Liver stem cells: When the going gets tough they get going

International Journal of Experimental Pathology

Volumn 78, Issue 6, 1997, Pages 365-381

  Alison, Malcolm R ^a   Golding, Matthew ^a   Sarraf, Catherine E ^a  

^a ICSM   (United Kingdom)

Author keywords

Bile ducts; Cholangiocarcinoma; Hepatocellular carcinoma; Liver; Oval cells; Stem cells

Indexed keywords

KERATINOCYTE GROWTH FACTOR; LIOTHYRONINE; PARATHYROID HORMONE RELATED PROTEIN; SCATTER FACTOR;

BILE DUCT; BILE DUCT LIGATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; GENE THERAPY; HUMAN; LIVER CANCER; LIVER CELL; LIVER REGENERATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 0031438036     PISSN: 09599673     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2613.1997.500375.x     Document Type: Review

References (166)

1. ALISON M.R. (1986) Regulation of liver growth. Physiol. Rev. 66, 499-541.
2. ALISON M.R., NASIM M., ANILKUMAR T.V. & SARRAF C.E. (1993a) Transforming growth factor-α immunoreactivity in a variety of epithelial tissues. Cell Prolif. 26, 449-460.
3. ALISON M.R., POULSOM R., JEFFERY R., ANILKUMAR T.V., JAGOE R. & SARRAF C.E. (1993b) Expression of hepatocyte growth factor mRNA during oval cell activation in the rat liver. J. Pathol. 171, 291-299.
4. ALISON M.R., GOLDING M., SARRAF C.E., EDWARDS R.J. & LALANI E.N. (1996) Liver damage in the rat induces hepatocyte stem cells from biliary epithelial cells. Gastroenterol. 110, 1182-1190.
5. ALISON M., GOLDING M., LALANI E.N., NAGY P., THORGEIRSSON S. & SARRAF C. (1997) Wholesale hepatocytic differentiation in the rat from ductular oval cells, the progeny of biliary stem cells. J. Hepatol. 26, 343-352.
6. ALPINI G., ARAGONA E., DABEVA M., SALVI R., SHAFRITZ D.A. & TAVOLONI N. (1992) Distribution of albumin and alpha-fetoprotein mRNAs in normal, hyperplastic, and preneoplastic rat liver. Am. J. Pathol. 141, 623-632.
7. ALPINI G., ROBERTS S., KUNTZ S.M., UENO Y., GUBBA S., PODILA P.V., LESAGE G. & LARUSSO N.F. (1996) Morphological, molecular, and functional heterogeneity of cholangiocytes from normal rat liver. Gastroenterol. 110, 1636-1643.
8. ALPINI G., GLASER S., ROBERTSON W., RODGERS R.E.D., PHINIZY J.L., LASATER J. & LESAGE G.D. (1997) Large but not small intrahepatic bile ducts are involved in secretin-regulated ductal bile secretion. Am. J. Physiol. 272, G1064-G1074.
9. ANILKUMAR T.V., GOLDING M., EDWARDS R.J., LALANI E.-N., SARRAF C.E. & ALISON M.R. (1995) The resistant hepatocyte model of carcinogenesis in the rat: the apparent independent development of oval cell proliferation and early nodules. Carcinogenesis 16, 845-853.
10. ARTHUR M.J. & IREDALE J.P. (1994) Hepatic lipocytes, TIMP-1 and liver fibrosis. J. R. Coll. Physicians Lond. 28, 200-208.
11. ARTHUR M.J., FRIEDMAN S.L., ROLL F.J. & BISSELL D.M. (1989) Lipocytes from normal rat liver release a neutral metalloproteinase that degrades basement membrane (type IV) collagen. J. Clin. Invest. 84, 1076-1085.
12. ATERMAN K. (1992) The stem cells of the liver - a selective review [editorial]. J. Cancer Res. Clin. Oncol. 118, 87-115.
13. BARROS E.J., SANTOS O.F., MATSUMOTO K., NAKAMURA T. & NIGAM S.K. (1995) Differential tubulogenic and branching morphogenetic activities of growth factors: implications for epithelial tissue development. Proc. Natl. Acad. Sci. USA 92, 4412-4416.
14. BETTO H., KANEDA K., YAMAMOTO T., KOJIMA A. & SAKURAI M. (1996) Development of intralobular bile ductules after spontaneous hepatitis in Long-Evans mutant rats. Lab. Invest. 75, 43-53.
15. BHATHAL P.S. & CHRISTIE G.S. (1969) A fluorescence microscopic study of bile duct proliferation induced in guinea pigs by alphanaphthyl isothiocyanate. Lab. Invest. 20, 480-487.
16. BISGAARD H.C., NAGY P., TON P.T., HU Z. & THORGEIRSSON S.S. (1994) Modulation of keratin 14 and alpha-fetoprotein expression during hepatic oval cell proliferation and liver regeneration. J. Cell. Physiol. 159, 475-484.
