Hepatic stem cells in liver regeneration

FASEB Journal

Volumn 10, Issue 11, 1996, Pages 1249-1256

  Thorgeirsson, Snorri S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

bile duct epithelial cells; differentiation; growth factors; hepatocytes; liver parenchyma; liver stem cell biology; oval cells; partial hepatectomy; proliferation; stem cell activation

Indexed keywords

GROWTH FACTOR;

CELL DIFFERENTIATION; CELL REGENERATION; CELLULAR DISTRIBUTION; HUMAN; HUMAN CELL; LIVER CELL; LIVER REGENERATION; LIVER RESECTION; MITOSIS; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 0029819783     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.10.11.8836038     Document Type: Review

References (68)

1. Van Thiel, D. H., Gavaler, J. S., Kam, I., Francavilla, A., Polimeno, L., Schade, P. R., Smith, J., Diven, W., Penkrot, R. J., and Starzl, T. E. (1989) Rapid growth of an intact human liver transplanted into a recipient larger than the donor. Gastroenterology 93, 1414-1419
2. Lajtha, L. G. (1970) Stem cell concepts. Nouv. Rev. Fr. Hematol. 21, 59-65
3. Rhim, J. A., Sandgren, E. P., Degen, J. L., Palmiter, R. D., and Brinster, R. L. (1994) Replacement of diseased mouse liver by hepatic cell transplantation. Science 263, 1149-1152
4. Potten, C. S., and Loeffler, M. (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Development 110, 1001-1020
5. Grisham, J. W., and Thorgeirsson, S. S. (1996) Liver stem cells. In The Stem Cell Handbook (Potten, C. S., ed) Academic Press, New York In press
6. Van Eyken, P., and Desmet, V. J. (1992) Development of intrahepatic bile ducts, ductular metaplasia of hepatocytes, and cytokeratin patterns in various types of human hepatic neoplasms. In The Role of Cell Types in Hepatocarcinogenesis (Sirica, A. E., ed) pp. 227-263, CRC Press, Boca Raton, Florida
7. Van Eyken, P., Sciot, R., Callea, F., and Desmet, V. J. (1989) A cytokeratin-immunohistochemical study of focal nodular hyperplasia of the liver: further evidence that ductular metaplasia of hepatocytes contributes to ductular "proliferation." Liver 9, 372-377
8. Thorgeirsson, S. S. (1993) Commentary. Hepatic stem cells. Am. J. Pathol. 142, 1331-1333
9. Fausto, N. (1990) Oval cells and liver carcinogenesis: an analysis of cell lineages in hepatic tumors using oncogene transfection techniques. Prog. Clin. Biol. Res. 331, 325-334
10. Sell, S. (1990) Is there a liver stem cell? Cancer Res. 50, 3811-3815
11. Sigal, S. H., Brill, S., and Reid, L. M. (1992) The liver as a stem cell and lineage system. Am. J. Physiol. 263, G139-G148
12. Grisham, J. W. (1980) Cell types in long-term propagable cultures of rat liver. Ann. N.Y. Acad. Sci. 349, 128-137
13. Kinosita, R. (1937) Studies on the carcinogenic chemical substances. Trans. Soc. Pathol. Jpn. 27, 665-727
14. Price, J. M., Harman, J. W., Miller, E. C., and Miller, J. A. (1952) Progressive microscopic alterations in the livers of rats fed the hepatic carcinogens 3′-methyl-4-dimethylaminoazobenzene and 4′-fluoro-4-dimethylaminoazobenzene. Cancer Res. 12, 192-200
15. Farber, E. (1956) Similarities in the sequence of early histological changes induced in the liver of the rat by ethionine, 2-acetylaminofluorene, and 3′-methyl-4-dimethylaminoazobenzene. Cancer Res. 16, 142-148
16. Wilson, J. W., and Leduc, E. H. (1958) Role of cholangioles in restoration of the liver of the mouse after dietary injury. J. Pathol. Bacteriol. 76, 441-449
17. Marceau, N. (1990) Biology of disease. Cell lineage and differentiation programs in epidermal, urothelial and hepatic tissues and their neoplasms. Lab. Invest. 63, 4-20
18. Inaoka, Y. (1967) Significance of the so-called oval cell proliferation during azo-dye hepatocarcinogenesis. Gann 58, 355-366
