Multi-genome identification and characterization of chlamydiae-specific type III secretion substrates: The Inc proteins

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Dehoux, Pierre ^a   Flores, Rhonda ^b   Dauga, Catherine ^a   Zhong, Guangming ^b   Subtil, Agathe ^a,c  

^a INSTITUT PASTEUR   (France)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; BACTERIAL PROTEIN; CYSTEINE RICH PROTEIN A; INCLUSION MEMBRANE PROTEIN; INCLUSION MEMBRANE PROTEIN A; INCLUSION MEMBRANE PROTEIN B; INCLUSION MEMBRANE PROTEIN C; INCLUSION MEMBRANE PROTEIN D; INCLUSION MEMBRANE PROTEIN E; INCLUSION MEMBRANE PROTEIN F; INCLUSION MEMBRANE PROTEIN G; TETRATRICOPEPTIDE REPEAT PROTEIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PROTEOME;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; BIOINFORMATICS; CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDOPHILA PNEUMONIAE; CONTROLLED STUDY; GENE SEQUENCE; HUMAN; HUMAN CELL; HYDROPHOBICITY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM; AMINO ACID SEQUENCE; BACTERIAL SECRETION SYSTEM; BIOLOGY; GENETICS; HELA CELL; MOLECULAR GENETICS; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

CHLAMYDIA TRACHOMATIS; CHLAMYDIAE; CHLAMYDOPHILA PNEUMONIAE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CHLAMYDIA; COMPUTATIONAL BIOLOGY; GENOME, BACTERIAL; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; PROTEOME; SEQUENCE ALIGNMENT;

EID: 79951553486     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-109     Document Type: Article

References (82)

1. Horn M. Chlamydiae as symbionts in eukaryotes. Annu Rev Microbiol 2008, 62:113-131.
2. Wright HR, Turner A, Taylor HR. Trachoma. Lancet 2008, 371(9628):1945-1954.
3. Gerbase AC, Rowley JT, Heymann DHL, Berkley SFB, Piot P. Global prevalence and incidence estimates of selected curable STDs. Sex Transm Infect 1998, 74:S12-S16.
4. Blasi F, Tarsia P, Aliberti S. Chlamydophila pneumoniae. Clinical Microbiology And Infection 2009, 15(1):29-35.
5. AbdelRahman YM, Belland RJ. The chlamydial developmental cycle. FEMS Microbiol Rev 2005, 29(5):949-959.
6. Moore ER, Fischer ER, Mead DJ, Hackstadt T. The Chlamydial Inclusion Preferentially Intercepts Basolaterally Directed Sphingomyelin-Containing Exocytic Vacuoles. Traffic 2008, 9(12):2130-2140.
7. Beatty WL. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 2008, 76(7):2872-2881.
8. Kumar Y, Cocchiaro J, Valdivia RH. The obligate intracellular pathogen Chiamydia trachomatis targets host lipid droplets. Curr Biol 2006, 16(16):1646-1651.
9. Hasegawa A, Sogo LF, Tan M, Sutterlin C. Host Complement Regulatory Protein CD59 Is Transported to the Chlamydial Inclusion by a Golgi Apparatus-Independent Pathway. Infect Immun 2009, 77(4):1285-1292.
10. Rockey DD, Heinzen RA, Hackstadt T. Cloning and characterization of a Chlamydia psittaci gene coding for a protein localized in the inclusion membrane of infected cells. Mol Microbiol 1995, 15:617-626.
11. Hackstadt T, Scidmore-Carlson MA, Shaw EI, Fischer ER. The Chlamydia trachomatis IncA protein is required for homotypic vesicle fusion. Cell Microbiol 1999, 1:119-130.
12. Suchland RJ, Rockey DD, Bannantine JP, Stamm WE. Isolates of Chlamydia trachomatis that occupy nonfusogenic inclusions lack IncA, a protein localized to the inclusion membrane. Infect Immun 2000, 68:360-367.
13. Delevoye C, Nilges M, Dehoux P, Paumet F, Perrinet S, Dautry-Varsat A, Subtil A. SNARE protein mimicry by an intracellular bacterium. PLoS Pathog 2008, 4(3):e1000022.
14. Bannantine JP, Rockey DD, Hackstadt T. Tandem genes of Chlamydia psittaci that encode proteins localized to the inclusion membrane. Mol Microbiol 1998, 28(5):1017-1026.
