Quo vadis? Interferon-inducible GTPases go to their target membranes via the LC3-conjugation system of autophagy

References

• Randow F, MacMicking JD, James LC. Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 2013; 340:701-6; PMID:23661752; https://doi.org/10.1126/science.1233028
   PubMed Web of Science ®Google Scholar
• Coers J. Self and non-self discrimination of intracellular membranes by the innate immune system. PLoS Pathog 2013; 9:e1003538; PMID:24068918
   PubMed Web of Science ®Google Scholar
• Kim B-H, Shenoy AR, Kumar P, Bradfield CJ, MacMicking JD. IFN-Inducible GTPases in Host Cell Defense. Cell Host Microbe 2012; 12:432-44; PMID:23084913; https://doi.org/10.1016/j.chom.2012.09.007
   PubMed Web of Science ®Google Scholar
• Pilla-Moffett D, Barber MF, Taylor GA, Coers J. Interferon-Inducible GTPases in Host Resistance, Inflammation and Disease. Journal of Molecular Biology 2016; PMID:27181197
   PubMed Web of Science ®Google Scholar
• Hunn JP, Feng CG, Sher A, Howard JC. The immunity-related GTPases in mammals: a fast-evolving cell-autonomous resistance system against intracellular pathogens. Mamm Genome 2010; 22:43-54; PMID:21052678; https://doi.org/10.1007/s00335-010-9293-3
   PubMed Web of Science ®Google Scholar
• Kim BH, Shenoy AR, Kumar P, Das R, Tiwari S, MacMicking JD. A family of IFN- -inducible 65-kD GTPases protects against bacterial infection. Science 2011; 332:717-21; PMID:21551061; https://doi.org/10.1126/science.1201711
   PubMed Web of Science ®Google Scholar
• Meunier E, Dick MS, Dreier RF, Schürmann N, Broz DK, Kenzelmann Broz D, Warming S, Roose-Girma M, Bumann D, Kayagaki N, et al. Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases. Nature 2014; 509:366-70; PMID:24739961; https://doi.org/10.1038/nature13157
   PubMed Web of Science ®Google Scholar
• Meunier E, Broz P. Interferon-inducible GTPases in cell autonomous and innate immunity. Cell Microbiol 2016; 18:168-180; PMID:26572694; https://doi.org/10.1111/cmi.12546
   PubMed Web of Science ®Google Scholar
• Hunn JP, Koenen-Waisman S, Papic N, Schroeder N, Pawlowski N, Lange R, Kaiser F, Zerrahn J, Martens S, Howard JC. Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO J 2008; 27:2495-509; PMID:18772884; https://doi.org/10.1038/emboj.2008.176
   PubMed Web of Science ®Google Scholar
• Haldar AK, Saka HA, Piro AS, Dunn JD, Henry SC, Taylor GA, Frickel EM, Valdivia RH, Coers J. IRG and GBP host resistance factors target aberrant, “non-self” vacuoles characterized by the missing of ‘self’ IRGM proteins. PLoS Pathog 2013; 9:e1003414; PMID:23785284; https://doi.org/10.1371/journal.ppat.1003414
   PubMed Web of Science ®Google Scholar
• MacMicking JD. Immune control of phagosomal bacteria by p47 GTPases. Curr Opin Microbiol 2005; 8:74-82; PMID:15694860; https://doi.org/10.1016/j.mib.2004.12.012
   PubMed Web of Science ®Google Scholar
• Sinai AP. Biogenesis of and activities at the Toxoplasma gondii parasitophorous vacuole membrane. Subcell Biochem 2008; 47:155-64; PMID:18512349; https://doi.org/10.1007/978-0-387-78267-6_12
   PubMedGoogle Scholar
• Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, Howard JC. Disruption of Toxoplasma gondii Parasitophorous Vacuoles by the Mouse p47-Resistance GTPases. PLoS Pathog 2005; 1:e24; PMID:16304607; https://doi.org/10.1371/journal.ppat.0010024
   PubMed Web of Science ®Google Scholar
• Ling YM, Shaw MH, Ayala C, Coppens I, Taylor GA, Ferguson DJP, Yap GS. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med 2006; 203:2063-71; PMID:16940170; https://doi.org/10.1084/jem.20061318
   PubMed Web of Science ®Google Scholar
