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PMID: 10854224 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Proliferation and differentiation of fetal liver epithelial progenitor cells after transplantation into adult rat liver.

The American journal of pathology ·Vol. 156 ·No. 6 ·2000-06-00 ·Pages 2017-31

Dabeva MD, Petkov PM, Sandhu J, Oren R, Laconi E, Hurston E, Shafritz DA

Abstract

To identify cells that have the ability to proliferate and differentiate into all epithelial components of the liver lobule, we isolated fetal liver epithelial cells (FLEC) from ED 14 Fischer (F) 344 rats and transplanted these cells in conjunction with two-thirds partial hepatectomy into the liver of normal and retrorsine (Rs) treated syngeneic dipeptidyl peptidase IV mutant (DPPIV(-)) F344 rats. Using dual label immunohistochemistry/in situ hybridization, three subpopulations of FLEC were identified: cells expressing both alpha-fetoprotein (AFP) and albumin, but not CK-19; cells expressing CK-19, but not AFP or albumin, and cells expressing AFP, albumin, and cytokeratins-19 (CK-19). Proliferation, differentiation, and expansion of transplanted FLEC differed significantly in the two models. In normal liver, 1 to 2 weeks after transplantation, mainly cells with a single phenotype, hepatocytic (expressing AFP and albumin) or bile ductular (expressing only CK-19), had proliferated. In Rs-treated rats, in which the proliferative capacity of endogenous hepatocytes is impaired, transplanted cells showed mainly a dual phenotype (expressing both AFP/albumin and CK-19). One month after transplantation, DPPIV(+) FLEC engrafted into the parenchyma exhibited an hepatocytic phenotype and generated new hepatic cord structures. FLEC, localized in the vicinity of bile ducts, exhibited a biliary epithelial phenotype and formed new bile duct structures or were incorporated into pre-existing bile ducts. In the absence of a proliferative stimulus, ED 14 FLEC did not proliferate or differentiate. Our results demonstrate that 14-day fetal liver contains lineage committed (unipotential) and uncommitted (bipotential) progenitor cells exerting different repopulating capacities, which are affected by the proliferative status of the recipient liver and the host site within the liver where the transplanted cells become engrafted. These findings have important implications in future studies directed toward liver repopulation and ex vivo gene therapy.

