Liver regeneration

Translational Research

Volumn 163, Issue 4, 2014, Pages 352-362

  Mao, Shennen A ^a   Glorioso, Jaime M ^a   Nyberg, Scott L ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; EPIDERMAL GROWTH FACTOR; GALACTOSAMINE; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGENIC AGENT; PARACETAMOL; SCATTER FACTOR; SCATTER FACTOR RECEPTOR; SOMATOMEDIN BINDING PROTEIN; STAT3 PROTEIN; TISSUE SCAFFOLD; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR;

ACUTE LIVER FAILURE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL METABOLISM; CELL POPULATION; CIRCADIAN RHYTHM; CYTOKINE RELEASE; DNA MODIFICATION; DNA REPLICATION; DNA SYNTHESIS; EXPERIMENTAL MODEL; EXTRACELLULAR MATRIX; GRAFT FAILURE; HUMAN; IMMEDIATE EARLY GENE; INNATE IMMUNITY; LIVER CELL; LIVER PROGENITOR CELL; LIVER REGENERATION; LIVER TOXICITY; LIVER TRANSPLANTATION; MITOGENESIS; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; REVIEW; RODENT MODEL; SMALL FOR SIZE SYNDROME; STEM CELL; STEM CELL EXPANSION; ZEBRA FISH;

ANIMALS; HEPATOCYTES; HUMANS; LIVER REGENERATION; LIVER TRANSPLANTATION; STEM CELLS;

EID: 84897484608     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2014.01.005     Document Type: Review

References (107)

1. J.L. Farber, and R.J. Gerson Mechanisms of cell injury with hepatotoxic chemicals Pharmacol Rev 36 1984 71S 75S
2. J.M. Lemire, N. Shiojiri, and N. Fausto Oval cell proliferation and the origin of small hepatocytes in liver injury induced by D-galactosamine Am J Pathol 139 1991 535 552
3. T. Matsuo, S. Yamaguchi, and S. Mitsui et al. Control mechanism of the circadian clock for timing of cell division in vivo Science 302 2003 255 259
4. U. Schibler Liver regeneration clocks on Science 302 2003 234 235
5. T.C. Weglarz, and E.P. Sandgren Timing of hepatocyte entry into DNA synthesis after partial hepatectomy is cell autonomous Proc Natl Acad Sci U S A 97 2000 12595 12600
6. G.M. Higgins, and R.M. Anderson Experimental pathology of the liver: I. Restoration of the liver of the white rat following partial surgical removal Arch Pathol 12 1931 186 202
7. J. Chu, and K.C. Sadler New school in liver development: lessons from zebrafish Hepatology 50 2009 1656 1663
8. K.C. Sadler, K.N. Krahn, and N.A. Gaur et al. Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1 Proc Natl Acad Sci U S A 104 2007 1570 1575
9. G.K. Michalopoulos Liver regeneration J Cell Physiol 213 2007 286 300
10. K. Decker, and D. Keppler Galactosamine induced liver injury Prog Liver Dis 4 1972 183 199
11. T.M. Rahman, and H.J. Hodgson Animal models of acute hepatic failure Int J Exp Pathol 81 2000 145 157
12. J.E. Fisher, T.J. McKenzie, and J.B. Lillegard et al. Role of Kupffer cells and Toll-like receptor 4 in acetaminophen-induced acute liver failure J Surg Res 180 2013 147 155
13. H. Azuma, N. Paulk, and A. Ranade et al. Robust expansion of human hepatocytes in Fah-/-/Rag2-/-/Il2rg-/- mice Nat Biotechnol 25 2007 903 910
14. R.D. Hickey, J.B. Lillegard, and J.E. Fisher et al. Efficient production of Fah-null heterozygote pigs by chimeric adeno-associated virus-mediated gene knockout and somatic cell nuclear transfer Hepatology 54 2011 1351 1359
15. K.-D. Bissig, S.F. Wieland, and P. Tran et al. Human liver chimeric mice provide a model for hepatitis B and C virus infection and treatment J Clin Invest 120 2010 924 930
16. N. Fausto, J.S. Campbell, and K.J. Riehle Liver regeneration Hepatology 43 2006 S45 S53
17. M. Arai, O. Yokosuka, and T. Chiba et al. Gene expression profiling reveals the mechanism and pathophysiology of mouse liver regeneration J Biol Chem 278 2003 29813 29818
18. B.A. Haber, K.L. Mohn, and R.H. Diamond et al. Induction patterns of 70 genes during nine days after hepatectomy define the temporal course of liver regeneration J Clin Invest 91 1993 1319 1326
