Commonly prescribed β-lactam antibiotics induce c.trachomatis persistence/stress in culture at physiologically relevant concentrations

Frontiers in Cellular and Infection Microbiology

Volumn 4, Issue , 2014, Pages

  Kintner, Jennifer ^a   Lajoie, Dawn ^a   Hall, Jennifer ^a   Whittimore, Judy ^a   Schoborg, Robert V ^a  

^a East Tennessee State University   (United States)

Author keywords

Antibiotic chlamydial stress response; Chlamydia trachomatis; Penicillin; lactam; Stressed chlamydiae

Indexed keywords

AMOXICILLIN; AMPICILLIN; AZTREONAM; BETA LACTAM; CARBENICILLIN; CEFOTAXIME; CEFTRIAXONE; CLAVULANIC ACID; GENOMIC DNA; PENICILLIN G; PENICILLIN V; PIPERACILLIN; TETRACYCLINE; ANTIINFECTIVE AGENT; BACTERIAL DNA; PENICILLIN DERIVATIVE; RNA 16S;

ARTICLE; BIOACCUMULATION; CHLAMYDIA TRACHOMATIS; CHLAMYDIAL INFECTIVITY ASSAY; CHLAMYDIASIS; CONTROLLED STUDY; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEXUALLY TRANSMITTED DISEASE; TRANSMISSION ELECTRON MICROSCOPY; TREATMENT FAILURE; CELL CULTURE; CELL LINE; DRUG EFFECTS; GENETICS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; ULTRASTRUCTURE;

ANTI-BACTERIAL AGENTS; BETA-LACTAMS; CELL LINE; CELLS, CULTURED; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; DNA, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; PENICILLINS; RNA, RIBOSOMAL, 16S; STRESS, PHYSIOLOGICAL;

EID: 84924844470     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2014.00044     Document Type: Article

References (55)

