Identification of Novel Type III Secretion Chaperone-Substrate Complexes of Chlamydia trachomatis

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Pais, Sara V ^a   Milho, Catarina ^a   Almeida, Filipe ^a   Mota, Luís Jaime ^a,b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; PROTEIN CT082; PROTEIN CT274; PROTEIN CT584; PROTEIN CT694; PROTEIN CT695; PROTEIN CT790; PROTEIN MCSC; PROTEIN SCC4; PROTEIN SLC1; PROTEIN TARP; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; BINDING ASSAY; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; IMMUNOPRECIPITATION; NONHUMAN; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; TWO HYBRID SYSTEM; TYPE III SECRETION SYSTEM; YERSINIA ENTEROCOLITICA;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CHLAMYDIA TRACHOMATIS; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; TWO-HYBRID SYSTEM TECHNIQUES; YERSINIA ENTEROCOLITICA;

EID: 84874196853     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056292     Document Type: Article

References (75)

1. Cornelis GR, (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
2. Thomas NA, Ma I, Prasad ME, Rafuse C, (2012) Expanded Roles for Multicargo and Class 1B Effector Chaperones in Type III Secretion. J Bacteriol 194: 3767-3773.
3. Feldman M, Cornelis GR, (2003) The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol Lett 219: 151-158.
4. Letzelter M, Sorg I, Mota LJ, Meyer S, Stalder J, et al. (2006) The discovery of SycO highlights a new function for type III secretion effector chaperones. EMBO J 25: 3223-3233.
5. Stebbins CE, Galan JE, (2001) Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81.
6. Boyd AP, Lambermont I, Cornelis GR, (2000) Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J Bacteriol 182: 4811-4821.
7. Birtalan SC, Phillips RM, Ghosh P, (2002) Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell 9: 971-980.
8. Lee SH, Galan JE, (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol Microbiol 51: 483-495.
9. Lilic M, Vujanac M, Stebbins CE, (2006) A common structural motif in the binding of virulence factors to bacterial secretion chaperones. Mol Cell 21: 653-664.
10. Parsot C, Hamiaux C, Page AL, (2003) The various and varying roles of specific chaperones in type III secretion systems. Curr Opin Microbiol 6: 7-14.
11. Bebear C, de Barbeyrac B, (2009) Genital Chlamydia trachomatis infections. Clin Microbiol Infect 15: 4-10.
12. Wright HR, Turner A, Taylor HR, (2008) Trachoma. Lancet 371: 1945-1954.
13. Abdelrahman YM, Belland RJ, (2005) The chlamydial developmental cycle. FEMS Microbiol Rev 29: 949-959.
14. Peters J, Wilson DP, Myers G, Timms P, Bavoil PM, (2007) Type III secretion a la Chlamydia. Trends Microbiol 15: 241-251.
15. Betts HJ, Wolf K, Fields KA, (2009) Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal. Curr Opin Microbiol 12: 81-87.
16. Binet R, Maurelli AT, (2009) Transformation and isolation of allelic exchange mutants of Chlamydia psittaci using recombinant DNA introduced by electroporation. Proc Natl Acad Sci USA 106: 292-297.
17. Kari L, Goheen MM, Randall LB, Taylor LD, Carlson JH, et al. (2011) Generation of targeted Chlamydia trachomatis null mutants. Proc Natl Acad Sci USA 108: 7189-7193.
18. Nguyen BD, Valdivia RH, (2012) Virulence determinants in the obligate intracellular pathogen Chlamydia trachomatis revealed by forward genetic approaches. Proc Natl Acad Sci USA 109: 1263-1268.
19. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, et al. (2011) Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLoS Pathog 7: e1002258.
20. Ho TD, Starnbach MN, (2005) The Salmonella enterica serovar typhimurium-encoded type III secretion systems can translocate Chlamydia trachomatis proteins into the cytosol of host cells. Infect Immun 73: 905-911.
21. Subtil A, Delevoye C, Balana ME, Tastevin L, Perrinet S, et al. (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.
22. Muschiol S, Boncompain G, Vromman F, Dehoux P, Normark S, et al. (2011) Identification of a family of effectors secreted by the type III secretion system that are conserved in pathogenic Chlamydiae. Infect Immun 79: 571-580.
23. Fields KA, Hackstadt T, (2000) Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol Microbiol 38: 1048-1060.
24. Clifton DR, Fields KA, Grieshaber SS, Dooley CA, Fischer ER, et al. (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.
25. Hower S, Wolf K, Fields KA, (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.
26. Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E, et al. (2009) Sequence-based prediction of type III secreted proteins. PLoS Pathog 5: e1000376.
