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PMID: 10980117 Published · ppublish English Journal Article

Temporal analysis of hepatocyte differentiation by small hepatocyte-like progenitor cells during liver regeneration in retrorsine-exposed rats.

The American journal of pathology ·Vol. 157 ·No. 3 ·2000-09-00 ·Pages 771-86

Gordon GJ, Coleman WB, Grisham JW

Abstract

Liver regeneration after two-thirds surgical partial hepatectomy (PH) in rats treated with the pyrrolizidine alkaloid retrorsine is accomplished through the activation, expansion, and differentiation of a population of small hepatocyte-like progenitor cells (SHPCs). We have examined expression of the major liver-enriched transcription factors, cytochrome P450 (CYP) enzymes, and other markers of hepatocytic differentiation in SHPCs during the protracted period of liver regeneration after PH in retrorsine-exposed rats. Early-appearing SHPCs (at 3-7 days after PH) express mRNAs for all of the major liver-enriched transcription factors at varying levels compared to fully differentiated hepatocytes. In addition, SHPCs lack (or have significantly reduced) expression of mRNA for hepatocyte markers tyrosine aminotransferase and alpha-1 antitrypsin, but their expression levels of mRNA and/or protein for WT1 and alpha-fetoprotein (AFP) are increased. With the exception of AFP expression, SHPCs resembled fully differentiated hepatocytes by 14 days after PH. Expression of AFP was maintained by most SHPCs through 14 days after PH, gradually declined through 23 days after PH, and was essentially absent from SHPC progeny by 30 days after PH. Furthermore, early appearing SHPCs lack (or have reduced expression) of hepatic CYP proteins known to be induced in rat livers after retrorsine exposure. The resistance of SHPCs to the mitoinhibitory effects of retrorsine may be directly related to a lack of CYP enzymes required to metabolize retrorsine to its toxic derivatives. These results suggest that SHPCs represent a unique parenchymal (less differentiated) progenitor cell population of adult rodent liver that is phenotypically distinct from fully differentiated hepatocytes, biliary epithelial cells, and (ductular) oval cells.

MeSH Terms
Animals Antineoplastic Agents, Phytogenic/pharmacology Biomarkers/analysis Cell Differentiation Cytochrome P-450 Enzyme System/genetics,metabolism DNA Primers/chemistry DNA-Binding Proteins/genetics,metabolism Dipeptidyl Peptidase 4/genetics Hepatectomy Immunoenzyme Techniques Liver/cytology,drug effects,metabolism,surgery Liver Regeneration/drug effects,physiology Male Pyrrolizidine Alkaloids/pharmacology RNA/analysis RNA, Messenger/metabolism Rats Rats, Inbred F344 Reverse Transcriptase Polymerase Chain Reaction Stem Cells/cytology,drug effects,metabolism Time Factors Transcription Factors/genetics,metabolism Tyrosine Transaminase/genetics,metabolism WT1 Proteins alpha 1-Antitrypsin/genetics,metabolism alpha-Fetoproteins/genetics,metabolism
Chemicals
Antineoplastic Agents, Phytogenic Biomarkers DNA Primers DNA-Binding Proteins Pyrrolizidine Alkaloids RNA, Messenger Transcription Factors WT1 Proteins alpha 1-Antitrypsin alpha-Fetoproteins RNA Cytochrome P-450 Enzyme System Tyrosine Transaminase Dipeptidyl Peptidase 4 retrorsine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Gordon G J
Department of Pathology and Laboratory Medicine, Curriculum in Toxicology, UNC Lineberger Comprehensive Cancer Center, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599, USA.
Coleman W B
Grisham J W
References (77)
77 references, click to expand
  1. Repression of the insulin-like growth factor II gene by the Wilms tumor suppressor WT1.
    Science. 1992 Jul 31;257(5070):674-8 PMID: 1323141
  2. Laser-capture microdissection: opening the microscopic frontier to molecular analysis.
    Trends Genet. 1998 Jul;14(7):272-6 PMID: 9676529
  3. Microdissection-based genetic discovery and analysis applied to cancer progression.
    Cancer J Sci Am. 1997 Sep-Oct;3(5):259-65 PMID: 9327146
  4. MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine.
    Cell. 1996 Nov 1;87(3):507-17 PMID: 8898203
  5. Oval cell differentiation into hepatocytes in the acetylaminofluorene-treated regenerating rat liver.
    Hepatology. 1995 Oct;22(4 Pt 1):1243-53 PMID: 7557877
  6. The effect of spironolactone treatment on the cytochrome P450-mediated metabolism of the pyrrolizidine alkaloid senecionine by hepatic microsomes from rats and guinea pigs.
