Hepatocyte differentiation of mesenchymal stem cells

Hepatobiliary and Pancreatic Diseases International

Volumn 11, Issue 4, 2012, Pages 360-371

  Wu, Xu Bo ^a   Tao, Ran ^b  

^a The Central Hospital of Minhang District   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Differentiation; Hepatocyte; Mesenchymal stem cells; References

Indexed keywords

CYTOKINE; HORMONE; TRANSCRIPTION FACTOR;

CELL CULTURE; CELL DIFFERENTIATION; CLINICAL TRIAL; COCULTURE; HUMAN; IMMUNOLOGY; IN VIVO STUDY; LIVER CELL; LIVER DISEASE; LIVER REGENERATION; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PATIENT SAFETY; REVIEW;

EID: 84865139200     PISSN: 14993872     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1499-3872(12)60193-3     Document Type: Review

References (95)

1. Eckersley-Maslin MA, Warner FJ, Grzelak CA, McCaughan GW, Shackel NA. Bone marrow stem cells and the liver: are they relevant? J Gastroenterol Hepatol 2009;24:1608-1616.
2. Colter DC, Class R, DiGirolamo CM, Prockop DJ. Rapid expansion of recycling stem cells in cultures of plasticadherent cells from human bone marrow. Proc Natl Acad Sci U S A 2000;97:3213-3218.
3. Le Blanc K, Ringdén O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 2007;262:509-525.
4. Swenson ES, Kuwahara R, Krause DS, Theise ND. Physiological variations of stem cell factor and stromal-derived factor-1 in murine models of liver injury and regeneration. Liver Int 2008;28:308-318.
5. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, et al. Bone marrow as a potential source of hepatic oval cells. Science 1999;284:1168-1170.
6. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6:1229-1234.
7. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49.
8. Jang YY, Collector MI, Baylin SB, Diehl AM, Sharkis SJ. Hematopoietic stem cells convert into liver cells within days without fusion. Nat Cell Biol 2004;6:532-539.
9. di Bonzo LV, Ferrero I, Cravanzola C, Mareschi K, Rustichell D, Novo E, et al. Human mesenchymal stem cells as a twoedged sword in hepatic regenerative medicine: engraftment and hepatocyte differentiation versus profibrogenic potential. Gut 2008;57:223-231.
10. Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, et al. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 2002;109:1291-1302.
11. Lee KD, Kuo TK, Whang-Peng J, Chung YF, Lin CT, Chou SH, et al. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 2004;40:1275-1284.
12. Anjos-Afonso F, Siapati EK, Bonnet D. In vivo contribution of murine mesenchymal stem cells into multiple cell-types under minimal damage conditions. J Cell Sci 2004;117:5655-5664.
13. Aurich I, Mueller LP, Aurich H, Luetzkendorf J, Tisljar K, Dollinger MM, et al. Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 2007;56:405-415.
14. Christ B, Dollinger MM. The generation of hepatocytes from mesenchymal stem cells and engraftment into the liver. Curr Opin Organ Transplant 2010 Dec 9.
15. Ochiya T, Yamamoto Y, Banas A. Commitment of stem cells into functional hepatocytes. Differentiation 2010;79:65-73.
16. Xie C, Zheng YB, Zhu HP, Peng L, Gao ZL. Human bone marrow mesenchymal stem cells are resistant to HBV infection during differentiation into hepatocytes in vivo and in vitro. Cell Biol Int 2009;33:493-500.
17. Shu SN, Wei L, Wang JH, Zhan YT, Chen HS, Wang Y. Hepatic differentiation capability of rat bone marrow-derived mesenchymal stem cells and hematopoietic stem cells. World J Gastroenterol 2004;10:2818-2822.
18. Baertschiger RM, Serre-Beinier V, Morel P, Bosco D, Peyrou M, Clément S, et al. Fibrogenic potential of human multipotent mesenchymal stromal cells in injured liver. PLoS One 2009;4: e6657.
19. Seo MJ, Suh SY, Bae YC, Jung JS. Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochem Biophys Res Commun 2005;328:258-264.
