DOI QR코드

DOI QR Code

Immune Cells in the Female Reproductive Tract

  • Lee, Sung Ki (Department of Obstetrics and Gynecology, College of Medicine, Konyang University) ;
  • Kim, Chul Jung (Department of Obstetrics and Gynecology, College of Medicine, Konyang University) ;
  • Kim, Dong-Jae (Department of Obstetrics and Gynecology, College of Medicine, Konyang University) ;
  • Kang, Jee-Hyun (Department of Family Medicine, College of Medicine, Konyang University)
  • 투고 : 2014.12.06
  • 심사 : 2015.01.28
  • 발행 : 2015.02.28

초록

The female reproductive tract has two main functions: protection against microbial challenge and maintenance of pregnancy to term. The upper reproductive tract comprises the fallopian tubes and the uterus, including the endocervix, and the lower tract consists of the ectocervix and the vagina. Immune cells residing in the reproductive tract play contradictory roles: they maintain immunity against vaginal pathogens in the lower tract and establish immune tolerance for sperm and an embryo/fetus in the upper tract. The immune system is significantly influenced by sex steroid hormones, although leukocytes in the reproductive tract lack receptors for estrogen and progesterone. The leukocytes in the reproductive tract are distributed in either an aggregated or a dispersed form in the epithelial layer, lamina propria, and stroma. Even though immune cells are differentially distributed in each organ of the reproductive tract, the predominant immune cells are T cells, macrophages/dendritic cells, natural killer (NK) cells, neutrophils, and mast cells. B cells are rare in the female reproductive tract. NK cells in the endometrium significantly expand in the late secretory phase and further increase their number during early pregnancy. It is evident that NK cells and regulatory T (Treg) cells are extremely important in decidual angiogenesis, trophoblast migration, and immune tolerance during pregnancy. Dysregulation of endometrial/decidual immune cells is strongly related to infertility, miscarriage, and other obstetric complications. Understanding the immune system of the female reproductive tract will significantly contribute to women's health and to success in pregnancy.

키워드

참고문헌

  1. Trifonova, R. T., J. Lieberman, and B. D. van. 2014. Distribution of immune cells in the human cervix and implications for HIV transmission. Am. J. Reprod. Immunol. 71: 252-264. https://doi.org/10.1111/aji.12198
  2. Lee, S., J. Kim, B. Jang, S. Hur, U. Jung, K. Kil, B. Na, M. Lee, Y. Choi, A. Fukui, A. Gilman-Sachs, and J. Y. Kwak-Kim. 2010. Fluctuation of peripheral blood T, B, and NK cells during a menstrual cycle of normal healthy women. J. Immunol. 185: 756-762. https://doi.org/10.4049/jimmunol.0904192
  3. Wira, C. R., J. V. Fahey, M. Rodriguez-Garcia, Z. Shen, and M. V. Patel. 2014. Regulation of mucosal immunity in the female reproductive tract: the role of sex hormones in immune protection against sexually transmitted pathogens. Am. J. Reprod. Immunol. 72: 236-258. https://doi.org/10.1111/aji.12252