17. BISGAARD H.C., NAGY P., SANTONIRUGIU E. & THORGEIRSSON S.S. (1996) Proliferation, apoptosis, and induction of hepatic transcription factors are characteristics of the early response of biliary epithelial (oval) cells to chemical carcinogens. Hepatol. 23, 62-70.
18. BLOUIN R., BLOUIN M.J., ROYAL I., GRENIER A., ROOP D.R., LORANGER A. & MARCEAU N. (1992) Cytokeratin 14 expression in rat liver cells in culture and localization in vivo. Differentiation 52, 45-54.
19. BRALET M.P., BRANCHEREAU S., BRECHOT C. & FERRY N. (1994) Cell lineage study in the liver using retroviral mediated gene transfer. Evidence against the streaming of hepatocytes in normal liver. Am. J. Pathol. 144, 896-905.
20. BRILL S., HOLST P., SIGAL S., ZVIBEL I., FIORINO A., OCHS A., SOMASUNDARAN U. & REID L.M. (1993) Hepatic progenitor populations in embryonic, neonatal, and adult liver. Proc. Soc. Exp. Biol. Med. 204, 261-269.
21. BRINKMANN V., FOROUTAN H., SACHS M., WEIDNER K. & BIRCHMEIER W. (1995) Hepatocyte growth factor/scatter factor induces a variety of tissue specific morphogenic programs in epithelial cells. J. Cell Biol. 131, 1573-1586.
22. BURR A.W., CARPENTER M.R., HINES J.E., GULLICK W.J. & BURT A.D. (1993) Intrahepatic distribution of transforming growth factor-alpha (TGF alpha) during liver regeneration following carbon tetrachloride-induced necrosis. J. Pathol. 170, 95-100.
23. BURT A.D. & MACSWEEN R.N. (1993) Bile duct proliferation - its true significance? Histopathol 23, 599-602.
24. CABRERA J.A., WILSON J.M. & RAPER S.E. (1996) Targeted retroviral gene transfer into the rat biliary tract. Somatic Cell Mol Genet 22, 21-29.
25. CHEN J.-R., TSAO M.-S. & DUGUID W.P. (1995) Hepatocyte differentiation of cultured rat pancreatic ductal epithelial cells after in vivo implantation. Am. J. Pathol. 147, 707-717.
26. CHU Y.-W., SEFTOR E., ROMER L.H. & HENDRIX M.J.C. (1996) Experimental coexpression of vimentin and keratin intermediate filaments in human melanoma cells augments motility. Am. J. Pathol. 148, 63-69.
27. COLEMAN W.B., WENNERBERG A.E., SMITH G.J. & GRISHAM J.W. (1993) Regulation of the differentiation of diploid and some aneuploid rat liver epithelial (stemlike) cells by the hepatic microenvironment. Am. J. Pathol. 142, 1373-1382.
28. CORRESPONDENCE. (1995) Do livers 'Stream'? Am. J. Pathol. 146, 772-776.
29. DABEVA M.D. & SHAFRITZ D.A. (1993) Activation, proliferation, and differentiation of progenitor cells into hepatocytes in the D-galactosamine model of liver regeneration. Am. J. Pathol. 143, 1606-1620.
30. DELLADETSIMA J.K., KYRIAKOU V., VAFIADIS I., KARAKITSOS P., SMYRNOFF T. & TASSOPOULOS N.C. (1995) Ductular structures in acute hepatitis. J. Pathol. 175, 69-76.
31. DE-VOS R. & DESMET V. (1992) Ultrastructural characteristics of novel epithelial cell types identified in human pathologic liver specimens with chronic ductular reaction. Am. J. Pathol. 140, 1441-1450.
32. DUNSFORD H.A., MASET R., SALMAN J. & SELL S. (1985) Connection of ductlike structures induced by a chemical hepatocarcinogen to portal bile ducts in the rat liver detected by injection of bile ducts with a pigmented barium gelatin medium. Am. J. Pathol. 118, 218-224.
33. ELMORE L.W. & SIRICA A.E. (1991) Phenotypic characterization of metaplastic intestinal glands and ductular hepatocytes in cholangiofibrotic lesions rapidly induced in the caudate liver lobe of rats treated with furan. Cancer Res. 51, 5752-5759.
34. ELMORE L.W. & SIRICA A.E. (1993) 'Intestinal-type' of adenocarcinoma preferentially induced in right/caudate liver lobes of rats treated with furan. Cancer Res. 53, 254-259.
35. ENGELHARDT N.V., FACTOR V.M., YASOVA A.K., POLTORANINA V.S., BARANOV V.N. & LASAREVA M.N. (1990) Common antigens of mouse oval and biliary epithelial cells. Expression on newly formed hepatocytes. Differentiation 45, 29-37.
36. ENJOJI M., NAKASHIMA M., HONDA M., SAKAI H. & NAWATA H. (1997) Hepatocytic phenotypes induced in sarcomatous cholangiocarcinoma cells treated with 5-azacytidine. Hepatol. 26, 288-294.
37. ENOMOTO K., DEMPO K., MORI M. & ONOE T. (1978) Histopathological and ultrastructural study on extramedullary hematopoietic foci in early stage of 3′-methyl-4-(dimethylamino) azobenzene hepatocarcinogenesis. Gann 69, 249-254.