• Zhao YO, Khaminets A, Hunn JP, Howard JC. Disruption of the toxoplasma gondii parasitophorous vacuole by IFNγ-inducible immunity-related GTPases (IRG Proteins) triggers necrotic cell death. PLoS Pathog 2009; 5:e1000288; PMID:19197351; https://doi.org/10.1371/journal.ppat.1000288
   PubMed Web of Science ®Google Scholar
• Khaminets A, Hunn JP, Könen-Waisman S, Zhao YO, Preukschat D, Coers J, Boyle JP, Ong Y-C, Boothroyd JC, Reichmann G, et al. Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole. Cell Microbiol 2010; 12:939-61; PMID:20109161; https://doi.org/10.1111/j.1462-5822.2010.01443.x
   PubMed Web of Science ®Google Scholar
• Traver MK, Henry SC, Cantillana V, Oliver T, Hunn JP, Howard JC, Beer S, Pfeffer K, Coers J, Taylor GA. Immunity-related GTPase M (IRGM) proteins influence the localization of guanylate-binding protein 2 (GBP2) by modulating macroautophagy. J Biol Chem 2011; 286:30471-80; PMID:21757726; https://doi.org/10.1074/jbc.M111.251967
   PubMed Web of Science ®Google Scholar
• Lee Y, Sasai M, Ma JS, Sakaguchi N, Ohshima J, Bando H, Saitoh T, Akira S, Yamamoto M. p62 Plays a specific role in interferon-γ-induced presentation of a toxoplasma vacuolar antigen. Cell Rep 2015; 13:223-233; PMID:26440898; https://doi.org/10.1016/j.celrep.2015.09.005
   PubMed Web of Science ®Google Scholar
• Haldar AK, Foltz C, Finethy R, Piro AS, Feeley EM, Pilla-Moffett DM, Komatsu M, Frickel E-M, Coers J. Ubiquitin systems mark pathogen-containing vacuoles as targets for host defense by guanylate binding proteins. Proc Natl Acad Sci USA 2015; 112:E5628-37; PMID:26417105; https://doi.org/10.1073/pnas.1515966112
   PubMed Web of Science ®Google Scholar
• Selleck EM, Fentress SJ, Beatty WL, Degrandi D, Pfeffer K, Virgin HW, MacMicking JD, Sibley LD. Guanylate-binding Protein 1 (Gbp1) Contributes to Cell-autonomous Immunity against Toxoplasma gondii. PLoS Pathog 2013; 9:e1003320; PMID:23633952; https://doi.org/10.1371/journal.ppat.1003320
   PubMed Web of Science ®Google Scholar
• Haldar AK, Piro AS, Pilla DM, Yamamoto M, Coers J. The E2-like conjugation enzyme Atg3 promotes binding of IRG and Gbp proteins to chlamydia- and toxoplasma-containing vacuoles and host resistance. PLoS One 2014; 9:e86684; PMID:24466199; https://doi.org/10.1371/journal.pone.0086684
   PubMed Web of Science ®Google Scholar
• Zhao Z, Fux B, Goodwin M, Dunay IR, Strong D, Miller BC, Cadwell K, Delgado MA, Ponpuak M, Green KG, et al. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe 2008; 4:458-69; PMID:18996346; https://doi.org/10.1016/j.chom.2008.10.003
   PubMed Web of Science ®Google Scholar
• Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; https://doi.org/10.1038/nature09782
   PubMed Web of Science ®Google Scholar
• Papic N, Hunn JP, Pawlowski N, Zerrahn J, Howard JC. Inactive and Active States of the Interferon-inducible Resistance GTPase, Irga6, in Vivo. J Biol Chem 2008; 283:32143-51; PMID:18784077; https://doi.org/10.1074/jbc.M804846200
   PubMed Web of Science ®Google Scholar
• Choi J, Park S, Biering SB, Selleck E, Liu CY, 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; 40:924-35; PMID:24931121; https://doi.org/10.1016/j.immuni.2014.05.006
   PubMed Web of Science ®Google Scholar
• Rubinsztein DC, Codogno P, Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012; 11:709-30; PMID:22935804; https://doi.org/10.1038/nrd3802
   PubMed Web of Science ®Google Scholar
• Rubinsztein DC, Shpilka T, Elazar Z. Mechanisms of Autophagosome Biogenesis. Current Biology 2012; 22:R29-R34; PMID:22240478; https://doi.org/10.1016/j.cub.2011.11.034
