Liver-specific deletion of augmenter of liver regeneration accelerates development of steatohepatitis and hepatocellular carcinoma in mice

Gastroenterology

Volumn 148, Issue 2, 2015, Pages 379-391.e4

  Gandhi, Chandrashekhar R ^a,b,c,d   Chaillet, J Richard ^e   Nalesnik, Michael A ^d,e   Kumar, Sudhir ^a   Dangi, Anil ^b,c   Demetris, A Jake ^d,e   Ferrell, Robert ^f   Wu, Tong ^g   Divanovic, Senad ^a   Stankeiwicz, Traci ^a   Shaffer, Benjamin ^e   Stolz, Donna B ^e   Harvey, Stephen A K ^e   Wang, Jiang ^h   Starzl, Thomas E ^d  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

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

^f UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^g TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

ALD; Augmenter of Liver Regeneration; Mouse Model; NASH

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE; ALBUMIN; AUGMENTER OF LIVER REGENERATION; CARBAMYL PALMITOYL TRANSFERASE 1A; CRE RECOMBINASE; MITOCHONDRIAL DNA; PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSFERASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; CYTOCHROME REDUCTASE; GFER PROTEIN, HUMAN; GFER PROTEIN, MOUSE; OXIDOREDUCTASE;

ALCOHOL LIVER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIRTH; CELL DEATH; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA DAMAGE; DUCTULAR PROLIFERATION; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM STRESS; ENZYME SYNTHESIS; FATTY ACID TRANSPORT; FATTY LIVER; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INFLAMMATION; KNOCKOUT MOUSE; LIPID HOMEOSTASIS; LIPID METABOLISM; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LIVER DISEASE; LIVER FIBROSIS; LIVER HISTOLOGY; LIVER NECROSIS; LIVER REGENERATION; LOXP SITE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION SWELLING; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; CARCINOMA, HEPATOCELLULAR; LIVER CIRRHOSIS, EXPERIMENTAL; LIVER NEOPLASMS; MITOCHONDRION; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CYTOCHROME REDUCTASES; FATTY LIVER; HUMANS; LIPID METABOLISM; LIVER CIRRHOSIS, EXPERIMENTAL; LIVER NEOPLASMS; LIVER REGENERATION; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS;

EID: 84921331962     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.10.008     Document Type: Article

References (52)

