Early expression of the type III secretion system of Parachlamydia acanthamoebae during a replicative cycle within its natural host cell Acanthamoeba castellanii

Pathogens and Disease

Volumn 69, Issue 3, 2013, Pages 159-175

  Croxatto, Antony ^a   Murset, Valérie ^a,b   Chassot, Bérénice ^a,c   Greub, Gilbert ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Chlamydia; Intracellular bacteria; Type III secretion system

Indexed keywords

BACTERIAL RNA; CHAPERONIN 60; DNA TOPOISOMERASE (ATP HYDROLYSING) B; RNA 16S; RNA POLYMERASE BETA SUBUNIT; SECY PROTEIN;

ACANTHAMOEBA CASTELLANII; ARTICLE; BACTERIAL GROWTH; CELL VACUOLE; CHLAMYDIA TRACHOMATIS; CHLAMYDIACEAE; CONFOCAL MICROSCOPY; INTRACELLULAR BACTERIUM; NONHUMAN; PARACHLAMYDIA ACANTHAMOEBAE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOZOITE; TYPE III SECRETION SYSTEM; WESTERN BLOTTING;

CHLAMYDIA; INTRACELLULAR BACTERIA; TYPE III SECRETION SYSTEM;

ACANTHAMOEBA CASTELLANII; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CHLAMYDIACEAE INFECTIONS; CHLAMYDIALES; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; HOST-PATHOGEN INTERACTIONS; LIFE CYCLE STAGES; RNA, RIBOSOMAL, 16S; TRANSCRIPTION, GENETIC;

EID: 84900309817     PISSN: None     EISSN: 2049632X     Source Type: Journal    
DOI: 10.1111/2049-632X.12065     Document Type: Article

References (49)