19. W. Li, X. Liang, and J.I. Leu et al. Global changes in interleukin-6-dependent gene expression patterns in mouse livers after partial hepatectomy Hepatology 33 2001 1377 1386
20. J.W. Grisham A morphologic study of deoxyribonucleic acid synthesis and cell proliferation in regenerating rat liver: autoradiography with thymidine-H3 Cancer Res 22 1962 842 849
21. M. FitzGerald, E. Webber, and J. Donovan et al. Rapid DNA binding by nuclear factor kappa B in hepatocytes at the start of liver regeneration Cell Growth Differ 6 1995 417 427
22. D.E. Cressman, R.H. Diamond, and R. Taub Rapid activation of the Stat3 transcription complex in liver regeneration Hepatology 21 1995 1443 1449
23. R. Taub Liver regeneration: from myth to mechanism Nat Rev Mol Cell Biol 5 2004 836 847
24. P. Akerman, P. Cote, and S.Q. Yang et al. Antibodies to tumor necrosis factor-alpha inhibit liver regeneration after partial hepatectomy Am J Physiol 263 1992 G579 G585
25. D.E. Cressman, L.E. Greenbaum, and R.A. DeAngelis et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice Science 274 1996 1379 1383
26. Y. Yamada, I. Kirillova, and J.J. Peschon et al. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor Proc Natl Acad Sci U S A 94 1997 1441 1446
27. H. Hayashi, M. Nagaki, and M. Imose et al. Normal liver regeneration and liver cell apoptosis after partial hepatectomy in tumor necrosis factor-α-deficient mice Liver Int 25 2005 162 170
28. R.P. Cornell, B.L. Liljequist, and K.F. Bartizal Depressed liver regeneration after partial hepatectomy of germ-free, athymic and lipopolysaccharide-resistant mice Hepatology 11 1990 916 922
29. J.S. Campbell, K.J. Riehle, and J.T. Brooling et al. Proinflammatory cytokine production in liver regeneration is Myd88-dependent, but independent of Cd14, Tlr2, and Tlr4 J Immunol 176 2006 2522 2528
30. J. Vaquero, J.S. Campbell, and J. Haque et al. Toll-like receptor 4 and myeloid differentiation factor 88 provide mechanistic insights into the cause and effects of interleukin-6 activation in mouse liver regeneration Hepatology 54 2011 597 608
31. C.W. Strey, M. Markiewski, and D. Mastellos et al. The proinflammatory mediators C3a and C5a are essential for liver regeneration J Exp Med 198 2003 913 923
32. P.C. Heinrich, I. Behrmann, and S. Haan et al. Principles of interleukin (IL)-6-type cytokine signalling and its regulation Biochem J 374 2003 1 20
33. X. Ren, C. Hogaboam, and A. Carpenter et al. Stem cell factor restores hepatocyte proliferation in IL-6 knockout mice following 70% hepatectomy J Clin Invest 112 2003 1407 1418
34. K. Nakamura, H. Nonaka, and H. Saito et al. Hepatocyte proliferation and tissue remodeling is impaired after liver injury in oncostatin M receptor knockout mice Hepatology 39 2004 635 644
35. W. Li, X. Liang, and C. Kellendonk et al. STAT3 contributes to the mitogenic response of hepatocytes during liver regeneration J Biol Chem 277 2002 28411 28417
36. R. Taub Hepatoprotection via the IL-6/Stat3 pathway J Clin Invest 112 2003 978 980
37. K. Kovalovich, W. Li, and R. DeAngelis et al. Interleukin-6 protects against Fas-mediated death by establishing a critical level of anti-apoptotic hepatic proteins FLIP, Bcl-2, and Bcl-xL J Biol Chem 276 2001 26605 26613
38. M. Menjo, K. Ikeda, and M. Nakanishi Regulation of G1 cyclin-dependent kinases in liver regeneration J Gastroenterol Hepatol 13 1998 S100 S105
39. J.H. Albrecht, J.S. Hoffman, and B.T. Kren et al. Cyclin and cyclin-dependent kinase 1 mRNA expression in models of regenerating liver and human liver diseases Am J Physiol 265 1993 G857 G864
40. G.K. Michalopoulos, and Z. Khan Liver regeneration, growth factors, and amphiregulin Gastroenterology 128 2005 503 506
41. M. Shimizu, A. Hara, and M. Okuno et al. Mechanism of retarded liver regeneration in plasminogen activator-deficient mice: impaired activation of hepatocyte growth factor after Fas-mediated massive hepatic apoptosis Hepatology 33 2001 569 576