1. Barbour, A. G., Amano, K., Hackstadt, T., Perry, L., and Caldwell, H. D. (1982). Chlamydia trachomatis has penicillin-binding proteins but not detectable muramic acid. J. Bacteriol. 151, 420-428.
2. Bartholow, M. (2011). Top 200 Prescription Drugs of 2011. Pharmacy Times 2011. Available online at: http://www.pharmacytimes.com/_media/_ pdf/Top_200_Drugs_2011_Total_Rx.pdf (Accessed October 21, 2013).
3. Beale, A. S., Faulds, E., Hurn, S. E., Tyler, J., and Slocombe, B. (1991). Comparative activities of amoxycillin, amoxycillin/clavulanic acid and tetracycline against Chlamydia trachomatis in cell culture and in an experimental mouse pneumonitis. J. Antimicrob. Chemother. 27, 627-638.
4. Centers for Disease Control and Prevention. (2010). Sexually Transmitted Diseases Treatment Guidelines. Atlanta: U.S. Department of Health and Human Services, 2011. Available online at: http://www.cdc.gov/std/treatment/2010 (Accessed October 21, 2013).
5. Centers for Disease Control and Prevention. (2011). Sexually Transmitted Diseases Surveillance. Atlanta: U.S. Department of Health and Human Services, 2012. Available online at: http://www.cdc.gov/std/stats11/default.htm (Accessed October 21, 2013).
6. 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
7. Deka, S., Vanover, J., Dessus-Babus, S, Whittimore, J., Howett, M. K., Wyrick, P. B., et al. (2006). Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cell. Microbiol. 8, 149-162. doi: 10.1111/j.1462-5822.2005.00608.x
8. Deka, S., Vanover, J., Sun, J., Kintner, J., Whittimore, J., and Schoborg, R. V. (2007). An early event in the herpes simplex virus type-2 replication cycle is sufficient to induce Chlamydia trachomatis persistence. Cell. Microbiol. 9, 725-737. doi: 10.1111/j.1462-5822.2006.00823.x
9. Detels, R., Green, A. M., Klausner, J. D., Katzenstein, D., Gaydos, C., Handsfield, H., et al. (2011). The incidence and correlates of symptomatic and asymptomatic Chlamydia trachomatis and Neisseria gonorrhoeae infections in selected populations in five countries. Sex. Transm. Dis. 38, 503-509. doi: 10.1097/OLQ.0b013e318206c288
10. Dreses-Werringloer, U., Padubrin, I., Jürgens-Saathoff, B., Hudson, A. P., Zeidler, H., and Köhler, L. (2000). Persistence of Chlamydia trachomatis is induced by ciprofloxacin and ofloxacin in vitro. Antimicrob. Agents Chemother. 44, 3288-3297. doi: 10.1128/AAC.44.12.3288-3297.2000
11. Dreses-Werringloer, U., Padubrin, I., Zeidler, H., and Köhler, L. (2001). Effects of azithromycin and rifampin on Chlamydia trachomatis infection in vitro. Antimicrob. Agents. Chemother. 45, 3001-3008. doi: 10.1128/AAC.45.11.3001- 3008.2001
12. Fortenberry, J. D., Brizendine, E. J., Katz, B. P. Wools, K. K., Blythe, M. J., and Orr, D. P. (1999). Subsequent sexually transmitted infections among adolescent women with genital infection due to Chlamydia trachomatis, Neisseria gonorrhoeae, or Trichomonas vaginalis. Sex Transm. Dis. 26, 26-32. doi: 10.1097/00007435-199901000-00005
13. Galasso, G. J., and Manire, G. P. (1961). Effect of antiserum and antibiotics on persistent infection of HeLa cells with meningopneumonitis virus. J. Immunol. 86, 382-385.
14. Gerard, H. C., Branigan, P. J., Schumacher, H. R., and Hudson, A. P. (1998). Synovial Chlamydia trachomatis in patients with reactive arthritis/Reiter's syndrome are viable but show aberrant gene expression. J. Rheumatol. 25, 734-742.
15. Gerard, H. C., Krausse-Opatz, B., Wang, Z., Rudy, D., Rao, J. P., Zeidler, H., et al. (2001). Expression of Chlamydia trachomatis genes encoding products required for DNA synthesis and cell division during active versus persistent infection. Mol. Microbiol. 41, 731-741. doi: 10.1046/j.1365-2958.2001.02550.x
16. Gieffers, J., Rupp, J., Gebert, A., Solbach, W., and Klinger, M. (2004). Firstchoice antibiotics at subinhibitory concentrations induce persistence of Chlamydia pneumoniae. Antimicrob. Agents Chemother. 48, 1402-1405. doi: 10.1128/AAC.48.4.1402-1405.2004
