Biliary fibrosis drives liver repopulation and phenotype transition of transplanted hepatocytes

Journal of Hepatology

Volumn 64, Issue 6, 2016, Pages 1348-1357

  Yovchev, Mladen I ^a   Locker, Joseph ^a   Oertel, Michael ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Bile duct ligation; Cell transplantation; Hepatocyte dedifferentiation; Hepatocyte transdifferentiation; Osteopontin

Indexed keywords

CLAUDIN 7; CYTOKERATIN 19; DIPEPTIDYL PEPTIDASE IV; FIBROBLAST GROWTH FACTOR 18; GREEN FLUORESCENT PROTEIN; GROWTH FACTOR; HEPATOCYTE NUCLEAR FACTOR 1BETA; HEPATOCYTE NUCLEAR FACTOR 6; INTERLEUKIN 6; MESSENGER RNA; OSTEOPONTIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ITG BETA4; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; BILIARY TRACT FIBROSIS; CELL COUNT; CELL DEDIFFERENTIATION; CELL MATURATION; CELL POPULATION; CELL TRANSDIFFERENTIATION; COMMON BILE DUCT; CONTROLLED STUDY; DISEASE COURSE; ENGRAFTMENT; EPITHELIUM CELL; GENE EXPRESSION; HEPATOCYTE TRANSPLANTATION; INJURY SEVERITY; LIVER; LIVER CELL; LIVER CELL CULTURE; LIVER FIBROSIS; MALE; NONHUMAN; PARTIAL HEPATECTOMY; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; SPLEEN; UPREGULATION; ANIMAL; BILIARY CIRRHOSIS; CELL CULTURE; FISCHER 344 RAT; PATHOLOGY; TRANSPLANTATION;

ANIMALS; CELL DEDIFFERENTIATION; CELLS, CULTURED; DIPEPTIDYL PEPTIDASE 4; HEPATOCYTES; LIVER; LIVER CIRRHOSIS, BILIARY; PHENOTYPE; RATS; RATS, INBRED F344;

EID: 84961798870     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2016.01.036     Document Type: Article

References (44)

