The inflammatory bowel disease-associated autophagy gene Atg16L1T300A acts as a dominant negative variant in mice

Journal of Immunology

Volumn 198, Issue 6, 2017, Pages 2457-2467

  Gao, Ping ^a   Liu, Hongtao ^a,b   Huang, Huarong ^a,b   Zhang, Qi ^a   Strober, Warren ^c   Zhang, Fuping ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; INTERLEUKIN 1BETA; THREONINE; TUMOR NECROSIS FACTOR; ATG16L1 PROTEIN, HUMAN; AUTOPHAGY RELATED PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATG16L1 GENE; BACTERIAL CLEARANCE; COLITIS; CONTROLLED STUDY; CROHN DISEASE; FEMALE; GENE FUNCTION; GENETIC POLYMORPHISM; GENETIC VARIATION; HETEROZYGOTE; HOMOZYGOTE; INFLAMMATORY BOWEL DISEASE; MACROPHAGE; MOUSE; NONHUMAN; REGULATOR GENE; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; ANIMAL; APOPTOSIS; AUTOPHAGY; BACTERIOLYSIS; C57BL MOUSE; GENE TARGETING; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; SALMONELLA;

ANIMALS; APOPTOSIS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; BACTERIOLYSIS; COLITIS; CROHN DISEASE; GENE KNOCK-IN TECHNIQUES; HETEROZYGOTE; HOMOZYGOTE; HUMANS; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED C57BL; MUTATION; POLYMORPHISM, GENETIC; SALMONELLA; SALMONELLA INFECTIONS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85014592975     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502652     Document Type: Article

References (37)

