IRGM governs the core autophagy machinery to conduct antimicrobial defense

Molecular Cell

Volumn 58, Issue 3, 2015, Pages 507-521

  Chauhan, Santosh ^a   Mandell, Michael A ^a   Deretic, Vojo ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ATG14L PROTEIN; ATG16L1 PROTEIN; BECLIN 1; CASPASE RECRUITMENT DOMAIN PROTEIN 15; GAMMA INTERFERON; INTERLEUKIN 1BETA; IRGM PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN; PROTEIN BCL 2; ULK1 PROTEIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; APOPTOSIS REGULATORY PROTEIN; ATG16L1 PROTEIN, HUMAN; BECN1 PROTEIN, HUMAN; CARRIER PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; IRGM PROTEIN, HUMAN; MEMBRANE PROTEIN; NOD2 PROTEIN, HUMAN; PATTERN RECOGNITION RECEPTOR; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; ULK1 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BACTERIAL CLEARANCE; BACTERIAL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ESCHERICHIA COLI INFECTION; GENE SILENCING; INNATE IMMUNITY; MITOCHONDRION; NEGATIVE FEEDBACK; NONHUMAN; OLIGOMERIZATION; PATHOGEN CLEARANCE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; UBIQUITINATION; CONFOCAL MICROSCOPY; CROHN DISEASE; GENE EXPRESSION; GENETICS; HCT116 CELL LINE; HEK293 CELL LINE; HELA CELL LINE; HT 29 CELL LINE; HUMAN; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE; U937 CELL LINE; WESTERN BLOTTING;

ANTI-INFECTIVE AGENTS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE, TUMOR; CROHN DISEASE; GENE EXPRESSION; GTP-BINDING PROTEINS; HCT116 CELLS; HEK293 CELLS; HELA CELLS; HT29 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; NOD2 SIGNALING ADAPTOR PROTEIN; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, PATTERN RECOGNITION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; U937 CELLS; UBIQUITINATION;

EID: 84928926952     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.03.020     Document Type: Article

References (47)