20. Sgodda M, Aurich H, Kleist S, Aurich I, König S, Dollinger MM, et al. Hepatocyte differentiation of mesenchymal stem cells from rat peritoneal adipose tissue in vitro and in vivo. Exp Cell Res 2007;313:2875-2886.
21. Aurich H, Sgodda M, Kaltwasser P, Vetter M, Weise A, Liehr T, et al. Hepatocyte differentiation of mesenchymal stem cells from human adipose tissue in vitro promotes hepatic integration in vivo. Gut 2009;58:570-581.
22. Hong SH, Gang EJ, Jeong JA, Ahn C, Hwang SH, Yang IH, et al. In vitro differentiation of human umbilical cord bloodderived mesenchymal stem cells into hepatocyte-like cells. Biochem Biophys Res Commun 2005;330:1153-1161.
23. Kang XQ, Zang WJ, Bao LJ, Li DL, Song TS, Xu XL, et al. Fibroblast growth factor-4 and hepatocyte growth factor induce differentiation of human umbilical cord bloodderived mesenchymal stem cells into hepatocytes. World J Gastroenterol 2005;11:7461-7465.
24. Ling L, Ni Y, Wang Q, Wang H, Hao S, Hu Y, et al. Transdifferentiation of mesenchymal stem cells derived from human fetal lung to hepatocyte-like cells. Cell Biol Int 2008; 32:1091-1098.
25. Cho KA, Ju SY, Cho SJ, Jung YJ, Woo SY, Seoh JY, et al. Mesenchymal stem cells showed the highest potential for the regeneration of injured liver tissue compared with other subpopulations of the bone marrow. Cell Biol Int 2009;33: 772-777.
26. Snykers S, Vanhaecke T, Papeleu P, Luttun A, Jiang Y, Vander Heyden Y, et al. Sequential exposure to cytokines reflecting embryogenesis: the key for in vitro differentiation of adult bone marrow stem cells into functional hepatocyte-like cells. Toxicol Sci 2006;94:330-341; discussion 235-239.
27. Taléns-Visconti R, Bonora A, Jover R, Mirabet V, Carbonell F, Castell JV, et al. Human mesenchymal stem cells from adipose tissue: Differentiation into hepatic lineage. Toxicol In Vitro 2007;21:324-329.
28. Forte G, Minieri M, Cossa P, Antenucci D, Sala M, Gnocchi V, et al. Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 2006;24:23-33.
29. Ruhnke M, Ungefroren H, Zehle G, Bader M, Kremer B, Fändrich F. Long-term culture and differentiation of rat embryonic stem cell-like cells into neuronal, glial, endothelial, and hepatic lineages. Stem Cells 2003;21:428-436.
30. Chivu M, Dima SO, Stancu CI, Dobrea C, Uscatescu V, Necula LG, et al. In vitro hepatic differentiation of human bone marrow mesenchymal stem cells under differential exposure to liver-specific factors. Transl Res 2009;154:122-132.
31. Kinoshita T, Sekiguchi T, Xu MJ, Ito Y, Kamiya A, Tsuji K, et al. Hepatic differentiation induced by oncostatin M attenuates fetal liver hematopoiesis. Proc Natl Acad Sci U S A 1999;96:7265-7270.
32. Lysy PA, Smets F, Najimi M, Sokal EM. Leukemia inhibitory factor contributes to hepatocyte-like differentiation of human bone marrow mesenchymal stem cells. Differentiation 2008; 76:1057-1067.
33. Sato F, Mitaka T, Mizuguchi T, Mochizuki Y, Hirata K. Effects of nicotinamide-related agents on the growth of primary rat hepatocytes and formation of small hepatocyte colonies. Liver 1999;19:481-488.
34. Zhang Q, Chen X, Gui G, Zheng W. Spheroid formation and differentiation into hepatocyte-like cells of rat mesenchymal stem cell induced by co-culture with liver cells. DNA Cell Biol 2007;26:497-503.
35. Lange C, Bruns H, Kluth D, Zander AR, Fiegel HC. Hepatocytic differentiation of mesenchymal stem cells in cocultures with fetal liver cells. World J Gastroenterol 2006; 12:2394-2397.
36. Chen Y, Dong XJ, Zhang GR, Shao JZ, Xiang LX. In vitro differentiation of mouse bone marrow stromal stem cells into hepatocytes induced by conditioned culture medium of hepatocytes. J Cell Biochem 2007;102:52-63.
37. Yamazaki S, Miki K, Hasegawa K, Sata M, Takayama T, Makuuchi M. Sera from liver failure patients and a demethylating agent stimulate transdifferentiation of murine bone marrow cells into hepatocytes in coculture with nonparenchymal liver cells. J Hepatol 2003;39:17-23.
