A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae

Molecular and Cellular Proteomics

Volumn 10, Issue 6, 2011, Pages

  Dokudovskaya, Svetlana ^a   Waharte, Francois ^b   Schlessinger, Avner ^c   Pieper, Ursula ^c   Devos, Damien P ^d   Cristea, Ileana M ^e   Williams, Rosemary ^f   Salamero, Jean ^b   Chait, Brian T ^f   Sali, Andrej ^c   Field, Mark C ^g   Rout, Michael P ^d,f   Dargemont, Catherine ^a,d  

^a INSTITUT JACQUES MONOD   (France)

^b INSTITUT CURIE   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e PRINCETON UNIVERSITY   (United States)

^f ROCKEFELLER UNIVERSITY   (United States)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COATOMER COMPLEX I; COATOMER COMPLEX II; COATOMER PROTEIN; FUNGAL PROTEIN; NITROGEN; NPR2 PROTEIN; NPR3 PROTEIN; NUCLEOPORIN; PHOSPHOTRANSFERASE; REGULATOR PROTEIN; SEC13 PROTEIN; SEH1 ASSOCIATED PROTEIN; SEH1 ASSOCIATED PROTEIN 1; SEH1 ASSOCIATED PROTEIN 4; SEH1 PROTEIN; TORC1 KINASE; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; SACCHAROMYCES CEREVISIAE PROTEIN; SEC13 PROTEIN, S CEREVISIAE; SEH1 PROTEIN, S CEREVISIAE;

ARTICLE; AUTOPHAGY; BIOCHEMISTRY; BIOGENESIS; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; FUNGAL CELL; GENETIC ANALYSIS; IN VIVO STUDY; NONHUMAN; NUCLEAR PORE COMPLEX; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; CELL FRACTIONATION; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANE; METABOLISM; PHENOTYPE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; STRUCTURAL HOMOLOGY;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

AUTOPHAGY; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANES; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEAR PORE COMPLEX PROTEINS; PHENOTYPE; PHYLOGENY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; SUBCELLULAR FRACTIONS; VACUOLES;

EID: 79957971892     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.006478     Document Type: Article

References (76)

