“What do we know about regulatory T cells and endometriosis? A systematic review”

Journal of Reproductive Immunology

Volumn 120, Issue , 2017, Pages 48-55

  de Barros, Isabela Bottura Leite ^a   Malvezzi, Helena ^a   Gueuvoghlanian Silva, Bárbara Yasmin ^a   Piccinato, Carla Azevedo ^a   Rizzo, Luiz Vicente ^a   Podgaec, Sergio ^a  

^a HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

Author keywords

Endometriosis; Immune response; Regulatory T cell

Indexed keywords

TRANSCRIPTION FACTOR FOXP3;

CD4+ CD25+ T LYMPHOCYTE; EMBASE; ENDOMETRIOSIS; FEMALE; HUMAN; IMMUNE RESPONSE; MEDLINE; NONHUMAN; PERITONEAL FLUID; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SYSTEMATIC REVIEW; ANIMAL; CHORISTOMA; ENDOMETRIUM; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE COUNT; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CHORISTOMA; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMANS; IMMUNOMODULATION; LYMPHOCYTE COUNT; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 85018340932     PISSN: 01650378     EISSN: 18727603     Source Type: Journal    
DOI: 10.1016/j.jri.2017.04.003     Document Type: Review

References (65)

1. 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.
2. Akoum, A., Lemay, A., Maheux, R., Estradiol and interleukin-1beta exert a synergistic stimulatory effect on the expression of the chemokine regulated upon activation, normal T cell expressed, and secreted in endometriotic cells. J. Clin. Endocrinol. Metab. 87 (2002), 5785–5792.
3. American Society for Reproductive Medicine, Revised american society for reproductive medicine classification of endometriosis: 1996. Fertil. Steril. 67 (1997), 817–821.
4. Antsiferova, Y.S., Sotnikova, N.Y., Posiseeva, L.V., Shor, A.L., Changes in the T-helper cytokine profile and in lymphocyte activation at the systemic and local levels in women with endometriosis. Fertil. Steril. 84 (2005), 1705–1711.
5. Bacci, M., Capobianco, A., Monno, A., Cottone, L., Di Puppo, F., Camisa, B., et al. Macrophages are alternatively activated in patients with endometriosis and required for growth and vascularization of lesions in a mouse model of disease. Am. J. Pathol. 175 (2009), 547–556.
6. Basta, P., Koper, K., Kazmierczak, W., Wisniewski, M., Makarewicz, A., Dutsch-Wicherek, M., et al. The biological role of Treg cells in ectopic endometrium homeostasis. Histol. Histopathol. 29 (2014), 1217–1233.
7. + regulatory T cells in ectopic endometrium and ectopic decidua. Reprod. Biol. Endocrinol., 8, 2010, 116.
8. Bellelis, P., Barbeiro, D.F., Rizzo, L.V., Baracat, E.C., Abrao, M.S., Podgaec, S., Transcriptional changes in the expression of chemokines related to natural killer and T-regulatory cells in patients with deep infiltrative endometriosis. Fertil. Steril. 99 (2013), 1987–1993.
9. Berbic, M., Fraser, I.S., Regulatory T cells and other leukocytes in the pathogenesis of endometriosis. J. Reprod. Immunol. 88 (2011), 149–155.
10. + regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition. Hum. Reprod. 25 (2010), 900–907.
11. Bianco, B., Andre, G.M., Vilarino, F.L., Peluso, C., Mafra, F.A., Christofolini, D.M., et al. The possible role of genetic variants in autoimmune-related genes in the development of endometriosis. Hum. Immunol. 73 (2012), 306–315.
12. Braundmeier, A., Jackson, K., Hastings, J., Koehler, J., Nowak, R., Fazleabas, A., Induction of endometriosis alters the peripheral and endometrial regulatory T cell population in the non-human primate. Hum. Reprod. 27 (2012), 1712–1722.
13. + regulatory T cells. Dis. Model. Mech. 2 (2009), 593–603.
14. Burney, R.O., Giudice, L.C., Pathogenesis and pathophysiology of endometriosis. Fertil Steril. 98 (2012), 511–519.
15. Chaouat, G., Inflammation, NK cells and implantation: friend and foe (the good, the bad and the ugly?.): Replacing placental viviparity in an evolutionary perspective. J. Reprod. Immunol. 97 (2013), 2–13.
16. Chen, S., Zhang, J., Huang, C., Lu, W., Liang, Y., Wan, X., Expression of the T regulatory cell transcription factor Foxp3 in peri-implantation phase endometrium in infertile women with endometriosis. Reprod. Biol. Endocrinol., 10, 2012, 34.
