A role for IRF3-dependent RXRα repression in hepatotoxicity associated with viral infections

Journal of Experimental Medicine

Volumn 203, Issue 12, 2006, Pages 2589-2602

  Chow, Edward K ^a   Castrillo, Antonio ^a   Shahangian, Arash ^a   Pei, Liming ^a   O'Connell, Ryan M ^a   Modlin, Robert L ^a   Tontonoz, Peter ^a   Cheng, Genhong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; BILE ACID; INTERFERON REGULATORY FACTOR 3; RETINOID X RECEPTOR ALPHA;

ARTICLE; CONTROLLED STUDY; DEFENSE MECHANISM; DISEASE ASSOCIATION; DOWN REGULATION; DRUG INHIBITION; DRUG MECHANISM; GENE TARGETING; HUMAN; IMMUNE RESPONSE; IN VIVO STUDY; LIVER TOXICITY; METABOLIC DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REYE SYNDROME; VIRUS INFECTION;

ANIMALS; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION, VIRAL; HEPATITIS, VIRAL, ANIMAL; INTERFERON REGULATORY FACTOR-3; MICE; MICE, KNOCKOUT; RETINOID X RECEPTOR ALPHA; REYE SYNDROME; RHABDOVIRIDAE INFECTIONS; VESICULAR STOMATITIS-INDIANA VIRUS;

EID: 33751531470     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20060929     Document Type: Article

References (75)

1. Alber, D.G., K.L. Powell, P. Vallance, D.A. Goodwin, and C. Grahame-Clarke. 2000. Herpesvirus infection accelerates atherosclerosis in the apolipoprotein E-deficient mouse. Circulation. 102:779-785.
2. Ruben, F.L., E.J. Streiff, M. Neal, and R.H. Michaels. 1976. Epidemiologic studies of Reye's syndrome: cases seen in Pittsburgh, October 1973-April 1975. Am. J. Public Health. 66:1096-1098.
3. Mondy, K., and P. Tebas. 2003. Emerging bone problems in patients infected with human immunodeficiency virus. Clin. Infect. Dis. 36:S101-S105.
4. Shaker, J.L., W.R. Reinus, and M.P. Whyte. 1998. Hepatitis C-associated osteosclerosis: late onset after blood transfusion in an elderly woman. J. Clin. Endocrinol. Metab. 83:93-98.
5. Ratziu, V., A. Heurtier, L. Bonyhay, T. Poynard, and P. Giral. 2005. Review article: an unexpected virus-host interaction - the hepatitis C virus-diabetes link. Aliment. Pharmacol. Ther. 22:56-60.
6. Michitaka, K., N. Horiike, Y. Chen, T.N. Duong, I. Konishi, T. Mashiba, Y. Tokumoto, Y. Hiasa, Y. Tanaka, M. Mizokami, and M. Onji. 2004. Gianotti-Crosti syndrome caused by acute hepatitis B virus genotype D infection. Intern. Med. 43:696-699.
7. Shi, L., N. Tu, and P.H. Patterson. 2005. Maternal influenza infection is likely to alter fetal brain development indirectly: the virus is not detected in the fetus. Int. J. Dev. Neurosci. 23:299-305.
8. Carlberg, C., I. Bendik, A. Wyss, E. Meier, L.J. Sturzenbecker, J.F. Grippo, and W. Hunziker. 1993. Two nuclear signalling pathways for vitamin D. Nature. 361:657-660.
9. Leid, M., P. Kastner, R. Lyons, H. Nakshatri, M. Saunders, T. Zacharewski, J.Y. Chen, A. Staub, J.M. Garnier, S. Mader, et al. 1992. Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell. 68:377-395.
10. Pascussi, J.M., Y. Jounaidi, L. Drocourt, J. Domergue, C. Balabaud, P. Maurel, and M.J. Vilarem. 1999. Evidence for the presence of a functional pregnane X receptor response element in the CYP3A7 promoter gene. Biochem. Biophys. Res. Commun. 260:377-381.