38. EVARTS R.P., NAGY P., MARSDEN E. & THORGEIRSSON S.S. (1987) A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 8, 1737-1740.
39. EVARTS R.P., NAGY P., NAKATSUKASA H., MARSDEN E. & THORGEIRSSON S.S. (1989) In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res. 49, 1541-1547.
40. EVARTS R.P., NAKATSUKASA H., MARSDEN E.R., HSIA C.C., DUNSFORD H.A. & THORGEIRSSON S.S. (1990) Cellular and molecular changes in the early stages of chemical hepatocarcinogenesis in the rat. Cancer Res. 50, 3439-3444.
41. EVARTS R.P., NAKATSUKASA H., MARSDEN E.R., HU Z. & THOROEIRSSON S.S. (1992) Expression of transforming growth factor-alpha in regenerating liver and during hepatic differentiation. Mol. Carcinog. 5, 25-31.
42. EVARTS R.P., HU Z., FUJIO K., MARSDEN E.R. & THORGEIRSSON S.S. (1993) Activation of hepatic stem cell compartment in the rat: role of transforming growth factor Q, hepatocyte growth factor, and acidic fibroblast growth factor in early proliferation. Cell Growth Diff. 4, 555-561.
43. FABRIKANT J.I. (1968) The kinetics of cellular proliferation in regenerating liver. J. Cell Biol. 36, 551-565.
44. FACTOR V.M., RADAEVA S.A. & THORGEIRSSON S.S. (1994) Origin and fate of oval cells in dipin-induced hepatocarcinogenesis in the mouse. Am. J. Pathol. 145, 409-422.
45. FARBER E. (1955) Similarities in the sequences 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.
46. FAUSTO N., LEMIRE J.M. & SHIOJIRI N. (1993) Cell lineages in hepatic development and the identification of progenitor cells in normal and injured liver. Proc. Soc. Exp. Biol. Med. 204, 237-241.
47. FUJIO K., EVARTS R.P., HU Z., MARSDEN E.R. & 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.
48. GALIMI F., BAGNARA G., BONSI L., COTTONE E., FOLLENZI A., SIMEONE A. & COMOGLIO P. (1994) Hepatocyte growth factor induces proliferation and differentiation of multipotent and erythroid hemopoietic progenitors. J. Cell Biol. 127, 1743-1754.
49. GARFIELD S., HUBER B.E., NAGY P., CORDINGLEY M.G. & THORGEIRSSON S.S. (1988) Neoplastic transformation and lineage switching of rat liver epithelial cells by retrovirus-associated oncogenes. Mol. Carcinog. 1, 189-195.
50. GERLACH C., SAKKAB D.Y., SCHOLZEN T., DASSLER R., ALISON M.R. & GERDES J. (1997) Ki-67 expression during rat liver regeneration after partial hepatectomy. Hepatol. 26, 573-578.
51. GERMAIN L., BLOUIN M.J. & 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.
52. GILLES C., POLETTE M., PIETTE J., DELVIGNE A.C., THOMPSON E.W., FOIDART J.M. & BIREMBAUT P. (1996) Vimentin expression in cervical carcinomas: association with invasive and migratory potential. J. Pathol. 180, 175-180.
53. GOLDING M., SARRAF C.E., LALANI E.-N., ANILKUMAR T.V., EDWARDS R.J., NAGY P., THORGEIRSSON S.S. & ALISON M.R. (1995) Oval cell differentiation into hepatocytes in the acetylaminofluorene-treated regenerating rat liver. Hepatol. 22, 1243-1253.
54. GRAHAM G.J. & WRIGHT E.G. (1997) Haemopoietic stem cells: their heterogeneity and regulation. Int. J. Exp. Pathol. 78, 197-218.
55. GRIFFITHS M.R., SHEPHERD M., FERRIER R., SCHUPPAN D., JAMES O.F.W. & BURT A.D. (1992) Light microscopic and ultrastructural distribution of type VI collagen in human liver: alterations in chronic biliary disease. Histopathol 21, 335-344.
56. GRISHAM J.W. (1962) A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver; autoradiography with thymidine H-3. Cancer Res. 22, 842-849.
57. GRISHAM J.W. (1980) Cell types in long-term propagable cultures of rat liver. Ann. NY Acad. Sci. 349, 128-137.
58. GRISHAM J.W. (1994) Migration of hepatocytes along hepatic plates and stem cell-fed hepatocyte lineages. Am. J. Pathol. 144, 849-854.
59. GRISHAM J.W. & PORTA E.A. (1964) Origin and fate of proliferated hepatic ductal cells in the rat: electronmicroscopic and autoradiographic studies. Exp. Mol. Pathol. 2, 242-261.
60. GRISHAM J.W., COLEMAN W.B. & SMITH G.J. (1993) Isolation, culture, and transplantation of rat hepatocytic precursor (stem-like) cells. Proc. Soc. Exp. Biol. Med. 204, 270-279.