42. C.-G. Huh, V.M. Factor, and A. Sánchez et al. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair Proc Natl Acad Sci U S A 101 2004 4477 4482
43. M. Borowiak, A.N. Garratt, and T. Wüstefeld et al. Met provides essential signals for liver regeneration Proc Natl Acad Sci U S A 101 2004 10608 10613
44. M. Ozaki, S. Haga, and H.Q. Zhang et al. Inhibition of hypoxia/reoxygenation-induced oxidative stress in HGF-stimulated antiapoptotic signaling: role of PI3-K and Akt kinase upon rac1 Cell Death Diff 10 2003 508
45. P. Skov Olsen, S. Boesby, and P. Kirkegaard et al. Influence of epidermal growth factor on liver regeneration after partial hepatectomy in rats Hepatology 8 1988 992 996
46. J.E. Mead, and N. Fausto Transforming growth factor alpha may be a physiological regulator of liver regeneration by means of an autocrine mechanism Proc Natl Acad Sci U S A 86 1989 1558 1562
47. E.M. Webber, J.C. Wu, and L. Wang et al. Overexpression of transforming growth factor-alpha causes liver enlargement and increased hepatocyte proliferation in transgenic mice Am J Pathol 145 1994 398 408
48. W.E. Russell, W.K. Kaufmann, and S. Sitaric et al. Liver regeneration and hepatocarcinogenesis in transforming growth factor-alpha-targeted mice Mol Carcinog 15 1996 183 189
49. S. Kiso, S. Kawata, and S. Tamura et al. Role of heparin-binding epidermal growth factor-like growth factor as a hepatotrophic factor in rat liver regeneration after partial hepatectomy Hepatology 22 1995 1584 1590
50. C. Mitchell, M. Nivison, and L.F. Jackson et al. Heparin-binding epidermal growth factor-like growth factor links hepatocyte priming with cell cycle progression during liver regeneration J Biol Chem 280 2005 2562 2568
51. G.K. Michalopoulos Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas Am J Pathol 176 2010 2 13
52. M. Lesurtel, R. Graf, and B. Aleil et al. Platelet-derived serotonin mediates liver regeneration Science 312 2006 104 107
53. H. Talarmin, C. Rescan, and S. Cariou et al. The mitogen-activated protein kinase kinase/extracellular signal-regulated kinase cascade activation is a key signalling pathway involved in the regulation of G1 phase progression in proliferating hepatocytes Mol Cell Biol 19 1999 6003 6011
54. A. Coutant, C. Rescan, and D. Gilot et al. PI3K-FRAP/mTOR pathway is critical for hepatocyte proliferation whereas MEK/ERK supports both proliferation and survival Hepatology 36 2002 1079 1088
55. J.I. Leu, M.A.S. Crissey, and J.P. Leu et al. Interleukin-6-induced STAT3 and AP-1 amplify hepatocyte nuclear factor 1-mediated transactivation of hepatic genes: an adaptive response to liver injury Mol Cell Biol 21 2001 414 424
56. E. Weir, Q. Chen, and M.C. DeFrances et al. Rapid induction of mRNAs for liver regeneration factor and insulin-like growth factor binding protein-1 in primary cultures of rat hepatocytes by hepatocyte growth factor and epidermal growth factor Hepatology 20 1994 955 960
57. J.I. Leu, M.A.S. Crissey, and R. Taub Massive hepatic apoptosis associated with TGF-β1 activation after Fas ligand treatment of IGF binding protein-1-deficient mice J Clin Invest 111 2003 129 139
58. C.J. Nelsen, D.G. Rickheim, and N.A. Timchenko et al. Transient expression of cyclin D1 is sufficient to promote hepatocyte replication and liver growth in vivo Cancer Res 61 2001 8564 8568
59. J. McGowan, V. Atryzek, and N. Fausto Effects of protein-deprivation on the regeneration of rat liver after partial hepatectomy Biochem J 180 1979 25 35
60. J.E. Mead, L. Braun, and D.A. Martin et al. Induction of replicative competence ("priming") in normal liver Cancer Res 50 1990 7023 7030
61. K.A. Martin, and J. Blenis Coordinate regulation of translation by the PI 3-kinase and mTOR pathways Adv Cancer Res 86 2002 1 39
62. D.H. Kim, and D.M. Sabatini Raptor and mTOR: subunits of a nutrient-sensitive complex Curr Top Microbiol Immunol 279 2004 259 270
