Subtomogram averaging of COPII assemblies reveals how coat organization dictates membrane shape

Nature Communications

Volumn 9, Issue 1, 2018, Pages

  Hutchings, Joshua ^a   Stancheva, Viktoriya ^b   Miller, Elizabeth A ^b   Zanetti, Giulia ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL COMPONENT; CELL ORGANELLE; EUKARYOTE; MEMBRANE; MOLECULAR ANALYSIS; PROTEIN; SECRETION; SHAPE;

EUKARYOTA;

CARRIER PROTEIN; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL; CELL MEMBRANE; CHEMISTRY; COP-COATED VESICLE; CRYOELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; ENDOPLASMIC RETICULUM; GENETICS; METABOLISM; PROTEIN TRANSPORT; SF9 CELL LINE; SPODOPTERA; ULTRASTRUCTURE;

ANIMALS; CELL MEMBRANE; COP-COATED VESICLES; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; ENDOPLASMIC RETICULUM; MEMBRANE TRANSPORT PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE PROTEINS; SF9 CELLS; SPODOPTERA;

EID: 85054559719     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-018-06577-4     Document Type: Article

References (31)

1. Barlowe, C. et al. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895–907 (1994).
2. Zanetti, G., Pahuja, K. B., Studer, S., Shim, S. & Schekman, R. COPII and the regulation of protein sorting in mammals. Nat. Cell Biol. 14, 20–28 (2012).
3. Lee, M. C. S. et al. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle. Cell 122, 605–617 (2005).
4. Zanetti, G. et al. The structure of the COPII transport-vesicle coat assembled on membranes. eLife 2, e00951 (2013).
5. Stagg, S. M. et al. Structure of the Sec13/31 COPII coat cage. Nature 439, 234–238 (2006).
6. Stagg, S. M. et al. Structural basis for cargo regulation of COPII coat assembly. Cell 134, 474–484 (2008).
7. Antonny, B., Madden, D., Hamamoto, S., Orci, L. & Schekman, R. Dynamics of the COPII coat with GTP and stable analogues. Nat. Cell Biol. 3, 531–537 (2001).
8. Bi, X., Mancias, J. D. & Goldberg, J. Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31. Dev. Cell 13, 635–645 (2007).
9. Ma, W. & Goldberg, J. TANGO1/cTAGE5 receptor as a polyvalent template for assembly of large COPII coats. Proc. Natl. Acad. Sci. USA 113, 10061–10066 (2016).
10. Whittle, J. R. R. & Schwartz, T. U. Structure of the Sec13-Sec16 edge element, a template for assembly of the COPII vesicle coat. J. Cell Biol. 190, 347–361 (2010).
11. Supek, F., Madden, D. T., Hamamoto, S., Orci, L. & Schekman, R. Sec16p potentiates the action of COPII proteins to bud transport vesicles. J. Cell Biol. 158, 1029–1038 (2002).
12. Saito, K., Maeda, M. & Katada, T. Regulation of the Sar1 GTPase cycle is necessary for large cargo secretion from the endoplasmic reticulum. Front. Cell Dev. Biol. 5, 75 (2017).
13. Bacia, K. et al. Multibudded tubules formed by COPII on artificial liposomes. Sci. Rep. 1, 17 (2011).
14. Fromme, J. C. et al. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell 13, 623–634 (2007).
15. Bi, X., Corpina, R. A. & Goldberg, J. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419, 271–277 (2002).
16. Kim, D. E., Chivian, D. & Baker, D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32, W526–W531 (2004).
17. McMahon, H. T. & Gallop, J. L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596 (2005).
18. Malhotra, V. & Erlmann, P. The pathway of collagen secretion. Annu. Rev. Cell. Dev. Biol. 31, 109–124 (2015).
19. Saito, K. et al. Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export. J. Cell. Biol. 206, 751–762 (2014).
20. Kung, L. F. et al. Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO J. 31, 1014–1027 (2012).
21. Matsuoka, K. et al. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93, 263–275 (1998).
22. Hagen, W. J. H., Wan, W. & Briggs, J. A. G. Implementation of a cryo-electron tomography tilt-scheme optimized for high resolution subtomogram averaging. J. Struct. Biol. 197, 191–198 (2017).
23. Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
24. Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
25. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71–76 (1996).
26. Grant, T. & Grigorieff, N. Measuring the optimal exposure for single particle cryo-EM using a 2.6 Å reconstruction of rotavirus VP6. eLife 4, e06980 (2015).
27. Rohou, A. & Grigorieff, N. CTFFIND4: Fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
28. Turoňová, B., Schur, F. K. M., Wan, W. & Briggs, J. A. G. Efficient 3D-CTF correction for cryo-electron tomography using NovaCTF improves subtomogram averaging resolution to 3.4Å. J. Struct. Biol. 199, 187–195 (2017).
29. Castaño-Díez, D., Kudryashev, M., Arheit, M. & Stahlberg, H. Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J. Struct. Biol. 178, 139–151 (2012).
30. Scheres, S. H. W. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).
31. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).