61. GUALDI R., BOSSARD P., ZHENG M., HAMADA Y., COLEMAN J.R. & ZARET K.S. (1996) Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 10, 1670-1682.
62. HAQUE S., HARUNA Y., SAITO K., NALESNIK M.A., ATILLASOY E., THUNG S.N. & GERBER M.A. (1996) Identification of bipotential progenitor cells in human liver regeneration. Lab. Invest. 75, 699-705.
63. HARUNA Y., SAITO K., SPAULDING S., NALESNIK M.A. & GERBER M.A. (1996) Identification of bipotential progenitor cells in human liver development. Hepatol. 23, 476-481.
64. HAYNER N.T., BRAUN L., YASWEN P., BROOKS M. & FAUSTO N. (1984) Isozyme profiles of oval cells, parenchymal cells, and biliary cells isolated by centrifugal elutriation from normal and pre-neoplastic livers. Cancer Res. 44, 332-338.
65. HE X.Y., SMITH G.J., ENNO A. & NICHOLSON R.C. (1994) Short-term diethylnitrosamine-induced oval cell responses in three strains of mice. Pathol 26, 154-160.
66. HENDRIX M.J.C., SEFTOR E.A., SEFTOR R.E.B. & TREVOR K.T. (1997) Experimental co expression of vimentin and keratin intermediate filaments in human breast cancer cells results in phenotypic interconversion and increased invasive behavior. Am. J. Pathol. 150, 483-495.
67. HIRUMA M., SEKI A., ONO A. & KURIHARA T. (1993) Early hepatic lesions with marked glandular structures induced in rats by 0.1% ethionine in a choline deficient diet. Jikken Dobutsu 42, 197-201.
68. HSIA C.C., EVARTS R.P., NAKATSUKASA H., MARSDEN E.R. & THORGEIRSSON S.S. (1992) Occurrence of oval-type cells in hepatitis B virus-associated human hepatocarcinogenesis. Hepatol. 16, 1327-1333.
69. HU Z., EVARTS R.P., FUJIO K., MARSDEN E.R. & 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.
70. IDE H., SUBBARAO V., REDDY J.K. & RAO M.S. (1993) Formation of ductular structures in vitro by rat pancreatic epithelial oval cells. Exp. Cell Res. 209, 38-44.
71. ISHIKURA H., KIRIMOTO K., SHAMOTO M., MIYAMOTO Y., YAMAGIWA H., ITOH T. & AIZAWA M. (1986) Hepatoid adenocarcinomas of the stomach. An analysis of seven cases. Cancer 58, 119-126.
72. ISHIKURA H., ISHIGURO T., ENATSU C., FUJII H., KAKUTA Y., KANDA M. & YOSHIKI T. (1991) Hepatoid adenocarcinoma of the renal pelvis producing alpha-fetoprotein of hepatic type and bile pigment. Cancer 67, 3051-3056.
73. JOHNSON S.J., HINES J.E. & BURT A.D. (1992) Macrophage and perisinusoidal cell kinetics in acute liver injury. J. Pathol. 166, 351-358.
74. JOPLIN R., HISHIDA T., TSUBOUCHI H., DAIKUHARA Y., AYRES R., NEUBERGER J.M. & STRAIN A.J. (1992) Human intrahepatic biliary epithelial cells proliferate in vitro in response to human hepatocyte growth factor. J. Clin. Invest. 90, 1284-1289.
75. KARAKI Y., MUNAKATA S., SAEKI T., HIROTA S. & FUJIMAKI M. (1991) Appearance of a carcinoid-like pattern in rat hepatic tumors induced by 3′-methyl-4-dimethyl-aminoazobenzene. Jpn. J. Cancer Res. 82, 397-402.
76. KENNEDY S., RETTINGER S., FLYE M.W. & PARKER-PONDER K. (1995) Experiments in transgenic mice show that hepatocytes are the source for postnatal liver growth and do not stream. Hepatol. 22, 160-168.
77. KESHET E., LYMAN S.D., WILLIAMS D.E., AHDERSON D.M., JENKINS N.A., COPELAND N.G. & PARADA L.F. (1991) Embryonic RNA expression patterns of the c-kit receptor and its cognate ligand suggests multiple functional roles in mouse development. EMBO J. 10, 2425-2435.
78. KIM T.-H., MARS W.M., STOLZ D.B., PETERSEN B.E. & MICHALOPOULOS G.K. (1997) Extracellular matrix remodeling at the early stages of liver regeneration in the rat. Hepatol. 26, 896-904.
79. KOUKOULIS G., RAYNER A., TAN K.C., WILLIAMS R. & PORTMANN B. (1992) Immunolocalization of regenerating cells after sub-massive liver necrosis using PCNA staining. J. Pathol. 166, 359-368.
80. KROESE E.D., BANNENBERG G., DOGTEROM P., NOACH A.B., NAGELKERKE J.F. & MEERMAN J.H. (1990) Lipid peroxidation and protein thiol. depletion are not involved in the cytotoxicity of N-hydroxy-2-acetylaminofluorene in isolated rat hepatocytes. Biochem., Pharmacol. 40, 1885-1892.
