Liver stem cells: A scientific and clinical perspective

Journal of Gastroenterology and Hepatology (Australia)

Volumn 23, Issue 5, 2008, Pages 687-698

  Dan, Yock Young ^a,b   Yeoh, George C ^c  

^a Dept Medicine Endocrinol Diabet   (Singapore)

^b NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Artificial liver support; Hepatology; Liver regeneration; Stem cell biology

Indexed keywords

BIOARTIFICIAL LIVER; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL FUSION; CELL SELECTION; CELL THERAPY; CORD BLOOD STEM CELL TRANSPLANTATION; DEVELOPMENTAL BIOLOGY; EMBRYONIC STEM CELL; ETHICS; EXPERIMENTAL MODEL; FETUS LIVER; GENE THERAPY; HEMATOPOIETIC STEM CELL; HORIZONTAL GENE TRANSFER; HUMAN; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; LIVER; LIVER CELL; LIVER DEVELOPMENT; LIVER FUNCTION; LIVER INJURY; LIVER REGENERATION; MESENCHYMAL STEM CELL; MICROCHIMERISM; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; SAFETY; STEM CELL; STEM CELL TRANSPLANTATION; TOXICOLOGY; TREATMENT PLANNING;

EID: 42049113047     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/j.1440-1746.2008.05383.x     Document Type: Review

References (92)