38. Deng X, Chen YX, Zhang X, Zhang JP, Yin C, Yue HY, et al. Hepatic stellate cells modulate the differentiation of bone marrow mesenchymal stem cells into hepatocyte-like cells. J Cell Physiol 2008;217:138-144.
39. Tao XR, Li WL, Su J, Jin CX, Wang XM, Li JX, et al. Clonal mesenchymal stem cells derived from human bone marrow can differentiate into hepatocyte-like cells in injured livers of SCID mice. J Cell Biochem 2009;108:693-704.
40. Lu HF, Chua KN, Zhang PC, Lim WS, Ramakrishna S, Leong KW, et al. Three-dimensional co-culture of rat hepatocyte spheroids and NIH/3T3 fibroblasts enhances hepatocyte functional maintenance. Acta Biomater 2005;1:399-410.
41. Thomas RJ, Bhandari R, Barrett DA, Bennett AJ, Fry JR, Powe D, et al. The effect of three-dimensional co-culture of hepatocytes and hepatic stellate cells on key hepatocyte functions in vitro. Cells Tissues Organs 2005;181:67-79.
42. Hanada S, Kayano H, Jiang J, Kojima N, Miyajima A, Sakoda A, et al. Enhanced in vitro maturation of subcultivated fetal human hepatocytes in three dimensional culture using poly-L-lactic acid scaffolds in the presence of oncostatin M. Int J Artif Organs 2003;26:943-951.
43. Kudryavtseva EI, Engelhardt NV. Requirement of 3D extracellular network for maintenance of mature hepatocyte morphology and suppression of alpha-fetoprotein synthesis in vitro. Immunol Lett 2003;90:25-31.
44. Kazemnejad S, Allameh A, Soleimani M, Gharehbaghian A, Mohammadi Y, Amirizadeh N, et al. Biochemical and molecular characterization of hepatocyte-like cells derived from human bone marrow mesenchymal stem cells on a novel three-dimensional biocompatible nanofibrous scaffold. J Gastroenterol Hepatol 2009;24:278-287.
45. Lin N, Lin J, Bo L, Weidong P, Chen S, Xu R. Differentiation of bone marrow-derived mesenchymal stem cells into hepatocyte-like cells in an alginate scaffold. Cell Prolif 2010; 43:427-434.
46. Ishii K, Yoshida Y, Akechi Y, Sakabe T, Nishio R, Ikeda R, et al. Hepatic differentiation of human bone marrow-derived mesenchymal stem cells by tetracycline-regulated hepatocyte nuclear factor 3beta. Hepatology 2008;48:597-606.
47. Sato Y, Araki H, Kato J, Nakamura K, Kawano Y, Kobune M, et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005;106:756-763.
48. Dai LJ, Li HY, Guan LX, Ritchie G, Zhou JX. The therapeutic potential of bone marrow-derived mesenchymal stem cells on hepatic cirrhosis. Stem Cell Res 2009;2:16-25.
49. Hardjo M, Miyazaki M, Sakaguchi M, Masaka T, Ibrahim S, Kataoka K, et al. Suppression of carbon tetrachloride-induced liver fibrosis by transplantation of a clonal mesenchymal stem cell line derived from rat bone marrow. Cell Transplant 2009;18:89-99.
50. Yagi H, Parekkadan B, Suganuma K, Soto-Gutierrez A, Tompkins RG, Tilles AW, et al. Long-term superior performance of a stem cell/hepatocyte device for the treatment of acute liver failure. Tissue Eng Part A 2009;15:3377-3388.
51. Dan YY. Bioengineering the artificial liver with non-hepatic cells: where are we headed? J Gastroenterol Hepatol 2009;24: 171-173
52. Stock P, Staege MS, Müller LP, Sgodda M, Völker A, Volkmer I, et al. Hepatocytes derived from adult stem cells. Transplant Proc 2008;40:620-623.
53. Pournasr B, Mohamadnejad M, Bagheri M, Aghdami N, Shahsavani M, Malekzadeh R, et al. In vitro differentiation of human bone marrow mesenchymal stem cells into hepatocyte-like cells. Arch Iran Med 2011;14:244-249.
54. Campard D, Lysy PA, Najimi M, Sokal EM. Native umbilical cord matrix stem cells express hepatic markers and differentiate into hepatocyte-like cells. Gastroenterology 2008;134:833-848.
55. Wang X, Willenbring H, Akkari Y, Torimaru Y, Foster M, Al-Dhalimy M, et al. Cell fusion is the principal source of bonemarrow-derived hepatocytes. Nature 2003;422:897-901.