81. KURUMAYA H., OHTA G. & NAKANUMA Y. (1989) Endocrine cells in the intrahepatic biliary tree in normal livers and hepatolithiasis. Arch. Pathol. Lab. Med. 113, 143-147.
82. LEDDA G.M., SELLS M.A., YOKOYAMA S. & LOMBARDI B. (1983) Metabolic properties of isolated rat liver cell preparations enriched in epithelial cells other than hepatocytes. Int. J. Cancer 31, 231-237.
83. LEMIRE J.M. & FAUSTO N. (1991) Multiple alpha-fetoprotein RNAs in adult rat liver: cell type-specific expression and differential regulation. Cancer Res. 51, 4656-4664.
84. LEMIRE J.M., SHIOJIRI N. & 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.
85. LENZI R., LIU M.H., TARSETTI F., SLOTT P.A., ALPINI G., ZHAI W.R., PARONETTO F., LENZEN R. & TAVOLONI N. (1992) Histogenesis of bile duct-like cells proliferating during ethionine hepatocarcinogenesis. Evidence for a biliary epithelial nature of oval cells. Lab. Invest. 66, 390-402.
86. MAKINO Y., YAMAMOTO K. & TSUJI T. (1988) Three-dimensional arrangement of ductular structures formed by oval cells during hepatocarcinogenesis. Acta Med. Okayama 42, 143-150.
87. MARCEAU N. (1990) Cell lineages and differentiation programs in epidermal, urothelial and hepatic tissues and their neoplasms. Lab. Invest. 63, 4-20.
88. MARCEAU N., GERMAIN L., GOYETTE R., NOEL M. & 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.
89. MARSDEN E.R., HU Z., FUJIO K., NAKATSUKASA H., THORGEIRSSON S.S. & EVARTS R.P. (1992) Expression of acidic fibroblast growth factor in regenerating liver and during hepatic differentiation [see comments]. Lab. Invest. 67, 427-433.
90. MARTINEZ-HERNANDEZ A. & AMENTA P. (1995) The extracellular matrix in hepatic regeneration. FASEB J. 9, 1401-1410.
91. MATHIS G.A., WALLS S.A., D'AMICO P., GENGO T.F. & SIRICA A.E. (1989) Enzyme profile of rat bile ductular epithelial cells in reference to the resistance phenotype in hepatocarcinogenesis. Hepatol. 9, 477-485.
92. MEYBEHM M., FISCHER H.P. & PFEIFER U. (1993) Expression of HBs- and HBc-antigen in neoductular epithelium in chronic active hepatitis B. A further support for hepato-ductular metaplasia. Virchows Arch. B Cell Pathol. 63, 167-172.
93. MIETTINEN P.J., EBNER R., LOPEZ A.R. & DERYNCK R. (1994) TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 127, 2021-2036.
94. MILANI S., HERBST H., SCHUPPAN D., NIEDOBITEK G., KIM K.Y. & STEIN H. (1989) Vimentin expression of newly formed rat bile duct epithelial cells in secondary biliary fibrosis. Virchows Arch. A Pathol. Anat. Histopathol. 415, 237-242.
95. MILANI S., HERBST H., SCHUPPAN D., STEIN H. & SURRENTI C. (1991) Transforming growth factors beta 1 and beta 2 are differentially expressed in fibrotic liver disease. Am. J. Pathol. 139, 1221-1229.
96. MILLWARD-SADLER G.H. & JEZEQUEL A.-M. (1992) Normal histology and ultrastructure. In Wright's liver and biliary disease, Vol. 1 Eds G. H. Millward-Sadler, R. Wright & M. J. P. Arthur. Cambridge: W.B. Saunders Company Ltd. pp. 12-42.
97. MITAKA T., NORIOKA K., NAKAMURA T. & MOCHIZUKI Y. (1993) Effects of mitogens and co-mitogens on the formation of small-cell colonies in primary cultures of rat hepatocytes. J. Cell. Physiol. 157, 461-468.
98. MOLL R., FRANKE W.W., SCHILLER D.L., GEIGER B. & KREPLER R. (1982) The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 31, 11-24.
99. NAGY P., EVARTS R.P., MCMAHON J.B. & THOHGEIRSSON S.S. (1989) Role of TGF-beta in normal differentiation and oncogenesis in rat liver. Mol. Carcinog. 2, 345-354.
100. NAGY P., BISGAARD H.C. & THORGEIRSSON S.S. (1994) Expression of hepatic transcription factors during liver development and oval cell differentiation. J. Cell Biol. 126, 223-233.
101. NOMOTO M., UCHIKOSI Y., KAJIKAZAWA N., TANAKA Y. & ASAKURA H. (1992) Appearance of hepatocytelike cells in the interlobular bile ducts of human liver in various liver disease states. Hepatol. 16, 1199-1205.
102. NOVIKOFF P.M., IKEDA T., HIXSON D.C. & YAM A. (1991) Characterizations of and interactions between bile ductule cells and hepatocytes in early stages of rat hepatocarcinogenesis induced by ethionine. Am. J. Pathol. 139, 1351-1368.
