SUMO modification regulates the transcriptional activity of XBP1

Biochemical Journal

Volumn 429, Issue 1, 2010, Pages 95-102

  Chen, Hui ^a   Qi, Ling ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Post translational modification; Protein inhibitor of activated signal transducer and activator of transcription (PIAS); Small ubiquitin related modifier (SUMO); Transcriptional regulation; Unfolded protein response (UPR); X box binding protein 1 (XBP1)

Indexed keywords

ACTIVATED SIGNAL; BINDING PROTEINS; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN INHIBITORS; SMALL UBIQUITIN-RELATED MODIFIER (SUMO); SMALL UBIQUITIN-RELATED MODIFIERS; TRANSCRIPTIONAL REGULATION; UNFOLDED PROTEIN RESPONSE;

AMINO ACIDS; BODY FLUIDS; CHEMICAL ACTIVATION; TRANSCRIPTION FACTORS; TRANSDUCERS;

TRANSCRIPTION;

HISTONE DEACETYLASE 5; STAT2 PROTEIN; SUMO 3 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; LYSINE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENDOPLASMIC RETICULUM; HOMEOSTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SUMOYLATION; TRANSACTIVATION; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION;

ANIMALS; CELL LINE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; HOMEOSTASIS; HUMANS; LYSINE; MICE; MUTAGENESIS, SITE-DIRECTED; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SUMO-1 PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 77954525706     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100193     Document Type: Article

References (35)