56. Asawa S, Saito T, Satoh A, Ohtake K, Tsuchiya T, Okada H, et al. Participation of bone marrow cells in biliary fibrosis after bile duct ligation. J Gastroenterol Hepatol 2007;22:2001-2008.
57. Khurana S, Mukhopadhyay A. Characterization of the potential subpopulation of bone marrow cells involved in the repair of injured liver tissue. Stem Cells 2007;25:1439-1447.
58. Asano Y, Iimuro Y, Son G, Hirano T, Fujimoto J. Hepatocyte growth factor promotes remodeling of murine liver fibrosis, accelerating recruitment of bone marrow-derived cells into the liver. Hepatol Res 2007;37:1080-1094.
59. Kienstra KA, Jackson KA, Hirschi KK. Injury mechanism dictates contribution of bone marrow-derived cells to murine hepatic vascular regeneration. Pediatr Res 2008;63:131-136.
60. Allameh A, Esmaeli S, Kazemnejad S, Soleimani M. Differential expression of glutathione S-transferases P1-1 and A1-1 at protein and mRNA levels in hepatocytes derived from human bone marrow mesenchymal stem cells. Toxicol In Vitro 2009;23:674-679.
61. Yamamoto Y, Banas A, Murata S, Ishikawa M, Lim CR, Teratani T, et al. A comparative analysis of the transcriptome and signal pathways in hepatic differentiation of human adipose mesenchymal stem cells. FEBS J 2008;275:1260-1273.
62. Ke Z, Zhou F, Wang L, Chen S, Liu F, Fan X, et al. Downregulation of Wnt signaling could promote bone marrowderived mesenchymal stem cells to differentiate into hepatocytes. Biochem Biophys Res Commun 2008;367:342-348.
63. Milhem M, Mahmud N, Lavelle D, Araki H, DeSimone J, Saunthararajah Y, et al. Modification of hematopoietic stem cell fate by 5aza 2'deoxycytidine and trichostatin A. Blood 2004;103:4102-4110.
64. Snykers S, Vanhaecke T, De Becker A, Papeleu P, Vinken M, Van Riet I, et al. Chromatin remodeling agent trichostatin A: a key-factor in the hepatic differentiation of human mesenchymal stem cells derived of adult bone marrow. BMC Dev Biol 2007;7:24.
65. Chen L, Tredget EE, Liu C, Wu Y. Analysis of allogenicity of mesenchymal stem cells in engraftment and wound healing in mice. PLoS One 2009;4:e7119.
66. Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, et al. T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci 2005;12:47-57.
67. Griffin MD, Ritter T, Mahon BP. Immunological aspects of allogeneic mesenchymal stem cell therapies. Hum Gene Ther 2010;21:1641-1655.
68. Fibbe WE, Nauta AJ, Roelofs H. Modulation of immune responses by mesenchymal stem cells. Ann N Y Acad Sci. 2007;1106:272-278.
69. Crop MJ, Korevaar SS, de Kuiper R, Ijzermans JN, van Besouw NM, Baan CC, et al. Human mesenchymal stem cells are susceptible to lysis by CD8+ T-cells and NK cells. Cell Transplant 2011 Mar 7.
70. Yang XF. Immunology of stem cells and cancer stem cells. Cell Mol Immunol 2007;4:161-171.
71. Huang XP, Sun Z, Miyagi Y, McDonald Kinkaid H, Zhang L, Weisel RD, et al. Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 2010;122:2419-2429.
72. Technau A, Froelich K, Hagen R, Kleinsasser N. Adipose tissue-derived stem cells show both immunogenic and immunosuppressive properties after chondrogenic differentiation. Cytotherap 2011;13:310-317.
73. Goren A, Dahan N, Goren E, Baruch L, Machluf M. Encapsulated human mesenchymal stem cells: a unique hypoimmunogenic platform for long-term cellular therapy. FASEB J 2010;24:22-31.
74. de la Garza-Rodea AS, Verweij MC, Boersma H, van der Velde-van Dijke I, de Vries AA, Hoeben RC, et al. Exploitation of herpesvirus immune evasion strategies to modify the immunogenicity of human mesenchymal stem cell transplants. PLoS One 2011;6:e14493.
75. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499-3506.
76. Zhang B, Liu R, Shi D, Liu X, Chen Y, Dou X, et al. Mesenchymal stem cells induce mature dendritic cells into a novel Jagged-2-dependent regulatory dendritic cell population. Blood 2009;113:46-57.
