Pathogenesis of fallopian tube damage caused by Chlamydia trachomatis infections

Contraception

Volumn 92, Issue 2, 2015, Pages 108-115

  Hafner, Louise M ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

Chlamydia trachomatis; Fallopian tube damage; Fibrosis; Immunopathogenesis

Indexed keywords

ACTIVIN; CHAPERONIN 60; EARLY PREGNANCY FACTOR; INDUCIBLE NITRIC OXIDE SYNTHASE;

ALTERNATIVE HYPOTHESIS; ARTICLE; CHLAMYDIASIS; CLINICAL OBSERVATION; CONTRACEPTION; EXTRACELLULAR MATRIX; FALLOPIAN TUBE DAMAGE; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; INFERTILITY; NONHUMAN; POSITIVE FEEDBACK; TUBAL FACTOR INFERTILITY; UTERINE TUBE; UTERINE TUBE DISEASE; ADAPTIVE IMMUNITY; ANIMAL; BIOLOGICAL MODEL; CHLAMYDIA TRACHOMATIS; EPITHELIUM; FALLOPIAN TUBE; FEMALE; FIBROSIS; IMMUNOLOGY; INFERTILITY, FEMALE; INNATE IMMUNITY; MACROPHAGE; MICROBIOLOGY; NEUTROPHIL; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; SALPINGITIS; UTERINE TUBE STERILIZATION;

ADAPTIVE IMMUNITY; ANIMALS; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; EPITHELIUM; FALLOPIAN TUBES; FEMALE; FIBROSIS; HUMANS; IMMUNITY, INNATE; INFERTILITY, FEMALE; MACROPHAGES; MODELS, IMMUNOLOGICAL; NEUTROPHILS; SALPINGITIS; STERILIZATION, TUBAL;

EID: 84937515634     PISSN: 00107824     EISSN: 18790518     Source Type: Journal    
DOI: 10.1016/j.contraception.2015.01.004     Document Type: Review

References (53)

