Morphologic and molecular evaluation of Chlamydia trachomatis growth in human endocervix reveals distinct growth patterns

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue JUN, 2014, Pages

  Lewis, Maria E ^a   Belland, Robert J ^b   AbdelRahman, Yasser M ^b,c   Beatty, Wandy L ^d   Aiyar, Ashok A ^a   Zea, Arnold H ^a   Greene, Sheila J ^a   Marrero, Luis ^a   Buckner, Lyndsey R ^a   Tate, David J ^a   McGowin, Chris L ^a   Kozlowski, Pamela A ^a   O'Brien, Michelle ^a   Lillis, Rebecca A ^a   Martin, David H ^a   Quayle, Alison J ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c CAIRO UNIVERSITY   (Egypt)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bacterial persistence; Chlamydia trachomatis; Endocervix; Human; Indole; Interferon gamma

Indexed keywords

GAMMA INTERFERON; CYTOKINE; INDOLE;

ADULT; ARTICLE; CHLAMYDIA TRACHOMATIS; EPIFLUORESCENCE MICROSCOPY; FEMALE; FLOW CYTOMETRY; FUNGUS GROWTH; GENE DOSAGE; GENOTYPING TECHNIQUE; HUMAN; IMMUNOFLUORESCENCE; MOLECULAR BIOLOGY; MORPHOLOGICAL TRAIT; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; UTERINE CERVICITIS; UTERINE ENDOCERVIX; VAGINA FLORA; ADOLESCENT; BACTERIAL LOAD; BACTERIAL PERSISTENCE; CHLAMYDIASIS; CYTOLOGY; ELECTRON MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENETICS; GENITAL TRACT INFECTION; ISOLATION AND PURIFICATION; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PATHOLOGY; UTERINE CERVIX; YOUNG ADULT;

BACTERIAL PERSISTENCE; CHLAMYDIA TRACHOMATIS; ENDOCERVIX; HUMAN; INDOLE; INTERFERON GAMMA;

ADOLESCENT; ADULT; BACTERIAL LOAD; CERVIX UTERI; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; CYTOKINES; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HUMANS; MICROBIOLOGICAL TECHNIQUES; MICROSCOPY, ELECTRON; PATHOLOGY; REPRODUCTIVE TRACT INFECTIONS; YOUNG ADULT;

EID: 84907174467     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2014.00071     Document Type: Article

References (61)