1. +/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756
2. Cox, J. S., Shamu, C. E. and Walter, P. (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206
3. Cox, J. S. and Walter, P. (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87, 391-404
4. Sidrauski, C., Cox, J. S. and Walter, P. (1996) tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87, 405-413 (Pubitemid 26374315)
5. Sidrauski, C. and Walter, P. (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031-1039
6. Calfon, M., Zeng, H., Urano, F., Till, J. H., Hubbard, S. R., Harding, H. P., Clark, S. G. and Ron, D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96
7. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and 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
8. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H., Mori, K. and Kaufman, R. J. (2002) IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16, 452-466
9. Shen, X., Ellis, R. E., Lee, K., Liu, C. Y., Yang, K., Solomon, A., Yoshida, H., Morimoto, R., Kurnit, D. M., Mori, K. and Kaufman, R. J. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107, 893-903
10. Lee, A. H., Iwakoshi, N. N. and Glimcher, L. H. (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459
11. Ron, D. and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529
12. Lee, A. H., Chu, G. C., Iwakoshi, N. N. and Glimcher, L. H. (2005) XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24, 4368-4380
13. Masaki, T., Yoshida, M. and Noguchi, S. (1999) Targeted disruption of CRE-binding factor TREB5 gene leads to cellular necrosis in cardiac myocytes at the embryonic stage. Biochem. Biophys. Res. Commun. 261, 350-356
14. Reimold, A. M., Etkin, A., Clauss, I., Perkins, A., Friend, D. S., Zhang, J., Horton, H. F., Scott, A., Orkin, S. H., Byrne, M. C. et al. (2000) An essential role in liver development for transcription factor XBP-1. Genes Dev. 14, 152-157
15. Reimold, A. M., Iwakoshi, N. N., Manis, J., Vallabhajosyula, P., Szomolanyi-Tsuda, E., Gravallese, E. M., Friend, D., Grusby, M. J., Alt, F. and Glimcher, L. H. (2001) Plasma cell differentiation requires the transcription factor XBP-1. Nature 412, 300-307 (Pubitemid 32691837)
16. Zhang, K., Wong, H. N., Song, B., Miller, C. N., Scheuner, D. and Kaufman, R. J. (2005) The unfolded protein response sensor IRE1α is required at two distinct steps in B cell lymphopoiesis. J. Clin. Invest. 115, 268-281
17. Lee, A. H., Scapa, E. F., Cohen, D. E. and Glimcher, L. H. (2008) Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320, 1492-1496
18. Sha, H., He, Y., Chen, H., Wang, C., Zenno, A., Shi, H., Yang, X., Zhang, X. and Qi, L. (2009) The IRE1α-XBP1 pathway of the unfolded protein response is required for adipogenesis. Cell Metab. 9, 556-564
19. Hay, R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1-12
20. Rytinki, M. M., Kaikkonen, S., Pehkonen, P., Jaaskelainen, T. and Palvimo, J. J. (2009) PIAS proteins: pleiotropic interactors associated with SUMO. Cell. Mol. Life Sci. 66, 3029-3041
21. Golebiowski, F., Matic, I., Tatham, M. H., Cole, C., Yin, Y., Nakamura, A., Cox, J., Barton, G. J., Mann, M. and Hay, R. T. (2009) System-wide changes to SUMO modifications in response to heat shock. Sci. Signaling 2, ra24
22. Johnson, E. S. (2004) Protein modification by SUMO. Annu. Rev. Biochem. 73, 355-382
23. Oishi, Y., Manabe, I., Tobe, K., Ohsugi, M., Kubota, T., Fujiu, K., Maemura, K., Kubota, N., Kadowaki, T. and Nagai, R. (2008) SUMOylation of Kruppel-like transcription factor 5 acts as a molecular switch in transcriptional programs of lipid metabolism involving PPAR-δ. Nat. Med. 14, 656-666
24. Stankovic-Valentin, N., Deltour, S., Seeler, J., Pinte, S., Vergoten, G., Guerardel, C., Dejean, A. and Leprince, D. (2007) An acetylation/deacetylation- SUMOylation switch through a phylogenetically conserved psiKXEP motif in the tumor suppressor HIC1 regulates transcriptional repression activity. Mol. Cell. Biol. 27, 2661-2675
25. Duprez, E., Saurin, A. J., Desterro, J. M., Lallemand-Breitenbach, V., Howe, K., Boddy, M. N., Solomon, E., de The, H., Hay, R. T. and Freemont, P. S. (1999) SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J. Cell Sci. 112, 381-393 (Pubitemid 29080660)
26. Rodriguez, M. S., Dargemont, C. and Hay, R. T. (2001) SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276, 12654-12659
27. Girdwood, D., Bumpass, D., Vaughan, O. A., Thain, A., Anderson, L. A., Snowden, A. W., Garcia-Wilson, E., Perkins, N. D. and Hay, R. T. (2003) P300 transcriptional repression is mediated by SUMO modification. Mol. Cell 11, 1043-1054
28. Shiio, Y. and Eisenman, R. N. (2003) Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 100, 13225-13230
29. Yang, S. H. and Sharrocks, A. D. (2004) SUMO promotes HDAC-mediated transcriptional repression. Mol. Cell 13, 611-617
30. Clauss, I. M., Chu, M., Zhao, J. L. and Glimcher, L. H. (1996) The basic domain/leucine zipper protein hXBP-1 preferentially binds to and transactivates CRE-like sequences containing an ACGT core. Nucleic Acids Res. 24, 1855-1864
31. Iwakoshi, N. N., Lee, A. H., Vallabhajosyula, P., Otipoby, K. L., Rajewsky, K. and Glimcher, L. H. (2003) Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 4, 321-329
32. Shaffer, A. L., Shapiro-Shelef, M., Iwakoshi, N. N., Lee, A. H., Qian, S. B., Zhao, H., Yu, X., Yang, L., Tan, B. K. and Rosenwald, A. et al. (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21, 81-93
33. Yoshida, H. (2007) ER stress and diseases. FEBS J. 274, 630-658
34. Kaser, A., Lee, A. H., Franke, A., Glickman, J. N., Zeissig, S., Tilg, H., Nieuwenhuis, E. E., Higgins, D. E., Schreiber, S., Glimcher, L. H. and Blumberg, R. S. (2008) XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134, 743-756
35. Kim, I., Xu, W. and Reed, J. C. (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 7, 1013-1030