17. Clark, D.A., The importance of being a regulatory T cell in pregnancy. J. Reprod. Immunol. 116 (2016), 60–69.
18. Coleman, K.D., Ghosh, M., Crist, S.G., Wright, J.A., Rossoll, R.M., Wira, C.R., et al. Modulation of hepatocyte growth factor secretion in human female reproductive tract stromal fibroblasts by poly (i:C) and estradiol. Am. J. Reprod. Immunol. 67 (2012), 44–53.
19. Corthay, A., How do regulatory T cells work?. Scand. J. Immunol. 70 (2009), 326–336.
20. Cunningham, D.S., Hansen, K.A., Coddington, C.C., Changes in T-cell regulation of responses to self antigens in women with pelvic endometriosis. Fertil. Steril. 58 (1992), 114–119.
21. Dmowski, W.P., Steele, R.W., Baker, G.F., Deficient cellular immunity in endometriosis. Am. J. Obstet. Gynecol. 141 (1981), 377–383.
22. Fazleabas, A.T., Braundmeier, A., Parkin, K., Endometriosis-induced changes in regulatory T cells – insights towards developing permanent contraception. Contraception 92 (2015), 116–119.
23. Geginat, J., Paroni, M., Maglie, S., Alfen, J.S., Kastirr, I., Gruarin, P., et al. Plasticity of human CD4T cell subsets. Front. Immunol., 5, 2014, 630.
24. Ginsburg, E.S., Xiao, L., Gargiulo, A.R., Kung, F.T., Politch, J.A., Schust, D.J., et al. T-helper 2 and 3 type immunity to trophoblast in successful in vitro fertilization-embryo transfer. Fertil. Steril. 83 (2005), 1659–1664.
25. Gleicher, N., Dmowski, W.P., Siegel, I., Liu, T.L., Friberg, J., Radwanska, E., et al. Lymphocyte subsets in endometriosis. Obstet. Gynecol. 63 (1984), 463–466.
26. Gogacz, M., Winkler, I., Bojarska-Junak, A., Tabarkiewicz, J., Semczuk, A., Rechberger, T., et al. T regulatory lymphocytes in patients with endometriosis. Mol. Med. Rep. 10 (2014), 1072–1076.
27. Halme, J., Hammond, M.G., Hulka, J.F., Raj, S.G., Talbert, L.M., Retrograde menstruation in healthy women and in patients with endometriosis. Obstet. Gynecol. 64 (1984), 151–154.
28. Hever, A., Roth, R.B., Hevezi, P., Marin, M.E., Acosta, J.A., Acosta, H., et al. Human endometriosis is associated with plasma cells and overexpression of B lymphocyte stimulator. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 12451–12456.
29. Hirata, T., Osuga, Y., Hamasaki, K., Yoshino, O., Ito, M., Hasegawa, A., et al. Interleukin (IL)-17a stimulates IL-8 secretion, cyclooxygensase-2 expression, and cell proliferation of endometriotic stromal cells. Endocrinology 149 (2008), 1260–1267.
30. + lymphocyte subpopulation are decreased in women with stage iii-iv endometriosis. Hum. Reprod. 10 (1995), 2671–2675.
31. Illanes, S.E., Maisey, K., Sandoval, M., Reyes, F.E., Figueroa-Gaete, C., Perez-Sepulveda, A., et al. Fas ligand(+) fallopian tube epithelium induces apoptosis in both fas receptor(+) T lymphocytes and endometrial cells. Fertil. Steril. 100 (2013), 550–560 e553.
32. Jasper, M.J., Tremellen, K.P., Robertson, S.A., Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol. Hum. Reprod. 12 (2006), 301–308.
33. Josefowicz, S.Z., Lu, L.F., Rudensky, A.Y., Regulatory T cells: Mechanisms of differentiation and function. Annu. Rev. Immunol. 30 (2012), 531–564.
34. Khoufache, K., Michaud, N., Harir, N., Kibangou Bondza, P., Akoum, A., Anomalies in the inflammatory response in endometriosis and possible consequences: a review. Minerva Endocrinol. 37 (2012), 75–92.
35. Kisielewski, R., Tolwinska, A., Mazurek, A., Laudanski, P., Inflammation and ovarian cancer: current views. Ginekol. Pol. 84 (2013), 293–297.
36. Kralickova, M., Vetvicka, V., Immunological aspects of endometriosis: a review. Ann. Transl. Med., 3, 2015, 153.
37. Lambropoulou, M., Tamiolakis, D., Venizelos, J., Liberis, V., Galazios, G., Tsikouras, P., et al. Imbalance of mononuclear cell infiltrates in the placental tissue from foetuses after spontaneous abortion versus therapeutic termination from 8th to 12th weeks of gestational age. Clin. Exp. Med. 6 (2006), 171–176.
38. Lebovic, D.I., Chao, V.A., Martini, J.F., Taylor, R.N., IL-1beta induction of RANTES (regulated upon activation, normal T cell expressed and secreted) chemokine gene expression in endometriotic stromal cells depends on a nuclear factor-κB site in the proximal promoter. J. Clin. Endocrinol. Metab. 86 (2001), 4759–4764.
