Hybrid Periportal Hepatocytes Regenerate the Injured Liver without Giving Rise to Cancer

Cell

Volumn 162, Issue 4, 2015, Pages 766-779

  Font Burgada, Joan ^a   Shalapour, Shabnam ^a   Ramaswamy, Suvasini ^e   Hsueh, Brian ^f   Rossell, David ^g   Umemura, Atsushi ^a,j   Taniguchi, Koji ^a   Nakagawa, Hayato ^a,h   Valasek, Mark A ^b   Ye, Li ^f   Kopp, Janel L ^c,i   Sander, Maike ^c   Carter, Hannah ^d   Deisseroth, Karl ^f   Verma, Inder M ^e   Karin, Michael ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^g UNIVERSITY OF WARWICK   (United Kingdom)

^h UNIVERSITY OF TOKYO   (Japan)

ⁱ UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^j KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

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Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR SOX9; SOX9 PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT; CELL DIFFERENTIATION; CELL FUNCTION; CELL LABELING; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; LIVER CELL; LIVER CELL CARCINOMA; LIVER INJURY; LIVER REGENERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL TRANSPLANTATION; CLASSIFICATION; CYTOLOGY; GENETICS; INJURIES; LIVER; LIVER TUMOR; PHYSIOLOGY; PROCEDURES; REGENERATION; TRANSPLANTATION;

ANIMALS; BILE DUCTS; CELL PROLIFERATION; CELL TRANSPLANTATION; HEPATOCYTES; LIVER; LIVER NEOPLASMS; MICE; REGENERATION; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTOME;

EID: 84939216194     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.07.026     Document Type: Article

References (52)