1. A. Francavilla, M. Hagiya, and K.A. Porter Augmenter of liver regeneration: Its place in the universe of hepatic growth factors Hepatology 20 1994 747 757
2. C.R. Gandhi Augmenter of liver regeneration Fibrogenesis Tissue Repair 5 2012 10
3. M. Hagiya, A. Francavilla, and L. Polimeno Cloning and sequence analysis of the rat augmenter of liver regeneration (ALR) gene: expression of biologically active recombinant ALR and demonstration of tissue distribution Proc Natl Acad Sci U S A 91 1994 8142 8146
4. R. Giorda, M. Hagiya, and T. Seki Analysis of the structure and expression of the augmenter of liver regeneration (ALR) gene Mol Med 2 1996 97 108
5. C.R. Gandhi, R. Kuddus, and V.M. Subbotin A fresh look at augmenter of liver regeneration in rats Hepatology 29 1999 1435 1445
6. A. Tury, G. Mairet-Coello, and T. Lisowsky Expression of the sulfhydryl oxidase ALR (augmenter of liver regeneration) in adult rat brain Brain Res 1048 2005 87 97
7. S.R. Farrell, and C. Thorpe Augmenter of liver regeneration: a flavin-dependent sulfhydryl oxidase with cytochrome c reductase activity Biochemistry 44 2005 1532 1541
8. S. Allen, V. Balabanidou, and D.P. Sideris Erv1 mediates the Mia40-dependent protein import pathway and provides a functional link to the respiratory chain by shuttling electrons to cytochrome c J Mol Biol 353 2005 937 944
9. H. Lange, T. Lisowsky, and J. Gerber An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins EMBO Rep 2 2001 715 720
10. A. Francavilla, N.L. Vujanovic, and L. Polimeno The in vivo effect of hepatotrophic factors augmenter of liver regeneration, hepatocyte growth factor, and insulin-like growth factor-II on liver natural killer cell functions Hepatology 25 1997 411 415
11. C.R. Gandhi, N. Murase, and T.E. Starzl Cholera toxin-sensitive GTP-binding protein-coupled activation of augmenter of liver regeneration (ALR) receptor and its function in rat Kupffer cells J Cell Physiol 222 2010 365 373
12. C. Thirunavukkarasu, L.F. Wang, and S.A. Harvey Augmenter of liver regeneration: an important intracellular survival factor for hepatocytes J Hepatol 48 2008 578 588
13. M.R. Dyer, and J.E. Walker Sequences of members of the human gene family for the c subunit of mitochondrial ATP synthase Biochem J 293 1993 51 64
14. H.S. Li, J.Y. Zhang, and B.S. Thompson Rat mitochondrial ATP synthase ATP5G3: cloning and upregulation in pancreas after chronic ethanol feeding Physiol Genom 6 2001 91 98
15. V. Tiranti, E. Rossi, and A. Ruiz-Carrillo Chromosomal localization of mitochondrial transcription factor A (TCF6), single-stranded DNA-binding protein (SSBP), and endonuclease G (ENDOG), three human housekeeping genes involved in mitochondrial biogenesis Genomics 25 1995 559 564
16. J.J. Lemasters, and R.G. Thurman Hypoxia and reperfusion injury to liver Prog Liver Dis 11 1993 85 114
17. N. Kaplowitz, and H. Tsukamoto Oxidative stress and liver disease Prog Liver Dis 14 1996 131 159
18. S. Kanvah, J. Joseph, and G.B. Schuster Oxidation of DNA: damage to nucleobases Acc Chem Res 43 2010 280 287
19. K.C. Cheng, D.S. Cahill, and H. Kasai 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and C→A substitutions J Biol Chem 267 1992 166 172
20. R.A. Chalmers, C.A. Stanley, and N. English Mitochondrial carnitine-acylcarnitine translocase deficiency presenting as sudden neonatal death J Pediatr 131 1997 220 225
21. M. Rakhshandehroo, B. Knoch, and M. Müller Peroxisome proliferator-activated receptor alpha target genes PPAR Res 2010 2010 ID612089
22. J. Riemer, N. Bulleid, and J.M. Herrmann Disulfide formation in the ER and mitochondria: two solutions to a common process Science 324 2009 1284 1287
23. K. Bihlmaier, N. Mesecke, and N. Terziyska The disulfide relay system of mitochondria is connected to the respiratory chain J Cell Biol 179 2007 389 395
24. L. Banci, I. Bertini, and V. Calderone Molecular recognition and substrate mimicry drive the electron-transfer process between MIA40 and ALR Proc Natl Acad Sci U S A 108 2011 4811 4816
25. D.V. Dabir, S.A. Hasson, and K. Setoguchi A small molecule inhibitor of redox-regulated protein translocation into mitochondria Dev Cell 25 2013 81 92