  4. Givan, A. L., H. D. White, J. E. Stern, E. Colby, E. J. Gosselin, P. M. Guyre, and C. R. Wira. 1997. Flow cytometric analysis of leukocytes in the human female reproductive tract: comparison of fallopian tube, uterus, cervix, and vagina. Am. J. Reprod. Immunol. 38: 350-359. https://doi.org/10.1111/j.1600-0897.1997.tb00311.x
  5. Johansson, E. L., A. Rudin, L. Wassen, and J. Holmgren. 1999. Distribution of lymphocytes and adhesion molecules in human cervix and vagina. Immunology 96: 272-277. https://doi.org/10.1046/j.1365-2567.1999.00675.x
  6. Pudney, J., A. J. Quayle, and D. J. Anderson. 2005. Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation zone. Biol. Reprod. 73: 1253-1263. https://doi.org/10.1095/biolreprod.105.043133
  7. King, A. 2000. Uterine leukocytes and decidualization. Hum. Reprod. Update 6: 28-36. https://doi.org/10.1093/humupd/6.1.28
  8. Yeaman, G. R., J. E. Collins, M. W. Fanger, C. R. Wira, and P. M. Lydyard. 2001. $CD8^+$ T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking. Immunology 102: 434-440. https://doi.org/10.1046/j.1365-2567.2001.01199.x
  9. van den, H. M., C. Peralta, S. Bashar, S. Taylor, J. Horrocks, and B. A. Croy. 2005. Trafficking of peripheral blood CD56(bright) cells to the decidualizing uterus--new tricks for old dogmas? J. Reprod. Immunol. 67: 21-34. https://doi.org/10.1016/j.jri.2005.03.004
  10. Kitaya, K., T. Yamaguchi, T. Yasuo, T. Okubo, and H. Honjo. 2007. Post-ovulatory rise of endometrial CD16(-) natural killer cells: in situ proliferation of residual cells or selective recruitment from circulating peripheral blood? J. Reprod. Immunol. 76: 45-53. https://doi.org/10.1016/j.jri.2007.03.010
  11. Keskin, D. B., D. S. Allan, B. Rybalov, M. M. Andzelm, J. N. Stern, H. D. Kopcow, L. A. Koopman, and J. L. Strominger. 2007. TGFbeta promotes conversion of $CD16^+$ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. U. S. A. 104: 3378-3383. https://doi.org/10.1073/pnas.0611098104
  12. Manaster, I., and O. Mandelboim. 2010. The unique properties of uterine NK cells. Am. J. Reprod. Immunol. 63: 434-444. https://doi.org/10.1111/j.1600-0897.2009.00794.x
  13. Salamonsen, L. A., and D. E. Woolley. 1999. Menstruation: induction by matrix metalloproteinases and inflammatory cells. J. Reprod. Immunol. 44: 1-27. https://doi.org/10.1016/S0165-0378(99)00002-9
  14. Salamonsen, L. A., and L. J. Lathbury. 2000. Endometrial leukocytes and menstruation. Hum. Reprod. Update 6: 16-27. https://doi.org/10.1093/humupd/6.1.16
  15. Lee, J. Y., M. Lee, and S. K. Lee. 2011. Role of endometrial immune cells in implantation. Clin. Exp. Reprod. Med. 38: 119-125. https://doi.org/10.5653/cerm.2011.38.3.119
  16. Song, J. Y., and I. S. Fraser. 1995. Effects of progestogens on human endometrium. Obstet. Gynecol. Surv. 50: 385-394. https://doi.org/10.1097/00006254-199505000-00026
  17. Salamonsen, L. A., J. Zhang, and M. Brasted. 2002. Leukocyte networks and human endometrial remodelling. J. Reprod. Immunol. 57: 95-108. https://doi.org/10.1016/S0165-0378(02)00011-6
