The contraceptive depot medroxyprogesterone acetate impairs mycobacterial control and inhibits cytokine secretion in mice infected with Mycobacterium tuberculosis

Infection and Immunity

Volumn 81, Issue 4, 2013, Pages 1234-1244

  Kleynhans, Léanie ^a   Du Plessis, Nelita ^a   Allie, Nasiema ^b   Jacobs, Muazzam ^b,c   Kidd, Martin ^d   van Helden, Paul D ^a   Walzl, Gerhard ^a   Ronachera, Katharina ^a  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c NATIONAL HEALTH LABORATORY SERVICE   (South Africa)

^d STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MEDROXYPROGESTERONE ACETATE; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE SEVERITY; FEMALE; INFECTION CONTROL; LUNG; LUNG TUBERCULOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL;

ANIMALS; CONTRACEPTIVE AGENTS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOLOGIC FACTORS; IMMUNOSUPPRESSION; MEDROXYPROGESTERONE ACETATE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

EID: 84875492604     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01189-12     Document Type: Article

References (47)

1. Kleynhans L, Du Plessis N, Black GF, Loxton AG, Kidd M, van Helden PD, Walzl G, Ronacher K. 2011. Medroxyprogesterone acetate alters Mycobacterium bovis BCG-induced cytokine production in peripheral blood mononuclear cells of contraceptive users. PLoS One 6:e24639. doi: 10.1371/journal.pone.0024639.
2. Heffron R, Donnell D, Rees H, Celum C, Mugo N, Were E, de Bruyn G, Nakku-Joloba E, Ngure K, Kiarie J, Coombs RW, Baeten JM. 2012. Use of hormonal contraceptives and risk of HIV-1 transmission: a prospective cohort study. Lancet Infect. Dis. 12:19-26.
3. Morrison CS, Chen PL, Kwok C, Richardson BA, Chipato T, Mugerwa R, Byamugisha J, Padian N, Celentano DD, Salata RA. 2010. Hormonal contraception and HIV acquisition: reanalysis using marginal structural modeling. AIDS 24:1778-1781.
4. Leclerc PM, Dubois-Colas N, Garenne M. 2008. Hormonal contraception and HIV prevalence in four African countries. Contraception 77:371-376.
5. Morrison CS, Skoler-Karpoff S, Kwok C, Chen PL, van de Wijgert J, Gehret-Plagianos M, Patel S, Ahmed K, Ramjee G, Friedland B, Lahteenmaki P. 2012. Hormonal contraception and the risk of HIV acquisition among women in South Africa. AIDS 26:497-504.
6. Myer L, Denny L, Wright TC, Kuhn L. 2007. Prospective study of hormonal contraception and women's risk of HIV infection in South Africa. Int. J. Epidemiol. 36:166-174.
7. Overton ET, Shacham E, Singhatiraj E, Nurutdinova D. 2008. Incidence of sexually transmitted infections among HIV-infected women using depot medroxyprogesterone acetate contraception. Contraception 78:125-130.
8. Bentel JM, Birrell SN, Pickering MA, Holds DJ, Horsfall DJ, Tilley WD. 1999. Androgen receptor agonist activity of the synthetic progestin, medroxyprogesterone acetate, in human breast cancer cells. Mol. Cell. Endocrinol. 154:11-20.
9. Strahle U, Klock G, Schutz G. 1987. A DNA sequence of 15 base pairs is sufficient to mediate both glucocorticoid and progesterone induction of gene expression. Proc. Natl. Acad. Sci. U. S. A. 84:7871-7875.
10. Zhou Z, Corden JL, Brown TR. 1997. Identification and characterization of a novel androgen response element composed of a direct repeat. J. Biol. Chem. 272:8227-8235.
11. Kontula K, Paavonen T, Luukkainen T, Andersson LC. 1983. Binding of progestins to the glucocorticoid receptor. Correlation to their glucocorticoid- like effects on in vitro functions of human mononuclear leukocytes. Biochem. Pharmacol. 32:1511-1518.
12. Koubovec D, Ronacher K, Stubsrud E, Louw A, Hapgood JP. 2005. Synthetic progestins used in HRT have different glucocorticoid agonist properties. Mol. Cell. Endocrinol. 242:23-32.
13. Zhao Q, Pang J, Favata MF, Trzaskos JM. 2003. Receptor density dictates the behavior of a subset of steroid ligands in glucocorticoid receptor-mediated transrepression. Int. Immunopharmacol. 3:1803-1817.
