Clinical and Experimental Reproductive Medicine

  • 제45권1호
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  • Pages.1-9
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  • 2018
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  • 2233-8233(pISSN)
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  • 2233-8241(eISSN)
대한생식의학회 (The Korean Society for Reproductive Medicine)
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DOI QR Code

Variable localization of Toll-like receptors in human fallopian tube epithelial cells

  • Amjadi, Fatemehsadat (Department of Anatomical Sciences, School of Medicine, Iran University of Medical Sciences) ;
  • Zandieh, Zahra (Department of Anatomical Sciences, School of Medicine, Iran University of Medical Sciences) ;
  • Salehi, Ensieh (Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR) ;
  • Jafari, Reza (Department of Immunology, Iran University of Medical Sciences) ;
  • Ghasemi, Nasrin (Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Aflatoonian, Abbas (Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Fazeli, Alireza (Academic Unit of Reproductive and Developmental Medicine, Department of Oncology and Metabolism, University of Sheffield) ;
  • Aflatoonian, Reza (Department of Endocrinology and Female Infertility, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR)
  • 투고 : 2017.09.02
  • 심사 : 2017.10.14
  • 발행 : 2018.03.31
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초록

Objective: To determine the localization, expression, and function of Toll-like receptors (TLRs) in fallopian tube epithelial cells. Methods: The localization of TLRs in fallopian tube epithelial cells was investigated by immunostaining. Surprisingly, the intensity of staining was not equal in the secretory and ciliated cells. After primary cell culture of fallopian tube epithelial cells, ring cloning was used to isolate colonies of ciliated epithelial cells, distinct from non-ciliated epithelial cells. The expression of TLRs 1-10 was examined by quantitative real-time polymerase chain reaction, and protein localization was confirmed by immunostaining. The function of the TLRs was determined by interleukin (IL)-6 and IL-8 production in response to TLR2, TLR3, TLR5, TLR7, and TLR9 ligands. Results: Fallopian tube epithelial cells expressed TLRs 1-10 in a cell-type-specific manner. Exposing fallopian tube epithelial cells to TLR2, TLR3, TLR5, TLR7, and TLR9 agonists induced the secretion of proinflammatory cytokines such as IL-6 and IL-8. Conclusion: Our findings suggest that TLR expression in the fallopian tubes is cell-type-specific. According to our results, ciliated cells may play more effective role than non-ciliated cells in the innate immune defense of the fallopian tubes, and in interactions with gametes and embryos.