1. Abdelrahman, Y. M., and Belland, R. J. (2005). The chlamydial developmental cycle. FEMS Microbiol. Rev. 29, 949-959. doi: 10.1016/j.femsre.2005.03.002
2. Aiyar, A., Quayle, A. J., Buckner, L. R., Sherchand, S. P., Chang, T. L., Zea, A. H., et al. (2014). Influence of the tryptophan-indole-IFNγ axis on human genital Chlamydia trachomatis infection: role of vaginal co-infections. Front. Microbiol. 4:72. doi: 10.3389/fcimb.2014.00072
3. Alzhanov, D. T., Weeks, S. K., Burnett, J. R., and Rockey, D. D. (2009). Cytokinesis is blocked in mammalian cells transfected with Chlamydia trachomatis gene CT223. BMC Microbiol. 9:2. doi: 10.1186/1471-2180-9-2
4. Beatty, W. L., Belanger, T. A., Desai, A. A., Morrison, R. P., and Byrne, G. I. (1994a). Tryptophan depletion as a mechanism of gamma interferon-mediated chlamydial persistence. Infect. Immun. 62, 3705-3711.
5. Beatty, W. L., Byrne, G. I., and Morrison, R. P. (1993). Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc. Natl. Acad. Sci. U.S.A. 90, 3998-4002. doi: 10.1073/pnas.90.9.3998
6. Beatty, W. L., Morrison, R. P., and Byrne, G. I. (1994b). Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 58, 686-699.
7. Belland, R. J., Nelson, D. E., Virok, D., Crane, D. D., Hogan, D., Sturdevant, D., et al. (2003a). Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc. Natl. Acad. Sci. U.S.A. 100, 15971-15976. doi: 10.1073/pnas.2535394100
8. Belland, R. J., Zhong, G., Crane, D. D., Hogan, D., Sturdevant, D., Sharma, J., et al. (2003b). Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. Proc. Natl. Acad. Sci. U.S.A. 100, 8478-8483. doi: 10.1073/pnas.1331135100
9. Bragina, E. Y., Gomberg, M. A., and Dmitriev, G. A. (2001). Electron microscopic evidence of persistent chlamydial infection following treatment. J. Eur. Acad. Dermatol. Venereol. 15, 405-409. doi: 10.1046/j.1468-3083.2001.00342.x
10. Braley, A. E. (1938). Inclusion Blennorrhea. Am. J. Opthalmol. 21, 1203-1208.
11. Brunham, R. C., and Rey-Ladino, J. (2005). Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat. Rev. Immunol. 5, 149-161. doi: 10.1038/nri1551
12. Buckner, L. R., Lewis, M. E., Greene, S. J., Foster, T. P., and Quayle, A. J. (2013). Chlamydia trachomatis infection results in a modest pro-inflammatory cytokine response and a decrease in T cell chemokine secretion in human polarized endocervical epithelial cells. Cytokine 63, 151-165. doi: 10.1016/j.cyto.2013.04.022
13. Buckner, L. R., Schust, D. J., Ding, J., Nagamatsu, T., Beatty, W., Chang, T. L., et al. (2011). Innate immune mediator profiles and their regulation in a novel polarized immortalized epithelial cell model derived from human endocervix. J. Reprod. Immunol. 92, 8-20. doi: 10.1016/j.jri.2011.08.002
14. Byrne, G. I., Carlin, J. M., Merkert, T. P., and Arter, D. L. (1989). Long-term effects of gamma interferon on chlamydia-infected host cells: microbicidal activity follows microbistasis. Infect. Immun. 57, 1318-1320.
15. Byrne, G. I., Lehmann, L. K., and Landry, G. J. (1986). Induction of tryptophan catabolism is the mechanism for gamma-interferon-mediated inhibition of intracellular Chlamydia psittaci replication in T24 cells. Infect. Immun. 53, 347-351.
16. Byrne, G. I., Ouellette, S. P., Wang, Z., Rao, J. P., Lu, L., Beatty, W. L., et al. (2001). Chlamydia pneumoniae expresses genes required for DNA replication but not cytokinesis during persistent infection of HEp-2 cells. Infect. Immun. 69, 5423-5429. doi: 10.1128/IAI.69.9.5423-5429.2001
17. Caldwell, H. D., Wood, H., Crane, D., Bailey, R., Jones, R. B., Mabey, D., et al. (2003). Polymorphisms in Chlamydia trachomatis tryptophan synthase genes differentiate between genital and ocular isolates. J. Clin. Invest. 111, 1757-1769. doi: 10.1172/JCI17993
18. Carlin, J. M., Borden, E. C., and Byrne, G. I. (1989). Interferon-induced indoleamine 2, 3-dioxygenase activity inhibits Chlamydia psittaci replication in human macrophages. J. Interferon Res. 9, 329-337. doi: 10.1089/jir.1989.9.329
19. Clark, R. B., Schatzki, P. F., and Dalton, H. P. (1982). Ultrastructural effect of penicillin and cycloheximide on Chlamydia trachomatis strain HAR-13. Med. Microbiol. Immunol. 171, 151-159. doi: 10.1007/BF02123623
20. Cohen, C. R., and Brunham, R. C. (1999). Pathogenesis of Chlamydia induced pelvic inflammatory disease. Sex. Transm. Infect. 75, 21-24. doi: 10.1136/sti.75.1.21
21. Dean, D., Suchland, R. J., and Stamm, W. E. (2000). Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J. Infect. Dis. 182, 909-916. doi: 10.1086/315778
