Transformation of Chlamydia muridarum reveals a role for Pgp5 in suppression of plasmid-dependent gene expression

Journal of Bacteriology

Volumn 196, Issue 5, 2014, Pages 989-998

  Liu, Yuanjun ^a,b   Chen, Chaoqun ^a   Gong, Siqi ^a   Hou, Shuping ^b   Qi, Manli ^b   Liu, Quanzhong ^b   Baseman, Joel ^a   Zhong, Guangming ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CHLAMYDIA MURIDARUM; CLONING, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HELA CELLS; HUMANS; MICE; P-GLYCOPROTEIN; PLASMIDS; TRANSFORMATION, GENETIC;

EID: 84893794661     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01161-13     Document Type: Article

References (33)

1. Sherman KJ, Daling JR, Stergachis A, Weiss NS, Foy HM, Wang SP, Grayston JT. 1990. Sexually transmitted diseases and tubal pregnancy. Sex. Transm. Dis. 17:115-121. http://dx.doi.org/10.1097/00007435-199007000-00001.
2. Ricci S, Ratti G, Scarlato V. 1995. Transcriptional regulation in the Chlamydia trachomatis pCT plasmid. Gene 154:93-98. http://dx.doi.org /10.1016/0378-1119(94)00825-D.
3. Li Z, Chen D, Zhong Y, Wang S, Zhong G. 2008. The chlamydial plasmid-encoded protein pgp3 is secreted into the cytosol of Chlamydiainfected cells. Infect. Immun. 76:3415-3428. http://dx.doi.org/10.1128/IAI.01377-07.
4. Seth-Smith HM, Harris SR, Persson K, Marsh P, Barron A, Bignell A, Bjartling C, Clark L, Cutcliffe LT, Lambden PR, Lennard N, Lockey SJ, Quail MA, Salim O, Skilton RJ, Wang Y, Holland MJ, Parkhill J, Thomson NR, Clarke IN. 2009. Co-evolution of genomes and plasmids within Chlamydia trachomatis and the emergence in Sweden of a new variant strain. BMC Genomics 10:239. http://dx.doi.org/10.1186/1471-2164-10-239.
5. Kari L, Goheen MM, Randall LB, Taylor LD, Carlson JH, Whitmire WM, Virok D, Rajaram K, Endresz V, McClarty G, Nelson DE, Caldwell HD. 2011. Generation of targeted Chlamydia trachomatis null mutants. Proc. Natl. Acad. Sci. U. S. A. 108:7189-7193. http://dx.doi.org/10.1073/pnas.1102229108.
6. O'Connell CM, Ingalls RR, Andrews CW, Jr, Scurlock AM, Darville T. 2007. Plasmid-deficient Chlamydia muridarum fail to induce immune pathology and protect against oviduct disease. J. Immunol. 179:4027-4034. http://www.jimmunol.org/content/179/6/4027.long.
7. Carlson JH, Whitmire WM, Crane DD, Wicke L, Virtaneva K, Sturdevant DE, Kupko JJ, III, Porcella SF, Martinez-Orengo N, Heinzen RA, Kari L, Caldwell HD. 2008. The Chlamydia trachomatis plasmid is a transcriptional regulator of chromosomal genes and a virulence factor. Infect. Immun. 76:2273-2283. http://dx.doi.org/10.1128/IAI.00102-08.
8. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, Clarke IN. 2011. Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLoS Pathog. 7:e1002258. http://dx.doi.org/10.1371/journal.ppat .1002258.
9. Song L, Carlson JH, Whitmire WM, Kari L, Virtaneva K, Sturdevant DE, Watkins H, Zhou B, Sturdevant GL, Porcella SF, McClarty G, Caldwell HD. 2013. Chlamydia trachomatis plasmid-encoded Pgp4 is a transcriptional regulator of virulence-associated genes. Infect. Immun. 81:636-644. http://dx.doi.org/10.1128/IAI.01305-12.
10. Gong S, Yang Z, Lei L, Shen L, Zhong G. 2013. Characterization of Chlamydia trachomatis plasmid-encoded open reading frames. J. Bacteriol. 195:3819-3826. http://dx.doi.org/10.1128/JB.00511-13.
11. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, Persson K, Bjartling C, Clarke IN. 2013. Genetic transformation of a clinical (genital tract), plasmid-free isolate of Chlamydia trachomatis: engineering the plasmid as a cloning vector. PLoS One 8:e59195. http://dx.doi.org/10.1371/journal.pone.0059195.
12. Wang Y, Cutcliffe LT, Skilton RJ, Persson K, Bjartling C, Clarke IN. 2013. Transformation of a plasmid-free, genital tract isolate of Chlamydia trachomatis with a plasmid vector carrying a deletion in CDS6 revealed that this gene regulates inclusion phenotype. Pathog. Dis. 67:100-103. http://dx.doi.org/10.1111/2049-632X.12024.
13. Ding H, Gong S, Tian Y, Yang Z, Brunham R, Zhong G. 2013. Transformation of sexually transmitted infection-causing serovars of Chlamydia trachomatis using blasticidin for selection. PLoS One 8:e80534. http://dx.doi.org/10.1371/journal.pone.0080534.
14. Song L, Carlson JH, Zhou B, Virtaneva K, Whitmire WM, Sturdevant GL, Porcella SF, McClarty G, Caldwell HD. 11 November 2013. Plasmidmediated transformation tropism of chlamydial biovars. Pathog. Dis. http://dx.doi.org/10.1111/2049-632X.12104.
