DeLiver'in regeneration: Injury response and development

Seminars in Liver Disease

Volumn 30, Issue 3, 2010, Pages 288-295

  Curado, Silvia ^a   Stainier, Didier Y R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

biliary cell; damage; hepatectomy; hepatocyte; Hepatopathology; liver; oval cell

Indexed keywords

PROSTAGLANDIN E2; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; EXPERIMENTAL MODEL; GENETIC SCREENING; IMMUNE SYSTEM; LIVER CELL; LIVER DEVELOPMENT; LIVER FUNCTION; LIVER INJURY; LIVER REGENERATION; LIVER RESECTION; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; REVIEW; SURGICAL TECHNIQUE; ZEBRA FISH;

ANIMALS; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; HEPATECTOMY; HUMANS; LIVER; LIVER DISEASES; LIVER REGENERATION; MICE; MODELS, ANIMAL; SIGNAL TRANSDUCTION; ZEBRAFISH;

EID: 77954961991     PISSN: 02728087     EISSN: 10988971     Source Type: Journal    
DOI: 10.1055/s-0030-1255357     Document Type: Review

References (98)

1. Power C, Rasko J E. Whither Prometheus' liver? Greek myth and the science of regeneration. Ann Intern Med 2008 149 421-426
2. Cruveilhier L JB. Anatomie Pathologique du Corps Humain, ou, Description avec Figures Lithographiees et Coloriees, des Diverses Alterations Morbides dont le Corps Humain est Susceptible. Paris Bailliere 1829-1833 398-399
3. Andral G. Medical Clinic. Vol. 1. Diseases of the Abdomen. Philadelphia Barrington & Haswell 1843 345-348
4. Tillmanns H. Experimental und anatomische Untersuchungen uber Wundun der Leber und Niere. Virchows Arch 1879 78 437-465
5. Higgins G M., Anderson R M. Experimental pathology of the liver. Restoration of the liver of the white rat following partial surgical removal. Arch Pathol (Chic) 1931 12 186-202
6. Michalopoulos G K. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 2010 176 2-13
7. Palmes D, Spiegel H U. Animal models of liver regeneration. Biomaterials 2004 25 1601-1611
8. Burkhardt-Holm P, Oulmi Y, Schroeder A, Storch V, Braunbeck T. Toxicity of 4-chloroaniline in early life stages of zebrafish (Danio rerio): II. Cytopathology and regeneration of liver and gills after prolonged exposure to waterborne 4-chloroaniline. Arch Environ Contam Toxicol 1999 37 85-102
9. Sadler K C., Krahn K N., Gaur N A., Ukomadu C. Liver growth in the embryo and during liver regeneration in zebrafish requires the cell cycle regulator, uhrf1. Proc Natl Acad Sci U S A 2007 104 1570-1575
10. Curado S, Anderson R M., Jungblut B, Mumm J, Schroeter E, Stainier D Y. Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev Dyn 2007 236 1025-1035
11. Curado S, Stainier D Y., Anderson R M. Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat Protocols 2008 3 948-954
12. Curado S, Ober E A., Walsh S, Cortes-Hernandez P, Verkade H, Koehler C M., Stainier D YR. The mitochondrial import genetomm22is specifically required for hepatocyte survival and provides a liver regeneration model. Dis Model Mech 2010 In press
13. Dong J, Stuart G W. Transgene manipulation in zebrafish by using recombinases. Methods Cell Biol 2004 77 363-379
14. Ouyang X, Shestopalov I A., Sinha S et al. Versatile synthesis and rational design of caged morpholinos. J Am Chem Soc 2009 131 13255-13269
15. Shestopalov I A., Sinha S, Chen J K. Light-controlled gene silencing in zebrafish embryos. Nat Chem Biol 2007 3 650-651
16. Wienholds E, van Eeden F, Kosters M, Mudde J, Plasterk R H., Cuppen E. Efficient target-selected mutagenesis in zebrafish. Genome Res 2003 13 2700-2707
17. Doyon Y, McCammon J M., Miller J C. et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 2008 26 702-708
18. Meng X, Noyes M B., Zhu L J., Lawson N D., Wolfe S A. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 2008 26 695-701
19. Chu J, Sadler K C. New school in liver development: lessons from zebrafish. Hepatology 2009 50 1656-1663
20. Si-Tayeb K, Lemaigre F P., Duncan S A. Organogenesis and development of the liver. Dev Cell 2010 18 175-189
21. Stcker E, Heine W D. Regeneration of liver parenchyma under normal and pathological conditions. Beitr Pathol 1971 144 400-408
