Structure of AscE and induced burial regions in AscE and AscG upon formation of the chaperone needle-subunit complex of type III secretion system in Aeromonas hydrophila

Protein Science

Volumn 17, Issue 10, 2008, Pages 1748-1760

  Yih, Wan Tan ^a,b   Hong, Bing Yu ^a,c   Ka, Yin Leung ^a   Sivaraman, J ^a   Mok, Yu Keung ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Chaperones AscE and AscG; Induced folding; Limited protease digestion; Needle subunit AscF; Type III secretion system

Indexed keywords

CHAPERONE; HELIX LOOP HELIX PROTEIN; PROTEIN ASC E; PROTEIN ASC G; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

AEROMONAS HYDROPHILA; ARTICLE; CRYSTAL STRUCTURE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; TYPE III SECRETION SYSTEM;

AEROMONAS HYDROPHILA; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CLONING, MOLECULAR; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SEQUENCE ALIGNMENT;

AEROMONAS HYDROPHILA;

EID: 52949139839     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.036798.108     Document Type: Article

References (46)

1. Allaoui, A., Schulte, R., and Cornelis, G.R. 1995. Mutational analysis of the Yersinia enterocolitica virC operon: Characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR. Mol. Microbiol. 18: 343-355.
2. Austin, B. and Adams, C. 1996. Fish pathogen. In The genus Aeromonas (eds. B. Austin et al.), pp. 197-229. John Wiley and Sons, New York.
3. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., and Bourne, P.E. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235-242.
4. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., Sansonetti, P., and Allaoui, A. 2001. Structure and composition of the Shigella flexneri "needle complex," a part of its type III secreton. Mol. Microbiol. 39: 652-663.
5. Blocker, A., Komoriya, K., and Aizawa, S.-I. 2003. Type III secretion systems and bacterial flagella: Insights into their function from structural similarities. Proc. Natl. Acad. Sci. 100: 3027-3030.
6. Braun, M., Stuber, K., Schlatter, Y., Wahli, T., Kuhnert, P., and Frey, J. 2002. Characterization of an ADP-ribosyltransferase toxin (AexT) from Aeromonas salmonicida subsp. salmonicida. J. Bacteriol. 184: 1851-1858.
7. 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.
8. Cordes, F.S., Daniell, S., Kenjale, R., Saurya, S., Picking, W.L., Picking, W.D., Booy, F., Lea, S.M., and Blocker, A. 2005. Helical packing of needles from functionally altered Shigella type III secretion systems. J. Mol. Biol. 354: 206-211.
9. Cornelis, G.R. and Van Gijsegem, F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54: 735-774.
10. Darboe, N., Kenjale, R., Picking, W.L., Picking, W.D., and Middaugh, C.R. 2006. Physical characterization of MxiH and PrgI, the needle component of the type III secretion apparatus from Shigella and Salmonella. Protein Sci. 15: 543-552.
11. 28. Nat. Struct. Biol. 4: 285-291.
12. Day, J.B., Guller, I., and Plano, G.V. 2000. Yersinia pestis YscG protein is a Syc-like chaperone that directly binds YscE. Infect. Immun. 68: 6466-6471.
13. Deane, J.E., Roversi, P., Cordes, F.S., Johnson, S., Kenjale, R., Daniell, S., Booy, F., Picking, W.D., Picking, W.L., Blocker, A.J., et al. 2006. Molecular model of a type III secretion system needle: Implications for host-cell sensing. Proc. Natl. Acad. Sci. 103: 12529-12533.
14. Fehr, D., Casanova, C., Liverman, A., Blazkova, H., Orth, K., Dobbelaere, D., Frey, J., and Burr, S.E. 2006. AopP, a type III effector protein of Aeromonas salmonicida, inhibits the NF-κB signalling pathway. Microbiology 152: 2809-2818.
15. Finlay, B.B. and Cossart, P. 1997. Exploitation of mammalian host cell functions by bacterial pathogens. Science 276: 718-725.
16. Ghosh, P. 2004. Process of protein transport by the type III secretion system. Microbiol. Mol. Biol. Rev. 68: 771-795.
17. Ho, S.N., Hunt, H.D., Horton, J.K., Pullen, J.K., and Pease, L.R. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
18. Hoiczyk, E. and Blobel, G. 2001. Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc. Natl. Acad. Sci. 98: 4669-4674.
19. Janda, J.M. 2001. Aeromonas and Plesiomonas. In Molecular medical microbiology (ed. M. Sussman), pp. 1237-1270. Academic Press, San Diego, CA.
20. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
21. Kenjale, R., Wilson, J., Zenk, S.F., Saurya, S., Picking, W.L., Picking, W.D., and Blocker, A. 2005. The needle component of the type III secretion of Shigella regulates the activity of the secretion apparatus. J. Biol. Chem. 280: 42929-42937.
