Role of neutrophilic granulocytes in the development of endometriosis


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Abstract

Contemporary literature data have been analyzed to consider the role of neutrophilic granulocytes in the development of inflammation as one of the leading pathogenetic mechanisms of endometriosis development. It has been shown that the idea of neutrophilic granulocytes in the innate immunity system that plays one of the central roles in protecting the body from adverse effects has now expanded. The neutrophils exhibit a diverse spectrum of effector (generation of oxidative radicals, release of granules and formation of neutrophilic extracellular networks) and regulatory (production of cytokines, chemokines, angiogenic and fibrogenic factors) functions, which is due to the existence of a great number of neutrophil phenotypes that have different receptors that determine their functional capabilities. When interacting with other cells of the innate and adaptive immunity systems, the neutrophils are actively involved in the development of inflammation. Taken together, these data highlight the new role of neutrophils, which is associated with the pathogenesis of endometriosis in early events, such as angiogenesis and modulation of the local inflammatory environment. Conclusion. The potentiated response to formyl peptide due to spontaneous neutrophil stimulation in pregnant women with preeclampsia suggests that their peripheral blood contain primed cells. This total response may suggest that the mechanism of stimulation of neutrophils due to their adhesion on the cell wall and to fMLP stimulation is different, additive in nature, and is carried out by different processes

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About the authors

Evgeny I. Astashkin

Russian Medical Academy of Continuing Professional Education, Ministry of Health of Russia; Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

Email: ast-med@mail.ru
PhD, MD(Medicine) Professor, Department of General Pathology and Pathophysiology

Lubov V. Krechetova

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

Email: l_krechetova@oparina4.ru
PhD, MD(Medicine), Head of the laboratory of clinical immunology

Lubov V. Krechetova

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia

Email: L_Vanko@oparina4.ru
PhD, MD(Medicine) Professor, leading researcher of the Laboratory of clinical immunology