22. Dunlop, E. M., Garner, A., Darougar, S., Treharne, J. D., and Woodland, R. M. (1989). Colposcopy, biopsy, and cytology results in women with chlamydial cervicitis. Genitourin. Med. 65, 22-31.
23. Fehlner-Gardiner, C., Roshick, C., Carlson, J. H., Hughes, S., Belland, R. J., Caldwell, H. D., et al. (2002). Molecular basis defining human Chlamydia trachomatis tissue tropism. A possible role for tryptophan synthase. J. Biol. Chem. 277, 26893-26903. doi: 10.1074/jbc.M203937200
24. Ficarra, M., Ibana, J. S., Poretta, C., Ma, L., Myers, L., Taylor, S. N., et al. (2008). A distinct cellular profile is seen in the human endocervix during Chlamydia trachomatis infection. Am. J. Reprod. Immunol. 60, 415-425. doi: 10.1111/j.1600-0897.2008.00639.x
25. Geisler, W. M., Wang, C., Morrison, S. G., Black, C. M., Bandea, C. I., and Hook, E. W. 3rd (2008). The natural history of untreated Chlamydia trachomatis infection in the interval between screening and returning for treatment. Sex. Transm. Dis. 35, 119-123. doi: 10.1097/OLQ.0b013e318151497d
26. Golden, M. R., Schillinger, J. A., Markowitz, L., and St. Louis, M. E. (2000). Duration of untreated genital infections with Chlamydia trachomatis: a review of the literature. Sex. Transm. Dis. 27, 329-337. doi: 10.1097/00007435-200007000-00006
27. Hogan, R. J., Mathews, S. A., Mukhopadhyay, S., Summersgill, J. T., and Timms, P. (2004). Chlamydial persistence: beyond the biphasic paradigm. Infect. Immun. 72, 1843-1855. doi: 10.1128/IAI.72.4.1843-1855.2004
28. Hybiske, K., and Stephens, R. S. (2007). Mechanisms of host cell exit by the intracellular bacterium Chlamydia. Proc. Natl. Acad. Sci. U.S.A. 104, 11430-11435. doi: 10.1073/pnas.0703218104
29. Ibana, J. A., Belland, R. J., Zea, A. H., Schust, D. J., Nagamatsu, T., Abdelrahman, Y. M., et al. (2011). Inhibition of indoleamine 2, 3-dioxygenase activity by levo-1-methyl tryptophan blocks gamma interferon-induced Chlamydia trachomatis persistence in human epithelial cells. Infect. Immun. 79, 4425-4437. doi: 10.1128/IAI.05659-11
30. Igietseme, J. U., Ananaba, G. A., Candal, D. H., Lyn, D., and Black, C. M. (1998). Immune control of Chlamydial growth in the human epithelial cell line RT4 involves multiple mechanisms that include nitric oxide induction, tryptophan catabolism and iron deprivation. Microbiol. Immunol. 42, 617-625. doi: 10.1111/j.1348-0421.1998.tb02332.x
31. Joyner, J. L., Douglas, J. M. Jr., Foster, M., and Judson, F. N. (2002). Persistence of Chlamydia trachomatis infection detected by polymerase chain reaction in untreated patients. Sex. Transm. Dis. 29, 196-200. doi: 10.1097/00007435-200204000-00002
32. Koumans, E. H., Sternberg, M., Bruce, C., McQuillan, G., Kendrick, J., Sutton, M., et al. (2007). The prevalence of bacterial vaginosis in the United States, 2001-2004; associations with symptoms, sexual behaviors, and reproductive health. Sex. Transm. Dis. 34, 864-869. doi: 10.1097/OLQ.0b013e318074e565
33. Kozlowski, P. A., Lynch, R. M., Patterson, R. R., Cu-Uvin, S., Flanigan, T. P., and Neutra, M. R. (2000). Modified wick method using Weck-Cel sponges for collection of human rectal secretions and analysis of mucosal HIV antibody. J. Acquir. Immune Defic. Syndr. 24, 297-309. doi: 10.1097/00126334-200008010-00001
34. Matsumoto, A., and Manire, G. P. (1970). Electron microscopic observations on the effects of penicillin on the morphology of Chlamydia psittaci. J. Bacteriol. 101, 278-285.
35. Molano, M., Meijer, C. J., Weiderpass, E., Arslan, A., Posso, H., Franceschi, S., et al. (2005). The natural course of Chlamydia trachomatis infection in asymptomatic Colombian women: a 5-year follow-up study. J. Infect. Dis. 191, 907-916. doi: 10.1086/428287
36. Morre, S. A., Van Den Brule, A. J., Rozendaal, L., Boeke, A. J., Voorhorst, F. J., De Blok, S., et al. (2002). The natural course of asymptomatic Chlamydia trachomatis infections: 45% clearance and no development of clinical PID after one-year follow-up. Int. J. STD AIDS 13(Suppl.) 2, 12-18. doi: 10.1258/095646202762226092
37. Morrison, R. P. (2003). New insights into a persistent problem-chlamydial infections. J. Clin. Invest. 111, 1647-1649. doi: 10.1172/JCI18770
38. Nagasaki, T. (1987). A high prevalence of chlamydial cervicitis in postmenopausal women. Am. J. Obstet. Gynecol. 156, 31-32. doi: 10.1016/0002-9378(87)90198-0
39. Nugent, R. P., Krohn, M. A., and Hillier, S. L. (1991). Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J. Clin. Microbiol. 29, 297-301.
