of Gastroenterology and Hepatology, vol. 16, no. 12, pp. 1347–1354, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. F. L. Dulley, E. J. Kanfer, F. R. Appelbaum et al., “Venocclusive disease of the liver after chemoradiotherapy and autologous bone marrow transplantation,” Transplantation, vol. 43, no. 6, pp. 870–873, 1987. View at Scopus
  40. G. B. McDonald, H. M. Shulman, J. L. Wolford, and G. D. Spencer, “Liver disease after human marrow transplantation,” Seminars in Liver Disease, vol. 7, no. 3, pp. 210–229, 1987. View at Scopus
  41. S. Y. Ma, W. Y. Au, I. O. Ng et al., “Hepatitic graft-versus-host disease after hematopoietic stem cell transplantation: clinicopathologic features and prognostic implication,” Transplantation, vol. 77, no. 8, pp. 1252–1259, 2004. View at Scopus
  42. M. Shi, Z. Zhang, R. Xu et al., “Human mesenchymal stem cell transfusion is safe and improves liver function in acute-on-chronic liver failure patients,” Stem Cells Translational Medicine, vol. 1, no. 10, pp. 725–731, 2012. View at Publisher · View at Google Scholar
  43. S. H. Kim, K. A. Kang, R. Zhang et al., “Protective effect of esculetin against oxidative stress-induced cell damage via scavenging reactive oxygen species,” Acta Pharmacologica Sinica, vol. 29, no. 11, pp. 1319–1326, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. M. H. Lü, C. Z. Li, C. J. Hu et al., “MicroRNA-27b suppresses mouse MSC migration to the liver by targeting SDF-1α in vitro,” Biochemical and Biophysical Research Communications, vol. 421, no. 2, pp. 389–395, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. M. J. Price, C. C. Chou, M. Frantzen et al., “Intravenous mesenchymal stem cell therapy early after reperfused acute myocardial infarction improves left ventricular function and alters electrophysiologic properties,” International Journal of Cardiology, vol. 111, no. 2, pp. 231–239, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Nomura, O. Honmou, K. Harada, K. Houkin, H. Hamada, and J. D. Kocsis, “I.V. infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat,” Neuroscience, vol. 136, no. 1, pp. 161–169, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. N. Mahmud, W. Pang, C. Cobbs et al., “Studies of the route of administration and role of conditioning with radiation on unrelated allogeneic mismatched mesenchymal stem cell engraftment in a nonhuman primate model,” Experimental Hematology, vol. 32, no. 5, pp. 494–501, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. Q. Li, X. Zhou, Y. Shi et al., “In vivo tracking and comparison of the therapeutic effects of MSCs and HSCs for liver injury,” PLoS ONE, vol. 8, no. 4, Article ID e62363, 2013.
  49. G. A. Nasir, S. Mohsin, M. Khan et al., “Mesenchymal stem cells and Interleukin-6 attenuate liver fibrosis in mice,” Journal of Translational Medicine, vol. 11, article 78, 2013. View at Publisher · View at Google Scholar
  50. T. Yamashita, M. Shoge, E. Oda et al., “The free-radical scavenger, edaravone, augments NO release from vascular cells and platelets after laser-induced, acute endothelial injury in vivo,” Platelets, vol. 17, no. 3, pp. 201–206, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. M. H. Gaugler, “A unifying system: does the vascular endothelium have a role to play in multi-organ failure following radiation exposure?” The British Journal of Radiology Supplement, vol. 27, pp. 100–105, 2005.
  52. G. Y. Rochefort, P. Vaudin, N. Bonnet et al., “Influence of hypoxia on the domiciliation of mesenchymal stem cells after infusion into rats: possibilities of targeting pulmonary artery remodeling via cells therapies?” Respiratory Research, vol. 6, article 125, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. F. Baron and R. Storb, “Mensenchymal stromal cells: a new tool against graft-versus-host disease?” Biology of Blood and Marrow Transplantation, vol. 18, no. 6, pp. 822–840, 2012. View at Publisher · View at Google Scholar · View at Scopus