19. Shinozuka, H., Lombardi, B., Sell, S., and Iammarino, R. M. (1978) Early histological and functional alterations of ethionine liver carcinogenesis in rats fed a choline-deficient diet. Cancer Res. 38, 1092-1098
20. Sell, S., and Salman, J. (1984) Light- and electron-microscopic autoradiographic analysis of proliferating cells during the early stages of chemical hepatocarcinogenesis in the rat induced by feeding N-2-fluorenyl-acetamide in a choline-deficient diet. Am. J. Pathol. 114, 287-300
21. Tatematsu, M., Ho, R. H., Kaku, T., Ekem, J. K., and Farber, E. (1984) Studies on the proliferation and fate of oval cells in the liver of rats treated with 2-acetylaminofluorene and partial hepatectomy. Am. J. Pathol. 114, 418-430
22. Lesch, R., Reutter, W., Keppler, D., and Decker, K. (1970) Liver restitution after acute galactosamine hepatitis: autoradiographic and biochemical studies in rats. Exp. Mol. Pathol. 12, 58-69
23. Farber, E. (1984) Cellular biochemistry of the stepwise development of cancer with chemicals. Cancer Res. 44, 5463-5474
24. Evarts, R. P., Nagy, P., Marsden, E., and Thorgeirsson, S. S. (1987) A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 8, 1737-1740
25. Gerber, M. A., Thung, S. N., Shen, S., Stromeyer, F. W., and Ishak, K. G. (1983) Phenotypic characterization of hepatic proliferation: antigenic expression of proliferating epithelial cells in fetal liver, massive hepatic necrosis, and nodular transformation of the liver. Am. J. Pathol. 110, 70-74
26. Hsia, C. C., Evarts, R. P., Nakatsukasa, N., Marsden, E. R., and Thorgeirsson, S. S. (1992) Occurrence of oval-type cells in hepatitis B virus-associated human hepatocarcinogenesis. Hepatology 16, 1327-1333
27. Hixson, D. C., Faris, R. A., and Thompson, N. L. (1990) An antigenic portrait of the liver during carcinogenesis. Pathobiology 58, 65-77
28. Factor, V. M., Radaeva, S. A., and Thorgeirsson, S. S. (1994) Origin and fate of oval cells in Dipin-induced hepatocarcinogenesis in the mouse. Am. J. Pathol. 145, 409-422
29. Thorgeirsson, S. S., Evarts, R. P., Fujio, K., and Hu, Z. (1994) Cellular biology of the rat hepatic stem cell compartment. In Liver Carcinogenesis (Skouteris, C. G., ed) pp. 129-145, NATO ASI Series, Vol. H88, Springer-Verlag, Berlin/Heidelberg
30. Lemire, J. M., Shiojiri, N., and Fausto, N. (1991) Oval cell proliferation and the origin of small hepatocytes in liver injury induced by D-galactosamine. Am. J. Pathol. 139, 535-552
31. Tatematsu, M., Kaku, T., Medline, A., and Farber, E. (1985) Intestinal metaplasia as a common option of oval cells in relation to cholangiofibrosis in the livers of rats exposed to 2-acetylaminofluorene. Lab. Invest. 52, 354-362
32. Hayner, N. T., Braun, L., Yaswen, P., Brooks, M., and Fausto, N. (1984) Isozyme profiles of oval cells, parenchymal cells, and biliary cells isolated by centrifugal elutriation from normal and preneoplastic livers. Cancer Res. 44, 332-338
33. Germain, L., Goyette, R., and Marceau, N. (1985) Differential cytokeratin and α-fetoprotein expression in morphologically distinct epithelial cells emerging at the early stages of rat hepatocarcinogenesis. Cancer Res. 45, 673-681
34. Germain, L., Noel, H., Gourdeau, H., and Marceau, N. (1988) Promotion of growth and differentiation of rat ductular oval cells in primary culture. Cancer Res. 48, 368-378
35. Thorgeirsson, S. S., and Evarts, R. P. (1992) Growth and differentiation of stem cells in adult liver. In The Role of Cell Types of Hepatocarcinogenesis (Sirica, A. E., ed) pp. 100-120, CRC Press, Boca Raton, Florida
