Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses

Cell

Volumn 150, Issue 5, 2012, Pages 1029-1041

  Dong, Na ^a   Zhu, Yongqun ^b   Lu, Qiuhe ^a   Hu, Liyan ^a   Zheng, Yuqing ^a   Shao, Feng ^a  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; ARGININE; BACTERIAL PROTEIN; ESPG PROTEIN; GLUTAMINE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; INTERLEUKIN 8; RAB1 PROTEIN; UNCLASSIFIED DRUG; VIRA PROTEIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CATALYSIS; CRYSTAL STRUCTURE; CYTOKINE RELEASE; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GOLGI COMPLEX; HELA CELL; HOST RESISTANCE; HUMAN; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHIGELLA FLEXNERI; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SHIGELLA FLEXNERI; VIRUSES;

EID: 84865693202     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.06.050     Document Type: Article

References (49)

1. S. Albert, E. Will, and D. Gallwitz Identification of the catalytic domains and their functionally critical arginine residues of two yeast GTPase-activating proteins specific for Ypt/Rab transport GTPases EMBO J. 18 1999 5216 5225
2. H. Ashida, M. Ogawa, M. Kim, S. Suzuki, T. Sanada, C. Punginelli, H. Mimuro, and C. Sasakawa Shigella deploy multiple countermeasures against host innate immune responses Curr. Opin. Microbiol. 14 2011 16 23
3. F. Barr, and D.G. Lambright Rab GEFs and GAPs Curr. Opin. Cell Biol. 22 2010 461 470
4. J.H. Brumell, and M.A. Scidmore Manipulation of rab GTPase function by intracellular bacterial pathogens Microbiol. Mol. Biol. Rev. 71 2007 636 652
5. H. Chen, and P. De Camilli The association of epsin with ubiquitinated cargo along the endocytic pathway is negatively regulated by its interaction with clathrin Proc. Natl. Acad. Sci. USA 102 2005 2766 2771
6. A. Clements, K. Smollett, S.F. Lee, E.L. Hartland, M. Lowe, and G. Frankel EspG of enteropathogenic and enterohemorrhagic E. coli binds the Golgi matrix protein GM130 and disrupts the Golgi structure and function Cell. Microbiol. 13 2011 1429 1439
7. J. Davis, J. Wang, J.E. Tropea, D. Zhang, Z. Dauter, D.S. Waugh, and A. Wlodawer Novel fold of VirA, a type III secretion system effector protein from Shigella flexneri Protein Sci. 17 2008 2167 2173
8. A. De Antoni, J. Schmitzová, H.H. Trepte, D. Gallwitz, and S. Albert Significance of GTP hydrolysis in Ypt1p-regulated endoplasmic reticulum to Golgi transport revealed by the analysis of two novel Ypt1-GAPs J. Biol. Chem. 277 2002 41023 41031
9. N. Dong, L. Liu, and F. Shao A bacterial effector targets host DH-PH domain RhoGEFs and antagonizes macrophage phagocytosis EMBO J. 29 2010 1363 1376
10. M.S. Donnenberg, and J.B. Kaper Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector Infect. Immun. 59 1991 4310 4317
11. S.J. Elliott, E.O. Krejany, J.L. Mellies, R.M. Robins-Browne, C. Sasakawa, and J.B. Kaper EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri Infect. Immun. 69 2001 4027 4033
12. K.L. Germane, and B.W. Spiller Structural and functional studies indicate that the EPEC effector, EspG, directly binds p21-activated kinase Biochemistry 50 2011 917 919
13. K.L. Germane, R. Ohi, M.B. Goldberg, and B.W. Spiller Structural and functional studies indicate that Shigella VirA is not a protease and does not directly destabilize microtubules Biochemistry 47 2008 10241 10243
14. P.R. Hardwidge, W. Deng, B.A. Vallance, I. Rodriguez-Escudero, V.J. Cid, M. Molina, and B.B. Finlay Modulation of host cytoskeleton function by the enteropathogenic Escherichia coli and Citrobacter rodentium effector protein EspG Infect. Immun. 73 2005 2586 2594
15. J. Huang, C.L. Birmingham, S. Shahnazari, J. Shiu, Y.T. Zheng, A.C. Smith, K.G. Campellone, W.D. Heo, S. Gruenheid, and T. Meyer Antibacterial autophagy occurs at PI(3)P-enriched domains of the endoplasmic reticulum and requires Rab1 GTPase Autophagy 7 2011 17 26
16. A.H. Hutagalung, and P.J. Novick Role of Rab GTPases in membrane traffic and cell physiology Physiol. Rev. 91 2011 119 149
17. A. Ingmundson, A. Delprato, D.G. Lambright, and C.R. Roy Legionella pneumophila proteins that regulate Rab1 membrane cycling Nature 450 2007 365 369
18. E.S. Masuda, Y. Luo, C. Young, M. Shen, A.B. Rossi, B.C. Huang, S. Yu, M.K. Bennett, D.G. Payan, and R.H. Scheller Rab37 is a novel mast cell specific GTPase localized to secretory granules FEBS Lett. 470 2000 61 64
19. B.D. Moyer, B.B. Allan, and W.E. Balch Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis - Golgi tethering Traffic 2 2001 268 276
20. R.M. Nottingham, and S.R. Pfeffer Defining the boundaries: Rab GEFs and GAPs Proc. Natl. Acad. Sci. USA 106 2009 14185 14186