15. Scidmore-Carlson MA, Shaw EI, Dooley CA, Fischer ER, Hackstadt T. Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol Microbiol 1999, 33:753-765.
16. Bannantine JP, Griffiths RS, Viratyosin W, Brown WJ, Rockey DD. A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell Microbiol 2000, 2:35-47.
17. Toh H, Miura K, Shirai M, Hattori M. In silico inference of inclusion membrane protein family in obligate intracellular parasites chlamydiae. DNA Res 2003, 10(1):9-17.
18. Li Z, Chen C, Chen D, Wu Y, Zhong Y, Zhong G. Characterization of fifty putative inclusion membrane proteins encoded in the Chlamydia trachomatis genome. Infect Immun 2008, 76(6):2746-2757.
19. Rockey DD, Grosenbach D, Hruby DE, Peacock MG, Heinzen RA, Hackstadt T. Chlamydia psittaci IncA is phosphorylated by the host cell and is exposed on the cytoplasmic face of the developing inclusion. Mol Microbiol 1997, 24:217-228.
20. Cortes C, Rzomp MA, Tvinnereim A, Scidmore MA, Wizel B. Chlamydia pneumoniae inclusion membrane protein cpn0585 interacts with multiple rab GTPases. Infect Immun 2007, 75(12):5586-5596.
21. Scidmore MA, Hackstadt T. Mammalian 14-3-3 beta associates with the Chlamydia trachomatis inclusion membrane via its interaction with IncG. Mol Microbiol 2001, 39(6):1638-1650.
22. Wolf K, Plano GV, Fields KA. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs IL-17 signaling via interaction with human Act1. Cell Microbiol 2009, 11(5):769-779.
23. Fields KA, Mead DJ, Dooley CA, Hackstadt T. Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol Microbiol 2003, 48(3):671-683.
24. Subtil A, Parsot C, Dautry-Varsat A. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol Microbiol 2001, 39(3):792-800.
25. Shaw EI, Dooley CA, Fischer ER, Scidmore MA, Fields KA, Hackstadt T. Three temporal classes of gene expression during the Chlamydia trachomatis developmental cycle. Molecular Microbiology [print] 2000, 37(4):913-925.
26. Belland RJ, Zhong GM, Crane DD, Hogan D, Sturdevant D, Sharma J, Beatty WL, Caldwell HD. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc Natl Acad Sci USA 2003, 100(14):8478-8483.
27. von Heijne G. The membrane protein universe: what's out there and why bother?. J Intern Med 2007, 261(6):543-557.
28. Juretić D, Zoranić L, Zucić D. Basic charge clusters and predictions of membrane protein topology. J Chem Inf Comput Sci 2002, 42(3):620-632.
29. Hermansson M, Monné M, von Heijne G. Formation of helical hairpins during membrane protein integration into the endoplasmic reticulum membrane. Role of the N and C-terminal flanking regions. J Mol Biol 2001, 313(5):1171-1179.
30. Monné M, Hermansson M, von Heijne G. A turn propensity scale for transmembrane helices. J Mol Biol 1999, 288(1):141-145.
31. Bernsel A, Viklund H, Falk J, Lindahl E, von Heijne G, Elofsson A. Prediction of membrane-protein topology from first principles. Proc Natl Acad Sci USA 2008, 105(20):7177-7181.
32. Monné M, Nilsson I, Elofsson A, von Heijne G. Turns in transmembrane helices: determination of the minimal length of a "helical hairpin" and derivation of a fine-grained turn propensity scale. J Mol Biol 1999, 293(4):807-814.
33. Käll L, Krogh A, Sonnhammer ELL. An HMM posterior decoder for sequence feature prediction that includes homology information. Bioinformatics 2005, 21(Suppl 1):i251-257.
34. Alexeyenko A, Tamas I, Liu G, Sonnhammer EL. Automatic clustering of orthologs and inparalogs shared by multiple proteomes. Bioinformatics 2006, 22(14):e9-15.
35. Mital J, Miller NJ, Fischer ER, Hackstadt T. Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network. Cellular Microbiology 2010, 12(9):1235.
36. Subtil A, Delevoye C, Balañá ME, Tastevin L, Perrinet S, Dautry-Varsat A. A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol Microbiol 2005, 56(6):1636-1647.
37. Luo J, Liu G, Zhong Y, Jia T, Liu K, Chen D, Zhong G. Characterization of hypothetical proteins Cpn0146, 0147, 0284 & 0285 that are predicted to be in the Chlamydia pneumoniae inclusion membrane. BMC Microbiol 2007, 7:38.