15. Xu S, Battaglia L, Bao X, Fan H. 2013. Chloramphenicol acetyltransferase as a selection marker for chlamydial transformation. BMC Res. Notes 6:377. http://dx.doi.org/10.1186/1756-0500-6-377.
16. Agaisse H, Derre I. 2013. A Chlamydia trachomatis cloning vector and the generation of C. trachomatis strains expressing fluorescent proteins under the control of a C. trachomatis promoter. PLoS One 8:e57090. http://dx.doi.org/10.1371/journal.pone.0057090.
17. Wickstrum J, Sammons LR, Restivo KN, Hefty PS. 2013. Conditional gene expression in Chlamydia trachomatis using the tet system. PLoS One 8:e76743. http://dx.doi.org/10.1371/journal.pone.0076743.
18. Morrison RP, Caldwell HD. 2002. Immunity to murine chlamydial genital infection. Infect. Immun. 70:2741-2751. http://dx.doi.org/10.1128/IAI.70.6.2741-2751.2002.
19. Shah AA, Schripsema JH, Imtiaz MT, Sigar IM, Kasimos J, Matos PG, Inouye S, Ramsey KH. 2005. Histopathologic changes related to fibrotic oviduct occlusion after genital tract infection of mice with Chlamydia muridarum. Sex. Transm. Dis. 32:49-56. http://dx.doi.org/10.1097/01.olq.0000148299.14513.11.
20. de la Maza LM, Pal S, Khamesipour A, Peterson EM. 1994. Intravaginal inoculation of mice with the Chlamydia trachomatis mouse pneumonitis biovar results in infertility. Infect. Immun. 62:2094-2097.
21. Strandell A, Waldenstrom U, Nilsson L, Hamberger L. 1994. Hydrosalpinx reduces in-vitro fertilization/embryo transfer pregnancy rates. Hum. Reprod. 9:861-863.
22. Vasquez G, Boeckx W, Brosens I. 1995. Prospective study of tubal mucosal lesions and fertility in hydrosalpinges. Hum. Reprod. 10:1075-1078.
23. Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF, White O, Hickey EK, Peterson J, Utterback T, Berry K, Bass S, Linher K, Weidman J, Khouri H, Craven B, Bowman C, Dodson R, Gwinn M, Nelson W, DeBoy R, Kolonay J, McClarty G, Salzberg SL, Eisen J, Fraser CM. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397-1406. http://dx.doi.org/10.1093/nar/28.6.1397.
24. Zhong G, Fan P, Ji H, Dong F, Huang Y. 2001. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J. Exp. Med. 193:935-942. http://dx.doi.org/10.1084/jem.193.8.935.
25. Matsumoto A, Izutsu H, Miyashita N, Ohuchi M. 1998. Plaque formation by and plaque cloning of Chlamydia trachomatis biovar trachoma. J. Clin. Microbiol. 36:3013-3019.
26. Thomas NS, Lusher M, Storey CC, Clarke IN. 1997. Plasmid diversity in Chlamydia. Microbiology 143(Pt 6):1847-1854. http://dx.doi.org/10.1099/00221287-143-6-1847.
27. Zhong G, Reis e Sousa C, Germain RN. 1997. Production, specificity, and functionality of monoclonal antibodies to specific peptide-major histocompatibility complex class II complexes formed by processing of exogenous protein. Proc. Natl. Acad. Sci. U. S. A. 94:13856-13861. http://dx.doi.org/10.1073/pnas.94.25.13856.
28. Fan T, Lu H, Hu H, Shi L, McClarty GA, Nance DM, Greenberg AH, Zhong G. 1998. Inhibition of apoptosis in chlamydia-infected cells: blockade of mitochondrial cytochrome c release and caspase activation. J. Exp. Med. 187:487-496. http://dx.doi.org/10.1084/jem.187.4.487.
29. Zhong G, Castellino F, Romagnoli P, Germain RN. 1996. Evidence that binding site occupancy is necessary and sufficient for effective major histocompatibility complex (MHC) class II transport through the secretory pathway redefines the primary function of class II-associated invariant chain peptides (CLIP). J. Exp. Med. 184:2061-2066. http://dx.doi.org/10.1084/jem.184.5.2061.
30. Lu C, Lei L, Peng B, Tang L, Ding H, Gong S, Li Z, Wu Y, Zhong G. 2013. Chlamydia trachomatis GlgA is secreted into host cell cytoplasm. PLoS One 8:e68764. http://dx.doi.org/10.1371/journal.pone.0068764.
31. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R, Aravind L, Mitchell W, Olinger L, Tatusov RL, Zhao Q, Koonin EV, Davis RW. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759. http://dx.doi.org/10.1126/science.282.5389.754.
32. Ricci S, Cevenini R, Cosco E, Comanducci M, Ratti G, Scarlato V. 1993. Transcriptional analysis of the Chlamydia trachomatis plasmid pCT identifies temporally regulated transcripts, antisense RNA and sigma 70-selected promoters. Mol. Gen. Genet. 237:318-326.
33. Abdelrahman YM, Rose LA, Belland RJ. 2011. Developmental expression of noncoding RNAs in Chlamydia trachomatis during normal and persistent growth. Nucleic Acids Res. 39:1843-1854. http://dx.doi.org/10.1093/nar/gkq1065.