Cell transplantation of adipose tissue-derived stem cells in combination with heparin attenuated acute liver failure in mice

Cell Transplantation

Volumn 18, Issue 5-6, 2009, Pages 611-618

  Yukawa, Hiroshi ^a   Noguchi, Hirofumi ^b   Oishi, Koichi ^a   Takagi, Soichi ^a   Hamaguchi, Michinari ^a   Hamajima, Nobuyuki ^a   Hayashi, Shuji ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b BAYLOR RESEARCH INSTITUTE   (United States)

Author keywords

Acute liver failure; Adipose tissue derived stem cells (ASCs); Cell transplantation; Heparin

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CARBON TETRACHLORIDE; HEPARIN; LACTATE DEHYDROGENASE; SCATTER FACTOR;

ADIPOSE TISSUE CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; LIVER FAILURE; LIVER PROTECTION; LIVER REGENERATION; LUNG INJURY; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION;

MUS;

EID: 70349255610     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.1177/096368970901805-617     Document Type: Article

References (43)

1. Abe, W.; Ikejima, K.; Lang, T.; Okumura, K.; Enomoto, N.; Kitamura, T.; Takei, Y.; Sato, N. Low molecular weight heparin prevents hepatic fibrogenesis caused by carbon tetrachloride in the rat. J. Hepatol. 46(2):286-294; 2007. (Pubitemid 44959153)
2. Alison, M. R.; Poulsom, R.; Jeffery, R.; Dhillon, A. P.; Quaglia, A.; Jacob, J.; Novelli, M.; Prentice, G.; Williamson, J.; Wright, N. A. Hepatocytes from non-hepatic adult stem cells. Nature 406(6793):257; 2000.
3. Alvarez-Dolado, M.; Pardal, R.; Garcia-Verdugo, J. M.; Fike, J. R.; Lee, H. O.; Pfeffer, K.; Lois, C.; Morrison, S. J.; Alvarez-Buylla, A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425(6961):968-973; 2003.
4. Anjos-Afonso, F.; Siapati, E. K.; Bonnet, D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J. Cell Sci. 117(Pt. 23):5655-5664; 2004.
5. Aurich, I.; Mueller, L. P.; Aurich, H.; Luetzkendorf, J.; Tisljar, K.; Dollinger, M. M.; Schormann, W.; Walldorf, J.; Hengstler, J. G.; Fleig, W. E.; Christ, B. Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 56(3):405-415; 2007. (Pubitemid 46579773)
6. Barry, F. P.; Murphy, J. M. Mesenchymal stem cells: clinical applications and biological characterization. Int. J. Biochem. Cell Biol. 36(4):568-584; 2004
7. Cai, L.; Johnstone, B. H.; Cook, T. G.; Liang, Z.; Traktuev, D.; Cornetta, K.; Ingram, D. A.; Rosen, E. D.; March, K. L. Suppression of hepatocyte growth factor production impairs the ability of adipose-derived stem cells to promote ischemic tissue revascularization. Stem Cells 25(12):3234-3243; 2007.
8. Hamano, K.; Li, T. S.; Kobayashi, T.; Hirata, K.; Yano, M.; Kohno, M.; Matsuzaki, M. Therapeutic angiogenesis induced by local autologous bone marrow cell implantation. Ann. Thorac. Surg. 73(4):1210-1215; 2002.
9. Jiang, Y.; Jahagirdar, B. N.; Reinhardt, R. L.; Schwartz, R. E.; Keene, C. D.; Ortiz-Gonzalez, X. R.; Reyes, M.; Lenvik, T.; Lund, T.; Blackstad, M.; Du, J.; Aldrich, S.; Lisberg, A.; Low, W. C.; Largaespada, D. A.; Verfaillie, C. M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418(6893):41-49; 2002.
10. Kassem, M.; Kristiansen, M.; Abdallah, B. M. Mesenchymal stem cells: Cell biology and potential use in therapy. Basic Clin. Pharmacol. Toxicol. 95(5):209-214; 2004.
11. Kilroy, G. E.; Foster, S. J.; Wu, X.; Ruiz, J.; Sherwood, S.; Heifetz, A.; Ludlow, J. W.; Stricker, D. M.; Potiny, S.; Green, P.; Halvorsen, Y. D.; Cheatham, B.; Storms, R. W.; Gimble, J. M. Cytokine profile of human adipose-derived stem cells: Expression of angiogenic, hematopoietic, and pro-inflammatory factors. J. Cell. Physiol. 212(3):702-709; 2007.
