Hrd1 suppresses Nrf2-mediated cellular protection during liver cirrhosis

Genes and Development

Volumn 28, Issue 7, 2014, Pages 708-722

  Wu, Tongde ^a   Zhao, Fei ^a   Gao, Beixue ^b   Tan, Can ^b   Yagishita, Naoko ^c   Nakajima, Toshihiro ^c,d   Wong, Pak K ^e   Chapman, Eli ^a   Fang, Deyu ^b   Zhang, Donna D ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d TOKYO MEDICAL UNIVERSITY   (Japan)

^e University of Arizona   (United States)

Author keywords

Hrd1; Liver cirrhosis; Nrf2

Indexed keywords

HRD1 PROTEIN; TRANSCRIPTION FACTOR NRF2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CELL PROTECTION; CELLULAR STRESS RESPONSE; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LIVER CIRRHOSIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

HRD1; LIVER CIRRHOSIS; NRF2;

ANIMALS; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; LIVER CIRRHOSIS; MICE; NF-E2-RELATED FACTOR 2; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84898874270     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.238246.114     Document Type: Article

References (49)

1. Amano T., Yamasaki S, Yagishita N, Tsuchimochi K, Shin H, Kawahara K., Aratani S, Fujita H, Zhang L, Ikeda R, et al. 2003. Synoviolin/Hrd1, an E3 ubiquitin ligase, as a novel pathogenic factor for arthropathy. Genes Dev 17: 2436-2449.
2. Calfon M., Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark S. G, Ron D. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96.
3. Carvalho P., Goder V, Rapoport TA. 2006. Distinct ubiquitinligase complexes define convergent pathways for the degradation of ER proteins. Cell 126: 361-373.
4. Chen W., Sun Z, Wang XJ, Jiang T, Huang Z, Fang D, Zhang DD. 2009. Direct interaction between Nrf2 and p21(Cip1/WAF1) upregulates the Nrf2-mediated antioxidant response. Mol Cell 34: 663-673.
5. Chen S., Zou L, Li L, Wu T. 2013. The protective effect of glycyrrhetinic acid on carbon tetrachloride-induced chronic liver fibrosis in mice via upregulation of Nrf2. PLoS ONE 8: e53662.
6. Chowdhry S., Zhang Y, McMahon M, Sutherland C, Cuadrado A, Hayes J.D. 2013. Nrf2 is controlled by two distinct β-TrCP recognition motifs in its Neh6 domain, one of which can be modulated by GSK-3 activity. Oncogene 32: 3765-3781.
7. Cross B. C, Bond PJ, Sadowski PG, Jha BK, Zak J, Goodman JM, Silverman R. H, Neubert TA, Baxendale IR, Ron D, et al. 2012. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci 109: E869-E878.
8. Gao B., Lee SM, Chen A, Zhang J, Zhang DD, Kannan K, Ortmann R. A, Fang D. 2008. Synoviolin promotes IRE1 ubiquitination and degradation in synovial fibroblasts from mice with collagen-induced arthritis. EMBO Rep 9: 480-485.
9. Hasegawa D., Fujii R, Yagishita N, Matsumoto N, Aratani S, Izumi T., Azakami K, Nakazawa M, Fujita H, Sato T, et al. 2010. E3 ubiquitin ligase synoviolin is involved in liver fibrogenesis. PLoS ONE 5: e13590.
10. Hernandez-Gea V, Friedman SL. 2011. Pathogenesis of liver fibrosis. Annu Rev Pathol 6: 425-456.
11. Itoh K., Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13: 76-86.
12. Jaramillo M. C, Zhang DD. 2013. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 27: 2179-2191.
13. Jiang T., Huang Z, Chan JY, Zhang DD. 2009. Nrf2 protects against As(III)-induced damage in mouse liver and bladder. Toxicol Appl Pharmacol 240: 8-14.
14. Kawata K., Kobayashi Y, Souda K, Kawamura K, Sumiyoshi S, Takahashi Y., Noritake H, Watanabe S, Suehiro T, Nakamura H. 2010. Enhanced hepatic Nrf2 activation after ursodeoxycholic acid treatment in patients with primary biliary cirrhosis. Antioxid Redox Signal 13: 259-268.
15. Kensler T. W, Wakabayashi N, Biswal S. 2007. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47: 89-116.
16. Kobayashi A., Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K., Yamamoto M. 2004. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24: 7130-7139.
17. Kurzawski M., Dziedziejko V, Urasinska E, Post M, Wojcicki M, Mietkiewski J., Drozdzik M. 2012. Nuclear factor erythroid 2-like 2 (Nrf2) expression in end-stage liver disease. Environ Toxicol Pharmacol 34: 87-95.
18. Lotersztajn S., Julien B, Teixeira-Clerc F, Grenard P, Mallat A. 2005. Hepatic fibrosis: molecular mechanisms and drug targets. Annu Rev Pharmacol Toxicol 45: 605-628.
19. Ma Q., He X. 2012. Molecular basis of electrophilic and oxidative defense: promises and perils of Nrf2. Pharmacol Rev 64: 1055-1081.
20. Magesh S., Chen Y, Hu L. 2012. Small molecule modulators of Keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents. Med Res Rev 32: 687-726.
21. McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD. 2006. Dimerization of substrate adaptors can facilitate cullinmediated ubiquitylation of proteins by a 'tethering' mechanism: a two-site interaction model for the Nrf2-Keap1 complex. J Biol Chem 281: 24756-24768.
22. More V. R, Cheng Q, Donepudi AC, Buckley DB, Lu ZJ, Cherrington N. J, Slitt AL. 2013. Alcohol cirrhosis alters nuclear receptor and drug transporter expression in human liver. Drug Metab Dispos 41: 1148-1155.