  18. Flynn, L., B. Byrne, J. Carton, P. Kelehan, C. O'Herlihy, and C. O'Farrelly. 2000. Menstrual cycle dependent fluctuations in NK and T-lymphocyte subsets from non-pregnant human endometrium. Am. J. Reprod. Immunol. 43: 209-217. https://doi.org/10.1111/j.8755-8920.2000.430405.x
  19. Jones, R. K., J. N. Bulmer, and R. F. Searle. 1998. Phenotypic and functional studies of leukocytes in human endometrium and endometriosis. Hum. Reprod. Update 4: 702-709. https://doi.org/10.1093/humupd/4.5.702
  20. Kodama, T., T. Hara, E. Okamoto, Y. Kusunoki, and K. Ohama. 1998. Characteristic changes of large granular lymphocytes that strongly express CD56 in endometrium during the menstrual cycle and early pregnancy. Hum. Reprod. 13: 1036-1043. https://doi.org/10.1093/humrep/13.4.1036
  21. Jeziorska, M., L. A. Salamonsen, and D. E. Woolley. 1995. Mast cell and eosinophil distribution and activation in human endometrium throughout the menstrual cycle. Biol. Reprod. 53: 312-320. https://doi.org/10.1095/biolreprod53.2.312
  22. Bonatz, G., M. L. Hansmann, F. Buchholz, L. Mettler, H. J. Radzun, and K. Semm. 1992. Macrophage- and lymphocyte- subtypes in the endometrium during different phases of the ovarian cycle. Int. J. Gynaecol. Obstet. 37: 29-36. https://doi.org/10.1016/0020-7292(92)90974-N
  23. Schulke, L., F. Manconi, R. Markham, and I. S. Fraser. 2008. Endometrial dendritic cell populations during the normal menstrual cycle. Hum. Reprod. 23: 1574-1580. https://doi.org/10.1093/humrep/den030
  24. Somerset, D. A., Y. Zheng, M. D. Kilby, D. M. Sansom, and M. T. Drayson. 2004. Normal human pregnancy is associated with an elevation in the immune suppressive $CD25^+$ $CD4^+$ regulatory T-cell subset. Immunology 112: 38-43. https://doi.org/10.1111/j.1365-2567.2004.01869.x
  25. Quinn, K. H., D. Y. Lacoursiere, L. Cui, J. Bui, and M. M. Parast. 2011. The unique pathophysiology of early-onset severe preeclampsia: role of decidual T regulatory cells. J. Reprod. Immunol. 91: 76-82. https://doi.org/10.1016/j.jri.2011.05.006
  26. Tilburgs, T., D. L. Roelen, B. J. van der Mast, G. M. de Groot-Swings, C. Kleijburg, S. A. Scherjon, and F. H. Claas. 2008. Evidence for a selective migration of fetus-specific $CD4^+$ $CD25^{bright}$ regulatory T cells from the peripheral blood to the decidua in human pregnancy. J. Immunol. 180: 5737-5745. https://doi.org/10.4049/jimmunol.180.8.5737
  27. Sasaki, Y., M. Sakai, S. Miyazaki, S. Higuma, A. Shiozaki, and S. Saito. 2004. Decidual and peripheral blood $CD4^+$ $CD25^+$ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol. Hum. Reprod. 10: 347-353. https://doi.org/10.1093/molehr/gah044
  28. Mjosberg, J., G. Berg, M. C. Jenmalm, and J. Ernerudh. 2010. $FOXP3^+$ regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol. Reprod. 82: 698-705. https://doi.org/10.1095/biolreprod.109.081208
  29. Nakashima, A., M. Ito, S. Yoneda, A. Shiozaki, T. Hidaka, and S. Saito. 2010. Circulating and decidual Th17 cell levels in healthy pregnancy. Am. J. Reprod. Immunol. 63: 104-109.
