Two translation products of Yersinia yscQ assemble to form a complex essential to type III secretion

Biochemistry

Volumn 51, Issue 8, 2012, Pages 1669-1677

  Bzymek, Krzysztof P ^a,b   Hamaoka, Brent Y ^a   Ghosh, Partho ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL FLAGELLAR; BUILDING BLOCKES; C-TERMINUS; CONFORMATIONAL DIFFERENCES; HOMODIMERS; ORTHOLOGS; SINGLE MOLECULE; TRANSLATION INITIATION SITE; TYPE III SECRETIONS;

ENCODING (SYMBOLS);

PROTEINS;

BACTERIAL PROTEIN; BACTERIAL PROTEIN FLIM; BACTERIAL PROTEIN FLIN; BACTERIAL PROTEIN YSCQ; HOMODIMER; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; FLAGELLUM; GENE LOCUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE; TRANSLATION INITIATION; TYPE III SECRETION SYSTEM; YERSINIA;

BACTERIAL PROTEINS; ESCHERICHIA COLI; MEMBRANE PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; YERSINIA;

BACTERIA (MICROORGANISMS); YERSINIA;

EID: 84857553241     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201792p     Document Type: Article

References (41)

1. Galan, J. E. and Wolf-Watz, H. (2006) Protein delivery into eukaryotic cells by type III secretion machines Nature 444, 567-573
2. Cornelis, G. R. (2006) The type III secretion injectisome Nat. Rev. Microbiol. 4, 811-825
3. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galan, J. E., and Aizawa, S. I. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system Science 280, 602-605
4. Akopyan, K., Edgren, T., Wang-Edgren, H., Rosqvist, R., Fahlgren, A., Wolf-Watz, H., and Fallman, M. (2011) Translocation of surface-localized effectors in type III secretion Proc. Natl. Acad. Sci. U.S.A. 108, 1639-1644
5. Ghosh, P. (2004) Process of protein transport by the type III secretion system Microbiol. Mol. Biol. Rev. 68, 771-795
6. Thomas, D. R., Francis, N. R., Xu, C., and DeRosier, D. J. (2006) The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium J. Bacteriol. 188, 7039-7048
7. Erhardt, M. and Hughes, K. T. (2010) C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation Mol. Microbiol. 75, 376-393
8. Brown, P. N., Mathews, M. A., Joss, L. A., Hill, C. P., and Blair, D. F. (2005) Crystal structure of the flagellar rotor protein FliN from Thermotoga maritima J. Bacteriol. 187, 2890-2902
9. Sarkar, M. K., Paul, K., and Blair, D. F. (2010) Subunit organization and reversal-associated movements in the flagellar switch of Escherichia coli J. Biol. Chem. 285, 675-684
10. Mathews, M. A., Tang, H. L., and Blair, D. F. (1998) Domain analysis of the FliM protein of Escherichia coli J. Bacteriol. 180, 5580-5590
11. Diepold, A., Amstutz, M., Abel, S., Sorg, I., Jenal, U., and Cornelis, G. R. (2010) Deciphering the assembly of the Yersinia type III secretion injectisome EMBO J. 29, 1928-1940
12. Morita-Ishihara, T., Ogawa, M., Sagara, H., Yoshida, M., Katayama, E., and Sasakawa, C. (2006) Shigella Spa33 is an essential C-ring component of type III secretion machinery J. Biol. Chem. 281, 599-607
13. 2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis J. Bacteriol. 176, 569-579
14. Lara-Tejero, M., Kato, J., Wagner, S., Liu, X., and Galan, J. E. (2011) A sorting platform determines the order of protein secretion in bacterial type III systems Science 331, 1188-1191
15. Biemans-Oldehinkel, E., Sal-Man, N., Deng, W., Foster, L. J., and Finlay, B. B. (2011) Quantitative Proteomic Analysis Reveals Formation of an EscL-EscQ-EscN Type III Complex in Enteropathogenic Escherichia coli J. Bacteriol. 193, 5514-5519
16. Yu, X. J., Liu, M., Matthews, S., and Holden, D. W. (2011) Tandem Translation Generates a Chaperone for the Salmonella Type III Secretion System Protein SsaQ J. Biol. Chem. 286, 36098-36107
17. Jackson, M. W. and Plano, G. V. (2000) Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system FEMS Microbiol. Lett. 186, 85-90