11. Tontonoz, P., E. Hu, and B.M. Spiegelman. 1994. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell. 79:1147-1156.
12. Tontonoz, P., E. Hu, R.A. Graves, A.I. Budavari, and B.M. Spiegelman. 1994. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8:1224-1234.
13. Willy, P.J., K. Umesono, E.S. Ong, R.M. Evans, R.A. Heyman, and D.J. Mangelsdorf. 1995. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9:1033-1045.
14. Honkakoski, P., I. Zelko, T. Sueyoshi, and M. Negishi. 1998. The nuclear orphan receptor CAR-retinoid X receptor heterodimer activates the phenobarbital-responsive enhancer module of the CYP2B gene. Mol. Cell. Biol. 18:5652-5658.
15. Laffitte, B.A., H.R. Kast, C.M. Nguyen, A.M. Zavacki, D.D. Moore, and P.A. Edwards. 2000. Identification of the DNA binding specificity and potential target genes for the farnesoid X-activated receptor. J. Biol. Chem. 275:10638-10647.
16. Issemann, I., R.A. Prince, J.D. Tugwood, and S. Green. 1993. The retinoid X receptor enhances the function of the peroxisome proliferator activated receptor. Biochimie. 75:251-256.
17. Gearing, K.L., M. Gottlicher, M. Teboul, E. Widmark, and J.A. Gustafsson. 1993. Interaction of the peroxisome-proliferator-activated receptor and retinoid X receptor. Proc. Natl. Acad. Sci. USA. 90:1440-1444.
18. Xie, W., A. Radominska-Pandya, Y. Shi, C.M. Simon, M.C. Nelson, E.S. Ong, D.J. Waxman, and R.M. Evans. 2001. An essential role for nuclear receptors SXR/PXR in detoxification of cholestatic bile acids. Proc. Natl. Acad. Sci. USA. 98:3375-3380.
19. Sucov, H.M., E. Dyson, C.L. Gumeringer, J. Price, K.R. Chien, and R.M. Evans. 1994. RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev. 8:1007-1018.
20. Janowski, B.A., P.J. Willy, T.R. Devi, J.R. Falck, and D.J. Mangelsdorf. 1996. An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature. 383:728-731.
21. Kliewer, S.A., J.T. Moore, L. Wade, J.L. Staudinger, M.A. Watson, S.A. Jones, D.D. McKee, B.B. Oliver, T.M. Willson, R.H. Zetterstrom, et al. 1998. An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell. 92:73-82.
22. Sakashita, A., M. Kizaki, S. Pakkala, G. Schiller, N. Tsuruoka, R. Tomosaki, J.F. Cameron, M.I. Dawson, and H.P. Koeffler. 1993. 9-cis-retinoic acid: effects on normal and leukemic hematopoiesis in vitro. Blood. 81:1009-1016.
23. Wu, Y., X. Zhang, F. Bardag-Gorce, R.C. Robel, J. Aguilo, L. Chen, Y. Zeng, K. Hwang, S.W. French, S.C. Lu, and Y.J. Wan. 2004. Retinoid X receptor alpha regulates glutathione homeostasis and xenobiotic detoxification processes in mouse liver. Mol. Pharmacol. 65:550-557.
24. Makishima, M., A.Y. Okamoto, J.J. Repa, H. Tu, R.M. Learned, A. Luk, M.V. Hull, K.D. Lustig, D.J. Mangelsdorf, and B. Shan. 1999. Identification of a nuclear receptor for bile acids. Science. 284:1362-1365.
25. Makishima, M., T.T. Lu, W. Xie, G.K. Whitfield, H. Domoto, R.M. Evans, M.R. Haussler, and D.J. Mangelsdorf. 2002. Vitamin D receptor as an intestinal bile acid sensor. Science. 296:1313-1316.
26. Imai, T., M. Jiang, P. Chambon, and D. Metzger. 2001. Impaired adipogenesis and lipolysis in the mouse upon selective ablation of the retinoid X receptor alpha mediated by a tamoxifen-inducible chimeric Cre recombinase (Cre-ERT2) in adipocytes. Proc. Natl. Acad. Sci. USA. 98:224-228.