38. Dani N, Stilla A, Marchegiani A, Tamburro A, Till S, Ladurner AG, Corda D, Di Girolamo M. Combining affinity purification by ADP-ribose-binding macro domains with mass spectrometry to define the mammalian ADP-ribosyl proteome. Proc Natl Acad Sci USA 2009, 106(11):4243-4248.
39. Karras GI, Kustatscher G, Buhecha HR, Allen MD, Pugieux C, Sait F, Bycroft M, Ladurner AG. The macro domain is an ADP-ribose binding module. The EMBO Journal 2005, 24(11):1911-1920.
40. Neuvonen M, Ahola T. Differential activities of cellular and viral macro domain proteins in binding of ADP-ribose metabolites. J Mol Biol 2009, 385(1):212-225.
41. Delahay RM, Frankel G. Coiled-coil proteins associated with type III secretion systems: a versatile domain revisited. Mol Microbiol 2002, 45(4):905-916.
42. Gazi AD, Charova SN, Panopoulos NJ, Kokkinidis M. Coiled-coils in type III secretion systems: structural flexibility, disorder and biological implications. Cell Microbiol 2009, 11(5):719-729.
43. D'Andrea LD, Regan L. TPR proteins: the versatile helix. Trends Biochem Sci 2003, 28(12):655-662.
44. Liu J, Rost B. Comparing function and structure between entire proteomes. Protein Sci 2001, 10(10):1970-1979.
45. Odgren P, Harvie LJ, Fey E. Phylogenetic occurrence of coiled coil proteins: implications for tissue structure in metazoa via a coiled coil tissue matrix. Proteins 1996, 24:467-484.
46. Rose A, Schraegle SJ, Stahlberg EA, Meier I. Coiled-coil protein composition of 22 proteomes--differences and common themes in subcellular infrastructure and traffic control. BMC Evol Biol 2005, 5:66.
47. Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E, Behrens S, Niinikoski A, Mewes HW, Horn M, Rattei T. Sequence-based prediction of type III secreted proteins. PLoS Pathog 2009, 5(4):e1000376.
48. Samudrala R, Heffron F, McDermott JE. Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLoS Pathog 2009, 5(4):e1000375.
49. Parsot C, Hamiaux C, Page AL. The various and varying roles of specific chaperones in type III secretion systems. Curr Opin Microbiol 2003, 6(1):7-14.
50. Remm M, Storm CE, Sonnhammer EL. Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J Mol Biol 2001, 314(5):1041-1052.
51. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
52. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, et al. CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 2009, (37 Database):D205-210.
53. Eddy SR. Profile hidden Markov models. Bioinformatics 1998, 14(9):755-763.
54. Krogh A, Brown M, Mian IS, Sjölander K, Haussler D. Hidden Markov models in computational biology. Applications to protein modeling. J Mol Biol 1994, 235(5):1501-1531.
55. Pirovano W, Feenstra KA, Heringa J. PRALINETM: a strategy for improved multiple alignment of transmembrane proteins. Bioinformatics 2008, 24(4):492-497.
56. Brendel V, Bucher P, Nourbakhsh IR, Blaisdell BE, Karlin S. Methods and algorithms for statistical analysis of protein sequences. Proc Natl Acad Sci USA 1992, 89(6):2002-2006.
57. Montgomerie S, Cruz JA, Shrivastava S, Arndt D, Berjanskii M, Wishart DS. PROTEUS2: a web server for comprehensive protein structure prediction and structure-based annotation. Nucleic Acids Res 2008, (36 Web Server):W202-209.
58. Lupas A, Van Dyke M, Stock J. Predicting coiled coils from protein sequences. Science 1991, 252(5009):1162-1164.
59. Delorenzi M, Speed T. An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 2002, 18(4):617-625.
60. Gautier R, Douguet D, Antonny B, Drin G. HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 2008, 24(18):2101-2102.
61. Karpenahalli MR, Lupas AN, Söding J. TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinformatics 2007, 8:2.
62. Bornberg-Bauer E, Rivals E, Vingron M. Computational approaches to identify leucine zippers. Nucleic Acids Res 1998, 26(11):2740-2746.
63. Allaoui A, Sansonetti PJ, Parsot C. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri lpa invasins. Mol Microbiol 1993, 7(1):59-68.
