Adult stem cells in progression and therapy of hepatocellular carcinoma

International Journal of Cancer

Volumn 121, Issue 9, 2007, Pages 1875-1882

  Herr, Ingrid ^a   Groth, Ariane ^a   Schemmer, Peter ^a   Büchler, Markus W ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Bone marrow; Cirrhosis; Fibrosis; Haematologic stem cells; Hepatic progenitor cells; Hepatocellular carcinoma; Intermediate hepatocytes; Liver; Mesenchymal stem cells; Oval cells; Patient study; Phase I study; Stem cells; Transplantation

Indexed keywords

CELL DIFFERENTIATION; CELL TYPE; HUMAN; LIVER CELL CARCINOMA; LIVER FIBROSIS; LIVER REGENERATION; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; STEM CELL TRANSPLANTATION;

ADULT STEM CELLS; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL DIFFERENTIATION; DISEASE PROGRESSION; HUMANS; REGENERATION;

EID: 34648833496     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23041     Document Type: Short Survey

References (79)

1. Dawe RS. Hepatocellular carcinoma. Lancet 2004;363:899.
2. Friedman SL. Mechanisms of disease: mechanisms of hepatic fibrosis and therapeutic implications. Nat Clin Pract Gastroenterol Hepatol 2004;1:98-105.
3. Lotersztajn S, Julien B, Teixeira-Clerc F, Grenard P, Mallat A. Hepatic fibrosis: molecular mechanisms and drug targets. Annu Rev Pharmacol Toxicol 2005;45:605-28.
4. Laurent-Puig P, Zucman-Rossi J. Genetics of hepatocellular tumors. Oncogene 2006;25:3778-86.
5. El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology 2004;126:460-8.
6. Stieger B, Peters R, Sidler MA, Meier PJ. Hepatocyte transplantation: potential of hepatocyte progenitor cells and bone marrow derived stem cells. Swiss Med Wkly 2006;136:552-6.
7. Ramadori G, Saile B. Mesenchymal cells in the liver - one cell type or two? Liver 2002;22:283-94.
8. Roskams T. Liver stem cells and their implication in hepatocellular and cholangiocarcinoma. Oncogene 2006;25:3818-22.
9. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-18.
10. Purohit V, Brenner DA. Mechanisms of alcohol-induced hepatic fibrosis: a summary of the Ron Thurman Symposium. Hepatology (Baltimore, MD) 2006;43:872-8.
11. Kawada N. Human hepatic stellate cells are resistant to apoptosis: implications for human fibrogenic liver disease. Gut 2006;55:1073-4.
12. Iredale JP. Hepatic stellate cell behavior during resolution of liver injury. Semin Liver Dis 2001;21:427-36.
13. Albanis E, Friedman SL. Antifibrotic agents for liver disease. Am J Transplant 2006;6:12-19.
14. Brenner DA, Waterboer T, Choi SK, Lindquist JN, Stefanovic B, Burchardt E, Yamauchi M, Gillan A, Rippe RA. New aspects of hepatic fibrosis. J Hepatol 2000;32:32-8.
15. Pinzani M, Milani S, Grappone C, Weber FL, Jr, Gentium P, Abboud HE. Expression of platelet-derived growth factor in a model of acute liver injury. Hepatology (Baltimore, MD) 1994;19:701-7.
16. Dooley S, Delvoux B, Lahme B, Mangasser-Stephan K, Gressner AM. Modulation of transforming growth factor beta response and signaling during transdifferentiation of rat hepatic stellate cells to myofibroblasts. Hepatology (Baltimore, MD) 2000;31:1094-106.
17. Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Nakatani T, Tsujinoue H, Yanase K, Namisaki T, Imazu H, Fukui H. Tissue inhibitor of metalloproteinases-1 attenuates spontaneous liver fibrosis resolution in the transgenic mouse. Hepatology (Baltimore, MD) 2002;36:850-60.
18. Iredale JP. Tissue inhibitors of metalloproteinases in liver fibrosis. Int J Biochem Cell Biol 1997;29:43-54.