27. Staudinger, J.L., B. Goodwin, S.A. Jones, D. Hawkins-Brown, K.I. MacKenzie, A. LaTour, Y. Liu, C.D. Klaassen, K.K. Brown, J. Reinhard, et al. 2001. The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc. Natl. Acad. Sci. USA. 98:3369-3374.
28. Beigneux, A.P., A.H. Moser, J.K. Shigenaga, C. Grunfeld, and K.R. Feingold. 2000. The acute phase response is associated with retinoid X receptor repression in rodent liver. J. Biol. Chem. 275:16390-16399.
29. Beigneux, A.P., A.H. Moser, J.K. Shigenaga, C. Grunfeld, and K.R. Feingold. 2002. Reduction in cytochrome P-450 enzyme expression is associated with repression of CAR (constitutive androstane receptor) and PXR (pregnane X receptor) in mouse liver during the acute phase response. Biochem. Biophys. Res. Commun. 293:145-149.
30. Kim, M.S., J. Shigenaga, A. Moser, K. Feingold, and C. Grunfeld. 2003. Repression of farnesoid X receptor during the acute phase response. J. Biol. Chem. 278:8988-8995.
31. Castrillo, A., S.B. Joseph, S.A. Vaidya, M. Haberland, A.M. Fogelman, G. Cheng, and P. Tontonoz. 2003. Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol. Cell. 12:805-816.
32. Perry, A.K., E.K. Chow, J.B. Goodnough, W.C. Yeh, and G. Cheng. 2004. Differential requirement for TANK-binding kinase-1 in type I interferon responses to Toll-like receptor activation and viral infection. J. Exp. Med. 199:1651-1658.
33. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science. 301:640-643.
34. Li, K., Z. Chen, N. Kato, M. Gale Jr., and S.M. Lemon. 2005. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J. Biol. Chem. 280:16739-16747.
35. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.
36. Fitzgerald, K.A., D.C. Rowe, B.J. Barnes, D.R. Caffrey, A. Visintin, E. Latz, B. Monks, P.M. Pitha, and D.T. Golenbock. 2003. LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the Toll adapters TRAM and TRIF. J. Exp. Med. 198:1043-1055.
37. Jiang, Z., T.W. Mak, G. Sen, and X. Li. 2004. Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc. Natl. Acad. Sci. USA. 101:3533-3538.
38. Leung, T.H., A. Hoffmann, and D. Baltimore. 2004. One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers. Cell. 118:453-464.
39. Ogawa, S., J. Lozach, C. Benner, G. Pascual, R.K. Tangirala, S. Westin, A. Hoffmann, S. Subramaniam, M. David, M.G. Rosenfeld, and C.K. Glass. 2005. Molecular determinants of crosstalk between nuclear receptors and toll-like receptors. Cell. 122:707-721.
40. Li, M., A.K. Indra, X. Warot, J. Brocard, N. Messaddeq, S. Kato, D. Metzger, and P. Chambon. 2000. Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature. 407:633-636.
41. Wan, Y.J., D. An, Y. Cai, J.J. Repa, T. Hung-Po Chen, M. Flores, C. Postic, M.A. Magnuson, J. Chen, K.R. Chien, et al. 2000. Hepatocyte-specific mutation establishes retinoid X receptor alpha as a heterodimeric integrator of multiple physiological processes in the liver. Mol. Cell. Biol. 20:4436-4444.
42. Gianni, M., A. Bauer, E. Garattini, P. Chambon, and C. Rochette-Egly. 2002. Phosphorylation by p38MAPK and recruitment of SUG-1 are required for RA-induced RAR gamma degradation and transactivation. EMBO J. 21:3760-3769.
43. Porsch-Ozcurumez, M., T. Langmann, S. Heimerl, H. Borsukova, W.E. Kaminski, W. Drobnik, C. Honer, C. Schumacher, and G. Schmitz. 2001. The zinc finger protein 202 (ZNF202) is a transcriptional repressor of ATP binding cassette transporter A1 (ABCA1) and ABCG1 gene expression and a modulator of cellular lipid efflux. J. Biol. Chem. 276:12427-12433.