1. Fausto N. Liver regeneration and repair: hepatocytes, progenitor cells, and stem cells. Hepatology 2004 39 : 1477 87.
2. Lazaro CA, Rhim JA, Yamada Y, Fausto N. Generation of hepatocytes from oval cell precursors in culture. Cancer Res. 1998 58 : 5514 22.
3. Dunsford HA, Karnasuta C, Hunt JM, Sell S. Different lineages of chemically induced hepatocellular carcinoma in rats defined by monoclonal antibodies. Cancer Res. 1989 49 : 4894 900.
4. Theise ND, Saxena R, Portmann BC et al. The canals of Hering and hepatic stem cells in humans. Hepatology 1999 30 : 1425 33.
5. Roskams T. Different types of liver progenitor cells and their niches. J. Hepatol. 2006 45 : 1 4.
6. Lowes KN, Brennan BA, Yeoh GC, Olynyk JK. Oval cell numbers in human chronic liver diseases are directly related to disease severity. Am. J. Pathol. 1999 154 : 537 41.
7. Roskams T, Yang SQ, Koteish A et al. Oxidative stress and oval cell accumulation in mice and humans with alcoholic and nonalcoholic fatty liver disease. Am. J. Pathol. 2003 163 : 1301 11.
8. Sakaida I. Autologous bone marrow cell infusion therapy for liver cirrhosis. J. Gastroenterol. Hepatol. 2008 (in press).
9. Laurson J, Selden C, Hodgson HJ. Hepatocyte progenitors in man and in rodents - multiple pathways, multiple candidates. Int. J. Exp Pathol 2005 86 : 1 18.
10. Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990 110 : 1001 20.
11. ISSCR. Glossary, International Society for Stem Cell Research. Northbrook, IL : USA The International Society for Stem Cell Research, 2007.
12. Overturf K, al-Dhalimy M, Ou CN, Finegold M, Grompe M. Serial transplantation reveals the stem-cell-like regenerative potential of adult mouse hepatocytes. Am. J. Pathol. 1997 151 : 1273 80.
13. Tateno C, Yoshizane Y, Saito N et al. Near completely humanized liver in mice shows human-type metabolic responses to drugs. Am. J. Pathol. 2004 165 : 901 12.
14. Gordon GJ, Coleman WB, Hixson DC, Grisham JW. Liver regeneration in rats with retrorsine-induced hepatocellular injury proceeds through a novel cellular response. Am. J. Pathol. 2000 156 : 607 19.
15. Evarts RP, Nagy P, Marsden E, Thorgeirsson SS. A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 1987 8 : 1737 40.
16. Petersen BE, Zajac VF, Michalopoulos GK. Hepatic oval cell activation in response to injury following chemically induced periportal or pericentral damage in rats. Hepatology 1998 27 : 1030 8.
17. Lemire JM, Shiojiri N, Fausto N. Oval cell proliferation and the origin of small hepatocytes in liver injury induced by d-galactosamine. Am. J. Pathol. 1991 139 : 535 52.
18. Shinozuka H, Lombardi B, Sell S, Iammarino RM. Early histological and functional alterations of ethionine liver carcinogenesis in rats fed a choline-deficient diet. Cancer Res. 1978 38 : 1092 8.
19. Akhurst B, Croager EJ, Farley-Roche CA et al. A modified choline-deficient, ethionine-supplemented diet protocol effectively induces oval cells in mouse liver. Hepatology 2001 34 : 519 22.
20. Crosby HA, Kelly DA, Strain AJ. Human hepatic stem-like cells isolated using c-kit or CD34 can differentiate into biliary epithelium. Gastroenterology 2001 120 : 534 44.
21. Yovchev MI, Grozdanov PN, Zhou H, Racherla H, Guha C, Dabeva MD. Identification of adult hepatic progenitor cells capable of repopulating injured rat liver. Hepatology 2008 47 : 636 47.
22. Sicklick JK, Choi SS, Bustamante M et al. Evidence for epithelial-mesenchymal transitions in adult liver cells. Am. J. Physiol. Gastrointest Liver Physiol. 2006 291 : G575 83.
23. Fougere-Deschatrette C, Imaizumi-Scherrer T, Strick-Marchand H et al. Plasticity of hepatic cell differentiation: bipotential adult mouse liver clonal cell lines competent to differentiate in vitro and in vivo. Stem Cells 2006 24 : 2098 109.
24. Herrera MB, Bruno S, Buttiglieri S et al. Isolation and characterization of a stem cell population from adult human liver. Stem Cells 2006 24 : 2840 50.
25. Schmelzer E, Wauthier E, Reid LM. The phenotypes of pluripotent human hepatic progenitors. Stem Cells 2006 24 : 1852 8.
26. Schmelzer E, Zhang L, Bruce A et al. Human hepatic stem cells from fetal and postnatal donors. J. Exp. Med. 2007 204 : 1973 87.
27. Germain L, Blouin MJ, Marceau N. Biliary epithelial and hepatocytic cell lineage relationships in embryonic rat liver as determined by the differential expression of cytokeratins, alpha-fetoprotein, albumin, and cell surface-exposed components. Cancer Res. 1988 48 : 4909 18.
28. Rogler LE. Selective bipotential differentiation of mouse embryonic hepatoblasts in vitro. Am. J. Pathol. 1997 150 : 591 602.
29. Suzuki A, Zheng YW, Kaneko S et al. Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. J. Cell Biol. 2002 156 : 173 84.
30. Strick-Marchand H, Morosan S, Charneau P, Kremsdorf D, Weiss MC. Bipotential mouse embryonic liver stem cell lines contribute to liver regeneration and differentiate as bile ducts and hepatocytes. Proc. Natl Acad. Sci. USA 2004 101 : 8360 5.
31. Oertel M, Menthena A, Chen YQ, Shafritz DA. Properties of cryopreserved fetal liver stem/progenitor cells that exhibit long-term repopulation of the normal rat liver. Stem Cells 2006 24 : 2244 51.
