Dynamics of autophagosome formation: A pulse and a sequence of waves

Biochemical Society Transactions

Volumn 42, Issue 5, 2014, Pages 1389-1395

  Ktistakis, Nicholas T ^a   Karanasios, Eleftherios ^a   Manifava, Maria ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

Autophagy; Mammalian (or mechanistic) target of rapamycin complex 1 (mTORC1); Phosphatidylinositol 3 phosphate (PI3P); Phosphoinositide; Unc 51 like kinase (ULK) complex; Vacuolar protein sorting 34 (VPS34) complex I

Indexed keywords

AUTOPHAGOSOME; AUTOPHAGY; CELL MEMBRANE; CELL ORGANELLE; ENDOPLASMIC RETICULUM; HUMAN; MAMMAL CELL; PROTEIN ASSEMBLY; REVIEW; ANIMAL; BIOLOGICAL MODEL; EUKARYOTIC CELL; KINETICS; METABOLISM; PHAGOSOME; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; EUKARYOTIC CELLS; HUMANS; KINETICS; MODELS, BIOLOGICAL; PHAGOSOMES; SIGNAL TRANSDUCTION;

EID: 84907195506     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20140183     Document Type: Review

References (62)

1. Mizushima, N. (2007) Autophagy: process and function. Genes Dev. 21, 2861-2873 CrossRef PubMed
2. Devenish, R.J. and Klionsky, D.J. (2012) Autophagy: mechanism and physiological relevance 'brewed' from yeast studies. Front Biosci. (Schol. Ed.) 4, 1354-1363 CrossRef PubMed
3. Nakatogawa, H., Suzuki, K., Kamada, Y. and Ohsumi, Y. (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 10, 458-467 CrossRef PubMed
4. 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
5. Levine, B. and Klionsky, D.J. (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463-477 CrossRef PubMed
6. Mizushima, N., Levine, B., Cuervo, A.M. and Klionsky, D.J. (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 CrossRef PubMed
7. Yang, Z. and Klionsky, D.J. (2010) Eaten alive: a history of macroautophagy. Nat. Cell Biol. 12, 814-822 CrossRef PubMed
8. Eskelinen, E.L., Reggiori, F., Baba, M., Kovacs, A.L. and Seglen, P.O. (2011) Seeing is believing: the impact of electron microscopy on autophagy research. Autophagy 7, 935-956 CrossRef PubMed
9. Dunn, Jr, W.A., Schroeder, L.A. and Aris, J.P. (2013) Historical overview of autophagy. Curr. Cancer Res. 8, 1-24
10. Tooze, S.A. and Yoshimori, T. (2010) The origin of the autophagosomal membrane. Nat. Cell Biol. 12, 831-835 CrossRef PubMed
11. Shibutani, S.T. and Yoshimori, T. (2014) A current perspective of autophagosome biogenesis. Cell Res. 24, 58-68 CrossRef PubMed
12. 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
13. Rubinsztein, D.C., Shpilka, T. and Elazar, Z. (2012) Mechanisms of autophagosome biogenesis. Curr. Biol. 22, R29-R34 CrossRef PubMed
14. Weidberg, H., Shvets, E. and Elazar, Z. (2011) Biogenesis and cargo selectivity of autophagosomes. Annu. Rev. Biochem. 80, 125-156 CrossRef PubMed
15. Efeyan, A., Zoncu, R. and Sabatini, D.M. (2012) Amino acids and mTORC1: from lysosomes to disease. Trends Mol. Med. 18, 524-533 CrossRef PubMed
16. Russell, R.C., Yuan, H.X. and Guan, K.L. (2014) Autophagy regulation by nutrient signaling. Cell Res. 24, 42-57 CrossRef PubMed
17. Chan, E.Y. (2009) mTORC1 phosphorylates the ULK1-mAtg13-FIP200 autophagy regulatory complex. Sci. Signal 2, pe51 CrossRef PubMed
18. Burman, C. and Ktistakis, N.T. (2010) Autophagosome formation in mammalian cells. Semin. Immunopathol. 32, 397-413 CrossRef PubMed
19. 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