    Toxicol Appl Pharmacol. 1994 Aug;127(2):314-9 PMID: 8048076
  7. The mouse multidrug resistance gene family: structural and functional analysis.
    Int Rev Cytol. 1993;137C:169-97 PMID: 8098020
  8. Oval cell proliferation and the origin of small hepatocytes in liver injury induced by D-galactosamine.
    Am J Pathol. 1991 Sep;139(3):535-52 PMID: 1716045
  9. Immuno-LCM: laser capture microdissection of immunostained frozen sections for mRNA analysis.
    Am J Pathol. 1999 Jan;154(1):61-6 PMID: 9916919
  10. Distribution of albumin and alpha-fetoprotein mRNAs in normal, hyperplastic, and preneoplastic rat liver.
    Am J Pathol. 1992 Sep;141(3):623-32 PMID: 1381559
  11. Monoclonal antibodies recognizing oval cells induced in the liver of rats by N-2-fluorenylacetamide or ethionine in a choline-deficient diet.
    Cancer Res. 1985 Aug;45(8):3750-60 PMID: 2410100
  12. Analysis of anterior pituitary hormone mRNA expression in immunophenotypically characterized single cells after laser capture microdissection.
    Lab Invest. 1999 Apr;79(4):511-2 PMID: 10212004
  13. CD34: structure, biology, and clinical utility.
    Blood. 1996 Jan 1;87(1):1-13 PMID: 8547630
  14. Expression and inducibility of P450 enzymes during liver ontogeny.
    Microsc Res Tech. 1997 Dec 1;39(5):424-35 PMID: 9408909
  15. Cellular response to partial hepatectomy.
    Proc Soc Exp Biol Med. 1963 Feb;112:338-40 PMID: 14033567
  16. Expression and activity of P-glycoprotein, a multidrug efflux pump, in human hematopoietic stem cells.
    Cell. 1991 Jul 12;66(1):85-94 PMID: 1712673
  17. Gene expression profiles of laser-captured adjacent neuronal subtypes.
    Nat Med. 1999 Jan;5(1):117-22 PMID: 9883850
  18. Induction of rat WT1 gene expression correlates with human chromosome 11p11.2-p12-mediated suppression of tumorigenicity in rat liver epithelial tumor cell lines.
    Int J Oncol. 1999 May;14(5):957-63 PMID: 10200348
  19. Occurrence and inducibility of cytochrome P450IIIA in maternal and fetal rats during prenatal development.
    Biochemistry. 1989 May 30;28(11):4871-9 PMID: 2765516
  20. 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
  21. Evaluation of the differentiation potential of WB-F344 rat liver epithelial stem-like cells in vivo. Differentiation to hepatocytes after transplantation into dipeptidylpeptidase-IV-deficient rat liver.
    Am J Pathol. 1997 Aug;151(2):353-9 PMID: 9250149
  22. Isolation, propagation, and characterization of rat liver serosal mesothelial cells.
    Am J Pathol. 1994 Dec;145(6):1432-43 PMID: 7992846
  23. The kinetics of cellular proliferation in regenerating liver.
    J Cell Biol. 1968 Mar;36(3):551-65 PMID: 5645547
  24. WT1 suppresses synthesis of the epidermal growth factor receptor and induces apoptosis.
    EMBO J. 1995 Oct 2;14(19):4662-75 PMID: 7588596
  25. Metabolic properties of isolated rat liver cell preparations enriched in epithelial cells other than hepatocytes.
    Int J Cancer. 1983 Feb 15;31(2):231-7 PMID: 6131033
  26. Repression of the transforming growth factor-beta 1 gene by the Wilms' tumor suppressor WT1 gene product.
    Mol Endocrinol. 1994 May;8(5):595-602 PMID: 8058069
  27. Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat.
