Differential Glucocorticoid Receptor-Mediated Effects on Immunomodulatory Gene Expression by Progestin Contraceptives: Implications for HIV-1 Pathogenesis

American Journal of Reproductive Immunology

Volumn 71, Issue 6, 2014, Pages 505-512

  Hapgood, Janet P ^a   Ray, Roslyn M ^a   Govender, Yashini ^a   Avenant, Chanel ^a   Tomasicchio, Michele ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Contraception; Glucocorticoid receptor; HIV 1; Medroxyprogesterone acetate; Norethisterone; Progestin

Indexed keywords

CONTRACEPTIVE AGENT; GESTAGEN; GLUCOCORTICOID RECEPTOR; INJECTABLE CONTRACEPTIVE AGENT; MEDROXYPROGESTERONE ACETATE; NORETHISTERONE ENANTATE; PROGESTERONE; PROGESTERONE RECEPTOR; NORETHISTERONE; ORAL CONTRACEPTIVE AGENT; PROGESTERONE DERIVATIVE;

AFRICA SOUTH OF THE SAHARA; ARTICLE; DRUG EFFECT; GENE EXPRESSION; HORMONAL CONTRACEPTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOMODULATION; INFECTION RISK; NONHUMAN; ORAL CONTRACEPTION; PRIORITY JOURNAL; VIRUS PATHOGENESIS; ANALOGS AND DERIVATIVES; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; PATHOGENICITY; PATHOLOGY; TRANSMISSION;

AFRICA SOUTH OF THE SAHARA; CONTRACEPTIVE AGENTS; CONTRACEPTIVE AGENTS, FEMALE; CONTRACEPTIVES, ORAL, SYNTHETIC; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOSUPPRESSION; MEDROXYPROGESTERONE ACETATE; NORETHINDRONE; PROGESTERONE CONGENERS; RECEPTORS, GLUCOCORTICOID;

EID: 84900791081     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12214     Document Type: Article

References (47)