References

  1. Адамян Л.В., Кулаков В.И., Андреева Е.Н. Эндометриозы. М.: Медицина; 2006. 416с. [Adamyan L.V., Kulakov V.I., Andreeva E.N. Endometriosis. Moscow: Meditsina; 2006. 416 p. (in Russian)].
  2. Burney R.O., Giudice L.C. Pathogenesis and pathophysiology of endometriosis. Fertil. Steril. 2012; 98(3): 511-9. https://dx.doi.org/10.1016/j. fertnstert.2012.06.029.
  3. Koninckx P.R., Ussia A., Keckstein J., Wattiez A., Adamyan L. Epidemiology of subtle, typical, cystic, аnd deep endometriosis: a systematic review. Gynecol. Surg. 2016; 13: 457-67. https://dx.doi.org/10.1007/s10397-016-0970-4.
  4. Bulun S.E., Yilmaz B.D., Sison Ch., Miyazaki K., Bernardi L., Liu Sh. et al. Endometriosis. Endocr. Rev. 2019; 40(4):1048-79. https://dx.doi.org/10.1210/ er.2018-00242.
  5. Bulun S.E., Monsavais D., Pavone M.E., Dyson M., Xue Q., Attar E. et al. Role of estrogen receptor-β in endometriosis. Nat. Med. 2012; 18(7): 1016-8. https:// dx.doi.org/10.1038/nm.2855.
  6. Shao R., Cao S., Wang X., Feng Y., Billig H. The elusive and controversial roles of estrogen and progesterone receptors in human endometriosis. Am. J. Transl. Res. 2014; 6(2): 104-13.
  7. Bulun S.E., Monsivais D., Kakinuma T., Furukawa Y., Bernardi L., Pavone M.E., Dyson M. Molecular biology of endometriosis: from aromatase to genomic abnormalities. Semin. Reprod. Med. 2015; 33(3): 220-4. https://dx.doi. org/10.1055/s-0035-1554053.
  8. Izumi G., Koga K., Takamura M., Makabe T., Satake E., Takeuchi A. et al. Involvement of immune cells in the pathogenesis of endometriosis. J. Obstet. Gynaecol. Res. 2018; 44(2): 191-8. https://dx.doi.org/10.1111/jog.13559.
  9. Khan Kh.N., Fujishita A., Hiraki K., Kitajima M., Nakashima M., Fushiki S., Kitawaki J. Bacterial contamination hypothesis: a new concept in endometriosis. Reprod. Med. Biol. 2018; 17(2): 125-33. https://dx.doi.org/10.1002/rmb2.12083.
  10. Augoulea A., Alexandrou A., Creatsa M., Vrachnis N., Lambrinoudaki I. Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch. Gynecol. Obstet. 2012; 286(1): 99-103. https://dx.doi.org/10.1007/ s00404-012-2357-8.
  11. Kobayashi H., Higashiura Y., Shigetomi H., Kajihara H. Pathogenesis of endometriosis: The role of initial infection and subsequent sterile inflammation (Review). Mol. Med. Rep. 2013; 9(1): 9-15. https://dx.doi.org/10.3892/ mmr.2013.1755.
  12. Lin Y.H., Chen Y.H., Chang H.Y.,Au H.K., Tzeng C.R., Huang Y.H. Chronic niche inflammation in endometriosis-associated infertility: current understanding and future therapeutic strategies. Int. J. Mol. Sci. 2018; 19(8): 2385. https://dx.doi. org/10.3390/ijms19082385.
  13. Ahn S.H., Monsanto S.P., Miller C., Singh S.S., Thomas R., Tayade C. Pathophysiology and immune dysfunction in endometriosis. Biomed. Res. Int. 2015; 2015: 795976. https://dx.doi.org/10.1155/2015/795976.
  14. Scapini P., Cassatella M.A. Social networking of human neutrophils within the immune system. Blood. 2014; 124(5): 710-9. https://dx.doi.org/10.1182/blood-2014-03-453217.
  15. Mantovani A., Cassatella M.A., Costantini C., Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 2011; 11(8): 519-31. https://dx.doi.org/10.1038/nri3024.
  16. Rieber N., Gille C., Kostlin N., Schafer I., Spring B., Ost M. et al. Neutrophilic myeloid-derived suppressor cells in cord blood modulate innate and adaptive immune responses. Clin. Exp. Immunol. 2013; 174(1): 45-52. https://dx.doi. org/10.1111/cei.12143.
  17. Greten T.F, Manns M.P., Korangy F. Myeloid derived suppressor cells in human diseases. Int. Immunopharmacol. 2011; 11(7): 802-7. htths://dx.doi. org/10.1016/j.intimp.2011.01.003.
  18. Pillay J., Tak T., Kamp V.M., Koenderman L. Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell. Mol. Life Sci. 2013; 70(20): 3813-27. https://dx.doi.org/10.1007/s00018- 013-1286-4.
  19. Zhang T., Zhou J., Man G.C.W., Leung K.T., Liang B., Xiao B. et al. MDSCs drive the process of endometriosis by enhancing angiogenesis and are a new potential therapeutic target. Eur. J. Immunol. 2018; 48(6): 1059-73. https:// dx.doi.org/10.1002/eji.201747417.
  20. Jiang H., Bi K., Wang K., Lu Z., Xu Y., Guo P. et al. Reduction of myeloid derived suppressor cells by inhibiting Notch pathway prevents the progression of endometriosis in mice model. Int. Immunopharmacol. 2020; 82: 106352. https://dx.doi.org/10.1016/j.intimp.2020.106352.
  21. Нестерова И.В., Колесникова Н.В., Чудилова Г.А., Ломтатидзе Л.В., Ковалева С.В., Евглевский А.А., Нгуен Т.Л. Новый взгляд на нейтрофильные гранулоциты: переосмысление старых догм. Часть 2. Инфекция и иммунитет. 2018; 8(1): 7-18. [Nesterova I.V., Kolesnikova N.V., Chudilova G.A., Lomtatidze L.V., Kovaleva S.V., Evglevsky A.A., Nguen T.L. A new look at neutrophilic granulocytes: rethinking old dogmas. Part 2. Infection and immunity. 2018; 8(1): 7-18. doi.org/10.15789/2220-7619-2018-1-7-18. (in Russian)]. https://dx.doi.org/10.15789/2220-7619-2018-1-7-18.