   PubMed Web of Science ®Google Scholar
• Ohshima J, Lee Y, Sasai M, Saitoh T, Su Ma J, Kamiyama N, Matsuura Y, Pann-Ghill S, Hayashi M, Ebisu S, et al. Role of mouse and human autophagy proteins in IFN-γ-induced cell-autonomous responses against Toxoplasma gondii. J Immunol 2014; 192:3328-35; PMID:24563254; https://doi.org/10.4049/jimmunol.1302822
   PubMed Web of Science ®Google Scholar
• Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 2008; 19:2092-100; PMID:18321988; https://doi.org/10.1091/mbc.E07-12-1257
   PubMed Web of Science ®Google Scholar
• Shpilka T, Weidberg H, Pietrokovski S, Elazar Z. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol 2011; 12:226; PMID:21867568; https://doi.org/10.1186/gb-2011-12-7-226
   PubMed Web of Science ®Google Scholar
• Weidberg H, Shvets E, Shpilka T, Shimron F, Shinder V, Elazar Z. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010; 29:1792-802; PMID:20418806; https://doi.org/10.1038/emboj.2010.74
   PubMed Web of Science ®Google Scholar
• Engedal N, Seglen PO. Autophagy of cytoplasmic bulk cargo does not require LC3. Autophagy 2016; 12:439-41; PMID:26237084; https://doi.org/10.1080/15548627.2015.1076606
   PubMed Web of Science ®Google Scholar
• Lystad AH, Ichimura Y, Takagi K, Yang Y, Pankiv S, Kanegae Y, Kageyama S, Suzuki M, Saito I, Mizushima T, et al. Structural determinants in GABARAP required for the selective binding and recruitment of ALFY to LC3B-positive structures. EMBO Rep 2014; 15:557-65; PMID:24668264; https://doi.org/10.1002/embr.201338003
   PubMed Web of Science ®Google Scholar
• Olsvik HL, Lamark T, Takagi K, Larsen KB, Evjen G, Øvervatn A, Mizushima T, Johansen T. FYCO1 contains a C-terminally extended, LC3A/B-preferring LC3-interacting Region (LIR) motif required for efficient maturation of autophagosomes during basal autophagy. J Biol Chem 2015; 290:29361-74; PMID:26468287; https://doi.org/10.1074/jbc.M115.686915
   PubMed Web of Science ®Google Scholar
• Szalai P, Hagen LK, Sætre F, Luhr M, Sponheim M, Øverbye A, Mills IG, Seglen PO, Engedal N. Autophagic bulk sequestration of cytosolic cargo is independent of LC3, but requires GABARAPs. Exp Cell Res 2015; 333:21-38; PMID:25684710; https://doi.org/10.1016/j.yexcr.2015.02.003
   PubMed Web of Science ®Google Scholar
• Park S, Choi J, Biering SB, Dominici E, Williams LE. Targeting by AutophaGy proteins (TAG): Targeting of IFNG-inducible GTPases to membranes by the LC3 conjugation system of autophagy. Autophagy 2016; 12:1153-67; PMID:27172324; https://doi.org/10.1080/15548627.2016.1178447
   PubMed Web of Science ®Google Scholar
• Haruki H, Nishikawa J, Laemmli UK. The Anchor-away technique: rapid, conditional establishment of yeast mutant phenotypes. Mol Cell 2008; 31:925-32; PMID:18922474; https://doi.org/10.1016/j.molcel.2008.07.020
   PubMed Web of Science ®Google Scholar
• Fu M-M, Nirschl JJ, Holzbaur ELF. LC3 Binding to the Scaffolding protein JIP1 regulates processive dynein-driven transport of autophagosomes. Dev Cell 2014; 29:577-90; PMID:24914561; https://doi.org/10.1016/j.devcel.2014.04.015
   PubMed Web of Science ®Google Scholar
• Singh SB, Davis AS, Taylor GA, Deretic V. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006; 313:1438-41; PMID:16888103; https://doi.org/10.1126/science.1129577
   PubMed Web of Science ®Google Scholar
• He S, Wang C, Dong H, Xia F, Zhou H, Jiang X, Pei C, Ren H, Li H, Li R, et al. Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke. Autophagy 2012; 8:1621-7; PMID:22874556; https://doi.org/10.4161/auto.21561
   PubMed Web of Science ®Google Scholar
