Chlamydia trachomatis Slc1 is a type III secretion chaperone that enhances the translocation of its invasion effector substrate TARP

Molecular Microbiology

Volumn 82, Issue 1, 2011, Pages 131-144

  Brinkworth, Amanda J ^a,b   Malcolm, Denise S ^a   Pedrosa, António T ^a   Roguska, Katarzyna ^a   Shahbazian, Sevanna ^a   Graham, James E ^b   Hayward, Richard D ^c   Carabeo, Rey A ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b University of Louisville School of Medicine   (United States)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; CHAPERONE; HOMODIMER; PROTEIN SLC1; TRANSLOCATED ACTING RECRUITING PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; CROSS LINKING; GEL FILTRATION; GEL PERMEATION CHROMATOGRAPHY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HYBRID; IMMUNOPRECIPITATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STOICHIOMETRY; TYPE III SECRETION SYSTEM; YERSINIA ENTEROCOLITICA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; HELA CELLS; HUMANS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); CHLAMYDIA TRACHOMATIS; MAMMALIA; YERSINIA ENTEROCOLITICA;

EID: 80053243913     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07802.x     Document Type: Article

References (46)

1. Akeda, Y., and Galan, J.E. (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911-915.
2. Beeckman, D.S.A., and Vanrompay, D.C.G. (2010) Bacterial secretion systems with an emphasis on the chlamydial type III secretion system. Curr Issues Mol Biol 12: 17-41.
3. Belland, R.J., Nelson, D.E., Virok, D., Crane, D.D., Hogan, D., Sturdevant, D., etal. (2003) Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc Natl Acad Sci USA 100: 15971-15976.
4. Birtalan, S., and Ghosh, P. (2001) Structure of the Yersinia type III secretory system chaperone SycE. Nat Struct Biol 8: 974-978.
5. Buttner, C.R., Cornelis, G.R., Heinz, D.W., and Niemann, H.H. (2005) Crystal structure of Yersinia enterocolitica type III secretion chaperone SycT. Protein Sci 14: 1993-2002.
6. Byrne, G.I. (1976) Requirements for ingestion of Chlamydia psittaci by mouse fibroblasts (L cells). Infect Immun 14: 645-651.
7. Caldwell, H.D., Kromhout, J., and Schachter, J. (1981) Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun 31: 1161-1176.
8. Carabeo, R.A., Grieshaber, S.S., Fischer, E., and Hackstadt, T. (2002) Chlamydia trachomatis induces remodeling of the actin cytoskeleton during attachment and entry into HeLa cells. Infect Immun 70: 3793-3803.
9. Charpentier, X., and Oswald, E. (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486-5495.
10. Clifton, D.R., Fields, K.A., Grieshaber, S.S., Dooley, C.A., Fischer, E.R., Mead, D.J., etal. (2004) A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. Proc Natl Acad Sci USA 101: 10166-10171.
11. Clifton, D.R., Dooley, C.A., Grieshaber, S.S., Carabeo, R.A., Fields, K.A., and Hackstadt, T. (2005) Phosphorylation of the chlamydial effector protein Tarp is species specific and not required for the recruitment of actin. Infect Immun 73: 3860-3868.
12. Cornelis, G.R., and Van Gijsegem, F. (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54: 735-774.
13. Creasey, E.A., Delahay, R.M., Bishop, A.A., Shaw, R.K., Kenny, B., Knutton, S., and Frankel, G. (2003) CesT is a bivalent enteropathogenic Escherichia coli chaperone required for translocation of both Tir and Map. Mol Microbiol 47: 209-221.
14. Elliott, S.J., Hutcheson, S.W., Dubois, M.S., Mellies, J.L., Wainwright, L.A., Batchelor, M., etal. (1999) Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol Microbiol 33: 1176-1189.
15. Fields, K.A., and Hackstadt, T. (2002) The chlamydial inclusion: escape from the endocytic pathway. Annu Rev Cell Dev Biol 18: 221-245.
16. Fields, K.A., Fischer, E.R., Mead, D.J., and Hackstadt, T. (2005) Analysis of putative Chlamydia trachomatis chaperones Scc2 and Scc3 and their use in the identification of type III secretion substrates. J Bacteriol 187: 6466-6478.
17. Fraser, G.M., Gonzalez-Pedrajo, B., Tame, J.R., and Macnab, R.M. (2003) Interactions of FliJ with the Salmonella type III flagellar export apparatus. J Bacteriol 185: 5546-5554.
18. Ghosh, P. (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
19. Griffith, K.L., and Wolf, R.E., Jr (2002) Measuring beta-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. Biochem Biophys Res Commun 290: 397-402.
20. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
21. Hower, S., Wolf, K., and Fields, K.A. (2009) Evidence that CT694 is a novel Chlamydia trachomatis T3S substrate capable of functioning during invasion or early cycle development. Mol Microbiol 72: 1423-1437.