  22. Fuchs T.A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007; 176(2): 231-41. https://dx.doi.org/10.1083/jcb.200606027.
  23. Stoiber W., Obermayer A., Steinbacher P., Krautgartner W.D. The role of reactive oxygen species (ROS) in the formation of extracellular traps (ETs) in humans. Biomolecules. 2015; 5(2): 702-23. https://dx.doi.org/10.3390/biom5020702.
  24. Berkes E., Oehmke F., Tinneberg H.R., Preissner K.T., Saffarzadeh M. Association of neutrophil extracellular traps with endometriosis-related chronic inflammation. Eur. J. Obstet. Gynecol. Reprod. Biol. 2014; 183: 193-200. https://dx.doi.org/10.1016/j.ejogrb.2014.10.040.
  25. Christoffersson G., Phillipson M. The neutrophil: one cell on many missions or many cells with different agendas? Cell Tissue Res. 2018; 371(3): 415-23. https://dx.doi.org/10.1007/s00441-017-2780-z.
  26. Wright H.L., Thomas H.B., Moots R.J., Edwards S.W. RNA-Seq reveals activation of both common and cytokine-specific pathways following neutrophil priming. PLoS One. 2013; 8(3): e58598. https://dx.doi.org/10.1371/journal. pone.0058598.
  27. El Benna J., Hurtado Nedelec M., Marzaioli V., Marie J.C., Gougerot Pocidalo M.A., Pham My-Chan Dang. Priming of the neutrophil respiratory burst: role in host defense and inflammation. Immunol. Rev. 2016; 273(1): 18093. https://dx.doi.org/10.1111/imr.12447.
  28. Egholm C., Heeb L.E.M., Impellizzieri D., Boyman O. The regulatory effects of interleukin-4 receptor signaling on neutrophils in type 2 immune responses. Front. Immunol. 2019; 10: 2507. https://dx.doi.org/10.3389/fimmu.2019.02507.
  29. Huhtinen K., Desai R., Stahle M., Salminen A., Handelsman D.J., Perheentupa A., Poutanen M. Endometrial and endometriotic concentrations of estrone and estradiol are determined by local metabolism rather than circulating levels. J. Clin. Endocrinol. Metab. 2012; 97(11): 4228-35. https://dx.doi.org/10.1210/ jc.2012-1154.
  30. Bulun S.E., Cheng Y.H., Pavone M.E., Xue Q., Attar E, Trukhacheva E. et al. Estrogen receptor-beta, estrogen receptor-alpha, and progesterone resistance in endometriosis. Semin. Reprod. Med. 2010; 28(1): 36-43. https://dx.doi. org/10.1055/s-0029-1242991.
  31. Burns K.A., Thomas S.Y., Hamilton K.J., Young S.L, Cook D.N., Korach K.S. Early endometriosis in females is directed by immune-mediated estrogen receptor a and IL-6 cross-talk. Endocrinology. 2018; 159(1): 103-18. https:// dx.doi.org/10.1210/en.2017-00562.
  32. Takamura M., Koga K., Izumi G., Ur at a Y., Nagai M., Hasegawa A. et al. Neutrophil depletion reduces endometriotic lesion formation in mice. Am. J. Reprod. Immunol. 2016; 76(3): 193-8. https://dx.doi.org/10.1111/aji.12540.
  33. Milewski L., Dziunycz P., Barcz E., Radomski D., Roszkowski P.I., Korczak-Kowalska G. et al. Increased levels of human neutrophil peptides 1, 2, and 3 in peritoneal fluid of patients with endometriosis: association with neutrophils, T cells and IL-8. J. Reprod. Immunol. 2011; 91(1-2): 64-70. https://dx.doi.org/10.1016/j.jri.2011.05.008.
  34. Tariverdian N., Siedentopf F., Rucke M., Blois S.M., Klapp B.F., Arck P.C. Intraperitoneal immune cell status in infertile women with and without endometriosis. Reprod. Immunol. 2009; 80(1-2): 80-90. https://dx.doi.org/10.1016/j.jri.2008.12.005.
  35. Yang H., Lang J.H., Zhu L., Wang S., Sha G.H., Zhang Y. Diagnostic value of the neutrophil-to-lymphocyte ratio and the combination of serum CA-125 for stages III and IV endometriosis. Chin. Med. J. (Engl.). 2013; 126(11): 2011-4.
  36. Lin Y.J., Lai M.D., Lei H.Y., Wing L.Y. Neutrophils and macrophages promote angiogenesis in the early stage of endometriosis in a mouse model. Endocrinology. 2006; 147(3): 1278-86. https://dx.doi.org/10.1210/en.2005-0790.
  37. Rocha A.L., Reis F.M., Taylor R.N. Angiogenesis and endometriosis. Obstet. Gynecol. Int. 2013; 2013: 859619. https://dx.doi.org/10.1155/2013/859619.
  38. Sikora J., Smycz-Kubanska M., Mielczarek-Palacz A., Kondera-Anasz Z. Abnormal peritoneal regulation of chemokine activation-The role of IL-8 in pathogenesis of endometriosis. Am. J. Reprod. Immunol. 2017; 77(4): e12622. https://dx.doi.org/10.1111/aji.12622.
  39. Delbandi A.A., Mahmoudi M., Shervin A., Heidari S., Kolahdouz-Mohammadi R., Zarnani A.H. Evaluation of apoptosis and angiogenesis in ectopic and eutopic stromal cells of patients with endometriosis compared to non-endometriotic controls. BMC Womens Health. 2020; 20(1): 3. https://dx.doi.org/10.1186/ s12905-019-0865-4.
  40. Symons L.K., Miller J.E., Tyryshkin K., Monsanto S.P., Marks R.M., Lingegowda H. et al. Neutrophil recruitment and function in endometriosis patients and a syngeneic murine model. FASEB J. 2020; 34(1): 1558-75. https://dx.doi. org/10.1096/fj.201902272R.

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