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Fas and Fas-Ligand in Eutopic and Ectopic Endometrium of Women With Endometriosis: The Possible Immune Privilege of Ectopic Endometrium

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Abstract

The Fas/Fas-Ligand system is an important mediator of apoptosis. We analyzed their expression in tissue specimens obtained from 33 women with severe endometriosis and 18 women without endometriosis. Immunostaining for Fas-Ligand in the eutopic endometrium was stronger in the epithelial cells of secretory phase, while the epithelial cells of endometriotic lesions showed a significantly stronger staining for Fas-Ligand independently from the menstrual phase (P < 0.01). Immunostaining for Fas in the eutopic endometrium showed a reduced staining during the proliferative phase, whereas it was strong in the secretory phase. The epithelial cells of the ectopic endometrium showed a reduced staining for Fas independently from the menstrual phase with respect to the eutopic tissue (P < 0.01). The reduced expression of Fas in the ectopic endometrium with the contemporary higher expression of Fas-Ligand in the corresponding cells suggests a possible immune privilege of this tissue.

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References

  1. Olive DL, Pritts EA. Treatment of endometriosis. N Engl J Med. 2001;345(4):266–275.

    CAS  PubMed  Google Scholar 

  2. Sørensen SS, Andersen LF, Lose G. Endometriosis by implantation: a complication of endometrial ablation. Lancet. 1994;343(8907):1226.

    PubMed  Google Scholar 

  3. Gleicher N, El-Roy A, Confino E, Friberg J. Abnormal autoantibodies in endometriosis: is endometriosis an autoimmune disease? Obstet Gynecol. 1987;70(1):115–122.

    CAS  PubMed  Google Scholar 

  4. Hill JA. Immunology and endometriosis. Fertil Steril. 1992;58(2):262–264.

    CAS  PubMed  Google Scholar 

  5. Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001;75(1):1–10.

    CAS  PubMed  Google Scholar 

  6. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science. 1995;267(5203):1456–62.

    CAS  PubMed  Google Scholar 

  7. Taylor HS, Fei X. Emx2 regulates mammalian reproduction by altering endometrial cell proliferation. Mol Endocrinol. 2005;19(11):2839–2846.

    CAS  PubMed  Google Scholar 

  8. Yang H, Taylor HS, Lei C, Cheng C, Zhang W. Hormonal regulation of galectin 3 in trophoblasts and its effects on endometrium. Reprod Sci. 2011;18(11):1118–1127.

    CAS  PubMed  Google Scholar 

  9. Taniguchi F, Kaponis A, Izawa M, et al. Apoptosis and endometriosis. Front Biosci. 2011;3:648–662.

    Google Scholar 

  10. Penna I, Du H, Ferriani R, Taylor HS. Calpain5 expression is decreased in endometriosis and regulated by HOXA10 in human endometrial cells. Mol Hum Reprod. 2008;14(10):613–618.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Pacchiarotti A, Caserta D, Sbracia M, Moscarini M. Expression of oct-4 and c-kit antigens in endometriosis. Fertil Steril. 2011;95(3):1171–1173.

    CAS  PubMed  Google Scholar 

  12. Song J, Rutherford T, Naftolin F, Brown S, Mor G. Hormonal regulation of apoptosis and the Fas and Fas ligand system in human endometrial cells. Mol Hum Reprod. 2002;8(5):447–455.

    CAS  PubMed  Google Scholar 

  13. Selam B, Kayisli UA, Mulayim N, Arici A. Regulation of Fas ligand expression by estradiol and progesterone in human endometrium. Biol Reprod. 2001;65(4):979–985.

    CAS  PubMed  Google Scholar 

  14. Otsuki Y. Apoptosis in human endometrium: apoptotic detection methods and signaling. Med Electron Microsc. 2001;34(3):166–173.