MeSH Terms
Animals Bile Ducts/cytology Cell Differentiation/drug effects Cell Division/drug effects Cell Line Cell Transplantation Epithelial Cells/cytology Fetal Tissue Transplantation Hepatectomy/methods Liver/cytology,embryology,surgery Mitogens/pharmacology Postoperative Period Pyrrolizidine Alkaloids/pharmacology Rats Rats, Inbred F344 Stem Cells/cytology Transplantation, Isogeneic Triiodothyronine/pharmacology
Chemicals
Mitogens Pyrrolizidine Alkaloids Triiodothyronine retrorsine
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Dabeva M D
Marion Bessin Liver Research Center, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
Petkov P M
Sandhu J
Oren R
Laconi E
Hurston E
Shafritz D A
References (53)
53 references, click to expand
  1. Histochemical and ultrastructural demonstration of gamma-glutamyl transpeptidase activity.
    J Histochem Cytochem. 1969 Aug;17(8):517-26 PMID: 5816239
  2. HISTOGENESIS OF THE LIVER.
    Ann N Y Acad Sci. 1963 Dec 30;111:8-24 PMID: 14085884
  3. Localization in the cell cycle of the antimitotic action of the pyrrolizidine alkaloid, lasiocarpine and of its metabolite, dehydroheliotridine.
    Chem Biol Interact. 1975 Mar;10(3):185-97 PMID: 1126005
  4. An experimental analysis of liver development.
    Med Biol. 1975 Dec;53(6):427-55 PMID: 765644
  5. Improved method for the histochemical demonstration of glucose-6-phosphatase activity.
    Histochemistry. 1978 Aug 25;57(2):107-17 PMID: 211104
  6. Differentiation of the mouse hepatic primordium. I. An analysis of tissue interactions in hepatocyte differentiation.
    Cell Differ. 1980 Oct;9(5):269-79 PMID: 7438211
  7. The establishment of hepatocyte cell surface polarity during fetal liver development.
    Dev Biol. 1987 Sep;123(1):73-84 PMID: 3305113
  8. Intrahepatic bile duct development in the rat: a cytokeratin-immunohistochemical study.
    Lab Invest. 1988 Jul;59(1):52-9 PMID: 2455831
  9. 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 Sep 1;48(17):4909-18 PMID: 2457432
  10. Alteration in the regulation of plasma membrane glycoproteins of the hepatocyte during ontogeny.
    Exp Cell Res. 1990 Apr;187(2):299-308 PMID: 1969354
  11. An antigenic portrait of the liver during carcinogenesis.
    Pathobiology. 1990;58(2):65-77 PMID: 2193646
  12. A Fischer rat substrain deficient in dipeptidyl peptidase IV activity makes normal steady-state RNA levels and an altered protein. Use as a liver-cell transplantation model.
    Biochem J. 1991 Feb 1;273 ( Pt 3):497-502 PMID: 1705112
  13. Cell lineages and oval cell progenitors in rat liver development.
    Cancer Res. 1991 May 15;51(10):2611-20 PMID: 1708696
  14. Hepatocyte differentiation initiates during endodermal-mesenchymal interactions prior to liver formation.
    Development. 1991 Sep;113(1):217-25 PMID: 1764997
  15. Evidence of metabolic activity of adult and fetal rat hepatocytes transplanted into solid supports.
    Transplantation. 1992 Aug;54(2):210-4 PMID: 1496531
  16. Proliferation and differentiation of fetal liver cells transplanted into rat spleen.
    Transplant Proc. 1992 Dec;24(6):2960-1 PMID: 1361269
  17. Differentiation of functional hepatocytes and biliary epithelial cells from immature hepatocytes of the fetal mouse in vitro.
    Anat Embryol (Berl). 1993 Mar;187(3):221-9 PMID: 8470822
  18. Cell lineages in hepatic development and the identification of progenitor cells in normal and injured liver.
    Proc Soc Exp Biol Med. 1993 Dec;204(3):237-41 PMID: 7694302
  19. Activation, proliferation, and differentiation of progenitor cells into hepatocytes in the D-galactosamine model of liver regeneration.
    Am J Pathol. 1993 Dec;143(6):1606-20 PMID: 7504886
  20. Characterization and enrichment of fetal rat hepatoblasts by immunoadsorption ("panning") and fluorescence-activated cell sorting.
    Hepatology. 1994 Apr;19(4):999-1006 PMID: 7511129
  21. Cellular origin of cancer: dedifferentiation or stem cell maturation arrest?
    Environ Health Perspect. 1993 Dec;101 Suppl 5:15-26 PMID: 7516873
  22. Transplantation of normal hepatocytes modulates the development of chronic liver lesions induced by a pyrrolizidine alkaloid, lasiocarpine.
    Carcinogenesis. 1995 Jan;16(1):139-42 PMID: 7834799
  23. Specialization switch in differentiating embryonic rat liver progenitor cells in response to sodium butyrate.
    Exp Cell Res. 1995 Mar;217(1):22-30 PMID: 7867717
  24. Demonstration of differentiation in hepatocyte progenitor cells using dipeptidyl peptidase IV deficient mutant rats.
    Cell Mol Biol Res. 1995;41(1):39-47 PMID: 7550451
  25. Long-term effects of intrasplenically transplanted adult hepatocytes and fetal liver in hyperbilirubinemic Gunn rats.
    Transpl Int. 1995;8(4):262-7 PMID: 7546147
  26. Maturation-dependent changes in the regulation of liver-specific gene expression in embryonal versus adult primary liver cultures.