1. Abbott D.W., Yang Y., Hutti J.E., Madhavarapu S., Kelliher M.A., Cantley L.C. Coordinated regulation of Toll-like receptor and NOD2 signaling by K63-linked polyubiquitin chains. Mol. Cell. Biol. 2007, 27:6012-6025.
2. Bekpen C., Marques-Bonet T., Alkan C., Antonacci F., Leogrande M.B., Ventura M., Kidd J.M., Siswara P., Howard J.C., Eichler E.E. Death and resurrection of the human IRGM gene. PLoS Genet. 2009, 5:e1000403.
3. Brest P., Lapaquette P., Souidi M., Lebrigand K., Cesaro A., Vouret-Craviari V., Mari B., Barbry P., Mosnier J.F., Hébuterne X., et al. Asynonymous variant in IRGM alters a binding site for miR-196 and causesderegulation of IRGM-dependent xenophagy in Crohn's disease. Nat. Genet. 2011, 43:242-245.
4. Chan W.M., Mak M.C., Fung T.K., Lau A., Siu W.Y., Poon R.Y. Ubiquitination of p53 at multiple sites in the DNA-binding domain. Mol. Cancer Res. 2006, 4:15-25.
5. Choi J., Park S., Biering S.B., Selleck E., Liu C.Y., Zhang X., Fujita N., Saitoh T., Akira S., Yoshimori T., et al. The parasitophorous vacuole membrane of Toxoplasma gondii is targeted for disruption by ubiquitin-like conjugation systems of autophagy. Immunity 2014, 40:924-935.
6. Cooney R., Baker J., Brain O., Danis B., Pichulik T., Allan P., Ferguson D.J., Campbell B.J., Jewell D., Simmons A. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat. Med. 2010, 16:90-97.
7. Craddock N., Hurles M.E., Cardin N., Pearson R.D., Plagnol V., Robson S., Vukcevic D., Barnes C., Conrad D.F., Giannoulatou E., et al. Genome-wide association study of CNVs in 16,000 cases of eight common diseases and 3,000 shared controls. Nature 2010, 464:713-720. Wellcome Trust Case Control Consortium.
8. Criollo A., Niso-Santano M., Malik S.A., Michaud M., Morselli E., Mariño G., Lachkar S., Arkhipenko A.V., Harper F., Pierron G., et al. Inhibition of autophagy by TAB2 and TAB3. EMBO J. 2011, 30:4908-4920.
9. Deretic V., Kimura T., Timmins G., Moseley P., Chauhan S., Mandell M. Immunologic manifestations of autophagy. J.Clin. Invest. 2015, 125:75-84.
10. Dooley H.C., Razi M., Polson H.E., Girardin S.E., Wilson M.I., Tooze S.A. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol. Cell 2014, 55:238-252.
11. Egan D.F., Shackelford D.B., Mihaylova M.M., Gelino S., Kohnz R.A., Mair W., Vasquez D.S., Joshi A., Gwinn D.M., Taylor R., et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011, 331:456-461.
12. Fimia G.M., Stoykova A., Romagnoli A., Giunta L., Di Bartolomeo S., Nardacci R., Corazzari M., Fuoco C., Ucar A., Schwartz P., et al. Ambra1 regulates autophagy and development of the nervous system. Nature 2007, 447:1121-1125.
13. Fung T.K., Yam C.H., Poon R.Y. The N-terminal regulatory domain of cyclin A contains redundant ubiquitination targeting sequences and acceptor sites. Cell Cycle 2005, 4:1411-1420.
14. Gammoh N., Florey O., Overholtzer M., Jiang X. Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and -independent autophagy. Nat. Struct. Mol. Biol. 2013, 20:144-149.
15. Grégoire I.P., Richetta C., Meyniel-Schicklin L., Borel S., Pradezynski F., Diaz O., Deloire A., Azocar O., Baguet J., Le Breton M., et al. IRGM is a common target of RNA viruses that subvert the autophagy network. PLoS Pathog. 2011, 7:e1002422.
16. Gutierrez M.G., Master S.S., Singh S.B., Taylor G.A., Colombo M.I., Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004, 119:753-766.
17. Hasegawa M., Fujimoto Y., Lucas P.C., Nakano H., Fukase K., Núñez G., Inohara N. A critical role of RICK/RIP2 polyubiquitination in Nod-induced NF-kappaB activation. EMBO J. 2008, 27:373-383.
18. Høyer-Hansen M., Bastholm L., Szyniarowski P., Campanella M., Szabadkai G., Farkas T., Bianchi K., Fehrenbacher N., Elling F., Rizzuto R., et al. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 2007, 25:193-205.
19. Hugot J.P., Chamaillard M., Zouali H., Lesage S., Cézard J.P., Belaiche J., Almer S., Tysk C., O'Morain C.A., Gassull M., et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411:599-603.
20. Intemann C.D., Thye T., Niemann S., Browne E.N., Amanua Chinbuah M., Enimil A., Gyapong J., Osei I., Owusu-Dabo E., Helm S., et al. Autophagy gene variant IRGM -261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog. 2009, 5:e1000577.
21. Itakura E., Kishi C., Inoue K., Mizushima N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 2008, 19:5360-5372.
22. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
