Autophagy, microbial sensing, endoplasmic reticulum stress, and epithelial function in inflammatory bowel disease

Gastroenterology

Volumn 140, Issue 6, 2011, Pages 1738-1747.e2

  Kaser, Arthur ^a,b   Blumberg, Richard S ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Autophagy; Crohn's Disease; Endoplasmic Reticulum Stress; Genetics; Inflammatory Bowel Disease; Innate Immunity; Pathogenesis; Ulcerative Colitis; Unfolded Protein Response

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15;

ARTICLE; ATG16L1 GENE; AUTOPHAGY; CROHN DISEASE; ENDOPLASMIC RETICULUM STRESS; ENTERITIS; GENE; GENETIC RISK; HUMAN; INNATE IMMUNITY; INTESTINE EPITHELIUM; INTESTINE FLORA; IRGM GENE; NONHUMAN; ORMDL3 GENE; PANETH CELL; PRIORITY JOURNAL; ULCERATIVE COLITIS; XBP1 GENE;

EID: 79955555098     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2011.02.048     Document Type: Article

References (117)

1. A. Kaser, S. Zeissig, and R.S. Blumberg Inflammatory bowel disease Annu Rev Immunol 28 2010 573 621
2. C. Abraham, and J.H. Cho Inflammatory bowel disease N Engl J Med 361 2009 2066 2078
3. R. Hansen, J.M. Thomson, and E.M. El-Omar The role of infection in the aetiology of inflammatory bowel disease J Gastroenterol 45 2010 266 276
4. P.L. Lakatos Environmental factors affecting inflammatory bowel disease: have we made progress? Dig Dis 27 2009 215 225
5. R.H. Duerr, K.D. Taylor, and S.R. Brant A genome-wide association study identifies IL23R as an inflammatory bowel disease gene Science 314 2006 1461 1463 (Pubitemid 44871953)
6. Wellcome Trust Case Control Consortium Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls Nature 447 2007 661 678
7. J. Van Limbergen, D.C. Wilson, and J. Satsangi The genetics of Crohn's disease Annu Rev Genomics Hum Genet 10 2009 89 116
8. J.C. Barrett, S. Hansoul, and D.L. Nicolae Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease Nat Genet 40 2008 955 962
9. D.P. McGovern, A. Gardet, and L. Torkvist Genome-wide association identifies multiple ulcerative colitis susceptibility loci Nat Genet 42 2010 332 337
10. A. Franke, T. Balschun, and C. Sina Genome-wide association study for ulcerative colitis identifies risk loci at 7q22 and 22q13 (IL17REL) Nat Genet 42 2010 292 294
11. A. Kaser, A.H. Lee, and A. Franke XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease Cell 134 2008 743 756
12. I. Surolia, S.P. Pirnie, and V. Chellappa Functionally defective germline variants of sialic acid acetylesterase in autoimmunity Nature 466 2010 243 247
13. E.O. Glocker, D. Kotlarz, and K. Boztug Inflammatory bowel disease and mutations affecting the interleukin-10 receptor N Engl J Med 361 2009 2033 2045
14. E.O. Glocker, N. Frede, and M. Perro Infant colitisit's in the genes Lancet 376 2010 1272
15. A. Franke, D.P. McGovern, and J.C. Barrett Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci Nat Genet 42 2010 1118 1125
16. J. Hampe, A. Franke, and P. Rosenstiel A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1 Nat Genet 39 2007 207 211 (Pubitemid 46184351)
17. J.D. Rioux, R.J. Xavier, and K.D. Taylor Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis Nat Genet 39 2007 596 604 (Pubitemid 46676115)
18. M. Parkes, J.C. Barrett, and N.J. Prescott Sequence variants in the autophagy gene IRGM and multiple other replicating loci contribute to Crohn's disease susceptibility Nat Genet 39 2007 830 832 (Pubitemid 47014496)
19. S.A. McCarroll, A. Huett, and P. Kuballa Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn's disease Nat Genet 40 2008 1107 1112
20. C. He, and D.J. Klionsky Regulation mechanisms and signaling pathways of autophagy Annu Rev Genet 43 2009 67 93
