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International Journal of Hepatology
Volume 2013, Article ID 310612, 7 pages
http://dx.doi.org/10.1155/2013/310612
Review Article

Implication for Bone Marrow Derived Stem Cells in Hepatocyte Regeneration after Orthotopic Liver Transplantation

1Division of Transplantation, Department of Surgery, Medical University of Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria
2Surgical Research Laboratories, Department of Surgery, Medical University of Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria

Received 14 June 2013; Revised 5 August 2013; Accepted 12 August 2013

Academic Editor: Arno W. Tilles

Copyright © 2013 N. Pilat 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. Blachier, H. Leleu, M. Peck-Radosavljevic, D. C. Valla, and F. Roudot-Thoraval, “The burden of liver disease in Europe: a review of available epidemiological data,” Journal of Hepatology, vol. 58, no. 3, pp. 593–608, 2013. View at Google Scholar
  2. S. K. Asrani, J. J. Larson, B. Yawn, T. M. Therneau, and W. R. Kim, “Underestimation of liver-related mortality in the United States,” Gastroenterology, vol. 145, no. 2, pp. 375–382, 2013. View at Publisher · View at Google Scholar
  3. M. Colombo, J. L. Raoul, R. Lencioni et al., “Multidisciplinary strategies to improve treatment outcomes in hepatocellular carcinoma: a European perspective,” European Journal of Gastroenterology & Hepatology, vol. 25, no. 6, pp. 639–651, 2013. View at Publisher · View at Google Scholar
  4. R. Adam, V. Karam, V. Delvart et al., “Evolution of indications and results of liver transplantation in Europe. A report from the European Liver Transplant Registry (ELTR),” Journal of Hepatology, vol. 57, no. 3, pp. 675–688, 2012. View at Publisher · View at Google Scholar
  5. A. Nussler, S. Konig, M. Ott et al., “Present status and perspectives of cell-based therapies for liver diseases,” Journal of Hepatology, vol. 45, no. 1, pp. 144–159, 2006. View at Publisher · View at Google Scholar
  6. A. Dhawan, J. Puppi, R. D. Hughes, and R. R. Mitry, “Human hepatocyte transplantation: current experience and future challenges,” Nature Reviews Gastroenterology and Hepatology, vol. 7, no. 5, pp. 288–298, 2010. View at Publisher · View at Google Scholar
  7. B. E. Petersen, B. Grossbard, H. Hatch, L. Pi, J. Deng, and E. W. Scott, “Mouse A6-positive hepatic oval cells also express several hematopoietic stem cell markers,” Hepatology, vol. 37, no. 3, pp. 632–640, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. H. M. Hatch, D. Zheng, M. L. Jorgensen, and B. E. Petersen, “SDF-1α/CXCR4: a mechanism for hepatic oval cell activation and bone marrow stem cell recruitment to the injured liver of rats,” Cloning and Stem Cells, vol. 4, no. 4, pp. 339–351, 2002. View at Google Scholar · View at Scopus
  9. B. E. Petersen, W. C. Bowen, K. D. Patrene et al., “Bone marrow as a potential source of hepatic oval cells,” Science, vol. 284, no. 5417, pp. 1168–1170, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Lagasse, H. Connors, M. Al-Dhalimy et al., “Purified hematopoietic stem cells can differentiate into hepatocytes in vivo,” Nature Medicine, vol. 6, no. 11, pp. 1229–1234, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. A. J. Wagers, R. I. Sherwood, J. L. Christensen, and I. L. Weissman, “Little evidence for developmental plasticity of adult hematopoietic stem cells,” Science, vol. 297, no. 5590, pp. 2256–2259, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Wang, H. Willenbring, Y. Akkari et al., “Cell fusion is the principal source of bone-marrow-derived hepatocytes,” Nature, vol. 422, no. 6934, pp. 897–901, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Vassilopoulos, P.-R. Wang, and D. W. Russell, “Transplanted bone marrow regenerates liver by cell fusion,” Nature, vol. 422, no. 6934, pp. 901–904, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. M. R. Alison, R. Poulsom, R. Jeffery et al., “Hepatocytes from non-hepatic adult stem cells,” Nature, vol. 406, no. 6793, p. 257, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. N. D. Theise, M. Nimmakayalu, R. Gardner et al., “Liver from bone marrow in humans,” Hepatology, vol. 32, no. 1, pp. 11–16, 2000. View at Google Scholar · View at Scopus
