WIPI2b and Atg16L1: Setting the stage for autophagosome formation

Biochemical Society Transactions

Volumn 42, Issue 5, 2014, Pages 1327-1334

  Wilson, Michael I ^a   Dooley, Hannah C ^b   Tooze, Sharon A ^b  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Atg12 5 16; Autophagosome; Autophagy; LC3 conjugation; Phosphatidylinositol 3 phosphate; WIPI2

Indexed keywords

AUTOPHAGY RELATED PROTEIN 16 LIKE 1; CELL PROTEIN; UNCLASSIFIED DRUG; WIPI2 PROTEIN; ATG16L1 PROTEIN, HUMAN; CARRIER PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; POLYPHOSPHOINOSITIDE; WIPI-2 PROTEIN, HUMAN;

AUTOPHAGOSOME; BINDING SITE; CELL METABOLISM; CONJUGATION; CRYSTAL STRUCTURE; ENDOPLASMIC RETICULUM; HUMAN; KLUYVEROMYCES MARXIANUS; MICROAUTOPHAGY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REVIEW; ANIMAL; AUTOPHAGY; CHEMICAL STRUCTURE; CHEMISTRY; DIMERIZATION; INTRACELLULAR MEMBRANE; METABOLISM; PHAGOSOME; PROTEIN CONFORMATION; PROTEIN DOMAIN;

ANIMALS; AUTOPHAGY; BINDING SITES; CARRIER PROTEINS; DIMERIZATION; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MODELS, MOLECULAR; PHAGOSOMES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84907211285     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140177     Document Type: Review

References (54)