23. Kim J., Kim Y.C., Fang C., Russell R.C., Kim J.H., Fan W., Liu R., Zhong Q., Guan K.L. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 2013, 152:290-303.
24. Lapaquette P., Glasser A.L., Huett A., Xavier R.J., Darfeuille-Michaud A. Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly. Cell. Microbiol. 2010, 12:99-113.
25. Levine B., Mizushima N., Virgin H.W. Autophagy in immunity and inflammation. Nature 2011, 469:323-335.
26. Matsunaga K., Saitoh T., Tabata K., Omori H., Satoh T., Kurotori N., Maejima I., Shirahama-Noda K., Ichimura T., Isobe T., et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat. Cell Biol. 2009, 11:385-396.
27. McCarroll S.A., Huett A., Kuballa P., Chilewski S.D., Landry A., Goyette P., Zody M.C., Hall J.L., Brant S.R., Cho J.H., et al. Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn's disease. Nat. Genet. 2008, 40:1107-1112.
28. Mihaylova M.M., Shaw R.J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 2011, 13:1016-1023.
29. Mizushima N., Kuma A., Kobayashi Y., Yamamoto A., Matsubae M., Takao T., Natsume T., Ohsumi Y., Yoshimori T. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J.Cell Sci. 2003, 116:1679-1688.
30. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
31. Nazio F., Strappazzon F., Antonioli M., Bielli P., Cianfanelli V., Bordi M., Gretzmeier C., Dengjel J., Piacentini M., Fimia G.M., Cecconi F. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat. Cell Biol. 2013, 15:406-416.
32. Ogura Y., Bonen D.K., Inohara N., Nicolae D.L., Chen F.F., Ramos R., Britton H., Moran T., Karaliuskas R., Duerr R.H., et al. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001, 411:603-606.
33. Romanello V., Guadagnin E., Gomes L., Roder I., Sandri C., Petersen Y., Milan G., Masiero E., Del Piccolo P., Foretz M., et al. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J. 2010, 29:1774-1785.
34. Sabbah A., Chang T.H., Harnack R., Frohlich V., Tominaga K., Dube P.H., Xiang Y., Bose S. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 2009, 10:1073-1080.
35. Shi C.S., Kehrl J.H. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci. Signal. 2010, 3:ra42.
36. Singh S.B., Davis A.S., Taylor G.A., Deretic V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006, 313:1438-1441.
37. Singh S.B., Ornatowski W., Vergne I., Naylor J., Delgado M., Roberts E., Ponpuak M., Master S., Pilli M., White E., et al. Human IRGM regulates autophagy and cell-autonomous immunity functions through mitochondria. Nat. Cell Biol. 2010, 12:1154-1165.
38. Song J.H., Kim S.Y., Chung K.S., Moon C.M., Kim S.W., Kim E.Y., Jung J.Y., Park M.S., Kim Y.S., Kim S.K., et al. Association between genetic variants in the IRGM gene and tuberculosis in a Korean population. Infection 2014, 42:655-660.
39. Stolz A., Ernst A., Dikic I. Cargo recognition and trafficking inselective autophagy. Nat. Cell Biol. 2014, 16:495-501.
40. Sun Q., Fan W., Chen K., Ding X., Chen S., Zhong Q. Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 2008, 105:19211-19216.
41. Tanabe T., Chamaillard M., Ogura Y., Zhu L., Qiu S., Masumoto J., Ghosh P., Moran A., Predergast M.M., Tromp G., et al. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J. 2004, 23:1587-1597.
42. Travassos L.H., Carneiro L.A., Ramjeet M., Hussey S., Kim Y.G., Magalhães J.G., Yuan L., Soares F., Chea E., Le Bourhis L., et al. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 2010, 11:55-62.
43. Turkieh A., Caubère C., Barutaut M., Desmoulin F., Harmancey R., Galinier M., Berry M., Dambrin C., Polidori C., Casteilla L., et al. Apolipoprotein O is mitochondrial and promotes lipotoxicity in heart. J.Clin. Invest. 2014, 124:2277-2286.
44. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007, 447:661-678. Wellcome Trust Case Control Consortium.
45. Yang Y., Yin C., Pandey A., Abbott D., Sassetti C., Kelliher M.A. NOD2 pathway activation by MDP or Mycobacterium tuberculosis infection involves the stable polyubiquitination of Rip2. J.Biol. Chem. 2007, 282:36223-36229.
46. Yang D., Chen J., Zhang L., Cha Z., Han S., Shi W., Ding R., Ma L., Xiao H., Shi C., et al. Mycobacterium leprae upregulates IRGM expression in monocytes and monocyte-derived macrophages. Inflammation 2014, 37:1028-1034.
47. Zurek B., Schoultz I., Neerincx A., Napolitano L.M., Birkner K., Bennek E., Sellge G., Lerm M., Meroni G., Söderholm J.D., Kufer T.A. TRIM27 negatively regulates NOD2 by ubiquitination and proteasomal degradation. PLoS ONE 2012, 7:e41255.