1. WHO: Hormonal Contraception and HIV: Technical Statement. 2012. Available from: http://www.who.int/reproductivehealth/publications/family_planning/rhr_12_8/en/index.html
2. USAID: Technical Brief: Hormonal Contraception and HIV 2013. Available from: http://www.usaid.gov/sites/default/files/documents/1864/hormonal-contraception-and-HIV.pdf
3. Hapgood JP, Koubovec D, Louw A, Africander D: Not all progestins are the same: implications for usage. Trends Pharmacol Sci 2004; 25:554-557.
4. Africander D, Verhoog N, Hapgood JP: Molecular mechanisms of steroid receptor-mediated actions by synthetic progestins used in HRT and contraception. Steroids 2011; 76:636-652.
5. Stanczyk FZ, Hapgood JP, Winer S, Mishell DR Jr: Progestogens used in postmenopausal hormone therapy: differences in their pharmacological properties, intracellular actions, and clinical effects. Endocr Rev 2013; 34:171-208.
6. FHI: Expanding access to injectable contraception. FHI 360 Website. 2013. Available from: http://www.fhi360.org/resource/expanding-access-injectable-contraception.
7. Smit JA, Beksinska ME: Hormonal contraceptive continuation and switching in South Africa: implications for evaluating the association of injectable hormonal contraceptive use and HIV. J Acquir Immune Defic Syndr 2013; 62:363-365.
8. Abdool Karim Q, Abdool Karim SS, Frohlich JA, Grobler AC, Baxter C, Mansoor LE, Kharsany ABM, Sibeko S, Mlisana KP, Omar Z, Gengiah TN, Maarschalk S, Arulappan N, Mlotshwa M, Morris L, Taylor D: Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 2010; 329:1168-1174.
9. Polis CB, Curtis KM: Use of hormonal contraceptives and HIV acquisition in women: a systematic review of the epidemiological evidence. Lancet Infect Dis 2013; 13:797-808.
10. McCoy SI, Zheng W, Montgomery ET, Blanchard K, van der Straten A, de Bruyn G, Padian NS: Oral and injectable contraception use and risk of HIV acquisition among women in sub-Saharan Africa. AIDS 2013; 27:1001-1009.
11. Wand H, Ramjee G: The effects of injectable hormonal contraceptives on HIV seroconversion and on sexually transmitted infections. AIDS 2012; 26:375-380.
12. Morrison CS, Chen P, Kwok C, Richardson BA, Chipato T, Mugerwa R, Byamugisha J, Padian N, Celentano DD, Salata RA: Hormonal contraception and HIV acquisition: reanalysis using marginal structural modeling. AIDS 2010; 24:1778-1781.
13. Kiddugavu M, Makumbi F, Wawer MJ, Serwadda D, Sewankambo NK, Wabwire-Mangen F, Lutalo T, Meehan M, Xianbin Li, Gray RH: Hormonal contraceptive use and HIV-1 infection in a population-based cohort in Rakai, Uganda. AIDS 2003; 17:233-240.
14. Baeten JM, Lavreys L, Overbaugh J: The influence of hormonal contraceptive use on HIV-1 transmission and disease progression. Clin Infect Dis 2007; 45:360-369.
15. Myer L, Denny L, Wright TC, Kuhn L: Prospective study of hormonal contraception and women's risk of HIV infection in South Africa. Int J Epidemiol 2007; 36:166-174.
16. Heffron R, Donnell D, Rees H, Celum C, Mugo N, Were E, De Bruyn G, Nakku-Joloba E, Ngure K: Use of hormonal contraceptives and risk of HIV-1 transmission: a prospective cohort study. Lancet Infect Dis 2012; 12:19-26.
17. Mostad SB, Kreiss JK, Ryncarz a J, Mandaliya K, Chohan B, Ndinya-Achola J, Bwayo JJ, Corey L: Cervical shedding of herpes simplex virus in human immunodeficiency virus-infected women: effects of hormonal contraception, pregnancy, and vitamin A deficiency. J Infect Dis 2000; 181:58-63.
18. Wang CC, Mcclelland RS, Overbaugh J, Reilly M, Devange D, Mandaliya K, Chohan B, Lavreys L, Ndinya-Achola J, Kreis JK: The effect of hormonal contraception on genital tract shedding of HIV-1. AIDS 2004; 18:205-209.
19. Mostad SB, Overbaugh J, Devange DM, Welch MJ, Chohan B, Mandaliya K, Nyange P, Martin HL Jr, Ndinya-Achola J, Bwayo JJ, Kreiss JK: 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.
20. Lavreys L, Baeten J, Martin H Jr, Overbaugh J, Mandaliya K, Ndinya-Achola J, Kreiss JK: Hormonal contraception and risk of HIV-1 acquisition: results of a 10-year prospective study. AIDS 2004; 18:695-697.
21. Morrison CS, Bright P, Wong EL, Kwok C, Yacobson I, Gaydos CA, Tucker HT, Blumenthal PD: Hormonal contraceptive use, cervical ectopy, and the acquisition of cervical infections. Sex Transm Dis 2004; 31:561-567.
22. Trunova N, Tsai L, Tung S, Schneider E, Harouse J, Gettie A, Simon V, Blanchard J, Cheng-Mayer C: Progestin-based contraceptive suppresses cellular immune responses in SHIV-infected rhesus macaques. Virology 2006; 352:169-177.
23. Phillips SJ, Curtis KM, Polis CB: Effect of hormonal contraceptive methods on HIV disease progression: a systematic review. AIDS 2013; 27:787-794.
