Clonal mesenchymal stem cells derived from human bone marrow can differentiate into hepatocyte-like cells in injured livers of scid mice

Journal of Cellular Biochemistry

Volumn 108, Issue 3, 2009, Pages 693-704

  Tao, Xin Rong ^a,b   Li, Wen Lin ^a   Juan, Su ^a   Jin, Cai Xia ^a   Wang, Xin Min ^a   Li, Jian Xiu ^a   Hu, Jun Kai ^a   Xiang, Zhen Hua ^a   Lau, Joseph T Y ^c   Hu, Yi Ping ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b ANHUI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Cell therapy; Hepatic differentiation; Human mesenchymal stem cells; Stem cell transplantation

Indexed keywords

ALPHA 1 ANTITRYPSIN; CARBON TETRACHLORIDE; ENHANCED GREEN FLUORESCENT PROTEIN; HUMAN ALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENGRAFTMENT; HEMATOPOIETIC STEM CELL; HEPATOCYTE TRANSPLANTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; LIVER INJURY; LIVER PARENCHYMA; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SCID MOUSE;

ANIMALS; BIOLOGICAL MARKERS; BONE MARROW CELLS; CARBON TETRACHLORIDE; CELL DIFFERENTIATION; CELL FUSION; CELL LINEAGE; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; CLONE CELLS; DNA; HEPATOCYTES; HUMANS; LIVER; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, SCID; PLOIDIES;

MUS;

EID: 70350176493     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22306     Document Type: Article

References (46)

