Molecular architecture and function of the SEA complex, a modulator of the TORC1 pathway

Molecular and Cellular Proteomics

Volumn 13, Issue 11, 2014, Pages 2855-2870

  Algret, Romain ^a   Fernandez Martinez, Javier ^b   Shi, Yi ^b   Kim, Seung Joong ^c   Pellarin, Riccardo ^c   Cimermancic, Peter ^c   Cochet, Emilie ^a   Sali, Andrej ^c   Chait, Brian T ^b   Rout, Michael P ^b   Dokudovskaya, Svetlana ^a  

^a UMR 8126   (France)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MITOCHONDRIAL PROTEIN; SEA PROTEIN; TORC1 PROTEIN; UNCLASSIFIED DRUG; NITROGEN; NUCLEOPORIN; SACCHAROMYCES CEREVISIAE PROTEIN; TORC1 PROTEIN COMPLEX, S CEREVISIAE; TRANSCRIPTION FACTOR;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL STRAIN; FUNGUS GROWTH; GEL PERMEATION CHROMATOGRAPHY; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RING FINGER MOTIF; STOICHIOMETRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; ULTRASTRUCTURE;

AUTOPHAGY; GENE EXPRESSION REGULATION, FUNGAL; MITOCHONDRIA; NITROGEN; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84910612231     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.039388     Document Type: Article

References (73)