  30. Lidstrom, C., L. Matthiesen, G. Berg, S. Sharma, J. Ernerudh, and C. Ekerfelt. 2003. Cytokine secretion patterns of NK cells and macrophages in early human pregnancy decidua and blood: implications for suppressor macrophages in decidua. Am. J. Reprod. Immunol. 50: 444-452. https://doi.org/10.1046/j.8755-8920.2003.00112.x
  31. Miyazaki, S., H. Tsuda, M. Sakai, S. Hori, Y. Sasaki, T. Futatani, T. Miyawaki, and S. Saito. 2003. Predominance of Th2-promoting dendritic cells in early human pregnancy decidua. J. Leukoc. Biol. 74: 514-522. https://doi.org/10.1189/jlb.1102566
  32. Mei, S., J. Tan, H. Chen, Y. Chen, and J. Zhang. 2010. Changes of $CD4^+$ $CD25^{high}$ regulatory T cells and FOXP3 expression in unexplained recurrent spontaneous abortion patients. Fertil. Steril. 94: 2244-2247. https://doi.org/10.1016/j.fertnstert.2009.11.020
  33. Galazka, K., L. Wicherek, K. Pitynski, J. Kijowski, K. Zajac, W. Bednarek, M. Dutsch-Wicherek, K. Rytlewski, J. Kalinka, A. Basta, and M. Majka. 2009. Changes in the subpopulation of $CD25^+$ $CD4^+$ and $FOXP3^+$ regulatory T cells in decidua with respect to the progression of labor at term and the lack of analogical changes in the subpopulation of suppressive B7-H4 macrophages--a preliminary report. Am. J. Reprod. Immunol. 61: 136-146. https://doi.org/10.1111/j.1600-0897.2008.00674.x
  34. Schwede, S., J. Alfer, and R. U. von. 2014. Differences in regulatory T-cell and dendritic cell pattern in decidual tissue of placenta accreta/increta cases. Placenta 35: 378-385. https://doi.org/10.1016/j.placenta.2014.03.004
  35. Lee, S. K., J. Y. Kim, S. E. Hur, C. J. Kim, B. J. Na, M. Lee, A. Gilman-Sachs, and J. Kwak-Kim. 2011. An imbalance in interleukin-17-producing T and $FOXP3^+$ regulatory T cells in women with idiopathic recurrent pregnancy loss. Hum. Reprod. 26: 2964-2971. https://doi.org/10.1093/humrep/der301
  36. Toldi, G., J. Rigo, Jr., B. Stenczer, B. Vasarhelyi, and A. Molvarec. 2011. Increased prevalence of IL-17-producing peripheral blood lymphocytes in pre-eclampsia. Am. J. Reprod. Immunol. 66: 223-229. https://doi.org/10.1111/j.1600-0897.2011.00987.x
  37. Ito, M., A. Nakashima, T. Hidaka, M. Okabe, N. D. Bac, S. Ina, S. Yoneda, A. Shiozaki, S. Sumi, K. Tsuneyama, T. Nikaido, and S. Saito. 2010. A role for IL-17 in induction of an inflammation at the fetomaternal interface in preterm labour. J. Reprod. Immunol. 84: 75-85. https://doi.org/10.1016/j.jri.2009.09.005
  38. Wang, W. J., C. F. Hao, L. Yi, G. J. Yin, S. H. Bao, L. H. Qiu, and Q. D. Lin. 2010. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J. Reprod. Immunol. 84: 164-170. https://doi.org/10.1016/j.jri.2009.12.003
  39. Lee, S. K., J. Y. Kim, M. Lee, A. Gilman-Sachs, and J. Kwak-Kim. 2012. Th17 and regulatory T cells in women with recurrent pregnancy loss. Am. J. Reprod. Immunol. 67: 311-318. https://doi.org/10.1111/j.1600-0897.2012.01116.x
  40. Chao, K. H., Y. S. Yang, H. N. Ho, S. U. Chen, H. F. Chen, H. J. Dai, S. C. Huang, and T. J. Gill, III. 1995. Decidual natural killer cytotoxicity decreased in normal pregnancy but not in anembryonic pregnancy and recurrent spontaneous abortion. Am. J. Reprod. Immunol. 34: 274-280. https://doi.org/10.1111/j.1600-0897.1995.tb00953.x
  41. Clifford, K., A. M. Flanagan, and L. Regan. 1999. Endometrial $CD56^+$ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Hum. Reprod. 14: 2727-2730. https://doi.org/10.1093/humrep/14.11.2727