27. Samudrala R, Heffron F, McDermott JE, (2009) Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLoS Pathog 5: e1000375.
28. Lower M, Schneider G, (2009) Prediction of type III secretion signals in genomes of gram-negative bacteria. PLoS One 4: e5917.
29. Spaeth KE, Chen YS, Valdivia RH, (2009) The Chlamydia type III secretion system C-ring engages a chaperone-effector protein complex. PLoS Pathog 5: e1000579.
30. Valdivia RH, (2008) Chlamydia effector proteins and new insights into chlamydial cellular microbiology. Curr Opin Microbiol 11: 53-59.
31. Fling SP, Sutherland RA, Steele LN, Hess B, D'Orazio SE, et al. (2001) CD8+ T cells recognize an inclusion membrane-associated protein from the vacuolar pathogen Chlamydia trachomatis. Proc Natl Acad Sci USA 98: 1160-1165.
32. Hobolt-Pedersen AS, Christiansen G, Timmerman E, Gevaert K, Birkelund S, (2009) Identification of Chlamydia trachomatis CT621, a protein delivered through the type III secretion system to the host cell cytoplasm and nucleus. FEMS Immunol Med Microbiol 57: 46-58.
33. Li Z, Chen C, Chen D, Wu Y, Zhong Y, et al. (2008) Characterization of fifty putative inclusion membrane proteins encoded in the Chlamydia trachomatis genome. Infect Immun 76: 2746-2757.
34. Mital J, Miller NJ, Fischer ER, Hackstadt T, (2010) Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network. Cell Microbiol 12: 1235-1249.
35. Brinkworth AJ, Malcolm DS, Pedrosa AT, Roguska K, Shahbazian S, et al. (2011) Chlamydia trachomatis Slc1 is a type III secretion chaperone that enhances the translocation of its invasion effector substrate TARP. Mol Microbiol 82: 131-144.
36. Silva-Herzog E, Joseph SS, Avery AK, Coba JA, Wolf K, et al. (2011) Scc1 (CP0432) and Scc4 (CP0033) function as a type III secretion chaperone for CopN of Chlamydia pneumoniae. J Bacteriol 193: 3490-3496.
37. Betts HJ, Twiggs LE, Sal MS, Wyrick PB, Fields KA, (2008) Bioinformatic and biochemical evidence for the identification of the type III secretion system needle protein of Chlamydia trachomatis. J Bacteriol 190: 1680-1690.
38. Fields KA, Fischer ER, Mead DJ, 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.
39. Scidmore MA (2005) Cultivation and Laboratory Maintenance of Chlamydia trachomatis. Curr Protoc Microbiol Chapter 11: Unit 11A 11.
40. Iriarte M, Cornelis GR, (1998) YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol Microbiol 29: 915-929.
41. Almeida F, Borges V, Ferreira R, Borrego MJ, Gomes JP, et al. (2012) Polymorphisms in Inc Proteins and Differential Expression of inc Genes among Chlamydia trachomatis Strains Correlate with Invasiveness and Tropism of Lymphogranuloma Venereum Isolates. J Bacteriol 194: 6574-6585.
42. Sorg I, Wagner S, Amstutz M, Muller SA, Broz P, et al. (2007) YscU recognizes translocators as export substrates of the Yersinia injectisome. EMBO J 26: 3015-3024.
43. Karimova G, Pidoux J, Ullmann A, Ladant D, (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
44. Kovach ME, Elzer PE, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
45. Studier FW, (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234.
46. Sambrook J, Russel DW (2001) Molecular Cloning: a laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
47. Thomson NR, Holden MT, Carder C, Lennard N, Lockey SJ, et al. (2008) Chlamydia trachomatis: genome sequence analysis of lymphogranuloma venereum isolates. Genome Res 18: 161-171.
48. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, et al. (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282: 754-759.
49. Pallen MJ, Francis MS, Futterer K, (2003) Tetratricopeptide-like repeats in type-III-secretion chaperones and regulators. FEMS Microbiol Lett 223: 53-60.
50. Markham AP, Jaafar ZA, Kemege KE, Middaugh CR, Hefty PS, (2009) Biophysical characterization of Chlamydia trachomatis CT584 supports its potential role as a type III secretion needle tip protein. Biochemistry 48: 10353-10361.
51. Stone CB, Sugiman-Marangos S, Bulir DC, Clayden RC, Leighton TL, et al. (2012) Structural characterization of a novel Chlamydia pneumoniae type III secretion-associated protein, Cpn0803. PLoS ONE 7: e30220.