1. Loewith, R., and Hall, M. N. (2011) Target of rapamycin (TOR) in nutrient signaling and growth control. Genetics 189, 1177-1201
2. Laplante, M., and Sabatini, D. M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293
3. Sancak, Y., Peterson, T. R., Shaul, Y. D., Lindquist, R. A., Thoreen, C. C., Bar-Peled, L., and Sabatini, D. M. (2008) The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320, 1496-1501
4. Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A. L., Nada, S., and Sabatini, D. M. (2010) Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303
5. Bar-Peled, L., Schweitzer, L. D., Zoncu, R., and Sabatini, D. M. (2012) Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell 150, 1196-1208
6. Binda, M., Peli-Gulli, M. P., Bonfils, G., Panchaud, N., Urban, J., Sturgill, T. W., Loewith, R., and De Virgilio, C. (2009) The Vam6 GEF controls TORC1 by activating the EGO complex. Mol. Cell 35, 563-573
7. Bonfils, G., Jaquenoud, M., Bontron, S., Ostrowicz, C., Ungermann, C., and De Virgilio, C. (2012) Leucyl-tRNA synthetase controls TORC1 via the EGO complex. Mol. Cell 46, 105-110
8. Zoncu, R., Bar-Peled, L., Efeyan, A., Wang, S., Sancak, Y., and Sabatini, D. M. (2011) mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(-)-ATPase. Science 334, 678-683
9. Han, J. M., Jeong, S. J., Park, M. C., Kim, G., Kwon, N. H., Kim, H. K., Ha, S. H., Ryu, S. H., and Kim, S. (2012) Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 149, 410-424
10. 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
11. Dokudovskaya, S., Waharte, F., Schlessinger, A., Pieper, U., Devos, D. P., Cristea, I. M., Williams, R., Salamero, J., Chait, B. T., Sali, A., Field, M. C., Rout, M. P., and Dargemont, C. (2011) A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae. Mol. Cell. Proteomics 10, M110.006478
12. Dokudovskaya, S., and Rout, M. P. (2011) A novel coatomer-related SEA complex dynamically associates with the vacuole in yeast and is implicated in the response to nitrogen starvation. Autophagy 7, 1392-1393
13. Algret, R., and Dokudovskaya, S. (2012) The SEA complex-the beginning. Biopolymers Cell 28, 281-284
14. Nookala, R. K., Langemeyer, L., Pacitto, A., Ochoa-Montano, B., Donaldson, J. C., Blaszczyk, B. K., Chirgadze, D. Y., Barr, F. A., Bazan, J. F., and Blundell, T. L. (2012) Crystal structure of folliculin reveals a hidDENN function in genetically inherited renal cancer. Open Biol. 2, 120071
15. Zhang, D., Iyer, L. M., He, F., and Aravind, L. (2012) Discovery of novel DENN proteins: implications for the evolution of eukaryotic intracellular membrane structures and human disease. Front. Genet. 3, 283
16. Levine, T. P., Daniels, R. D., Wong, L. H., Gatta, A. T., Gerondopoulos, A., and Barr, F. A. (2013) Discovery of new Longin and Roadblock domains that form platforms for small GTPases in Ragulator and TRAPP-II. Small GTPases 4, 1-8
17. Panchaud, N., Peli-Gulli, M. P., and De Virgilio, C. (2013) Amino acid deprivation inhibits TORC1 through a GTPase-activating protein complex for the Rag family GTPase Gtr1. Sci. Signal. 6, ra42
18. Graef, M., and Nunnari, J. (2011) Mitochondria regulate autophagy by conserved signalling pathways. EMBO J. 30, 2101-2114
19. Panchaud, N., Peli-Gulli, M. P., and De Virgilio, C. (2013) SEACing the GAP that nEGOCiates TORC1 activation: evolutionary conservation of Rag GTPase regulation. Cell Cycle 12, 1-5
20. Wu, X., and Tu, B. P. (2011) Selective regulation of autophagy by the Iml1-Npr2-Npr3 complex in the absence of nitrogen starvation. Mol. Biol. Cell 22, 4124-4133
21. Bar-Peled, L., Chantranupong, L., Cherniack, A. D., Chen, W. W., Ottina, K. A., Grabiner, B. C., Spear, E. D., Carter, S. L., Meyerson, M., and Sabatini, D. M. (2013) A tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1. Science 340, 1100-1106
22. Fernandez-Martinez, J., Phillips, J., Sekedat, M. D., Diaz-Avalos, R., Velazquez-Muriel, J., Franke, J. D., Williams, R., Stokes, D. L., Chait, B. T., Sali, A., and Rout, M. P. (2012) Structure-function mapping of a heptameric module in the nuclear pore complex. J. Cell Biol. 196, 419-434
23. Leitner, A., Reischl, R., Walzthoeni, T., Herzog, F., Bohn, S., Forster, F., and Aebersold, R. (2012) Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol. Cell. Proteomics 11, M111.014126
24. Olsen, J. V., Macek, B., Lange, O., Makarov, A., Horning, S., and Mann, M. (2007) Higher-energy C-trap dissociation for peptide modification analysis. Nat. Methods 4, 709-712