32. Malhi H, Irani AN, Gagandeep S, Gupta S. Isolation of human progenitor liver epithelial cells with extensive replication capacity and differentiation into mature hepatocytes. J. Cell Sci. 2002 115 : 2679 88.
33. Nowak G, Ericzon BG, Nava S, Jaksch M, Westgren M, Sumitran-Holgersson S. Identification of expandable human hepatic progenitors which differentiate into mature hepatic cells in vivo. Gut 2005 54 : 972 9.
34. Dan YY, Riehle KJ, Lazaro C et al. Isolation of multipotent progenitor cells from human fetal liver capable of differentiating into liver and mesenchymal lineages. Proc. Natl Acad. Sci. USA 2006 103 : 9912 17.
35. Heo J, Factor VM, Uren T et al. Hepatic precursors derived from murine embryonic stem cells contribute to regeneration of injured liver. Hepatology 2006 44 : 1478 86.
36. Choi D, Oh HJ, Chang UJ et al. In vivo differentiation of mouse embryonic stem cells into hepatocytes. Cell Transplant. 2002 11 : 359 68.
37. Teratani T, Yamamoto H, Aoyagi K et al. Direct hepatic fate specification from mouse embryonic stem cells. Hepatology 2005 41 : 836 46.
38. Cai J, Zhao Y, Liu Y et al. Directed differentiation of human embryonic stem cells into functional hepatic cells. Hepatology 2007 45 : 1229 39.
39. Chen Y, Soto-Gutierrez A, Navarro-Alvarez N et al. Instant hepatic differentiation of human embryonic stem cells using activin A and a deleted variant of HGF. Cell Transplant. 2006 15 : 865 71.
40. Rambhatla L, Chiu CP, Kundu P, Peng Y, Carpenter MK. Generation of hepatocyte-like cells from human embryonic stem cells. Cell Transplant. 2003 12 : 1 11.
41. Ishii T, Yasuchika K, Fujii H et al. In vitro differentiation and maturation of mouse embryonic stem cells into hepatocytes. Exp. Cell Res. 2005 309 : 68 77.
42. Soto-Gutierrez A, Navarro-Alvarez N, Zhao D et al. Differentiation of mouse embryonic stem cells to hepatocyte-like cells by co-culture with human liver nonparenchymal cell lines. Nat. Protoc. 2007 2 : 347 56.
43. Cho CH, Parashurama N, Park EY et al. Homogeneous differentiation of hepatocyte-like cells from embryonic stem cells: applications for the treatment of liver failure. FASEB J. 2008 22 : 898 909.
44. Yamamoto H, Quinn G, Asari A et al. Differentiation of embryonic stem cells into hepatocytes: biological functions and therapeutic application. Hepatology 2003 37 : 983 93.
45. Duan Y, Catana A, Meng Y et al. Differentiation and enrichment of hepatocyte-like cells from human embryonic stem cells in vitro and in vivo. Stem Cells 2007 25 : 3058 68.
46. Kumashiro Y, Asahina K, Ozeki R et al. Enrichment of hepatocytes differentiated from mouse embryonic stem cells as a transplantable source. Transplantation 2005 79 : 550 7.
47. Soto-Gutierrez A, Kobayashi N, Rivas-Carrillo JD et al. Reversal of mouse hepatic failure using an implanted liver-assist device containing ES cell-derived hepatocytes. Nat. Biotechnol. 2006 24 : 1412 19.
48. Alison MR, Poulsom R, Jeffery R et al. Hepatocytes from non-hepatic adult stem cells. Nature 2000 406 : 257.
49. Theise ND, Badve S, Saxena R et al. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 2000 31 : 235 40.
50. Lagasse E, Connors H, Al-Dhalimy M et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat. Med. 2000 6 : 1229 34.
51. Willenbring H, Bailey AS, Foster M et al. Myelomonocytic cells are sufficient for therapeutic cell fusion in liver. Nat. Med. 2004 10 : 744 8.
52. Harris RG, Herzog EL, Bruscia EM, Grove JE, Van Arnam JS, Krause DS. Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 2004 305 : 90 3.
53. Kallis YN, Alison MR, Forbes SJ. Bone marrow stem cells and liver disease. Gut 2007 56 : 716 24.
54. Cantz T, Sharma AD, Jochheim-Richter A et al. Reevaluation of bone marrow-derived cells as a source for hepatocyte regeneration. Cell Transplant. 2004 13 : 659 66.
55. Menthena A, Deb N, Oertel M et al. Bone marrow progenitors are not the source of expanding oval cells in injured liver. Stem Cells 2004 22 : 1049 61.
56. Vig P, Russo FP, Edwards RJ et al. The sources of parenchymal regeneration after chronic hepatocellular liver injury in mice. Hepatology 2006 43 : 316 24.
57. Oh SH, Witek RP, Bae SH et al. Bone marrow-derived hepatic oval cells differentiate into hepatocytes in 2-acetylaminofluorene/partial hepatectomy-induced liver regeneration. Gastroenterology 2007 132 : 1077 87.
58. Thorgeirsson SS, Grisham JW. Hematopoietic cells as hepatocyte stem cells: a critical review of the evidence. Hepatology 2006 43 : 2 8.
59. Sakaida I, Terai S, Yamamoto N et al. Transplantation of bone marrow cells reduces CCl4-induced liver fibrosis in mice. Hepatology 2004 40 : 1304 11.
60. Oyagi S, Hirose M, Kojima M et al. Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats. J. Hepatol. 2006 44 : 742 8.
61. Fang B, Shi M, Liao L, Yang S, Liu Y, Zhao RC. Systemic infusion of FLK1(+) mesenchymal stem cells ameliorate carbon tetrachloride-induced liver fibrosis in mice. Transplantation 2004 78 : 83 8.
62. Russo FP, Alison MR, Bigger BW et al. The bone marrow functionally contributes to liver fibrosis. Gastroenterology 2006 130 : 1807 21.