22. Overturf K, al-Dhalimy M, Ou C N., Finegold M, Grompe M. Serial transplantation reveals the stem-cell-like regenerative potential of adult mouse hepatocytes. Am J Pathol 1997 151 1273-1280 (Pubitemid 27479757)
23. Laconi S, Pillai S, Porcu P P., Shafritz D A., Pani P, Laconi E. Massive liver replacement by transplanted hepatocytes in the absence of exogenous growth stimuli in rats treated with retrorsine. Am J Pathol 2001 158 771-777
24. Azuma H, Paulk N, Ranade A et al. Robust expansion of human hepatocytes in Fah-/-/Rag2-/-/Il2rg-/- mice. Nat Biotechnol 2007 25 903-910
25. Fausto N, Campbell J S., Riehle K J. Liver regeneration. Hepatology 2006 43 (2 Suppl 1) S45-S53
26. Mancone C, Conti B, Amicone L et al. Proteomic analysis reveals a major role for contact inhibition in the terminal differentiation of hepatocytes. J Hepatol 2010 52 234-243
27. Tatematsu M, Ho R H., Kaku T, Ekem J K., Farber E. Studies on the proliferation and fate of oval cells in the liver of rats treated with 2-acetylaminofluorene and partial hepatectomy. Am J Pathol 1984 114 418-430
28. Evarts R P., Nagy P, Nakatsukasa H, Marsden E, Thorgeirsson S S. In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res 1989 49 1541-1547
29. Preisegger K H., Factor V M., Fuchsbichler A, Stumptner C, Denk H, Thorgeirsson S S. Atypical ductular proliferation and its inhibition by transforming growth factor beta1 in the 3,5-diethoxycarbonyl-1,4- dihydrocollidine mouse model for chronic alcoholic liver disease. Lab Invest 1999 79 103-109
30. Factor V M., Radaeva S A., Thorgeirsson S S. Origin and fate of oval cells in dipin-induced hepatocarcinogenesis in the mouse. Am J Pathol 1994 145 409-422
31. Duncan A W., Dorrell C, Grompe M. Stem cells and liver regeneration. Gastroenterology 2009 137 466-481
32. Michalopoulos G K. Liver regeneration: alternative epithelial pathways. Int J Biochem Cell Biol 2009 September 27 (Epub ahead of print)
33. Shinozuka H, Lombardi B, Sell S, Iammarino R M. Early histological and functional alterations of ethionine liver carcinogenesis in rats fed a choline-deficient diet. Cancer Res 1978 38 1092-1098
34. Sackett S D., Li Z, Hurtt R et al. Foxl1 is a marker of bipotential hepatic progenitor cells in mice. Hepatology 2009 49 920-929
35. Haque S, Haruna Y, Saito K et al. Identification of bipotential progenitor cells in human liver regeneration. Lab Invest 1996 75 699-705 (Pubitemid 26392800)
36. Fiel M I., Antonio L B., Nalesnik M A., Thung S N., Gerber M A. Characterization of ductular hepatocytes in primary liver allograft failure. Mod Pathol 1997 10 348-353
37. Faktor V M., Engel'gardt N V., Iazova A K., Lazareva M N., Poltoranina V S., Rudinskaia T D. Common antigens of oval cells and cholangiocytes in the mouse. Their detection by using monoclonal antibodies. Ontogenez 1990 21 625-632
38. Dorrell C, Erker L, Lanxon-Cookson K M. et al. Surface markers for the murine oval cell response. Hepatology 2008 48 1282-1291
39. Rao M S., Subbarao V, Reddy J K. Induction of hepatocytes in the pancreas of copper-depleted rats following copper repletion. Cell Differ 1986 18 109-117
40. Reddy J K., Rao M S., Qureshi S A., Reddy M K., Scarpelli D G., Lalwani N D. Induction and origin of hepatocytes in rat pancreas. J Cell Biol 1984 98 2082-2090
41. Scarpelli D G., Rao M S. Differentiation of regenerating pancreatic cells into hepatocyte-like cells. Proc Natl Acad Sci U S A 1981 78 2577-2581
42. Wang X, Al-Dhalimy M, Lagasse E, Finegold M, Grompe M. Liver repopulation and correction of metabolic liver disease by transplanted adult mouse pancreatic cells. Am J Pathol 2001 158 571-579
43. Deutsch G, Jung J, Zheng M, Lra J, Zaret K S. A bipotential precursor population for pancreas and liver within the embryonic endoderm. Development 2001 128 871-881
44. Chung W S., Shin C H., Stainier D Y. Bmp2 signaling regulates the hepatic versus pancreatic fate decision. Dev Cell 2008 15 738-748
45. Dong P D., Munson C A., Norton W et al. Fgf10 regulates hepatopancreatic ductal system patterning and differentiation. Nat Genet 2007 39 397-402