40. Omsland, A., Sager, J., Nair, V., Sturdevant, D. E., and Hackstadt, T. (2012). Developmental stage-specific metabolic and transcriptional activity of Chlamydia trachomatis in an axenic medium. Proc. Natl. Acad. Sci. U.S.A. 109, 19781-19785. doi: 10.1073/pnas.1212831109
41. Parks, K. S., Dixon, P. B., Richey, C. M., and Hook, E. W. 3rd (1997). Spontaneous clearance of Chlamydia trachomatis infection in untreated patients. Sex. Transm. Dis. 24, 229-235. doi: 10.1097/00007435-199704000-00008
42. Patton, D. L., Askienazy-Elbhar, M., Henry-Suchet, J., Campbell, L. A., Cappuccio, A., Tannous, W., et al. (1994). Detection of Chlamydia trachomatis in fallopian tube tissue in women with postinfectious tubal infertility. Am. J. Obstet. Gynecol. 171, 95-101. doi: 10.1016/S0002-9378(94)70084-2
43. Pettengill, M. A., Lam, V. W., and Ojcius, D. M. (2009). The danger signal adenosine induces persistence of chlamydial infection through stimulation of A2b receptors. PLoS ONE 4:e8299. doi: 10.1371/journal.pone.0008299
44. Rank, R. G., and Whittum-Hudson, J. A. (2010). Protective immunity to chlamydial genital infection: evidence from animal studies. J. Infect. Dis. 201(Suppl. 2), S168-S177. doi: 10.1086/652399
45. Raulston, J. E. (1997). Response of Chlamydia trachomatis serovar E to iron restriction in vitro and evidence for iron-regulated chlamydial proteins. Infect. Immun. 65, 4539-4547.
46. Rosario, C. J., and Tan, M. (2012). The early gene product EUO is a transcriptional repressor that selectively regulates promoters of Chlamydia late genes. Mol. Microbiol. 84, 1097-1107. doi: 10.1111/j.1365-2958.2012.08077.x
47. Salkowski, E. (1885). Uber das verhalten der skatolcarbonsaure im organismus. Z. Physiol. Chem. 9, 23-33.
48. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682. doi: 10.1038/nmeth.2019
49. Schoborg, R. V. (2011). Chlamydia persistence-a tool to dissect chlamydia-host interactions. Microbes Infect. 13, 649-662. doi: 10.1016/j.micinf.2011.03.004
50. Shemer, Y., and Sarov, I. (1985). Inhibition of growth of Chlamydia trachomatis by human gamma interferon. Infect. Immun. 48, 592-596.
51. Skilton, R. J., Cutcliffen, L. T., Barlow, D., Wang, Y., Salim, O., Lambden, P. R., et al. (2009). Penicillin induced persistence in Chlamydia trachomatis: high quality time lapse video analysis of the developmental cycle. PLoS ONE 4:e7723. doi: 10.1371/journal.pone.0007723
52. Sutton, M., Sternberg, M., Koumans, E. H., McQuillan, G., Berman, S., and Markowitz, L. (2007). The prevalence of Trichomonas vaginalis infection among reproductive-age women in the United States, 2001-2004. Clin. Infect. Dis. 45, 1319-1326. doi: 10.1086/522532
53. Swanson, J., Eschenbach, D. A., Alexander, E. R., and Holmes, K. K. (1975). Light and electron microscopic study of Chlamydia trachomatis infection of the uterine cervix. J. Infect. Dis. 131, 678-687. doi: 10.1093/infdis/131.6.678
54. Szkop, M., Sikora, P., and Orzechowski, S. (2012). A novel, simple, and sensitive colorimetric method to determine aromatic amino acid aminotransferase activity using the Salkowski reagent. Folia Microbiol. (Praha). 57, 1-4. doi: 10.1007/s12223-011-0089-y
55. Taylor, M. W., and Feng, G. S. (1991). Relationship between interferon-gamma, indoleamine 2, 3-dioxygenase, and tryptophan catabolism. FASEB J. 5, 2516-2522.
56. Vanover, J., Sun, J., Deka, S., Kintner, J., Duffourc, M. M., and Schoborg, R. V. (2008). Herpes simplex virus co-infection-induced Chlamydia trachomatis persistence is not mediated by any known persistence inducer or anti-chlamydial pathway. Microbiology 154, 971-978. doi: 10.1099/mic.0.2007/012161-0
57. Ward, M. E. (1983). Chlamydial classification, development and structure. Br. Med. Bull. 39, 109-115.
58. Wyrick, P. B. (2010). Chlamydia trachomatis persistence in vitro: an overview. J. Infect. Dis. 201(Suppl. 2), S88-S95. doi: 10.1086/652394
59. Zhang, L., Douglas, A. L., and Hatch, T. P. (1998). Characterization of a Chlamydia psittaci DNA binding protein (EUO) synthesized during the early and middle phases of the developmental cycle. Infect. Immun. 66, 1167-1173.
60. Zhang, L., Howe, M. M., and Hatch, T. P. (2000). Characterization of in vitro DNA binding sites of the EUO protein of Chlamydia psittaci. Infect. Immun. 68, 1337-1349. doi: 10.1128/IAI.68.3.1337-1349.2000
61. Zhang, Y. X., Watkins, N. G., Stewart, S., and Caldwell, H. D. (1987). The low-molecular-mass, cysteine-rich outer membrane protein of Chlamydia trachomatis possesses both biovar-and species-specific epitopes. Infect. Immun. 55, 2570-2573.