44. Steffensen, K.R., E. Holter, N. Alikhani, W. Eskild, and J.A. Gustafsson. 2003. Glucocorticoid response and promoter occupancy of the mouse LXRalpha gene. Biochem. Biophys. Res. Commun. 312:716-724.
45. Aguilera, C., R. Hoya-Arias, G. Haegeman, L. Espinosa, and A. Bigas. 2004. Recruitment of IkappaBalpha to the hes1 promoter is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA. 101:16537-16542.
46. Nuthall, H.N., J. Husain, K.W. McLarren, and S. Stifani. 2002. Role for Hes1-induced phosphorylation in Groucho-mediated transcriptional repression. Mol. Cell. Biol. 22:389-399.
47. Ciotti, M., A. Marrone, C. Potter, and I.S. Owens. 1997. Genetic polymorphism in the human UGT1A6 (planar phenol) UDP-glucuronosyltransferase: pharmacological implications. Pharmacogenetics. 7:485-495.
48. Vyhlidal, C.A., P.K. Rogan, and J.S. Leeder. 2004. Development and refinement of pregnane X receptor (PXR) DNA binding site model using information theory: insights into PXR-mediated gene regulation. J. Biol. Chem. 279:46779-46786.
49. Belay, E.D., J.S. Bresee, R.C. Holman, A.S. Khan, A. Shahriari, and L.B. Schonberger. 1999. Reye's syndrome in the United States from 1981 through 1997. N. Engl. J. Med. 340:1377-1382.
50. Mitchell, R.A., J.S. Partin, E.L. Arcinue, J.C. Partin, M.L. Ram, and A.P. Sarnaik. 1985. Prognosis and diagnosis of Reye syndrome by discriminant analysis. Exp. Mol. Pathol. 43:268-273.
51. Davis, L.E., B.M. Woodfin, T.Q. Tran, L.S. Caskey, J.M. Wallace, O.U. Scremin, and K.S. Blisard. 1993. The influenza B virus mouse model of Reye's syndrome: pathogenesis of the hypoglycaemia. Int. J. Exp. Pathol. 74:251-258.
52. Dolphin, C.T., J. Caldwell, and R.L. Smith. 1987. Effect of interferon synthesis upon the metabolism of [carboxyl-14C]-aspirin in the mouse. Biochem. Pharmacol. 36:2437-2442.
53. Dupont, I., F. Berthou, P. Bodenez, L. Bardou, C. Guirriec, N. Stephan, Y. Dreano, and D. Lucas. 1999. Involvement of cytochromes P-450 2E1 and 3A4 in the 5-hydroxylation of salicylate in humans. Drug Metab. Dispos. 27:322-326.
54. Lindell, M., M.O. Karlsson, H. Lennernas, L. Pahlman, and M.A. Lang. 2003. Variable expression of CYP and Pgp genes in the human small intestine. Eur. J. Clin. Invest. 33:493-499.
55. Kuehl, G.E., J. Bigler, J.D. Potter, and J.W. Lampe. 2006. Glucuronidation of the aspirin metabolite salicylic acid by expressed UDP-glucuronosyltransferases and human liver microsomes. Drug Metab. Dispos. 34:199-202.
56. Trost, L.C., and J.J. Lemasters. 1997. Role of the mitochondrial permeability transition in salicylate toxicity to cultured rat hepatocytes: implications for the pathogenesis of Reye's syndrome. Toxicol. Appl. Pharmacol. 147:431-441.
57. Pronicka, E. 1999. Reye's syndrome - diagnostic challenge. [In Polish.] Pediatr. Pol. 74:107-110.
58. Iwanczak, F., J. Prandota, and Z. Smykowa. 1973. Two cases of Stevens-Johnson syndrome in children. [In Polish.] Wiad. Lek. 26:1539-1542.
59. Reye, R.D., G. Morgan, and J. Baral. 1963. Encephalopathy and fatty degeneration of the viscera. A disease entity in childhood. Lancet. 91:749-752.