17. Goossens, H., Ferech, M., Stichele, R. V., and Elseviers, M. (2005). Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet 365, 579-587. doi: 10.1016/S0140-6736(05)17907-0.
18. Gozlan, I., Rotstein, A., and Avisar, D. (2010). Investigation of an amoxicillin oxidative degradation product formed under controlled environmental conditions. Environ. Chem. 7, 435-442. doi: 10.1071/EN10037
19. Heberer, T. (2002). Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett. 131, 5-17. doi: 10.1016/S0378-4274(02)00041-3
20. 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
21. Holmes, K. K., Johnson, D. W., Floyd, T. M., and Kvale, P. A. (1967). Studies of venereal disease. II. Observations on the incidence, etiology, and treatment of the postgonococcal urethritis syndrome. JAMA 202, 467-473. doi: 10.1001/jama.1967.03130190073009
22. Horner, P. (2006). The case for further treatment studies of uncomplicated genital Chlamydia trachomatis infection. Sex. Transm. Infect. 82, 340-343. doi: 10.1136/sti.2005.019158
23. Johnson, F. W., and Hobson, D. (1977). The effect of penicillin on genital strains of Chlamydia trachomatis in tissue culture. J. Antimicrob. Chemother. 3, 49-56. doi: 10.1093/jac/3.1.49
24. Kolpin, D. W., Furlong, E. T., Meyer, M. T., Thurman, E. M., Zaugg, S. D., Barber, L. B., et al. (2002). Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 36, 1202-1211. doi: 10.1021/es011055j
25. Kümmerer, K., and Henninger, A. (2003). Promoting resistance by the emission of antibiotics from hospitals and households into effluent. Clin. Microbiol. Infect. Dis. 9, 1203-1214. doi: 10.1111/j.1469-0691.2003.00739.x
26. Kutlin, A., Roblin, P. M., and Hammerschlag, M. R. (1999). In vitro activities of azithromycin and ofloxacin against Chlamydia pneumoniae in a continuousinfection model. Antimicrob. Agents and Chemother. 43, 2268-2272.
27. Lambden, P. R., Pickett, M. A., and Clarke, I. N. (2006). The effect of penicillin on Chlamydia trachomatis DNA replication. Microbiology 152, 2573-2578. doi: 10.1099/mic.0.29032-0
28. 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.
29. McEvoy, G. K. (2004). American Hospital Formulary Service Drug Information. Bethesda, MD: American Society of Health-System Pharmacists.
30. Nanagara, R., Li, F., Beutler, A., Hudson, A., and Schumacher, H. R. Jr. (1995). Alteration of Chlamydia trachomatis biologic behavior in synovial membranes. Suppression of surface antigen production in reactive arthritis and Reiter's syndrome. Arthritis Rheum. 8, 1410-1417. doi: 10.1002/art. 1780381008
31. Neu, H. C., and Fu, K. P. (1978). Clavulanic acid, a novel inhibitor of beta-lactamases. Antimicrob. Agents Chemother. 14, 650-655. doi: 10.1128/AAC.14.5.650
32. Ouellette, S. P., Karimova, G., Subtil, A., and Ladant, D. (2012). Chlamydia coopts the rod shape-determining proteins MreB and Pbp2 for cell division. Mol. Microbiol. 85, 164-178. doi: 10.1111/j.1365-2958.2012.08100.x
33. 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
34. Phillips-Campbell, R., Kintner, J., and Schoborg, R. V. (2014). Induction of the Chlamydia muridarum stress/persistence response increases azithromycintreatment failure in a murine model of infection. Antimicrob. Agents Chemother. 58, 1782-1784. doi: 10.1128/AAC.02097-13
35. Phillips-Campbell, R., Kintner, J., Whittimore, J., and Schoborg, R. V. (2012). Chlamydia muridarum enters a viable but non-infectious state in amoxicillin-treated BALB/c mice. Microbes. Infect. 14, 1177-1185. doi: 10.1016/j.micinf.2012.07.017
36. Pitt, R. A., Alexander, S., Horner, P. J., and Ison, C. A. (2013). Presentation of clinically suspected persistent chlamydial infection: a case series. Int. J. STD AIDS 24, 469-475. doi: 10.1177/0956462412472815
