ER–plasma membrane contact sites contribute to autophagosome biogenesis by regulation of local PI3P synthesis

EMBO Journal

Volumn 36, Issue 14, 2017, Pages 2018-2033

  Nascimbeni, Anna Chiara ^a,b   Giordano, Francesca ^b,c   Dupont, Nicolas ^a,b   Grasso, Daniel ^d   Vaccaro, Maria I ^d   Codogno, Patrice ^a,b   Morel, Etienne ^a,b  

^a INSTITUT NECKER ENFANTS MALADES   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CNRS   (France)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

autophagosome; contact sites; extended synaptotagmins; organelle biogenesis; PI3P

Indexed keywords

AUTOPHAGY RELATED PROTEIN 12; BAFILOMYCIN A1; BECLIN 1; BINDING PROTEIN; CALNEXIN; MITOCHONDRIAL PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN SERINE THREONINE KINASE VPS15; SYNAPTOTAGMIN; SYNAPTOTAGMIN II; SYNTAXIN; SYNTAXIN 17; UNCLASSIFIED DRUG; CARRIER PROTEIN; MEMBRANE PROTEIN; POLYPHOSPHOINOSITIDE; VMP1 PROTEIN, HUMAN; ZFYVE1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BINDING AFFINITY; BIOGENESIS; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM MEMBRANE; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; ANIMAL; DOG; ENDOPLASMIC RETICULUM; HELA CELL LINE; MDCK CELL LINE; METABOLISM; ORGANELLE BIOGENESIS;

ANIMALS; AUTOPHAGOSOMES; CARRIER PROTEINS; CELL MEMBRANE; DOGS; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE PROTEINS; ORGANELLE BIOGENESIS; PHOSPHATIDYLINOSITOL PHOSPHATES; SYNAPTOTAGMINS;

EID: 85019885623     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201797006     Document Type: Article

References (52)

