The endoplasmic reticulum stress sensor IRE1 α in intestinal epithelial cells is essential for protecting against colitis

Journal of Biological Chemistry

Volumn 290, Issue 24, 2015, Pages 15237-15336

  Zhang, Hai Sheng ^a   Chen, Ying ^a   Fan, Li ^a   Xi, Qiu Lei ^b   Wu, Guo Hao ^b   Li, Xiu Xiu ^a   Yuan, Tang Long ^a   He, Sheng Qi ^a   Yu, Yue ^a   Shao, Meng Le ^a   Liu, Yang ^a   Bai, Chen Guang ^c   Ling, Zhi Qiang ^d   Li, Min ^f   Liu, Yong ^a   Fang, Jing ^a,b,e  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b FUDAN UNIVERSITY   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

^d ZHEJIANG CANCER HOSPITAL   (China)

^e BEIJING HOSPITAL   (China)

^f UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL MEMBRANES; CYTOLOGY; DISEASES; MAMMALS; PHYSIOLOGY;

APOPTOTIC PROTEINS; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL BARRIER; GENETIC ABLATION; INFLAMMATORY BOWEL DISEASE; INTESTINAL EPITHELIAL CELLS; INTESTINAL EPITHELIUM; LIPOPOLYSACCHARIDES;

CELLS;

CASPASE 3; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROTEIN IRE1; PROTEIN IRE1 ALPHA; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ERN1 PROTEIN, MOUSE; PRIMER DNA; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; COLITIS; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENZYME PHOSPHORYLATION; FEMALE; GENE EXPRESSION; GOBLET CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; IL 1BETA GENE; IL 6 GENE; IN VITRO STUDY; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA PERMEABILITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RNA SPLICING; STOMACH PROTECTION; TNF ALPHA GENE; UPREGULATION; ANIMAL; CELL LINE; ENDOPLASMIC RETICULUM; GENETICS; INTESTINE MUCOSA; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

MUS;

ANIMALS; BASE SEQUENCE; CELL LINE; COLITIS; DNA PRIMERS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; HOMEOSTASIS; INTESTINAL MUCOSA; MICE; MICE, TRANSGENIC; POLYMERASE CHAIN REACTION; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING;

EID: 84931272479     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.633560     Document Type: Article

References (47)