36. Golding, M., Sarraf, C. E., Lalani, E. N., Anilkumar, T. V., Edwards, R. J., Nagy, P., Thorgeirsson, S. S., and Alison, M.R. (1995) Oval cell differentiation into hepatocytes in the acetylamino-fluorene-treated regenerating rat liver. Hepatology 22, 1243-1253
37. Evarts, R. P., Nakatsukasa, H., Marsden, E. R., Hu, Z., and Thorgeirsson, S. S. (1992) Expression of transforming growth factor-α in regenerating liver and during hepatic differentiation. Mol. Carcinogen. 5, 25-31
38. Evarts, R. P., Hu, Z., Fujio, K., Marsden, E. R., and Thorgeirsson, S. S. (1993) Activation of hepatic stem cell compartment in the rat: Role of transforming growth factor-α, hepatocyte growth factor, and acidic fibroblast growth factor in early proliferation. Cell Growth & Differ. 4, 555-561
39. Hu, Z., Evarts, R. P., Fujio, K., Marsden, E. R., and Thorgeirsson, S. S. (1993) Expression of hepatocyte growth factor and c-met genes during hepatic differentiation and liver development in the rat. Am. J. Pathol. 142, 1823-1830
40. Marsden, E. R., Hu, Z., Fujio, K., Nakatsukasa, H., Thorgeirsson, S. S., and Evarts, R. P. (1992) Expression of acidic fibroblast growth factor in regenerating liver and during hepatic differentiation. Lab. Invest. 67, 427-433
41. Michalopoulos, C. (1990) Liver regeneration: molecular mechanisms of growth control. FASEB J. 4, 176-187
42. Mead, J. E., and Fausto, N. (1989) Transforming growth factor α may be a physiological regulator of liver regeneration by means of autocrine mechanisms. Proc. Natl. Acad. Sci. USA 86, 1558-1562
43. Evarts, R. P., Nakatsukasa, H., Marsden, E. R., Hsia, C. C., Dunsford, H. A., and Thorgeirsson, S. S. (1990) Cellular and molecular changes in the early stages of chemical hepatocarcinogenesis in the rat. Cancer Res. 50, 3439-3444
44. Lenzi, R., Liu, M. H., Tarsetti, F., Slott, P. A., Alpini, G., Xhai, W. R., Paronetto, F., Lenzen, R., and Tavolini, N. (1992) Histogenesis of bile duct-like cells proliferating during ethionine hepatocarcinogenesis. Lab. Invest. 66, 390-402
45. Hu, Z., Evarts, R. P., Fujio, K., Omori, N., Omori, M., Marsden, E. R., and Thorgeirsson, S.S. (1996) Expression of transforming growth factor alpha/epidermal growth factor receptor, hepatocyte growth factor/c-met and acidic fibroblast growth factor/fibroblast growth factor receptors during hepatocarcinogenesis. Carcinogenesis 17, 931-938
46. Fujio, K., Evarts, R. P., Hu, Z., Marsden, E. R., and Thorgeirsson, S. S. (1994) Expression of stem cell factor and its receptor, c-kit, during liver regeneration from putative stem cells in adult rat. Lab. Invest. 70, 511-516
47. Morrison-Graham, K., and Takahashi, Y. (1993) Steel factor and c-kit receptor: from mutants to a growth factor system. BioEssays 15, 77-84
48. Metcalf, D. (1991) Lineage commitment of hemopoietic progenitor cells in developing blast cell colonies: influence of colony-stimulating factors. Proc. Natl. Acad. Sci. USA 88, 11310-11314
49. Fujio, K., Hu, Z., Evarts, R. P., Marsden, E. R., Niu, C.-H., and Thorgeirsson, S. S. (1996) Coexpression of stem cell factor and c-kit in embryonic and adult liver. Exp. Cell Res. 224, 243-250
50. Lemire, J. M., and Fausto, N. (1991) Multiple alpha-fetoprotein RNAs in adult rat liver: cell type-specific expression and differential regulation. Cancer Res. 51, 4656-4664
51. Bisgaard, H. C., Nagy P., Santoni-Rugiu E., and Thorgeirsson, S. S. (1996) Proliferation, apoptosis, and induction of hepatic transcription factors are characteristic of the early response of biliary epithelial (oval) cells to chemical carcinogens. Hepatology 23, 62-70
52. Nagy, P., Bisgaard, H. C., Santoni-Rugiu, E., and Thorgeirsson, S. S. (1996) In vivo infusion of growth factors enhances the mitogenic response of rat hepatic ductal (oval) cells following administration of 2-acetylaminofluorene. Hepatology 23, 71-79
