deLiver'in Regeneration: Injury Response and Development

Silvia Curado; Didier Y.R. Stainier

doi:10.1055/s-0030-1255357

Seminars in Liver Disease, Inhaltsverzeichnis

Semin Liver Dis 2010; 30(3): 288-295
DOI: 10.1055/s-0030-1255357

deLiver'in Regeneration: Injury Response and Development

Silvia Curado¹ , Didier Y.R. Stainier¹

¹Department of Biochemistry and Biophysics, Programs in Developmental Biology, Genetics and Human Genetics, Liver Center, Diabetes Center and the Cardiovascular Research Institute, University of California, San Francisco, California

Abstract

ABSTRACT

Liver regeneration has traditionally been investigated in mammalian models. Recent technological developments in mouse genetics have greatly enhanced the resolving power of these studies. In addition, the zebrafish system has emerged as a complementary genetic system to study liver regeneration. One of the most promising attributes of the zebrafish system is its amenability to large-scale screens including genetic and chemical screens. Also, as our understanding of liver development is becoming more detailed, it is important to evaluate the commonalities and differences between organ development and regeneration.

KEYWORDS

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

Volltext

Referenzen

REFERENCES

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 gene—tomm22—is 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 Stöcker 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
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
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, Lóra 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, Wüstefeld 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

Silvia CuradoPh.D.

Department of Biochemistry and Biophysics, Programs in Developmental Biology, Genetics and Human Genetics, Liver Center, Diabetes Center and the Cardiovascular Research Institute, University of California, San Francisco

1550 Fourth Street, San Francisco, CA 94158-2324

eMail: Silvia.Curado@med.nyu.edu