1. Baumgart, D. C, and Carding, S. R. (2007) Inflammatory bowel disease: cause and immunobiology. Lancet 369, 1627-1640
2. Braus, N. A., and Elliott, D. E. (2009) Advances in the pathogenesis and treatment of IBD. Clin. Immunol. 132, 1-9
3. Rutgeerts, P., Vermeire, S., and Van Assche, G. (2009) Biological therapies for inflammatory bowel diseases. Gastroenterology 136, 1182-1197
4. Abraham, C, and Cho, J. H. (2009) Inflammatory bowel disease. N. Engl. J. Med. 361, 2066-2078
5. Hall, P. A., Coates, P. J., Ansari, B., and Hopwood, D. (1994) Regulation of cell number in the mammalian gastrointestinal tract: the importance of apoptosis. J. Cell Sci. 107, 3569-3577
6. Schulzke, J. D., Ploeger, S., Amasheh, M., Fromm, A., Zeissig, S., Troeger, H., Richter, J., Bojarski, C., Schumann, M., and Fromm, M. (2009) Epithelial tight junctions in intestinal inflammation. Ann. N. Y. Acad. Sci. 1165, 294-300
7. Ron, D., and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev. Mol. Cell Biol. 8, 519-529
8. Todd, D. J., Lee, A.-H., and Glimcher, L. H. (2008) The endoplasmic reticulum stress response in immunity and autoimmunity. Nat. Rev. Immunol. 8, 663-674
9. 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
10. Mori, K., Ma, W., Gething, M.-J., and Sambrook, J. (1993) A transmembrane protein with a cdc2+CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756
11. Bertolotti, A., Wang, X., Novoa, I., Jungreis, R., Schlessinger, K., Cho, J. H., West, A. B., and Ron, D. (2001) Increased sensitivity to dextran sodium sulfate colitis in IRE1β-deficient mice. J. Clin. Investig. 107, 585-593
12. Hetz, C. (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102
13. Sano, R., and Reed, J. C. (2013) ER stress-induced cell death mechanisms. Biochim. Biophys. Acta 1833, 3460-3470
14. Oyadomari, S., and Mori, M. (2004) Roles of CHOP//GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11, 381-389
15. Shore, G. C., Papa, F. R., and Oakes, S. A. (2011) Signaling cell death from the endoplasmic reticulum stress response. Curr. Opin. Cell Biol. 23, 143-149
16. Tabas, I., and Ron, D. (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat. Cell Biol. 13, 184-190
17. Eri, R. D., Adams, R. J., Tran, T. V., Tong, H., Das, I., Roche, D. K., Oancea, I., Png, C. W., Jeffery, P. L., Radford-Smith, G. L., Cook, M. C., Florin, T. H., and McGuckin, M. A. (2011) An intestinal epithelial defect conferring ER stress results in inflammation involving both innate and adaptive immunity. Mucosal Immunol. 4, 354-364
18. Heazlewood, C K., Cook, M. C., Eri, R., Price, G. R., Tauro, S. B., Taupin, D., Thornton, D. J., Png, C W., Crockford, T. L., Cornall, R. J., Adams, R., Kato, M., Nelms, K. A., Hong, N. A., Florin, T. H., Goodnow, C C, and McGuckin, M. A. (2008) Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis. PLoS Med. 5, e54
19. 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
20. Shkoda, A., Ruiz, P. A., Daniel, H., Kim, S. C., Rogler, G., Sartor, R. B., and Haller, D. (2007) Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 132, 190-207
21. Tsuru, A., Fujimoto, N., Takahashi, S., Saito, M., Nakamura, D., Iwano, M., Iwawaki, T., Kadokura, H., Ron, D., and Kohno, K. (2013) Negative feedback by IRE1β optimizes mucin production in goblet cells. Proc. Natl. Acad. Sci. U. S. A. 110, 2864-2869
22. El Marjou, F., Janssen, K.-P., Chang, B. H., Li, M., Hindie, V., Chan, L., Louvard, D., Chambon, P., Metzger, D., and Robine, S. (2004) Tissuespecific and inducible Cre-mediated recombination in the gut epithelium. genesis 39, 186-193
23. Shao, M., Shan, B., Liu, Y., Deng, Y., Yan, C., Wu, Y., Mao, T., Qiu, Y., Zhou, Y., Jiang, S., Jia, W., Li, J., Li, J., Rui, L., Yang, L., and Liu, Y. (2014) Hepatic IRE1α regulates fasting-induced metabolic adaptive programs through the XBP1s: PPARα axis signalling. Nat Commun. 5, 3528
24. Tambuwala, M. M., Cummins, E. P., Lenihan, C. R., Kiss, J., Stauch, M., Scholz, C. C., Fraisl, P., Lasitschka, F., Mollenhauer, M., Saunders, S. P., Maxwell, P. H., Carmeliet, P., Fallon, P. G., Schneider, M., and Taylor, C. T. (2010) Loss of prolyl hydroxylase-1 protects against colitis through reduced epithelial cell apoptosis and increased barrier function. Gastroenterology 139, 2093-2101
25. Al-Sadi, R., Khatib, K., Guo, S., Ye, D., Youssef, M., and Ma, T. (2011) Occludin regulates macromolecule flux across the intestinal epithelial tight junction barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G1054-1064
