Intricately regulated: A cellular toolbox for fine-tuning XBP1 expression and activity

Cells

Volumn 1, Issue 4, 2012, Pages 738-753

  Byrd, Andrew E ^a   Brewer, Joseph W ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

Endoplasmic reticulum; Endoplasmic reticulum stress; Unfolded protein response; XBP1

Indexed keywords

MESSENGER RNA; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P85; RIBONUCLEASE; TRANSCRIPTION FACTOR FKHR; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; X BOX BINDING PROTEIN 1S; X BOX BINDING PROTEIN 1U;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; ENDOPLASMIC RETICULUM; GENE CLUSTER; HUMAN; LIVER CELL CARCINOMA; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PATHOPHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA SPLICING; SUMOYLATION; UNFOLDED PROTEIN RESPONSE;

EID: 84888399764     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells1040738     Document Type: Article

References (64)

1. Walter, P.; Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334, 1081-1086.
2. Harding, H.P.; Zhang, Y.; Bertolotti, A.; Zeng, H.; Ron, D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 2000, 5, 897-904.
3. Harding, H.P.; Zhang, Y.; Ron, D. Protein translation and folding are coupled by an endoplasmicreticulum-resident kinase. Nature 1999, 397, 271-274.
4. Scheuner, D.; Song, B.; McEwen, E.; Liu, C.; Laybutt, R.; Gillespie, P.; Saunders, T.; Bonner-Weir, S.; Kaufman, R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 2001, 7, 1165-1176.
5. Shi, Y.; Vattem, K.M.; Sood, R.; An, J.; Liang, J.; Stramm, L.; Wek, R.C. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 1998, 18, 7499-7509.
6. Adachi, Y.; Yamamoto, K.; Okada, T.; Yoshida, H.; Harada, A.; Mori, K. ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct. Funct. 2008, 33, 75-89.
7. Haze, K.; Okada, T.; Yoshida, H.; Yanagi, H.; Yura, T.; Negishi, M.; Mori, K. Identification of the g13 (camp-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response. Biochem. J. 2001, 355, 19-28.
8. Haze, K.; Yoshida, H.; Yanagi, H.; Yura, T.; Mori, K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 1999, 10, 3787-3799.
9. Wu, J.; Rutkowski, D.T.; Dubois, M.; Swathirajan, J.; Saunders, T.; Wang, J.; Song, B.; Yau, G.D.; Kaufman, R.J. ATF6α optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 2007, 13, 351-364.
10. Yamamoto, K.; Sato, T.; Matsui, T.; Sato, M.; Okada, T.; Yoshida, H.; Harada, A.; Mori, K. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6α and XBP1. Dev. Cell 2007, 13, 365-376.
11. Calfon, M.; Zeng, H.; Urano, F.; Till, J.H.; Hubbard, S.R.; Harding, H.P.; Clark, S.G.; Ron, D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. 2002, 415, 92-96.
12. Shen, X.; Ellis, R.; Lee, K.; Liu, C.-Y.; Yang, K.; Solomon, A.; Yoshida, H.; Morimoto, R.; Kurnit, D.M.; Mori, K.; et al. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 2001, 107, 893-903.
13. Yoshida, H.; Matsui, T.; Yamamoto, A.; Okada, T.; Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107, 881-891.
14. Tabas, I.; Ron, D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 2011, 13, 184-190.
15. Byrd, A.E.; Aragon, I.V.; Brewer, J.W. MicroRNA-30c-2* limits expression of proadaptive factor XBP1 in the unfolded protein response. J. Cell Biol. 2012, 196, 689-698.
16. Chen, H.; Qi, L. SUMO modification regulates the transcriptional activity of XBP1. Biochem. J. 2011, 429, 95-102.
17. Lee, J.; Sun, C.; Zhou, Y.; Lee, J.; Gokalp, D.; Herrema, H.; Park, S.W.; Davis, R.J.; Ozcan, U. p38 MAPK-mediated regulation of Xbp1s is crucial for glucose homeostasis. Nat. Med. 2011, 17, 1251-1260.
18. Majumder, M.; Huang, C.; Snider, M.D.; Komar, A.A.; Tanaka, J.; Kaufman, R.J.; Krokowski, D.; Hatzoglou, M. A novel feedback loop regulates the response to endoplasmic reticulum stress via the cooperation of cytoplasmic splicing and mRNA translation. Mol. Cell. Biol. 2012, 32, 992-1003.