  42. Tuckerman, E., S. M. Laird, A. Prakash, and T. C. Li. 2007. Prognostic value of the measurement of uterine natural killer cells in the endometrium of women with recurrent miscarriage. Hum. Reprod. 22: 2208-2213. https://doi.org/10.1093/humrep/dem141
  43. McGrath, E., E. J. Ryan, L. Lynch, L. Golden-Mason, E. Mooney, M. Eogan, C. O'Herlihy, and C. O'Farrelly. 2009. Changes in endometrial natural killer cell expression of CD94, CD158a and CD158b are associated with infertility. Am. J. Reprod. Immunol. 61: 265-276. https://doi.org/10.1111/j.1600-0897.2009.00688.x
  44. Yamamoto, T., Y. Takahashi, N. Kase, and H. Mori. 1999. Decidual natural killer cells in recurrent spontaneous abortion with normal chromosomal content. Am. J. Reprod. Immunol. 41: 337-342. https://doi.org/10.1111/j.1600-0897.1999.tb00447.x
  45. Matteo, M., G. Serviddio, F. Massenzio, G. Scillitani, L. Castellana, G. Picca, F. Sanguedolce, M. Cignarelli, E. Altomare, P. Bufo, P. Greco, and A. Liso. 2010. Reduced percentage of natural killer cells associated with impaired cytokine network in the secretory endometrium of infertile women with polycystic ovary syndrome. Fertil. Steril. 94: 2222-2227. https://doi.org/10.1016/j.fertnstert.2010.01.049
  46. Zhang, Y., A. Zhao, X. Wang, G. Shi, H. Jin, and Q. Lin. 2008. Expressions of natural cytotoxicity receptors and NKG2D on decidual natural killer cells in patients having spontaneous abortions. Fertil. Steril. 90: 1931-1937. https://doi.org/10.1016/j.fertnstert.2007.08.009
  47. Varla-Leftherioti, M., M. Spyropoulou-Vlachou, T. Keramitsoglou, M. Papadimitropoulos, C. Tsekoura, O. Graphou, C. Papadopoulou, M. Gerondi, and C. Stavropoulos-Giokas. 2005. Lack of the appropriate natural killer cell inhibitory receptors in women with spontaneous abortion. Hum. Immunol. 66: 65-71.
  48. Schonkeren, D., M. L. van der Hoorn, P. Khedoe, G. Swings, B. E. van, F. Claas, K. C. van, H. E. de, and S. Scherjon. 2011. Differential distribution and phenotype of decidual macrophages in preeclamptic versus control pregnancies. Am. J. Pathol. 178: 709-717. https://doi.org/10.1016/j.ajpath.2010.10.011
  49. Aagaard, K., J. Ma, K. M. Antony, R. Ganu, J. Petrosino, and J. Versalovic. 2014. The placenta harbors a unique microbiome. Sci. Transl. Med. 6: 237ra65. https://doi.org/10.1126/scitranslmed.3008599
  50. Park, D. W., H. J. Lee, C. W. Park, S. R. Hong, J. Kwak-Kim, and K. M. Yang. 2010. Peripheral blood NK cells reflect changes in decidual NK cells in women with recurrent miscarriages. Am. J. Reprod. Immunol. 63: 173-180. https://doi.org/10.1111/j.1600-0897.2009.00777.x
  51. Fukui, A., A. Funamizu, M. Yokota, K. Yamada, R. Nakamua, R. Fukuhara, H. Kimura, and H. Mizunuma. 2011. Uterine and circulating natural killer cells and their roles in women with recurrent pregnancy loss, implantation failure and preeclampsia. J. Reprod. Immunol. 90: 105-110. https://doi.org/10.1016/j.jri.2011.04.006
  52. Moffett, A., L. Regan, and P. Braude. 2004. Natural killer cells, miscarriage, and infertility. BMJ 329: 1283-1285. https://doi.org/10.1136/bmj.329.7477.1283

피인용 문헌

  1. Effects of Oriental Medicine Kyung-Ok-Ko on Uterine Abnormality in Hyperandrogenized Rats vol.19, pp.6, 2015, https://doi.org/10.1089/rej.2015.1787
  2. Seminal Fluid-Mediated Inflammation in Physiology and Pathology of the Female Reproductive Tract vol.2016, pp.None, 2015, https://doi.org/10.1155/2016/9707252