20. Codogno, P., Mehrpour, M. and Proikas-Cezanne, T. (2011) Canonical and non-canonical autophagy: variations on a common theme of self-eating? Nat. Rev. Mol. Cell Biol. 13, 7-12
21. Moreau, K. and Rubinsztein, D.C. (2012) The plasma membrane as a control center for autophagy. Autophagy 8, 861-863 CrossRef PubMed
22. Shimizu, S., Honda, S., Arakawa, S. and Yamaguchi, H. (2014) Alternative macroautophagy and mitophagy. Int. J. Biochem. Cell Biol. 50, 64-66 CrossRef PubMed
23. Bodemann, B.O., Orvedahl, A., Cheng, T., Ram, R.R., Ou, Y.H., Formstecher, E., Maiti, M., Hazelett, C.C., Wauson, E.M., Balakireva, M. et al. (2011) RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 144, 253-267 CrossRef PubMed
24. Yang, Z. and Klionsky, D.J. (2010) Mammalian autophagy: core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22, 124-131 CrossRef PubMed
25. Wong, P.M., Puente, C., Ganley, I.G. and Jiang, X. (2013) The ULK1 complex: sensing nutrient signals for autophagy activation. Autophagy 9, 124-137 CrossRef PubMed
26. Kim, J. and Guan, K.L. (2011) Amino acid signaling in TOR activation. Annu. Rev. Biochem. 80, 1001-1032 CrossRef PubMed
27. McKnight, N.C. and Zhenyu, Y. (2013) Beclin 1, an essential component and master regulator of PI3K-III in health and disease. Curr. Pathobiol. Rep. 1, 231-238 CrossRef PubMed
28. Yuan, H.X., Russell, R.C. and Guan, K.L. (2013) Regulation of PIK3C3/VPS34 complexes by MTOR in nutrient stress-induced autophagy. Autophagy 9, 1983-1995 CrossRef PubMed
29. Furuya, T., Kim, M., Lipinski, M., Li, J., Kim, D., Lu, T., Shen, Y., Rameh, L., Yankner, B., Tsai, L.H. and Yuan, J. (2010) Negative regulation of Vps34 by Cdk mediated phosphorylation. Mol. Cell 38, 500-511 CrossRef PubMed
30. Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N.T., Izumi, T., Noda, T. and Yoshimori, T. (2010) Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 190, 511-521 CrossRef PubMed
31. Roberts, R. and Ktistakis, N.T. (2013) Omegasomes: PI3P platforms that manufacture autophagosomes. Essays Biochem. 55, 17-27 CrossRef PubMed
32. Yla-Anttila, P., Vihinen, H., Jokitalo, E. and Eskelinen, E.L. (2009) 3D tomography reveals connections between the phagophore and endoplasmic reticulum. Autophagy 5, 1180-1185 CrossRef PubMed
33. 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
34. Uemura, T., Yamamoto, M., Kametaka, A., Sou, Y.S., Yabashi, A., Yamada, A., Annoh, H., Kametaka, S., Komatsu, M. and Waguri, S. (2014) A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane. Mol. Cell. Biol. 34, 1695-1706 CrossRef PubMed
35. Duke, E.M., Razi, M., Weston, A., Guttmann, P., Werner, S., Henzler, K., Schneider, G., Tooze, S.A. and Collinson, L.M. (2014) Imaging endosomes and autophagosomes in whole mammalian cells using correlative cryo-fluorescence and cryo-soft X-ray microscopy (cryo-CLXM). Ultramicroscopy 143, 77-87 CrossRef PubMed
36. 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
37. Dooley, H.C., Razi, M., Polson, H.E., 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
38. Suzuki, K., Kubota, Y., Sekito, T. and Ohsumi, Y. (2007) Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells 12, 209-218 CrossRef PubMed
39. Itakura, E. and Mizushima, N. (2010) Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy 6, 764-776 CrossRef PubMed
40. 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
41. 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