1. Dacks, J. B., and Field, M. C. (2007) Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J. Cell Sci. 120, 2977-2985
2. DeGrasse, J. A., DuBois, K. N., Devos, D., Siegel, T. N., Sali, A., Field, M. C., Rout, M. P., and Chait, B. T. (2009) Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol. Cell Proteomics 8, 2119-2130
3. Devos, D., Dokudovskaya, S., Alber, F., Williams, R., Chait, B. T., Sali, A., and Rout, M. P. (2004) Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol. 2, e380
4. Devos, D., Dokudovskaya, S., Williams, R., Alber, F., Eswar, N., Chait, B. T., Rout, M. P., and Sali, A. (2006) Simple fold composition and modular architecture of the nuclear pore complex. Proc. Natl. Acad. Sci. U.S.A. 103, 2172-2177
5. Lee, C., and Goldberg, J. (2010) Structure of Coatomer Cage Proteins and the Relationship among COPI, COPII, and Clathrin Vesicle Coats. Cell 142, 123-132
6. Bonifacino, J. S., and Glick, B. S. (2004) The mechanisms of vesicle budding and fusion. Cell 116, 153-166 (Pubitemid 38167309)
7. Gürkan, C., Stagg, S. M., Lapointe, P., and Balch, W. E. (2006) The COPII cage: unifying principles of vesicle coat assembly. Nat. Rev. Mol. Cell Biol. 7, 727-738
8. Edeling, M. A., Smith, C., and Owen, D. (2006) Life of a clathrin coat: insights from clathrin and AP structures. Nat. Rev. Mol. Cell Biol. 7, 32-44
9. Field, M. C., and Dacks, J. B. (2009) First and last ancestors: reconstructing evolution of the endomembrane system with ESCRTs, vesicle coat proteins, and nuclear pore complexes. Curr. Opin. Cell Biol. 21, 4-13
10. Alber, F., Dokudovskaya, S., Veenhoff, L. M., Zhang, W., Kipper, J., Devos, D., Suprapto, A., Karni-Schmidt, O., Williams, R., Chait, B. T., Rout, M. P., and Sali, A. (2007) Determining the architectures of macromolecular assemblies. Nature 450, 683-694 (Pubitemid 350207700)
11. Alber, F., Dokudovskaya, S., Veenhoff, L. M., Zhang, W., Kipper, J., Devos, D., Suprapto, A., Karni-Schmidt, O., Williams, R., Chait, B. T., Sali, A., and Rout, M. P. (2007) The molecular architecture of the nuclear pore complex. Nature 450, 695-701 (Pubitemid 350207701)
12. Santarella-Mellwig, R., Franke, J., Jaedicke, A., Gorjanacz, M., Bauer, U., Budd, A., Mattaj, I. W., and Devos, D. P. (2010) The compartmentalized bacteria of the planctomycetes-verrucomicrobia-chlamydiae superphylum have membrane coat-like proteins. PLoS Biol. 8, e1000281
13. Stagg, S. M., Gürkan, C., Fowler, D. M., LaPointe, P., Foss, T. R., Potter, C. S., Carragher, B., and Balch, W. E. (2006) Structure of the Sec13/31 COPII coat cage. Nature 439, 234-238
14. Stagg, S. M., LaPointe, P., Razvi, A., Gürkan, C., Potter, C. S., Carragher, B., and Balch, W. E. (2008) Structural basis for cargo regulation of COPII coat assembly. Cell 134, 474-484
15. Fath, S., Mancias, J. D., Bi, X., and Goldberg, J. (2007) Structure and organization of coat proteins in the COPII cage. Cell 129, 1325-1336 (Pubitemid 46962091)
16. Brohawn, S. G., Partridge, J. R., Whittle, J. R., and Schwartz, T. U. (2009) The nuclear pore complex has entered the atomic age. Structure 17, 1156-1168
17. Jékely, G., and Arendt, D. (2006) Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 28, 191-198
18. Jin, H., White, S. R., Shida, T., Schulz, S., Aguiar, M., Gygi, S. P., Bazan, J. F., and Nachury, M. V. (2010) The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141, 1208-1219
19. Nickerson, D. P., Brett, C. L., and Merz, A. J. (2009) Vps-C complexes: gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21, 543-551
20. Rout, M. P., Aitchison, J. D., Suprapto, A., Hjertaas, K., Zhao, Y., and Chait, B. T. (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635-651
21. Cristea, I. M., Williams, R., Chait, B. T., and Rout, M. P. (2005) Fluorescent proteins as proteomic probes. Mol. Cell Proteomics 4, 1933-1941 (Pubitemid 41830187)
22. Luo, Y., Li, T., Yu, F., Kramer, T., and Cristea, I. M. (2010) Resolving the composition of protein complexes using a MALDI LTQ Orbitrap. J. Am. Soc. Mass Spectrom. 21, 34-46
23. Dokudovskaya, S., Williams, R., Devos, D., Sali, A., Chait, B. T., and Rout, M. P. (2006) Protease accessibility laddering: a proteomic tool for probing protein structure. Structure 14, 653-660 (Pubitemid 43670512)
24. McGuffin, L. J., Bryson, K., and Jones, D. T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16, 404-405
25. Dosztányi, Z., Csizmók, V., Tompa, P., and Simon, I. (2005) The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins. J. Mol. Biol. 347, 827-839
26. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337, 635-645