21. M. Ogawa, T. Yoshimori, T. Suzuki, H. Sagara, N. Mizushima, and C. Sasakawa Escape of intracellular Shigella from autophagy Science 307 2005 727 731
22. X. Pan, S. Eathiraj, M. Munson, and D.G. Lambright TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism Nature 442 2006 303 306
23. S.R. Pfeffer Unsolved mysteries in membrane traffic Annu. Rev. Biochem. 76 2007 629 645
24. S. Pfeffer, and D. Aivazian Targeting Rab GTPases to distinct membrane compartments Nat. Rev. Mol. Cell Biol. 5 2004 886 896
25. A. Rak, R. Fedorov, K. Alexandrov, S. Albert, R.S. Goody, D. Gallwitz, and A.J. Scheidig Crystal structure of the GAP domain of Gyp1p: first insights into interaction with Ypt/Rab proteins EMBO J. 19 2000 5105 5113
26. K. Rittinger, P.A. Walker, J.F. Eccleston, S.J. Smerdon, and S.J. Gamblin Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue Nature 389 1997 758 762
27. V.M. Rivera, X. Wang, S. Wardwell, N.L. Courage, A. Volchuk, T. Keenan, D.A. Holt, M. Gilman, L. Orci, and F. Cerasoli Jr. Regulation of protein secretion through controlled aggregation in the endoplasmic reticulum Science 287 2000 826 830
28. F.E. Rivera-Molina, and P.J. Novick A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway Proc. Natl. Acad. Sci. USA 106 2009 14408 14413
29. S.P. Salcedo, and D.W. Holden Bacterial interactions with the eukaryotic secretory pathway Curr. Opin. Microbiol. 8 2005 92 98
30. K. Scheffzek, M.R. Ahmadian, W. Kabsch, L. Wiesmüller, A. Lautwein, F. Schmitz, and A. Wittinghofer The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants Science 277 1997 333 338
31. A.S. Selyunin, S.E. Sutton, B.A. Weigele, L.E. Reddick, R.C. Orchard, S.M. Bresson, D.R. Tomchick, and N.M. Alto The assembly of a GTPase-kinase signalling complex by a bacterial catalytic scaffold Nature 469 2011 107 111
32. F. Shao, P.M. Merritt, Z. Bao, R.W. Innes, and J.E. Dixon A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis Cell 109 2002 575 588
33. N.L. Slagowski, R.W. Kramer, M.F. Morrison, J. LaBaer, and C.F. Lesser A functional genomic yeast screen to identify pathogenic bacterial proteins PLoS Pathog. 4 2008 e9
34. H. Stenmark Rab GTPases as coordinators of vesicle traffic Nat. Rev. Mol. Cell Biol. 10 2009 513 525
35. M. Strom, P. Vollmer, T.J. Tan, and D. Gallwitz A yeast GTPase-activating protein that interacts specifically with a member of the Ypt/Rab family Nature 361 1993 736 739
36. K. Uchiya, T. Tobe, K. Komatsu, T. Suzuki, M. Watarai, I. Fukuda, M. Yoshikawa, and C. Sasakawa Identification of a novel virulence gene, virA, on the large plasmid of Shigella, involved in invasion and intercellular spreading Mol. Microbiol. 17 1995 241 250
37. L.A. Volpicelli-Daley, Y. Li, C.J. Zhang, and R.A. Kahn Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic Mol. Biol. Cell 16 2005 4495 4508
38. T. Weide, M. Bayer, M. Köster, J.P. Siebrasse, R. Peters, and A. Barnekow The Golgi matrix protein GM130: a specific interacting partner of the small GTPase rab1b EMBO Rep. 2 2001 336 341
39. S. Yoshida, Y. Handa, T. Suzuki, M. Ogawa, M. Suzuki, A. Tamai, A. Abe, E. Katayama, and C. Sasakawa Microtubule-severing activity of Shigella is pivotal for intercellular spreading Science 314 2006 985 989
40. F.C. Zoppino, R.D. Militello, I. Slavin, C. Alvarez, and M.I. Colombo Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites Traffic 11 2010 1246 1261
41. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. (1998). Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54, 905-921.
42. Collaborative Computational Project, Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763.
43. Donnenberg, M.S., and Kaper, J.B. (1991). Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59, 4310-4317.
44. Elliott, S.J., Krejany, E.O., Mellies, J.L., Robins-Browne, R.M., Sasakawa, C., and Kaper, J.B. (2001). EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect. Immun. 69, 4027-4033.
45. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
46. Laskowski, A.R., MacArthur, W.M., Moss, S.D., and Thornton, M.J. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 283-291.
47. Miller, R., Gallo, S.M., Khalak, H.G., and Weeks, C.M. (1994). SnB: crystal structure determination via shake-and-bake. J. Appl. Crystallogr. 27, 613-621.
48. Pan, X., Eathiraj, S., Munson, M., and Lambright, D.G. (2006). TBC-domain GAPs for Rab GTPases accelerate GTP hydrolysis by a dual-finger mechanism. Nature 442, 303-306.
49. Shao, F., Merritt, P.M., Bao, Z., Innes, R.W., and Dixon, J.E. (2002). A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109, 575-588.