The em structure of the TRAPPIII complex leads to the identification of a requirement for COPII vesicles on the macroautophagy pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 48, 2013, Pages 19432-19437

  Tan, Dongyan ^a,b   Cai, Yiying ^c   Wang, Juan ^d,e   Zhang, Jinzhong ^d,e   Menon, Shekar ^d,e,f   Chou, Hui Ting ^a,b   Ferro Novick, Susan ^d,e   Reinisch, Karin M ^c   Walz, Thomas ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Affymetric Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; COAT PROTEIN COMPLEX II; SNARE PROTEIN; TRANSPORT PROTEIN PARTICLE I COMPLEX; TRANSPORT PROTEIN PARTICLE III COMPLEX; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHAGOSOME; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENZYME BINDING; ESCHERICHIA COLI; FLUORESCENCE; MACROAUTOPHAGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

ANIMALS; AUTOPHAGY; CERCOPITHECUS AETHIOPS; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; COP-COATED VESICLES; COS CELLS; ELECTROPORATION; ESCHERICHIA COLI; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84888350190     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316356110     Document Type: Article

References (48)

1. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y (2009) Dynamics and diversity in autophagy mechanisms: Lessons from yeast. Nat Rev Mol Cell Biol 10(7): 458-467.
2. Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451(7182): 1069-1075.
3. Tooze SA, Yoshimori T (2010) The origin of the autophagosomal membrane. Nat Cell Biol 12(9): 831-835.
4. Yamamoto H, et al. (2012) Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol 198(2): 219-233.
5. Meijer WH, van der Klei IJ, Veenhuis M, Kiel JA (2007) ATG genes involved in nonselective autophagy are conserved from yeast to man, but the selective Cvt and pexophagy pathways also require organism-specific genes. Autophagy 3(2): 106-116.
6. Kabeya Y, et al. (2009) Characterization of the Atg17-Atg29-Atg31 complex specifically required for starvation-induced autophagy in Saccharomyces cerevisiae. Biochem Biophys Res Commun 389(4): 612-615.
7. Suzuki K, Kubota Y, Sekito T, Ohsumi Y (2007) Hierarchy of Atg proteins in preautophagosomal structure organization. Genes Cells 12(2): 209-218.
8. Lynch-Day MA, et al. (2010) Trs85 directs a Ypt1 GEF, TRAPPIII, to the phagophore to promote autophagy. Proc Natl Acad Sci USA 107(17): 7811-7816.
9. Wang J, et al. (2013) Ypt1 recruits the Atg1 kinase to the preautophagosomal structure. Proc Natl Acad Sci USA 110(24): 9800-9805.
10. Barrowman J, Bhandari D, Reinisch K, Ferro-Novick S (2010) TRAPP complexes in membrane traffic: Convergence through a common Rab. Nat RevMol Cell Biol 11(11): 759-763.
11. Cai Y, et al. (2008) The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 133(7): 1202-1213.
12. Kim YG, et al. (2006) The architecture of the multisubunit TRAPP I complex suggests a model for vesicle tethering. Cell 127(4): 817-830.
13. Lord C, et al. (2011) Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473(7346): 181-186.
14. Hamasaki M, et al. (2013) Autophagosomes form at ER-mitochondria contact sites. Nature 495(7441): 389-393.
15. Radermacher M (1988) Three-dimensional reconstruction of single particles from random and nonrandom tilt series. J Electron Microsc Tech 9(4): 359-394.
16. Gedeon AK, et al. (1999) Identification of the gene (SEDL) causing X-linked spondyloepiphyseal dysplasia tarda. Nat Genet 22(4): 400-404.
17. Gedeon AK, et al. (2001) The molecular basis of X-linked spondyloepiphyseal dysplasia tarda. Am J Hum Genet 68(6): 1386-1397.
18. Zong M, et al. (2011) The adaptor function of TRAPPC2 in mammalian TRAPPs explains TRAPPC2-associated SEDT and TRAPPC9-associated congenital intellectual disability. PLoS ONE 6(8):e23350.
19. Klionsky DJ (2007) Monitoring autophagy in yeast: The Pho8Delta60 assay. Methods Mol Biol 390: 363-371.