12. Lagasse, E.; Connors, H.; Al-Dhalimy, M.; Reitsma, M.; Dohse, M.; Osborne, L.; Wang, X.; Finegold, M.; Weissman, I. L.; Grompe, M. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med. 6(11):1229-1234; 2000.
13. Le Blanc, K.; Pittenger, M. Mesenchymal stem cells: Progress toward promise. Cytotherapy 7(1):36-45; 2005. (Pubitemid 40542402)
14. Lee, K. D.; Kuo, T. K.; Whang-Peng, J.; Chung, Y. F.; Lin, C. T.; Chou, S. H.; Chen, J. R.; Chen, Y. P.; Lee, O. K. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 40(6):1275-1284; 2004.
15. Matsumori, A.; Ono, K.; Okada, M.; Miyamoto, T.; Sato, Y.; Sasayama, S. Immediate increase in circulating hepatocyte growth factor/scatter factor by heparin. J. Mol. Cell. Cardiol. 30(10):2145-2149; 1998.
16. Matsumoto, K.; Nakamura, T. Heparin functions as a hepatotrophic factor by inducing production of hepatocyte growth factor. Biochem. Biophys. Res. Commun. 227(2):455-461; 1996.
17. Moreno, E.; Meneu, J. C.; Calvo, J.; Pérez, B.; Sesma, A. G.; Manrique, A.; Vegh, I.; Aragón, A. M.; Grau, M.; Gimeno, A.; Jiménez, C.; Gómez, R.; Moreno, A.; Abradelo, M.; García, I.; de la Calle, A. Modulation of hepatocyte growth factor plasma levels in relation to the dose of exogenous heparin administered: An experimental study in rats. Transplant. Proc. 37(9):3943-3947; 2005.
18. Naka, D.; Ishii, T.; Shimomura, T.; Hishida, T.; Hara, H. Heparin modulates the receptor-binding and mitogenic activity of hepatocyte growth factor on hepatocytes. Exp. Cell Res. 209(2):317-324; 1993.
19. Nakagami, H.; Maeda, K.; Morishita, R.; Iguchi, S.; Nishikawa, T.; Takami, Y.; Kikuchi, Y.; Saito, Y.; Tamai, K.; Ogihara, T.; Kaneda, Y. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arterioscler. Thromb. Vasc. Biol. 25(12):2542-2547; 2005.
20. Nakao, T.; Arii, S.; Kaido, T.; Mori, A.; Murata, T.; Matsumori, A.; Imamura, M. Heparin accelerates liver regeneration following portal branch ligation in normal and cirrhotic rats with increased plasma hepatocyte growth factor levels. J. Hepatol. 37(1):87-92; 2002. (Pubitemid 34713059)
21. Oh, S. H.; Miyazaki, M.; Kouchi, H.; Inoue, Y.; Sakaguchi, M.; Tsuji, T.; Shima, N.; Higashio, K.; Namba, M. Hepatocyte growth factor induces differentiation of adult rat bone marrow cells into a hepatocyte lineage in vitro. Biochem. Biophys. Res. Commun. 279(2):500-504; 2000.
22. Oishi, K.; Noguchi, H.; Yukawa, H.; Miyazaki, T.; Kato, R.; Kitagawa, Y.; Ueda, M.; Hayashi, S. Cryopreservation of mouse adipose tissue-derived stem/progenitor cells. Cell Transplant. 17(1-2):35-41; 2008. (Pubitemid 351551378)
23. Okada, M.; Matsumori, A.; Ono, K.; Miyamoto, T.; Takahashi, M.; Sasayama, S. Hepatocyte growth factor is a major mediator in heparin-induced angiogenesis. Biochem. Biophys. Res. Commun. 255(1):80-87; 1999.
24. Petersen, B. E.; Bowen, W. C.; Patrene, K. D.; Mars, W. M.; Sullivan, A. K.; Murase, N.; Boggs, S. S.; Greenberger, J. S.; Goff, J. P. Bone marrow as a potential source of hepatic oval cells. Science 284(5417):1168-1170; 1999.
25. Puissant, B.; Barreau, C.; Bourin, P.; Clavel, C.; Corre, J.; Bousquet, C.; Taureau, C.; Cousin, B.; Abbal, M.; Laharrague, P.; Penicaud, L.; Casteilla, L.; Blancher, A. Immunomodulatory effect of human adipose tissue-derived adult stem cells: Comparison with bone marrow mesenchymal stem cells. Br. J. Haematol. 129(1):118-129; 2005.
26. Rehman, J.; Traktuev, D.; Li, J.; Merfeld-Clauss, S.; Temm-Grove, C. J.; Bovenkerk, J. E.; Pell, C. L.; Johnstone, B. H.; Considine, R. V.; March, K. L. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109(10):1292-1298; 2004.