1. Lamb, C.A., Yoshimori, T. and Tooze, S.A. (2013) The autophagosome: origins unknown, biogenesis complex. Nat. Rev. Mol. Cell Biol. 14, 759-774 CrossRef PubMed
2. Kaushik, S. and Cuervo, A.M. (2012) Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol. 22, 407-417 CrossRef PubMed
3. Sahu, R., Kaushik, S., Clement, C.C., Cannizzo, E.S., Scharf, B., Follenzi, A., Potolicchio, I., Nieves, E., Cuervo, A.M. and Santambrogio, L. (2011) Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 20, 131-139 CrossRef PubMed
4. Slobodkin, M.R. and Elazar, Z. (2013) The Atg8 family: multifunctional ubiquitin-like key regulators of autophagy. Essays Biochem. 55, 51-64 CrossRef PubMed
5. Dooley, H.C., Razi, M., Polson, H.E.J., Girardin, S.E., Wilson, M.I. and Tooze, S.A. (2014) WIPI2 links LC3-conjugation with PI3P, autophagosome formation and pathogen clearance by recruiting Atg12-5-16L1. Mol. Cell 55, 238-252 CrossRef PubMed
6. de Duve, C. and Wattiaux, R. (1966) Functions of lysosomes. Annu. Rev. Physiol. 28, 435-492 CrossRef PubMed
7. Hayashi-Nishino, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T. and Yamamoto, A. (2009) A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437 CrossRef PubMed
8. Mizushima, N., Yoshimori, T. and Ohsumi, Y. (2011) The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132 CrossRef PubMed
9. Rabinowitz, J.D. and White, E. (2010) Autophagy and metabolism. Science 330, 1344-1348 CrossRef PubMed
10. Musiwaro, P., Smith, M., Manifava, M., Walker, S.A. and Ktistakis, N.T. (2013) Characteristics and requirements of basal autophagy in HEK 293 cells. Autophagy 9, 1407-1417 CrossRef PubMed
11. Green, D.R. and Levine, B. (2014) To be or not to be? How selective autophagy and cell death govern cell fate. Cell 157, 65-75 CrossRef PubMed
12. Stolz, A., Ernst, A. and Dikic, I. (2014) Cargo recognition and trafficking in selective autophagy. Nature 16, 495-501
13. Rogov, V., Dötsch, V., Johansen, T. and Kirkin, V. (2014) Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol. Cell 53, 167-178 CrossRef PubMed
14. Saitoh, T., Jang, M.H., Uematsu, S., Yang, B.-G., Satoh, T., Noda, T., Yamamoto, N., Komatsu, M., Tanaka, K., Kawai, T. et al. (2008) Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production. Nature 456, 264-268 CrossRef PubMed
15. Shi, C.-S., Shenderov, K., Huang, N.-N., Kabat, J., Abu-Asab, M., Fitzgerald, K.A., Sher, A. and Kehrl, J.H. (2012) Activation of autophagy by inflammatory signals limits IL-1β production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13, 255-263 CrossRef PubMed
16. Cadwell, K., Liu, J.Y., Brown, S.L., Miyoshi, H., Loh, J., Lennerz, J.K., Kishi, C., Kc, W., Carrero, J.A., Hunt, S. et al. (2008) A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 456, 259-263 CrossRef PubMed
17. Romao, S., Gasser, N., Becker, A.C., Guhl, B., Bajagic, M., Vanoaica, D., Ziegler, U., Roesler, J., Dengjel, J., Reichenbach, J. and Münz, C. (2013) Autophagy proteins stabilize pathogen-containing phagosomes for prolonged MHC II antigen processing. J. Cell Biol. 203, 757-766 CrossRef PubMed
18. Huang, J. and Brumell, J.H. (2014) Bacteria-autophagy interplay: a battle for survival. Nat. Rev. Microbiol. 12, 101-104 CrossRef PubMed
19. Philpott, D.J., Sorbara, M.T., Robertson, S.J., Croitoru, K. and Girardin, S.E. (2014) NOD proteins: regulators of inflammation in health and disease. Nat. Rev. Immunol. 14, 9-23 CrossRef PubMed
20. Axe, E.L., Walker, S.A., Manifava, M., Chandra, P., Roderick, H.L., Habermann, A., Griffiths, G. and Ktistakis, N.T. (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 182, 685-701 CrossRef PubMed
21. Matsunaga, K., Saitoh, T., Tabata, K., Satoh, T., Kurotori, N., Maejima, I., Shirahama-Noda, K., Ichimura, T., Isobe, T., Akira, S. et al. (2009) Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nature 11, 385-396