42. Hamasaki, M., Furuta, N., Matsuda, A., Nezu, A., Yamamoto, A., Fujita, N., Oomori, H., Noda, T., Haraguchi, T., Hiraoka, Y., Amano, A. and Yoshimori, T. (2013) Autophagosomes form at ER-mitochondria contact sites. Nature 495, 389-393 CrossRef PubMed
43. Karanasios, E., Stapleton, E., Walker, S.A., Manifava, M. and Ktistakis, N.T. (2013) Live cell imaging of early autophagy events: omegasomes and beyond. J. Vis. Exp., doi:10.3791/50484 CrossRef PubMed
44. Mari, M., Griffith, J., Rieter, E., Krishnappa, L., Klionsky, D.J. and Reggiori, F. (2010) An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. J. Cell Biol. 190, 1005-1022 CrossRef PubMed
45. Orsi, A., Razi, M., Dooley, H.C., Robinson, D., Weston, A.E., Collinson, L.M. and Tooze, S.A. (2012) Dynamic and transient interactions of Atg9 with autophagosomes, but not membrane integration, are required for autophagy. Mol. Biol. Cell 23, 1860-1873 CrossRef PubMed
46. Reggiori, F. and Tooze, S.A. (2012) Autophagy regulation through Atg9 traffic. J. Cell Biol. 198, 151-153 CrossRef PubMed
47. Graef, M., Friedman, J.R., Graham, C., Babu, M. and Nunnari, J. (2013) ER exit sites are physical and functional core autophagosome biogenesis components. Mol. Biol. Cell 24, 2918-2931 CrossRef PubMed
48. Ktistakis, N.T., Andrews, S. and Long, J. (2011) What is the advantage of a transient precursor in autophagosome biogenesis? Autophagy 7, 118-122 CrossRef PubMed
49. Ktistakis, N.T., Kao, C.Y. and Lang, D. (1988) In vitro assembly of the outer shell of bacteriophage phi 6 nucleocapsid. Virology 166, 91-102 CrossRef PubMed
50. Hurley, J.H. and Schulman, B.A. (2014) Atomistic autophagy: the structures of cellular self-digestion. Cell 157, 300-311 CrossRef PubMed
51. Chew, L.H. and Yip, C.K. (2014) Structural biology of the macroautophagy machinery. Front. Biol. 9, 18-34 CrossRef
52. Miller, S., Tavshanjian, B., Oleksy, A., Perisic, O., Houseman, B.T., Shokat, K.M. and Williams, R.L. (2010) Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327, 1638-1642 CrossRef PubMed
53. Krick, R., Busse, R.A., Scacioc, A., Stephan, M., Janshoff, A., Thumm, M. and Kuhnel, 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
54. 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
55. Pelham, H.R. (1994) About turn for the COPs? Cell 79, 1125-1127 CrossRef PubMed
56. Pelham, H.R. and Rothman, J.E. (2000) The debate about transport in the Golgi: two sides of the same coin? Cell 102, 713-719 CrossRef PubMed
57. Papanikou, E. and Glick, B.S. (2014) Golgi compartmentation and identity. Curr. Opin. Cell Biol. 29C, 74-81 CrossRef PubMed
58. Young, A.R., Chan, E.Y., Hu, X.W., Kochl, R., Crawshaw, S.G., High, S., Hailey, D.W., Lippincott-Schwartz, J. and Tooze, S.A. (2006) Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119, 3888-3900 CrossRef PubMed
59. Martin, K.R., Barua, D., Kauffman, A.L., Westrate, L.M., Posner, R.G., Hlavacek, W.S. and Mackeigan, J.P. (2013) Computational model for autophagic vesicle dynamics in single cells. Autophagy 9, 74-92 CrossRef PubMed
60. 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. Nat. Cell Biol. 16, 415-424 CrossRef PubMed
61. Ge, L., Melville, D., Zhang, M. and Schekman, R. (2013) The ER-Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis. eLife 2, e00947 CrossRef PubMed
62. Kaufmann, A., Beier, V., Franquelim, H.G. and Wollert, T. (2014) Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell 156, 469-481 CrossRef PubMed