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참고문헌

  1. Lyons RA, Saridogan E, Djahanbakhch O. The reproductive significance of human fallopian tube cilia. Hum Reprod Update 2006;12:363-72. https://doi.org/10.1093/humupd/dml012
  2. Patek E. The epithelium of the human fallopian tube: a surface ultrastructural and cytochemical study. Acta Obstet Gynecol Scand Suppl 1974;31:1-28.
  3. Critoph FN, Dennis KJ. Ciliary activity in the human oviduct. Obstet Gynecol Surv 1977;32:602-3. https://doi.org/10.1097/00006254-197709000-00015
  4. Witkin SS. Immunological aspects of genital chlamydia infections. Best Pract Res Clin Obstet Gynaecol 2002;16:865-74. https://doi.org/10.1053/beog.2002.0326
  5. Mardh PA. Tubal factor infertility, with special regard to chlamydial salpingitis. Curr Opin Infect Dis 2004;17:49-52. https://doi.org/10.1097/00001432-200402000-00010
  6. Cates W Jr, Rolfs RT Jr, Aral SO. Sexually transmitted diseases, pelvic inflammatory disease, and infertility: an epidemiologic update. Epidemiol Rev 1990;12:199-220. https://doi.org/10.1093/oxfordjournals.epirev.a036054
  7. Westrom L, Wolner-Hanssen P. Pathogenesis of pelvic inflammatory disease. Genitourin Med 1993;69:9-17.
  8. Mardh PA. Influence of infection with Chlamydia trachomatis on pregnancy outcome, infant health and life-long sequelae in infected offspring. Best Pract Res Clin Obstet Gynaecol 2002;16:847-64. https://doi.org/10.1053/beog.2002.0329
  9. Nasu K, Narahara H. Pattern recognition via the toll-like receptor system in the human female genital tract. Mediators Inflamm 2010;2010:976024.
  10. Portou MJ, Baker D, Abraham D, Tsui J. The innate immune system, toll-like receptors and dermal wound healing: a review. Vascul Pharmacol 2015;71:31-6. https://doi.org/10.1016/j.vph.2015.02.007
  11. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell 2002;111:927-30. https://doi.org/10.1016/S0092-8674(02)01201-1
  12. De Nardo D. Toll-like receptors: activation, signalling and transcriptional modulation. Cytokine 2015;74:181-9. https://doi.org/10.1016/j.cyto.2015.02.025
  13. Akira S, Takeda K, Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001;2:675-80. https://doi.org/10.1038/90609
  14. Lim KH, Staudt LM. Toll-like receptor signaling. Cold Spring Harb Perspect Biol 2013;5:a011247. https://doi.org/10.1101/cshperspect.a011247
  15. Hacker H, Vabulas RM, Takeuchi O, Hoshino K, Akira S, Wagner H. Immune cell activation by bacterial CpG-DNA through myeloid differentiation marker 88 and tumor necrosis factor receptor-associated factor (TRAF)6. J Exp Med 2000;192:595-600. https://doi.org/10.1084/jem.192.4.595
  16. Amjadi F, Salehi E, Mehdizadeh M, Aflatoonian R. Role of the innate immunity in female reproductive tract. Adv Biomed Res 2014;3:1. https://doi.org/10.4103/2277-9175.124626
  17. Lee MS, Kim YJ. Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 2007;76:447-80. https://doi.org/10.1146/annurev.biochem.76.060605.122847
  18. Aflatoonian R, Fazeli A. Toll-like receptors in female reproductive tract and their menstrual cycle dependent expression. J Reprod Immunol 2008;77:7-13. https://doi.org/10.1016/j.jri.2007.03.014
  19. Kannaki TR, Shanmugam M, Verma PC. Toll-like receptors and their role in animal reproduction. Anim Reprod Sci 2011;125:1-12. https://doi.org/10.1016/j.anireprosci.2011.03.008
  20. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robanya I, Richards JS. Induced expression of pattern recognition receptors in cumulus oocyte complexes: novel evidence for innate immunelike functions during ovulation. Mol Endocrinol 2006;20:3228-39. https://doi.org/10.1210/me.2006-0194
  21. Liu Z, Shimada M, Richards JS. The involvement of the Toll-like receptor family in ovulation. J Assist Reprod Genet 2008;25:223-8. https://doi.org/10.1007/s10815-008-9219-0
  22. Zandieh Z, Amjadi F, Ashrafi M, Aflatoonian A, Fazeli A, Aflatoonian R. The effect of estradiol and progesterone on toll like receptor gene expression in a human fallopian tube epithelial cell line. Cell J 2016;17:678-91.
  23. Monkkonen KS, Aflatoonian R, Lee KF, Yeung WS, Tsao SW, Laitinen JT, et al. Localization and variable expression of G alpha(i2) in human endometrium and fallopian tubes. Hum Reprod 2007;22:1224-30. https://doi.org/10.1093/humrep/dem022
  24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262
  25. Aboussahoud W, Aflatoonian R, Bruce C, Elliott S, Ward J, Newton S, et al. Expression and function of Toll-like receptors in human endometrial epithelial cell lines. J Reprod Immunol 2010;84:41-51. https://doi.org/10.1016/j.jri.2009.09.008