  3. The mouse endometrium contains epithelial, endothelial and leucocyte populations expressing the stem cell marker telomerase reverse transcriptase vol.22, pp.4, 2015, https://doi.org/10.1093/molehr/gav076
  4. Broadly neutralizing antibody specificities detected in the genital tract of HIV-1 infected women vol.30, pp.7, 2015, https://doi.org/10.1097/qad.0000000000001038
  5. Progresses in Vaginal Microflora Physiology and Implications for Bacterial Vaginosis and Candidiasis vol.12, pp.3, 2015, https://doi.org/10.2217/whe.16.5
  6. Restoration of immune and renal function in aged females by re-establishment of active ovarian function vol.29, pp.10, 2017, https://doi.org/10.1071/rd16333
  7. Characterization of the Growth of Chlamydia trachomatis in In Vitro -Generated Stratified Epithelium vol.7, pp.None, 2015, https://doi.org/10.3389/fcimb.2017.00438
  8. The Human Penis Is a Genuine Immunological Effector Site vol.8, pp.None, 2017, https://doi.org/10.3389/fimmu.2017.01732
  9. Modified Vaccinia Virus Ankara Vector Induces Specific Cellular and Humoral Responses in the Female Reproductive Tract, the Main HIV Portal of Entry vol.199, pp.5, 2017, https://doi.org/10.4049/jimmunol.1700320
  10. The human female urogenital microbiome: complexity in normality vol.1, pp.4, 2015, https://doi.org/10.1042/etls20170042
  11. Endometrial cancer evolution: new molecular-biologic types and hormonal-metabolic shifts vol.13, pp.28, 2017, https://doi.org/10.2217/fon-2017-0217
  12. Literature Review on the Role of Uterine Fibroids in Endometrial Function vol.25, pp.5, 2015, https://doi.org/10.1177/1933719117725827
  13. Estrogen Receptor-Alpha (ESR1) Governs the Lower Female Reproductive Tract Vulnerability to Candida albicans vol.9, pp.None, 2015, https://doi.org/10.3389/fimmu.2018.01033
  14. Niches for the Long-Term Maintenance of Tissue-Resident Memory T Cells vol.9, pp.None, 2015, https://doi.org/10.3389/fimmu.2018.01214
  15. The Vaginal Microenvironment: The Physiologic Role of Lactobacilli vol.5, pp.None, 2015, https://doi.org/10.3389/fmed.2018.00181
  16. Autoantibodies against HSF1 and CCDC155 as Biomarkers of Early-Stage, High-Grade Serous Ovarian Cancer vol.27, pp.2, 2015, https://doi.org/10.1158/1055-9965.epi-17-0752
  17. Tissue distribution of some immune cells in bovine reproductive tract during follicular and luteal phase vol.81, pp.3, 2018, https://doi.org/10.1002/jemt.22983
  18. Immune Cells at the Fetomaternal Interface: How the Microenvironment Modulates Immune Cells To Foster Fetal Development vol.201, pp.2, 2018, https://doi.org/10.4049/jimmunol.1800058
  19. Implications of uterine NK cells and regulatory T cells in the endometrium of infertile women vol.79, pp.9, 2018, https://doi.org/10.1016/j.humimm.2018.07.003
  20. The relationship between sex hormones, the vaginal microbiome and immunity in HIV-1 susceptibility in women vol.11, pp.9, 2015, https://doi.org/10.1242/dmm.035147
  21. Pre‐ and post‐puberty expression of genes and proteins in the uterus of Bos indicus heifers: the luteal phase effect post‐puberty vol.49, pp.6, 2015, https://doi.org/10.1111/age.12721
  22. Trichomonas vaginalis Induces NLRP3 Inflammasome Activation and Pyroptotic Cell Death in Human Macrophages vol.11, pp.1, 2015, https://doi.org/10.1159/000493585
  23. Does the endometrial cavity have a molecular microbial signature? vol.9, pp.None, 2019, https://doi.org/10.1038/s41598-019-46173-0