    CAS  PubMed  Google Scholar 

  15. Watanabe H, Kanzaki H, Narukawa S, et al. Bcl-2 and FAS expression in eutopic and ectopic human endometrium during the menstrual cycle in relation to endometrial cell apoptosis. Am J Obstet Gynecol. 1997;176(2):360–368.

    CAS  PubMed  Google Scholar 

  16. Yamashita H, Otsuki Y, Matsumoto K, Ueki K, Ueki M. Fas ligand, Fas antigen and Bcl-2expression in human endometrium during the menstrual cycle. Mol Hum Reprod. 1999;5(4):358–364.

    CAS  PubMed  Google Scholar 

  17. Harada M, Suganuma N, Furuhashi M, et al. Detection of apoptosis in human endometriotic tissues. Mol Hum Reprod. 1996;2(5):307–15.

    CAS  PubMed  Google Scholar 

  18. Garcia-Velasco JA, Mulayim N, Kayisli UA, Arici A. Elevated soluble Fas ligand levels may suggest a role for apoptosis in women with endometriosis. Fertil Steril. 2002;78(4):855–859.

    PubMed  Google Scholar 

  19. The American Fertility Society. Revised American Fertility Society classification of endometriosis:1985. Fertil Steril. 1985;43(3):351–352.

    Google Scholar 

  20. Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981;29(4):577–580.

    CAS  PubMed  Google Scholar 

  21. McCarty KS, Miller LS, Cox EB. Estrogen receptor analysis, correlation of biochemical and immunohistochemical methods using monoclonal anti-receptor antibodies. Arch Pathol Lab Med. 1985;109(8):716–721.

    PubMed  Google Scholar 

  22. Hopwood D, Levison DA. Atrophy and apoptosis in the cyclical human endometrium. J Pathol. 1976;119(3):159–166.

    CAS  PubMed  Google Scholar 

  23. Kokawa K, Shikone T, Nakano R. Apoptosis in the human uterine endometrium during the menstrual cycle. J Clin Endocrinol Metab. 1996;81(11):4144–4147.

    CAS  PubMed  Google Scholar 

  24. Illanes SE, Maisey K, Sandoval M. Fas ligand(+) fallopian tube epithelium induces apoptosis in both Fas receptor(+) T lymphocytes and endometrial cells. Fertil Steril. 2013:100(2):550–560.

    CAS  PubMed  Google Scholar 

  25. Tabibzadeh S, Zupi E, Babaknia A, Liu R, Marconi D, Romanini C. Site and menstrual cycle-dependent expression of proteins of the tumour necrosis factor (TNF) receptor family, and BCL-2oncoprotein and phase-specific production of TNF alpha in human endometrium. Hum Reprod. 1995;10(2):277–286.

    CAS  PubMed  Google Scholar 

  26. Sturlese E, Salmeri FM, Retto G, et al. Dysregulation of the Fas/FasL system in mononuclear cells recovered from peritoneal fluid of women with endometriosis. J Reprod Immunol. 2011;92(1–2):74–81.

    CAS  PubMed  Google Scholar 

  27. Chung HW, Wen Y, Chun SH, Nezhat C, Woo BH, Lake Polan M. Matrix metalloproteinase-9 andtissue inhibitor of metalloproteinase-3 mRNA expression in ectopic and eutopic endometrium inwomen with endometriosis: a rationale for endometriotic invasiveness. Fertil Steril. 2001;75(1):152–159.

    CAS  PubMed  Google Scholar 

  28. Chung HW, Lee JY, Moon HS, et al. Matrix metalloproteinase-2, membranous type 1 matrix metalloproteinase, and tissue inhibitor of metalloproteinase-2 expression inectopic and eutopic endometrium. Fertil Steril. 2002;78(4):787–795.

    PubMed  Google Scholar 

  29. Osteen KG, Yeaman GR, Bruner-Tran KL. Matrix metalloproteinases and endometriosis. Semin Reprod Med. 2003;21(2):155–164.