46. Wang H H., Lautt W W. Evidence of nitric oxide, a flow-dependent factor, being a trigger of liver regeneration in rats. Can J Physiol Pharmacol 1998 76 1072-1079
47. Thevananther S, Sun H, Li D et al. Extracellular ATP activates c-jun N-terminal kinase signaling and cell cycle progression in hepatocytes. Hepatology 2004 39 393-402
48. Gonzales E, Julien B, Serriere-Lanneau V et al. ATP release after partial hepatectomy regulates liver regeneration in the rat. J Hepatol 2009 October 24 (Epub ahead of print)
49. Crumm S, Cofan M, Juskeviciute E, Hoek J B. Adenine nucleotide changes in the remnant liver: an early signal for regeneration after partial hepatectomy. Hepatology 2008 48 898-908
50. Jirtle R L., Carr B I., Scott C D. Modulation of insulin-like growth factor-II/mannose 6-phosphate receptors and transforming growth factor-beta 1 during liver regeneration. J Biol Chem 1991 266 22444-22450
51. Huang W, Ma K, Zhang J et al. Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration. Science 2006 312 233-236
52. Steinhardt A A., Gayyed M F., Klein A P. et al. Expression of Yes-associated protein in common solid tumors. Hum Pathol 2008 39 1582-1589
53. Lu L, Li Y, Kim S M. et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci U S A 2010 107 1437-1442
54. Song H, Mak K K., Topol L et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci U S A 2010 107 1431-1436
55. Apte U, Gkretsi V, Bowen W C. et al. Enhanced liver regeneration following changes induced by hepatocyte-specific genetic ablation of integrin-linked kinase. Hepatology 2009 50 844-851
56. Lindroos P M., Zarnegar R, Michalopoulos G K. Hepatocyte growth factor (hepatopoietin A) rapidly increases in plasma before DNA synthesis and liver regeneration stimulated by partial hepatectomy and carbon tetrachloride administration. Hepatology 1991 13 743-750
57. Matthews V B., Klinken E, Yeoh G C. Direct effects of interleukin-6 on liver progenitor oval cells in culture. Wound Repair Regen 2004 12 650-656
58. Knight B, Yeoh G C., Husk K L. et al. Impaired preneoplastic changes and liver tumor formation in tumor necrosis factor receptor type 1 knockout mice. J Exp Med 2000 192 1809-1818
59. Brooling J T., Campbell J S., Mitchell C, Yeoh G C., Fausto N. Differential regulation of rodent hepatocyte and oval cell proliferation by interferon gamma. Hepatology 2005 41 906-915
60. Jung Y, Brown K D., Witek R P. et al. Accumulation of hedgehog-responsive progenitors parallels alcoholic liver disease severity in mice and humans. Gastroenterology 2008 134 1532-1543
61. Fleig S V., Choi S S., Yang L et al. Hepatic accumulation of Hedgehog-reactive progenitors increases with severity of fatty liver damage in mice. Lab Invest 2007 87 1227-1239
62. Jakubowski A, Ambrose C, Parr M et al. TWEAK induces liver progenitor cell proliferation. J Clin Invest 2005 115 2330-2340
63. Fausto N. Tweaking liver progenitor cells. Nat Med 2005 11 1053-1054
64. Michalopoulos G K. Liver regeneration. J Cell Physiol 2007 213 286-300
65. Lepper C, Conway S J., Fan C M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 2009 460 627-631
66. Otu H H., Naxerova K, Ho K et al. Restoration of liver mass after injury requires proliferative and not embryonic transcriptional patterns. J Biol Chem 2007 282 11197-11204
67. Zhang L, Theise N, Chua M, Reid L M. The stem cell niche of human livers: symmetry between development and regeneration. Hepatology 2008 48 1598-1607
68. Burke Z, Oliver G. Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mech Dev 2002 118 147-155
69. Calmont A, Wandzioch E, Tremblay K D. et al. An FGF response pathway that mediates hepatic gene induction in embryonic endoderm cells. Dev Cell 2006 11 339-348
70. Jung J, Zheng M, Goldfarb M, Zaret K S. Initiation of mammalian liver development from endoderm by fibroblast growth factors. Science 1999 284 1998-2003
71. Rossi J M., Dunn N R., Hogan B L., Zaret K S. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev 2001 15 1998-2009
72. Shin D, Shin C H., Tucker J et al. Bmp and Fgf signaling are essential for liver specification in zebrafish. Development 2007 134 2041-2050