22. Kimbrough, T.G. and Miller, S.I. 2000. Contribution of Salmonella typhimurium type III secretion components to needle complex formation. Proc. Natl. Acad. Sci. 97: 11008-11013.
23. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26: 283-291.
24. Matthews, B.W. 1968. Solvent content of protein crystals. J. Mol. Biol. 33: 491-497.
25. Nicholls, A., Sharp, K.A., and Honig, B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296.
26. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. In Methods in enzymology (eds. J. Carter et al.), pp. 307-326. Academic Press, San Diego, CA.
27. Pastor, A., Chabert, J., Louwagie, M., Garin, J., and Attree, I. 2005. PscF is a major component of the Pseudomonas aeruginosa type III secretion needle. FEMS Microbiol. Lett. 253: 95-101.
28. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.
29. Phan, J., Austin, B.P., and Waugh, D.S. 2005. Crystal structure of the Yersinia type III secretion protein YscE. Protein Sci. 14: 2759-2763.
30. Quinaud, M., Chabert, J., Faudry, E., Neumann, E., Lemaire, D., Pastor, A., Elsen, S., Dessen, A., and Attree, I. 2005. The PscE-PscF-PscG complex controls type III secretion needle biogenesis in Pseudomonas aeruginosa. J. Biol. Chem. 280: 36293-36300.
31. Quinaud, M., Plé, S., Job, V., Contreras-Martel, C., Simorre, J.-P., Attree, I., and Dessen, A. 2007. Structure of the heterotrimetric complex that regulates type III secretion needle formation. Proc. Natl. Acad. Sci. 104: 7803-7808.
32. Samatey, F.A., Imada, K., Nagashima, S., Vonderviszt, F., Kumasaka, T., Yamamoto, M., and Namba, K. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410: 331-337.
33. Sha, J., Wang, S.F., Suarez, G., Sierra, J.C., Fadl, A.A., Erova, T.E., Foltz, S.M., Khajanchi, B.K., Silver, A.C., Graf, J., et al. 2007. Further characterization of a type III secretion system (T3SS) and of a new effector protein from a clinical isolate of Aeromonas hydrophila - Part I. Microb. Pathog. 43: 127-146.
34. Sierra, J.C., Suarez, G., Sha, J., Foltz, S.M., Popov, V.L., Galindo, C.L., Garner, H.R., and Chopra, A.K. 2007. Biological characterization of a new type III secretion system effector from a clinical isolate of Aeromonas hydrophila - Part II. Microb. Pathog. 43: 147-160.
35. Sun, P., Tropea, J.E., Austin, B.P., Cherry, S., and Waugh, D.S. 2008. Structural characterization of the Yersinia pestis type III secretion system needle protein YscF in complex with its heterodimeric chaperone YscE/YscG. J. Mol. Biol. 377: 819-830.
36. Terwilliger, T.C. 1999. Reciprocal-space solvent flattening. Acta Crystallogr. D Biol. Crystallogr. 55: 1863-1871.
37. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
38. Thune, R.L., Stanley, L.A., and Cooper, K. 1993. Pathogenesis of Gram-negative bacterial infections in warmwater fish. Annu. Rev. Fish Dis. 3: 37-68.
39. Vilches, S., Wilhelms, M., Yu, H.B., Leung, K.Y., Tomás, J.M., and Merino, S. 2007. Aeromonas hydrophila AH-3 AexT is an ADP-ribosylating toxin secreted through the type III secretion system. Microb. Pathog. 44: 1-12.
40. Wang, Y., Ouellette, A.N., Egan, C.W., Rathinavelan, T., Im, W., and De Guzman, R.N. 2007. Differences in the electrostatic surfaces of the type III secretion needle proteins PrgI, BsaL, and MxiH. J. Mol. Biol. 371: 1304-1314.
41. Weeks, C.M., Blessing, R.H., Miller, R., Mungee, R., Potter, S.A., Rappleye, J., Smith, G.D., Xu, H., and Furey, W. 2002. Towards automated protein structure determination: BnP, the SnB-PHASES interface. Z. Kristallogr. 217: 686-693.
42. Yonekura, K., Maki, S., Morgan, D.G., DeRosier, D.J., Vonderviszt, F., Imada, K., and Namba, K. 2000. The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290: 2148-2152.
43. Yonekura, K., Maki-Yonekura, S., and Namba, K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424: 643-650.
44. Yu, H.B., Srinivasa Rao, P.S., Lee, H.C., Vilches, S., Merino, S., Tomas, J.M., and Leung, K.Y. 2004. A type III secretion system is required for Aeromonas hydrophila AH-1 pathogenesis. Infect. Immun. 72: 1248-1256.
45. Yu, H.B., Kaur, R., Lim, S., Wang, X.H., and Leung, K.Y. 2007. Characterization of extracellular proteins produced by Aeromonas hydrophila AH-1. Proteomics 7: 436-449.
46. Zhang, L., Wang, Y., Picking, W.L., Picking, W.D., and DeGuzman, R.N. 2006. Solution structure of monomeric BsaL, the type III secretion needle protein of Burkholderia pseudomallei. J. Mol. Biol. 359: 322-330.