Increased prevalence of sexually transmitted viral infections in women: The role of female sex hormones in regulating susceptibility and immune responses

Journal of Reproductive Immunology

Volumn 88, Issue 2, 2011, Pages 204-209

  Kaushic, Charu ^a   Roth, Kristy L ^a   Anipindi, Varun ^a   Xiu, Fangming ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Female genital tract; Mucosal immune responses; Sex hormones; Sexually transmitted infections; Susceptibility

Indexed keywords

ALPHA INTERFERON; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; ESTRADIOL; ESTROGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MEDROXYPROGESTERONE; ORAL CONTRACEPTIVE AGENT; PROGESTERONE; SEX HORMONE; TRANSFORMING GROWTH FACTOR BETA; VASCULAR CELL ADHESION MOLECULE 1;

ADAPTIVE IMMUNITY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CANDIDIASIS; CELLULAR IMMUNITY; CHLAMYDIASIS; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; CYTOTOXIC T LYMPHOCYTE; DISEASE COURSE; ESTROGEN ACTIVITY; FEMALE GENITAL SYSTEM; GONORRHEA; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HORMONAL CONTRACEPTION; HORMONAL REGULATION; HORMONE ACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOREGULATION; INFECTION RISK; INFECTION SENSITIVITY; INNATE IMMUNITY; MENSTRUAL CYCLE; MICROENVIRONMENT; MUCOSAL IMMUNITY; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; SEX DIFFERENCE; SEXUALLY TRANSMITTED DISEASE; SIDE EFFECT; VIRUS INFECTION;

ANIMALS; DISEASE SUSCEPTIBILITY; FEMALE; GENITALIA, FEMALE; GONADAL STEROID HORMONES; HUMANS; PREVALENCE; SEX FACTORS; SEXUALLY TRANSMITTED DISEASES; VIRUS DISEASES;

EID: 79952695920     PISSN: 01650378     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jri.2010.12.004     Document Type: Article

References (77)