1. Bailey L, Gylfe A, Sundin C, Muschiol S, Elofsson M, Nordstrom P et al. (2007) Small molecule inhibitors of type III secretion in Yersinia block the Chlamydia pneumoniae infection cycle. FEBS Lett 581: 587-595.
2. Bannantine JP, Griffiths RS, Viratyosin W, Brown WJ & Rockey DD (2000) A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane. Cell Microbiol 2: 35-47.
3. Beeckman DS & Vanrompay DC (2010) Bacterial secretion systems with an emphasis on the chlamydial Type III secretion system. Curr Issues Mol Biol 12: 17-41.
4. Beeckman DS, Geens T, Timmermans JP, Van Oostveldt P & Vanrompay DC (2008) Identification and characterization of a type III secretion system in Chlamydophila psittaci. Vet Res 39: 27.
5. Bertelli C, Collyn F, Croxatto A, Ruckert C, Polkinghorne A, Kebbi-Beghdadi C et al. (2010) The Waddlia genome: a window into chlamydial biology. PLoS ONE 5: e10890.
6. 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.
7. Betts-Hampikian HJ & Fields KA (2010) The chlamydial type III secretion mechanism: revealing cracks in a tough nut. Front Microbiol 1: 114.
8. Case ED, Peterson EM & Tan M (2010) Promoters for Chlamydia type III secretion genes show a differential response to DNA supercoiling that correlates with temporal expression pattern. J Bacteriol 192: 2569-2574.
9. Casson N, Medico N, Bille J & Greub G (2006) Parachlamydia acanthamoebae enters and multiplies within pneumocytes and lung fibroblasts. Microbes Infect 8: 1294-1300.
10. Casson N, Entenza JM, Borel N, Pospischil A & Greub G (2008) Murine model of pneumonia caused by Parachlamydia acanthamoebae. Microb Pathog 45: 92-97.
11. Chellas-Gery B, Wolf K, Tisoncik J, Hackstadt T & Fields KA (2011) Biochemical and localization analyses of putative type III secretion translocator proteins CopB and CopB2 of Chlamydia trachomatis reveal significant distinctions. Infect Immun 79: 3036-3045.
12. Clifton DR, Fields KA, Grieshaber SS, Dooley CA, Fischer ER, Mead DJ et al. (2004) A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. P Natl Acad Sci USA 101: 10166-10171.
13. Coburn B, Sekirov I & Finlay BB (2007) Type III secretion systems and disease. Clin Microbiol Rev 20: 535-549.
14. Collingro A, Tischler P, Weinmaier T, Penz T, Heinz E, Brunham RC et al. (2011) Unity in variety - the pan-genome of the Chlamydiae. Mol Biol Evol 28: 3253-3270.
15. Cornelis GR (2002) The Yersinia Ysc-Yop 'type III' weaponry. Nat Rev Mol Cell Biol 3: 742-752.
16. Corsaro D & Greub G (2006) Pathogenic potential of novel Chlamydiae and diagnostic approaches to infections due to these obligate intracellular bacteria. Clin Microbiol Rev 19: 283-297.
17. Diepold A, Amstutz M, Abel S, Sorg I, Jenal U & Cornelis GR (2010) Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J 29: 1928-1940.
18. Fields KA & Hackstadt T (2000) Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol Microbiol 38: 1048-1060.
19. Fields KA & Hackstadt T (2006) The Chlamydia Type III secretion system: structure and implications for pathogenesis. Chlamydia: Genomics and Pathogenesis. (Wyrick PB & Bavoil PM, eds), pp. 219-233. Horizon Bioscience, Norfolk, UK.
20. Fields KA, Mead DJ, Dooley CA & Hackstadt T (2003) Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol Microbiol 48: 671-683.
21. Francis MS, Wolf-Watz H & Forsberg A (2002) Regulation of type III secretion systems. Curr Opin Microbiol 5: 166-172.
22. Goss JW, Sorg JA, Ramamurthi KS, Ton-That H & Schneewind O (2004) The secretion signal of YopN, a regulatory protein of the Yersinia enterocolitica type III secretion pathway. J Bacteriol 186: 6320-6324.
23. Goy G, Croxatto A & Greub G (2008) Waddlia chondrophila enters and multiplies within human macrophages. Microbes Infect 10: 556-562.
24. Greub G (2009) Parachlamydia acanthamoebae, an emerging agent of pneumonia. Clin Microbiol Infect 15: 18-28.
25. Greub G & Raoult D (2002) Crescent bodies of Parachlamydia acanthamoeba and its life cycle within Acanthamoeba polyphaga: an electron micrograph study. Appl Environ Microbiol 68: 3076-3084.
26. Greub G & Raoult D (2003) History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. Appl Environ Microbiol 69: 5530-5535.
27. Greub G & Raoult D (2004) Microorganisms resistant to free-living amoebae. Clin Microbiol Rev 17: 413-433.
28. Greub G, Mege JL & Raoult D (2003a) Parachlamydia acanthamoebae enters and multiplies within human macrophages and induces their apoptosis. Infect Immun 71: 5979-5985.
29. Greub G, Berger P, Papazian L & Raoult D (2003b) Parachlamydiaceae as rare agents of pneumonia. Emerg Infect Dis 9: 755-756.
30. Greub G, Boyadjiev I, La Scola B, Raoult D & Martin C (2003c) Serological hint suggesting that Parachlamydiaceae are agents of pneumonia in polytraumatized intensive care patients. Ann N Y Acad Sci 990: 311-319.
31. Greub G, Desnues B, Raoult D & Mege JL (2005a) Lack of microbicidal response in human macrophages infected with Parachlamydia acanthamoebae. Microbes Infect 7: 714-719.
32. Greub G, Mege JL, Gorvel JP, Raoult D & Meresse S (2005b) Intracellular trafficking of Parachlamydia acanthamoebae. Cell Microbiol 7: 581-589.
33. Greub G, Kebbi-Beghdadi C, Bertelli C, Collyn F, Riederer BM, Yersin C et al. (2009) High throughput sequencing and proteomics to identify immunogenic proteins of a new pathogen: the dirty genome approach. PLoS ONE 4: e8423.
34. Hefty PS & Stephens RS (2007) Chlamydial type III secretion system is encoded on ten operons preceded by sigma 70-like promoter elements. J Bacteriol 189: 198-206.
35. Horn M, Collingro A, Schmitz-Esser S, Beier CL, Purkhold U, Fartmann B et al. (2004) Illuminating the evolutionary history of chlamydiae. Science 304: 728-730.
36. Huang J, Lesser CF & Lory S (2008) The essential role of the CopN protein in Chlamydia pneumoniae intracellular growth. Nature 456: 112-115.
37. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
38. Jackson MW & Plano GV (2000) Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol Lett 186: 85-90.
39. Jamison WP & Hackstadt T (2008) Induction of type III secretion by cell-free Chlamydia trachomatis elementary bodies. Microb Pathog 45: 435-440.
40. Joseph SS & Plano GV (2007) Identification of TyeA residues required to interact with YopN and to regulate Yop secretion. Adv Exp Med Biol 603: 235-245.
41. Lamoth F & Greub G (2009) Amoebal pathogens as emerging causal agents of pneumonia. FEMS Microbiol Rev 34: 260-280.
42. Lugert R, Kuhns M, Polch T & Gross U (2004) Expression and localization of type III secretion-related proteins of Chlamydia pneumoniae. Med Microbiol Immunol 193: 163-171.
43. Mota LJ & Cornelis GR (2005) The bacterial injection kit: type III secretion systems. Ann Med 37: 234-249.
44. Muschiol S, Bailey L, Gylfe A, Sundin C, Hultenby K, Bergstrom S et al. (2006) A small-molecule inhibitor of type III secretion inhibits different stages of the infectious cycle of Chlamydia trachomatis. P Natl Acad Sci USA 103: 14566-14571.
45. Noursadeghi M, Tsang J, Haustein T, Miller RF, Chain BM & Katz DR (2008) Quantitative imaging assay for NF-kappaB nuclear translocation in primary human macrophages. J Immunol Methods 329: 194-200.
46. Peters J, Wilson DP, Myers G, Timms P & Bavoil PM (2007) Type III secretion a la Chlamydia. Trends Microbiol 15: 241-251.
47. Riordan KE & Schneewind O (2008) YscU cleavage and the assembly of Yersinia type III secretion machine complexes. Mol Microbiol 68: 1485-1501.
48. Slepenkin A, Motin V, de la Maza LM & Peterson EM (2003) Temporal expression of type III secretion genes of Chlamydia pneumoniae. Infect Immun 71: 2555-2562.
49. Subtil A, Delevoye C, Balana ME, Tastevin L, Perrinet S & 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.