26. T. Lisowsky Dual function of a new nuclear gene for oxidative phosphorylation and vegetative growth in yeast Mol Gen Genet 232 1992 58 64
27. T. Lisowsky ERV1 is involved in the cell-division cycle and the maintenance of mitochondrial genomes in Saccharomyces cerevisiae Curr Genet 26 1994 15 20
28. C. Postic, M. Shiota, and K.D. Niswender Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase J Biol Chem 274 1999 305 315
29. J. Gu, Y. Weng, and Q.Y. Zhang Liver-specific deletion of the NADPH-cytochrome P450 reductase gene: impact on plasma cholesterol homeostasis and the function and regulation of microsomal cytochrome P450 and heme oxygenase J Biol Chem 278 2003 25895 25901
30. Z. Xu, L. Chen, and L. Leung Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia Proc Natl Acad Sci U S A 102 2005 4120 4125
31. G.K. Michalopoulos Liver regeneration: alternative epithelial pathways Int J Biochem Cell Biol 43 2011 173 179
32. J. Best, L. Dollé, and P. Manka Role of liver progenitors in acute liver injury Front Physiol 4 2013 258
33. K.J. Riehle, Y.Y. Dan, and J.S. Campbell New concepts in liver regeneration J Gastroenterol Hepatol 26 Suppl 1 2011 203 212
34. S.M. Tilghman, and A. Belayew Transcriptional control of the murine albumin/alpha-fetoprotein locus during development Proc Natl Acad Sci U S A 79 1982 5254 5257
35. D. Boison, L. Scheurer, and V. Zumsteg Neonatal hepatic steatosis by disruption of the adenosine kinase gene Proc Natl Acad Sci U S A 99 2002 6985 6990
36. B. Fromenty, and D. Pessayre Inhibition of mitochondrial β-oxidation as a mechanism of hepatotoxicity Pharmacol Ther 67 1995 101 154
37. C. Lu, Y. Li, and Y. Zhao Intracrine hepatopoietin potentiates AP-1 activity through JAB1 independent of MAPK pathway FASEB J 16 2002 90 92
38. L. Libbrecht, and T. Roskams Hepatic progenitor cells (HPCs) in human liver tumor development Semin Cell Dev Biol 13 2002 389 396
39. K.N. Lowes, B.A. Brennan, and G.C. Yeoh Oval cell numbers in human chronic liver diseases are directly related to disease severity Am J Pathol 154 1999 537 541
40. T.A. Roskams, L. Libbrecht, and V.J. Desmet Progenitor cells in diseased human liver Semin Liver Dis 23 2003 385 396
41. E.E. Powell, W.G. Cooksley, and R. Hanson The natural history of nonalcoholic steatohepatitis: a follow-up study of forty-two patients for up to 21 years Hepatology 11 1990 74 80
42. C. Day, and S. Saksena Non-alcoholic steatohepatitis: definitions and pathogenesis J Gastroenterol Hepatol 17 2002 S377 S384
43. E.M. Brunt Nonalcoholic steatohepatitis Semin Liver Dis 24 2004 3 20
44. W.E. Thasler, T. Schlott, and P. Thelen Expression of augmenter of liver regeneration (ALR) in human liver cirrhosis and carcinoma Histopathology 47 2005 57 66
45. M. Lakso, J.G. Pichel, and J.R. Gorman Efficient in vivo manipulation of mouse genomic sequences at the zygote stage Proc Natl Acad Sci U S A 93 1996 5860 5865
46. C.R. Gandhi, R. Kuddus, and V.M. Subbotin A fresh look at augmenter of liver regeneration in rats Hepatology 29 1999 1435 1445
47. J.G. Lunz 3rd, H. Tsuji, and I. Nozaki An inhibitor of cyclin-dependent kinase, stress-induced p21Waf-1/Cip-1, mediates hepatocyte mito-inhibition during the evolution of cirrhosis Hepatology 41 2005 1262 1271
48. C. Thirunavukkarasu, Y. Yang, and V.M. Subbotin Endothelin receptor antagonist TAK-044 arrests and reverses the development of carbon tetrachloride-induced cirrhosis in rats Gut 53 2004 1010 1019
49. F. Sweat, H. Puchtler, and S. Rosenthal Sirius red F3BA as a stain for connective tissue Arch Pathol Lab Med 78 1964 69 72
50. S.A.K. Harvey, A. Dangi, and A. Tandon The transcriptomic response of rat hepatic stellate cells to endotoxin: implications for hepatic inflammation and immune regulation PLoS ONE 8 2013 e82159
51. R. Stewart, A. Dangi, and C. Huang A novel mouse model of depletion of stellate cells clarifies their role in ischemia/reperfusion- and endotoxin-induced acute liver injury J Hepatol 60 2014 298 305
52. L.L. Bieber, T. Abraham, and T. Helmrath A rapid spectrophotometric assay for carnitine palmitoyltransferase Anal Biochem 50 1972 509 518