  16. M. Körbling, R. L. Katz, A. Khanna et al., “Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells,” The New England Journal of Medicine, vol. 346, no. 10, pp. 738–746, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Fogt, K. H. Beyser, C. Poremba, R. L. Zimmerman, U. Khettry, and J. Ruschoff, “Recipient-derived hepatocytes in liver transplants: a rare event in sex-mismatched transplants,” Hepatology, vol. 36, no. 1, pp. 173–176, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. W. Kleeberger, T. Rothämel, S. Glöckner, P. Flemming, U. Lehmann, and H. Kreipe, “High frequency of epithelial chimerism in liver transplants demonstrated by microdissection and STR-analysis,” Hepatology, vol. 35, no. 1, pp. 110–116, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Wu, K. Cieply, M. A. Nalesnik et al., “Minimal evidence of transdifferentiation from recipient bone marrow to parenchymal cells in regenerating and long-surviving human allografts,” American Journal of Transplantation, vol. 3, no. 9, pp. 1173–1181, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. W. R. ten Hove, B. van Hoek, I. M. Bajema, J. Ringers, J. H. J. M. van Krieken, and E. L. Lagaaij, “Extensive chimerism in liver transplants: vascular endothelium, bile duct epithelium, and hepatocytes,” Liver Transplantation, vol. 9, no. 6, pp. 552–556, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. I. O.-L. Ng, K.-L. Chan, W.-H. Shek et al., “High frequency of chimerism in transplanted livers,” Hepatology, vol. 38, no. 4, pp. 989–998, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Idilman, E. Erden, I. Kuzu et al., “Recipient-derived hepatocytes in sex-mismatched liver allografts after liver transplantation: early versus late transplant biopsies,” Transplantation, vol. 78, no. 11, pp. 1647–1652, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Idilman, E. Erden, I. Kuzu, S. Ersoz, and S. Karayalcin, “The fate of recipient-derived hepatocytes in sex-mismatched liver allograft following liver transplantation,” Clinical Transplantation, vol. 21, no. 2, pp. 202–206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Pilat, S. Schoppmann, J. Stift, P. Mazal, T. Wekerle, and G. A. Berlakovich, “No evidence for recipient-derived hepatocytes in serial biopsies of sex-mismatched liver transplants,” Transplantation, vol. 94, no. 9, pp. 953–957, 2012. View at Publisher · View at Google Scholar
  25. W. Aini, A. Miyagawa-Hayashino, M. Ozeki et al., “Frequent hepatocyte chimerism in long-term human liver allografts independent of graft outcome,” Transplant Immunology, vol. 28, no. 2-3, pp. 2100–2135, 2013. View at Publisher · View at Google Scholar
  26. T. Okabayashi, A. M. Cameron, M. Hisada, R. A. Montgomery, G. M. Williams, and Z. Sun, “Mobilization of host stem cells enables long-term liver transplant acceptance in a strongly rejecting rat strain combination,” American Journal of Transplantation, vol. 11, no. 10, pp. 2046–2056, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Fausto, “Liver regeneration and repair: hepatocytes, progenitor cells, and stem cells,” Hepatology, vol. 39, no. 6, pp. 1477–1487, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. P. S. Randhawa, T. Starzl, H. C. Ramos, M. A. Nalesnik, and J. Demetris, “Allografts surviving for 26 to 29 years following living-related kidney transplantation: analysis by light microscopy, in situ hybridization for the Y chromosome, and anti-HLA antibodies,” American Journal of Kidney Diseases, vol. 24, no. 1, pp. 72–77, 1994. View at Google Scholar · View at Scopus
