Targeting by AutophaGy proteins (TAG): Targeting of IFNG-inducible GTPases to membranes by the LC3 conjugation system of autophagy

Autophagy

Volumn 12, Issue 7, 2016, Pages 1153-1167

  Park, Sungwoo ^a   Choi, Jayoung ^a   Biering, Scott B ^a   Dominici, Erin ^a   Williams, Lelia E ^a   Hwang, Seungmin ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

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

Indexed keywords

AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 16L1; AUTOPHAGY PROTEIN 5; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; LIGHT CHAIN 3; PHOSPHOLIPID; PROTEASOME; PROTEIN; PROTEIN GABARAP; PROTEIN GABARAPL1; PROTEIN GABARAPL2; UBIQUITIN; UNCLASSIFIED DRUG; AUTOPHAGY RELATED PROTEIN; IFNG PROTEIN, MOUSE; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; UBIQUITIN CONJUGATING ENZYME;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; MEMBRANE STRUCTURE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PARASITOPHORUS VACUOLE MEMBRANE; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REGULATORY MECHANISM; TOXOPLASMA GONDII; TOXOPLASMOSIS; ANIMAL; CELL CULTURE; METABOLISM; PHYSIOLOGY; TOXOPLASMA;

ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; CELLS, CULTURED; GTP PHOSPHOHYDROLASES; INTERFERON-GAMMA; MICE; MICROTUBULE-ASSOCIATED PROTEINS; TOXOPLASMA; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84979036004     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1178447     Document Type: Article

References (59)