1. Aurich I, Mueller LP, Aurich H, Luetzkendorf J, Tisljar K, Dollinger MM, Schormann W, Walldorf J, Hengstler JG, Fleig WE, Christ B. 2007. Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 56:405-415. (Pubitemid 46579773)
2. Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, Miller L, Guetta E, Zipori D, Kedes LH, Kloner RA, Leor J. 2003. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 108:863-868. (Pubitemid 37022130)
3. Boyd NL, Robbins KR, Dhara SK, West FD, Stice SL. 2009. Human embryonic stem cell-derived mesoderm-like epithelium transitions to mesenchymal progenitor cells. Tissue Eng Part A [Ahead of print] DOI: 10.1089/ten. tea.2008.0351.
4. Bruno S, Bussolati B, Grange C, Collino F, Verdun Cantogno L, Herrera MB, Biancone L, Tetta C, Segoloni G, Camussi G. 2009. Isolation and characterization of resident mesenchymal stem cells in human glomeruli. Stem Cells Dev 18:867-880.
5. Chamberlain J, Yamagami T, Colletti E, Theise ND, Desai J, Frias A, Pixley J, Zanjani ED, Porada CD, Almeida-Porada G. 2007. Efficient generation of human hepatocytes by the intrahepatic delivery of clonal human mesenchymal stem cells in fetal sheep. Hepatology 46:1935-1945.
6. Coleman WB, McCullough KD, Esch GL, Faris RA, Hixson DC, Smith GJ, Grisham JW. 1997. Evaluation of the differentiation potential of WB-F344 rat liver epithelial stem-like cells in vivo. Differentiation to hepatocytes after transplantation into dipeptidylpeptidase-IV-deficient rat liver. Am J Pathol 151:353-359.
7. Colter DC, Sekiya I, Prockop DJ. 2001. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci USA 98:7841-7845. (Pubitemid 32642648)
8. Dahlke MH, Popp FC, Larsen S, Schlitt HJ, Rasko JE. 2004. Stem cell therapy of the liver - Fusion or fiction? Liver Transpl 10:471-479.
9. D'Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC. 2004. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 117:2971-2981. (Pubitemid 39117672)
10. Dirks C, Miller AD. 2001. Many nonmammalian cells exhibit postentry blocks to transduction by gammaretroviruses pseudotyped with various viral envelopes, including vesicular stomatitis virus G glycoprotein. J Virol 75: 6375-6383. (Pubitemid 32578156)
11. Fang B, Shi M, Liao L, Yang S, Liu Y, Zhao RC. 2004. Systemic infusion of FLK1(+) mesenchymal stem cells ameliorate carbon tetrachloride-induced liver fibrosis in mice. Transplantation 78:83-88. (Pubitemid 38938288)
12. Gerdes HH, Bukoreshtliev NV, Barroso JF. 2007. Tunneling nanotubes: A new route for the exchange of components between animal cells. FEBS Lett 581:2194-2201.
13. Gupta S, Chowdhury JR. 2002. Therapeutic potential of hepatocyte transplantation. Semin Cell Dev Biol 13:439-446.
14. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. 2002. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896-904. (Pubitemid 34845893)
15. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49. (Pubitemid 34742565)
16. Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, Markham AF, Jack A, Emery P, McGonagle D. 2002. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349-3360. (Pubitemid 35453547)
17. Kakinuma S, Tanaka Y, Chinzei R, Watanabe M, Shimizu-Saito K, Hara Y, Teramoto K, Arii S, Sato C, Takase K, Yasumizu T, Teraoka H. 2003. Human umbilical cord blood as a source of transplantable hepatic progenitor cells. Stem Cells 21:217-227. (Pubitemid 36331764)
18. Kollet O, Shivtiel S, Chen YQ, Suriawinata J, Thung SN, Dabeva MD, Kahn J, Spiegel A, Dar A, Samira S, Goichberg P, Kalinkovich A, Arenzana-Seisdedos F, Nagler A, Hardan I, Revel M, Shafritz DA, Lapidot T. 2003. HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. J Clin Invest 112:160-169. (Pubitemid 38056352)
19. Koyanagi M, Brandes RP, Haendeler J, Zeiher AM, Dimmeler S. 2005. Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: A novel mechanism for cell fate changes? Circ Res 96:1039-1041.
20. Kuo TK, Hung SP, Chuang CH, Chen CT, Shih YR, Fang SC, Yang VW, Lee OK. 2008. Stem cell therapy for liver disease: Parameters governing the success of using bone marrow mesenchymal stem cells. Gastroenterology 134:2111-2121.
21. Lagasse E, Connors H, Al Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. 2000. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:1229-1234. (Pubitemid 30950849)
22. Lee KD, Kuo TK, Whang-Peng J, Chung YF, Lin CT, Chou SH, Chen JR, Chen YP, Lee OK. 2004. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 40:1275-1284.
23. Malhi H, Irani AN, Gagandeep S, Gupta S. 2002. Isolation of human progenitor liver epithelial cells with extensive replication capacity and differentiation into mature hepatocytes. J Cell Sci 115:2679-2688. (Pubitemid 34846509)
24. Munoz-Elias G, Marcus AJ, Coyne TM, Woodbury D, Black IB. 2004. Adult bone marrow stromal cells in the embryonic brain: Engraftment, migration, differentiation, and long-term survival. J Neurosci 24:4585-4595. (Pubitemid 38656614)