25. Yang, B., Wu, Y. J., Zhu, M., Fan, S. B., Lin, J., Zhang, K., Li, S., Chi, H., Li, Y. X., Chen, H. F., Luo, S. K., Ding, Y. H., Wang, L. H., Hao, Z., Xiu, L. Y., Chen, S., Ye, K., He, S. M., and Dong, M. Q. (2012) Identification of cross-linked peptides from complex samples. Nat. Methods 9, 904-906
26. Qin, J., and Chait, B. T. (1995) Preferential fragmentation of protonated gas-phase peptide ions adjacent to acidic amino-acid-residues. J. Am. Chem. Soc. 117, 5411-5412
27. Michalski, A., Neuhauser, N., Cox, J., and Mann, M. (2012) A systematic investigation into the nature of tryptic HCD spectra. J. Proteome Res. 11, 5479-5491
28. 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
29. 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
30. Lasker, K., Phillips, J. L., Russel, D., Velazquez-Muriel, J., Schneidman-Duhovny, D., Tjioe, E., Webb, B., Schlessinger, A., and Sali, A. (2010) Integrative structure modeling of macromolecular assemblies from proteomics data. Mol. Cell. Proteomics 9, 1689-1702
31. Lasker, K., Sali, A., and Wolfson, H. J. (2010) Determining macromolecular assembly structures by molecular docking and fitting into an electron density map. Proteins 78, 3205-3211
32. Russel, D., Lasker, K., Webb, B., Velazquez-Muriel, J., Tjioe, E., Schneidman-Duhovny, D., Peterson, B., and Sali, A. (2012) Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies. PLoS Biol. 10, e1001244
33. 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
34. Debler, E. W., Ma, Y., Seo, H. S., Hsia, K. C., Noriega, T. R., Blobel, G., and Hoelz, A. (2008) A fence-like coat for the nuclear pore membrane. Mol. Cell 32, 815-826
35. Soding, J., Biegert, A., and Lupas, A. N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248
36. Bryson, K., Cozzetto, D., and Jones, D. T. (2007) Computer-assisted protein domain boundary prediction using the Dom-Pred server. Curr. Protein Peptide Sci. 8, 181-188
37. McGuffin, L. J., Bryson, K., and Jones, D. T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16, 404-405
38. 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
39. Menke, M., Berger, B., and Cowen, L. (2010) Markov random fields reveal an N-terminal double beta-propeller motif as part of a bacterial hybrid two-component sensor system. Proc. Natl. Acad. Sci. U.S.A. 107, 4069-4074
40. Shen, M. Y., and Sali, A. (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci. 15, 2507-2524
41. Sali, A., and Blundell, T. L. (1993) Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815
42. Kohn, J. E., Millett, I. S., Jacob, J., Zagrovic, B., Dillon, T. M., Cingel, N., Dothager, R. S., Seifert, S., Thiyagarajan, P., Sosnick, T. R., Hasan, M. Z., Pande, V. S., Ruczinski, I., Doniach, S., and Plaxco, K. W. (2004) Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl. Acad. Sci. U.S.A. 101, 12491-12496
43. Oliphant, T. E. (2007) Python for scientific computing. Comput. Sci. Eng. 9, 10-20
44. 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
45. Gurkan, 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
46. Seebacher, J., Mallick, P., Zhang, N., Eddes, J. S., Aebersold, R., and Gelb, M. H. (2006) Protein cross-linking analysis using mass spectrometry, isotope-coded cross-linkers, and integrated computational data processing. J. Proteome Res. 5, 2270-2282
47. Herzog, F., Kahraman, A., Boehringer, D., Mak, R., Bracher, A., Walzthoeni, T., Leitner, A., Beck, M., Hartl, F. U., Ban, N., Malmstrom, L., and Aebersold, R. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 337, 1348-1352
48. Chen, Z. A., Jawhari, A., Fischer, L., Buchen, C., Tahir, S., Kamenski, T., Rasmussen, M., Lariviere, L., Bukowski-Wills, J. C., Nilges, M., Cramer, P., and Rappsilber, J. (2010) Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J. 29, 717-726
49. Archambault, V., Chang, E. J., Drapkin, B. J., Cross, F. R., Chait, B. T., and Rout, M. P. (2004) Targeted proteomic study of the cyclin-Cdk module. Mol. Cell 14, 699-711
50. Tackett, A. J., DeGrasse, J. A., Sekedat, M. D., Oeffinger, M., Rout, M. P., and Chait, B. T. (2005) I-DIRT, a general method for distinguishing between specific and nonspecific protein interactions. J. Proteome Res. 4, 1752-1756
51. Niepel, M., Strambio-de-Castillia, C., Fasolo, J., Chait, B. T., and Rout, M. P. (2005) The nuclear pore complex-associated protein, Mlp2p, binds to the yeast spindle pole body and promotes its efficient assembly. J. Cell Biol. 170, 225-235