• Chauhan S, Mandell MA, Deretic V. IRGM governs the core autophagy machinery to conduct antimicrobial defense. Mol Cell 2015; 58:507-21; PMID:25891078; https://doi.org/10.1016/j.molcel.2015.03.020
   PubMed Web of Science ®Google Scholar
• Al-Zeer MA, Al-Younes HM, Braun PR, Zerrahn J, Meyer TF. IFN-γ-Inducible Irga6 mediates host resistance against chlamydia trachomatis via autophagy. PLoS ONE 2009; 4:e4588; PMID:19242543
   PubMed Web of Science ®Google Scholar
• Hwang S, Maloney NS, Bruinsma MW, Goel G, Duan E, Zhang L, Shrestha B, Diamond MS, Dani A, Sosnovtsev SV, et al. Nondegradative role of Atg5-Atg12/ Atg16L1 autophagy protein complex in antiviral activity of interferon gamma. Cell Host Microbe 2012; 11:397-409; PMID:22520467; https://doi.org/10.1016/j.chom.2012.03.002
   PubMed Web of Science ®Google Scholar
• Maric-Biresev J, Hunn JP, Krut O, Helms JB, Martens S, Howard JC. Loss of the interferon-γ-inducible regulatory immunity-related GTPase (IRG), Irgm1, causes activation of effector IRG proteins on lysosomes, damaging lysosomal function and predicting the dramatic susceptibility of Irgm1-deficient mice to infection. BMC Biology 2016; 14:1-20; PMID:26728391; https://doi.org/10.1186/s12915-016-0255-4
   PubMed Web of Science ®Google Scholar
• da Fonseca Ferreira-da-Silva M, Springer-Frauenhoff HM, Bohne W, Howard JC. Identification of the Microsporidian Encephalitozoon cuniculi as a New Target of the IFNγ-Inducible IRG Resistance System. PLoS Pathog 2014; 10:e1004449; PMID:25356593; https://doi.org/10.1371/journal.ppat.1004449
   PubMed Web of Science ®Google Scholar
• Springer HM, Schramm M, Taylor GA, Howard JC. Irgm1 (LRG-47), a regulator of cell-autonomous immunity, does not localize to mycobacterial or listerial phagosomes in IFN-γ-induced mouse cells. J Immunol 2013; 191:1765-1774; PMID:23842753; https://doi.org/10.4049/jimmunol.1300641
   PubMed Web of Science ®Google Scholar
• Blader IJ, Manger ID, Boothroyd JC. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J Biol Chem 2001; 276:24223-31; PMID:11294868; https://doi.org/10.1074/jbc.M100951200
   PubMed Web of Science ®Google Scholar
• Yarovinsky F. Innate immunity to Toxoplasma gondiiinfection. Nat Rev Immunol 2014; 14:109-21; PMID:24457485; https://doi.org/10.1038/nri3598
   PubMed Web of Science ®Google Scholar
• Muniz-Feliciano L, Van Grol J, Portillo J-AC, Liew L, Liu B, Carlin CR, Carruthers VB, Matthews S, Subauste CS. Toxoplasma gondii-Induced Activation of EGFR Prevents Autophagy Protein-Mediated Killing of the Parasite. PLoS Pathog 2013; 9:e1003809; PMID:24367261; https://doi.org/10.1371/journal.ppat.1003809
   PubMed Web of Science ®Google Scholar
• Huang R, Xu Y, Wan W, Shou X, Qian J, You Z, Liu B, Chang C, Zhou T, Lippincott-Schwartz J, et al. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell 2015; 57:456-66; PMID:25601754; https://doi.org/10.1016/j.molcel.2014.12.013
   PubMed Web of Science ®Google Scholar
• He H. Post-translational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 2003; 278:29278-87; PMID:12740394; https://doi.org/10.1074/jbc.M303800200
   PubMed Web of Science ®Google Scholar
• Xie Y, Kang R, Sun X, Zhong M, Huang J, Klionsky DJ, Tang D. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy 2015; 11:28-45; PMID:25484070; https://doi.org/10.4161/15548627.2014.984267
   PubMed Web of Science ®Google Scholar
• Wilkinson DS, Jariwala JS, Anderson E, Mitra K, Meisenhelder J, Chang JT, Ideker T, Hunter T, Nizet V, Dillin A, et al. Phosphorylation of LC3 by the Hippo Kinases STK3/STK4 Is Essential for Autophagy. Mol Cell 2015; 57:55-68; PMID:25544559; https://doi.org/10.1016/j.molcel.2014.11.019