19. Navon, A.; Gatushkin, A.; Zelcbuch, L.; Shteingart, S.; Farago, M.; Hadar, R.; Tirosh, B. Direct proteasome binding and subsequent degradation of unspliced XBP-1 prevent its intracellular aggregation. FEBS Letters 2010, 584, 67-73.
20. Park, S.W.; Zhou, Y.; Lee, J.; Lu, A.; Sun, C.; Chung, J.; Ueki, K.; Ozcan, U. The regulatory subunits of PI3K, p85α and p85, interact with XBP-1 and increase its nuclear translocation. Nat. Med. 2010, 16, 429-437.
21. Tirosh, B.; Iwakoshi, N.N.; Glimcher, L.H.; Ploegh, H.L. Rapid turnover of unspliced Xbp-1 as a factor that modulates the unfolded protein response. J. Biol. Chem. 2006, 281, 5852-5860.
22. Wang, F.-M.; Chen, Y.-J.; Ouyang, H.-J. Regulation of unfolded protein response modulator XBP1s by acetylation and deacetylation. Biochem. J. 2011, 433, 245-252.
23. Winnay, J.N.; Boucher, J.; Mori, M.A.; Ueki, K.; Kahn, C.R. A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response. Nat. Med. 2010, 16, 438-445.
24. Yanagitani, K.; Imagawa, Y.; Iwawaki, T.; Hosoda, A.; Saito, M.; Kimata, Y.; Kohno, K. Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol. Cell 2009, 34, 191-200.
25. Yanagitani, K.; Kimata, Y.; Kadokura, H.; Kohno, K. Translational pausing ensures membrane targeting and cytoplasmic splicing of XBP1u mRNA. Science 2011, 331, 586-589.
26. Yoshida, H.; Oku, M.; Suzuki, M.; Mori, K. pXBP1(u) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(s) in mammalian ER stress response. J. Cell. Biol. 2006, 172, 565-575.
27. Liou, H.C.; Boothby, M.R.; Finn, P.W.; Davidon, R.; Nabavi, N.; Zeleznik-Le, N.J.; Ting, J.P.; Glimcher, L.H. A new member of the leucine zipper class of proteins that binds to the HLA DR α promoter. Science 1990, 247, 1581-1584.
28. Glimcher, L.H. XBP1: The last two decades. Ann. Rheum. Dis. 2010, 69 (Suppl. 1), i67-i71.
29. Reimold, A.M.; Iwakoshi, N.N.; Manis, J.; Vallabhajosyula, P.; Szomolanyi-Tsuda, E.; Gravallese, E.M.; Friend, D.; Grusby, M.J.; Alt, F.; Glimcher, L.H. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001, 412, 300-307.
30. Lee, A.H.; Chu, G.C.; Iwakoshi, N.N.; Glimcher, L.H. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 2005, 24, 4368-4380.
31. Lee, A.-H.; Heidtman, K.; Hotamisligil, G.S.; Glimcher, L.H. Dual and opposing roles of the unfolded protein response regulated by IRE1α and XBP1 in proinsulin processing and insulin secretion. Proc. Natl. Acad. Sci. USA 2011, 108, 8885-8890.
32. Lee, A.-H.; Scapa, E.F.; Cohen, D.E.; Glimcher, L.H. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 2008, 320, 1492-1496.
33. 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. An essential role in liver development for transcription factor XBP-1. Genes Dev. 2000, 14, 152-157.
34. Iwakoshi, N.N.; Pypaert, M.; Glimcher, L.H. The transcription factor XBP-1 is essential for the development and survival of dendritic cells. J. Exp. Med. 2007, 204, 2267-2275.
35. Martinon, F.; Chen, X.; Lee, A.-H.L.; Glimcher, L.H. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 2010, 11, 411-418.
36. Kaser, A.; Lee, A.-H.; Franke, A.; Glickman, J.N.; Zeissig, S.; Tilg, H.; Nieuwenhuis, E.E.S.; Higgins, D.E.; Schreiber, S.; Glimcher, L.H. et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008, 134, 743-756.
37. Ozcan, U.; Cao, Q.; Yilmaz, E.; Lee, A.H.; Iwakoshi, N.N.; Ozdelen, E.; Tuncman, G.; Gorgun, C.; Glimcher, L.H.; Hotamisligil, G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306, 457-461.
38. Cox, J.S.; Shamu, C.E.; Walter, P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 1993, 73, 1197-1206.
39. Mori, K.; Ma, W.; Gething, M.J.; Sambrook, J. A transmembrane protein with a cdc2+/cdc28-related kinase activity is required for signaling from the ER to the nucleus. Cell 1993, 74, 743-756.
40. Sidrauski, C.; Walter, P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 1997, 90, 1031-1039.