1. B. Akhurst, E.J. Croager, C.A. Farley-Roche, J.K. Ong, M.L. Dumble, B. Knight, and G.C. Yeoh A modified choline-deficient, ethionine-supplemented diet protocol effectively induces oval cells in mouse liver Hepatology 34 2001 519 522
2. M.R. Alison, S. Islam, and S. Lim Stem cells in liver regeneration, fibrosis and cancer: the good, the bad and the ugly J. Pathol. 217 2009 282 298
3. K.-D.D. Bissig, T.T. Le, N.-B.B. Woods, and I.M. Verma Repopulation of adult and neonatal mice with human hepatocytes: a chimeric animal model Proc. Natl. Acad. Sci. USA 104 2007 20507 20511
4. C. Blanpain, and E. Fuchs Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration Science 344 2014 1242281
5. R. Carpentier, R.E. Suñer, N. van Hul, J.L. Kopp, J.B. Beaudry, S. Cordi, A. Antoniou, P. Raynaud, S. Lepreux, P. Jacquemin, and et al. Embryonic ductal plate cells give rise to cholangiocytes, periportal hepatocytes, and adult liver progenitor cells Gastroenterology 141 2011 1432 1438.e1-e4
6. T.H. Cheung, and T.A. Rando Molecular regulation of stem cell quiescence Nat. Rev. Mol. Cell Biol. 14 2013 329 340
7. K. Chung, J. Wallace, S.Y. Kim, S. Kalyanasundaram, A.S. Andalman, T.J. Davidson, J.J. Mirzabekov, K.A. Zalocusky, J. Mattis, A.K. Denisin, and et al. Structural and molecular interrogation of intact biological systems Nature 497 2013 332 337
8. C. Dorrell, L. Erker, J. Schug, J.L. Kopp, P.S. Canaday, A.J. Fox, O. Smirnova, A.W. Duncan, M.J. Finegold, M. Sander, and et al. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice Genes Dev. 25 2011 1193 1203
9. R. Español-Suñer, R. Carpentier, N. Van Hul, V. Legry, Y. Achouri, S. Cordi, P. Jacquemin, F. Lemaigre, and I.A. Leclercq Liver progenitor cells yield functional hepatocytes in response to chronic liver injury in mice Gastroenterology 143 2012 1564 1575.e7
10. T.G. Fellous, S. Islam, P.J. Tadrous, G. Elia, H.M. Kocher, S. Bhattacharya, L. Mears, D.M. Turnbull, R.W. Taylor, L.C. Greaves, and et al. Locating the stem cell niche and tracing hepatocyte lineages in human liver Hepatology 49 2009 1655 1663
11. K.E. Fleming, and I.R. Wanless Glutamine synthetase expression in activated hepatocyte progenitor cells and loss of hepatocellular expression in congestion and cirrhosis Liver Int. 33 2013 525 534
12. S.J. Forbes, S. Gupta, and A. Dhawan Cell therapy for liver disease: From liver transplantation to cell factory J. Hepatol. 62 2015 S157 S169
13. M. Fujii, Y. Shibazaki, K. Wakamatsu, Y. Honda, Y. Kawauchi, K. Suzuki, S. Arumugam, K. Watanabe, T. Ichida, H. Asakura, and H. Yoneyama A murine model for non-alcoholic steatohepatitis showing evidence of association between diabetes and hepatocellular carcinoma Med. Mol. Morphol. 46 2013 141 152
14. K. Furuyama, Y. Kawaguchi, H. Akiyama, M. Horiguchi, S. Kodama, T. Kuhara, S. Hosokawa, A. Elbahrawy, T. Soeda, M. Koizumi, and et al. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine Nat. Genet. 43 2011 34 41
15. M. Grompe Liver stem cells, where art thou? Cell Stem Cell 15 2014 257 258
16. M. Grompe, S. Lindstedt, M. al-Dhalimy, N.G. Kennaway, J. Papaconstantinou, C.A. Torres-Ramos, C.N. Ou, and M. Finegold Pharmacological correction of neonatal lethal hepatic dysfunction in a murine model of hereditary tyrosinaemia type I Nat. Genet. 10 1995 453 460
17. G. He, D. Dhar, H. Nakagawa, J. Font-Burgada, H. Ogata, Y. Jiang, S. Shalapour, E. Seki, S.E. Yost, K. Jepsen, and et al. Identification of liver cancer progenitors whose malignant progression depends on autocrine IL-6 signaling Cell 155 2013 384 396
18. M. Huch, C. Dorrell, S.F. Boj, J.H. van Es, V.S. Li, M. van de Wetering, T. Sato, K. Hamer, N. Sasaki, M.J. Finegold, and et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration Nature 494 2013 247 250
19. M. Huch, H. Gehart, R. van Boxtel, K. Hamer, F. Blokzijl, M.M. Verstegen, E. Ellis, M. van Wenum, S.A. Fuchs, J. de Ligt, and et al. Long-term culture of genome-stable bipotent stem cells from adult human liver Cell 160 2015 299 312
20. L. Hui, L. Bakiri, A. Mairhorfer, N. Schweifer, C. Haslinger, L. Kenner, V. Komnenovic, H. Scheuch, H. Beug, and E.F. Wagner p38alpha suppresses normal and cancer cell proliferation by antagonizing the JNK-c-Jun pathway Nat. Genet. 39 2007 741 749
21. K. Isse, A. Lesniak, K. Grama, J. Maier, S. Specht, M. Castillo-Rama, J. Lunz, B. Roysam, G. Michalopoulos, and A.J. Demetris Preexisting epithelial diversity in normal human livers: a tissue-tethered cytometric analysis in portal/periportal epithelial cells Hepatology 57 2013 1632 1643
22. K. Jungermann, and N. Katz Functional specialization of different hepatocyte populations Physiol. Rev. 69 1989 708 764
23. K. Kaneko, K. Kamimoto, A. Miyajima, and T. Itoh Adaptive remodeling of the biliary architecture underlies liver homeostasis Hepatology 61 2015 2056 2066
24. J.S. Kang, H. Wanibuchi, K. Morimura, F.J. Gonzalez, and S. Fukushima Role of CYP2E1 in diethylnitrosamine-induced hepatocarcinogenesis in vivo Cancer Res. 67 2007 11141 11146
25. M. Karin Nuclear factor-kappaB in cancer development and progression Nature 441 2006 431 436