27. Sakaida, I.; Terai, S.; Yamamoto, N.; Aoyama, K.; Ishikawa, T.; Nishina, H.; Okita, K. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. Hepatology 40(6):1304-1311; 2004. (Pubitemid 39657004)
28. Salbach, P. B.; Brückmann, M.; Turovets, O.; Kreuzer, J.; Kübler, W.; Walter-Sack, I. Heparin-mediated selective release of hepatocyte growth factor in humans. Br. J. Clin. Pharmacol. 50(3):221-226; 2000.
29. Sanchez-Ramos, J.; Song, S.; Cardozo-Pelaez, F.; Hazzi, C.; Stedeford, T.; Willing, A.; Freeman, T. B.; Saporta, S.; Janssen, W.; Patel, N.; Cooper, D. R.; Sanberg, P. R. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 164(2):247-256; 2000.
30. Schwartz, R. E.; Reyes, M.; Koodie, L.; Jiang, Y.; Blackstad, M.; Lund, T.; Lenvik, T.; Johnson, S.; Hu, W. S.; Verfaillie, C. M. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J. Clin. Invest. 109(10):1291-1302; 2002.
31. Seo, M. J.; Suh, S. Y.; Bae, Y. C.; Jung, J. S. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem. Biophys. Res. Commun. 328(1):258-264; 2005.
32. Sgodda, M.; Aurich, H.; Kleist, S.; Aurich, I.; König, S.; Dollinger, M. M.; Fleig, W. E.; Christ, B. Hepatocyte differentiation of mesenchymal stem cells from rat peritoneal adipose tissue in vitro and in vivo. Exp. Cell Res. 313(13):2875-2886; 2007.
33. Shu, S. N.; Wei, L.; Wang, J. H.; Zhan, Y. T.; Chen, H. S.; Wang, Y. Hepatic differentiation capability of rat bone marrow-derived mesenchymal stem cells and hematopoietic stem cells. World J. Gastroenterol. 10(19):2818-2822; 2004.
34. Stamm, C.; Westphal, B.; Kleine, H. D.; Petzsch, M.; Kittner, C.; Klinge, H.; Schümichen, C.; Nienaber, C. A.; Freund, M.; Steinhoff, G. Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361(9351):45-46; 2003. (Pubitemid 36050962)
35. Tateishi-Yuyama, E.; Matsubara, H.; Murohara, T.; Ikeda, U.; Shintani, S.; Masaki, H.; Amano, K.; Kishimoto, Y.; Yoshimoto, K.; Akashi, H.; Shimada, K.; Iwasaka, T.; Imaizumi, T.; Therapeutic Angiogenesis Using Cell Transplantation (TACT) Study Investigators. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: A pilot study and a randomised controlled trial. Lancet 360(9331):427-435; 2002.
36. 4 model - translational research project: The development of cell therapy using autologous bone marrow cells in patients with liver cirrhosis. J. Hepatobiliary Pancreat. Surg. 12(3):203-207; 2005.
37. Theise, N. D.; Badve, S.; Saxena, R.; Henegariu, O.; Sell, S.; Crawford, J. M.; Krause, D. S. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31(1):235-240; 2000.
38. Traktuev, D. O.; Merfeld-Clauss, S.; Li, J.; Kolonin, M.; Arap, W.; Pasqualini, R.; Johnstone, B. H.; March, K. L. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ. Res. 102(1):77-85; 2008.
39. Vassilopoulos, G.; Wang, P. R.; Russell, D. W. Transplanted bone marrow regenerates liver by cell fusion. Nature 422(6934):901-904; 2003.
40. Wang, X.; Willenbring, H.; Akkari, Y.; Torimaru, Y.; Foster, M.; Al-Dhalimy, M.; Lagasse, E.; Finegold, M.; Olson, S.; Grompe, M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422(6934):897-901; 2003. (Pubitemid 36520042)
41. Wexler, S. A.; Donaldson, C.; Denning-Kendall, P.; Rice, C.; Bradley, B.; Hows, J. M. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br. J. Haematol. 121(2):368-374; 2003.
42. Woodbury, D.; Schwarz, E. J.; Prockop, D. J.; Black, I. B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61(4):364-370; 2000.
43. Yukawa, H.; Noguchi, H.; Oishi, K.; Miyazaki, T.; Kitagawa, Y.; Inoue, M.; Hasegawa, M.; Hayashi, S. Recombinant sendai virus-mediated gene transfer to adipose tissue-derived stem cells (ASCs). Cell Transplant. 17(1-2):43-50; 2008. (Pubitemid 351551379)