22. Hurley, J.H. and Schulman, B.A. (2014) Atomistic autophagy: the structures of cellular self-digestion. Cell 157, 300-311 CrossRef PubMed
23. Taherbhoy, A.M., Tait, S.W., Kaiser, S.E., Williams, A.H., Deng, A., Nourse, A., Hammel, M., Kurinov, I., Rock, C.O., Green, D.R. and Schulman, B.A. (2011) Atg8 transfer from atg7 to atg3: a distinctive e1-e2 architecture and mechanism in the autophagy pathway. Mol. Cell 44, 451-461 CrossRef PubMed
24. Metlagel, Z., Otomo, C., Takaesu, G. and Otomo, T. (2013) Structural basis of ATG3 recognition by the autophagic ubiquitin-like protein ATG12. Proc. Natl. Acad. Sci. U.S.A. 110, 18844-18849 CrossRef PubMed
25. Kaiser, S.E., Mao, K., Taherbhoy, A.M., Yu, S., Olszewski, J.L., Duda, D.M., Kurinov, I., Deng, A., Fenn, T.D., Klionsky, D.J. and Schulman, B.A. (2012) Noncanonical E2 recruitment by the autophagy E1 revealed by Atg7-Atg3 and Atg7-Atg10 structures. Nat. Struct. Mol. Biol. 19, 1242-1249 CrossRef PubMed
26. Romanov, J., Walczak, M., Ibiricu, I., Schüchner, S., Ogris, E., Kraft, C. and Martens, S. (2012) Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. EMBO J. 31, 4304-4317 CrossRef PubMed
27. Sakoh-Nakatogawa, M., Matoba, K., Asai, E., Kirisako, H., Ishii, J., Noda, N.N., Inagaki, F., Nakatogawa, H. and Ohsumi, Y. (2013) Atg12-Atg5 conjugate enhances E2 activity of Atg3 by rearranging its catalytic site. Nat. Struct. Mol. Biol. 20, 433-439 CrossRef PubMed
28. Nath, S., Dancourt, J., Shteyn, V., Puente, G., Fong, W.M., Nag, S., Bewersdorf, J., Yamamoto, A., Antonny, B. and Melia, T.J. (2014) Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nature 16, 415-424
29. Fujioka, Y., Noda, N.N., Nakatogawa, H., Ohsumi, Y. and Inagaki, F. (2010) Dimeric coiled-coil structure of Saccharomyces cerevisiae Atg16 and its functional significance in autophagy. J. Biol. Chem. 285, 1508-1515 CrossRef PubMed
30. Fujita, N., Itoh, T., Omori, H., Fukuda, M., Noda, T. and Yoshimori, T. (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19, 2092-2100 CrossRef PubMed
31. Saitoh, T., Kageyama, S., Akira, S., Noda, T. and Yoshimori, T. (2009) Differential involvement of Atg16L1 in Crohn disease and canonical autophagy: analysis of the organization of the Atg16L1 complex in fibroblasts. J. Biol. Chem. 284, 32602-32609 CrossRef PubMed
32. Fujita, N., Morita, E., Itoh, T., Tanaka, A., Nakaoka, M., Osada, Y., Umemoto, T., Saitoh, T., Nakatogawa, H., Kobayashi, S. et al. (2013) Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J. Cell Biol. 203, 115-128 CrossRef PubMed
33. Ishibashi, K., Fujita, N., Kanno, E., Omori, H., Yoshimori, T., Itoh, T. and Fukuda, M. (2011) Atg16L2, a novel isoform of mammalian Atg16L that is not essential for canonical autophagy despite forming an Atg12-5-16L2 complex. Autophagy 7, 1500-1513 CrossRef PubMed
34. Nishimura, T., Kaizuka, T., Cadwell, K., Sahani, M.H., Saitoh, T., Akira, S., Virgin, H.W. and Mizushima, N. (2013) FIP200 regulates targeting of Atg16L1 to the isolation membrane. EMBO Rep. 14, 284-291 CrossRef PubMed
35. Gammoh, N., Florey, O., Overholtzer, M. and Jiang, X. (2012) Interaction between FIP200 and ATG16L1 distinguishes ULK1 complex-dependent and -independent autophagy. Nat. Struct. Mol. Biol. 20, 144-149 CrossRef PubMed
36. Murthy, A., Li, Y., Peng, I., Reichelt, M., Katakam, A.K., Noubade, R., Roose-Girma, M., DeVoss, J., Diehl, L., Graham, R.R. and van Lookeren Campagne, M. (2014) A Crohn's disease variant in Atg16l1 enhances its degradation by caspase 3. Nature 506, 456-462 CrossRef PubMed
37. Otomo, C., Metlagel, Z., Takaesu, G. and Otomo, T. (2013) Structure of the human ATG12-ATG5 conjugate required for LC3 lipidation in autophagy. Nat. Struct. Mol. Biol. 20, 59-66 CrossRef PubMed