52. Dehoux P, Flores R, Dauga C, Zhong G, Subtil A, (2011) Multi-genome identification and characterization of chlamydiae-specific type III secretion substrates: the Inc proteins. BMC Genomics 12: 109.
53. Chellas-Gery B, Linton CN, Fields KA, (2007) Human GCIP interacts with CT847, a novel Chlamydia trachomatis type III secretion substrate, and is degraded in a tissue-culture infection model. Cell Microbiol 9: 2417-2430.
54. Saka HA, Thompson JW, Chen YS, Kumar Y, Dubois LG, et al. (2011) Quantitative proteomics reveals metabolic and pathogenic properties of Chlamydia trachomatis developmental forms. Mol Microbiol 82: 1185-1203.
55. Journet L, Agrain C, Broz P, Cornelis GR, (2003) The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302: 1757-1760.
56. Lara-Tejero M, Kato J, Wagner S, Liu X, Galan JE, (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331: 1188-1191.
57. Sukhan A, Kubori T, Wilson J, Galan JE, (2001) Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J Bacteriol 183: 1159-1167.
58. Lee VT, Tam C, Schneewind O, (2000) LcrV, a substrate for Yersinia enterocolitica type III secretion, is required for toxin targeting into the cytosol of HeLa cells. J Biol Chem 275: 36869-36875.
59. Munera D, Crepin VF, Marches O, Frankel G, (2010) N-terminal type III secretion signal of enteropathogenic Escherichia coli translocator proteins. J Bacteriol 192: 3534-3539.
60. Pettersson J, Nordfelth R, Dubinina E, Bergman T, Gustafsson M, et al. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273: 1231-1233.
61. Stainier I, Iriarte M, Cornelis GR, (1997) YscM1 and YscM2, two Yersinia enterocolitica proteins causing down regulation of yop transcription. Mol Microbiol 26: 833-843.
62. Stainier I, Bleves S, Josenhans C, Karmani L, Kerbourch C, et al. (2000) YscP, a Yersinia protein required for Yop secretion that is surface exposed, and released in low Ca2+. Mol Microbiol 37: 1005-1018.
63. Lee VT, Mazmanian SK, Schneewind O, (2001) A program of Yersinia enterocolitica type III secretion reactions is activated by specific signals. J Bacteriol 183: 4970-4978.
64. Costa SC, Schmitz AM, Jahufar FF, Boyd JD, Cho MY, et al. (2012) A new means to identify type 3 secreted effectors: functionally interchangeable class IB chaperones recognize a conserved sequence. MBio 3: e00243-00211.
65. Bullock HD, Hower S, Fields KA, (2012) Domain Analyses Reveal That Chlamydia trachomatis CT694 Protein Belongs to the Membrane-localized Family of Type III Effector Proteins. J Biol Chem 287: 28078-28086.
66. Jewett TJ, Miller NJ, Dooley CA, Hackstadt T, (2010) The conserved Tarp actin binding domain is important for chlamydial invasion. PLoS Pathog 6: e1000997.
67. Lane BJ, Mutchler C, Al Khodor S, Grieshaber SS, Carabeo RA, (2008) Chlamydial entry involves TARP binding of guanine nucleotide exchange factors. PLoS Pathog 4: e1000014.
68. Olsson J, Edqvist PJ, Broms JE, Forsberg A, Wolf-Watz H, et al. (2004) The YopD translocator of Yersinia pseudotuberculosis is a multifunctional protein comprised of discrete domains. J Bacteriol 186: 4110-4123.
69. Neyt C, Cornelis GR, (1999) Role of SycD, the chaperone of the Yersinia translocators YopB and YopD. Mol Microbiol 31: 143-156.
70. Bennet JC, Hughes C, (2000) From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol 8: 202-204.
71. Yip CK, Finlay BB, Strynadka NC, (2005) Structural characterization of a type III secretion system filament protein in complex with its chaperone. Nat Struct Mol Biol 12: 75-81.
72. Kurushima J, Kuwae A, Abe A, (2012) Btc22 chaperone is required for secretion and stability of the type III secreted protein Bsp22 in Bordetella bronchiseptica. FEMS Microbiol Lett 331: 144-151.
73. Zurawski DV, Stein MA, (2004) The SPI2-encoded SseA chaperone has discrete domains required for SseB stabilization and export, and binds within the C-terminus of SseB and SseD. Microbiology 150: 2055-2068.
74. Rost B, Yachdav G, Liu J, (2004) The PredictProtein server. Nucleic Acids Res 32: W321-326.
75. Dyson HJ, Wright PE, (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208.