73. Zhang W, Yatskievych T A., Baker R K., Antin P B. Regulation of Hex gene expression and initial stages of avian hepatogenesis by Bmp and Fgf signaling. Dev Biol 2004 268 312-326
74. McLin V A., Rankin S A., Zorn A M. Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 2007 134 2207-2217
75. Ober E A., Verkade H, Field H A., Stainier D YR. Mesodermal Wnt2b signalling positively regulates liver specification. Nature 2006 442 688-691
76. Tan X, Yuan Y, Zeng G et al. Beta-catenin deletion in hepatoblasts disrupts hepatic morphogenesis and survival during mouse development. Hepatology 2008 47 1667-1679
77. Kung J W., Currie I S., Forbes S J., Ross J A. Liver development, regeneration, and carcinogenesis. J Biomed Biotechnol 2010 2010 984248
78. Monga S P., Pediaditakis P, Mule K, Stolz D B., Michalopoulos G K. Changes in WNT/beta-catenin pathway during regulated growth in rat liver regeneration. Hepatology 2001 33 1098-1109
79. Goessling W, North T E., Lord A M. et al. APC mutant zebrafish uncover a changing temporal requirement for Wnt signaling in liver development. Dev Biol 2008 320 161-174
80. Sodhi D, Micsenyi A, Bowen W C., Monga D K., Talavera J C., Monga S P. Morpholino oligonucleotide-triggered beta-catenin knockdown compromises normal liver regeneration. J Hepatol 2005 43 132-141
81. Tan X, Behari J, Cieply B, Michalopoulos G K., Monga S P. Conditional deletion of beta-catenin reveals its role in liver growth and regeneration. Gastroenterology 2006 131 1561-1572
82. Goessling W, North T E., Loewer S et al. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 2009 136 1136-1147
83. Monga S P. Role of Wnt/beta-catenin signaling in liver metabolism and cancer. Int J Biochem Cell Biol 2009 September 9 (Epub ahead of print)
84. Nejak-Bowen K, Monga S P. Wnt/beta-catenin signaling in hepatic organogenesis. Organogenesis 2008 4 92-99
85. Kan N G., Junghans D, Izpisua Belmonte J C. Compensatory growth mechanisms regulated by BMP and FGF signaling mediate liver regeneration in zebrafish after partial hepatectomy. FASEB J 2009 23 3516-3525
86. Steiling H, Wstefeld T, Bugnon P et al. Fibroblast growth factor receptor signalling is crucial for liver homeostasis and regeneration. Oncogene 2003 22 4380-4388
87. Sturm J, Keese M, Zhang H et al. Liver regeneration in FGF-2-deficient mice: VEGF acts as potential functional substitute for FGF-2. Liver Int 2004 24 161-168
88. Sugimoto H, Yang C, LeBleu V S. et al. BMP-7 functions as a novel hormone to facilitate liver regeneration. FASEB J 2007 21 256-264
89. Zaret K S. Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation. Nat Rev Genet 2008 9 329-340
90. Li L, Krantz I D., Deng Y et al. Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 1997 16 243-251
91. McDaniell R, Warthen D M., Sanchez-Lara P A. et al. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am J Hum Genet 2006 79 169-173
92. Oda T, Elkahloun A G., Pike B L. et al. Mutations in the human Jagged1 gene are responsible for Alagille syndrome. Nat Genet 1997 16 235-242
93. Macias-Silva M, Li W, Leu J I., Crissey M A., Taub R. Up-regulated transcriptional repressors SnoN and Ski bind Smad proteins to antagonize transforming growth factor-beta signals during liver regeneration. J Biol Chem 2002 277 28483-28490
94. Romero-Gallo J, Sozmen E G., Chytil A et al. Inactivation of TGF-beta signaling in hepatocytes results in an increased proliferative response after partial hepatectomy. Oncogene 2005 24 3028-3041
95. Thenappan A, Li Y, Kitisin K et al. Role of transforming growth factor beta signaling and expansion of progenitor cells in regenerating liver. Hepatology 2010 51 1373-1382
96. Nguyen L N., Furuya M H., Wolfraim L A. et al. Transforming growth factor-beta differentially regulates oval cell and hepatocyte proliferation. Hepatology 2007 45 31-41
97. Kuwahara R, Kofman A V., Landis C S., Swenson E S., Barendswaard E, Theise N D. The hepatic stem cell niche: identification by label-retaining cell assay. Hepatology 2008 47 1994-2002
98. Dovey M, Patton E E., Bowman T et al. Topoisomerase II alpha is required for embryonic development and liver regeneration in zebrafish. Mol Cell Biol 2009 29 3746-3753