1. Amory J.H., et al. Increased tumor necrosis factor-alpha in whole blood during the luteal phase of ovulatory cycles. J. Reprod. Med. 2004, 49:678-682.
2. Arici A., et al. Regulation of monocyte chemotactic protein-1 expression in human endometrial stromal cells by estrogen and progesterone. Biol. Reprod. 1999, 61:85-90.
3. Arruvito L., et al. Expansion of CD4+CD25+and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J. Immunol. 2007, 178:2572-2578.
4. Attanasio R., et al. Immunomodulatory effects of estrogen and progesterone replacement in a nonhuman primate model. J. Clin. Immunol. 2002, 22:263-269.
5. Baeten J.M., et al. Hormonal contraceptive use, herpes simplex virus infection, and risk of HIV-1 acquisition among Kenyan women. AIDS 2007, 21:1771-1777.
6. Beagley K.W., Gockel C.M. Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol. Med. Microbiol. 2003, 38:13-22.
7. Bhavanam S., et al. Systemic immunization under the effect of estradiol leads to better protection against genital HSV-2 challenge compared to progesterone. Vaccine 2008, 26:6165-6172.
8. Borel I.M., et al. Modulation of the immune response by progesterone-induced lymphocyte factors. Scand. J. Immunol. 1999, 49:244-250.
9. Brabin L. Interactions of the female hormonal environment, susceptibility to viral infections, and disease progression. AIDS Patient Care STDS 2002, 16:211-221.
10. Buchbinder S.P., et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the step study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008, 372:1881-1893.
11. Center for Disease Control and Prevention, C., 2009. Trends in Reportable Sexually Transmitted Diseases in the United States, 2007. Available at: http://www.cdc.gov/std/stats07.
12. Cherpes T.L., et al. Medroxyprogesterone acetate inhibits CD8+ T cell viral-specific effector function and induces herpes simplex virus type 1 reactivation. J. Immunol. 2008, 181:969-975.
13. Corey L., et al. Recombinant glycoprotein vaccine for the prevention of genital HSV-2 infection: two randomized controlled trials. Chiron HSV vaccine study group. JAMA 1999, 282:331-340.
14. Enomoto L.M., et al. Ex vivo effect of estrogen and progesterone compared with dexamethasone on cell-mediated immunity of HIV-infected and uninfected subjects. J. Acquir. Immune Defic. Syndr. 2007, 45:137-143.
15. Fauci A.S., et al. HIV vaccine research: the way forward. Science 2008, 321:530-532.
16. Gillgrass A., et al. Estradiol limits viral replication following intravaginal immunization leading to diminished mucosal IgG response and non-sterile protection against genital herpes challenge. Am. J. Reprod. Immunol. 2010, 63:299-309.
17. Gillgrass A.E., et al. Prolonged exposure to progesterone prevents induction of protective mucosal responses following intravaginal immunization with attenuated herpes simplex virus type 2. J. Virol. 2003, 77:9845-9851.
18. Gillgrass A.E., et al. Estradiol regulates susceptibility following primary exposure to genital herpes simplex virus type 2, while progesterone induces inflammation. J. Virol. 2005, 79:3107-3116.
19. Gillgrass A.E., et al. Protection against genital herpes infection in mice immunized under different hormonal conditions correlates with induction of vagina-associated lymphoid tissue. J. Virol. 2005, 79:3117-3126.
20. Gomez F., et al. Treatment with megestrol acetate improves human immunodeficiency virus-associated immune thrombocytopenia. Clin. Diagn. Lab. Immunol. 2002, 9:583-587.
21. Hild-Petito S., et al. Effects of two progestin-only contraceptives, depo-provera and norplant - II, on the vaginal epithelium of rhesus monkeys. AIDS Res. Hum. Retroviruses 1998, 14(Suppl. 1):S125-S130.
22. Hladik F., Mcelrath M.J. Setting the stage: host invasion by HIV. Nat. Rev. Immunol. 2008, 8:447-457.
23. Hughes G.C., et al. Cutting edge: progesterone regulates IFN-alpha production by plasmacytoid dendritic cells. J. Immunol. 2008, 180:2029-2033.
24. Ildgruben A.K., et al. Influence of hormonal contraceptives on the immune cells and thickness of human vaginal epithelium. Obstet. Gynecol. 2003, 102:571-582.
25. Inoue T., et al. Progesterone stimulates the induction of human endometrial CD56+ lymphocytes in an in vitro culture system. J. Clin. Endocrinol. Metab. 1996, 81:1502-1507.
26. Joura E.A., et al. Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet 2007, 369:1693-1702.
27. Kaushic C., et al. Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J. Virol. 2003, 77:4558-4565.
28. Kaushic C., et al. HIV infection in the female genital tract: discrete influence of the local mucosal microenvironment. Am. J. Reprod. Immunol. 2010, 63:566-575.
29. Kaushic C., et al. Influence of the estrous cycle on the presence and distribution of immune cells in the rat reproductive tract. Am. J. Reprod. Immunol. 1998, 39:209-216.
30. Klebanoff S.J., Coombs R.W. Viricidal effect of lactobacillus acidophilus on human immunodeficiency virus type 1: possible role in heterosexual transmission. J. Exp. Med. 1991, 174:289-292.
31. Koelle D.M. Vaccines for herpes simplex virus infections. Curr. Opin. Investig. Drugs 2006, 7:136-141.
32. Koutsky L.A., et al. A controlled trial of a human papillomavirus type 16 vaccine. N. Engl. J. Med. 2002, 347:1645-1651.
33. Kutteh W.H., et al. Mucosal immunity in the female reproductive tract: correlation of immunoglobulins, cytokines, and reproductive hormones in human cervical mucus around the time of ovulation. AIDS Res. Hum. Retroviruses 1998, 14(Suppl. 1):S51-S55.
34. Kutteh W.H., et al. Variations in immunoglobulins and IgA subclasses of human uterine cervical secretions around the time of ovulation. Clin. Exp. Immunol. 1996, 104:538-542.
35. Lavreys L., et al. Hormonal contraception and risk of HIV-1 acquisition: results of a 10-year prospective study. AIDS 2004, 18:695-697.
36. Leclerc P.M., et al. Hormonal contraception and HIV prevalence in four African countries. Contraception 2008, 77:371-376.