20. Yip CK, Berscheminski J, Walz T (2010) Molecular architecture of the TRAPPII complex and implications for vesicle tethering. Nat Struct Mol Biol 17(11): 1298-1304.
21. Taussig D, Lipatova Z, Kim JJ, Zhang X, Segev N (2013) Trs20 is required for TRAPP II assembly. Traffic 14(6): 678-690.
22. Lee MC, Miller EA, Goldberg J, Orci L, Schekman R (2004) Bi-directional protein transport between the ER and Golgi. Annu Rev Cell Dev Biol 20: 87-123.
23. Zanetti G, Pahuja KB, Studer S, Shim S, Schekman R (2012) COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14(1): 20-28.
24. Cai H, et al. (2007) TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 445(7130): 941-944.
25. Sacher M, et al. (2001) TRAPP I implicated in the specificity of tethering in ER-to-Golgi transport. Mol Cell 7(2): 433-442.
26. Bassik MC, et al. (2013) A systematic mammalian genetic interaction map reveals pathways underlying ricin susceptibility. Cell 152(4): 909-922.
27. Suzuki K, Akioka M, Kondo-Kakuta C, Yamamoto H, Ohsumi Y (2013) Fine mapping of autophagy-related proteins during autophagosome formation in Saccharomyces cerevisiae. J Cell Sci 126(Pt 11): 2534-2544.
28. GraefM, Friedman JR, Graham C, Babu M, Nunnari J (2013) ER exit sites are physical and functional core autophagosome biogenesis components. Mol Biol Cell 24(18): 2918-2931.
29. Kawamata T, Kamada Y, Kabeya Y, Sekito T, Ohsumi Y (2008) Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 19(5): 2039-2050.
30. Ragusa MJ, Stanley RE, Hurley JH (2012) Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell 151(7): 1501-1512.
31. Kamada Y, et al. (2000) Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150(6): 1507-1513.
32. Cao X, Ballew N, Barlowe C (1998) Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins. EMBO J 17(8): 2156-2165.
33. Ishihara N, et al. (2001) Autophagosome requires specific early Sec proteins for its formation and NSF/SNARE for vacuolar fusion. Mol Biol Cell 12(11): 3690-3702.
34. Novick P, Field C, Schekman R (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21(1): 205-215.
35. Lian JP, Ferro-Novick S (1993) Bos1p, an integral membrane protein of the endoplasmic reticulum to Golgi transport vesicles, is required for their fusion competence. Cell 73(4): 735-745.
36. Barlowe C, et al. (1994) COPII: A membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77(6): 895-907.
37. Cao X, Barlowe C (2000) Asymmetric requirements for a Rab GTPase and SNARE proteins in fusion of COPII vesicles with acceptor membranes. J Cell Biol 149(1): 55-66.
38. 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(13): 2257-2269.
39. Nair U, et al. (2011) SNARE proteins are required for macroautophagy. Cell 146(2): 290-302.
40. 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.
41. Puig O, et al. (2001) The tandem affinity purification (TAP) method: A general procedure of protein complex purification. Methods 24(3): 218-229.
42. Wang W, Sacher M, Ferro-Novick S (2000) TRAPP stimulates guanine nucleotide exchange on Ypt1p. J Cell Biol 151(2): 289-296.
43. Hailey DW, et al. (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141(4): 656-667.
44. Ohi M, Li Y, Cheng Y, Walz T (2004) Negative staining and image classification - powerful tools in modern electron microscopy. Biol Proced Online 6: 23-34.
45. Li Z, Hite RK, Cheng Y, Walz T (2010) Evaluation of imaging plates as recording medium for images of negatively stained single particles and electron diffraction patterns of two-dimensional crystals. J Electron Microsc (Tokyo) 59(1): 53-63.
46. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116(1): 190-199.
47. Böttcher B, Wynne SA, Crowther RA (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386(6620): 88-91.
48. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128(1): 82-97.