    Differentiation. 1995 Sep;59(2):95-102 PMID: 8522072
  27. Identification of bipotential progenitor cells in human liver development.
    Hepatology. 1996 Mar;23(3):476-81 PMID: 8617427
  28. Studies of liver repopulation using the dipeptidyl peptidase IV-deficient rat and other rodent recipients: cell size and structure relationships regulate capacity for increased transplanted hepatocyte mass in the liver lobule.
    Hepatology. 1996 Mar;23(3):482-96 PMID: 8617428
  29. Dual phenotypic expression of hepatocytes and bile ductular markers in developing and preneoplastic rat liver.
    Carcinogenesis. 1996 Feb;17(2):251-9 PMID: 8625446
  30. Molecular genetics of early liver development.
    Annu Rev Physiol. 1996;58:231-51 PMID: 8815794
  31. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control.
    Genes Dev. 1996 Jul 1;10(13):1670-82 PMID: 8682297
  32. Promotion by estriol of the development of grafted fetal livers in mice.
    Arch Histol Cytol. 1995 Dec;58(5):591-8 PMID: 8845241
  33. Pluripotential liver stem cells: facultative stem cells located in the biliary tree.
    Cell Prolif. 1996 Jul;29(7):373-402 PMID: 8883463
  34. STAT signaling is active during early mammalian development.
    Dev Dyn. 1997 Feb;208(2):190-8 PMID: 9022056
  35. Murine gastrulation requires HNF-4 regulated gene expression in the visceral endoderm: tetraploid rescue of Hnf-4(-/-) embryos.
    Development. 1997 Jan;124(2):279-87 PMID: 9053305
  36. Selective bipotential differentiation of mouse embryonic hepatoblasts in vitro.
    Am J Pathol. 1997 Feb;150(2):591-602 PMID: 9033273
  37. Hepatocyte transplantation: progress toward liver repopulation.
    Prog Liver Dis. 1996;14:199-222 PMID: 9055579
  38. Liver regeneration.
    Science. 1997 Apr 4;276(5309):60-6 PMID: 9082986
  39. Use of a rat cDNA probe specific for the Y chromosome to detect male-derived cells.
    J Androl. 1997 May-Jun;18(3):289-93 PMID: 9203057
  40. Differentiation of pancreatic epithelial progenitor cells into hepatocytes following transplantation into rat liver.
    Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7356-61 PMID: 9207095
  41. Antigenic phenotypes common to rat oval cells, primary hepatocellular carcinomas and developing bile ducts.
    Carcinogenesis. 1997 Jun;18(6):1169-75 PMID: 9214599
  42. Enzymatic activity and expression of cytochrome P450 LA omega within intrasplenically transplanted fetal hepatocytes in spontaneously hypertensive rats.
    Cell Transplant. 1997 Sep-Oct;6(5):531-4 PMID: 9331507
  43. Fetal rat hepatocytes: isolation, characterization, and transplantation in the Nagase analbuminemic rats.
    Transplantation. 1997 Nov 15;64(9):1240-8 PMID: 9371663
  44. The cut-homeodomain transcriptional activator HNF-6 is coexpressed with its target gene HNF-3 beta in the developing murine liver and pancreas.
    Dev Biol. 1997 Dec 15;192(2):228-46 PMID: 9441664
  45. Maturation-dependent gene expression in a conditionally transformed liver progenitor cell line.
    In Vitro Cell Dev Biol Anim. 1998 Mar;34(3):247-58 PMID: 9557943
  46. Long-term, near-total liver replacement by transplantation of isolated hepatocytes in rats treated with retrorsine.
    Am J Pathol. 1998 Jul;153(1):319-29 PMID: 9665494
  47. In situ hybridization with 33P-labeled RNA probes for determination of cellular expression patterns of liver transcription factors in mouse embryos.
    Methods. 1998 Sep;16(1):29-41 PMID: 9774514
  48. GATA transcription factors as potentiators of gut endoderm differentiation.
    Development. 1998 Dec;125(24):4909-17 PMID: 9811575
  49. Liver regeneration and alpha-fetoprotein messenger RNA expression in the retrorsine model for hepatocyte transplantation.
    Cancer Res. 1998 Dec 15;58(24):5825-34 PMID: 9865742
  50. Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins.
    Dev Biol. 1999 May 1;209(1):1-10 PMID: 10208738
  51. Initiation of mammalian liver development from endoderm by fibroblast growth factors.
    Science. 1999 Jun 18;284(5422):1998-2003 PMID: 10373120
  52. Role of thyroid hormone in stimulating liver repopulation in the rat by transplanted hepatocytes.
    Hepatology. 1999 Oct;30(4):903-13 PMID: 10498641
  53. The development of the hepatic megalocytosis of chronic pyrrolizidine alkaloid poisoning.
    Am J Pathol. 1969 Sep;56(3):405-21 PMID: 5822314
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
2000-06-00
Pages
2017-31
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1850065
Subset
IM
Grants
NIDDK NIH HHS · P30 DK041296 · United States
NIDDK NIH HHS · R01 DK056496 · United States
NIDDK NIH HHS · R01 DK017609 · United States
NIDDK NIH HHS · R01 DK17609 · United States
NIDDK NIH HHS · R01 DK56496 · United States
NIDDK NIH HHS · P30 DK41296 · United States
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