63. Sensken S, Waclawczyk S, Knaupp AS et al. In vitro differentiation of human cord blood-derived unrestricted somatic stem cells towards an endodermal pathway. Cytotherapy 2007 9 : 362 78.
64. Wang Y, Nan X, Li Y et al. Induction of umbilical cord blood-derived beta2m-c-Met+ cells into hepatocyte-like cells by coculture with CFSC/HGF cells. Liver Transpl. 2005 11 : 635 43.
65. Danet GH, Luongo JL, Butler G et al. C1qRp defines a new human stem cell population with hematopoietic and hepatic potential. Proc. Natl Acad. Sci. USA 2002 99 : 10441 5.
66. Nonome K, Li XK, Takahara T et al. Human umbilical cord blood-derived cells differentiate into hepatocyte-like cells in the Fas-mediated liver injury model. Am. J. Physiol. Gastrointest. Liver Physiol. 2005 289 : G1091 9.
67. Hong SH, Gang EJ, Jeong JA et al. In vitro differentiation of human umbilical cord blood-derived mesenchymal stem cells into hepatocyte-like cells. Biochem. Biophys. Res. Commun. 2005 330 : 1153 61.
68. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004 103 : 1669 75.
69. Zeng F, Chen MJ, Baldwin DA et al. Multiorgan engraftment and differentiation of human cord blood CD34+ Lin- cells in goats assessed by gene expression profiling. Proc. Natl Acad. Sci. USA 2006 103 : 7801 6.
70. Di Campli C, Piscaglia AC, Pierelli L et al. A human umbilical cord stem cell rescue therapy in a murine model of toxic liver injury. Dig. Liver Dis. 2004 36 : 603 13.
71. Almeida-Porada G, Porada CD, Chamberlain J, Torabi A, Zanjani ED. Formation of human hepatocytes by human hematopoietic stem cells in sheep. Blood 2004 104 : 2582 90.
72. Fujino H, Hiramatsu H, Tsuchiya A et al. Human cord blood CD34+ cells develop into hepatocytes in the livers of NOD/SCID/gamma (c) null mice through cell fusion. FASEB J. 2007 21 : 3499 510.
73. Newsome PN, Johannessen I, Boyle S et al. Human cord blood-derived cells can differentiate into hepatocytes in the mouse liver with no evidence of cellular fusion. Gastroenterology 2003 124 : 1891 900.
74. Tanabe Y, Tajima F, Nakamura Y et al. Analyses to clarify rich fractions in hepatic progenitor cells from human umbilical cord blood and cell fusion. Biochem. Biophys. Res. Commun. 2004 324 : 711 18.
75. Lee KD, Kuo TK, Whang-Peng J et al. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 2004 40 : 1275 84.
76. Aurich I, Mueller LP, Aurich H et al. Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 2007 56 : 405 15.
77. Banas A, Teratani T, Yamamoto Y et al. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 2007 46 : 219 28.
78. Habibullah CM, Syed IH, Qamar A, Taher-Uz Z. Human fetal hepatocyte transplantation in patients with fulminant hepatic failure. Transplantation 1994 58 : 951 2.
79. Strom SC, Fisher RA, Thompson MT et al. Hepatocyte transplantation as a bridge to orthotopic liver transplantation in terminal liver failure. Transplantation 1997 63 : 559 69.
80. Fox IJ, Chowdhury JR, Kaufman SS et al. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N. Engl. J. Med. 1998 338 : 1422 6.
81. Dhawan A, Mitry RR, Hughes RD. Hepatocyte transplantation for liver-based metabolic disorders. J. Inherited Metabolic Dis. 2006 29 : 431 5.
82. am Esch JS Knoefel WT, Klein M et al. Portal application of autologous CD133+ bone marrow cells to the liver: a novel concept to support hepatic regeneration. Stem Cells 2005 23 : 463 70.
83. Terai S, Ishikawa T, Omori K et al. Improved liver function in patients with liver cirrhosis after autologous bone marrow cell infusion therapy. Stem Cells 2006 24 : 2292 8.
84. Gordon MY, Levicar N, Pai M et al. Characterization and clinical application of human CD34+ stem/progenitor cell populations mobilized into the blood by granulocyte colony-stimulating factor. Stem Cells 2006 24 : 1822 30.
85. Lyra AC, Soares MB, da Silva LF et al. Feasibility and safety of autologous bone marrow mononuclear cell transplantation in patients with advanced chronic liver disease. World J. Gastroenterol. 2007 13 : 1067 73.
86. Gasbarrini A, Rapaccini GL, Rutella S et al. Rescue therapy by portal infusion of autologous stem cells in a case of drug-induced hepatitis. Dig. Liver Dis. 2007 39 : 878 82.
87. Mohamadnejad M, Namiri M, Bagheri M et al. Phase 1 human trial of autologous bone marrow-hematopoietic stem cell transplantation in patients with decompensated cirrhosis. World J. Gastroenterol. 2007 13 : 3359 63.
88. Dezso K, Jelnes P, Laszlo V et al. Thy-1 is expressed in hepatic myofibroblasts and not oval cells in stem cell-mediated liver regeneration. Am. J. Pathol. 2007 171 : 1529 37.
89. Meehan RR, Barlow DP, Hill RE, Hogan BL, Hastie ND. Pattern of serum protein gene expression in mouse visceral yolk sac and foetal liver. EMBO J. 1984 3 : 1881 5.
90. Brulport M, Schormann W, Bauer A et al. Fate of extrahepatic human stem and precursor cells after transplantation into mouse livers. Hepatology 2007 46 : 861 70.
91. Stevens AM, McDonnell WM, Mullarkey ME, Pang JM, Leisenring W, Nelson JL. Liver biopsies from human females contain male hepatocytes in the absence of transplantation. Lab. Invest. J. Techn Methods Pathol. 2004 84 : 1603 9.
92. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007 131 : 861 72.