103. NOVIKOFF P.M., YAM A. & OIKAWA I. (1996) Blast-like cell compartment in carcinogen-induced proliferating bile ductules. Am. J. Pathol. 148, 1473-1492.
104. OMORI M., EVARTS R.P., OMORI N., HU Z., MARSDEN E.R. & THORGEIRSSON S.S. (1997) Expression of alpha-fetoprotein and stem cell factor/c-kit system in bile duct ligated young rats. Hepatol. 25, 1115-1122.
105. ONOE T., KANEKO A., DEMPO K., OGAWA K. & MINASE T. (1975) Alpha-foetoprotein and early histological changes of hepatic tissue in DAB-hepatocarcinogenesis. Ann. NY Acad. Sci. 259, 168-180.
106. OPIE E.I. (1944) The pathogenesis of tumours of the liver produced by butter yellow. J. Exp. Med. 80, 231-246.
107. PAGAN R., LLOBERA M. & VILARO S. (1995) Epithelial-mesenchymal transition in cultured neonatal hepatocytes. Hepatol. 21, 820-831.
108. PAGAN R., MARTIN I., LLOBERA M. & VILARO S. (1997) Epithelial-mesenchymal transition of cultured rat neonatal hepatocytes is differentially regulated in response to epidermal growth factor and dimethyl sulfoxide. Hepatol. 25, 598-606.
109. PARK C.M., CHA I.H., CHUNG K.B., SUH W.H., LEE C.H., CHOI S.Y. & CHAE Y.S. (1991) Hepatocellular carcinoma in extrahepatic bile ducts. Acta Radiol. 32, 34-36.
110. PETERSEN B.E., ZAJAC V.F. & MICHALOPOULOS G.K. (1997) Bile ductular damage induced by methylene dianiline inhibits oval cell activation. Am. J. Pathol. 151, 905-909.
111. POTTEN C.S. & LOEFFLER M. (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Dev 110, 1001-1020.
112. POTTEN C.S., BOOTH C. & PRITCHARD D.M. (1997) The intestinal epithelial stem cell: the mucosal governor. Int. J. Exp. Pathol. 78, 219-243.
113. RAO K.N., SHINOZUKA H., KUNZ H.W. & GILL T.D. (1984) Enhanced susceptibility to a chemical carcinogen in rats carrying MHC-linked genes influencing development (GRC). Int. J. Cancer 34, 113-120.
114. RAO M.S., DWIVEDI R.S., YELDANDI A.V., SUBBARAO V., TAN X.D., USMAN M.I., THANGADA S., NEMALI M.R., KUMAR S. & SCARPELLI D.G. (1989) Role of periductal and ductular epithelial cells of the adult rat pancreas in pancreatic hepatocyte lineage. A change in the differentiation commitment. Am. J. Pathol. 134, 1069-1086.
115. RAY M.B., MENDENHALL C.L., FRENCH S.W. & GARTSIDE P.S. (1993) Bile duct changes in alcoholic liver disease. The Veterans Administration Cooperative Study Group. Liver 13, 36-45.
116. ROGLER L.E. (1997) Selective bipotential differentiation of mouse embryonic hepatoblasts in vitro. Am. J. Pathol. 150, 591-602.
117. ROSEN E.M., NIGAM S.K. & GOLDBERG I.D. (1994) Scatter factor and the c-met receptor: a paradigm for mesenchymal/epithelial interaction. J. Cell Biol. 127, 1783-1787.
118. ROSKAMS T., DE-VOS R., VAN-OORD J.J. & DESMET V. (1991) Cells with neuroendocrine features in regenerating human liver. APMIS Supplement 23, 32-39.
119. ROSKAMS T., CAMPOS R.V., DRUCKER D.J. & DESMET V.J. (1993a) Reactive human bile ductules express parathyroid hormone-related peptide. Histopathol 23, 11-19.
120. ROSKAMS T., WILLEMS M., CAMPOS R.V., DRUCKER D.J., YAP S.H. & DESMET V.J. (1993b) Parathyroid hormone-related peptide expression in primary and metastatic liver tumours. Histopathol 23, 519-525.
121. ROSKAMS T., MOSHAGE H., DEPLA E., WILLEMS M., DESMET V. & YAP P. (1995) Parathyroid hormone-related peptide is expressed and rapidly inducible in human liver cell cultures that have a bile duct phenotype. J. Hepatol. 23, 160-165.
122. SARRAF C.E., LALANI E.-N., GOLDING M., ANILKUMAR T.V., POULSOM R. & ALISON M.R. (1994) Cell behaviour in the acetylaminofluorene-treated regenerating rat liver. Light and microscopic observations. Am. J. Pathol. 145, 1114-1126.
123. SCHIRMACHER P., GEERTS A., PIETRANGELO A., DIENES H.P. & ROGLER C.E. (1992) Hepatocyte growth factor/hepatopoietin A is expressed in fat-storing cells from rat liver but not myofibroblast-like cells derived from fat-storing cells. Hepatol. 15, 5-11.