19. Alison MR, Lovell MJ. Liver cancer: the role of stem cells. Cell Prolif 2005;38:407-21.
20. Fiegel HC, Lange C, Kneser U, Lambrecht W, Zander AR, Rogiers X, Kluth D. Fetal and adult liver stem cells for liver regeneration and tissue engineering. J Cell Mol Med 2006;10:577-87.
21. Wang X, Foster M, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M. The origin and liver repopulating capacity of murine oval cells. Proc Natl Acad Sci USA 2003; 100 (Suppl 1):11881-8.
22. Mitaka T. The current status of primary hepatocyte culture. Int J Exp Pathol 1998;79:393-709.
23. Gao B, St Pierre MV, Stieger B, Meier PJ. Differential expression of bile salt and organic anion transporters in developing rat liver. J Hepatol 2004;41:201-8.
24. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. Bone marrow as a potential source of hepatic oval cells. Science 1999;284:1168-70.
25. Oh SH, Witek RP, Bae SH, Zheng D, Jung Y, Piscaglia AC, Petersen BE. Bone marrow-derived hepatic oval cells differentiate into hepatocytes in 2-acetylaminofluorene/partial hepatectomy-induced liver regeneration. Gastroenterology 2007;132:1077-87.
26. Oh SH, 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 2000;279:500-4.
27. Forbes SJ, Russo FP, Rey V, Burra P, Rugge M, Wright NA, Alison MR. A significant proportion of myofibroblasts are of bone marrow origin in human liver fibrosis. Gastroenterology 2004;126:955-63.
28. 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 2003;422:897-901.
29. Vassilopoulos G, Wang PR, Russell DW. Transplanted bone marrow regenerates liver by cell fusion. Nature 2003;422:901-4.
30. Newsome PN, Johannessen I, Boyle S, Dalakas E, McAulay KA, Samuel K, Rae F, Forrester L, Turner ML, Hayes PC, Harrison DJ, Bickmore WA 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.
31. 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;6:532-9.
32. Zhan Y, Wang Y, Wei L, Chen H, Cong X, Fei R, Gao Y, Liu F. Differentiation of hematopoietic stem cells into hepatocytes in liver fibrosis in rats. Transplant Proc 2006;38:3082-5.
33. Yamaguchi K, Itoh K, Masuda T, Umemura A, Baum C, Itoh Y, Okanoue T, Fujita J. In vivo selection of transduced hematopoietic stem cells and little evidence of their conversion into hepatocytes in vivo. J Hepatol 2006;45:681-7.
34. Lian G, Wang C, Teng C, Zhang C, Du L, Zhong Q, Miao C, Ding M, Deng H. Failure of hepatocyte marker-expressing hematopoietic progenitor cells to efficiently convert into hepatocytes in vitro. Exp Hematol 2006;34:348-58.
35. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.
36. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, Bagasra O, Prockop DJ. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA 1995;92:4857-61.
37. Aurich I, Mueller LP, Aurich H, Luetzkendorf J, Tisljar K, Dollinger MM, Schormann W, Walldorf J, Hengstler JG, Fleig WE, Christ B. Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 2007;56:405-15.
38. Lee KD, Kuo TK, Whang-Peng J, Chung YF, Lin CT, Chou SH, Chen JR, Chen YP, Lee OK. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology (Baltimore, MD) 2004;40:1275-84.
39. 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;12:2394-7.
40. 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;328:258-64.
41. Hong SH, Gang EJ, Jeong JA, Ahn C, Hwang SH, Yang IH, Park HK, Han H, Kim H. In vitro differentiation of human umbilical cord blood-derived mesenchymal stem cells into hepatocyte-like cells. Biochem Biophys Res Commun 2005;330:1153-61.