  29. S. H. Hong, E. J. Gang, J. A. Jeong et al., “In vitro differentiation of human umbilical cord blood-derived mesenchymal stem cells into hepatocyte-like cells,” Biochemical and Biophysical Research Communications, vol. 330, no. 4, pp. 1153–1161, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. D. S. Krause, N. D. Theise, M. I. Collector et al., “Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell,” Cell, vol. 105, no. 3, pp. 369–377, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. D. D. Houlihan and P. N. Newsome, “Critical review of clinical trials of bone marrow stem cells in liver disease,” Gastroenterology, vol. 135, no. 2, pp. 438–450, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. B. Fang, M. Shi, L. Liao, S. Yang, Y. Liu, and R. C. Zhao, “Systemic infusion of FLK1+ mesenchymal stem cells ameliorate carbon tetrachloride-induced liver fibrosis in mice,” Transplantation, vol. 78, no. 1, pp. 83–88, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. Q. Zhao, H. Ren, D. Zhu, and Z. Han, “Stem/progenitor cells in liver injury repair and regeneration,” Biology of the Cell, vol. 101, no. 10, pp. 557–571, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. 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
  35. D. van Poll, B. Parekkadan, C. H. Cho et al., “Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo,” Hepatology, vol. 47, no. 5, pp. 1634–1643, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Shi, G. Hu, J. Su et al., “Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair,” Cell Research, vol. 20, no. 5, pp. 510–518, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. J. M. Ryan, F. P. Barry, J. M. Murphy, and B. P. Mahon, “Mesenchymal stem cells avoid allogeneic rejection,” Journal of Inflammation, vol. 2, article 8, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. E. K. Moioli, P. A. Clark, M. Chen et al., “Synergistic actions of hematopoietic and mesenchymal stem/progenitor cells in vascularizing bioengineered tissues,” PLoS One, vol. 3, no. 12, Article ID e3922, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. T. E. Ichim, F. Solano, F. Lara et al., “Combination stem cell therapy for heart failure,” International Archives of Medicine, vol. 3, no. 1, article 5, 2010. View at Publisher · View at Google Scholar
  40. M. Kassem, “Mesenchymal stem cells: biological characteristics and potential clinical applications,” Cloning and Stem Cells, vol. 6, no. 4, pp. 369–374, 2004. View at Google Scholar · View at Scopus
  41. Y. Jiang, B. N. Jahagirdar, R. L. Reinhardt et al., “Pluripotency of mesenchymal stem cells derived from adult marrow,” Nature, vol. 418, no. 6893, pp. 41–49, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. 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. View at Google Scholar
  43. B. Christ and M. M. Dollinger, “The generation of hepatocytes from mesenchymal stem cells and engraftment into the liver,” Current Opinion in Organ Transplantation, vol. 16, no. 1, pp. 69–75, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Aurich, M. Sgodda, P. Kaltwaßer et al., “Hepatocyte differentiation of mesenchymal stem cells from human adipose tissue in vitro promotes hepatic integration in vivo,” Gut, vol. 58, no. 4, pp. 570–581, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. K.-D. Lee, T. K.-C. Kuo, J. Whang-Peng et al., “In vitro hepatic differentiation of human mesenchymal stem cells,” Hepatology, vol. 40, no. 6, pp. 1275–1284, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Banas, T. Teratani, Y. Yamamoto et al., “IFATS collection: in vivo therapeutic potential of human adipose tissue mesenchymal stem cells after transplantation into mice with liver injury,” Stem Cells, vol. 26, no. 10, pp. 2705–2712, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. A. W. Duncan, C. Dorrell, and M. Grompe, “Stem cells and liver regeneration,” Gastroenterology, vol. 137, no. 2, pp. 466–481, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. S. L. Friedman, “Liver fibrosis—from bench to bedside,” Journal of Hepatology, vol. 38, supplement 1, pp. S38–S53, 2003. View at Google Scholar · View at Scopus