21. B. Levine, and G. Kroemer Autophagy in the pathogenesis of disease Cell 132 2008 27 42
22. T. Kanki, and D.J. Klionsky The molecular mechanism of mitochondria autophagy in yeast Mol Microbiol 75 2010 795 800
23. W. Li, Q. Yang, and Z. Mao Chaperone-mediated autophagy: machinery, regulation and biological consequences Cell Mol Life Sci 68 2011 749 763
24. D.C. Rubinsztein, J.E. Gestwicki, and L.O. Murphy Potential therapeutic applications of autophagy Nat Rev Drug Discov 6 2007 304 312 (Pubitemid 46505881)
25. D.C. Massey, F. Bredin, and M. Parkes Use of sirolimus (rapamycin) to treat refractory Crohn's disease Gut 57 2008 1294 1296
26. W. Reinisch, J. Panes, and M. Lemann A multicenter, randomized, double-blind trial of everolimus versus azathioprine and placebo to maintain steroid-induced remission in patients with moderate-to-severe active Crohn's disease Am J Gastroenterol 103 2008 2284 2292
27. N. Mizushima, A. Kuma, and Y. Kobayashi Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate J Cell Sci 116 2003 1679 1688 (Pubitemid 36582155)
28. N. Fujita, T. Itoh, and H. Omori The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy Mol Biol Cell 19 2008 2092 2100
29. D.J. Klionsky, H. Abeliovich, and P. Agostinis Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes Autophagy 4 2008 151 175 (Pubitemid 351231180)
30. F. Martinon, A. Mayor, and J. Tschopp The inflammasomes: guardians of the body Annu Rev Immunol 27 2009 229 265
31. T. Saitoh, N. Fujita, and M.H. Jang Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production Nature 456 2008 264 268
32. Y. Chung, S.H. Chang, and G.J. Martinez Critical regulation of early Th17 cell differentiation by interleukin-1 signaling Immunity 30 2009 576 587
33. M. Veldhoen, R.J. Hocking, and C.J. Atkins TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells Immunity 24 2006 179 189 (Pubitemid 43214587)
34. A.C. Villani, M. Lemire, and G. Fortin Common variants in the NLRP3 region contribute to Crohn's disease susceptibility Nat Genet 41 2009 71 76
35. M. Imielinski, R.N. Baldassano, and A. Griffiths Common variants at five new loci associated with early-onset inflammatory bowel disease Nat Genet 41 2009 1335 1340
36. A. Zhernakova, E.M. Festen, and L. Franke Genetic analysis of innate immunity in Crohn's disease and ulcerative colitis identifies two susceptibility loci harboring CARD9 and IL18RAP Am J Hum Genet 82 2008 1202 1210
37. T. Sato, J.H. van Es, and H.J. Snippert Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts Nature 469 7330 2011 415 418
38. K. Cadwell, J.Y. Liu, and S.L. Brown A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells Nature 456 2008 259 263
39. K. Cadwell, K.K. Patel, and N.S. Maloney Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine Cell 141 2010 1135 1145
40. K.S. Kobayashi, M. Chamaillard, and Y. Ogura Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract Science 307 2005 731 734 (Pubitemid 40194644)
41. S.M. Mumphrey, H. Changotra, and T.N. Moore Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses J Virol 81 2007 3251 3263 (Pubitemid 46456634)
42. A. Biswas, Y.J. Liu, and L. Hao Induction and rescue of Nod2-dependent Th1-driven granulomatous inflammation of the ileum Proc Natl Acad Sci U S A 107 2010 14739 14744
43. R. Cooney, J. Baker, and O. Brain NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation Nat Med 16 2010 90 97
44. L.H. Travassos, L.A. Carneiro, and M. Ramjeet Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry Nat Immunol 11 2010 55 62
45. D.J. Klionsky Crohn's disease, autophagy, and the Paneth cell N Engl J Med 360 2009 1785 1786
46. T.D. Kanneganti, M. Lamkanfi, and G. Nunez Intracellular NOD-like receptors in host defense and disease Immunity 27 2007 549 559 (Pubitemid 47615512)
