Application of β-lactamase reporter fusions as an indicator of effector protein secretion during infections with the obligate intracellular pathogen Chlamydia trachomatis

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Mueller, Konrad E ^a   Fields, Kenneth A ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA LACTAMASE; BETA LACTAMASE TEM 1; EFFECTOR PROTEIN; UNCLASSIFIED DRUG; BETA-LACTAMASE TEM-1; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHOTOPROTEIN; RED FLUORESCENT PROTEIN; TYPE III SECRETION SYSTEM;

ARTICLE; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DISEASE COURSE; FOLLOW UP; HOST PATHOGEN INTERACTION; IMMUNOFLUORESCENCE TEST; NONHUMAN; PROTEIN DETERMINATION; PROTEIN SECRETION; BACTERIUM TRANSFORMATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; NEISSERIA MENINGITIDIS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLASMID; PROMOTER REGION; REPORTER GENE; SECRETION (PROCESS); TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; BASE SEQUENCE; BETA-LACTAMASES; CHLAMYDIA TRACHOMATIS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; PLASMIDS; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; TRANSFORMATION, BACTERIAL; TYPE III SECRETION SYSTEMS;

EID: 84942626926     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135295     Document Type: Article

References (58)

1. Schachter J (1999) Infection and disease epidemiology. In: Stephens RS, editor. Chlamydia; Intracellular biology, pathogenesis, and immunity. Washington, D. C.: ASM Press. pp. 139-169.
2. Nunes A, Gomes JP (2014) Evolution, phylogeny, and molecular epidemiology of Chlamydia. Infection, Genetics and Evolution 23:49-64. doi: 10.1016/j.meegid.2014.01.029 PMID: 24509351
3. Moulder JW (1991) Interaction of chlamydiae and host cells in vitro. Microbiol Rev 55:143-190. PMID: 2030670
4. Hybiske K, Stephens RS (2007) Mechanisms of host cell exit by the intracellular bacterium Chlamydia. PNAS 104:11430-11435. PMID: 17592133
5. Heinzen RA, Hackstadt T (1997) The Chlamydia trachomatis parasitophorous vacuolar membrane is not passively permeable to low-molecular-weight compounds. Infect Immun 65:1088-1094. PMID: 9038320
6. Betts-Hampikian HJ, Fields KA (2010) The chlamydial type III secretion mechanism: revealing cracks in a tough nut. Frontiers in Microbiol 1:114.
7. Saka HA, Thompson JW, Chen Y-S, Kumar Y, Dubois LG, Moseley M, et al. (2011) Quantitative proteomics reveals metabolic and pathogenic properties of Chlamydia trachomatis developmental forms. Molecular Microbiology 82:1185-1203. doi: 10.1111/j.1365-2958.2011.07877.x PMID: 22014092
8. Fields K, Mead D, Dooley C, Hackstadt T (2003) Chlamydia trachomatis type III secretion: evidence for afunctional apparatus during early-cycle development. Mol Microbiol 48:671-683. PMID: 12694613
9. Clifton D, Fields K, Grieshaber N, Dooley C, Fischer E, Mead D, 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. PMID: 15199184
10. Chen Y-S, Bastidas RJ, Saka HA, Carpenter VK, Richards KL, Plano G, et al. (2014) The Chlamydia trachomatis Type III Secretion Chaperone Slc1 Engages Multiple Early Effectors, Including TepP, a Tyrosine-phosphorylated Protein Required for the Recruitment of CrkI-II to Nascent Inclusions and Innate Immune Signaling. PLoS Pathog 10:e1003954. doi: 10.1371/journal.ppat.1003954 PMID: 24586162
11. 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. doi: 10.1111/j.1365-2958.2009.06732.x PMID: 19460098
12. Betts HJ, Wolf K, Fields KA (2009) Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal. CurrOpin Microbiol 12:81-87. doi: 10.1016/j.mib.2008.11.009 PMID: 19138553
13. Gauliard E, Ouellette SP, Rueden KJ, Ladant D (2015) Characterization of interactions between inclusion membrane proteins from Chlamydia trachomatis. Front Cell Infect Microbiol 5:1-11. doi: 10.3389/fcimb.2015.00001 PMID: 25674541
14. Mital J, Miller NJ, Dorward DW, Dooley CA, Hackstadt T (2013) Role for Chlamydial Inclusion Membrane Proteins in Inclusion Membrane Structure and Biogenesis. PLoS ONE 8:e63426. doi: 10.1371/journal.pone.0063426 PMID: 23696825
15. 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. PMID: 16159780