60. Duerksen, D.R., L.D. Jewell, A.L. Mason, and V.G. Bain. 1997. Coexistence of hepatitis A and adult Reye's syndrome. Gut. 41:121-124.
61. Orlowski, J.P., P. Campbell, and S. Goldstein. 1990. Reye's syndrome: a case control study of medication use and associated viruses in Australia. Cleve. Clin. J. Med. 57:323-329.
62. Ghosh, D., D. Dhadwal, A. Aggarwal, S. Mitra, S.K. Garg, R. Kumar, and B. Kaur. 1999. Investigation of an epidemic of Reye's syndrome in northern region of India. Indian Pediatr. 36:1097-1106.
63. Treon, S.P., and S.A. Broitman. 1992. Monoclonal antibody therapy in the treatment of Reye's syndrome. Med. Hypotheses. 39:238-242.
64. Partin, J.C., W.K. Schubert, and J.S. Partin. 1971. Mitochondrial ultrastructure in Reye's syndrome (encephalopathy and fatty degeneration of the viscera). N. Engl. J. Med. 285:1339-1343.
65. Martens, M.E., C.H. Chang, and C.P. Lee. 1986. Reye's syndrome: mitochondrial swelling and Ca2+ release induced by Reye's plasma, allantoin, and salicylate. Arch. Biochem. Biophys. 244:773-786.
66. Tomoda, T., K. Takeda, T. Kurashige, H. Enzan, and M. Miyahara. 1994. Acetylsalicylate (ASA)-induced mitochondrial dysfunction and its potentiation by Ca2+. Liver. 14:103-108.
67. Araya, Z., and K. Wikvall. 1999. 6alpha-hydroxylation of taurochenodeoxycholic acid and lithocholic acid by CYP3A4 in human liver microsomes. Biochim. Biophys. Acta. 1438:47-54.
68. Shaukat, A., H.T. Tsai, R. Rutherford, and F.A. Anania. 2005. Epstein-Barr virus induced hepatitis: an important cause of cholestasis. Hepatol. Res. 33:24-26.
69. Kastner, P., J.M. Grondona, M. Mark, A. Gansmuller, M. LeMeur, D. Decimo, J.L. Vonesch, P. Dolle, and P. Chambon. 1994. Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell. 78:987-1003.
70. Yoshida, M., N. Tsuda, T. Morihata, H. Sugino, and T. Iizuka. 2004. Five patients with localized facial eruptions associated with Gianotti-Crosti syndrome caused by primary Epstein-Barr virus infection. J. Pediatr. 145:843-844.
71. Doyle, S., S. Vaidya, R. O'Connell, H. Dadgostar, P. Dempsey, T. Wu, G. Rao, R. Sun, M. Haberland, R. Modlin, and G. Cheng. 2002. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity. 17:251-263.
72. Paul, A., L. Calleja, J. Camps, J. Osada, E. Vilella, N. Ferre, E. Mayayo, and J. Joven. 2000. The continuous administration of aspirin attenuates atherosclerosis in apolipoprotein E-deficient mice. Life Sci. 68:457-465.
73. Frank, C., H. Makkonen, T.W. Dunlop, M. Matilainen, S. Vaisanen, and C. Carlberg. 2005. Identification of pregnane X receptor binding sites in the regulatory regions of genes involved in bile acid homeostasis. J. Mol. Biol. 346:505-519.
74. Ross, D.A., P.K. Rao, and T. Kadesch. 2004. Dual roles for the Notch target gene Hes-1 in the differentiation of 3T3-L1 preadipocytes. Mol. Cell. Biol. 24:3505-3513.
75. Cao, X., W. Liu, F. Lin, H. Li, S.K. Kolluri, B. Lin, Y.H. Han, M.I. Dawson, and X.K. Zhang. 2004. Retinoid X receptor regulates Nur77/TR3-dependent apoptosis [corrected] by modulating its nuclear export and mitochondrial targeting. Mol. Cell. Biol. 24:9705-9725.