52. Oeffinger, M., Wei, K. E., Rogers, R., DeGrasse, J. A., Chait, B. T., Aitchison, J. D., and Rout, M. P. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4, 951-956
53. Peters, C., Baars, T. L., Buhler, S., and Mayer, A. (2004) Mutual control of membrane fission and fusion proteins. Cell 119, 667-678
54. Hayden, J., Williams, M., Granich, A., Ahn, H., Tenay, B., Lukehart, J., Highfill, C., Dobard, S., and Kim, K. (2013) Vps1 in the late endosometo-vacuole traffic. J. Biosci. 38, 73-83
55. Urban, J., Soulard, A., Huber, A., Lippman, S., Mukhopadhyay, D., Deloche, O., Wanke, V., Anrather, D., Ammerer, G., Riezman, H., Broach, J. R., De Virgilio, C., Hall, M. N., and Loewith, R. (2007) Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Mol. Cell 26, 663-674
56. Sturgill, T. W., Cohen, A., Diefenbacher, M., Trautwein, M., Martin, D. E., and Hall, M. N. (2008) TOR1 and TOR2 have distinct locations in live cells. Eukaryot. Cell 7, 1819-1830
57. Klionsky, D. J., Cuervo, A. M., and Seglen, P. O. (2007) Methods for monitoring autophagy from yeast to human. Autophagy 3, 181-206
58. Michaillat, L., Baars, T. L., and Mayer, A. (2012) Cell-free reconstitution of vacuole membrane fragmentation reveals regulation of vacuole size and number by TORC1. Mol. Biol. Cell 23, 881-895
59. Field, M. C., Sali, A., and Rout, M. P. (2011) Evolution: on a bender-BARs, ESCRTs, COPs, and finally getting your coat. J. Cell Biol. 193, 963-972
60. 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
61. 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
62. 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
63. 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
64. Takahara, T., and Maeda, T. (2012) Transient sequestration of TORC1 into stress granules during heat stress. Mol. Cell 47, 242-252
65. Baars, T. L., Petri, S., Peters, C., and Mayer, A. (2007) Role of the V-ATPase in regulation of the vacuolar fission-fusion equilibrium. Mol. Biol. Cell 18, 3873-3882
66. 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 cisplatininduced resistance in human non-small-cell lung cancer cells. Cancer Res. 66, 9682-9690
67. Otani, S., Takeda, S., Yamada, S., Sakakima, Y., Sugimoto, H., Nomoto, S., Kasuya, H., Kanazumi, N., Nagasaka, T., and Nakao, A. (2009) The tumor suppressor NPRL2 in hepatocellular carcinoma plays an important role in progression and can be served as an independent prognostic factor. J. Surg. Oncol. 100, 358-363
68. Seng, T. J., Ichimura, K., Liu, L., Tingby, O., Pearson, D. M., and Collins, V. P. (2005) Complex chromosome 22 rearrangements in astrocytic tumors identified using microsatellite and chromosome 22 tile path array analysis. Genes Chrom. Cancer 43, 181-193
69. Dibbens, L. M., de Vries, B., Donatello, S., Heron, S. E., Hodgson, B. L., Chintawar, S., Crompton, D. E., Hughes, J. N., Bellows, S. T., Klein, K. M., Callenbach, P. M., Corbett, M. A., Gardner, A. E., Kivity, S., Iona, X., Regan, B. M., Weller, C. M., Crimmins, D., O'Brien, T. J., Guerrero-Lopez, R., Mulley, J. C., Dubeau, F., Licchetta, L., Bisulli, F., Cossette, P., Thomas, P. Q., Gecz, J., Serratosa, J., Brouwer, O. F., Andermann, F., Andermann, E., van den Maagdenberg, A. M., Pandolfo, M., Berkovic, S. F., and Scheffer, I. E. (2013) Mutations in DEPDC5 cause familial focal epilepsy with variable foci. Nat. Genet. 45, 546-551
70. Ishida, S., Picard, F., Rudolf, G., Noe, E., Achaz, G., Thomas, P., Genton, P., Mundwiller, E., Wolff, M., Marescaux, C., Miles, R., Baulac, M., Hirsch, E., Leguern, E., and Baulac, S. (2013) Mutations of DEPDC5 cause autosomal dominant focal epilepsies. Nat. Genet. 45, 552-555
71. Kowalczyk, M. S., Hughes, J. R., Babbs, C., Sanchez-Pulido, L., Szumska, D., Sharpe, J. A., Sloane-Stanley, J. A., Morriss-Kay, G. M., Smoot, L. B., Roberts, A. E., Watkins, H., Bhattacharya, S., Gibbons, R. J., Ponting, C. P., Wood, W. G., and Higgs, D. R. (2012) Nprl3 is required for normal development of the cardiovascular system. Mamm. Genome 23, 404-415
72. Senger, S., Csokmay, J., Akbar, T., Jones, T. I., Sengupta, P., and Lilly, M. A. (2011) The nucleoporin Seh1 forms a complex with Mio and serves an essential tissue-specific function in Drosophila oogenesis. Development 138, 2133-2142
73. Wei, Y., and Lilly, M. A. (2014) The TORC1 inhibitors Nprl2 and Nprl3 mediate an adaptive response to amino-acid starvation in Drosophila. Cell Death Differ. 21(9), 1460-1468