    Hepatology. 1998 Feb;27(2):433-45 PMID: 9462642
  28. Pattern of serum protein gene expression in mouse visceral yolk sac and foetal liver.
    EMBO J. 1984 Aug;3(8):1881-5 PMID: 6479150
  29. Biochemistry of multidrug resistance mediated by the multidrug transporter.
    Annu Rev Biochem. 1993;62:385-427 PMID: 8102521
  30. Antigenic phenotypes common to rat oval cells, primary hepatocellular carcinomas and developing bile ducts.
    Carcinogenesis. 1997 Jun;18(6):1169-75 PMID: 9214599
  31. Sensitive immunoassay of tissue cell proteins procured by laser capture microdissection.
    Am J Pathol. 2000 Feb;156(2):445-52 PMID: 10666374
  32. Induction of cytochrome P450 enzymes in the livers of rats treated with the pyrrolizidine alkaloid retrorsine.
    Exp Mol Pathol. 2000 Aug;69(1):17-26 PMID: 10891289
  33. Expression of hepatic transcription factors during liver development and oval cell differentiation.
    J Cell Biol. 1994 Jul;126(1):223-33 PMID: 8027180
  34. Restoration of serum albumin levels in nagase analbuminemic rats by hepatocyte transplantation.
    Hepatology. 1999 Jan;29(1):75-81 PMID: 9862853
  35. Regulation of the proto-oncogenes bcl-2 and c-myc by the Wilms' tumor suppressor gene WT1.
    Cancer Res. 1995 Nov 15;55(22):5386-9 PMID: 7585606
  36. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues.
    Proc Natl Acad Sci U S A. 1987 Nov;84(21):7735-8 PMID: 2444983
  37. Differentiation status of rat ductal cells and ethionine-induced hepatic carcinomas defined with surface-reactive monoclonal antibodies.
    Exp Mol Pathol. 2000 Jun;68(3):152-69 PMID: 10816384
  38. Wholesale hepatocytic differentiation in the rat from ductular oval cells, the progeny of biliary stem cells.
    J Hepatol. 1997 Feb;26(2):343-52 PMID: 9059956
  39. Laser capture microdissection.
    Science. 1996 Nov 8;274(5289):998-1001 PMID: 8875945
  40. Transcriptional control in hepatocytes: a window on development.
    Trends Biochem Sci. 1991 Nov;16(11):427-30 PMID: 1776173
  41. The development of the hepatic megalocytosis of chronic pyrrolizidine alkaloid poisoning.
    Am J Pathol. 1969 Sep;56(3):405-21 PMID: 5822314
  42. Isolation, biochemical characterization, long-term culture, and phenotype modulation of oval cells from carcinogen-fed rats.
    Exp Cell Res. 1993 Feb;204(2):198-209 PMID: 7679995
  43. 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
  44. Multiple alpha-fetoprotein RNAs in adult rat liver: cell type-specific expression and differential regulation.
    Cancer Res. 1991 Sep 1;51(17):4656-64 PMID: 1714792
  45. Multiplex genotype analysis of invasive carcinoma and accompanying proliferative lesions microdissected from breast tissue.
    J Mol Diagn. 2000 Feb;2(1):29-36 PMID: 11272899
  46. Differential expression of prolactin receptor (PRLR) in normal and tumorous adrenal tissues: separation of cellular endocrine compartments by laser capture microdissection (LCM).
    Endocr Res. 1998 Aug-Nov;24(3-4):857-62 PMID: 9888587
  47. How cancer cells evade chemotherapy: sixteenth Richard and Hinda Rosenthal Foundation Award Lecture.
    Cancer Res. 1993 Feb 15;53(4):747-54 PMID: 8094031
  48. Ribonucleic acid isolated by cesium chloride centrifugation.
    Biochemistry. 1974 Jun 4;13(12):2633-7 PMID: 4831907
  49. Expression of the alpha-fetoprotein gene in adult rat liver.
    Arch Biochem Biophys. 1989 Apr;270(1):267-76 PMID: 2467624
  50. An antigenic portrait of the liver during carcinogenesis.
    Pathobiology. 1990;58(2):65-77 PMID: 2193646
  51. Wilms' tumor suppressor gene expression in rat and human mesothelioma.
    Cancer Res. 1994 Jun 15;54(12):3101-6 PMID: 8205524
  52. Differential patterns of expression of three C/EBP isoforms, HNF-1, and HNF-4 after partial hepatectomy in rats.
    Exp Cell Res. 1993 Sep;208(1):248-56 PMID: 8359219
  53. Increased expression of the insulin-like growth factor I receptor gene, IGF1R, in Wilms tumor is correlated with modulation of IGF1R promoter activity by the WT1 Wilms tumor gene product.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5828-32 PMID: 8390684
  54. Liver regeneration in rats with retrorsine-induced hepatocellular injury proceeds through a novel cellular response.
    Am J Pathol. 2000 Feb;156(2):607-19 PMID: 10666390
  55. In vivo differentiation of rat liver oval cells into hepatocytes.
    Cancer Res. 1989 Mar 15;49(6):1541-7 PMID: 2466557
  56. Precursor-product relationship between oval cells and hepatocytes: comparison between tritiated thymidine and bromodeoxyuridine as tracers.