1. Alers S, Loffler AS, Wesselborg S, Stork B (2012) The incredible ULKs. Cell Commun Signal 10: 7
2. Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182: 685–701
3. Boya P, Reggiori F, Codogno P (2013) Emerging regulation and functions of autophagy. Nat Cell Biol 15: 713–720
4. Calvo-Garrido J, King JS, Muñoz-Braceras S, Escalante R (2014) Vmp1 regulates PtdIns3P signaling during autophagosome formation in Dictyostelium discoideum. Traffic 15: 1235–1246
5. Carlos Martín Zoppino F, Damián Militello R, Slavin I, Álvarez C, Colombo MI (2010) Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic 11: 1246–1261
6. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651–657
7. Dooley HC, Razi M, Polson HEJ, Girardin SE, Wilson MI, Tooze SA (2014) WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell 55: 238–252
8. Dupont N, Chauhan S, Arko-Mensah J, Castillo EF, Masedunskas A, Weigert R, Robenek H, Proikas-Cezanne T, Deretic V (2014) Neutral lipid stores and lipase PNPLA5 contribute to autophagosome biogenesis. Curr Biol 24: 609–620
9. Elbaz Y, Schuldiner M (2011) Staying in touch: the molecular era of organelle contact sites. Trends Biochem Sci 36: 616–623
10. Fernández-Busnadiego R, Saheki Y, De Camilli P (2015) Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. Proc Natl Acad Sci USA 112: E2004–E2013
11. Friedman JR, Voeltz GK (2011) The ER in 3D: a multifunctional dynamic membrane network. Trends Cell Biol 21: 709–717
12. Ge L, Melville D, Zhang M, Schekman R (2013) The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. Elife 2: e00947
13. Geng J, Nair U, Yasumura-Yorimitsu K, Klionsky DJ (2010) Post-Golgi Sec proteins are required for autophagy in Saccharomyces cerevisiae. Mol Biol Cell 21: 2257–2269
14. Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153: 1494–1509
15. Gomez-Suaga P, Paillusson S, Stoica R, Noble W, Hanger DP, Miller CCJ (2017) The ER-mitochondria tethering complex VAPB-PTPIP51 regulates autophagy. Curr Biol 27: 371–385
16. Graef M, Friedman JR, Graham C, Babu M, Nunnari J (2013) ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell 24: 2918–2931
17. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141: 656–667
18. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, Amano A, Yoshimori T (2013) Autophagosomes form at ER-mitochondria contact sites. Nature 495: 389–393
19. Helle SCJ, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B (2013) Organization and function of membrane contact sites. Biochim Biophys Acta 1833: 2526–2541
20. Itakura E, Kishi C, Inoue K, Mizushima N (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19: 5360–5372
21. Itakura E, Mizushima N (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6: 764–776
22. Khaldoun SA, Emond-Boisjoly M-A, Chateau D, Carrière V, Lacasa M, Rousset M, Demignot S, Morel E (2014) Autophagosomes contribute to intracellular lipid distribution in enterocytes. Mol Biol Cell 25: 118–132
23. Kimura S, Noda T, Yoshimori T (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3: 452–460
24. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, Adhihetty PJ, Adler SG, Agam G, Agarwal R, Aghi MK, Agnello M, Agostinis P, Aguilar PV, Aguirre-Ghiso J, Airoldi EM et al (2016) Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12: 1–222
25. Lamb CA, Yoshimori T, Tooze SA (2013) The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 14: 759–774
26. Levine B, Liu R, Dong X, Zhong Q (2015) Beclin orthologs: integrative hubs of cell signaling, membrane trafficking, and physiology. Trends Cell Biol 25: 533–544
27. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402: 672–676
28. Liou J, Chang CL (2015) Unveiling physiological functions of extended synaptotagmins. Cell Cycle 14: 799–800
29. Marat AL, Haucke V (2016) Phosphatidylinositol 3-phosphates-at the interface between cell signalling and membrane traffic. EMBO J 35: 561–579
30. Molejon MI, Ropolo A, Lo Re A, Boggio V, Vaccaro MI (2013a) The VMP1-Beclin 1 interaction regulates autophagy induction. Sci Rep 3: 1055
31. Molejon MI, Ropolo A, Vaccaro MI (2013b) VMP1 is a new player in the regulation of the autophagy-specific phosphatidylinositol 3-kinase complex activation. Autophagy 9: 933–935
32. Molino D, Zemirli N, Codogno P, Morel E (2017) The journey of the autophagosome through mammalian cell organelles and membranes. J Mol Biol 429: 497–514
33. Nascimbeni AC, Codogno P, Morel E (2017) Phosphatidylinositol-3-phosphate in the regulation of autophagy membrane dynamics. FEBS J 284: 1267–1278
34. Orhon I, Dupont N, Zaidan M, Boitez V, Burtin M, Schmitt A, Capiod T, Viau A, Beau I, Wolfgang Kuehn E, Friedlander G, Terzi F, Codogno P (2016) Primary-cilium-dependent autophagy controls epithelial cell volume in response to fluid flow. Nat Cell Biol 18: 657–667
35. Pérez-Lara Á, Jahn R (2015) Extended synaptotagmins (E-Syts): architecture and dynamics of membrane contact sites revealed. Proc Natl Acad Sci USA 112: 4837–4838
36. Polson HEJ, de Lartigue J, Rigden DJ, Reedijk M, Urbé S, Clague MJ, Tooze SA (2010) Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6: 506–522
37. Powis G, Bonjouklian R, Berggren MM, Gallegos A, Abraham R, Ashendel C, Zalkow L, Matter WF, Dodge J, Grindey G (1994) Wortmannin, a potent and selective inhibitor of phosphatidylinositol-3-kinase. Cancer Res 54: 2419–2423
38. Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC (2013) Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 154: 1285–1299
39. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC (2010a) Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 12: 747–757
40. Ravikumar B, Moreau K, Rubinsztein DC (2010b) Plasma membrane helps autophagosomes grow. Autophagy 6: 1184–1186
41. Roberts R, Ktistakis NT (2013) Omegasomes: PI3P platforms that manufacture autophagosomes. Essays Biochem 55: 17–27
42. Rubinsztein DC, Shpilka T, Elazar Z (2012) Mechanisms of autophagosome biogenesis. Curr Biol 22: R29–R34
43. Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F, Wenk MR, De Camilli P, Reinisch KM (2014) Structure of a lipid-bound extended synaptotagmin indicates a role in lipid transfer. Nature 510: 552–555
44. Seaman MN, McCaffery JM, Emr SD (1998) A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol 142: 665–681
45. Shibata Y, Voss C, Rist JM, Hu J, Rapoport TA, Prinz WA, Voeltz GK (2008) The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J Biol Chem 283: 18892–18904
46. Shpilka T, Welter E, Borovsky N, Amar N, Mari M, Reggiori F, Elazar Z (2015) Lipid droplets and their component triglycerides and steryl esters regulate autophagosome biogenesis. EMBO J 34: 2117–2131
47. Slot JW, Geuze HJ (2007) Cryosectioning and immunolabeling. Nat Protoc 2: 2480–2491
48. Stefan CJ, Manford AG, Emr SD (2013) ER-PM connections: sites of information transfer and inter-organelle communication. Curr Opin Cell Biol 25: 434–442
49. Sun Q, Fan W, Chen K, Ding X, Chen S, Zhong Q (2008) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 105: 19211–19216
50. Tábara L-C, Escalante R (2016) VMP1 establishes ER-microdomains that regulate membrane contact sites and autophagy. PLoS One 11: e0166499
51. Tooze SA (2013) Current views on the source of the autophagosome membrane. Essays Biochem 55: 29–38
52. Wilson MII, Dooley HCC, Tooze SAA (2014) WIPI2b and Atg16L1: setting the stage for autophagosome formation. Biochem Soc Trans 42: 1327–1334