   PubMed Web of Science ®Google Scholar
• Haldar AK, Saka HA, Piro AS, Dunn JD, Henry SC, Taylor GA, Frickel EM, Valdivia RH, Coers J. IRG and GBP host resistance factors target aberrant, “non-self” vacuoles characterized by the missing of ‘self’ IRGM proteins. PLoS Pathog 2013; 9:e1003414-6; PMID:23785284; https://doi.org/10.1371/journal.ppat.1003414
   PubMed Web of Science ®Google Scholar
• Kubota C, Torii S, Hou N, Saito N, Yoshimoto Y, Imai H, Takeuchi T. Constitutive reactive oxygen species generation from autophagosome/lysosome in neuronal oxidative toxicity. J Biol Chem 2010; 285:667-74; PMID:19850931; https://doi.org/10.1074/jbc.M109.053058
   PubMed Web of Science ®Google Scholar
• Yu Z-Q, Ni T, Hong B, Wang H-Y, Jiang F-J, Zou S, Chen Y, Zheng X-L, Klionsky DJ, Liang Y, et al. Dual roles of Atg8−PE deconjugation by Atg4 in autophagy. Autophagy 2014; 8:883-92; PMID:NOT_FOUND; https://doi.org/10.4161/auto.19652
   PubMedGoogle Scholar
• Fernández AF, Lopez-Otin C. The functional and pathologic relevance of autophagy proteases. J Clin Invest 2015; 125:33-41; PMID:Can't; https://doi.org/10.1172/JCI73940
   PubMed Web of Science ®Google Scholar
• Bento CF, Renna M, Ghislat G, Puri C, Ashkenazi A, Vicinanza M, Menzies FM, Rubinsztein DC. Mammalian Autophagy: How Does It Work? Annu Rev Biochem 2016; 85:685-713; PMID:26865532; https://doi.org/10.1146/annurev-biochem-060815-014556
   PubMed Web of Science ®Google Scholar
• Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004; 119:753-66; PMID:15607973; https://doi.org/10.1016/j.cell.2004.11.038
   PubMed Web of Science ®Google Scholar
• GrEgoire IP, 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; PMID:22174682; https://doi.org/10.1371/journal.ppat.1002422
   PubMed Web of Science ®Google Scholar
• Koyama-Honda I, Itakura E, Fujiwara TK, Mizushima N. Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy 2013; 9:1491-1499; PMID:23884233; https://doi.org/10.4161/auto.25529
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152:657-68; PMID:11266458; https://doi.org/10.1083/jcb.152.4.657
   PubMed Web of Science ®Google Scholar
• Romanov J, Walczak M, Ibiricu I, Schüchner S, Ogris E, Kraft C, Martens S. Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J 2012; 31:4304-17; PMID:23064152; https://doi.org/10.1038/emboj.2012.278
   PubMed Web of Science ®Google Scholar
• Kuma A, Mizushima N, Ishihara N, Ohsumi Y. Formation of the approximately 350-kDa Apg12-Apg5.Apg16 multimeric complex, mediated by Apg16 oligomerization, is essential for autophagy in yeast. J Biol Chem 2002; 277:18619-25; PMID:11897782; https://doi.org/10.1074/jbc.M111889200
   PubMed Web of Science ®Google Scholar
• Dooley HC, Razi M, Polson HEJ, Girardin SE, Wilson MI, Tooze SA. WIPI2 links LC3-conjugation with PI3P, autophagosome formation and pathogen clearance by recruiting Atg12–5-16L1. Mol Cell 2014; 55:238-52; PMID:24954904; https://doi.org/10.1016/j.molcel.2014.05.021
   PubMed Web of Science ®Google Scholar
• Fujioka Y, Noda NN, Nakatogawa H, Ohsumi Y, Inagaki F. Dimeric coiled-coil structure of saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J Biol Chem 2010; 285:1508-15; PMID:19889643; https://doi.org/10.1074/jbc.M109.053520
   PubMed Web of Science ®Google Scholar
• Fujita N, Morita E, Itoh T, Tanaka A, Nakaoka M, Osada Y, Umemoto T, Saitoh T, Nakatogawa H, Kobayashi S, et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J Cell Biol 2013; 203:115-28; PMID:24100292; https://doi.org/10.1083/jcb.201304188
   PubMed Web of Science ®Google Scholar