Membrane morphology is actively transformed by covalent binding of the protein Atg8 to PE-lipids

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Knorr, Roland L ^a   Nakatogawa, Hitoshi ^b   Ohsumi, Yoshinori ^b   Lipowsky, Reinhard ^a   Baumgart, Tobias ^c   Dimova, Rumiana ^a  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PHOSPHATIDYLETHANOLAMINE; PROTEIN ATG8; UNCLASSIFIED DRUG; ATG8 PROTEIN, S CEREVISIAE; LIPOSOME; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; AUTOPHAGOSOME; CELL ADHESION; CELL MEMBRANE; CELL SHAPE; CELL VACUOLE; CHEMICAL COMPOSITION; CONJUGATION; COVALENT BOND; LIPID MEMBRANE; MEMBRANE STRUCTURE; POSITIVE FEEDBACK; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; SURFACE PROPERTY;

LIPOSOMES; MICROTUBULE-ASSOCIATED PROTEINS; PHOSPHATIDYLETHANOLAMINES; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84919341595     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115357     Document Type: Article

References (37)

1. Yang ZF, Klionsky DJ (2010) Eaten alive: a history of macroautophagy. Nature Cell Biology 12: 814-822.
2. Mizushima N (2009) Physiological functions of autophagy. Curr Top Microbiol Immunol 335: 71-84.
3. Levine B, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132: 27-42.
4. Yamamoto H, Kakuta S, Watanabe TM, Kitamura A, Sekito T, et al. (2012) Atg9 vesicles are an important membrane source during early steps of autophagosome formation. Journal of Cell Biology 198: 219-233.
5. Mari M, Griffith J, Rieter E, Krishnappa L, Klionsky DJ, et al. (2010) An Atg9-containing compartment that functions in the early steps of autophagosome biogenesis. Journal of Cell Biology 190: 1005-1022.
6. Köchl R, Hu XW, Chan EYW, Tooze SA (2006) Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic 7: 129-145.
7. Knorr RL, Dimova R, Lipowsky R (2012) Curvature of Double-Membrane Organelles Generated by Changes in Membrane Size and Composition. Plos One 7.
8. Xie Z, Nair U, Klionsky DJ (2008) Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell 19: 3290-3298.
9. Ichimura Y, Imamura Y, Emoto K, Umeda M, Noda T, et al. (2004) In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. Journal of Biological Chemistry 279: 40584-40592.
10. Sakoh-Nakatogawa M, Matoba K, Asai E, Kirisako H, Ishii J, et al. (2013) Atg12-Atg5 conjugate enhances E2 activity of Atg3 by rearranging its catalytic site. Nat Struct Mol Biol 20: 433-439.
11. Nath S, Dancourt J, Shteyn V, Puente G, Fong WM, et al. (2014) Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nature Cell Biology 16: 415-424.
12. Romanov J, Walczak M, Ibiricu I, Schuchner S, Ogris E, et al. (2012) Mechanism and functions of membrane binding by the Atg5-Atg12/Atg16 complex during autophagosome formation. Embo Journal 31: 4304-4317.
13. Kaufmann A, Beier V, Franquelim HG, Wollert T (2014) Molecular mechanism of autophagic membrane-scaffold assembly and disassembly. Cell 156: 469-481.
14. Galush WJ, Nye JA, Groves JT (2008) Quantitative fluorescence microscopy using supported lipid bilayer standards. Biophysical Journal 95: 2512-2519.
15. Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J, et al. (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc Natl Acad Sci U S A 109: 173-178.
16. Xie ZP, Nair U, Geng JF, Szefler MB, Rothman ED, et al. (2009) Indirect estimation of the area density of Atg8 on the phagophore. Autophagy 5: 217-220.
17. Nair U, Jotwani A, Geng J, Gammoh N, Richerson D, et al. (2011) SNARE proteins are required for macroautophagy. Cell 146: 290-302.
18. Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130: 165-178.
19. Lipowsky R (1996) Adhesion of Membranes via Anchored Stickers. Phys Rev Lett 77: 1652-1655.
20. Nikolaus J, Stockl M, Langosch D, Volkmer R, Herrmann A (2010) Direct Visualization of Large and Protein-Free Hemifusion Diaphragms. Biophysical Journal 98: 1192-1199.
21. Lipowsky R (2013) Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discussions 161: 305-331.
22. Stachowiak JC, Schmid EM, Ryan CJ, Ann HS, Sasaki DY, et al. (2012) Membrane bending by protein-protein crowding. Nature Cell Biology 14: 944-949.
23. Baumgart T, Capraro BR, Zhu C, Das SL (2011) Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annu Rev Phys Chem 62: 483-506.
24. Capraro BR, Yoon Y, Cho W, Baumgart T (2010) Curvature sensing by the epsin N-terminal homology domain measured on cylindrical lipid membrane tethers. J Am Chem Soc 132: 1200-1201.
25. Hatzakis NS, Bhatia VK, Larsen J, Madsen KL, Bolinger PY, et al. (2009) How curved membranes recruit amphipathic helices and protein anchoring motifs. Nature Chemical Biology 5: 835-841.
26. S Nath JD, Puente G, Nag S, Yamamoto A, Antonny B, et al. (2013) The Lipidation Machinery Involved in Autophagosome Growth is Only Functional on Highly Curved Membranes. Biophysical Journal 104.
27. Nakatogawa H, Ishii J, Asai E, Ohsumi Y (2012) Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis. Autophagy 8: 177-186.
28. Nakatogawa H, Ohsumi Y (2012) SDS-PAGE techniques to study ubiquitin-like conjugation systems in yeast autophagy. Methods Mol Biol 832: 519-529.
29. Rauch J, Gumperz J, Robinson C, Skold M, Roy C, et al. (2003) Structural features of the acyl chain determine self-phospholipid antigen recognition by a CD1d-restricted invariant NKT (iNKT) cell. Journal of Biological Chemistry 278: 47508-47515.
30. Lai MZ, Vail WJ, Szoka FC (1985) Acid- and calcium-induced structural changes in phosphatidylethanolamine membranes stabilized by cholesteryl hemisuccinate. Biochemistry 24: 1654-1661.
31. Angelova MI, Dimitrov DS (1986) Liposome Electroformation. Faraday Discussions 81: 303-+.
32. Dimova R, Riske KA, Aranda S, Bezlyepkina N, Knorr RL, et al. (2007) Giant vesicles in electric fields. Soft Matter 3: 817-827.
33. Knorr RL, Staykova M, Gracia RS, Dimova R (2010) Wrinkling and electroporation of giant vesicles in the gel phase. Soft Matter 6: 1990-1996.
34. Waugh R, Evans EA (1979) Thermoelasticity of red blood cell membrane. Biophysical Journal 26: 115-131.
35. Tian A, Baumgart T (2009) Sorting of lipids and proteins in membrane curvature gradients. Biophysical Journal 96: 2676-2688.
36. Jensen MB, Bhatia VK, Jao CC, Rasmussen JE, Pedersen SL, et al. (2011) Membrane Curvature Sensing by Amphipathic Helices a single liposome study using a-synuclein and annexin B12. Journal of Biological Chemistry 286: 42603-42614.
37. Kunding AH, Mortensen MW, Christensen SM, Stamou D (2008) A fluorescence-based technique to construct size distributions from single-object measurements: Application to the extrusion of lipid vesicles. Biophysical Journal 95: 1176-1188.