64. Ménard R, Sansonetti PJ, Parsot C. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 1993, 175(18):5899-5906.
65. Chen CQ, Chen D, Sharma J, Cheng W, Zhong YM, Liu KY, Jensen J, Shain R, Arulanandam B, Zhong GM. The hypothetical protein CT813 is localized in the Chlamydia trachomatis inclusion membrane and is immunogenic in women urogenitally infected with C. trachomatis. Infect Immun 2006, 74(8):4826-4840.
66. Sharma J, Zhong Y, Dong F, Piper JM, Wang G, Zhong G. Profiling of human antibody responses to Chlamydia trachomatis urogenital tract infection using microplates arrayed with 156 chlamydial fusion proteins. Infect Immun 2006, 74(3):1490-1499.
67. Zhong G, Toth I, Reid R, Brunham RC. Immunogenicity evaluation of a lipidic amino acid-based synthetic peptide vaccine for Chlamydia trachomatis. J Immunol 1993, 151(7):3728-3736.
68. Dong F, Zhong Y, Arulanandam B, Zhong G. Production of a proteolytically active protein, chlamydial protease/proteasome-like activity factor, by five different Chlamydia species. Infect Immun 2005, 73(3):1868-1872.
69. Fan T, Lu H, Hu H, Shi L, McClarty GA, Nance DM, Greenberg AH, Zhong G. Inhibition of apoptosis in Chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J Exp Med 1998, 187(4):487-496.
70. Greene W, Xiao Y, Huang Y, McClarty G, Zhong G. Chlamydia-infected cells continue to undergo mitosis and resist induction of apoptosis. Infect Immun 2004, 72(1):451-460.
71. Xiao Y, Zhong Y, Greene W, Dong F, Zhong G. Chlamydia trachomatis infection inhibits both Bax and Bak activation induced by staurosporine. Infect Immun 2004, 72(9):5470-5474.
72. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics (Oxford, England) 2009, 25(1):119-120.
73. Vretou E, Katsiki E, Psarrou E, Vougas K, Tsangaris GT. Identification and characterization of Inc766, an inclusion membrane protein in Chlamydophila abortus-infected cells. Microb Pathog 2008, 45(4):265-272.
74. Ohya K, Takahara Y, Kuroda E, Koyasu S, Hagiwara S, Sakamoto M, Hisaka M, Morizane K, Ishiguro S, Yamaguchi T, et al. Chlamydophila felis CF0218 Is a Novel TMH Family Protein with Potential as a Diagnostic Antigen for Diagnosis of C. felis Infection. Clin Vaccine Immunol %R 101128/CVI00134-08 2008, 15(10):1606-1615.
75. Luo J, Jia T, Flores R, Chen D, Zhong G. Hypothetical protein Cpn0308 is localized in the Chlamydia pneumoniae inclusion membrane. Infect Immun 2007, 75(1):497-503.
76. Luo J, Jia T, Zhong Y, Chen D, Flores R, Zhong G. Localization of the hypothetical protein Cpn0585 in the inclusion membrane of Chlamydia pneumoniae-infected cells. Microb Pathog 2007, 42(2-3):111-116.
77. Flores R, Luo J, Chen D, Sturgeon G, Shivshankar P, Zhong Y, Zhong G. Characterization of the hypothetical protein Cpn1027, a newly identified inclusion membrane protein unique to Chlamydia pneumoniae. Microbiology 2007, 153(Pt 3):777-786.
78. Delevoye C, Nilges M, Dautry-Varsat A, Subtil A. Conservation of the biochemical properties of IncA from Chlamydia trachomatis and Chlamydia caviae: oligomerization of IncA mediates interaction between facing membranes. J Biol Chem 2004, 279(45):46896-46906.
79. Rzomp KA, Moorhead AR, Scidmore MA. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 2006, 74(9):5362-5373.
80. Jia TJ, Liu DW, Luo JH, Zhong GM. [Localization of the hypothetical protein CT249 in the Chlamydia trachomatis inclusion membrane]. Wei Sheng Wu Xue Bao 2007, 47(4):645-648.
81. Sisko JL, Spaeth K, Kumar Y, Valdivia RH. Multifunctional analysis of Chlamydia-specific genes in a yeast expression system. Mol Microbiol 2006, 60(1):51-66.
82. Heinz E, Rockey DD, Montanaro J, Aistleitner K, Wagner M, Horn M. Inclusion membrane proteins of Protochlamydia amoebophila UWE25 reveal a conserved mechanism for host cell interaction among the Chlamydiae. J Bacteriol 2010, 192(19):5093-5102.