1. V. Hernandez-Gea, and S.L. Friedman Pathogenesis of liver fibrosis Annu Rev Pathol 6 2011 425 456
2. S.L. Murphy, J. Xu, and K.D. Kochanek Deaths: final data for 2010 Natl Vital Stat Rep 61 2013 1 117
3. A. Cárdenas, and P. Ginès Management of patients with cirrhosis awaiting liver transplantation Gut 60 2011 412 421
4. W.R. Kim, J.R. Lake, J.M. Smith, M.A. Skeans, D.P. Schladt, E.B. Edwards, and et al. OPTN/SRTR 2013 Annual Data Report: liver Am J Transplant 15 2015 1 28
5. B. Struecker, N. Raschzok, and I.M. Sauer Liver support strategies: cutting-edge technologies Nat Rev Gastroenterol Hepatol 11 2014 166 176
6. M. Oertel Fetal liver cell transplantation as a potential alternative to whole liver transplantation? J Gastroenterol 46 2011 953 965
7. R.C. Huebert, and J. Rakela Cellular therapy for liver disease Mayo Clin Proc 89 2014 414 424
8. R. Gramignoli, M. Vosough, K. Kannisto, R.C. Srinivasan, and S.C. Strom Clinical hepatocyte transplantation: practical limits and possible solutions Eur Surg Res 54 2015 162 177
9. J.A. Rhim, E.P. Sandgren, J.L. Degen, R.D. Palmiter, and R.L. Brinster Replacement of diseased mouse liver by hepatic cell transplantation Science 263 1994 1149 1152
10. K. Overturf, M. Al-Dhalimy, R. Tanguay, M. Brantly, C.N. Ou, M. Finegold, and et al. Hepatocytes corrected by gene therapy are selected in vivo in a murine model of hereditary tyrosinaemia type I Nat Genet 12 1996 266 273
11. E. Laconi, R. Oren, D.K. Mukhopadhyay, E. Hurston, S. Laconi, P. Pani, and et al. Long-term, near-total liver replacement by transplantation of isolated hepatocytes in rats treated with retrorsine Am J Pathol 153 1998 319 329
12. C. Guha, A. Sharma, S. Gupta, A. Alfieri, G.R. Gorla, S. Gagandeep, and et al. Amelioration of radiation-induced liver damage in partially hepatectomized rats by hepatocyte transplantation Cancer Res 59 1999 5871 5874
13. M.I. Yovchev, Y. Xue, D.A. Shafritz, J. Locker, and M. Oertel Repopulation of the fibrotic/cirrhotic rat liver by transplanted hepatic stem/progenitor cells and mature hepatocytes Hepatology 59 2014 284 295
14. M.I. Yovchev, M.D. Dabeva, and M. Oertel Isolation, characterization, and transplantation of adult liver progenitor cells Methods Mol Biol 976 2013 37 51
15. S. Gupta, P. Rajvanshi, H. Malhi, S. Slehria, R.P. Sokhi, S.R. Vasa, and et al. Cell transplantation causes loss of gap junctions and activates GGT expression permanently in host liver Am J Physiol Gastrointest Liver Physiol 279 2000 G815 G826
16. A. Antoniou, P. Raynaud, S. Cordi, Y. Zong, F. Tronche, B.Z. Stanger, and et al. Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9 Gastroenterology 136 2009 2325 2333
17. B.D. Tarlow, C. Pelz, W.E. Naugler, L. Wakefield, E.M. Wilson, M.J. Finegold, and et al. Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes Cell Stem Cell 15 2014 605 618
18. M. Sone, Y. Nishikawa, Y. Nagahama, E. Kumagai, Y. Doi, Y. Omori, and et al. Recovery of mature hepatocytic phenotype following bile ductular transdifferentiation of rat hepatocytes in vitro Am J Pathol 181 2012 2094 2104
19. M.C. Hu, W.R. Qiu, Y.P. Wang, D. Hill, B.D. Ring, S. Scully, and et al. FGF-18, a novel member of the fibroblast growth factor family, stimulates hepatic and intestinal proliferation Mol Cell Biol 18 1998 6063 6074
20. R. Urtasun, A. Lopategi, J. George, T.M. Leung, Y. Lu, X. Wang, and et al. Osteopontin, an oxidant stress sensitive cytokine, up-regulates collagen-I via integrin α(V)β(3) engagement and PI3K/pAkt/NFκB signaling Hepatology 55 2012 594 608
21. D. Fu, Y. Wakabayashi, J. Lippincott-Schwartz, and I.M. Arias Bile acid stimulates hepatocyte polarization through a cAMP-Epac-MEK-LKB1-AMPK pathway Proc Natl Acad Sci U S A 108 2011 1403 1408
22. Y. Popov, and D. Schuppan Targeting liver fibrosis: strategies for development and validation of antifibrotic therapies Hepatology 50 2009 1294 1306
23. J. Kountouras, B.H. Billing, and P.J. Scheuer Prolonged bile duct obstruction: a new experimental model for cirrhosis in the rat Br J Exp Pathol 65 1984 305 311
24. N.L. Thompson, D.C. Hixson, H. Callanan, M. Panzica, D. Flanagan, R.A. Faris, and et al. 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 273 1991 497 502