22. Jamison, W.P., and Hackstadt, T. (2008) Induction of type III secretion by cell-free Chlamydia trachomatis elementary bodies. Microb Pathog 45: 435-440.
23. Jewett, T.J., Fischer, E.R., Mead, D.J., and Hackstadt, T. (2006) Chlamydial TARP is a bacterial nucleator of actin. Proc Natl Acad Sci USA 103: 15599-15604.
24. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
25. Kim, J.F. (2001) Revisiting the chlamydial type III protein secretion system: clues to the origin of type III protein secretion. Trends Genet 17: 65-69.
26. Lane, B.J., Mutchler, C., Al Khodor, S., Grieshaber, S.S., and Carabeo, R.A. (2008) Chlamydial entry involves TARP binding of guanine nucleotide exchange factors. PLoS Pathog 4: e1000014.
27. Lee, V.T., Anderson, D.M., and Schneewind, O. (1998) Targeting of Yersinia Yop proteins into the cytosol of HeLa cells: one-step translocation of YopE across bacterial and eukaryotic membranes is dependent on SycE chaperone. Mol Microbiol 28: 593-601.
28. Letzelter, M., Sorg, I., Mota, L.J., Meyer, S., Stalder, J., Feldman, M., etal. (2006) The discovery of SycO highlights a new function for type III secretion effector chaperones. EMBO J 25: 3223-3233.
29. Luo, Y., Bertero, M.G., Frey, E.A., Pfuetzner, R.A., Wenk, M.R., Creagh, L., etal. (2001) Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat Struct Biol 8: 1031-1036.
30. Matsumoto, H., and Young, G.M. (2009) Essential role of the SycP chaperone in type III secretion of the YspP effector. J Bacteriol 191: 1703-1715.
31. Muschiol, S., Bailey, L., Gylfe, A., Sundin, C., Hultenby, K., Bergstrom, S., etal. (2006) A small-molecule inhibitor of type III secretion inhibits different stages of the infectious cycle of Chlamydia trachomatis. Proc Natl Acad Sci USA 103: 14566-14571.
32. Page, A.L., and Parsot, C. (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46: 1-11.
33. Page, A.L., Fromont-Racine, M., Sansonetti, P., Legrain, P., and Parsot, C. (2001) Characterization of the interaction partners of secreted proteins and chaperones of Shigella flexneri. Mol Microbiol 42: 1133-1145.
34. Pallen, M.J., Beatson, S.A., and Bailey, C.M. (2005) Bioinformatics, genomics and evolution of non-flagellar type-III secretion systems: a Darwinian perspective. FEMS Microbiol Rev 29: 201-229.
35. Rodgers, L., Gamez, A., Riek, R., and Ghosh, P. (2008) The type III secretion chaperone SycE promotes a localized disorder-to-order transition in the natively unfolded effector YopE. J Biol Chem 283: 20857-20863.
36. Schubot, F.D., Jackson, M.W., Penrose, K.J., Cherry, S., Tropea, J.E., Plano, G.V., and Waugh, D.S. (2005) Three-dimensional structure of a macromolecular assembly that regulates type III secretion in Yersinia pestis. J Mol Biol 346: 1147-1161.
37. Singer, A.U., Desveaux, D., Betts, L., Chang, J.H., Nimchuk, Z., Grant, S.R., etal. (2004) Crystal structures of the type III effector protein AvrPphF and its chaperone reveal residues required for plant pathogenesis. Structure 12: 1669-1681.
38. Skipp, P., Robinson, J., O'Connor, C.D. and Clarke, I.N. (2005) Shotgun proteomic analysis of Chlamydia trachomatis. Proteomics 5: 1558-1573.
39. Sory, M.P., and Cornelis, G.R. (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
40. Sory, M.P., Boland, A., Lambermont, I., and Cornelis, G.R. (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 92: 11998-12002.
41. 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.
42. Stebbins, C.E., and Galan, J.E. (2001) Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81.
43. Subtil, A., Delevoye, C., Balana, M.E., Tastevin, L., Perrinet, S., and Dautry-Varsat, A. (2005) A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol Microbiol 56: 1636-1647.
44. Thomas, N.A., Deng, W., Puente, J.L., Frey, E.A., Yip, C.K., Strynadka, N.C., and Finlay, B.B. (2005) CesT is a multi-effector chaperone and recruitment factor required for the efficient type III secretion of both LEE- and non-LEE-encoded effectors of enteropathogenic Escherichia coli. Mol Microbiol 57: 1762-1779.
45. Wolf, K., Betts, H.J., Chellas-Gery, B., Hower, S., Linton, C.N., and Fields, K.A. (2006) Treatment of Chlamydia trachomatis with a small molecule inhibitor of the Yersinia type III secretion system disrupts progression of the chlamydial developmental cycle. Mol Microbiol 61: 1543-1555.
46. Yip, C.K., and Strynadka, N.C. (2006) New structural insights into the bacterial type III secretion system. Trends Biochem Sci 31: 223-230.