1. M.E. Ward The immunobiology and immunopathology of chlamydial infections APMIS 103 11 1995 769 796
2. L. Weström, R. Joesoef, G. Reynolds, A. Hagdu, and S.E. Thompson Pelvic inflammatory disease and fertility. A cohort study of 1,844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results Sex Transm Dis 19 4 1992 185 192
3. W. Cheng, P. Shivshankar, Z. Li, L. Chen, I.T. Yeh, and G. Zhong Caspase-1 contributes to Chlamydia trachomatis-induced upper urogenital tract inflammatory pathologies without affecting the course of infection Infect Immun 76 2 2008 515 522
4. C.M. O'Connell, R.R. Ingalls, C.W. Andrews, A.M. Scurlock, and T. Darville Plasmid-deficient Chlamydia muridarum fail to induce immune pathology and protect against oviduct disease J Immunol 179 6 2007 4027 4034
5. N.M. Budrys, S. Gong, A.K. Rodgers, J. Wang, C. Louden, R. Shain, and et al. Chlamydia trachomatis antigens recognized in women with tubal factor infertility, normal fertility, and acute infection Obstet Gynecol 119 5 2012 1009 1016
6. A.K. Rodgers, J. Wang, Y. Zhang, A. Holden, B. Berryhill, N.M. Budrys, and et al. Association of tubal factor infertility with elevated antibodies to Chlamydia trachomatis caseinolytic protease P Am J Obstet Gynecol 203 5 2010 494.e7 494.e14
7. T. Darville, and T.J. Hiltke Pathogenesis of genital tract disease due to Chlamydia trachomatis J Infect Dis 201 Suppl. 2 2010 S114 S125
8. R.S. Stephens The cellular paradigm of chlamydial pathogenesis Trends Microbiol 11 1 2003 44 51
9. R. Hsia, H. Ohayon, P. Gounon, A. Dautry-Varsat, and P.M. Bavoil Phage infection of the obligate intracellular bacterium, Chlamydia psittaci strain guinea pig inclusion conjunctivitis Microbes Infect 2 2000 761 772
10. R.V. Schoborg Chlamydia persistence: a tool to dissect chlamydia-host interactions Microbes Infect 13 2011 649 662
11. J. Kintner, D. Lajoie, J. Hall, J. Whittimore, and R.V. Schoborg Commonly prescribed β-lactam antibiotics induce C. trachomatis persistence/stress in culture at physiologically relevant concentrations Front Cell Infect Microbiol 4 2014 44
12. M.E. Lewis, R.J. Belland, Y.M. Abdelrahman, W. Beatty, A.A. Aiyar, A.H. Zea, and et al. Morphologic and molecular evaluation of Chlamydia trachomatis growth in the human endocervix reveals distinct growth patterns Front Cell Infect Microbiol 4 2014 71
13. W.L. Beatty, G.I. Byrne, and R.P. Morrison Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro Proc Natl Acad Sci U S A 90 1993 3998 4002
14. F. Follmann, A.W. Olsen, K.T. Jensen, P.R. Hansen, P. Andersen, and M.J. Theisen Antigenic profiling of a Chlamydia trachomatis gene-expression library Infect Dis 197 6 2008 897 905
15. D. LaVerda, L.N. Albanese, P.E. Ruther, S.G. Morrison, R.P. Morrison, K.A. Ault, and et al. Seroreactivity to Chlamydia trachomatis Hsp10 correlates with severity of human genital tract disease Infect Immun 68 1 2000 303 309
16. D. LaVerda, M.V. Kalayoglu, and G.I. Byrne Chlamydial heat shock proteins and disease pathology: new paradigms for old problems? Infect Dis Obstet Gynecol 7 1-2 1999 64 71
17. R. Jha, H. Vardhan, S. Bas, S. Salhan, and A. Mittal Cervical epithelial cells from Chlamydia trachomatis-infected sites co-express higher levels of chlamydial heat shock proteins 60 and 10 in infertile women than in fertile women Gynecol Obstet Invest 68 3 2009 160 166
18. A. Hjelholt, G. Christiansen, T.G. Johannesson, H.J. Ingerslev, and S. Birkelund Tubal factor infertility is associated with antibodies against Chlamydia trachomatis heat shock protein 60 (HSP60) but not human HSP60 Hum Reprod 26 8 2011 2069 2076
19. R. Jha, H. Vardhan, S. Bas, S. Salhan, and A. Mittal Chlamydia trachomatis heat shock proteins 60 and 10 induce apoptosis in endocervical epithelial cells Inflamm Res 60 1 2011 69 78
20. A.K. Rodgers, N.M. Budrys, S. Gong, J. Wang, A. Holden, R.S. Schenken, and et al. Genome-wide identification of Chlamydia trachomatis antigens associated with tubal factor infertility Fertil Steril 96 3 2011 715 721