42. Sato Y, Araki H, Kato J, Nakamura K, Kawano Y, Kobune M, Sato T, Miyanishi K, Takayama T, Takahashi M, Takimoto R, Iyama S, et al. Human mesenchymal stem cells xenografted directly to rat liver are differentiated into human hepatocytes without fusion. Blood 2005;106:756-63.
43. Forbes SJ, Vig P, Poulsom R, Alison MR, Wright NA. Bone marrow-derived liver stem cells: their therapeutic potential. Gastroenterology 2002;123:654-5.
44. Theise ND. Liver stem cells: the fall and rise of tissue biology. Hepatology (Baltimore, MD) 2003;38:804-6.
45. De Silvestro G, Vicarioto M, Donadel C, Menegazzo M, Marson P, Corsini A. Mobilization of peripheral blood hematopoietic stem cells following liver resection surgery. Hepatogastroenterol 2004;51:805-10.
46. Fujii H, Hirose T, Oe S, Yasuchika K, Azuma H, Fujikawa T, Nagao M, Yamaoka Y. Contribution of bone marrow cells to liver regeneration after partial hepatectomy in mice. J Hepatol 2002;36:653-9.
47. Stamm C, Westphal B, Kleine HD, Petzsch M, Kittner C, Klinge H, Schumichen C, Nienaber CA, Freund M, Steinhoff G. Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 2003;361:45-6.
48. Menasche P. Cell therapy of heart failure. C R Biol 2002;325:731-8.
49. Perm EC, Dohmann HF, Borojevic R, Silva SA, Sousa AL, Mesquita CT, Rossi MI, Carvalho AC, Dutra HS, Dohmann HJ, Silva GV, Belem L, et al. Transendocardial, autologous bone marrow cell transplantation for severe, chronic ischemic heart failure. Circulation 2003;107:2294-302.
50. am Esch JS, II, Knoefel WT, Klein M, Ghodsizad A, Fuerst G, Poll LW, Piechaczek C, Burchardt ER, Feifel N, Stoldt V, Stockschlader M, Stoecklein N, et al. Portal application of autologous CD133+ bone marrow cells to the liver: a novel concept to support hepatic regeneration. Stem cells (Dayton, Ohio) 2005;23:463-70.
51. Gordon MY, Levicar N, Pai M, Bachellier P, Dimarakis I, Al-Allaf F, M'Hamdi H, Thalji T, Welsh JP, Marley SB, Davies J, Dazzi F, et al. Characterization and clinical application of human CD34+ stem/progenitor cell populations mobilized into the blood by granulocyte colony-stimulating factor. Stem cells (Dayton, Ohio) 2006;24:1822-30.
52. Terai S, Ishikawa T, Omori K, Aoyama K, Marumoto Y, Urata Y, Yokoyama Y, Uchida K, Yamasaki T, Fujii Y, Okita K, Sakaida I. Improved liver function in patients with liver cirrhosis after autologous bone marrow cell infusion therapy. Stem cells (Dayton, Ohio) 2006;24:2292-8.
53. Gasbarrini A, Rapaccini GL, Rutella S, Zocco MA, Tittoto P, Leone G, Pola P, Gasbarrini G, Di Campli C. Rescue therapy by portal infusion of autologous stem cells in a case of drug-induced hepatitis. Dig Liver Dis 2006, in press.
54. Furst G, Schulte am Esch J, Poll LW, Hosch SB, Fritz LB, Klein M, Godehardt E, Krieg A, Wecker B, Stoldt V, Stockschlader M, Eisenberger CF, et al. Portal vein embolization and autologous CD133+ bone marrow stem cells for liver regeneration: initial experience. Radiology 2007;243:171-9.
55. Kallis Y, Alison MR, Forbes SJ. Bone marrow stem cells and liver disease. Gut 2006;56:716-24.
56. Aldeguer X, Debonera F, Shaked A, Krasinkas AM, Gelman AE, Que X, Zamir GA, Hiroyasu S, Kovalovich KK, Taub R, Olthoff KM. Interleukin-6 from intrahepatic cells of bone marrow origin is required for normal murine liver regeneration. Hepatology (Baltimore, MD) 2002;35:40-8.
57. 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 (Baltimore, MD) 2004;40:1304-11.
58. 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.