    CAS  PubMed  Google Scholar 

  30. Ueda M, Yamashita Y, Takehara M, et al. Survivin gene expression in endometriosis. J Clin Endocrinol Metab. 2002;87(7):3452–3459.

    CAS  PubMed  Google Scholar 

  31. Abreu-Martin MT, Vidrich A, Lynch DH, Targan SR. Divergent induction of apoptosis and IL-8 secretion in HT-29 cells in response to TNF-alpha and ligation of Fas antigen. J Immunol. 1995;155(9):4147–4154.

    CAS  PubMed  Google Scholar 

  32. Arici A, Tazuke SI, Attar E, Kliman HJ, Olive DL. Interleukin-8 concentration in peritoneal fluidof patients with endometriosis and modulation of interleukin-8 expression in human mesothelial cells. Mol Hum Reprod. 1996;2(1):40–45.

    CAS  PubMed  Google Scholar 

  33. Kalu E, Sumar N, Giannopoulos T, et al. Cytokine profiles in serum and peritoneal fluid from infertile women with and without endometriosis. J Obstet Gynaecol Res. 2007;33(4):490–495.

    CAS  PubMed  Google Scholar 

  34. Selam B, Kayisli UA, Garcia-Velasco JA, Akbas GE, Arici A. Regulation of fas ligand expression by IL-8 in human endometrium. J Clin Endocrinol Metab. 2002;87(8):3921–3927.

    CAS  PubMed  Google Scholar 

  35. Gebel HM, Braun DP, Tambur A, Frame D, Rana N, Dmowski WP. Spontaneous apoptosis ofendometrial tissue is impaired in women with endometriosis. Fertil Steril. 1998;69(6):1042–1047.

    CAS  PubMed  Google Scholar 

  36. Gompel A, Sabourin JC, Martin A, et al. Bcl-2 expression in normal endometrium during the menstrual cycle. Am J Pathol. 1994;144(6):1195–1202.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. McLaren J, Prentice A, Charnock-Jones DS, Sharkey AM, Smith SK. Immunolocalization of the apoptosis regulating proteins bcl-2 and bax in human endometrium and isolated peritoneal fluid macrophages in endometriosis. Hum Reprod. 1997;12(1):146–152.

    CAS  PubMed  Google Scholar 

  38. Igarashi TM, Bruner-Tran KL, Yeaman GR, et al. Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fertil Steril. 2005;84(1):67–74.

    CAS  PubMed  Google Scholar 

  39. Kayisli UA, Guzeloglu-Kayisli O, Arici A. Endocrine-immune interactions in human endometrium. Ann N Y Acad Sci. 2004;1034:50–63.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Urologic and Gynaecologic Science, University of Tor Vergata, Rome, Italy

    Marco Sbracia MD

  2. Praxi Provita, Praxis DS, Via Magnagrecia 117, 00183, Rome, Italy

    Claudia Valeri BS, Giulio Biagiotti MD, Alessandro Pacchiarotti MD & Arianna Pacchiarotti MD, PhD

  3. Department of Urologic and Gynaecologic Science, University of Sapienza, Rome, Italy

    Gabriele Antonini MD, Alessandro Pacchiarotti MD & Arianna Pacchiarotti MD, PhD

Authors
  1. Marco Sbracia MD
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  2. Claudia Valeri BS
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  3. Gabriele Antonini MD
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  4. Giulio Biagiotti MD
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  5. Alessandro Pacchiarotti MD
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  6. Arianna Pacchiarotti MD, PhD
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Correspondence to Claudia Valeri BS.

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Sbracia, M., Valeri, C., Antonini, G. et al. Fas and Fas-Ligand in Eutopic and Ectopic Endometrium of Women With Endometriosis: The Possible Immune Privilege of Ectopic Endometrium. Reprod. Sci. 23, 81–86 (2016). https://doi.org/10.1177/1933719115594019

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  • DOI: https://doi.org/10.1177/1933719115594019

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