21. D.L. Patton, A. Teng, A. Randall, X. Liang, P.L. Felgner, and L.M. de la Maza Whole genome identification of C. trachomatis immunodominant antigens after genital tract infections and effect of antibiotic treatment of pigtailed macaques J Proteomics 108 2014 99 109
22. J. Rödel, C. Grosse, H. Yu, K. Wolf, G.P. Otto, E. Liebler-Tenorio, and et al. Persistent Chlamydia trachomatis infection of HeLa cells mediates apoptosis resistance through a Chlamydia protease-like activity factor-independent mechanism and induces high mobility group box 1 release Infect Immun 80 1 2012 195 205
23. A.M. Scurlock, L.C. Frazer, C.W. Andrews, C.M. O'Connell, I.P. Foote, S.L. Bailey, and et al. Interleukin-17 contributes to generation of Th1 immunity and neutrophil recruitment during Chlamydia muridarum genital tract infection but is not required for macrophage influx or normal resolution of infection Infect Immun 79 3 2011 1349 1362
24. L.C. Frazer, A.M. Scurlock, M.A. Zurenski, M.M. Riley, M. Mintus, D.A. Pociask, and et al. IL-23 induces IL-22 and IL-17 production in response to Chlamydia muridarum genital tract infection, but the absence of these cytokines does not influence disease pathogenesis Am J Reprod Immunol 70 6 2013 472 484
25. D.W. Andrew, M. Cochrane, J.H. Schripsema, K.H. Ramsey, S.J. Dando, C.P. O'Meara, and et al. The duration of Chlamydia muridarum genital tract infection and associated chronic pathological changes are reduced in IL-17 knockout mice but protection is not increased further by immunization PLoS One 8 9 2013 e76664
26. C.P. O'Meara, C.W. Armitage, M.C. Harvie, D.W. Andrew, P. Timms, N.Y. Lycke, and et al. Immunity against a Chlamydia infection and disease may be determined by a balance of IL-17 signaling Immunol Cell Biol 92 3 2014 287 297
27. R. Barral, R. Desai, X. Zheng, L.C. Frazer, G.S. Sucato, C.L. Haggerty, and et al. Frequency of Chlamydia trachomatis-specific T cell interferon-γ and interleukin-17 responses in CD4-enriched peripheral blood mononuclear cells of sexually active adolescent females J Reprod Immunol 103 2014 29 37
28. R. Jha, P. Srivastava, S. Salhan, A. Finckh, C. Gabay, A. Mittal, and et al. Spontaneous secretion of interleukin-17 and -22 by human cervical cells in Chlamydia trachomatis infection Microbes Infect 13 2 2011 167 178
29. H. Öhman Immunogenetic risk factors of Chlamydia-induced tubal factor infertility PhD Thesis 2012 National Institute for Health and Welfare Helsinki, Finland
30. J.E. den Hartog, S. Ouburg, J.A. Land, J.M. Lyons, J.I. Ito, A.S. Peña, and et al. Do host genetic traits in the bacterial sensing system play a role in the development of Chlamydia trachomatis-associated tubal pathology in subfertile women? BMC Infect Dis 6 2006 122
31. O. Karimi, S. Ouburg, H.J. de Vries, A.S. Peña, J. Pleijster, J.A. Land, and et al. TLR2 haplotypes in the susceptibility to and severity of Chlamydia trachomatis infections in Dutch women Drugs Today (Barc) 45 Suppl. B 2009 67 74
32. M. Al-Kuhlani, J. Rothchild, S. Pal, L.M. de la Maza, S. Ouburg, S.A. Morré, and et al. TRAIL-R1 is a negative regulator of pro-inflammatory responses and modulates long-term sequelae resulting from Chlamydia trachomatis infections in humans PLoS One 9 4 2014 e93939
33. S.J. Rasmussen, L. Eckmann, A.J. Quayle, L. Shen, Y.X. Zhang, D.J. Anderson, and et al. Secretion of proinflammatory cytokines by epithelial cells in response to Chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis J Clin Invest 99 1997 77 87
34. A.A. Abdul-Sater, N. Saïd-Sadier, E.V. Padilla, and D.M. Ojcius Chlamydial infection of monocytes stimulates IL-1β secretion through activation of the NLRP3 inflammasome Microbes and infection Institut Pasteur 12 0 2010 652 661
35. M.D. Cooper, J. Rapp, C. Jeffery-Wiseman, R.C. Barnes, and D.S. Stephens Chlamydia trachomatis infection of human fallopian tube organ cultures J Gen Microbiol 136 6 1990 1109 1115