53. Nagy, P., Bisgaard, H. C., and Thorgeirsson, S. S. (1994) Expression of hepatic liver transcription factors during liver development and oval cell differentiation. J. Cell Biol. 126, 223-233
54. Hsia, C.-C., Thorgeirsson, S. S., and Tabor, E. (1994) Expression of hepatitis B surface and core antigens and transforming growth factor-α in "oval cells" of the liver in patients with hepatocellular carcinoma. Med. Virol. 43, 216-221
55. Thorgeirsson, S. S. (1995) Target cell populations in virally associated hepatocarcinogenesis. Proceedings of the 25th Intl. Symposium of the Princess Takamatsu Cancer Research Fund on "Hepatitis C Virus and its Involvement in the Development of Carcinoma," pp. 163-170, Princeton Scientific Publishing Co., Princeton, New Jersey
56. Shiojiri, N., Lemire, J. M., and Fauston, N. (1991) Cell lineages and oval cell progenitors in rat liver development. Cancer Res. 51, 2611-2620
57. Van Eyken, P., and Desmet, V. J. (1993) Cytokeratins and the liver. Liver 13, 113-122
58. Germain, L., Blouin, M.-J., and Marceau, N. (1988) 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. 48, 4909-4918
59. Bisgaard, H. C., Nagy, P., Ton, P. T., Hu, Z., and Thorgeirsson, S. S. (1994) Modulation of keratin 14 and α-fetoprotein expression during hepatic oval cell proliferation and liver regeneration. J. Cell. Physiol. 159, 475-484
60. Bisgaard, H. C., Ton, P. T., Nagy, P., and Thorgeirsson, S. S. (1994) Phenotypic modulation of keratins, vimentin, and α-fetoprotein in cultured rat liver epithelial cells after chemical, oncogene, and spontaneous transformation. J. Cell. Physiol. 159, 485-494
61. Dunsford, H. A., and Sell, S. (1989) Production of monoclonal antibodies to preneoplastic liver cell populations induced by chemical carcinogens in rats and transplantable Morris hepatomas. Cancer Res. 49, 4887-4893
62. Marceau, N., Germain, L., Goyelle, R., Noel, M., and Gourdeau, H. (1986) Cell of origin of distinct cultured rat liver epithelial cells, as typed by cytokeratin and surface component selective expression. Biochem. Cell. Biol. 64, 788-802
63. Yang, L., Faris, R. A., and Hixson, D. C. (1993) Phenotypic heterogeneity within clonogenic ductal cell populations isolated from normal adult rat liver. Proc. Soc. Exp. Biol. Med. 204, 280-288
64. Marceau, N., Blouin, M.-J., Noël, M., Török, N., and Loranger, A. (1992) The role of bipotential progenitor cells in liver ontogenesis and neoplasia. In The Role of Cell Types in Hepatocarcinogenesis (Sirica, A. E., ed) pp. 121-149, CRC Press, Boca Raton, Florida
65. Hixson, D. C., and Allison, J. P. (1985) Monoclonal antibodies recognizing oval cells induced in the liver of rats by N-2-fluorenylacetamide or ethionine in a choline-deficient diet. Cancer Res. 45, 3750-3760
66. Faris, R. A., Monfils, B. A., Dunsford, H. A., and Hixson, D. (1991) Antigenic relationship between oval cells and a subpopulation of hepatic foci, nodules, and carcinomas induced by the "resistant hepatocyte" model system. Cancer Res. 51, 1308-1317
67. Engelhardt, N. V., Factor, V. M., Yasova, A. K., Poltoranina, V. S., Baranov, V. N., and Lasareva, M. N. (1990) Common antigens of mouse oval and biliary epithelial cells. Expression on newly formed hepatocytes. Differentiation 45, 29-37
68. Engelhardt, N. V., Factor, V. M., Medvinsky, A. L., Baranov, V. N., Lazareva, M. N., and Poltoranina, V. S. (1993) Common antigen of oval and biliary epithelial cells (A6) is a differentiation marker of epithelial and erythroid cell lineages in early development of the mouse. Differentiation 55, 19-26