26. T. Kisseleva, E. Gigante, and D.A. Brenner Recent advances in liver stem cell therapy Curr. Opin. Gastroenterol. 26 2010 395 402
27. A. Kuraishy, M. Karin, and S.I. Grivennikov Tumor promotion via injury- and death-induced inflammation Immunity 35 2011 467 477
28. R. Kuwahara, A.V. Kofman, C.S. Landis, E.S. Swenson, E. Barendswaard, and N.D. Theise The hepatic stem cell niche: identification by label-retaining cell assay Hepatology 47 2008 1994 2002
29. Y. Lavin, D. Winter, R. Blecher-Gonen, E. David, H. Keren-Shaul, M. Merad, S. Jung, and I. Amit Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment Cell 159 2014 1312 1326
30. T. Luedde, N. Beraza, V. Kotsikoris, G. van Loo, A. Nenci, R. De Vos, T. Roskams, C. Trautwein, and M. Pasparakis Deletion of NEMO/IKKgamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma Cancer Cell 11 2007 119 132
31. S. Maeda, H. Kamata, J.L. Luo, H. Leffert, and M. Karin IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis Cell 121 2005 977 990
32. Y. Malato, S. Naqvi, N. Schürmann, R. Ng, B. Wang, J. Zape, M.A. Kay, D. Grimm, and H. Willenbring Fate tracing of mature hepatocytes in mouse liver homeostasis and regeneration J. Clin. Invest. 121 2011 4850 4860
33. G.K. Michalopoulos Liver regeneration J. Cell. Physiol. 213 2007 286 300
34. A. Miyajima, M. Tanaka, and T. Itoh Stem/progenitor cells in liver development, homeostasis, regeneration, and reprogramming Cell Stem Cell 14 2014 561 574
35. H. Nakagawa, Y. Hikiba, Y. Hirata, J. Font-Burgada, K. Sakamoto, Y. Hayakawa, K. Taniguchi, A. Umemura, H. Kinoshita, K. Sakitani, and et al. Loss of liver E-cadherin induces sclerosing cholangitis and promotes carcinogenesis Proc. Natl. Acad. Sci. USA 111 2014 1090 1095
36. H. Nakagawa, A. Umemura, K. Taniguchi, J. Font-Burgada, D. Dhar, H. Ogata, Z. Zhong, M.A. Valasek, E. Seki, J. Hidalgo, and et al. ER stress cooperates with hypernutrition to trigger TNF-dependent spontaneous HCC development Cancer Cell 26 2014 331 343
37. M.M. Richardson, J.R. Jonsson, E.E. Powell, E.M. Brunt, B.A. Neuschwander-Tetri, P.S. Bhathal, J.B. Dixon, M.D. Weltman, H. Tilg, A.R. Moschen, and et al. Progressive fibrosis in nonalcoholic steatohepatitis: association with altered regeneration and a ductular reaction Gastroenterology 133 2007 80 90
38. D. Rodrigo-Torres, S. Affò, M. Coll, O. Morales-Ibanez, C. Millán, D. Blaya, A. Alvarez-Guaita, C. Rentero, J.J. Lozano, M.A. Maestro, and et al. The biliary epithelium gives rise to liver progenitor cells Hepatology 60 2014 1367 1377
39. T. Roskams Liver stem cells and their implication in hepatocellular and cholangiocarcinoma Oncogene 25 2006 3818 3822
40. T. Sakurai, G. He, A. Matsuzawa, G.Y. Yu, S. Maeda, G. Hardiman, and M. Karin Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis Cancer Cell 14 2008 156 165
41. J.R. Schaub, Y. Malato, C. Gormond, and H. Willenbring Evidence against a stem cell origin of new hepatocytes in a common mouse model of chronic liver injury Cell Rep. 8 2014 933 939
42. E. Schmelzer, L. Zhang, A. Bruce, E. Wauthier, J. Ludlow, H.L. Yao, N. Moss, A. Melhem, R. McClelland, W. Turner, and et al. Human hepatic stem cells from fetal and postnatal donors J. Exp. Med. 204 2007 1973 1987
43. S. Sell, and H.L. Leffert Liver cancer stem cells J. Clin. Oncol. 26 2008 2800 2805
44. J.M. Slack Metaplasia and transdifferentiation: from pure biology to the clinic Nat. Rev. Mol. Cell Biol. 8 2007 369 378
45. N. Tanimizu, Y. Nishikawa, N. Ichinohe, H. Akiyama, and T. Mitaka Sry HMG box protein 9-positive (Sox9+) epithelial cell adhesion molecule-negative (EpCAM-) biphenotypic cells derived from hepatocytes are involved in mouse liver regeneration J. Biol. Chem. 289 2014 7589 7598
46. B.D. Tarlow, M.J. Finegold, and M. Grompe Clonal tracing of Sox9+ liver progenitors in mouse oval cell injury Hepatology 60 2014 278 289
47. B.D. Tarlow, C. Pelz, W.E. Naugler, L. Wakefield, E.M. Wilson, M.J. Finegold, and M. Grompe Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes Cell Stem Cell 15 2014 605 618
48. C. Tomasetti, and B. Vogelstein Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions Science 347 2015 78 81
49. T.C. Weglarz, J.L. Degen, and E.P. Sandgren Hepatocyte transplantation into diseased mouse liver. Kinetics of parenchymal repopulation and identification of the proliferative capacity of tetraploid and octaploid hepatocytes Am. J. Pathol. 157 2000 1963 1974
50. F.W. Wong, W.Y. Chan, and S.S. Lee Resistance to carbon tetrachloride-induced hepatotoxicity in mice which lack CYP2E1 expression Toxicol. Appl. Pharmacol. 153 1998 109 118
51. K. Yanger, Y. Zong, L.R. Maggs, S.N. Shapira, R. Maddipati, N.M. Aiello, S.N. Thung, R.G. Wells, L.E. Greenbaum, and B.Z. Stanger Robust cellular reprogramming occurs spontaneously during liver regeneration Genes Dev. 27 2013 719 724
52. K. Yanger, D. Knigin, Y. Zong, L. Maggs, G. Gu, H. Akiyama, E. Pikarsky, and B.Z. Stanger Adult hepatocytes are generated by self-duplication rather than stem cell differentiation Cell Stem Cell 15 2014 340 349