124. SCHMITT-GRAF A., DRUGER S., BOCHARD F., GABBIANI G. & DENK H. (1991) Modulation of alpha smooth muscle actin and desmin expression in perisinusoidal cells of normal and diseased human livers. Am. J. Pathol. 138, 1233-1242.
125. SELL S. (1980) Heterogeneity of alpha-fetoprotein (AFP) and albumin containing cells in normal and pathological permissive states for AFP production: AFP containing cells induced in adult rats recapitulate the appearance of AFP containing hepatocytes in fetal rats. Oncodev. Biol. Med. 1, 93-105.
126. SELL S. (1990) Is there a liver stem cell? Cancer Res. 50, 3811-3815.
127. SELL S. (1993a) Cellular origin of cancer: dedifferentiation or stem cell maturation arrest? Environ. Health Perspect. 5, 15-26.
128. SELL S. (1993b) The role of determined stem-cells in the cellular lineage of hepatocellular carcinoma. Int. J. Dev. Biol. 37, 189-201.
129. SELL S., LEFFERT H.L., SHINOZUKA H., LOMBARDI B. & GOCHMAN N. (1981) Rapid development of large numbers of alpha-fetoprotein-containing 'oval' cells in the liver of rats fed N-2-fluorenylacetamide in a choline-devoid diet. Gann 72, 479-487.
130. SELL S. & 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-fluorenylacetamide in a choline-deficient diet. Am. J. Pathol. 114, 287-300.
131. SELL S. & DUNSFORD H.A. (1989) Evidence for the stem cell origin of hepatocellular carcinoma and cholangiocarcinoma. Am. J. Pathol. 134, 1347-1363.
132. SELL S. & PIERCE G.B. (1994) Maturation arrest of stem cell differentiation is a common pathway for the cellular origin of teratocarcinomas and epithelial cancers. Lab. Invest. 70, 6-22.
133. SHAH K.D. & GERBER M.A. (1990) Development of intrahepatic bile ducts in humans. Possible role of laminin. Arch. Pathol. Lab. Med. 114, 597-600.
134. SHINAGAWA T., TADOKORO M., MAEYAMA S., MAEDA C., YAMAGUCHI S., MOROHOSHI T. & ISHIKAWA E. (1995) Alpha fetoprotein-producing acinar cell carcinoma of the pancreas showing multiple lines of differentiation. Virchows Arch. 426, 419-423.
135. SHIOJIRI N., LEMIRE J.M. & FAUSTO N. (1991) Cell lineages and oval cell progenitors in rat liver development. Cancer Res. 51, 2611-2620.
136. SIRICA A.E., GAINEY T.W. & MUMAW V.R. (1994) Ductular hepatocytes. Evidence for a bile ductular cell origin in furan-treated rats. Am. J. Pathol. 145, 375-383.
137. STAMATOGLOU S.C. & HUGHES R.C. (1994) Cell adhesion molecules in liver function and pattern formation. FASEB J. 8, 420-427.
138. STEINBERG P., STEINBRECHER R., RADAEVA S., SCHIRMACHER P., DIENES H.P., OESCH F. & BANNASCH P. (1994) Oval cell lines OC/CDE 6 and OC/CDE 22 give rise to cholangio-cellular and undifferentiated carcinomas after transformation. Lab. Invest. 71, 700-709.
139. STEINER J. & CARRUTHERS J. (1961) Studies on the fine structure of the terminal branches of the biliary tree. Am. J. Pathol. 38, 639-661.
140. STOKER M. & PERRYMAN M. (1985) An epithelial scatter factor released by embryo fibroblasts. J. Cell Sci. 77, 209-213.
141. STRAIN A.J., ISMAIL T., TSUBOUCHI H., ARAKAKI N., HISHIDA T., KITAMURA N., DAIKUHARA Y. & MCMASTER P. (1991) Native and recombinant human hepatocyte growth factors are highly potent promoters of DNA synthesis in both human and rat hepatocytes. J. Clin. Invest. 87, 1853-1857.
142. STRAIN A.J., WALLACE L., JOPLIN R., DAIKUHARA Y., ISHII T., KELLY D.A. & NEUBERGER J.M. (1995) Characterization of biliary epithelial cells isolated from needle biopsies of human liver in the presence of hepatocyte growth factor. Am. J. Pathol. 146, 537-545.
143. TANIGUCHI H., TOYOSHIMA T., FUKAO K. & NAKAUCHI H. (1996) Presence of hematopoietic stem cells in the adult liver [see comments]. Nat. Med. 2, 198-203.
144. TARSETTI F., LENZI R., SALVI R., SCHULER E., RIJHSINGHANI K., LENZEN R. & TAVOLONI N. (1993) Liver carcinogenesis associated with feeding of ethionine in a choline-free diet: evidence against a role of oval cells in the emergence of hepatocellular carcinoma. Hepatol. 18, 596-603.
145. TATEMATSU M., KAKU T., MEDLINE A. & FARBER E. (1985) Intestinal metaplasia as a common option of oval cells in relation to cholangiofibrosis in liver of rats exposed to 2-acetylaminofluorene. Lab. Invest. 52, 354-362.