1. D.J.Klionsky, F.C.Abdalla, H.Abeliovich, R.T.Abraham, A.Acevedo-Arozena, K.Adeli, L.Agholme, M.Agnello, P.Agostinis, J.A.Aguirre-Ghiso, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445-544; PMID:22966490; http://dx.doi.org/10.4161/auto.19496
2. T.Shpilka, H.Weidberg, S.Pietrokovski, Z.Elazar. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol 2011; 12:226; PMID:21867568; http://dx.doi.org/10.1186/gb-2011-12-7-226
3. P.Wild, D.G.McEwan, I.Dikic. The LC3 interactome at a glance. J Cell Sci 2014; 127:3-9; PMID:24345374; http://dx.doi.org/10.1242/jcs.140426
4. M.-M.Fu, J.J.Nirschl, E.L.F.Holzbaur. LC3 binding to the scaffolding protein JIP1 regulates processive dynein-driven transport of autophagosomes. Dev Cell 2014; 29:577-90; PMID:24914561; http://dx.doi.org/10.1016/j.devcel.2014.04.015
5. M.A.Sanjuan, C.P.Dillon, S.W.G.Tait, S.Moshiach, F.Dorsey, S.Connell, M.Komatsu, K.Tanaka, J.L.Cleveland, S.Withoff, et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 2007; 450:1253-7; PMID:18097414; http://dx.doi.org/10.1038/nature06421
6. C.J.DeSelm, B.C.Miller, W.Zou, W.L.Beatty, E.van Meel, Y.Takahata, J.Klumperman, S.A.Tooze, S.L.Teitelbaum, H.W.Virgin. Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Dev Cell 2011; 21:966-74; PMID:22055344; http://dx.doi.org/10.1016/j.devcel.2011.08.016
7. K.K.Patel, H.Miyoshi, W.L.Beatty, R.D.Head, N.P.Malvin, K.Cadwell, J.-L.Guan, T.Saitoh, S.Akira, P.O.Seglen, et al. Autophagy proteins control goblet cell function by potentiating reactive oxygen species production. EMBO J 2013; 32:3130-44; PMID:24185898; http://dx.doi.org/10.1038/emboj.2013.233
8. S.Romao, C.Münz. LC3-associated phagocytosis. Autophagy 2014; 10:526-8; PMID:24413059; http://dx.doi.org/10.4161/auto.27606
9. J.Martinez, R.K.S.Malireddi, Q.Lu, L.D.Cunha, S.Pelletier, S.Gingras, R.Orchard, J.-L.Guan, H.Tan, J.Peng, et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol 2015; 17:893-906; PMID:26098576; http://dx.doi.org/10.1038/ncb3192
10. N.Fujita, T.Itoh, H.Omori, M.Fukuda, T.Noda, T.Yoshimori. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 2008; 19(5):2092-100; PMID:18321988; http://dx.doi.org/10.1091/mbc.E07-12-1257
11. J.Choi, S.Park, S.B.Biering, E.Selleck, C.Y.Liu, X.Zhang, N.Fujita, T.Saitoh, S.Akira, T.Yoshimori, 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; http://dx.doi.org/10.1016/j.immuni.2014.05.006
12. E.Suss-Toby, J.Zimmerberg, G.E.Ward. Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci USA 1996; 93:8413-8; PMID:8710885; http://dx.doi.org/10.1073/pnas.93.16.8413
13. A.P.Sinai. Biogenesis of and activities at the Toxoplasma gondii parasitophorous vacuole membrane. Subcell Biochem 2008; 47:155-64; PMID:18512349; http://dx.doi.org/10.1007/978-0-387-78267-6_12
14. I.J.Blader, A.A.Koshy. Toxoplasma gondii development of its replicative niche: in its host cell and beyond. Eukaryot Cell 2014; 13:965-76; PMID:24951442; http://dx.doi.org/10.1128/EC.00081-14
15. F.Yarovinsky. Innate immunity to Toxoplasma gondiiinfection. Nat Rev Immunol 2014; 14:109-21; PMID:24457485; http://dx.doi.org/10.1038/nri3598
16. C.A.Hunter, L.D.Sibley. Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat Rev Microbiol 2012; 10:766-78; PMID:23070557; http://dx.doi.org/10.1038/nrmicro2858
17. F.Reggiori, I.Monastyrska, M.H.Verheije, T.Calì, M.Ulasli, S.Bianchi, R.Bernasconi, C.A.M.de Haan, M.Molinari. Coronaviruses hijack the LC3-I-Positive EDEMosomes, ER-Derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 2010; 7:500-8; PMID:20542253; http://dx.doi.org/10.1016/j.chom.2010.05.013
18. G.M.Cann, C.Guignabert, L.Ying, N.Deshpande, J.M.Bekker, L.Wang, B.Zhou, M.Rabinovitch. Developmental expression of LC3α and β: Absence of fibronectin or autophagy phenotype in LC3β knockout mice. Dev Dyn 2007; 237:187-95; http://dx.doi.org/10.1002/dvdy.21392
19. H.Weidberg, E.Shvets, T.Shpilka, F.Shimron, V.Shinder, Z.Elazar. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J 2010; 29:1792-802; PMID:20418806; http://dx.doi.org/10.1038/emboj.2010.74
20. N.Engedal, P.O.Seglen. Autophagy of cytoplasmic bulk cargo does not require LC3. Autophagy 2016; 12(2):439–41; PMID:26237084; http://dx.doi.org/10.1080/15548627.2015.1076606