25. O. Tarcin, M. Basaranoglu, V. Tahan, G. Tahan, I. Sücüllü, N. Yilmaz, and et al. Time course of collagen peak in bile duct-ligated rats BMC Gastroenterol 11 2011 45
26. Y. Popov, D.Y. Sverdlov, K.R. Bhaskar, A.K. Sharma, G. Millonig, E. Patsenker, and et al. Macrophage-mediated phagocytosis of apoptotic cholangiocytes contributes to reversal of experimental biliary fibrosis Am J Physiol Gastrointest Liver Physiol 298 2010 G323 G334
27. R.L. Jirtle, C. Biles, and G. Michalopoulos Morphologic and histochemical analysis of hepatocytes transplanted into syngeneic hosts Am J Pathol 101 1980 115 126
28. M. Mito, M. Kusano, T. Onishi, T. Saito, and H. Ebata Hepatocellular transplantation -morphological study on hepatocytes transplanted into rat spleen- Gastroenterol Jpn 13 1978 480 490
29. S. Gupta, E. Aragona, R.P. Vemuru, K.K. Bhargava, R.D. Burk, and J.R. Chowdhury Permanent engraftment and function of hepatocytes delivered to the liver: implications for gene therapy and liver repopulation Hepatology 14 1991 144 149
30. M. Oertel, A. Menthena, M.D. Dabeva, and D.A. Shafritz Cell competition leads to a high level of normal liver reconstitution by transplanted fetal liver stem/progenitor cells Gastroenterology 130 2006 507 520
31. G.K. Michalopoulos, W.C. Bowen, K. Mulè, J.C. Lopez-Talavera, and W. Mars Hepatocytes undergo phenotypic transformation to biliary epithelium in organoid cultures Hepatology 36 2002 278 283
32. P.B. Limaye, W.C. Bowen, A.V. Orr, J. Luo, G.C. Tseng, and G.K. Michalopoulos Mechanisms of hepatocyte growth factor-mediated and epidermal growth factor-mediated signaling in transdifferentiation of rat hepatocytes to biliary epithelium Hepatology 47 2008 1702 1713
33. G.K. Michalopoulos, L. Barua, and W.C. Bowen Transdifferentiation of rat hepatocytes into biliary cells after bile duct ligation and toxic biliary injury Hepatology 41 2005 535 544
34. P.B. Limaye, W.C. Bowen, A. Orr, U.M. Apte, and G.K. Michalopoulos Expression of hepatocytic- and biliary-specific transcription factors in regenerating bile ducts during hepatocyte-to-biliary epithelial cell transdifferentiation Comp Hepatol 9 2010 9
35. K. Fukuda, A. Sugihara, K. Nakasho, T. Tsujimura, N. Yamada, A. Okaya, and et al. The origin of biliary ductular cells that appear in the spleen after transplantation of hepatocytes Cell Transplant 13 2004 27 33
36. H. Watanabe, M. Hata, N. Terada, H. Ueda, N. Yamada, K. Yamanegi, and et al. Transdifferentiation into biliary ductular cells of hepatocytes transplanted into the spleen Pathology 40 2008 272 276
37. K. Yanger, Y. Zong, L.R. Maggs, S.N. Shapira, R. Maddipati, N.M. Aiello, and et al. Robust cellular reprogramming occurs spontaneously during liver regeneration Genes Dev 27 2013 719 724
38. S. Sekiya, and A. Suzuki Hepatocytes, rather than cholangiocytes, can be the major source of primitive ductules in the chronically injured mouse liver Am J Pathol 184 2014 1468 1478
39. S. Nagoshi Osteopontin: Versatile modulator of liver diseases Hepatol Res 44 2014 22 30
40. W.K. Syn, S.S. Choi, E. Liaskou, G.F. Karaca, K.M. Agboola, Y.H. Oo, and et al. Osteopontin is induced by hedgehog pathway activation and promotes fibrosis progression in nonalcoholic steatohepatitis Hepatology 53 2011 106 115
41. J. Pritchett, E. Harvey, V. Athwal, A. Berry, C. Rowe, F. Oakley, and et al. Osteopontin is a novel downstream target of SOX9 with diagnostic implications for progression of liver fibrosis in humans Hepatology 56 2012 1108 1116
42. A. Couvelard, A.F. Bringuier, M.C. Dauge, M. Nejjari, E. Darai, J.L. Benifla, and et al. Expression of integrins during liver organogenesis in humans Hepatology 27 1998 839 847
43. C. Coffinier, L. Gresh, L. Fiette, F. Tronche, G. Schütz, C. Babinet, and et al. Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1beta Development 129 2002 1829 1838
44. F. Clotman, V.J. Lannoy, M. Reber, S. Cereghini, D. Cassiman, P. Jacquemin, and et al. The onecut transcription factor HNF6 is required for normal development of the biliary tract Development 129 2002 1819 1828