47. A. Sabbah, T.H. Chang, and R. Harnack Activation of innate immune antiviral responses by Nod2 Nat Immunol 10 2009 1073 1080
48. J.P. Ting, J.A. Duncan, and Y. Lei How the noninflammasome NLRs function in the innate immune system Science 327 2010 286 290
49. W. Strober, A. Kitani, and I. Fuss The molecular basis of NOD2 susceptibility mutations in Crohn's disease Mucosal Immunol 1 Suppl 1 2008 S5 S9
50. T. Watanabe, A. Kitani, and P.J. Murray NOD2 is a negative regulator of Toll-like receptor 2-mediated T helper type 1 responses Nat Immunol 5 2004 800 808 (Pubitemid 39172973)
51. T. Watanabe, A. Kitani, and P.J. Murray Nucleotide binding oligomerization domain 2 deficiency leads to dysregulated TLR2 signaling and induction of antigen-specific colitis Immunity 25 2006 473 485 (Pubitemid 44355006)
52. M. Hedl, J. Li, and J.H. Cho Chronic stimulation of Nod2 mediates tolerance to bacterial products Proc Natl Acad Sci U S A 104 2007 19440 19445
53. E. Noguchi, Y. Homma, and X. Kang A Crohn's disease-associated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1 Nat Immunol 10 2009 471 479
54. M.H. Shaw, T. Reimer, and C. Sanchez-Valdepenas T cell-intrinsic role of Nod2 in promoting type 1 immunity to Toxoplasma gondii Nat Immunol 10 2009 1267 1274
55. J. Wehkamp, N.H. Salzman, and E. Porter Reduced Paneth cell alpha-defensins in ileal Crohn's disease Proc Natl Acad Sci U S A 102 2005 18129 18134 (Pubitemid 41798513)
56. C.R. Homer, A.L. Richmond, and N.A. Rebert ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn's disease pathogenesis Gastroenterology 139 2010 1630 1641 1641 e1-2
57. S. Vaishnava, C.L. Behrendt, and A.S. Ismail Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface Proc Natl Acad Sci U S A 105 2008 20858 20863
58. M.E. Selsted, and A.J. Ouellette Mammalian defensins in the antimicrobial immune response Nat Immunol 6 2005 551 557 (Pubitemid 41710724)
59. N.H. Salzman, K. Hung, and D. Haribhai Enteric defensins are essential regulators of intestinal microbial ecology Nat Immunol 11 2010 76 83
60. L.G. van der Flier, and H. Clevers Stem cells, self-renewal, and differentiation in the intestinal epithelium Annu Rev Physiol 71 2009 241 260
61. N.N. Iwakoshi, A.H. Lee, and P. Vallabhajosyula Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1 Nat Immunol 4 2003 321 329 (Pubitemid 36432313)
62. N.N. Iwakoshi, M. Pypaert, and L.H. Glimcher The transcription factor XBP-1 is essential for the development and survival of dendritic cells J Exp Med 204 2007 2267 2275 (Pubitemid 47529314)
63. A.M. Reimold, N.N. Iwakoshi, and J. Manis Plasma cell differentiation requires the transcription factor XBP-1 Nature 412 2001 300 307 (Pubitemid 32691837)
64. D. Kamimura, and M.J. Bevan Endoplasmic reticulum stress regulator XBP-1 contributes to effector CD8+ T cell differentiation during acute infection J Immunol 181 2008 5433 5441
65. R. Brunsing, S.A. Omori, and F. Weber B- and T-cell development both involve activity of the unfolded protein response pathway J Biol Chem 283 2008 17954 17961
66. F. Martinon, X. Chen, and A.H. Lee TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages Nat Immunol 11 2010 411 418
67. K.L. Lipson, S.G. Fonseca, and S. Ishigaki Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1 Cell Metab 4 2006 245 254 (Pubitemid 44283955)
68. A.M. Reimold, A. Etkin, and I. Clauss An essential role in liver development for transcription factor XBP-1 Genes Dev 14 2000 152 157 (Pubitemid 30070980)
69. A.H. Lee, G.C. Chu, and N.N. Iwakoshi XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands EMBO J 24 2005 4368 4380 (Pubitemid 41828911)