38. Kim, J., Kim, Y.C., Fang, C., Russell, R.C., Kim, J.H., Fan, W., Liu, R., Zhong, Q. and Guan, K.-L. (2013) Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 152, 290-303 CrossRef PubMed
39. Pankiv, S., Alemu, E.A., Brech, A., Bruun, J.A., Lamark, T., Overvatn, A., Bjorkoy, G. and Johansen, T. (2010) FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J. Cell Biol. 188, 253-269 CrossRef PubMed
40. Filimonenko, M., Isakson, P., Finley, K.D., Anderson, M., Jeong, H., Melia, T.J., Bartlett, B.J., Myers, K.M., Birkeland, H.C.G., Lamark, T. et al. (2010) The selective macroautophagic degradation of aggregated proteins requires the PI3P-binding protein ALFY. Mol. Cell 38, 265-279 CrossRef PubMed
41. Michell, R.H., Heath, V.L., Lemmon, M.A. and Dove, S.K. (2006) Phosphatidylinositol 3,5-bisphosphate: metabolism and cellular functions. Trends Biochem. Sci. 31, 52-63 CrossRef PubMed
42. Krick, R., Tolstrup, J., Appelles, A., Henke, S. and Thumm, M. (2006) The relevance of the phosphatidylinositol phosphate-binding motif FRRGT of Atg18 and Atg21 for the Cvt pathway and autophagy. FEBS Lett. 580, 4632-4638 CrossRef PubMed
43. Busse, R.A., Scacioc, A., Hernandez, J.M., Krick, R., Stephan, M., Janshoff, A., Thumm, M. and Kühnel, K. (2013) Qualitative and quantitative characterization of protein-phosphoinositide interactions with liposome-based methods. Autophagy 9, 770-777 CrossRef PubMed
44. Baskaran, S., Ragusa, M.J., Boura, E. and Hurley, J.H. (2012) Two-site recognition of phosphatidylinositol 3-phosphate by PROPPINs in autophagy. Mol. Cell 47, 339-348 CrossRef PubMed
45. Krick, R., Busse, R.A., Scacioc, A., Stephan, M., Janshoff, A., Thumm, M. and Kühnel, K. (2012) Structural and functional characterization of the two phosphoinositide binding sites of PROPPINs, a β-propeller protein family. Proc. Natl. Acad. Sci. U.S.A. 109, E2042-E2049 CrossRef PubMed
46. Watanabe, Y., Kobayashi, T., Yamamoto, H., Hoshida, H., Akada, R., Inagaki, F., Ohsumi, Y. and Noda, N.N. (2012) Structure-based analyses reveal distinct binding sites for Atg2 and phosphoinositides in Atg18. J. Biol. Chem. 287, 31681-31690 CrossRef PubMed
47. Krick, R., Henke, S., Tolstrup, J. and Thumm, M. (2008) Dissecting the localization and function of Atg18, Atg21 and Ygr223c. Autophagy 4, 896-910 CrossRef PubMed
48. Gaugel, A., Bakula, D., Hoffmann, A. and Proikas-Cezanne, T. (2012) Defining regulatory and phosphoinositide-binding sites in the human WIPI-1 β-propeller responsible for autophagosomal membrane localization downstream of mTORC1 inhibition. J. Mol. Signal. 7, 1-16 CrossRef PubMed
49. Karanasios, E., Stapleton, E., Manifava, M., Kaizuka, T., Mizushima, N., Walker, S.A. and Ktistakis, N.T. (2013) Dynamic association of the ULK1 complex with omegasomes during autophagy induction. J. Cell Sci. 126, 5224-5238 CrossRef PubMed
50. Koyama-Honda, I., Itakura, E., Fujiwara, T.K. and Mizushima, N. (2013) Temporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site. Autophagy 9, 1491-1499 CrossRef PubMed
51. Polson, H.E., de Lartigue, J., Rigden, D.J., Reedijk, M., Urbé, S., Clague, M.J. and Tooze, S.A. (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6, 506-522 CrossRef PubMed
52. Mauthe, M., Jacob, A., Freiberger, S., Hentschel, K., Stierhof, Y.-D., Codogno, P. and Proikas-Cezanne, T. (2011) Resveratrol-mediated autophagy requires WIPI-1-regulated LC3 lipidation in the absence of induced phagophore formation. Autophagy 7, 1448-1461 CrossRef PubMed
53. Roy, A., Kucukural, A. and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738 CrossRef PubMed
54. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 CrossRef PubMed