Hepatocyte nuclear factor-1 as marker of epithelial phenotype reveals marrow-derived hepatocytes, but not duct cells, after liver injury in mice

Stem Cells

Volumn 26, Issue 7, 2008, Pages 1768-1777

  Swenson, E Scott ^a   Guest, Ian ^b   Ilic, Zoran ^c   Mazzeo Helgevold, Maria ^a   Lizardi, Pablo ^a   Hardiman, Camille ^a   Sell, Stewart ^b,c   Krause, Diane S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WADSWORTH CENTER   (United States)

^c ORDWAY RESEARCH INSTITUTE   (United States)

Author keywords

Bone marrow transplant; Ductal proliferation; Green fluorescent protein; Hepatocyte nuclear factor 1; Liver progenitor cell

Indexed keywords

1,4 DIHYDRO 2,4,6 TRIMETHYL 3,5 PYRIDINEDICARBOXYLIC ACID DIETHYL ESTER; CARBON TETRACHLORIDE; GREEN FLUORESCENT PROTEIN; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEPATOCYTE NUCLEAR FACTOR 1BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; IMMUNOFLUORESCENCE; LIVER CELL; LIVER INJURY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STEM CELL TRANSPLANTATION; Y CHROMOSOME;

ANIMALS; BONE MARROW CELLS; CARBON TETRACHLORIDE; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HEPATOCYTE NUCLEAR FACTOR 1; HEPATOCYTES; LIVER; MALE; MICE; MICE, KNOCKOUT; PHENOTYPE; PYRIDINES;

MUS;

EID: 55049141152     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2008-0148     Document Type: Article

References (54)