41. Tirasophon, W.; Welihinda, A.A.; Kaufman, R.J. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 1998, 12, 1812-1824.
42. Wang, X.Z.; Harding, H.P.; Zhang, Y.; Jolicoeur, E.M.; Kuroda, M.; Ron, D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 1998, 17, 5708-5717.
43. Lee, A.H.; Iwakoshi, N.N.; Glimcher, L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 2003, 23, 7448-7459.
44. Shaffer, A.L.; Shapiro-Shelef, M.; Iwakoshi, N.N.; Lee, A.H.; Qian, S.B.; Zhao, H.; Yu, X.; Yang, L.; Tan, B.K.; Rosenwald, A. et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 2004, 21, 81-93.
45. Bartoszewski, R.; Brewer, J.W.; Rab, A.; Crossman, D.K.; Bartoszewska, S.; Kapoor, N.; Fuller, C.; Collawn, J.F.; Bebok, Z. The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J. Biol. Chem. 2011, 286, 41862-41870.
46. Iwakoshi, N.N.; Lee, A.H.; Vallabhajosyula, P.; Otipoby, K.L.; Rajewsky, K.; Glimcher, L.H. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 2003, 4, 321-329.
47. Back, S.H.; Lee, K.; Vink, E.; Kaufman, R.J. Cytoplasmic IRE1α-mediated XBP1 mRNA splicing in the absence of nuclear processing and endoplasmic reticulum stress. J. Biol. Chem. 2006, 281, 18691-18706.
48. Uemura, A.; Oku, M.; Mori, K.; Yoshida, H. Unconventional splicing of XBP1 mRNA occurs in the cytoplasm during the mammalian unfolded protein response. J. Cell Sci. 2009, 122, 2877-2886.
49. Stephens, S.B.; Dodd, R.D.; Brewer, J.W.; Lager, P.J.; Keene, J.D.; Nicchitta, C.V. Stable ribosome binding to the endoplasmic reticulum enables compartment-specific regulation of mRNA translation. Mol. Biol. Cell 2005, 16, 5819-5831.
50. Duan, Q.; Wang, X.; Gong, W.; Ni, L.; Chen, C.; He, X.; Chen, F.; Yang, L.; Wang, P.; Wang, D.W. ER stress negatively modulates the expression of the mir-199a/214 cluster to regulate tumor survival and progression in human hepatocellular cancer. PLoS One 2012, 7, e31518.
51. Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136, 215-233.
52. Behrman, S.; Acosta-Alvear, D.; Walter, P. A CHOP-regulated microRNA controls rhodopsin expression. J. Cell Biol. 2011, 192, 919-927.
53. Deng, J.; Lu, P.D.; Zhang, Y.; Scheuner, D.; Kaufman, R.J.; Sonenberg, N.; Harding, H.P.; Ron, D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 2004, 24, 10161-10168.
54. Jiang, H.Y.; Wek, S.A.; McGrath, B.C.; Scheuner, D.; Kaufman, R.J.; Cavener, D.R.; Wek, R.C. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol. Cell. Biol. 2003, 23, 5651-5663.
55. Romero-Ramirez, L.; Cao, H.; Nelson, D.; Hammond, E.; Lee, A.-H.; Yoshida, H.; Mori, K.; Glimcher, L.H.; Denko, N.C.; Giaccia, A.J. et al. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth. Cancer Res. 2004, 64, 5943-5947.
56. Hay, R.T. SUMO: A history of modification. Mol. Cell 2005, 18, 1-12.
57. Lee, A.-H.; Iwakoshi, N.N.; Anderson, K.C.; Glimcher, L.H. Proteasome inhibitors disrupt the unfolded response in myeloma cells. Proc. Natl. Acad. Sci. 2003, 100, 9946-9951.
58. Zhou, Y.; Lee, J.; Reno, C.M.; Sun, C.; Park, S.W.; Chung, J.; Lee, J.; Fisher, S.J.; White, M.F.; Biddinger, S.B.; et al. Regulation of glucose homeostasis through a XBP-1-FoxO1 interaction. Nat. Med. 2011, 17, 356-365.
59. Accili, D.; Arden, K.C. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell 2004, 117, 421-426.
60. Gross, D.N.; van den Heuvel, A.P.J.; Birnbaum, M.J. The role of FoxO in the regulation of metabolism. Oncogene 2008, 27, 2320-2336.
61. Yoshida, H.; Uemura, A.; Mori, K. pXBP1(u), a negative regulator of the unfolded protein response activator pXBP1(s), targets ATF6 but not ATF4 in proteasome-mediated degradation. Cell Struct. Funct. 2009, 34, 1-10.
62. Newman, J.R.S.; Keating, A.E. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 2003, 300, 2097-2101.
63. Hotamisligil, G.S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140, 900-917.
64. Koong, A.C.; Chauhan, V.; Romero-Ramirez, L. Targeting XBP-1 as a novel anti-cancer strategy. Cancer Biol. Ther. 2006, 5, 756-759.