Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3

Nature Cell Biology

Volumn 16, Issue 5, 2014, Pages 415-424

  Nath, Sangeeta ^a   Dancourt, Julia ^a   Shteyn, Vladimir ^a   Puente, Gabriella ^a   Fong, Wendy M ^b   Nag, Shanta ^a   Bewersdorf, Joerg ^a   Yamamoto, Ai ^b   Antonny, Bruno ^c   Melia, Thomas J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAY RELATE PROTEIN 3; CARRIER PROTEINS AND BINDING PROTEINS; PROTEIN GABARAP; PROTEIN LC3; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR ASSOCIATED PROTEIN; MEMBRANE PROTEIN; PROTEIN ATG3;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL STRESS; CONTROLLED STUDY; HYDROPHOBICITY; IN VITRO STUDY; INTRACELLULAR MEMBRANE; LIPID MEMBRANE; LIPIDATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TARGETING; ANIMAL CELL; AUTOPHAGY; EMBRYO; HUMAN; MOUSE; NONHUMAN; PHAGOPHORE; PROTEIN MODIFICATION; PROTEIN STRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; ANIMALS; CELL MEMBRANE; CYTOSKELETAL PROTEINS; HELA CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPOSOMES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PHOSPHATIDYLETHANOLAMINES; RATS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSFECTION; UBIQUITIN-ACTIVATING ENZYMES; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84899844485     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2940     Document Type: Article

References (54)