16. Pais SV, Milho C, Almeida F, Mota LJ (2013) Identification of Novel Type III Secretion Chaperone-Substrate Complexes of Chlamydia trachomatis. PLoS ONE 8:e56292. doi: 10.1371/journal.pone. 0056292 PMID: 23431368
17. Hovis KM, Mojica S, McDermott JE, Pedersen L, Simhi C, Rank R, et al. (2013) Genus optimized strategy for the identification of chlamydial type III secretion substrates. Pathog Dis 0:1-10.
18. Da Cunha M, Milho C, Almeida F, Pais S, Borges V, Mauricio R, et al. (2014) Identification of type III secretion substrates of Chlamydia trachomatis using Yersinia enterocolitica as a heterologous system. BMC Microbiology 14:40. doi: 10.1186/1471-2180-14-40 PMID: 24533538
19. Subtil A, Delevoye C, Balana M, 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. PMID: 15916612
20. Fields K, Hackstadt T (2000) Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol Microbiol 38:1048-1060. PMID: 11123678
21. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, Clarke IN (2012) Development of a Transformation System for Chlamydia trachomatis: Restoration of Glycogen Biosynthesis by Acquisition of a Plasmid Shuttle Vector. PLoS Pathog 7:e1002258.
22. Agaisse H, Derré I (2013) A C. trachomatis Cloning Vector and the Generation of C. trachomatis Strains Expressing Fluorescent Proteins under the Control of aC. trachomatis Promoter. PLoS ONE 8:e57090. doi: 10.1371/journal.pone.0057090 PMID: 23441233
23. Wickstrum J, Sammons LR, Restivo KN, Hefty PS (2013) Conditional Gene Expression in Chlamydia trachomatis Using the Tet System. PLoS ONE 8:e76743. doi: 10.1371/journal.pone.0076743 PMID: 24116144
24. Bauler LD, Hackstadt T (2014) Expression and Targeting of Secreted Proteins from Chlamydia trachomatis. Journal of Bacteriology 196:1325-1334. doi: 10.1128/JB.01290-13 PMID: 24443531
25. Agaisse H, Derré I (2014) Expression of the Effector Protein IncD in Chlamydia trachomatis Mediates Recruitment of the Lipid Transfer Protein CERT and the Endoplasmic Reticulum-Resident Protein VAPB to the Inclusion Membrane. Infection and Immunity 82:2037-2047. doi: 10.1128/IAI.01530-14 PMID: 24595143
26. Campbell-Valois FX, Sansonetti PJ (2014) Tracking bacterial pathogens with genetically-encoded reporters. FEBS Letters 588:2428-2436. doi: 10.1016/j.febslet.2014.05.022 PMID: 24859085
27. Charpentier X, Oswald E (2004) Identification of the Secretion and Translocation Domain of the Enteropathogenic and Enterohemorrhagic Escherichia coli Effector Cif, Using TEM-1 (5-Lactamase as a New Fluorescence-Based Reporter. Journal of Bacteriology 186:5486-5495. PMID: 15292151
28. Carabeo R, Grieshaber S, Hasenkrug A, Dooley C, Hackstadt T (2004) Requirement for the Rac GTPage in Chlamydia trachomatis invasion of non-phagocytic cells. Traffic 5:418-425. PMID: 15117316
29. Caldwell HD, Kromhout J, Schachter J (1981) Purification and partial characterization of the major outer membrane protein of Chlamydia trachomatis. Infect Immun 31:1161-1176. PMID: 7228399
30. 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 atissue-culture infection model. Cell Microbiol 9:2417-2430. PMID: 17532760
31. Geiser M, Cebe R, Drewello D, Schmitz R (2001) Integration of PCR fragments at any specific site within cloning vectors without the use of restriction enzymes and DNAligase. BioTechniques 31:88-92. PMID: 11464525
32. Jamison WP, Hackstadt T (2008) Induction of type III secretion by cell-free Chlamydia trachomatis elementary bodies. Microb Pathog 45:435-440. doi: 10.1016/j.micpath.2008.10.002 PMID: 18984037
33. Scidmore-Carlson M, Shaw E, Dooley C, Fischer E, Hackstadt T (1999) Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol Microbiol 33:753-765. PMID: 10447885
34. Baehr W, Zhang YX, Joseph T, Su H, Nano FE, Everett KD, et al. (1988) Mapping antigenic domains expressed by Chlamydia trachomatis major outer membrane protein genes. Proc Natl Acad Sci USA 85:4000-4004. PMID: 2453883
35. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, et al. (1998) Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759. PMID: 9784136
36. Kingsford C, Ayanbule K, Salzberg SL (2007) Rapid, accurate computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8:R22. PMID: 17313685
37. Belland RJ, Zhong G, Crane DD, Hogan D, Sturdevant D, Sharma J et al. (2003) Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc Natl Acad Sci USA 100:8478-8483. PMID: 12815105