37. Looker K.J., et al. An estimate of the global prevalence and incidence of herpes simplex virus type 2 infection. Bull. World Health Organ. 2008, 86,. 805-12, A.
38. Lu F.X., et al. The strength of B cell immunity in female rhesus macaques is controlled by CD8+ T cells under the influence of ovarian steroid hormones. Clin. Exp. Immunol. 2002, 128:10-20.
39. Lu F.X., et al. Immunoglobulin concentrations and antigen-specific antibody levels in cervicovaginal lavages of rhesus macaques are influenced by the stage of the menstrual cycle. Infect. Immun. 1999, 67:6321-6328.
40. Lund J.M., et al. Cutting edge: plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J. Immunol. 2006, 177:7510-7514.
41. Martin H.L., et al. Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J. Infect. Dis. 1999, 180:1863-1868.
42. Marx P.A., et al. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat. Med. 1996, 2:1084-1089.
43. Mauck C.K., et al. The effect of one injection of depo-provera on the human vaginal epithelium and cervical ectopy. Contraception 1999, 60:15-24.
44. Miller L., et al. Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet. Gynecol. 2000, 96:431-439.
45. Morrison C.S., et al. Hormonal contraception and HIV acquisition: reanalysis using marginal structural modeling. AIDS 2010, 24:1778-1781.
46. Morrison C.S., et al. Hormonal contraception and the risk of HIV acquisition. AIDS 2007, 21:85-95.
47. Morrison C.S., et al. Highly effective contraception and acquisition of HIV and other sexually transmitted infections. Best Pract. Res. Clin. Obstet. Gynaecol. 2009, 23:263-284.
48. Mostad S.B., et al. Hormonal contraception, vitamin a deficiency, and other risk factors for shedding of HIV-1 infected cells from the cervix and vagina. Lancet 1997, 350:922-927.
49. O'brien S.M., et al. Impact of gender and menstrual cycle phase on plasma cytokine concentrations. Neuroimmunomodulation 2007, 14:84-90.
50. Paavonen T. Hormonal regulation of immune responses. Ann. Med. 1994, 26:255-258.
51. Parr M.B., Parr E.L. Vaginal immunity in the HSV-2 mouse model. Int. Rev. Immunol. 2003, 22:43-63.
52. Piccinni M.P., et al. Progesterone favors the development of human T helper cells producing TH2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established TH1 cell clones. J. Immunol. 1995, 155:128-133.
53. Polanczyk M.J., et al. Treg suppressive activity involves estrogen-dependent expression of programmed death-1 (PD-1). Int. Immunol. 2007, 19:337-343.
54. Scanlan J.M., et al. Natural killer cell activity is reduced in association with oral contraceptive use. Psychoneuroendocrinology 1995, 20:281-287.
55. Smith S.M., et al. Estrogen protects against vaginal transmission of Simian immunodeficiency virus. J. Infect. Dis. 2000, 182:708-715.
56. Smith S.M., et al. Topical estrogen protects against SIV vaginal transmission without evidence of systemic effect. AIDS 2004, 18:1637-1643.
57. Sodora D.L., et al. Vaginal transmission of SIV: assessing infectivity and hormonal influences in macaques inoculated with cell-free and cell-associated viral stocks. AIDS Res. Hum. Retroviruses 1998, 14(Suppl. 1):S119-S123.
58. Sonnex C. Influence of ovarian hormones on urogenital infection. Sex Transm. Infect. 1998, 74:11-19.
59. Souza S.S., et al. Influence of menstrual cycle on NK activity. J. Reprod. Immunol. 2001, 50:151-159.
60. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
61. Stringer E.M., et al. A randomized trial of the intrauterine contraceptive device vs hormonal contraception in women who are infected with the human immunodeficiency virus. Am. J. Obstet. Gynecol. 2007, 197(144):e1-8.
62. Szekeres-Bartho J., et al. Progesterone as an immunomodulatory molecule. Int. Immunopharmacol. 2001, 1:1037-1048.
63. Tang V.A., Rosenthal K.L. Intravaginal infection with herpes simplex virus type-2 (HSV-2) generates a functional effector memory T cell population that persists in the murine genital tract. J. Reprod. Immunol. 2010.
64. Trunova N., et al. Progestin-based contraceptive suppresses cellular immune responses in SHIV-infected rhesus macaques. Virology 2006, 352:169-177.
65. Unaids, 2006. Unaids Report on Aids Epidemic. September 2006.
66. Unaids, 2008. Unaids Report on Aids Epidemic. July 2008.
67. Veazey R.S., et al. Prevention of virus transmission to macaque monkeys by a vaginally applied monoclonal antibody to HIV-1 GP120. Nat. Med. 2003, 9:343-346.
68. Wang C.C., et al. The effect of hormonal contraception on genital tract shedding of HIV-1. AIDS 2004, 18:205-209.
69. White H.D., 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.
70. Willis C., et al. Cytokine production by peripheral blood monocytes during the normal human ovulatory menstrual cycle. Hum. Reprod. 2003, 18:1173-1178.
71. Wira C.R., et al. Sex hormone regulation of innate immunity in the female reproductive tract: The role of epithelial cells in balancing reproductive potential with protection against sexually transmitted pathogens. Am. J. Reprod. Immunol. 2010, 63:544-565.
72. Wira C.R., et al. Antigen presentation by vaginal cells: role of TGFbeta as a mediator of estradiol inhibition of antigen presentation. Endocrinology 2002, 143:2872-2879.
73. Wira C.R., Sandoe C.P. Sex steroid hormone regulation of immunoglobin G (IgG) and a (IgA) in rat uterine secretions. Nature 1977, 268:534-536.
74. Wira C.R., Sullivan D.A. Estradiol and progesterone regulation of immunoglobulin A and G and secretory component in cervicovaginal secretions of the rat. Biol. Reprod. 1985, 32:90-95.
75. Yeaman G.R., et al. Cd8+ T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking. Immunology 2001, 102:434-440.
76. Yovel G., et al. The effects of sex, menstrual cycle, and oral contraceptives on the number and activity of natural killer cells. Gynecol. Oncol. 2001, 81:254-262.
77. Zang Y.C., et al. Regulatory effects of estriol on T cell migration and cytokine profile: inhibition of transcription factor NF-kappa B. J. Neuroimmunol. 2002, 124:106-114.