21. A.H.Lystad, Y.Ichimura, K.Takagi, Y.Yang, S.Pankiv, Y.Kanegae, S.Kageyama, M.Suzuki, I.Saito, T.Mizushima, 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; http://dx.doi.org/10.1002/embr.201338003
22. H.L.Olsvik, T.Lamark, K.Takagi, K.B.Larsen, G.Evjen, A.Øvervatn, T.Mizushima, T.Johansen. 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; http://dx.doi.org/10.1074/jbc.M115.686915
23. P.Szalai, L.K.Hagen, F.Sætre, M.Luhr, M.Sponheim, A.Øverbye, I.G.Mills, P.O.Seglen, N.Engedal. Autophagic bulk sequestration of cytosolic cargo is independent of LC3, but requires GABARAPs. Exp Cell Res 2015; 333:21-38; PMID:25684710; http://dx.doi.org/10.1016/j.yexcr.2015.02.003
24. N.Mizushima. Mouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugate. J Cell Sci 2003; 116:1679-88; PMID:12665549; http://dx.doi.org/10.1242/jcs.00381
25. T.Itoh, N.Fujita, E.Kanno, A.Yamamoto, T.Yoshimori, M.Fukuda. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 2008; 19:2916-25; PMID:18448665; http://dx.doi.org/10.1091/mbc.E07-12-1231
26. N.Gammoh, O.Florey, M.Overholtzer, X.Jiang. Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and -independent autophagy. Nat Struct Mol Biol 2013; 20:144-9; PMID:23262492; http://dx.doi.org/10.1038/nsmb.2475
27. N.Fujita, E.Morita, T.Itoh, A.Tanaka, M.Nakaoka, Y.Osada, T.Umemoto, T.Saitoh, H.Nakatogawa, S.Kobayashi, et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J Cell Biol 2013; 203:115-28; PMID:24100292; http://dx.doi.org/10.1083/jcb.201304188
28. H.C.Dooley, M.Razi, H.E.J.Polson, S.E.Girardin, M.I.Wilson, S.A.Tooze. WIPI2 links LC3-Conjugation with PI3P, autophagosome formation and pathogen clearance by recruiting Atg12–5-16L1. Mol Cell 2014; 55:238-52; PMID:24954904; http://dx.doi.org/10.1016/j.molcel.2014.05.021
29. P.J.Roberts, N.Mitin, P.J.Keller, E.J.Chenette, J.P.Madigan, R.O.Currin, A.D.Cox, O.Wilson, P.Kirschmeier, C.J.Der. Rho family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J Biol Chem 2008; 283:25150-63; PMID:18614539; http://dx.doi.org/10.1074/jbc.M800882200
30. H.Haruki, J.Nishikawa, U.K.Laemmli. The anchor-away technique: rapid, conditional establishment of Yeast mutant phenotypes. Mol Cell 2008; 31:925-32; PMID:18922474; http://dx.doi.org/10.1016/j.molcel.2008.07.020
31. S.Park, S.-G.Choi, S.-M.Yoo, J.H.Son, Y.-K.Jung. Choline dehydrogenase interacts with SQSTM1/p62 to recruit LC3 and stimulate mitophagy. Autophagy 2014; 10:1906-20; PMID:25483962; http://dx.doi.org/10.4161/auto.32177
32. N.N.Noda, F.Inagaki. Mechanisms of autophagy. Annu Rev Biophys 2015; 44:101-22; PMID:25747593; http://dx.doi.org/10.1146/annurev-biophys-060414-034248
33. J.Romanov, M.Walczak, I.Ibiricu, S.Schüchner, E.Ogris, C.Kraft, S.Martens. Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J 2012; 31:4304-17; PMID:23064152; http://dx.doi.org/10.1038/emboj.2012.278
34. L.Muniz-Feliciano, J.Van Grol, J.-A.C.Portillo, L.Liew, B.Liu, C.R.Carlin, V.B.Carruthers, S.Matthews, C.S.Subauste. Toxoplasma gondii-induced activation of EGFR prevents autophagy protein-mediated killing of the parasite. PLoS Pathog 2013; 9:e1003809; PMID:24367261; http://dx.doi.org/10.1371/journal.ppat.1003809
35. J.Coers. Self and non-self discrimination of intracellular membranes by the innate immune system. PLoS Pathog 2013; 9:e1003538; PMID:24068918; http://dx.doi.org/10.1371/journal.ppat.1003538
36. J.P.Hunn, S.Koenen-Waisman, N.Papic, N.Schroeder, N.Pawlowski, R.Lange, F.Kaiser, J.Zerrahn, S.Martens, J.C.Howard. Regulatory interactions between IRG resistance GTPases in the cellular response to Toxoplasma gondii. EMBO J 2008; 27:2495-509; PMID:18772884; http://dx.doi.org/10.1038/emboj.2008.176
37. A.K.Haldar, H.A.Saka, A.S.Piro, J.D.Dunn, S.C.Henry, G.A.Taylor, E.M.Frickel, R.H.Valdivia, J.Coers. 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; http://dx.doi.org/10.1371/journal.ppat.1003414
38. S.B.Singh, A.S.Davis, G.A.Taylor, V.Deretic. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006; 313:1438-41; PMID:16888103; http://dx.doi.org/10.1126/science.1129577
39. S.He, C.Wang, H.Dong, F.Xia, H.Zhou, X.Jiang, C.Pei, H.Ren, H.Li, R.Li, et al. Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke. Autophagy 2012; 8:1621-7; PMID:22874556; http://dx.doi.org/10.4161/auto.21561