77. Aldinucci A, Rizzetto L, Pieri L, Nosi D, Romagnoli P, Biagioli T, et al. Inhibition of immune synapse by altered dendritic cell actin distribution: a new pathway of mesenchymal stem cell immune regulation. J Immunol 2010; 185:5102-5110.
78. Zhao S, Wehner R, Bornhäuser M, Wassmuth R, Bachmann M, Schmitz M. Immunomodulatory properties of mesenchymal stromal cells and their therapeutic consequences for immune-mediated disorders. Stem Cells Dev 2010;19:607-614.
79. Cui L, Yin S, Liu W, Li N, Zhang W, Cao Y. Expanded adipose-derived stem cells suppress mixed lymphocyte reaction by secretion of prostaglandin E2. Tissue Eng 2007; 13:1185-1195.
80. Barry FP, Murphy JM, English K, Mahon BP. Immunogenicity of adult mesenchymal stem cells: lessons from the fetal allograft. Stem Cells Dev 2005;14:252-265.
81. Ringden O, Le Blanc K. Mesenchymal stem cells for treatment of acute and chronic graft-versus-host disease, tissue toxicity and hemorrhages. Best Pract Res Clin Haematol 2011;24:65-72.
82. Ge W, Jiang J, Baroja ML, Arp J, Zassoko R, Liu W, et al. Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft tolerance. Am J Transplant 2009;9:1760-1772.
83. Newman RE, Yoo D, LeRoux MA, Danilkovitch-Miagkova A. Treatment of inflammatory diseases with mesenchymal stem cells. Inflamm Allergy Drug Targets 2009;8:110-123.
84. Mohamadnejad M, Alimoghaddam K, Mohyeddin-BonabM, Bagheri M, Bashtar M, Ghanaati H, et al. Phase 1 trial of autologous bone marrow mesenchymal stem cell transplantation in patients with decompensated liver cirrhosis. Arch Iran Med 2007;10:459-466.
85. Sawada R, Ito T, Tsuchiya T. Safety evaluation of tissue engineered medical devices using normal human mesenchymal stem cells. Yakugaku Zasshi 2007;127:851-856.
86. Russo FP, Alison MR, Bigger BW, Amofah E, Florou A, Amin F, et al. The bone marrow functionally contributes to liver fibrosis. Gastroenterology 2006;130:1807-1821.
87. Sharma AD, Cantz T, Richter R, Eckert K, Henschler R, Wilkens L, et al. Human cord blood stem cells generate human cytokeratin 18-negative hepatocyte-like cells in injured mouse liver. Am J Pathol 2005;167:555-564.
88. Shi XL, Zhang Y, Gu JY, Ding YT. Coencapsulation of hepatocytes with bone marrow mesenchymal stem cells improves hepatocyte-specific functions. Transplantation 2009;88:1178-1185.
89. Jung KH, Shin HP, Lee S, Lim YJ, Hwang SH, Han H, et al. Effect of human umbilical cord blood-derived mesenchymal stem cells in a cirrhotic rat model. Liver Int 2009;29:898-909.
90. Banas A, Teratani T, Yamamoto Y, Tokuhara M, Takeshita F, Osaki M, et al. IFATS collection: in vivo therapeutic potential of human adipose tissue mesenchymal stem cells after transplantation into mice with liver injury. Stem Cells 2008;26:2705-2712.
91. Kuo TK, Hung SP, Chuang CH, Chen CT, Shih YR, Fang SC, et al. Stem cell therapy for liver disease: parameters governing the success of using bone marrow mesenchymal stem cells. Gastroenterology 2008;134:2111-2121, 2121.e1-3.
92. van Poll D, Parekkadan B, Cho CH, Berthiaume F, Nahmias Y, Tilles AW, et al. Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo. Hepatology 2008;47:1634-1643.
93. Oyagi S, Hirose M, Kojima M, Okuyama M, Kawase M, Nakamura T, et al. Therapeutic effect of transplanting HGFtreated bone marrow mesenchymal cells into CCl4-injured rats. J Hepatol 2006;44:742-748.
94. Choi D, Kim JH, Lim M, Song KW, Paik SS, Kim SJ, et al. Hepatocyte-like cells from human mesenchymal stem cells engrafted in regenerating rat liver tracked with in vivo magnetic resonance imaging. Tissue Eng Part C Methods 2008;14:15-23.
95. Okumoto K, Saito T, Haga H, Hattori E, Ishii R, Karasawa T, et al. Characteristics of rat bone marrow cells differentiated into a liver cell lineage and dynamics of the transplanted cells in the injured liver. J Gastroenterol 2006;41:62-69.