1. Itakura, E. & Mizushima, N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6, 764-776 (2010).
2. Ichimura, Y. et al. A ubiquitin-like system mediates protein lipidation. Nature 408, 488-492 (2000).
3. Kabeya, Y. et al. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117, 2805-2812 (2004).
4. Nakatogawa, H., Ichimura, Y. & Ohsumi, Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130, 165-178 (2007).
5. Weidberg, H. et al. LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis. EMBO J. 29, 1792-1802 (2010).
6. Shpilka, T., Weidberg, H., Pietrokovski, S. & Elazar, Z. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol. 12, 226 (2011).
7. Sou, Y. S. et al. The Atg8 conjugation system is indispensable for proper development of autophagic isolation membranes in mice. Mol. Biol. Cell 19, 4762-4775 (2008).
8. Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434 (2005).
9. Nishida, Y. et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461, 654-658 (2009).
10. Mizushima, N. et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657-668 (2001).
11. Hayashi-Nishino, M. et al. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat. Cell Biol. 11, 1433-1437 (2009).
12. Fan, W., Nassiri, A. & Zhong, Q. Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc. Natl Acad. Sci. USA 108, 7769-7774 (2011).
13. Drin, G. & Antonny, B. Amphipathic helices and membrane curvature. FEBS Letters 584, 1840-1847 (2010).
14. Hayashi-Nishino, M. et al. Electron tomography reveals the endoplasmic reticulum as a membrane source for autophagosome formation. Autophagy 6, 301-303 (2009).
15. Ichimura, Y. et al. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J. Biol. Chem. 279, 40584-40592 (2004).
16. Sou, Y. S., Tanida, I., Komatsu, M., Ueno, T. & Kominami, E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. J. Biol. Chem. 281, 3017-3024 (2006).
17. Tanida, I., Sou, Y. S., Minematsu-Ikeguchi, N., Ueno, T. & Kominami, E. Atg8L/Apg8L is the fourth mammalian modifier of mammalian Atg8 conjugation mediated by human Atg4B, Atg7 and Atg3. FEBS J. 273, 2553-2562 (2006).
18. Choy, A. et al. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science 338, 1072-1076 (2012).
19. Oh-oka, K., Nakatogawa, H. & Ohsumi, Y. Physiological pH and acidic phospholipids contribute to substrate specificity in lipidation of Atg8. J. Biol. Chem. 283, 21847-21852 (2008).
20. Brownell, J. E. et al. Substrate-assisted inhibition of ubiquitin-like protein-activating enzymes: the NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ. Mol. Cell 37, 102-111 (2010).
21. Nair, U. et al. SNARE proteins are required for macroautophagy. Cell 146, 290-302 (2011).
22. Zimmerberg, J. & Kozlov, M. M. How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19 (2006).
23. Hatzakis, N. S. et al. How curved membranes recruit amphipathic helices and protein anchoring motifs. Nat. Chem. Biol. 5, 835-841 (2009).
24. Vamparys, L. et al. Conical lipids in flat bilayers induce packing defects similar to that induced by positive curvature. Biophys. J. 104, 585-593 (2013).
25. Vanni, S. et al. Amphipathic lipid packing sensor motifs: Probing bilayer defects with hydrophobic residues. Biophys. J. 104, 575-584 (2013).
26. Kamal, M. M., Mills, D., Grzybek, M. & Howard, J. Measurement of the membrane curvature preference of phospholipids reveals only weak coupling between lipid shape and leaflet curvature. Proc. Natl Acad. Sci. USA 106, 22245-22250 (2009).
27. Hope, M. J., Bally, M. B., Webb, G. & Cullis, P. R. Production of large unilamellar vesicles by a rapid extrusion procedure characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta. 812, 55-65 (1985).
28. Antonny, B. Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. (2010).
29. Gautier, R., Douguet, D., Antonny, B. & Drin, G. HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 24, 2101-2102 (2008).
30. Radoshevich, L. et al. ATG12 conjugation to ATG3 regulates mitochondrial homeostasis and cell death. Cell 142, 590-600 (2010).
31. Hanada, T. et al. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 282, 37298-37302 (2007).
32. Sakoh-Nakatogawa, M. et al. Atg12-Atg5 conjugate enhances E2 activity of Atg3 by rearranging its catalytic site. Nat. Struct. Mol. Biol. 20, 433-439 (2013).
33. Noda, N. N., Fujioka, Y., Hanada, T., Ohsumi, Y. & Inagaki, F. Structure of the Atg12-Atg5 conjugate reveals a platform for stimulating Atg8-PE conjugation. EMBO Rep. 14, 206-211 (2013).
34. Fujita, N. et al. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 19, 2092-2100 (2008).
35. Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (2004).
36. Hosokawa, N., Hara, Y. & Mizushima, N. Generation of cell lines with tetracycline-regulated autophagy and a role for autophagy in controlling cell size. FEBS Lett. 580, 2623-2629 (2006).
37. Kaufmann, A., Beier, V., Franquelim, H. G. & Wollert, T. Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell 156, 469-481 (2014).
38. Fujioka, Y. et al. In vitro reconstitution of plant Atg8 and Atg12 conjugation systems essential for autophagy. J. Biol. Chem. 283, 1921-1928 (2008).
39. Hanada, T., Satomi, Y., Takao, T. & Ohsumi, Y. The amino-terminal region of Atg3 is essential for association with phosphatidylethanolamine in Atg8 lipidation. FEBS Lett. 583, 1078-1083 (2009).
40. Pranke, I. M. et al. alpha-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding. J. Cell Biol. 194, 89-103 (2011).
41. Bigay, J., Casella, J. F., Drin, G., Mesmin, B. & Antonny, B. ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. EMBO J. 24, 2244-2253 (2005).
42. Sanjuan, M. A. et al. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257 (2007).
43. Yu, Z. Q. et al. Dual roles of Atg8-PE deconjugation by Atg4 in autophagy. Autophagy 8, (2012).
44. Nakatogawa, H., Ishii, J., Asai, E. & Ohsumi, Y. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy 8, 177-186 (2012).
45. Proikas-Cezanne, T. & Robenek, H. Freeze-fracture replica immunolabelling reveals human WIPI-1 and WIPI-2 as membrane proteins of autophagosomes. J. Cell. Mol. Med. 15, 2007-2010 (2011).
46. Mizushima, N., Yoshimori, T. & Ohsumi, Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107-132 (2011).
47. Ragusa, M. J., Stanley, R. E. & Hurley, J. H. Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 151, 1501-1512 (2012).
48. Helfrich, W. Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C 28, 693-703 (1973).
49. Jotwani, A., Richerson, D. N., Motta, I., Julca-Zevallos, O. & Melia, T. J. Approaches to the study of Atg8-mediated membrane dynamics in vitro. Methods Cell Biol. 108, 93-116 (2012).
50. Choy, A. et al. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science 338, 1072-1076 (2012).
51. Nair, U. et al. SNARE proteins are required for macroautophagy. Cell 146, 290-302 (2011).
52. Jotwani, A., Richerson, D. N., Motta, I., Julca-Zevallos, O. & Melia, T. J. Approaches to the study of Atg8-mediated membrane dynamics in vitro. Methods Cell Biol. 108, 93-116 (2012).
53. Melia, T. J. et al. Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158, 929-940 (2002).
54. Burnette, W. N. 'Western blotting': Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112, 195-203 (1981).