  24. Interplay among Vaginal Microbiome, Immune Response and Sexually Transmitted Viral Infections vol.20, pp.2, 2015, https://doi.org/10.3390/ijms20020266
  25. Immunity in the Cervix: Interphase between Immune and Cervical Epithelial Cells vol.2019, pp.None, 2015, https://doi.org/10.1155/2019/7693183
  26. Surfactant Protein D Reverses the Gene Signature of Transepithelial HIV-1 Passage and Restricts the Viral Transfer Across the Vaginal Barrier vol.10, pp.None, 2015, https://doi.org/10.3389/fimmu.2019.00264
  27. Uterine Immunity and Microbiota: A Shifting Paradigm vol.10, pp.None, 2015, https://doi.org/10.3389/fimmu.2019.02387
  28. Type I IFNs in the female reproductive tract: The first line of defense in an ever‐changing battleground vol.105, pp.2, 2015, https://doi.org/10.1002/jlb.mr0318-122rr
  29. Pregnancy-Associated Alterations of Peripheral Blood Immune Cell Numbers in Domestic Sows Are Modified by Social Rank vol.9, pp.3, 2019, https://doi.org/10.3390/ani9030112
  30. Uterine polyps, adenomyosis, leiomyomas, and endometrial receptivity vol.111, pp.4, 2015, https://doi.org/10.1016/j.fertnstert.2019.02.008
  31. Review: Chronic endometritis and its effect on reproduction vol.45, pp.5, 2015, https://doi.org/10.1111/jog.13937
  32. The biological mechanisms regulating sperm selection by the ovine cervix vol.158, pp.1, 2019, https://doi.org/10.1530/rep-18-0595
  33. The biological mechanisms regulating sperm selection by the ovine cervix vol.158, pp.1, 2019, https://doi.org/10.1530/rep-18-0595
  34. NK and trophoblast cells interaction: cytotoxic activity on recurrent pregnancy loss vol.35, pp.suppl1, 2019, https://doi.org/10.1080/09513590.2019.1632084
  35. Mechanisms of sexually transmitted infection‐induced inflammation in women: implications forHIVrisk vol.22, pp.suppl6, 2015, https://doi.org/10.1002/jia2.25346
  36. Innate Immune Cells and Toll-like Receptor-Dependent Responses at the Maternal-Fetal Interface vol.20, pp.15, 2019, https://doi.org/10.3390/ijms20153654
  37. The female reproductive tract contains multiple innate sialic acid-binding immunoglobulin-like lectins (Siglecs) that facilitate sperm survival vol.294, pp.31, 2015, https://doi.org/10.1074/jbc.ra119.008729
  38. The endometrial immune environment of women with endometriosis vol.25, pp.5, 2015, https://doi.org/10.1093/humupd/dmz018
  39. Role of Macrophages in Pregnancy and Related Complications vol.67, pp.5, 2015, https://doi.org/10.1007/s00005-019-00552-7
  40. Endometrial Immune Dysfunction in Recurrent Pregnancy Loss vol.20, pp.21, 2015, https://doi.org/10.3390/ijms20215332
  41. IL-36γ Is a Key Regulator of Neutrophil Infiltration in the Vaginal Microenvironment and Limits Neuroinvasion in Genital HSV-2 Infection vol.203, pp.10, 2015, https://doi.org/10.4049/jimmunol.1900280
  42. Comparative transcriptome analysis of the human endocervix and ectocervix during the proliferative and secretory phases of the menstrual cycle vol.9, pp.1, 2015, https://doi.org/10.1038/s41598-019-49647-3
  43. Melatonin Promotes Uterine and Placental Health: Potential Molecular Mechanisms vol.21, pp.1, 2015, https://doi.org/10.3390/ijms21010300
  44. Uterine Fluid Proteins for Minimally Invasive Assessment of Endometrial Receptivity vol.105, pp.1, 2020, https://doi.org/10.1210/clinem/dgz019
  45. Activation of Toll-Like Receptors Differentially Modulates Inflammation in the Human Reproductive Tract: Preliminary Findings vol.11, pp.None, 2015, https://doi.org/10.3389/fimmu.2020.01655