59. Zhao DC, Lei JX, Chen R, Yu WH, Zhang XM, Li SN, Xiang P. Bone marrow-derived mesenchymal stem cells protect against experimental liver fibrosis in rats. World J Gastroenterol 2005;11:3431-40.
60. Oyagi S, Hirose M, Kojima M, Okuyama M, Kawase M, Nakamura T, Ohgushi H, Yagi K. Therapeutic effect of transplanting HGF-treated bone marrow mesenchymal cells into CCl4-injured rats. J Hepatol 2006;44:742-8.
61. Matsuda-Hashii Y, Takai K, Ohta H, Fujisaki H, Tokimasa S, Osugi Y, Ozono K, Matsumoto K, Nakamura T, Hara J. Hepatocyte growth factor plays roles in the induction and autocrine maintenance of bone marrow stromal cell IL-11, SDF-1α, and stem cell factor. Exp Hematol 2004;32:955-61.
62. Russo FP, Alison MR, Bigger BW, Amofah E, Florou A, Amin F, Bou-Gharios G, Jeffery R, Iredale JP, Forbes SJ. The bone marrow functionally contributes to liver fibrosis. Gastroenterology 2006;130:1807-21.
63. 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, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-9.
64. Direkze NC, Hodivala-Dilke K, Jeffery R, Hunt T, Poulsom R, Oukrif D, Alison MR, Wright NA. Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res 2004;64:8492-5.
65. Neaud V, Faouzi S, Guirouilh J, Le Bail B, Balabaud C, Bioulac-Sage P, Rosenbaum J. Human hepatic myofibroblasts increase invasiveness of hepatocellular carcinoma cells: evidence for a role of hepatocyte growth factor. Hepatology (Baltimore, MD) 1997;26:1458-66.
66. von Schweinitz D, Faundez A, Teichmann B, Birnbaum T, Koch A, Hecker H, Gluer S, Fuchs J, Pietsch T. Hepatocyte growth-factor-scatter factor can stimulate post-operative tumor-cell proliferation in childhood hepatoblastoma. Int J Cancer 2000;85:151-9.
67. Baba S, Fujii H, Hirose T, Yasuchika K, Azuma H, Hoppo T, Naito M, Machimoto T, Ikai I. Commitment of bone marrow cells to hepatic stellate cells in mouse. J Hepatol 2004;40:255-60.
68. Forbes SJ, Alison MR. Side population (SP) cells: taking center stage in regeneration and liver cancer? Hepatology (Baltimore, MD) 2006;44:23-6.
69. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annual review of medicine 2007;58:267-84.
70. Ma S, Chan KW, Hu L, Lee TK, Wo JY, Ng 10, Zheng BJ, Guan XY. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007;132:2542-56.
71. Wu XZ, Chen D. Origin of hepatocellular carcinoma: role of stem cells. J Gastroenterol Hepatol 2006;21:1093-8.
72. Kim H, Park C, Han KH, Choi J, Kim YB, Kim JK, Park YN. Primary liver carcinoma of intermediate (hepatocyte-cholangiocyte) phenotype. J Hepatol 2004;40:298-304.
73. Fukuda K, Sugihara A, Nakasho K, Tsujimura T, Yamada N, Okaya A, Sakagami M, Terada N. The origin of biliary ductular cells that appear in the spleen after transplantation of hepatocytes. Cell Transplant 2004;13:27-33.
74. Yano T, Ishikura H, Wada T, Kishimoto T, Kondo S, Katoh H, Yoshiki T. Hepatoid adenocarcinoma of the pancreas. Histopathology 1999;35: 90-2.
75. Hruban RH, Molina JM, Reddy MN, Boitnott JK. A neoplasm with pancreatic and hepatocellular differentiation presenting with subcutaneous fat necrosis. Am J Clin Pathol 1987;88:639-45.
76. Coussens LM, Werb Z. Inflammation and cancer. Nature 2002;420:860-7.
77. Libbrecht L. Hepatic progenitor cells in human liver tumor development. World J Gastroenterol 2006;12:6261-5.
78. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 2006;351:820-4.
79. Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, Nakauchi H, Taniguchi H. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology (Baltimore, MD) 2006;44:240-51.