23. Mu Y. P, Ogawa T, Kawada N. 2010. Reversibility of fibrosis, inflammation, and endoplasmic reticulum stress in the liver of rats fed a methionine-choline-deficient diet. Lab Invest 90: 245-256.
24. Nair S., Xu C, Shen G, Hebbar V, Gopalakrishnan A, Hu R, Jain MR, Liew C, Chan JY, Kong AN. 2007. Toxicogenomics of endoplasmic reticulum stress inducer tunicamycin in the small intestine and liver of Nrf2 knockout and C57BL/6J mice. Toxicol Lett 168: 21-39.
25. Qiu Q., Zheng Z, Chang L, Zhao YS, Tan C, Dandekar A, Zhang Z, Lin Z., Gui M, Li X, et al. 2013. Toll-like receptor-mediated IRE1αactivation as a therapeutic target for inflammatory arthritis. EMBO J 32: 2477-2490.
26. Rada P., Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A. 2011. SCF/β-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 31: 1121-1133.
27. Rada P., Rojo AI, Evrard-Todeschi N, Innamorato NG, Cotte A, Jaworski T., Tobon-Velasco JC, Devijver H, Garcia-Mayoral MF, Van Leuven F, et al. 2012. Structural and functional characterization of Nrf2 degradation by the glycogen synthase kinase 3/β-TrCP axis. Mol Cell Biol 32: 3486-3499.
28. Ramani K., Tomasi ML, Yang H, Ko K, Lu SC. 2012. Mechanism and significance of changes in glutamate-cysteine ligase expression during hepatic fibrogenesis. J Biol Chem 287: 36341-36355.
29. Steffen J., Seeger M, Koch A, Kruger E. 2010. Proteasomal degradation is transcriptionally controlled by TCF11 via an ERAD-dependent feedback loop. Mol Cell 40: 147-158.
30. Sun Z., Zhang S, Chan JY, Zhang DD. 2007. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Mol Cell Biol 27: 6334-6349.
31. Sun Z., Chin YE, Zhang DD. 2009. Acetylation of Nrf2 by p300/ CBP augments promoter-specific DNA binding of Nrf2 during the antioxidant response. Mol Cell Biol 29: 2658-2672.
32. Sykiotis G. P, Bohmann D. 2010. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci Signal 3: re3.
33. Tanabe C., Maeda T, Zou K, Liu J, Liu S, Nakajima T, Komano H. 2012. The ubiquitin ligase synoviolin up-regulates amyloid β production by targeting a negative regulator of γ-secretase, Rer1, for degradation. J Biol Chem 287: 44203-44211.
34. Tong K. I, Kobayashi A, Katsuoka F, Yamamoto M. 2006. Twosite substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol Chem 387: 1311-1320.
35. Travers K. J, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
36. Tsang K. Y, Chan D, Bateman JF, Cheah KS. 2010. In vivo cellular adaptation to ER stress: survival strategies with doubleedged consequences. J Cell Sci 123: 2145-2154.
37. Tsuchiya Y., Morita T, Kim M, Iemura S, Natsume T, Yamamoto M, Kobayashi A. 2011. Dual regulation of the transcriptional activity of Nrf1 by β-TrCP-and Hrd1-dependent degradation mechanisms. Mol Cell Biol 31: 4500-4512.
38. Wang J. Q, Chen X, Zhang C, Tao L, Zhang ZH, Liu XQ, Xu YB, Wang H., Li J, Xu DX. 2013. Phenylbutyric acid protects against carbon tetrachloride-induced hepatic fibrogenesis in mice. Toxicol Appl Pharmacol 266: 307-316.
39. Wynn T. A, Ramalingam TR. 2012. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18: 1028-1040.
40. Yagishita N., Ohneda K, Amano T, Yamasaki S, Sugiura A, Tsuchimochi K., Shin H, Kawahara K, Ohneda O, Ohta T, et al. 2005. Essential role of synoviolin in embryogenesis. J Biol Chem 280: 7909-7916.
41. Yagishita N., Aratani S, Leach C, Amano T, Yamano Y, Nakatani K, Nishioka K, Nakajima T. 2012. RING-finger type E3 ubiquitin ligase inhibitors as novel candidates for the treatment of rheumatoid arthritis. Int J Mol Med 30: 1281-1286.
42. Yamamoto K., Suzuki N, Wada T, Okada T, Yoshida H, Kaufman RJ, Mori K. 2008. Human HRD1 promoter carries a functional unfolded protein response element to which XBP1 but not ATF6 directly binds. J Biochem 144: 477-486.
43. Yamasaki S., Yagishita N, Sasaki T, Nakazawa M, Kato Y, Yamadera T., Bae E, Toriyama S, Ikeda R, Zhang L, et al. 2007. Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'synoviolin'. EMBO J 26: 113-122.
44. Yoshida H., Matsui T, Yamamoto A, Okada T, Mori K. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
45. Zhang D. D, Hannink M. 2003. Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 23: 8137-8151.
46. Zhang D. D, Lo SC, Cross JV, Templeton DJ, Hannink M. 2004. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol 24: 10941-10953.
47. Zhang Y., Crouch DH, Yamamoto M, Hayes JD. 2006. Negative regulation of the Nrf1 transcription factor by its N-terminal domain is independent of Keap1: Nrf1, but not Nrf2, is targeted to the endoplasmic reticulum. Biochem J 399: 373-385.
48. Zheng H., Whitman SA, Wu W, Wondrak GT, Wong PK, Fang D, Zhang D.D. 2011a. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 60: 3055-3066.
49. Zheng Z., Zhang C, Zhang K. 2011b. Measurement of ER stress response and inflammation in the mouse model of nonalcoholic fatty liver disease. Methods Enzymol 489: 329-348.