  46. Killer Immunoglobulin-Like Receptor 2DL4 (CD158d) Regulates Human Mast Cells both Positively and Negatively: Possible Roles in Pregnancy and Cancer Metastasis vol.21, pp.3, 2015, https://doi.org/10.3390/ijms21030954
  47. The vaginal microbiome in uterine transplantation vol.127, pp.2, 2015, https://doi.org/10.1111/1471-0528.15881
  48. Viruses in the reproductive tract: On their way to the germ line? vol.286, pp.None, 2020, https://doi.org/10.1016/j.virusres.2020.198101
  49. Pregnancy-specific transcriptional changes upon endotoxin exposure in mice vol.48, pp.7, 2015, https://doi.org/10.1515/jpm-2020-0159
  50. Changes in subsets of immunocytes in endometrial hyperplasia vol.84, pp.4, 2020, https://doi.org/10.1111/aji.13295
  51. Distribution of estrogen receptor in the rabbit cervix during pregnancy with special reference to stromal elements: an immunohistochemical study vol.10, pp.1, 2015, https://doi.org/10.1038/s41598-020-70323-4
  52. Ex vivo rectal explant model reveals potential opposing roles of Natural Killer cells and Marginal Zone-like B cells in HIV-1 infection vol.10, pp.1, 2015, https://doi.org/10.1038/s41598-020-76976-5
  53. Human Tissue-Resident Memory T Cells in the Maternal–Fetal Interface. Lost Soldiers or Special Forces? vol.9, pp.12, 2015, https://doi.org/10.3390/cells9122699
  54. Immune Tolerance of the Human Decidua vol.10, pp.2, 2015, https://doi.org/10.3390/jcm10020351
  55. Neutrophil granulocytes: participation in homeostatic and reparative processes. Part II vol.11, pp.1, 2015, https://doi.org/10.15789/2220-7619-ngp-1258
  56. Understanding the Impact of Uterine Fibroids on Human Endometrium Function vol.9, pp.None, 2015, https://doi.org/10.3389/fcell.2021.633180
  57. Immunomodulatory properties of extracellular vesicles in the dialogue between placental and immune cells vol.85, pp.2, 2021, https://doi.org/10.1111/aji.13383
  58. The contribution of chronic endometritis to reproductive system disorders in patients with repeated implantation failures vol.23, pp.1, 2015, https://doi.org/10.26442/20795696.2021.1.200671
  59. TLR4-Associated IRF-7 and NFκB Signaling Act as a Molecular Link Between Androgen and Metformin Activities and Cytokine Synthesis in the PCOS Endometrium vol.106, pp.4, 2015, https://doi.org/10.1210/clinem/dgaa951
  60. Angiogenic Properties of NK Cells in Cancer and Other Angiogenesis-Dependent Diseases vol.10, pp.7, 2015, https://doi.org/10.3390/cells10071621
  61. Maternal Neutrophil Depletion Fails to Avert Systemic Lipopolysaccharide-Induced Early Pregnancy Defects in Mice vol.22, pp.15, 2021, https://doi.org/10.3390/ijms22157932
  62. Mechanobiology of the female reproductive system vol.20, pp.4, 2015, https://doi.org/10.1002/rmb2.12404
  63. Uterine natural killer cell biology and role in early pregnancy establishment and outcomes vol.2, pp.4, 2015, https://doi.org/10.1016/j.xfnr.2021.06.002
  64. Vaginal delivery of vaccines vol.178, pp.None, 2015, https://doi.org/10.1016/j.addr.2021.113956
  65. Building a stem cell-based primate uterus vol.4, pp.1, 2021, https://doi.org/10.1038/s42003-021-02233-8
  66. Inter‐species lateral gene transfer focused on the Chlamydia plasticity zone identifies loci associated with immediate cytotoxicity and inclusion stability vol.116, pp.6, 2021, https://doi.org/10.1111/mmi.14832