18. Blaylock, B., Riordan, K. E., Missiakas, D. M., and Schneewind, O. (2006) Characterization of the Yersinia enterocolitica type III secretion ATPase YscN and its regulator, YscL J. Bacteriol. 188, 3525-3534
19. Riordan, K. E., Sorg, J. A., Berube, B. J., and Schneewind, O. (2008) Impassable YscP substrates and their impact on the Yersinia enterocolitica type III secretion pathway J. Bacteriol. 190, 6204-6216
20. Johnson, D. L., Stone, C. B., and Mahony, J. B. (2008) Interactions between CdsD, CdsQ, and CdsL, three putative Chlamydophila pneumoniae type III secretion proteins J. Bacteriol. 190, 2972-2980
21. Spaeth, K. E., Chen, Y. S., and Valdivia, R. H. (2009) The Chlamydia type III secretion system C-ring engages a chaperone-effector protein complex PLoS Pathog. 5, e1000579
22. B-C, a conserved component of the bacterial type III secretion systems Proc. Natl. Acad. Sci. U.S.A. 101, 70-75
23. Bolin, I., Norlander, L., and Wolf-Watz, H. (1982) Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid Infect. Immun. 37, 506-512
24. Budisa, N., Karnbrock, W., Steinbacher, S., Humm, A., Prade, L., Neuefeind, T., Moroder, L., and Huber, R. (1997) Bioincorporation of telluromethionine into proteins: A promising new approach for X-ray structure analysis of proteins J. Mol. Biol. 270, 616-623
25. Kabsch, W. (2010) XDS Acta Crystallogr. D66, 125-132
26. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode, Vol. 276, Academic Press, New York.
27. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
28. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
29. Brünger, A. (1998) Crystallography & NMR system: A new software for macromolecular structure determination Acta Crystallogr. D54, 905-921
30. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr. D67, 235-242
31. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement Acta Crystallogr. D57, 122-133
32. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66, 12-21
33. Di Tommaso, P., Moretti, S., Xenarios, I., Orobitg, M., Montanyola, A., Chang, J. M., Taly, J. F., and Notredame, C. (2011) T-Coffee: A web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension Nucleic Acids Res. 39, W13-W17
34. Gouet, P., Robert, X., and Courcelle, E. (2003) ESPript/ENDscript: Extracting and rendering sequence and 3D information from atomic structures of proteins Nucleic Acids Res. 31, 3320-3323
35. Lathem, W. W., Price, P. A., Miller, V. L., and Goldman, W. E. (2007) A plasminogen-activating protease specifically controls the development of primary pneumonic plague Science 315, 509-513
36. Datsenko, K. A. and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645
37. Palmer, L. E., Hobbie, S., Galan, J. E., and Bliska, J. B. (1998) YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-α production and downregulation of the MAP kinases p38 and JNK Mol. Microbiol. 27, 953-965
38. Rodgers, L., Mukerjea, R., Birtalan, S., Friedberg, D., and Ghosh, P. (2010) A solvent-exposed patch in chaperone-bound YopE is required for translocation by the type III secretion system J. Bacteriol. 192, 3114-3122
39. Paul, K., Harmon, J. G., and Blair, D. F. (2006) Mutational analysis of the flagellar rotor protein FliN: Identification of surfaces important for flagellar assembly and switching J. Bacteriol. 188, 5240-5248
40. Fadouloglou, V. E., Bastaki, M. N., Ashcroft, A. E., Phillips, S. E., Panopoulos, N. J., Glykos, N. M., and Kokkinidis, M. (2009) On the quaternary association of the type III secretion system HrcQB-C protein: Experimental evidence differentiates among the various oligomerization models J. Struct. Biol. 166, 214-225
41. Paul, K. and Blair, D. F. (2006) Organization of FliN subunits in the flagellar motor of Escherichia coli J. Bacteriol. 188, 2502-2511