    Carcinogenesis. 1996 Oct;17(10):2143-51 PMID: 8895481
  57. Isolation, culture, and transplantation of intrahepatic biliary epithelial cells and oval cells.
    Pathobiology. 1990;58(1):44-64 PMID: 2187478
  58. Partial cloning of rat CD34 cDNA and expression during stem cell-dependent liver regeneration in the adult rat.
    Hepatology. 1997 Sep;26(3):720-7 PMID: 9303503
  59. Laser capture microdissection of single cells from complex tissues.
    Biotechniques. 1999 Feb;26(2):328-35 PMID: 10023545
  60. A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver; autoradiography with thymidine-H3.
    Cancer Res. 1962 Aug;22:842-9 PMID: 13902009
  61. Dose-related inhibition of the drug-metabolizing enzymes of rat liver by the pyrrolizidine alkaloid, monocrotaline.
    J Pharm Pharmacol. 1987 May;39(5):386-8 PMID: 2886588
  62. Regulation of the differentiation of diploid and some aneuploid rat liver epithelial (stemlike) cells by the hepatic microenvironment.
    Am J Pathol. 1993 May;142(5):1373-82 PMID: 8494041
  63. Developmental expression and in situ localization of the phenobarbital-inducible rat hepatic mRNAs for cytochromes CYP2B1, CYP2B2, CYP2C6, and CYP3A1.
    Mol Pharmacol. 1990 Oct;38(4):462-70 PMID: 2233688
  64. Role of thyroid hormone in stimulating liver repopulation in the rat by transplanted hepatocytes.
    Hepatology. 1999 Oct;30(4):903-13 PMID: 10498641
  65. Enzyme profile of rat bile ductular epithelial cells in reference to the resistance phenotype in hepatocarcinogenesis.
    Hepatology. 1989 Mar;9(3):477-85 PMID: 2563986
  66. Cell lineages and oval cell progenitors in rat liver development.
    Cancer Res. 1991 May 15;51(10):2611-20 PMID: 1708696
  67. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells.
    Cell. 1982 Nov;31(1):11-24 PMID: 6186379
  68. Laser capture microdissection: molecular analysis of tissue.
    Science. 1997 Nov 21;278(5342):1481,1483 PMID: 9411767
  69. Hepatic stem cells in liver regeneration.
    FASEB J. 1996 Sep;10(11):1249-56 PMID: 8836038
  70. The WT1 Wilms' tumor suppressor gene: how much do we really know?
    Biochim Biophys Acta. 1996 May 16;1287(1):1-28 PMID: 8639704
  71. Expression analysis of the mixed function oxidase system in rat brain by the polymerase chain reaction.
    Mol Cell Biochem. 1993 Mar 24;120(2):171-9 PMID: 8487757
  72. Enzymic differentiation in mammalian liver injection of fetal rats with hormones causes the premature formation of liver enzymes.
    Science. 1969 Feb 28;163(3870):891-5 PMID: 4387727
  73. Physiological and pathophysiological regulation of cytochrome P450.
    Drug Metab Dispos. 1998 Dec;26(12):1232-40 PMID: 9860933
  74. Involvement of cytochrome P450 3A in the metabolism and covalent binding of 14C-monocrotaline in rat liver microsomes.
    J Biochem Mol Toxicol. 1998;12(3):157-66 PMID: 9522275
  75. Constitutive expression of hepatic cytochrome P450 genes.
    FASEB J. 1996 Aug;10(10):1112-7 PMID: 8751713
  76. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  77. 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
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
2000-09-00
Pages
771-86
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1885692
Subset
IM
Grants
NCI NIH HHS · R01 CA078434 · United States
NCI NIH HHS · CA29323 · United States
NCI NIH HHS · CA78434 · United States
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