40. S.Chauhan, M.A.Mandell, V.Deretic. IRGM governs the core autophagy machinery to conduct antimicrobial defense. Mol Cell 2015; 58:507-21; PMID:25891078; http://dx.doi.org/10.1016/j.molcel.2015.03.020
41. M.A.Al-Zeer, H.M.Al-Younes, P.R.Braun, J.Zerrahn, T.F.Meyer. IFNG-Inducible Irga6 mediates host resistance against chlamydia trachomatis via autophagy. PLoS ONE 2009; 4:e4588; PMID:19242543; http://dx.doi.org/10.1371/journal.pone.0004588
42. R.Pifer, F.Yarovinsky. Innate responses to Toxoplasma gondii in mice and humans. Trends Parasitol 2011; 27:388-93; PMID:21550851; http://dx.doi.org/10.1016/j.pt.2011.03.009
43. J.Ohshima, Y.Lee, M.Sasai, T.Saitoh, J.Su Ma, N.Kamiyama, Y.Matsuura, S.Pann-Ghill, M.Hayashi, S.Ebisu, et al. Role of mouse and human autophagy proteins in IFNG-induced cell-autonomous responses against Toxoplasma gondii. J Immunol 2014; 192:3328-35; PMID:24563254; http://dx.doi.org/10.4049/jimmunol.1302822
44. E.M.Selleck, R.C.Orchard, K.G.Lassen, W.L.Beatty, R.J.Xavier, B.Levine, H.W.Virgin, L.D.Sibley. A noncanonical autophagy pathway restricts toxoplasma gondii growth in a strain-specific manner in IFNG-activated human cells. mBio 2015; 6:e01157-15; PMID:26350966; http://dx.doi.org/10.1128/mBio.01157-15
45. S.Hwang, N.S.Maloney, M.W.Bruinsma, G.Goel, E.Duan, L.Zhang, B.Shrestha, M.S.Diamond, A.Dani, S.V.Sosnovtsev, 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; http://dx.doi.org/10.1016/j.chom.2012.03.002
46. Å.B.Birgisdottir, T.Lamark, T.Johansen. The LIR motif - crucial for selective autophagy. J Cell Sci 2013; 126:3237-47; PMID:23908376
47. I.J.Blader, I.D.Manger, J.C.Boothroyd. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J Biol Chem 2001; 276:24223-31; PMID:11294868; http://dx.doi.org/10.1074/jbc.M100951200
48. R.Huang, Y.Xu, W.Wan, X.Shou, J.Qian, Z.You, B.Liu, C.Chang, T.Zhou, J.Lippincott-Schwartz, et al. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell 2015; 57:456-66; PMID:25601754; http://dx.doi.org/10.1016/j.molcel.2014.12.013
49. H.He. 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; http://dx.doi.org/10.1074/jbc.M303800200
50. Y.Xie, R.Kang, X.Sun, M.Zhong, J.Huang, D.J.Klionsky, D.Tang. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy 2015; 11:28-45; PMID:25484070; http://dx.doi.org/10.4161/15548627.2014.984267
51. D.S.Wilkinson, J.S.Jariwala, E.Anderson, K.Mitra, J.Meisenhelder, J.T.Chang, T.Ideker, T.Hunter, V.Nizet, A.Dillin, et al. Phosphorylation of LC3 by the hippo kinases STK3/STK4 is essential for autophagy. Mol Cell 2015; 57:55-68; PMID:25544559; http://dx.doi.org/10.1016/j.molcel.2014.11.019
52. S.Jiang, N.Dupont, E.F.Castillo, V.Deretic. Secretory versus degradative autophagy: unconventional secretion of inflammatory mediators. J Innate Immun 2013; 5(5):471-9; PMID:23445716; http://dx.doi.org/10.1159/000346707
53. K.D.Wilkinson. The discovery of ubiquitin-dependent proteolysis. Proc Natl Acad Sci USA 2005; 102:15280-2; PMID:16230621; http://dx.doi.org/10.1073/pnas.0504842102
54. M.D.Petroski. The ubiquitin system, disease, and drug discovery. BMC Biochem 2008; 9(Suppl 1):S7-S7; PMID:19007437; http://dx.doi.org/10.1186/1471-2091-9-S1-S7
55. B.Levine, N.Mizushima, H.W.Virgin. Autophagy in immunity and inflammation. Nature 2011; 469:323-35; PMID:21248839; http://dx.doi.org/10.1038/nature09782
56. C.Behrends, M.E.Sowa, S.P.Gygi, J.W.Harper. Network organization of the human autophagy system. Nature 2010; 466:68-76; PMID:20562859; http://dx.doi.org/10.1038/nature09204
57. S.Lee, L.Salwinski, C.Zhang, D.Chu, C.Sampankanpanich, N.A.Reyes, A.Vangeloff, F.Xing, X.Li, T.-T.Wu, et al. An integrated approach to elucidate the intra-viral and viral-cellular protein interaction networks of a gamma-herpesvirus. PLoS Pathog 2011; 7:e1002297-7; PMID:22028648; http://dx.doi.org/10.1371/journal.ppat.1002297
58. B.F.C.Kafsack, C.Beckers, V.B.Carruthers. Synchronous invasion of host cells by Toxoplasma gondii. Mol Biochem Parasitol 2004; 136:309-11; PMID:15478810; http://dx.doi.org/10.1016/j.molbiopara.2004.04.004
59. Z.Zhao, B.Fux, M.Goodwin, I.R.Dunay, D.Strong, B.C.Miller, K.Cadwell, M.A.Delgado, M.Ponpuak, K.G.Green, 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; http://dx.doi.org/10.1016/j.chom.2008.10.003