36. M. Kessler, J. Zielecki, O. Thieck, H.J. Mollenkopf, C. Fotopoulou, and T.F. Meyer Chlamydia trachomatis disturbs epithelial tissue homeostasis in fallopian tubes via paracrine Wnt signaling Am J Pathol 180 1 2012 186 198
37. M. Hvid, A. Baczynska, B. Deleuran, J. Fedder, H.J. Knudsen, C. Christiansen, and et al. Interleukin-1 is the initiator of Fallopian tube destruction during Chlamydia trachomatis infection Cell Microbiol 9 12 2007 2795 2803
38. M. Toth, J. Jeremias, W.J. Ledger, and S.S. Witkin In vivo tumor necrosis factor production in women with salpingitis Surg Gynecol Obstet 174 5 1992 359 362
39. B.S. Reddy, S. Rastogi, B. Das, S. Salhan, S. Verma, and A. Mittal Cytokine expression pattern in the genital tract of Chlamydia trachomatis positive infertile women - implication for T-cell responses Clin Exp Immunol 137 3 2004 552 558
40. D. Sbardella, G.F. Fasciglione, M. Gioia, C. Ciaccio, G.R. Tundo, S. Marini, and et al. Human matrix metalloproteinases: an ubiquitarian class of enzymes involved in several pathological processes Mol Aspects Med 33 2 2012 119 208
41. M.T. Imtiaz, J.H. Schripsema, I.M. Sigar, J.N. Kasimos, and K.H. Ramsey Inhibition of matrix metalloproteinases protects mice from ascending infection and chronic disease manifestations resulting from urogenital Chlamydia muridarum infection Infect Immun 74 10 2006 5513 5521
42. R. Springall, L.M. Amezcua-Guerra, H. Gonzalez-Pacheco, J. Furuzawa-Carballeda, L. Gomez-Garcia, R. Marquez-Velasco, and et al. Interferon-gamma increases the ratio of matrix metalloproteinase-9/tissue inhibitor of metalloproteinase-1 in peripheral monocytes from patients with coronary artery disease PLoS One 8 8 2013 e72291
43. M.S. Humphrys, T. Creasy, Y. Sun, A.C. Shetty, M.C. Chibucos, E.F. Drabek, and et al. Simultaneous transcriptional profiling of bacteria and their host cells PLoS One 8 12 2013 e80597
44. K.H. Ramsey, I.M. Sigar, J.H. Schripsema, N. Shaba, and K.P. Cohoon Expression of matrix metalloproteinases subsequent to urogenital Chlamydia muridarum infection of mice Infect Immun 73 2005 6962 6973
45. K.A. Ault, K.A. Kelly, P.E. Ruther, A.A. Izzo, L.S. Izzo, I.M. Sigar, and et al. Chlamydia trachomatis enhances the expression of matrix metalloproteinases in an in vitro model of the human fallopian tube infection Am J Obstet Gynecol 187 5 2002 1377 1383
46. J.U. Igietseme, L. Omosun, J. Partin, and et al. Prevention of Chlamydia-induced infertility by inhibition of local caspase activity J Infect Dis 207 2013 1095 1104
47. B.A. Refaat, A.O. Bahathiq, S. Sockanathan, R.L. Stewart, M. Wells, and W.L. Ledger Production and localization of activins and activin type IIA and IIB receptors by the human endosalpinx Reproduction 128 2 2004 249 255
48. B. Refaat, M. Al-Azemi, I. Geary, and A. Eley Ledger W Role of activins and inducible nitric oxide in the pathogenesis of ectopic pregnancy in patients with or without Chlamydia trachomatis infection Clin Vaccine Immunol 16 10 2009 1493 1503
49. J.L. Shaw, G.S. Wills, K.F. Lee, P.J. Horner, M.O. McClure, V.M. Abrahams, and et al. Chlamydia trachomatis infection increases fallopian tube PROKR2 via TLR2 and NFkappaB activation resulting in a microenvironment predisposed to ectopic pregnancy Am J Pathol 178 2011 253 260
50. J.L. Shaw, and A.W. Horne The paracrinology of tubal ectopic pregnancy Mol Cell Endocrinol 358 2 2012 216 222
51. D.J. Phillips, D.M. de Kretser, and M.P. Hedger Activin and related proteins in inflammation: not just interested bystanders Cytokine Growth Factor Rev 20 2 2009 153 164
52. R. Shao, S.X. Zhang, B. Weijdegård, S. Zou, E. Egecioglu, A. Norström, and et al. Nitric oxide synthases and tubal ectopic pregnancies induced by Chlamydia infection: basic and clinical insights Mol Hum Reprod 16 12 2010 907 915
53. P. Apari, J.D. de Sousa, and V. Müller Why sexually transmitted infections tend to cause infertility: an evolutionary hypothesis PLoS Pathog 10 8 2014 e1004111