25. Newsome PN, Johannessen I, Boyle S, Dalakas E, McAulay KA, Samuel K, Rae F, Forrester L, Turner ML, Hayes PC, Harrison DJ, Bickmore WA, Plevris JN. 2003. Human cord blood-derived cells can differentiate into hepatocytes in the mouse liver with no evidence of cellular fusion. Gastroenterology 124:1891-1900. (Pubitemid 36666784)
26. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. 1999. Bone marrow as a potential source of hepatic oval cells. Science 284:1168-1170. (Pubitemid 29288406)
27. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147. (Pubitemid 29282067)
28. Plotnikov EY, Khryapenkova TG, Vasileva AK, Marey MV, Galkina SI, Isaev NK, Sheval EV, Polyakov VY, Sukhikh GT, Zorov DB. 2008. Cell-to-cell cross-t alk between mesenchymal stem cells and cardiomyocytes in coculture. J Cell Mol Med 12:1622-1631.
29. Pochampally RR, Smith JR, Ylostalo J, Prockop DJ. 2004. Serum deprivation of human marrow stromal cells (hMSCs) selects for a subpopulation of early progenitor cells with enhanced expression of OCT-4 and other embryonic genes. Blood 103:1647-1652. (Pubitemid 38268955)
30. Pozzobon M, Piccoli M, Ditadi A, Bollini S, Destro R, André-Schmutz I, Masiero L, Lenzini E, Zanesco L, Petrelli L, Cavazzana-Calvo M, Gazzola MV, De Coppi P. 2009. Mesenchymal stromal cells can be derived from bone marrow CD133(+) cells: Implications for therapy. Stem Cells Dev 18:497-510.
31. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM. 2001. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98:2615-2625.
32. Rhim JA, Sandgren EP, Degen JL, Palmiter RD, Brinster RL. 1994. Replacement of diseased mouse liver by hepatic cell transplantation. Science 263: 1149-1152.
33. Richards M, Tan SP, Tan JH, Chan WK, Bongso A. 2004. The transcriptome profile of human embryonic stem cells as defined by SAGE. Stem Cells 22:51-64. (Pubitemid 38018781)
34. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes HH. 2004. Nanotubular highways for intercellular organelle transport. Science 303:1007-1010. (Pubitemid 38209703)
35. Sakaida I, Terai S, Yamamoto N, Aoyama K, Ishikawa T, Nishina H, Okita K. 2004. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. Hepatology 40:1304-1311. (Pubitemid 39657004)
36. Sato Y, Araki H, Kato J, Nakamura K, Kawano Y, Kobune M, Sato T, Miyanishi K, Takayama T, Takahashi M, Takimoto R, Iyama S, Matsunaga T, Ohtani S, Matsuura A, Hamada H, Niitsu Y. 2005. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 106:756-763. (Pubitemid 40981278)
37. Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, Lenvik T, Johnson S, Hu WS, Verfaillie CM. 2002. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 109:1291-1302. (Pubitemid 34546893)
38. Strick-Marchand H, Morosan S, Charneau P, Kremsdorf D, Weiss MC. 2004. Bipotential mouse embryonic liver stem cell lines contribute to liver regeneration and differentiate as bile ducts and hepatocytes. Proc Natl Acad Sci USA 101:8360-8365. (Pubitemid 38736580)
39. Sukhikh GT, Shtil' AA. 2002. Transplantation of embryonic hepatocytes. Experimental substantiation of a new approach to the therapy of liver failure. Bull Exp Biol Med 134:519-524.
40. Suzuki A, Zheng YW, Kaneko S, Onodera M, Fukao K, Nakauchi H, Taniguchi H. 2002. Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. J Cell Biol 156:173-184. (Pubitemid 34846945)
41. Tondreau T, Meuleman N, Delforge A, Dejeneffe M, Leroy R, Massy M, Mortier C, Bron D, Lagneaux L. 2005. Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: Proliferation, Oct4 expression, and plasticity. Stem Cells 23:1105-1112. (Pubitemid 41377726)
42. Vogel W, Grünebach F, Messam CA, Kanz L, Brugger W, Bühring HJ. 2003. Heterogeneity among human bone marrow-derived mesenchymal stem cells and neural progenitor cells. Haematologica 88:126-133. (Pubitemid 37101490)
43. von Mach MA, Hengstler JG, Brulport M, Eberhardt M, Schormann W, Hermes M, Prawitt D, Zabel B, Grosche J, Reichenbach A, Muller B, Weilemann LS, Zulewski H. 2004. In vitro cultured islet-derived progenitor cells of human origin express human albumin in severe combined immunodeficiency mouse liver in vivo. Stem Cells 22:1134-1141.
44. Wang X, Ge S, McNamara G, Hao QL, Crooks GM, Nolta JA. 2003. Albumin-expressing hepatocyte-like cells develop in the livers of immune-deficient mice that received transplants of highly purified human hematopoietic stem cells. Blood 101:4201-4208. (Pubitemid 36857905)
45. Watkins SC, Salter RD. 2005. Functional connectivity between immune cells mediated by tunneling nanotubules. Immunity 23:309-318.
46. Yamamoto N, Terai S, Ohata S, Watanabe T, Omori K, Shinoda K, Miyamoto K, Katada T, Sakaida I, Nishina H, Okita K. 2004. A subpopulation of bone marrow cells depleted by a novel antibody, anti-Liv8, is useful for cell therapy to repair damaged liver. Biochem Biophys Res Commun 313:1110-1118. (Pubitemid 38050107)