27. Shi, J., Blundell, T. L., and Mizuguchi, K. (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257
28. Lobley, A., Sadowski, M. I., and Jones, D. T. (2009) pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics 25, 1761-1767
29. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc 4, 363-371
30. Karplus, K. (2009) SAM-T08, HMM-based protein structure prediction. Nucleic Acids Res. 37, W492-497
31. Pieper, U., Eswar, N., Webb, B. M., Eramian, D., Kelly, L., Barkan, D. T., Carter, H., Mankoo, P., Karchin, R., Marti-Renom, M. A., Davis, F. P., and Sali, A. (2009) MODBASE, a database of annotated comparative protein structure models and associated resources. Nucleic Acids Res. 37, D347-354
32. Zhang, Y. (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69 Suppl 8, 108-117
33. Bateman, A., Birney, E., Durbin, R., Eddy, S. R., Howe, K. L., and Sonnhammer, E. L. (2000) The Pfam protein families database. Nucleic Acids Res. 28, 263-266
34. Shen, M. Y., and Sali, A. (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15, 2507-2524
35. Gabernet-Castello, C., Dacks, J. B., and Field, M. C. (2009) The single ENTH-domain protein of trypanosomes; endocytic functions and evolutionary relationship with epsin. Traffic 10, 894-911
36. Smith, T. F., and Waterman, M. S. (1981) Identification of common molecular subsequences. J. Mol. Biol. 147, 195-197
37. Henikoff, S., and Henikoff, J. G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. U.S.A. 89, 10915-10919
38. Huelsenbeck, J. P., and Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755 (Pubitemid 32851390)
39. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704
40. Stamatakis, A., Hoover, P., and Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst. Biol. 57, 758-771
41. Chessel, A., Cinquin, B., Bardin, S., Salamero, J., and Kervrann, C. (2009) Computational geometry-based scale-space and modal image decomposition application to light video-microscopy imaging. SSVM'09 proceedings. Lecture Notes Computer Sci. 5567, 770-781
42. Boulanger, J., Kervrann, C., Bouthemy, P., Elbau, P., Sibarita, J. B., and Salamero, J. (2010) Patch-based nonlocal functional for denoising fluorescence microscopy image sequences. IEEE Trans. Med. Imaging 29, 442-454
43. McEwen, C. R. (1967) Computation of density distributions in solutions at sedimentation equilibrium. Anal. Biochem. 19, 23-39
44. Vida, T. A., and Emr, S. D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779-792
45. Siniossoglou, S., Lutzmann, M., Santos-Rosa, H., Leonard, K., Mueller, S., Aebi, U., and Hurt, E. (2000) Structure and assembly of the Nup84p complex. J. Cell Biol. 149, 41-54
46. Neklesa, T. K., and Davis, R. W. (2009) A genome-wide screen for regulators of TORC1 in response to amino acid starvation reveals a conserved Npr2/3 complex. PLoS Genet. 5, e1000515
47. Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., Ding, H., Koh, J. L., Toufighi, K., Mostafavi, S., Prinz, J., St Onge, R. P., VanderSluis, B., Makhnevych, T., Vizeacoumar, F. J., Alizadeh, S., Bahr, S., Brost, R. L., Chen, Y., Cokol, M., Deshpande, R., Li, Z., Lin, Z. Y., Liang, W., Marback, M., Paw, J., San Luis, B. J., Shuteriqi, E., Tong, A. H., van, Dyk, N., Wallace, I. M., Whitney, J. A., Weirauch, M. T., Zhong, G., Zhu, H., Houry, W. A., Brudno, M., Ragibizadeh, S., Papp, B., Pál, C., Roth, F.P., Giaever, G., Nislow, C., Troyanskaya, O. G., Bussey, H., Bader, G. D., Gingras, A. C., Morris, Q. D., Kim, P. M., Kaiser, C. A., Myers, C. L., Andrews, B. J., and Boone, C. (2010) The genetic landscape of a cell. Science 327, 425-431
48. Breitkreutz, A., Choi, H., Sharom, J. R., Boucher, L., Neduva, V., Larsen, B., Lin, Z. Y., Breitkreutz, B. J., Stark, C., Liu, G., Ahn, J., Dewar-Darch, D., Reguly, T., Tang, X., Almeida, R., Qin, Z. S., Pawson, T., Gingras, A.C., Nesvizhskii, A.I., and Tyers, M. (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328, 1043-1046
49. Babor, S. M., and Fass, D. (1999) Crystal structure of the Sec18p N-terminal domain. Proc. Natl. Acad. Sci. U.S.A. 96, 14759-14764
50. Bi, X., Corpina, R. A., and Goldberg, J. (2002) Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419, 271-277
51. Doerks, T., Copley, R. R., Schultz, J., Ponting, C. P., and Bork, P. (2002) Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 12, 47-56 (Pubitemid 34070591)