26. Van Es, J. H., De Geest, N., Van De Born, M., Clevers, H., and Hassan, B. A. (2010) Intestinal stem cells lacking the Math1 tumour suppressor are refractory to Notch inhibitors. Nat Commun. 1, 18
27. Xue, J., Li, X., Jiao, S., Wei, Y., Wu, G., and Fang, J. (2010) Prolyl hydroxylase-3 is down-regulated in colorectal cancer cells and inhibits IKK/3 independent of hydroxylase activity. Gastroenterology 138, 606-615
28. Cummins, E. P., Seeballuck, F., Keely, S. J., Mangan, N. E., Callanan, J. J., Fallon, P. G., and Taylor, C. T. (2008) The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 134, 156-165.e151
29. Specian, R. D., and Oliver, M. G. (1991) Functional biology of intestinal goblet cells. Am. J. Physiol. 260, C183-C193
30. Seth, R., Raymond, F. D., and Makgoba, M. W. (1991) CirculatingICAM-1 isoforms: diagnostic prospects for inflammatory and immune disorders. Lancet 338, 83-84
31. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H. P., and Ron, D. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666
32. Alhusaini, S., McGee, K., Schisano, B., Harte, A., McTernan, P., Kumar, S., and Tripathi, G. (2010) Lipopolysaccharide, high glucose and saturated fatty acids induce endoplasmic reticulum stress in cultured primary human adipocytes: salicylate alleviates this stress. Biochem. Biophys. Res. Commun. 397, 472-478
33. Dong, M., Hu, N., Hua, Y., Xu, X., Kandadi, M. R., Guo, R., Jiang, S., Nair, S., Hu, D., and Ren, J. (2013) Chronic Akt activation attenuated lipopolysaccharide-induced cardiac dysfunction via Akt/GSK3β-dependent inhibition of apoptosis and ER stress. Biochim. Biophys. Acta 1832, 848-863
34. Endo, M., Mori, M., Akira, S., and Gotoh, T. (2006) C/EBP Homologous Protein (CHOP) Is crucial for the induction of caspase-11 and the pathogenesis of lipopolysaccharide-induced inflammation. J. Immunol. 176, 6245-6253
35. Jarry, A., Bossard, C., Bou-Hanna, C., Masson, D., Espaze, E., Denis, M. G., and Laboisse, C. L. (2008) Mucosal IL-10 and TGF-β play crucial roles in preventing LPS-driven, IFN-7-mediated epithelial damage in human colon explants. J. Clin. Investig. 118, 1132-1142
36. Yue, C., Wang, W., Tian, W. L., Huang, Q., Zhao, R. S., Zhao, Y. Z., Li, Q. R., and Li, J. S. (2013) Lipopolysaccharide-induced failure of the gut barrier is site-specific and inhibitable by growth hormone. Inflamm. Res. 62, 407-415
37. Strober, W., Fuss, I. J., and Blumberg, R. S. (2002) The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20, 495-549
38. Lin, J. H., Li, H., Yasumura, D., Cohen, H. R., Zhang, C., Panning, B., Shokat, K. M., Lavail, M. M., and Walter, P. (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318, 944-949
39. Malhotra, J. D., Miao, H., Zhang, K., Wolfson, A., Pennathur, S., Pipe, S. W., and Kaufman, R. J. (2008) Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proc. Natl. Acad. Sci. U. S. A. 105, 18525-18530
40. Abraham, C., and Medzhitov, R. (2011) Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 140, 1729-1737
41. Itoh, H., Beck, P. L., Inoue, N., Xavier, R., and Podolsky, D. K. (1999) A paradoxical reduction in susceptibility to colonic injury upon targeted transgenic ablation of goblet cells. J. Clin. Investig. 104, 1539-1547
42. Laukoetter, M. G., Nava, P., and Nusrat, A. (2008) Role of the intestinal barrier in inflammatory bowel disease. World J. Gastroenterol. 14, 401-407
43. Strugala, V., Dettmar, P. W., and Pearson, J. P. (2008) Thickness and continuity of the adherent colonic mucus barrier in active and quiescent ulcerative colitis and Crohn's disease. Int. J. Clin. Pract. 62, 762-769
44. Van Der Sluis, M., De Koning, B. A., De Bruijn, A. C., Velcich, A., Meijerink, J. P., Van Goudoever, J. B., Büller, H. A., Dekker, J., Van Seuningen, I., Renes, I. B., and Einerhand, A. W. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131, 117-129
45. Colgan, S. P., Curtis, V. F., and Campbell, E. L. (2013) The inflammatory tissue microenvironment in IBD. Inflamm. Bowel Dis. 19, 2238-2244
46. Kaser, A., and Blumberg, R. S. (2009) Endoplasmic reticulum stress in the intestinal epithelium and inflammatory bowel disease. Semin. Immunol. 21, 156-163
47. Rose, W. A., 2nd, Sakamoto, K., and Leifer, C. A. (2012) TLR9 is important for protection against intestinal damage and for intestinal repair. Sci. Rep. 2, 574