146. TATENO C. & YOSHIZATO K. (1996) Long term cultivation of adult rat hepatocytes that undergo multiple cell divisions and express normal parenchymal phenotypes. Am. J. Pathol. 148, 383-392.
147. TERADA T. & NAKANUMA Y. (1993) Development of human intrahepatic peribiliary glands. Histological, keratin immunohistochemical, and mucus histochemical analyses [see comments]. Lab. Invest. 68, 261-269.
148. TERADA T., OKADA Y. & NAKANUMA Y. (1995) Expression of matrix proteinases during human intrahepatic bile duct development. A possible role in biliary cell migration. Am. J. Pathol. 147, 1207-1213.
149. THORGEIRSSON S.S., EVARTS R.P., BISGAARD H.C., FUJIO K. & HU Z. (1993) Hepatic stem cell compartment: activation and lineage commitment. Proc. Soc. Exp. Biol. Med. 204, 253-260.
150. TSAO M.S., SMITH J.D., NELSON K.G. & GRISHAM J.W. (1984) A diploid epithelial cell line from normal adult rat liver with phenotypic properties of 'oval' cells. Exp. Cell Res. 154, 38-52.
151. TSAO M.S., GRISHAM J.W., NELSON K.G. & SMITH J.D. (1985) Phenotypic and karyotypic changes induced in cultured rat hepatic epithelial cells that express the 'oval' cell phenotype by exposure to N-methyl-N′-nitro-N-nitrosoguanidine. Am. J. Pathol. 118, 306-315.
152. TSAO M.S. & GRISHAM J.W. (1987) Hepatocarcinomas, cholangiocarcinomas, and hepatoblastomas produced by chemically transformed cultured rat liver epithelial cells. A light- and electron-microscopic analysis. Am. J. Pathol. 127, 168-181.
153. TYNER A.L., GODBOUT R., COMPTON R.S. & TILGHMAN S.M. (1990) The ontogeny of alpha-fetoprotein gene expression in the mouse gastrointestinal tract. J. Cell Biol. 110, 915-927.
154. UCHIDA T. & PETERS R.L. (1983) The nature and origin of proliferated bile ductules in alcoholic liver disease. Am. J. Clin. Pathol. 79, 326-333.
155. VANDERSTEENHOVEN A.M., BURCHETTE J. & MICHALOPOULOS G. (1990) Characterization of ductular hepatocytes in end-stage cirrhosis. Arch. Pathol. Lab. Med. 114, 403-406.
156. VAN-EYKEN P., SCIOT R., VAN CALLEA F.,. d. S.K., MOERMAN P. & DESMET V.J. (1988a) The development of the intrahepatic bile ducts in man: a keratin-immunohistochemical study. Hepatol. 8, 1586-1595.
157. VAN-EYKEN P., SCIOT R. & DESMET V.J. (1988b) A cytokeratin immunohistochemical study of alcoholic liver disease: evidence that hepatocytes can express 'bile duct-type' cytokeratins. Histopathol 13, 605-617.
158. VAN-EYKEN P., SCIOT R. & DESMET V.J. (1989) A cytokeratin immunohistochemical study of cholestatic liver disease: evidence that hepatocytes can express 'bile duct-type' cytokeratins. Histopathol 15, 125-135.
159. WILSON J. & LEDUC E.H. (1958) Role of cholangioles in restoration of the liver of the mouse after dietary injury. J. Path. Bact. 76, 441-449.
160. WRIGHT N. & ALISON M. (1984) The conditional renewal populations: The Liver. In: The biology of epithelial cell populations 2, Oxford: Clarendon Press. pp. 873-980.
161. WU H., WADE M., KRALL L., GRISHAM J., XIONG Y. & VANDYKE T. (1996) Targeted in vivo expression of the cyclin dependent kinase inhibitor p21 halts hepatocyte cell cycle progression, postnatal liver development, and regeneration. Genes Dev. 10, 245-260.
162. YASUI O., MIURA N., TERADA K., KAWARADA Y., KOYAMA K. & SUGIYAMA T. (1997) Isolation of oval cells from Long-Evans Cinnamon rats and their transformation into hepatocytes in vivo in the rat liver. Hepatol. 25, 329-334.
163. YASWEN P., GOYETTE M., SHANK P.R. & FAUSTO N. (1985) Expression of c-Ki-ras, c-Ha-ras, and c-myc in specific cell types during hepatocarcinogenesis. Mol. Cell Biol. 5, 780-786.
164. YAVORKOVSKY L., LAI E., ILIC Z. & SELL S. (1995) Participation of small intraportal stem cells in the restitutive response of the liver to periportal necrosis induced by allyl alcohol. Hepatol. 21, 1702-1712.
165. ZAJICEK G., OREN J. & WEINREB M. (1985) The streaming liver. Liver 5, 293-300.
166. ZALATNAI A. & SCHALLY A.V. (1990) Hepatic lesions in Syrian golden hamsters with pancreatic carcinoma induced by N-nitrosobis (2-oxopropyl) amine (BOP). Acta Morph. Hung. 38, 119-130.