  49. V. A. Dolgachev, M. R. Ullenbruch, N. W. Lukacs, and S. H. Phan, “Role of stem cell factor and bone marrow-derived fibroblasts in airway remodeling,” American Journal of Pathology, vol. 174, no. 2, pp. 390–400, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. S. B. Haudek, Y. Xia, P. Huebener et al., “Bone marrow-derived fibroblast precursors mediate ischemic cardiomyopathy in mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 48, pp. 18284–18289, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Nimphius, R. Moll, P. Olbert, A. Ramaswamy, and P. J. Barth, “CD34+ fibrocytes in chronic cystitis and noninvasive and invasive urothelial carcinomas of the urinary bladder,” Virchows Archiv, vol. 450, no. 2, pp. 179–185, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Kisseleva, H. Uchinami, N. Feirt et al., “Bone marrow-derived fibrocytes participate in pathogenesis of liver fibrosis,” Journal of Hepatology, vol. 45, no. 3, pp. 429–438, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. S. J. Forbes, F. P. Russo, V. Rey et al., “A significant proportion of myofibroblasts are of bone marrow origin in human liver fibrosis,” Gastroenterology, vol. 126, no. 4, pp. 955–963, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. B. D. Paredes, L. A. Faccioli, L. F. Quintanilha et al., “Bone marrow progenitor cells do not contribute to liver fibrogenic cells,” World Journal of Hepatology, vol. 4, no. 10, pp. 274–283, 2012. View at Publisher · View at Google Scholar
  55. I. Sakaida, S. Terai, N. Yamamoto et al., “Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice,” Hepatology, vol. 40, no. 6, pp. 1304–1311, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. K.-A. Cho, G.-W. Lim, S.-Y. Joo et al., “Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice,” Liver International, vol. 31, no. 7, pp. 932–939, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Nunes de Carvalho, E. Helal-Neto, D. C. de Andrade et al., “Bone marrow mononuclear cell transplantation increases metalloproteinase-9 and 13 and decreases tissue inhibitors of metalloproteinase-1 and 2 expression in the liver of cholestatic rats,” Cells, Tissues, Organs, 2013. View at Publisher · View at Google Scholar
  58. T. Takami, S. Terai, and I. Sakaida, “Stem cell therapy in chronic liver disease,” Current Opinion in Gastroenterology, vol. 28, no. 3, pp. 203–208, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. D. Schuppan and Y. O. Kim, “Evolving therapies for liver fibrosis,” The Journal of Clinical Investigation, vol. 123, no. 5, pp. 1887–1901, 2013. View at Publisher · View at Google Scholar
  60. G. Ferrari, G. Cusella-De Angelis, M. Coletta et al., “Muscle regeneration by bone marrow-derived myogenic progenitors,” Science, vol. 279, no. 5356, pp. 1528–1530, 1998. View at Publisher · View at Google Scholar · View at Scopus
  61. N. D. Theise, S. Badve, R. Saxena et al., “Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation,” Hepatology, vol. 31, no. 1, pp. 235–240, 2000. View at Google Scholar · View at Scopus
  62. D. Orlic, J. Kajstura, S. Chimenti et al., “Bone marrow cells regenerate infarcted myocardium,” Nature, vol. 410, no. 6829, pp. 701–705, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. E. Mezey, K. J. Chandross, G. Harta, R. A. Maki, and S. R. McKercher, “Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow,” Science, vol. 290, no. 5497, pp. 1779–1782, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. Z. Zhang, J. Liu, Y. Liu, Z. Li, W. Q. Gao, and Z. He, “Generation, characterization and potential therapeutic applications of mature and functional hepatocytes from stem cells,” Journal of Cellular Physiology, vol. 228, no. 2, pp. 298–305, 2013. View at Publisher · View at Google Scholar