70. A.H. Lee, E.F. Scapa, and D.E. Cohen Regulation of hepatic lipogenesis by the transcription factor XBP1 Science 320 2008 1492 1496 (Pubitemid 351929428)
71. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 2007 519 529 (Pubitemid 46985379)
72. S. Vermeire, P. Rutgeerts, and K. Van Steen Genome wide scan in a Flemish inflammatory bowel disease population: support for the IBD4 locus, population heterogeneity, and epistasis Gut 53 2004 980 986 (Pubitemid 38824156)
73. M.M. Barmada, S.R. Brant, and D.L. Nicolae A genome scan in 260 inflammatory bowel disease-affected relative pairs Inflamm Bowel Dis 10 2004 513 520 (Pubitemid 39276457)
74. J. Hampe, S. Schreiber, and S.H. Shaw A genomewide analysis provides evidence for novel linkages in inflammatory bowel disease in a large European cohort Am J Hum Genet 64 1999 808 816 (Pubitemid 30460424)
75. A. Bertolotti, X. Wang, and I. Novoa Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice J Clin Invest 107 2001 585 593 (Pubitemid 32205179)
76. K. Brandl, S. Rutschmann, and X. Li Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response Proc Natl Acad Sci U S A 106 2009 3300 3305
77. A. Kaser, and R.S. Blumberg Endoplasmic reticulum stress and intestinal inflammation Mucosal Immunol 3 2010 11 16
78. M.F. Moffatt, M. Kabesch, and L. Liang Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma Nature 448 2007 470 473 (Pubitemid 47123521)
79. M.F. Moffatt, I.G. Gut, and F. Demenais A large-scale, consortium-based genomewide association study of asthma N Engl J Med 363 2010 1211 1221
80. X. Liu, P. Invernizzi, and Y. Lu Genome-wide meta-analyses identify three loci associated with primary biliary cirrhosis Nat Genet 42 2010 658 660
81. J.C. Barrett, D.G. Clayton, and P. Concannon Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes Nat Genet 41 2009 703 707
82. J.A. Todd Etiology of type 1 diabetes Immunity 32 2010 457 467
83. L. Hjelmqvist, M. Tuson, and G. Marfany ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins Genome Biol 3 2002 RESEARCH0027
84. G. Cantero-Recasens, C. Fandos, and F. Rubio-Moscardo The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress Hum Mol Genet 19 2010 111 121
85. F. Zhao, R. Edwards, and D. Dizon Disruption of Paneth and goblet cell homeostasis and increased endoplasmic reticulum stress in Agr2-/- mice Dev Biol 338 2010 270 279
86. C.K. Heazlewood, M.C. Cook, and R. Eri Aberrant mucin assembly in mice causes endoplasmic reticulum stress and spontaneous inflammation resembling ulcerative colitis PLoS Med 5 2008 e54
87. R.E. Hammer, S.D. Maika, and J.A. Richardson Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders Cell 63 1990 1099 1112 (Pubitemid 120034950)
88. M.J. Turner, D.P. Sowders, and M.L. DeLay HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response J Immunol 175 2005 2438 2448 (Pubitemid 41113854)
89. J.D. Taurog, J.A. Richardson, and J.T. Croft The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats J Exp Med 180 1994 2359 2364 (Pubitemid 24351619)
90. T.M. Tran, N. Satumtira, and M.L. Dorris HLA-B27 in transgenic rats forms disulfide-linked heavy chain oligomers and multimers that bind to the chaperone BiP J Immunol 172 2004 5110 5119 (Pubitemid 38456440)
91. J. Grootjans, C.M. Hodin, and J.J. de Haan Level of activation of the unfolded protein response correlates with Paneth cell apoptosis in human small intestine exposed to ischemia-reperfusion Gastroenterology 140 2011 529 539.e3
92. J.R. Jheng, K.S. Lau, and W.F. Tang Endoplasmic reticulum stress is induced and modulated by enterovirus 71 Cell Microbiol 12 2010 796 813
93. Y. Futamura, E. Tashiro, and N. Hironiwa Trierixin, a novel Inhibitor of ER stress-induced XBP1 activation from Streptomyces sp II. structure elucidation J Antibiot (Tokyo) 60 2007 582 585
