Menopausal status influences the expression of programmed death (PD)-1 and its ligand PD-L1 on immune cells from the human female reproductive tract

American Journal of Reproductive Immunology

Volumn 76, Issue 2, 2016, Pages 118-125

  Shen, Zheng ^a   Rodriguez Garcia, Marta ^a   Patel, Mickey V ^a   Barr, Fiona D ^a   Wira, Charles R ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

CD4+ T cells; CD8+ T cells; dendritic cells; PD 1 PD L1, post menopausal; sex hormones

Indexed keywords

CD163 ANTIGEN; ESTRADIOL; GLYCOPROTEIN P 15095; PROGESTERONE; PROGRAMMED DEATH 1 LIGAND 1;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; DENDRITIC CELL; ENDOMETRIUM; FEMALE; FEMALE GENITAL SYSTEM; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MENOPAUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; UTERINE ENDOCERVIX;

EID: 84978196527     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12532     Document Type: Article

References (32)

1. Wira CR, Fahey JV, Sentman CL, Pioli PA, Shen L. Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol Rev. 2005;206:306–335.
2. Wira CR, Rodriguez-Garcia M, Patel MV. The role of sex hormones in immune protection of the female reproductive tract. Nat Rev Immunol. 2015;15:217–230.
3. Givan AL, White HD, Stern JE, et al. Flow cytometric analysis of leukocytes in the human female reproductive tract: comparison of Fallopian tube, uterus, cervix, and vagina. Am J Reprod Immunol. 1997;38:350–359.
4. White HD, Yeaman GR, Givan AL, Wira CR. Mucosal immunity in the human female reproductive tract: cytotoxic T lymphocyte function in the cervix and vagina of premenopausal and postmenopausal women. Am J Reprod Immunol. 1997;37:30–38.
5. Yeaman GR, Collins JE, Fanger MW, Wira CR, Lydyard PM. CD8+ T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking. Immunology. 2001;102:434–440.
6. Pioli PA, Weaver LK, Schaefer TM, Wright JA, Wira CR, Guyre PM. Lipopolysaccharide-induced IL-1 beta production by human uterine macrophages up-regulates uterine epithelial cell expression of human beta-defensin 2. J Immunol. 2006;176:6647–6655.
7. Mselle TF, Meadows SK, Eriksson M, et al. Unique characteristics of NK cells throughout the human female reproductive tract. Clin Immunol. 2007;124:69–76.
8. Kalkunte S, Chichester CO, Gotsch F, Sentman CL, Romero R, Sharma S. Evolution of non-cytotoxic uterine natural killer cells. Am J Reprod Immunol. 2008;59:425–432.
9. Shanmugasundaram U, Critchfield JW, Pannell J, et al. Phenotype and functionality of CD4+ and CD8+ T cells in the upper reproductive tract of healthy premenopausal women. Am J Reprod Immunol. 2014;71:95–108.
10. Rodriguez-Garcia M, Barr FD, Crist SG, Fahey JV, Wira CR. Phenotype and susceptibility to HIV infection of CD4+ Th17 cells in the human female reproductive tract. Mucosal Immunol. 2014;7:1375–1385.
11. White HD, Crassi KM, Givan AL, et al. CD3+ CD8+ CTL activity within the human female reproductive tract: influence of stage of the menstrual cycle and menopause. J Immunol. 1997;158:3017–3027.
12. Mselle TF, Howell AL, Ghosh M, Wira CR, Sentman CL. Human uterine natural killer cells but not blood natural killer cells inhibit human immunodeficiency virus type 1 infection by secretion of CXCL12. J Virol. 2009;83:11188–11195.
13. McKinnon LR, Nyanga B, Chege D, et al. Characterization of a human cervical CD4+ T cell subset coexpressing multiple markers of HIV susceptibility. J Immunol. 2011;187:6032–6042.
14. Keir ME, Francisco LM, Sharpe AH. PD-1 and its ligands in T-cell immunity. Curr Opin Immunol. 2007;19:309–314.
15. Jin HT, Ahmed R, Okazaki T. Role of PD-1 in regulating T-cell immunity. Curr Top Microbiol Immunol. 2011;350:17–37.
16. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677–704.
17. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010;236:219–242.
18. Zhang YH, Tian M, Tang MX, Liu ZZ, Liao AH. Recent Insight into the Role of the PD-1/PD-L1 Pathway in Feto-Maternal Tolerance and Pregnancy. Am J Reprod Immunol. 2015;74:201–208.
19. Enninga EA, Holtan SG, Creedon DJ, et al. Immunomodulatory effects of sex hormones: requirements for pregnancy and relevance in melanoma. Mayo Clin Proc. 2014;89:520–535.
20. Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol. 2004;4:336–347.
21. Wang S, Chen L. T lymphocyte co-signaling pathways of the B7-CD28 family. Cell Mol Immunol. 2004;1:37–42.
22. Greenwald RJ, Freeman GJ, Sharpe AH. The B7 family revisited. Annu Rev Immunol. 2005;23:515–548.
23. Kuipers H, Muskens F, Willart M, et al. Contribution of the PD-1 ligands/PD-1 signaling pathway to dendritic cell-mediated CD4+ T cell activation. Eur J Immunol. 2006;36:2472–2482.
24. McNatty KP, Baird DT, Bolton A, Chambers P, Corker CS, McLean H. Concentration of oestrogens and androgens in human ovarian venous plasma and follicular fluid throughout the menstrual cycle. J Endocrinol. 1976;71:77–85.
25. Omwandho CO, Konrad L, Halis G, Oehmke F, Tinneberg HR. Role of TGF-betas in normal human endometrium and endometriosis. Hum Reprod. 2010;25:101–109.
26. Thaxton JE, Sharma S. Interleukin-10: a multi-faceted agent of pregnancy. Am J Reprod Immunol. 2010;63:482–491.
27. Rodriguez-Garcia M, Porichis F, de Jong OG, et al. Expression of PD-L1 and PD-L2 on human macrophages is up-regulated by HIV-1 and differentially modulated by IL-10. J Leukoc Biol. 2011;89:507–515.
28. Taglauer ES, Yankee TM, Petroff MG. Maternal PD-1 regulates accumulation of fetal antigen-specific CD8+ T cells in pregnancy. J Reprod Immunol. 2009;80:12–21.
29. Fankhauser SC, Starnbach MN. PD-L1 limits the mucosal CD8+ T cell response to Chlamydia trachomatis. J Immunol. 2014;192:1079–1090.
30. Fujiwara H, Maeda Y, Kobayashi K, et al. Programmed death-1 pathway in host tissues ameliorates Th17/Th1-mediated experimental chronic graft-versus-host disease. J Immunol. 2014;193:2565–2573.
31. D'Addio F, Riella LV, Mfarrej BG, et al. The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J Immunol. 2011;187:4530–4541.
32. Park HJ, Park JS, Jeong YH, et al. PD-1 upregulated on regulatory T cells during chronic virus infection enhances the suppression of CD8+ T cell immune response via the interaction with PD-L1 expressed on CD8+ T cells. J Immunol. 2015;194:5801–5811.