37. Pospischil, A., Borel, N., Chowdhury, E. H., and Guscetti, F. (2009). Aberrant chlamydial developmental forms in the gastrointestinal tract of pigs spontaneously and experimentally infected with Chlamydia suis. Vet. Microbiol. 135, 147-156. doi: 10.1016/j.vetmic.2008.09.035
38. Rank, R. G., Whittimore, J., Bowlin, A. K., and Wyrick, P. B. (2011). In vivo ultrastructural analysis of the intimate relationship between polymorphonuclear leukocytes and the chlamydial developmental cycle. Infect. Immun. 79, 3291-3301. doi: 10.1128/IAI.00200-11
39. Ray, W. A., Murray, K. T., Hall, K., Arbogast, P. G., and Stein, C. M. (2012). Azithromycin and the risk of cardiovascular death. N. Engl. J. Med. 366, 1881-1890. doi: 10.1056/NEJMoa1003833
40. Reading, C., and Cole, M. (1977). Clavulanic acid: a beta-lactamase-inhibiting beta-lactam from Streptomyces clavuligerus. Antimicrob. Agents Chemother. 11, 852-857. doi: 10.1128/AAC.11.5.852
41. Reveneau, N., Crane, D. D., Fischer, E., and Caldwell, H. D. (2005). Bactericidal activity of first-choice antibiotics against gamma interferon-induced persistent infection of human epithelial cells by Chlamydia trachomatis. Antimicrob. Agents Chemother. 49, 1787-1793. doi: 10.1128/AAC.49.5.1787- 1793.2005
42. Richmond, S. J., Hilton, A. L., and Clarke, S. K. (1972). Chlamydial infection. Role of Chlamydia subgroup A in non-gonococcal and post-gonococcal urethritis. Br. J. Vener. Dis. 48, 437-444.
43. Schachter, J. (1999) "Infection and disease epidemiology," in Chlamydia: Intracellular Biology, Pathogenesis, and Immunology, ed R. S. Stephens (Washington, DC: ASM Press), 139-169.
44. Schachter, J., Stoner, E., and Moncada, J. (1983). Screening for chlamydial infections in women attending family planning clinics. West J. Med. 138, 375-379.
45. 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
46. Skowasch, D., Yeghiazaryan, K., Schrempf, S., Golubnitschaja, O., Welsch, U., Preusse, C. J., et al. (2003). Persistence of Chlamydia pneumoniae in degenerative aortic valve stenosis indicated by heat shock protein 60 homologues. J. Heart Valve Dis. 12, 68-75.
47. Spratt, B. G., Jobanputra, V., and Zimmermann, W. (1977). Binding of thienamycin and clavulanic acid to the penicillin-binding proteins of Escherichia coli K-12. Antimicrob. Agents Chemother. 12, 406-409. doi: 10.1128/AAC.12.3.406
48. Storey, C., and Chopra, I. (2001). Affinities of beta-lactams for penicillin binding proteins of Chlamydia trachomatis and their antichlamydial activities. Antimicrob. Agents Chemother. 45, 303-305. doi: 10.1128/AAC.45.1.303- 305.2001
49. Wang, S. A., Papp, J. R., Stamm, W. E., Peeling, R. W., Martin, D. H., and Holmes, K. K. (2005). Evaluation of antimicrobial resistance and treatment failures for Chlamydia trachomatis: a meeting report. J. Infect. Dis. 191, 917-923. doi: 10.1086/428290
50. Welch, H. (1956). Problems of antibiotics in food as the food and drug administration sees them. Am. J. Public Health Nations Health 47, 701-705. doi: 10.2105/AJPH.47.6.701
51. Welsh, L. E., Gaydos, C. A., and Quinn, T. C. (1992). In vitro evaluation of activities of azithromycin, erythromycin, and tetracycline against Chlamydia trachomatis and Chlamydia pneumoniae. Antimicrob. Agents Chemother. 36, 291-294. doi: 10.1128/AAC.36.2.291
52. Wolf, K., Fischer, E., and Hackstadt, T. (2000). Ultrastructural analysis of developmental events in Chlamydia pneumoniae-infected cells. Infect. Immun. 68, 2379-2385. doi: 10.1128/IAI.68.4.2379-2385.2000
53. Wyrick, P. B. (2000). Intracellular survival by Chlamydia. Cell. Microbiol. 2, 275-282. doi: 10.1046/j.1462-5822.2000.00059.x
54. Wyrick, P. B. (2010). Chlamydia trachomatis persistence in vitro: an overview. J. Infect. Dis. 201(Suppl. 2), S88-S95. doi: 10.1086/652394
55. Wyrick, P. B., and Knight, S. T. (2004). Pre-exposure of infected human endometrial epithelial cells to penicillin in vitro renders Chlamydia trachomatis refractory to azithromycin. J. Antimicrob. Chemother. 54, 79-85. doi: 10.1093/jac/dkh283