52. Nameki, N., Yoneyama, M., Koshiba, S., Tochio, N., Inoue, M., Seki, E., Matsuda, T., Tomo, Y., Harada, T., Saito, K., Kobayashi, N., Yabuki, T., Aoki, M., Nunokawa, E., Matsuda, N., Sakagami, N., Terada, T., Shirouzu, M., Yoshida, M., Hirota, H., Osanai, T., Tanaka, A., Arakawa, T., Carninci, P., Kawai, J., Hayashizaki, Y., Kinoshita, K., Güntert, P., Kigawa, T., and Yokoyama, S. (2004) Solution structure of the RWD domain of the mouse GCN2 protein. Protein Sci. 13, 2089-2100 (Pubitemid 38989613)
53. Rechsteiner, M., and Rogers, S. W. (1996) PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21, 267-271
54. Field, M. C., Gabernet-Castello, C., and Dacks, J. B. (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv. Exp. Med. Biol. 607, 84-96
55. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691
56. Fujiki, Y., Hubbard, A. L., Fowler, S., and Lazarow, P. B. (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
57. Axelrod, D. (2008) Chapter 7: Total internal reflection fluorescence microscopy. Methods Cell Biol. 89, 169-221
58. Simon, S. M. (2009) Partial internal reflections on total internal reflection fluorescent microscopy. Trends Cell Biol. 19, 661-668
59. Bugnicourt, A., Mari, M., Reggiori, F., Haguenauer-Tsapis, R., and Galan, J. M. (2008) Irs4p and Tax4p: two redundant EH domain proteins involved in autophagy. Traffic 9, 755-769
60. Klionsky, D. J., Cuervo, A. M., and Seglen, P. O. (2007) Methods for monitoring autophagy from yeast to human. Autophagy 3, 181-206
61. Fotin, A., Cheng, Y., Sliz, P., Grigorieff, N., Harrison, S. C., Kirchhausen, T., and Walz, T. (2004) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432, 573-579 (Pubitemid 39626257)
62. Spielewoy, N., Guaderrama, M., Wohlschlegel, J. A., Ashe, M., Yates, J.R., 3rd, and Wittenberg, C. (2010) Npr2, yeast homolog of the human tumor suppressor NPRL2, is a target of Grr1 required for adaptation to growth on diverse nitrogen sources. Eukaryot Cell 9, 592-601
63. Hong, W. (2005) SNAREs and traffic. Biochim. Biophys. Acta 1744, 120-144
64. Ballon, D. R., Flanary, P. L., Gladue, D. P., Konopka, J. B., Dohlman, H. G., and Thorner, J. (2006) DEP-domain-mediated regulation of GPCR signaling responses. Cell 126, 1079-1093 (Pubitemid 44380291)
65. Roberg, K. J., Bickel, S., Rowley, N., and Kaiser, C. A. (1997) Control of amino acid permease sorting in the late secretory pathway of Saccharomyces cerevisiae by SEC13, LST4, LST7 and LST8. Genetics 147, 1569-1584
66. Platani, M., Santarella-Mellwig, R., Posch, M., Walczak, R., Swedlow, J. R., and Mattaj, I. W. (2009) The Nup107-160 nucleoporin complex promotes mitotic events via control of the localization state of the chromosome passenger complex. Mol. Biol. Cell 20, 5260-5275
67. Lee, M. H., Lee, S. H., Kim, H., Jin, J. B., Kim, D. H., and Hwang, I. (2006) A WD40 repeat protein, Arabidopsis Sec13 homolog 1, may play a role in vacuolar trafficking by controlling the membrane association of AtDRP2A. Mol. Cells 22, 210-219 (Pubitemid 46357825)
68. Jeffery, C. J. (2003) Moonlighting proteins: old proteins learning new tricks. Trends Genet. 19, 415-417
69. Hillenmeyer, M. E., Fung, E., Wildenhain, J., Pierce, S. E., Hoon, S., Lee, W., Proctor, M., St Onge, R. P., Tyers, M., Koller, D., Altman, R. B., Davis, R. W., Nislow, C., and Giaever, G. (2008) The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 320, 362-365 (Pubitemid 351555656)
70. Yang, Z., and Klionsky, D. J. (2009) An overview of the molecular mechanism of autophagy. Curr. Top. Microbiol. Immunol. 335, 1-32
71. Kurata, A., Katayama, R., Watanabe, T., Tsuruo, T., and Fujita, N. (2008) TUSC4/NPRL2, a novel PDK1-interacting protein, inhibits PDK1 tyrosine phosphorylation and its downstream signaling. Cancer Sci. 99, 1827-1834
72. Koumandou, V. L., Dacks, J. B., Coulson, R. M., and Field, M. C. (2007) Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 7, 29
73. Iida, T., and Lilly, M. A. (2004) missing oocyte encodes a highly conserved nuclear protein required for the maintenance of the meiotic cycle and oocyte identity in Drosophila. Development 131, 1029-1039
74. Lerman, M. I., and Minna, J. D. (2000) The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium. Cancer Res. 60, 6116-6133
75. Ueda, K., Kawashima, H., Ohtani, S., Deng, W. G., Ravoori, M., Bankson, J., Gao, B., Girard, L., Minna, J. D., Roth, J. A., Kundra, V., and Ji, L. (2006) The 3p21.3 tumor suppressor NPRL2 plays an important role in cisplatin-induced resistance in human non-small-cell lung cancer cells. Cancer Res. 66, 9682-9690 (Pubitemid 44623668)
76. Brohawn, S. G., Leksa, N. C., Spear, E. D., Rajashankar, K. R., and Schwartz, T. U. (2008) Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. Science 322, 1369-1373