  26. Kunz G, Beil D, Deininger H, Wildt L, Leyendecker G. The dynamics of rapid sperm transport through the female genital tract: evidence from vaginal sonography of uterine peristalsis and hysterosalpingoscintigraphy. Hum Reprod 1996;11:627-32. https://doi.org/10.1093/HUMREP/11.3.627
  27. Piomboni P, Baccetti B. Spermatozoon as a vehicle for HIV-1 and other viruses: a review. Mol Reprod Dev 2000;56(2 Suppl):238-42. https://doi.org/10.1002/(SICI)1098-2795(200006)56:2+<238::AID-MRD5>3.0.CO;2-1
  28. Kotronias D, Kapranos N. Detection of herpes simplex virus DNA in human spermatozoa by in situ hybridization technique. In Vivo 1998;12:391-4.
  29. Schaefer TM, Desouza K, Fahey JV, Beagley KW, Wira CR. Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 2004;112:428-36. https://doi.org/10.1111/j.1365-2567.2004.01898.x
  30. Lin Z, Xu J, Jin X, Zhang X, Ge F. Modulation of expression of Tolllike receptors in the human endometrium. Am J Reprod Immunol 2009;61:338-45. https://doi.org/10.1111/j.1600-0897.2009.00700.x
  31. Aflatoonian R, Tuckerman E, Elliott SL, Bruce C, Aflatoonian A, Li TC, et al. Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum Reprod 2007;22:586-93. https://doi.org/10.1093/humrep/del388
  32. Ghasemi N, Amjadi F, Salehi E, Shakeri M, Aflatoonian A, Aflatoonian R. Expression of Toll-like receptors 7-10 in human fallopian tubes. Iran J Reprod Med 2014;12:389-94.
  33. Hirata T, Osuga Y, Hamasaki K, Hirota Y, Nose E, Morimoto C, et al. Expression of toll-like receptors 2, 3, 4, and 9 genes in the human endometrium during the menstrual cycle. J Reprod Immunol 2007;74:53-60. https://doi.org/10.1016/j.jri.2006.11.004
  34. Pioli PA, Amiel E, Schaefer TM, Connolly JE, Wira CR, Guyre PM. Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract. Infect Immun 2004;72:5799-806. https://doi.org/10.1128/IAI.72.10.5799-5806.2004
  35. Hart KM, Murphy AJ, Barrett KT, Wira CR, Guyre PM, Pioli PA. Functional expression of pattern recognition receptors in tissues of the human female reproductive tract. J Reprod Immunol 2009;80:33-40. https://doi.org/10.1016/j.jri.2008.12.004
  36. Ghosh M, Schaefer TM, Fahey JV, Wright JA, Wira CR. Antiviral responses of human fallopian tube epithelial cells to toll-like receptor 3 agonist poly(I:C). Fertil Steril 2008;89(5 Suppl):1497-506. https://doi.org/10.1016/j.fertnstert.2007.05.023
  37. Girling JE, Hedger MP. Toll-like receptors in the gonads and reproductive tract: emerging roles in reproductive physiology and pathology. Immunol Cell Biol 2007;85:481-9. https://doi.org/10.1038/sj.icb.7100086
  38. Saeidi S, Shapouri F, Amirchaghmaghi E, Hoseinifar H, Sabbaghian M, Sadighi Gilani MA, et al. Sperm protection in the male reproductive tract by Toll-like receptors. Andrologia 2014;46:784-90. https://doi.org/10.1111/and.12149
  39. Amirchaghmaghi E, Taghavi SA, Shapouri F, Saeidi S, Rezaei A, Aflatoonian R. The role of Toll like receptors in pregnancy. Int J Fertil Steril 2013;7:147-54.
  40. Shimada M, Yanai Y, Okazaki T, Noma N, Kawashima I, Mori T, et al. Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization. Development 2008;135:2001-11. https://doi.org/10.1242/dev.020461
  41. Zandieh Z, Ashrafi M, Jameie B, Amanpour S, Mosaffa N, Salman Yazdi R, et al. Evaluation of immunological interaction between spermatozoa and fallopian tube epithelial cells. Andrologia 2015;47:1120-30. https://doi.org/10.1111/and.12391
  42. Morrison DK. MAP kinase pathways. Cold Spring Harb Perspect Biol 2012;4:a011254.
  43. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010;11:373-84. https://doi.org/10.1038/ni.1863
  44. Desai N, Scarrow M, Lawson J, Kinzer D, Goldfarb J. Evaluation of the effect of interleukin-6 and human extracellullar matrix on embryonic development. Hum Reprod 1999;14:1588-92. https://doi.org/10.1093/humrep/14.6.1588
  45. Du MR, Wang SC, Li DJ. The integrative roles of chemokines at the maternal-fetal interface in early pregnancy. Cell Mol Immunol 2014;11:438-48. https://doi.org/10.1038/cmi.2014.68
  46. Raidt J, Werner C, Menchen T, Dougherty GW, Olbrich H, Loges NT, et al. Ciliary function and motor protein composition of human fallopian tubes. Hum Reprod 2015;30:2871-80. https://doi.org/10.1093/humrep/dev227
  47. O'Doherty AM, Di Fenza M, Kolle S. Lipopolysaccharide (LPS) disrupts particle transport, cilia function and sperm motility in an ex vivo oviduct model. Sci Rep 2016;6:24583. https://doi.org/10.1038/srep24583

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