1. Dexter TM, Spooncer E. Growth and differentiation in the hemopoietic system. Annu Rev Cell Biol 1987;3:423-441.
2. Orkin S. Hematopoietic stem cells: Molecular diversification and developmental interrelationships. In: Marshak D, Gardner RL, Gottlieb D, eds. Stem Cell Biology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2001:289-306.
3. Bonnet DA. Haematopoietic stem cells. J Pathol 2002;197:430-440.
4. Herzog EL, Chai L, Krause DS. Plasticity of marrow-derived stem cells. Blood 2003;102:3483-3493.
5. Eisenberg LM, Eisenberg CA. Stem cell plasticity, cell fusion, and transdifferentiation. Birth Defects Res C Embryo Today Rev 2003;69:209-218.
6. Theise N, Nimmakayalu M, Gardner R et al. Liver from bone marrow in humans. Hepatology 2000;32:11-16.
7. Krause DS, Theise ND, Collector MI et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001;105:369-377.
8. Simard A, Rivest S. Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J 2004;18:998-1000.
9. Nygren JM, Jovinge S, Breitbach M et al. Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation. Nat Med 2004;10:494-501.
10. Ianus A, Holz GG, Theise ND et al. In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion. J Clin Invest 2003;111:843-850.
11. Theise ND, Henegariu O, Grove J et al. Radiation pneumonitis in mice. A severe injury model for pneumocyte engraftment from bone marrow. Exp Hematol 2002;30:1333-1338.
12. Poulsom R, Forbes SJ, Hodivala-Dilke K et al. Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 2001;195:229-235.
13. Gussoni E, Soneoka Y, Strickland CD et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 1999;401:390-394.
14. Thorgeirsson SS, Grisham JW. Hematopoietic cells as hepatocyte stem cells: A critical review of the evidence. Hepatology 2006;43:2-8.
15. Bucher NL. Regeneration of mammalian liver. Int Rev Cytol 1963;15:245-300.
16. Grisham JW. A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver; autoradiography with thymidine-H3. Cancer Res 1962;22:842-849.
17. Portmann B, Talbot IC, Day DW et al. Histopathological changes in the liver following a paracetamol overdose: Correlation with clinical and biochemical parameters. J Pathol 1975;117:169-181.
18. Craig CE, Quaglia A, Selden C et al. The histopathology of regeneration in massive hepatic necrosis. Semin Liver Dis 2004;24:49-64.
19. Farber E. Similarities in the sequence of early histological changes induced in the liver of the rat by ethionine, 2-acetylamino-fluorene, and 3́-methyl-4-dimethylaminoazobenzene. Cancer Res 1956;16:142-148.
20. Theise ND, Saxena R, Portmann BC et al. The canals of Hering and hepatic stem cells in humans. Hepatology 1999;30:1425-1433.
21. Evarts RP, Nagy P, Nakatsukasa H et al. In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res 1989;49:1541-1547.
22. Fujio K, Evarts RP, Hu Z et al. Expression of stem cell factor and its receptor, c-kit, during liver regeneration from putative stem cells in adult rat. Lab Invest 1994;70:511-516.
23. Evarts RP, Nagy P, Marsden E et al. A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 1987;8:1737-1740.
24. Crosby HA, Kelly DA, Strain AJ. Human hepatic stem-like cells isolated using c-kit or CD34 can differentiate into biliary epithelium. Gastroenterology 2001;120:534-544.
25. Petersen BE, Grossbard B, Hatch H et al. Mouse A6-positive hepatic oval cells also express several hematopoietic stem cell markers. Hepatology 2003;37:632-640.
26. Petersen BE, Goff JP, Greenberger JS et al. Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat. Hepatology 1998;27:433-445.
27. Yovchev MI, Grozdanov PN, Zhou H et al. Identification of adult hepatic progenitor cells capable of repopulating injured rat liver. Hepatology 2008;47:636-647.
28. Dezso K, Jelnes P, Laszlo V et al. Thy-1 is expressed in hepatic myofibroblasts and not oval cells in stem cell-mediated liver regeneration. Am J Pathol 2007;171:1529-1537.
29. Dudas J, Mansuroglu T, Batusic D et al. Thy-1 is an in vivo and in vitro marker of liver myofibroblasts. Cell Tissue Res 2007;329:503-514.
30. Shimano K, Satake M, Okaya A et al. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am J Pathol 2003;163:3-9.
31. Libbrecht L, Roskams T. Hepatic progenitor cells in human liver diseases. Semin Cell Dev Biol 2002;13:389-396.
32. Brulport M, Schormann W, Bauer A et al. Fate of extrahepatic human stem and precursor cells after transplantation into mouse livers. Hepatology 2007;46:861-870.
33. Petersen BE, Bowen WC, Patrene KD et al. Bone marrow as a potential source of hepatic oval cells. Science 1999;284:1168-1170.
34. Oh SH, Witek RP, Bae SH et al. Bone marrow-derived hepatic oval cells differentiate into hepatocytes in 2-acetylaminofluorene/partial hepatectomy-induced liver regeneration. Gastroenterology 2007;132:1077-1087.
35. Menthena A, Deb N, Oertel M et al. Bone marrow progenitors are not the source of expanding oval cells in injured liver. STEM CELLS 2004;22:1049-1061.
36. Dabeva MD, Hwang SG, Vasa SR et al. Differentiation of pancreatic epithelial progenitor cells into hepatocytes following transplantation into rat liver. Proc Natl Acad Sci U S A 1997;94:7356-7361.
37. Micouin A, Bauvois B. Expression of dipeptidylpeptidase IV (DPP IV/CD26) activity on human myeloid and B lineage cells, and cell growth suppression by the inhibition of DPP IV activity. Adv Exp Med Biol 1997;421:201-205.
38. Bauvois B, Sanceau J, Wietzerbin J. Human U937 cell surface peptidase activities: Characterization and degradative effect on tumor necrosis factor-alpha. Eur J Immunol 1992;22:923-930.
39. Pontoglio M, Barra J, Hadchouel M et al. Hepatocyte nuclear factor 1 inactivation results in hepatic dysfunction, phenylketonuria, and renal Fanconi syndrome. Cell 1996;84:575-585.
40. Okabe M, Ikawa M, Kominami K et al. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997;407:313-319.
41. Grompe M, al-Dhalimy M, Finegold M et al. Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev 1993;7:2298-2307.
42. Grompe M, Lindstedt S, al-Dhalimy M et al. Pharmacological correction of neonatal lethal hepatic dysfunction in a murine model of hereditary tyrosinaemia type I. Nat Genet 1995;10:453-460.
43. Lagasse E, Connors H, Al-Dhalimy M et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6:1229-1234.
44. Wang X, Willenbring H, Akkari Y et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 2003;422:897-901.
45. Donnelly DS, Zelterman D, Sharkis S et al. Functional activity of murine CD34+ and CD34- hematopoietic stem cell populations. Exp Hematol 1999;27:788-796.
46. Swenson ES, Price JG, Brazelton T et al. Limitations of green fluorescent protein as a cell lineage marker. STEM CELLS 2007;25:2593-2600.
47. Theise ND, Badve S, Saxena R et al. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 2000;31:235-240.
48. Herzog EL, Van Arnam J, Hu B et al. Lung-specific nuclear reprogramming is accompanied by heterokaryon formation and Y chromosome loss following bone marrow transplantation and secondary inflammation. FASEB J 2007;21:2592-2601.
49. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-872.
50. Yu J, Vodyanik MA, Smuga-Otto K et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
51. Hengstler JG, Brulport M, Schormann W et al. Generation of human hepatocytes by stem cell technology: Definition of the hepatocyte. Expert Opin Drug Metab Toxicol 2005;1:61-74.
52. Wang X, Foster M, Al-Dhalimy M et al. The origin and liver repopulating capacity of murine oval cells. Proc Natl Acad Sci U S A 2003;100 Suppl 1:11881-11888.
53. Moritoki Y, Ueno Y, Kanno N et al. Lack of evidence that bone marrow cells contribute to cholangiocyte repopulation during experimental cholestatic ductal hyperplasia. Liver Int 2006;26:457-466.
54. Rountree CB, Wang X, Ge S et al. Bone marrow fails to differentiate into liver epithelium during murine development and regeneration. Hepatology 2007;45:1250-1260.