1. He, C., and D. J. Klionsky. 2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43: 67-93.
2. Lotze, M. T., H. J. Zeh, A. Rubartelli, L. J. Sparvero, A. A. Amoscato, N. R. Washburn, M. E. Devera, X. Liang, M. Tör, and T. Billiar. 2007. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol. Rev. 220: 60-81.
3. Kroemer, G., G. Marinõ, and B. Levine. 2010. Autophagy and the integrated stress response. Mol. Cell 40: 280-293.
4. Levine, B., and G. Kroemer. 2008. Autophagy in the pathogenesis of disease. Cell 132: 27-42.
5. Virgin, H. W., and B. Levine. 2009. Autophagy genes in immunity. Nat. Immunol. 10: 461-470.
6. Gannagé, M., D. Dormann, R. Albrecht, J. Dengjel, T. Torossi, P. C. Rämer, M. Lee, T. Strowig, F. Arrey, G. Conenello, et al. 2009. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 6: 367-380.
7. Sumpter, R., Jr., and B. Levine. 2011. Selective autophagy and viruses. Autophagy 7: 260-265.
8. Hampe, J., A. Franke, P. Rosenstiel, A. Till, M. Teuber, K. Huse, M. Albrecht, G. Mayr, F. M. De La Vega, J. Briggs, et al. 2007. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39: 207-211.
9. Rioux, J. D., R. J. Xavier, K. D. Taylor, M. S. Silverberg, P. Goyette, A. Huett, T. Green, P. Kuballa, M. M. Barmada, L. W. Datta, et al. 2007. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 39: 596-604.
10. Mizushima, N., A. Kuma, Y. Kobayashi, A. Yamamoto, M. Matsubae, T. Takao, T. Natsume, Y. Ohsumi, and T. Yoshimori. 2003. Mouse Apg16L, a novel WDrepeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J. Cell Sci. 116: 1679-1688.
11. Saitoh, T., N. Fujita, M. H. Jang, S. Uematsu, B. G. Yang, T. Satoh, H. Omori, T. Noda, N. Yamamoto, M. Komatsu, et al. 2008. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456: 264-268.
12. Plantinga, T. S., T. O. Crisan, M. Oosting, F. L. van de Veerdonk, D. J. de Jong, D. J. Philpott, J. W. van der Meer, S. E. Girardin, L. A. Joosten, and M. G. Netea. 2011. Crohn's disease-associated ATG16L1 polymorphism modulates proinflammatory cytokine responses selectively upon activation of NOD2. Gut 60: 1229-1235.
13. Plantinga, T. S., L. A. Joosten, and M. G. Netea. 2011. ATG16L1 polymorphisms are associated with NOD2-induced hyperinflammation. Autophagy 7: 1074-1075.
14. Cadwell, K., J. Y. Liu, S. L. Brown, H. Miyoshi, J. Loh, J. K. Lennerz, C. Kishi, W. Kc, J. A. Carrero, S. Hunt, et al. 2008. A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456: 259-263.
15. Murthy, A., Y. Li, I. Peng, M. Reichelt, A. K. Katakam, R. Noubade, M. Roose-Girma, J. DeVoss, L. Diehl, R. R. Graham, and M. van Lookeren Campagne. 2014. A Crohn's disease variant in Atg16l1 enhances its degradation by caspase 3. Nature 506: 456-462.
16. Sutterwala, F. S., Y. Ogura, M. Szczepanik, M. Lara-Tejero, G. S. Lichtenberger, E. P. Grant, J. Bertin, A. J. Coyle, J. E. Galán, P. W. Askenase, and R. A. Flavell. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
17. Nakahira, K., J. A. Haspel, V. A. Rathinam, S. J. Lee, T. Dolinay, H. C. Lam, J. A. Englert, M. Rabinovitch, M. Cernadas, H. P. Kim, et al. 2011. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12: 222-230.
18. Zhang, F., G. Meng, and W. Strober. 2008. Interactions among the transcription factors Runx1, RORgammat and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nat. Immunol. 9: 1297-1306.
19. Kum, W. W., S. Lee, G. A. Grassl, R. Bidshahri, K. Hsu, H. J. Ziltener, and B. B. Finlay. 2009. Lack of functional P-selectin ligand exacerbates Salmonella serovar typhimurium infection. J. Immunol. 182: 6550-6561.
20. Thiennimitr, P., S. E. Winter, M. G. Winter, M. N. Xavier, V. Tolstikov, D. L. Huseby, T. Sterzenbach, R. M. Tsolis, J. R. Roth, and A. J. Baümler. 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl. Acad. Sci. USA 108: 17480-17485.
21. Gutierrez, M. G., S. S. Master, S. B. Singh, G. A. Taylor, M. I. Colombo, and V. Deretic. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
22. Gao, P., C. Bauvy, S. Souquère, G. Tonelli, L. Liu, Y. Zhu, Z. Qiao, D. Bakula, T. Proikas-Cezanne, G. Pierron, et al. 2010. The Bcl-2 homology domain 3 mimetic gossypol induces both Beclin 1-dependent and Beclin 1-independent cytoprotective autophagy in cancer cells. J. Biol. Chem. 285: 25570-25581.
23. Levine, B., and V. Deretic. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7: 767-777.
24. Conway, K. L., P. Kuballa, J. H. Song, K. K. Patel, A. B. Castoreno, O. H. Yilmaz, H. B. Jijon, M. Zhang, L. N. Aldrich, E. J. Villablanca, et al. 2013. Atg16l1 is required for autophagy in intestinal epithelial cells and protection of mice from Salmonella infection. Gastroenterology 145: 1347-1357.
25. Lassen, K. G., P. Kuballa, K. L. Conway, K. K. Patel, C. E. Becker, J. M. Peloquin, E. J. Villablanca, J. M. Norman, T. C. Liu, R. J. Heath, et al. 2014. Atg16L1 T300A variant decreases selective autophagy resulting in altered cytokine signaling and decreased antibacterial defense. Proc. Natl. Acad. Sci. USA 111: 7741-7746.
26. McStay, G. P., G. S. Salvesen, and D. R. Green. 2008. Overlapping cleavage motif selectivity of caspases: implications for analysis of apoptotic pathways. Cell Death Differ. 15: 322-331.
27. Jost, P. J., S. Grabow, D. Gray, M. D. McKenzie, U. Nachbur, D. C. Huang, P. Bouillet, H. E. Thomas, C. Borner, J. Silke, et al. 2009. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature 460: 1035-1039.
28. Barthel, M., S. Hapfelmeier, L. Quintanilla-Martínez, M. Kremer, M. Rohde, M. Hogardt, K. Pfeffer, H. Russmann, and W. D. Hardt. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71: 2839-2858.
29. Prescott, N. J., S. A. Fisher, A. Franke, J. Hampe, C. M. Onnie, D. Soars, R. Bagnall, M. M. Mirza, J. Sanderson, A. Forbes, et al. 2007. A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn's disease and is independent of CARD15 and IBD5. Gastroenterology 132: 1665-1671.
30. Strisciuglio, C., E. Miele, M. E. Wildenberg, F. P. Giugliano, M. Andreozzi, A. Vitale, F. Capasso, A. Camarca, M. V. Barone, A. Staiano, et al. 2013. T300A variant of autophagy ATG16L1 gene is associated with decreased antigen sampling and processing by dendritic cells in pediatric Crohn's disease. Inflamm. Bowel Dis. 19: 2339-2348.
31. Choi, A. J., and S. W. Ryter. 2014. Inflammasomes: molecular regulation and implications for metabolic and cognitive diseases. Mol. Cells 37: 441-448.
32. Harijith, A., D. L. Ebenezer, and V. Natarajan. 2014. Reactive oxygen species at the crossroads of inflammasome and inflammation. Front. Physiol. 5: 352.
33. Lee, W. W., S. W. Kang, J. Choi, S. H. Lee, K. Shah, E. E. Eynon, R. A. Flavell, and I. Kang. 2010. Regulating human Th17 cells via differential expression of IL-1 receptor. Blood 115: 530-540.
34. Travassos, L. H., L. A. Carneiro, M. Ramjeet, S. Hussey, Y. G. Kim, J. G. Magalhaẽs, L. Yuan, F. Soares, E. Chea, L. Le Bourhis, et al. 2010. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 11: 55-62.
35. Chu, B., X. Zhou, K. Ren, B. Neese, M. Lin, Q. Wang, F. Bauer, and Q. M. Zhang. 2006. A dielectric polymer with high electric energy density and fast discharge speed. Science 313: 334-336.
36. Adolph, T. E., M. F. Tomczak, L. Niederreiter, H. J. Ko, J. Böck, E. Martinez-Naves, J. N. Glickman, M. Tschurtschenthaler, J. Hartwig, S. Hosomi, et al. 2013. Paneth cells as a site of origin for intestinal inflammation. Nature 503: 272-276.
37. Nguyen, H. T., G. Dalmasso, S. Muller, J. Carrière, F. Seibold, and A. Darfeuille-Michaud. 2014. Crohn's disease-associated adherent invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology 146: 508-519.