63. Y.-P. Jiang, L.M. Ballou, and R.Z. Lin Rapamycin-insensitive regulation of 4E-BP1 in regenerating rat liver J Biol Chem 276 2001 10943 10951
64. G. Song, A.D. Sharma, and G.R. Roll et al. MicroRNAs control hepatocyte proliferation during liver regeneration Hepatology 51 2010 1735 1743
65. N.J. Hand, Z.R. Master, and S.F. Eauclaire et al. The microRNA-30 family is required for vertebrate hepatobiliary development Gastroenterology 136 2009 1081 1090
66. R.E. Lanford, E.S. Hildebrandt-Eriksen, and A. Petri et al. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection Science 327 2010 198 201
67. J.S. Campbell, L. Prichard, and F. Schaper et al. Expression of suppressors of cytokine signaling during liver regeneration J Clin Invest 107 2001 1285 1292
68. T. Wüstefeld, T. Rakemann, and S. Kubicka et al. Hyperstimulation with interleukin 6 inhibits cell cycle progression after hepatectomy in mice Hepatology 32 2000 514 522
69. K.J. Riehle, J.S. Campbell, and R.S. McMahan et al. Regulation of liver regeneration and hepatocarcinogenesis by suppressor of cytokine signaling 3 J Exp Med 205 2008 91 103
70. R. Derynck, and Y.E. Zhang Smad-dependent and Smad-independent pathways in TGF-beta family signalling Nature 425 2003 577 584
71. G.K. Michalopoulos, W.C. Bowen, and K. Mulè et al. Histological organization in hepatocyte organoid cultures Am J Pathol 159 2001 1877 1887
72. R.S. Chari, D.T. Price, and S.R. Sue et al. Down-regulation of transforming growth factor beta receptor type I, II, and III during liver regeneration Am J Surg 169 1995 126 132
73. K.A. Houck, J.L. Cruise, and G. Michalopoulos Norepinephrine modulates the growth-inhibitory effect of transforming growth factor-beta in primary rat hepatocyte cultures J Cell Physiol 135 1988 551 555
74. S. Oe, E.R. Lemmer, and E.A. Conner et al. Intact signaling by transforming growth factor β is not required for termination of liver regeneration in mice Hepatology 40 2004 1098 1105
75. T. Ichikawa, Y.Q. Zhang, and K. Kogure et al. Transforming growth factor beta and activin tonically inhibit DNA synthesis in the rat liver Hepatology 34 2001 918 925
76. T. Wuestefeld, M. Pesic, and R. Rudalska et al. A direct in vivo RNAi screen identifies MKK4 as a key regulator of liver regeneration Cell 153 2013 389 401
77. E. Farber Similarities in the sequence of early histological changes induced in the liver of the rat by ethionine, 2-acetylamino-fluorene, and 3′-methyl-4-dimethylaminoazobenzene Cancer Res 16 1956 142 148
78. C.A. Lazaro, J.A. Rhim, and Y. Yamada et al. Generation of hepatocytes from oval cell precursors in culture Cancer Res 58 1998 5514 5522
79. H.A. Dunsford, C. Karnasuta, and J.M. Hunt et al. Different lineages of chemically induced hepatocellular carcinoma in rats defined by monoclonal antibodies Cancer Res 49 1989 4894 4900
80. R.P. Evarts, Z. Hu, and K. Fujio et al. Activation of hepatic stem cell compartment in the rat: role of transforming growth factor alpha, hepatocyte growth factor, and acidic fibroblast growth factor in early proliferation Cell Growth Diff 4 1993 555 561
81. R.P. Evarts, P. Nagy, and H. Nakatsukasa et al. In vivo differentiation of rat liver oval cells into hepatocytes Cancer Res 49 1989 1541 1547
82. N.D. Theise, R. Saxena, and B.C. Portmann et al. The canals of Hering and hepatic stem cells in humans Hepatology 30 1999 1425 1433
83. E. Lagasse, H. Connors, and M. Al-Dhalimy et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo Nat Med 6 2000 1229 1234
84. H. Willenbring, A.S. Bailey, and M. Foster et al. Myelomonocytic cells are sufficient for therapeutic cell fusion in liver Nat Med 10 2004 744 748
85. L. Zhang, N. Theise, and M. Chua et al. The stem cell niche of human livers: symmetry between development and regeneration Hepatology 48 2008 1598 1607