38. Albrecht M, Sharma CM, Reinhardt R, Vogel J, Rudel T (2010) Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome. Nucleic Acids Research 38:868-877. doi: 10.1093/nar/gkp1032 PMID: 19923228
39. 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. PMID: 17056752
40. 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. doi: 10.1371/journal.ppat.1000579 PMID: 19750218
41. Sharma J, Zhong Y, Dong F, Piper JM, Wang G, Zhong G (2006) Profiling of human antibody responses to Chlamydia trachomatis urogenital tract infection using microplates with 156 chlamydial fusion proteins. Infect Immun 74:1490-1499. PMID: 16495519
42. Moore ER, Mead DJ, Dooley CA, Sager J, Hackstadt T (2011) The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157:830-838. doi: 10.1099/mic.0. 045856-0 PMID: 21109560
43. Beare P, Sandoz K, Omsland A, Rockey D, Heinzen R (2011) Advances in genetic manipulation of obligate intracellular bacterial pathogens. Frontiers in Microbiology 2.
44. Voth DE, Beare PA, Howe D, Sharma UM, Samoilis G, Cockrell DC, et al. (2011) The Coxiella burnetii Cryptic Plasmid Is Enriched in Genes Encoding Type IV Secretion System Substrates. Journal of Bacteriology 193:1493-1503. doi: 10.1128/JB.01359-10 PMID: 21216993
45. Carey KL, Newton HJ, Lührmann A, Roy CR (2011) The Coxiella burnetii Dot/Icm System Delivers a Unique Repertoire of Type IV Effectors into Host Cells and Is Required for Intracellular Replication. PLoS Pathog 7:e1002056. doi: 10.1371/journal.ppat.1002056 PMID: 21637816
46. Rosario CJ, Hanson BR, Tan M (2014) The transcriptional repressor EUO regulates both subsets of Chlamydia late genes. Molecular Microbiology 94:888-897. doi: 10.1111/mmi.12804 PMID: 25250726
47. Rosario CJ, Tan M (2012) The early gene product EUO is a transcriptional repressor that selectively regulates promoters of Chlamydia late genes. Molecular Microbiology 84:1097-1107. doi: 10.1111/j. 1365-2958.2012.08077.x PMID: 22624851
48. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379-433. PMID: 9618447
49. Keyser P, Elofsson M, Rosell S, Wolf-Watz H (2008) Virulence blockers as alternatives to antibiotics: type III secretion inhibitors against Gram-negative bacteria. J Intern Med 264:17-29. doi: 10.1111/j. 1365-2796.2008.01941.x PMID: 18393958
50. Engström P, Nguyen BD, Normark J, Nilsson I, Bastidas RJ, Gylfe A, et al. (2013) Mutations in hemG mediate resistance to Salicylidene acylhydrazides: A novel link between protoporphyrinogen oxidase (HemG) and Chlamydia trachomatis infectivity. Journal of Bacteriology.
51. Slepenkin A, Enquist P, Hagglund U, De La Maza L, Elofsson M, Peterson EM (2007) Reversal of the antichlamydial activity of putative type III secretion inhibitors by iron. Infect Immun 75:3478-3489. PMID: 17470544
52. Mueller KE, Plano GV, Fields KA (2014) New Frontiers in Type III Secretion Biology: the Chlamydia Perspective. Infection and Immunity 82:2-9. doi: 10.1128/IAI.00917-13 PMID: 24126521
53. Sisko J, Spaeth K, Kumar Y, Valdivia R (2006) Multifunctional analysis of Chlamydia-specific genes in a yeast expression system. Mol Microbiol 60:51-66. PMID: 16556220
54. Bullock HD, Hower S, Fields KA (2012) Domain analyses reveal that C. trachomatis CT694 belongs to the membrane-localized family of type III effector proteins. J Biol Chem 287:28078-28086. doi: 10. 1074/jbc. M112.386904 PMID: 22711538
55. Fields KA (2012) Secretion Mechanisms and Chlamydia pathogenesis. In: Tan M, Bavoil P, editors. Intracellular Pathogens I: Chlamydiales. Washington, DC: ASM Press. pp. 192-216.
56. Mills E, Baruch K, Charpentier X, Kobi S, Rosenshine I (2008) Real-Time Analysis of Effector Translocation by the Type III Secretion System of Enteropathogenic Escherichia coli. Cell Host & Microbe 3:104-113.
57. Marketon MM, De Paolo RW, De Bord KL, Jabri B, Schneewind O (2005) Plague Bacteria Target Immune Cells During Infection. Science 309:1739-1741. PMID: 16051750
58. Copenhaver AM, Casson CN, Nguyen HT, Fung TC, Duda MM, Roy CR, et al. (2014) Alveolar Macrophages and Neutrophils Are the Primary Reservoirs for Legionella pneumophila and Mediate Cytosolic Surveillance of Type IV Secretion. Infection and Immunity 82:4325-4336. doi: 10.1128/IAI.01891-14 PMID: 25092908