24. Polis CB, Westreich D, Balkus JE, Heffron R: Assessing the effect of hormonal contraception on HIV acquisition in observational data: challenges and recommended analytic approaches. AIDS 2013; 27(Suppl 1):S35-S43.
25. Morrison CS, Nanda K: Hormonal contraception and HIV: an unanswered question. Lancet Infect Dis 2012; 12:2-3.
26. Blish CA, Baeten JM: Hormonal contraception and HIV-1 transmission. Am J Reprod Immunol 2011; 65:302-307.
27. Africander D, Louw R, Hapgood JP: Investigating the anti-mineralocorticoid properties of synthetic progestins used in hormone therapy. Biochem Biophys Res Commun 2013; 433:305-310.
28. Baschant U, Tuckermann J: The role of the glucocorticoid receptor in inflammation and immunity. J Steroid Biochem Mol Biol 2010; 120:69-75.
29. Coutinho AE, Chapman KE: The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol Cell Endocrinol 2011; 335:2-13.
30. De Bosscher K, Van Craenenbroeck K, Meijer OC, Haegeman G: Selective transrepression versus transactivation mechanisms by glucocorticoid receptor modulators in stress and immune systems. Eur J Pharmacol 2008; 583:290-302.
31. Koubovec D, Vanden Berghe W, Vermeulen L, Haegeman G, Hapgood JP: Medroxyprogesterone acetate downregulates cytokine gene expression in mouse fibroblast cells. Mol Cell Endocrinol 2004; 221:75-85.
32. Koubovec D, Ronacher K, Stubsrud E, Louw A, Hapgood JP: Synthetic progestins used in HRT have different glucocorticoid agonist properties. Mol Cell Endocrinol 2005; 242:23-32.
33. Ronacher K, Hadley K, Avenant C, Stubsrud E, Simons SS, Louw A, Hapgood JP: Ligand-selective transactivation and transrepression via the glucocorticoid receptor: role of cofactor interaction. Mol Cell Endocrinol 2009; 299:219-231.
34. Bamberger CM, Else T, Bamberger A, Beil FU, Schulte HM: Dissociative glucocorticoid activity of medroxyprogesterone acetate in normal human lymphocytes. J Clin Endocrinol Metab 1999; 84:4055-4061.
35. Tomasicchio M, Avenant C, Du Toit A, Ray RM, Hapgood JP: The progestin-only contraceptive medroxyprogesterone acetate, but not norethisterone acetate, enhances HIV-1 Vpr-mediated apoptosis in human CD4 + T cells through the glucocorticoid receptor. PLoS ONE 2013; 8:e62895.
36. Huijbregts RPH, Helton ES, Michel KG, Sabbaj S, Richter HE, Goepfert PA, Hel Z: Hormonal contraception and HIV-1 infection: medroxyprogesterone acetate suppresses innate and adaptive immune mechanisms. Endocrinology 2013; 154:1282-1295.
37. Eddleston J, Herschbach J, Wagelie-Steffen AL, Christiansen SC, Zuraw BL: The anti-inflammatory effect of glucocorticoids is mediated by glucocorticoid-induced leucine zipper in epithelial cells. J Allergy Clin Immunol 2007; 119:115-122.
38. Janeway CA Jr, Travers P, Walport M: Immunobiology, 8th Edn. K Murphy (ed). New York, Garland Science, 2012.
39. Aukrust P, Müller F, Frøland SS: Circulating levels of RANTES in human immunodeficiency virus type 1 infection: effect of potent antiretroviral therapy. J Infect Dis 1998; 177:1091-1096.
40. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P: Identification of RANTES, MIP-1alpha, and MIP-1beta as the Major HIV-Suppressive Factors Produced by CD8 + T Cells. Science 1995; 270:1811-1815.
41. Kleynhans L, Du Plessis N, Black GF, Loxton AG, Kidd M, Van Helden PD, Walzl G, Ronacher K: Medroxyprogesterone acetate alters mycobacterium bovis BCG-induced cytokine production in peripheral blood mononuclear cells of contraceptive users. PLoS ONE 2011; 6:e24639.
42. Kleynhans L, Du Plessis N, Allie N, Jacobs M, Kidd M, Van Helden PD, Walzl G, Ronacher K: The contraceptive depot medroxyprogesterone acetate impairs mycobacterial control and inhibits cytokine secretion in mice infected with Mycobacterium tuberculosis. Infect Immun 2013; 81:1234-1244.
43. Hapgood JP, Africander D, Louw R, Ray RM, Rohwer JM: Potency of progestogens used in hormonal therapy: toward understanding differential actions. J Steroid Biochem Mol Biol 2013; doi: 10.1016/j.jsbmb.2013.08.001.
44. Jain AK: Hormonal contraception and HIV acquisition risk: implications for individual users and public policies. Contraception 2012; 86:645-652.
45. Rodriguez MI, Reeves MF, Caughey AB: Evaluating the competing risks of HIV acquisition and maternal mortality in Africa: a decision analysis. BJOG 2012; 119:1067-1073.
46. Jain AK: Erratum to "Hormonal contraception and HIV acquisition risk: implications for individual users and public policies"[Contraception 86 (2012) 645-652]. Contraception 2013; 88:195.
47. Hapgood JP: Immunosuppressive biological mechanisms support reassessment of use of the injectable contraceptive medroxyprogesterone acetate. Endocrinology 2013; 154:985-988.