86. L. Yang, Y. Jung, and A. Omenetti et al. Fate-mapping evidence that hepatic stellate cells are epithelial progenitors in adult mouse livers Stem Cells 26 2008 2104 2113
87. D. Scholten, C.H. Osterreicher, and A. Scholten et al. Genetic labeling does not detect epithelial-to-mesenchymal transition of cholangiocytes in liver fibrosis in mice Gastroenterology 139 2010 987 998
88. K. Taura, K. Miura, and K. Iwaisako et al. Hepatocytes do not undergo epithelial-mesenchymal transition in liver fibrosis in mice Hepatology 51 2010 1027 1036
89. K.N. Lowes, B.A. Brennan, and G.C. Yeoh et al. Oval cell numbers in human chronic liver diseases are directly related to disease severity Am J Pathol 154 1999 537 541
90. A. Katoonizadeh, F. Nevens, and C. Verslype et al. Liver regeneration in acute severe liver impairment: a clinicopathological correlation study Liver Int 26 2006 1225 1233
91. L. Libbrecht, and T. Roskams Hepatic progenitor cells in human liver diseases Semin Cell Dev Biol 13 2002 389 396
92. L. Libbrecht, V. Desmet, and B. Van Damme et al. Deep intralobular extension of human hepatic "progenitor cells" correlates with parenchymal inflammation in chronic viral hepatitis: can "progenitor cells" migrate? J Pathol 192 2000 373 378
93. F. Dahm, P. Georgiev, and P.-A. Clavien Small-for-size syndrome after partial liver transplantation: definition, mechanisms of disease and clinical implications Am J Transplant 5 2005 2605 2610
94. O.N. Tucker, and N. Heaton The "small for size" liver syndrome Curr Opin Crit Care 11 2005 150 155
95. S. Gruttadauria, D. Pagano, and A. Luca et al. Small-for-size syndrome in adult-to-adult living-related liver transplantation World J Gastroenterol 16 2010 5011 5015
96. K. Lehmann, C. Tschuor, and A. Rickenbacher et al. Liver failure after extended hepatectomy in mice is mediated by a p21-dependent barrier to liver regeneration Gastroenterology 143 2012 1609 1619
97. T. Kiuchi, M. Kasahara, and K. Uryuhara et al. Impact of graft size mismatching on graft prognosis in liver transplantation from living donors Transplantation 67 1999 321 327
98. D.M. Kelly, A.J. Demetris, and J.J. Fung et al. Porcine partial liver transplantation: a novel model of the "small-for-size" liver graft Liver Transplant 10 2004 253 263
99. T. Ayuse, N. Brienza, and C.P. O'Donnell et al. Pressure-flow analysis of portal vein and hepatic artery interactions in porcine liver Am J Physiol 267 1994 H1233 H1242
100. X.H. Zhu, Y.F. Wu, and Y.D. Qiu et al. Liver-protecting effects of omega-3 fish oil lipid emulsion in liver transplantation World J Gastroenterol 18 2012 6141 6147
101. X.P. Yan, S. Wang, and Y. Yang et al. Effects of n-3 polyunsaturated fatty acids on rat livers after partial hepatectomy via LKB1-AMPK signaling pathway Transplant Proc 43 2011 3604 3612
102. S.M. Fouraschen, Q. Pan, and P.E. de Ruiter et al. Secreted factors of human liver-derived mesenchymal stem cells promote liver regeneration early after partial hepatectomy Stem Cells Dev 21 2012 2410 2419
103. J. Yu, S. Yin, and W. Zhang et al. Hypoxia preconditioned bone marrow mesenchymal stem cells promote liver regeneration in a rat massive hepatectomy model Stem Cell Res Ther 4 2013 83
104. H. Petrowsky, S. Breitenstein, and K. Slankamenac et al. Effects of pentoxifylline on liver regeneration: a double-blinded, randomized, controlled trial in 101 patients undergoing major liver resection Ann Surg 252 2010 813 822
105. S. Yagi, and S. Uemoto Small-for-size syndrome in living donor liver transplantation Hepatobiliary Pancreat Dis Int 11 2012 570 576
106. B.E. Uygun, A. Soto-Gutierrez, and H. Yagi et al. Organ reengineering through development of a transplantable recellularized liver graft using decellularized liver matrix Nat Med 16 2010 814 820
107. L.G. Koniaris, I.H. McKillop, and S.I. Schwartz et al. Liver regeneration J Am Coll Surg 197 2003 634 659