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

Small GTPases

Volumn 8, Issue 4, 2017, Pages 199-207

  Choi, Jayoung ^a   Biering, Scott B ^a   Hwang, Seungmin ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

autophagy; GBP; IFN; IRG; LC3; TAG; targeting; Toxoplasma gondii; ubiquitin

Indexed keywords

FAT DROPLET; GAMMA INTERFERON; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; INTERFERON; MICROTUBULE ASSOCIATED PROTEIN 1; PHOSPHATIDYLETHANOLAMINE; UBIQUITIN; MICROTUBULE ASSOCIATED PROTEIN;

AUTOPHAGOSOME; AUTOPHAGY; CHLAMYDIA TRACHOMATIS; HUMAN; NOTE; OLIGOMERIZATION; PATTERN RECOGNITION; PROTEIN LOCALIZATION; TOXOPLASMA GONDII; ANIMAL; CELL MEMBRANE; METABOLISM; PHYSIOLOGY; TOXOPLASMA;

ANIMALS; AUTOPHAGY; CELL MEMBRANE; GTP PHOSPHOHYDROLASES; HUMANS; INTERFERONS; MICROTUBULE-ASSOCIATED PROTEINS; TOXOPLASMA;

EID: 84981502098     PISSN: 21541248     EISSN: 21541256     Source Type: Journal    
DOI: 10.1080/21541248.2016.1213090     Document Type: Note

References (67)

1. 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
2. Coers J. Self and non-self discrimination of intracellular membranes by the innate immune system. PLoS Pathog 2013; 9:e1003538; PMID:24068918
3. 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. 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
15. 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
16. 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
17. 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
18. 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
19. 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
20. 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
21. 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
22. 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
23. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; https://doi.org/10.1038/nature09782
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. 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
31. 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
32. 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
33. 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
34. 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
35. 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
36. 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
37. 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
38. 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
39. 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
40. 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
41. 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
42. 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
43. 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
44. 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
45. 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
46. 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
47. 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
48. Yarovinsky F. Innate immunity to Toxoplasma gondiiinfection. Nat Rev Immunol 2014; 14:109-21; PMID:24457485; https://doi.org/10.1038/nri3598
49. 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
50. 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
51. 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
52. 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
53. 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
54. 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
55. 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
56. 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
57. 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
58. 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
59. 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
60. 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
61. 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
62. 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
63. 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
64. 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
65. 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
66. 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
67. 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