94. A.W. Paton, T. Beddoe, and C.M. Thorpe AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP Nature 443 2006 548 552 (Pubitemid 44527286)
95. N. Rolhion, N. Barnich, and M.A. Bringer Abnormally expressed ER stress response chaperone Gp96 in CD favours adherent-invasive Escherichia coli invasion Gut 59 2010 1355 1362
96. A. Darfeuille-Michaud, C. Neut, and N. Barnich Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease Gastroenterology 115 1998 1405 1413 (Pubitemid 28545991)
97. H.M. Martin, B.J. Campbell, and C.A. Hart Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer Gastroenterology 127 2004 80 93 (Pubitemid 38962277)
98. A. Darfeuille-Michaud, J. Boudeau, and P. Bulois High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease Gastroenterology 127 2004 412 421 (Pubitemid 39091889)
99. A. Shkoda, P.A. Ruiz, and H. Daniel Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation Gastroenterology 132 2007 190 207 (Pubitemid 46108743)
100. F. Urano, X. Wang, and A. Bertolotti Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666 (Pubitemid 30070916)
101. M. Ogata, S. Hino, and A. Saito Autophagy is activated for cell survival after endoplasmic reticulum stress Mol Cell Biol 26 2006 9220 9231 (Pubitemid 44904418)
102. W.X. Ding, H.M. Ni, and W. Gao Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability Am J Pathol 171 2007 513 524 (Pubitemid 47344684)
103. K.M. Rouschop, T. van den Beucken, and L. Dubois The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5 J Clin Invest 120 2010 127 141
104. P. Pasinelli, and R.H. Brown Molecular biology of amyotrophic lateral sclerosis: insights from genetics Nat Rev Neurosci 7 2006 710 723 (Pubitemid 44267495)
105. J.D. Atkin, M.A. Farg, and B.J. Turner Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1 J Biol Chem 281 2006 30152 30165 (Pubitemid 44537023)
106. C. Hetz, P. Thielen, and S. Matus XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy Genes Dev 23 2009 2294 2306
107. D. Bansal, and K.P. Campbell Dysferlin and the plasma membrane repair in muscular dystrophy Trends Cell Biol 14 2004 206 213 (Pubitemid 38447120)
108. E. Fujita, Y. Kouroku, and A. Isoai Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II) Hum Mol Genet 16 2007 618 629 (Pubitemid 46591117)
109. L. Yang, P. Li, and S. Fu Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance Cell Metab 11 2010 467 478
110. U. Ozcan, Q. Cao, and E. Yilmaz Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes Science 306 2004 457 461 (Pubitemid 39372439)
111. C.E. Richardson, T. Kooistra, and D.H. Kim An essential role for XBP-1 in host protection against immune activation in C. elegans Nature 463 2010 1092 1095
112. A. Kaser, and R.S. Blumberg Survive an innate immune response through XBP1 Cell Res 20 2010 506 507
113. S. Maeda, L.C. Hsu, and H. Liu Nod2 mutation in Crohn's disease potentiates NF-kappaB activity and IL-1beta processing Science 307 2005 734 738 (Pubitemid 40194645)
114. C. Zaph, A.E. Troy, and B.C. Taylor Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis Nature 446 2007 552 556 (Pubitemid 46514719)
115. A. Nenci, C. Becker, and A. Wullaert Epithelial NEMO links innate immunity to chronic intestinal inflammation Nature 446 2007 557 561 (Pubitemid 46514732)
116. O. Gutierrez, C. Pipaon, and N. Inohara Induction of Nod2 in myelomonocytic and intestinal epithelial cells via nuclear factor-kappa B activation J Biol Chem 277 2002 41701 41705 (Pubitemid 35257477)
117. T. Hisamatsu, M. Suzuki, and H.C. Reinecker CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells Gastroenterology 124 2003 993 1000 (Pubitemid 36389802)