39. + regulatory T cell differentiation mediated by endometrial stromal cell-derived teck promotes the growth and invasion of endometriotic lesions. Cell Death Dis., 5, 2014, e1436.
40. Li, P., Liu, C., Yu, Z., Wu, M., New insights into regulatory T cells: exosome- and non-coding rmediated regulation of homeostasis and resident Treg cells. Front. Immunol., 7, 2016, 574.
41. + T reg cells. J. Exp. Med. 203 (2006), 1701–1711.
42. Nava-Loya, G., Hernandez-Guerrero, C., Perez-Ocharan, M., Mojarra-Estrada, J.M., Gonzalez-Morales, M.E., Bustos-Lopez, H., et al. Peritoneal immune response in endometriosis. Ginecol. Obstet. Mex. 64 (1996), 147–153.
43. Oda, J.M., Hirata, B.K., Guembarovski, R.L., Watanabe, M.A., Genetic polymorphism in Foxp3 gene: imbalance in regulatory T-cell role and development of human diseases. J. Genet. 92 (2013), 163–171.
44. Ohkura, N., Kitagawa, Y., Sakaguchi, S., Development and maintenance of regulatory T cells. Immunity 38 (2013), 414–423.
45. + regulatory T cells in peripheral blood and peritoneal fluid of patients with endometriosis. Hum. Reprod. 28 (2013), 119–124.
46. Olovsson, M., Immunological aspects of endometriosis: an update. Am. J. Reprod. Immunol. 66:Suppl 1 (2011), 101–104.
47. Parkin, K.L., Fazleabas, A.T., Uterine leukocyte function and dysfunction: a hypothesis on the impact of endometriosis. Am. J. Reprod. Immunol. 75 (2016), 411–417.
48. Patel, B.G., Lessey, B.A., Clinical assessment and management of the endometrium in recurrent early pregnancy loss. Semin. Reprod. Med. 29 (2011), 491–506.
49. Podgaec, S., Barbeiro, D.F., Gueuvoghlanian-Silva, B.Y., Bellelis, P., Abrao, M.S., Baracat, E.C., Foxp3 expression in deep rectosigmoid endometriosis lesions and its association with chronic pelvic pain. J. Reprod. Immunol. 104-105 (2014), 96–99.
50. + cells increased in the peritoneal fluid of patients with endometriosis. Am. J. Reprod. Immunol. 68 (2012), 301–308.
51. Pradeu, T., Cooper, E.L., The danger theory: 20 years later. Front. Immunol., 3, 2012, 287.
52. + regulatory T-cell response?. Dis. Model. Mech. 4 (2011), 139–140.
53. Saito, S., Nakashima, A., Ito, M., Shima, T., Clinical implication of recent advances in our understanding of IL-17 and reproductive immunology. Expert Rev. Clin. Immunol. 7 (2011), 649–657.
54. + regulatory T cells in the human immune system. Nat. Rev. Immunol. 10 (2010), 490–500.
55. Sampson, J., Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity. Am. J. Obstet. Gynecol. 14 (1927), 422–469.
56. Schulke, L., Berbic, M., Manconi, F., Tokushige, N., Markham, R., Fraser, I.S., Dendritic cell populations in the eutopic and ectopic endometrium of women with endometriosis. Hum. Reprod. 24 (2009), 1695–1703.
57. Slabe, N., Meden-Vrtovec, H., Verdenik, I., Kosir-Pogacnik, R., Ihan, A., Cytotoxic T-cells in peripheral blood in women with endometriosis. Geburtshilfe Frauenheilkd. 73 (2013), 1042–1048.
58. Somigliana, E., Vigano, P., Gaffuri, B., Candiani, M., Busacca, M., Di Blasio, A.M., et al. Modulation of NK cell lytic function by endometrial secretory factors: Potential role in endometriosis. Am. J. Reprod. Immunol. 36 (1996), 295–300.
59. Szyllo, K., Tchorzewski, H., Banasik, M., Glowacka, E., Lewkowicz, P., Kamer-Bartosinska, A., The involvement of T lymphocytes in the pathogenesis of endometriotic tissues overgrowth in women with endometriosis. Mediators Inflamm. 12 (2003), 131–138.
60. + T lymphocyte in lesions and peripheral blood in endometriosis. Am. J. Reprod. Immunol. 74 (2015), 480–486.
61. + cells and prolongation of survival of fully allogeneic murine cardiac grafts by danazol. Transplant. Proc. 44 (2012), 1067–1069.
62. + cells in mice. Transpl. Int. 25 (2012), 357–365.
63. Vercellini, P., Vigano, P., Somigliana, E., Fedele, L., Endometriosis: pathogenesis and treatment. Nat. Rev. Endocrinol. 10 (2014), 261–275.
64. Vigano, P., Di Blasio, A.M., Busacca, M., Vignali, M., Immunosuppressive effect of danazol on lymphocyte-mediated cytotoxicity toward human endometrial stromal cells. Gynecol. Endocrinol. 8 (1994), 13–19.
65. + regulatory T cells reverses the increase in abortion rate caused by interleukin 17 in the CBA/JxBALB/c mouse model. Hum. Reprod. 29 (2014), 946–952.