14. Manabe YC, Kesavan AK, Lopez-Molina J, Hatem CL, Brooks M, Fujiwara R, Hochstein K, Pitt ML, Tufariello J, Chan J, McMurray DN, Bishai WR, Dannenberg AM, Jr, Mendez S. 2008. The aerosol rabbit model of TB latency, reactivation and immune reconstitution inflammatory syndrome. Tuberculosis (Edinb.) 88:187-196.
15. Scanga CA, Mohan VP, Joseph H, Yu K, Chan J, Flynn JL. 1999. Reactivation of latent tuberculosis: variations on the Cornell murine model. Infect. Immun. 67:4531-4538.
16. Howard AD, Zwilling BS. 1999. Reactivation of tuberculosis is associated with a shift from type 1 to type 2 cytokines. Clin. Exp. Immunol. 115:428-434.
17. Jick SS, Lieberman ES, Rahman MU, Choi HK. 2006. Glucocorticoid use, other associated factors, and the risk of tuberculosis. Arthritis Rheum. 55:19-26.
18. Ortiz A, Hirol M, Stanczyk FZ, Goebelsmann U, Mishell DR. 1977. Serum medroxyprogesterone acetate (MPA) concentrations and ovarian function following intramuscular injection of depo-MPA. J. Clin. Endocrinol. Metab. 44:32-38.
19. Harizi H, Mormede P, Corcuff JB. 2008. Inter-strain differences in glucocorticoid and mineralocorticoid effects on macrophage and lymphocyte functions in mice. J. Neuroimmunol. 204:38-42.
20. Redford PS, Boonstra A, Read S, Pitt J, Graham C, Stavropoulos E, Bancroft GJ, O'Garra A. 2010. Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 40: 2200-2210.
21. Tilley SL, Jaradat M, Stapleton C, Dixon D, Hua X, Erikson CJ, McCaskill JG, Chason KD, Liao G, Jania L, Koller BH, Jetten AM. 2007. Retinoid-related orphan receptor gamma controls immunoglobulin production and Th1/Th2 cytokine balance in the adaptive immune response to allergen. J. Immunol. 178:3208-3218.
22. Fang S, Sun D, Jiang H, Luo H. 2004. Concentration changes if medroxyprogesterone acetate in serum and milk in lactating women who used depo geston. J. Reprod. Contraception 15:157-162.
23. Smit J, Botha J, McFadyen L, Beksinska M. 2004. Serum medroxyprogesterone acetate levels in new and repeat users of depot medroxyprogesterone acetate at the end of the dosing interval. Contraception 69:3-7.
24. Pfizer. 2012. Depo-Provera U.S. physicians prescribing information. http://labeling.pfizer.com/ShowLabeling.aspx?id522. Pfizer, New York, NY.
25. Jeppsson S, Gershagen S, Johansson ED, Rannevik G. 1982. Plasma levels of medroxyprogesterone acetate (MPA), sex-hormone binding globulin, gonadal steroids, gonadotrophins and prolactin in women during long-term use of depo-MPA (Depo-Provera) as a contraceptive agent. Acta Endocrinol. (Copenh.) 99:339-343.
26. Beksinska ME, Smit JA, Kleinschmidt I, Milford C, Farley TM. 2010. Prospective study of weight change in new adolescent users of DMPA, NET-EN, COCs, nonusers and discontinuers of hormonal contraception. Contraception 81:30-34.
27. Ito K, Herbert C, Siegle JS, Vuppusetty C, Hansbro N, Thomas PS, Foster PS, Barnes PJ, Kumar RK. 2008. Steroid-resistant neutrophilic inflammation in a mouse model of an acute exacerbation of asthma. Am. J. Respir. Cell Mol. Biol. 39:543-550.
28. Dambuza I, Keeton R, Allie N, Hsu NJ, Randall P, Sebesho B, Fick L, Quesniaux VJ, Jacobs M. 2011. Reactivation of M. tuberculosis infection in trans-membrane tumour necrosis factor mice. PLoS One 6:e25121. doi: 10.1371/journal.pone.0025121.
29. Kaushic C, Ashkar AA, Reid LA, Rosenthal KL. 2003. Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J. Virol. 77:4558-4565.
30. Marx PA, Spira AI, Gettie A, Dailey PJ, Veazey RS, Lackner AA, Mahoney CJ, Miller CJ, Claypool LE, Ho DD, Alexander NJ. 1996. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat. Med. 2:1084-1089.
31. Wang CC, McClelland RS, Overbaugh J, Reilly M, Panteleeff DD, Mandaliya K, Chohan B, Lavreys L, Ndinya-Achola J, Kreiss JK. 2004. The effect of hormonal contraception on genital tract shedding of HIV-1. AIDS 18:205-209.
32. Cherpes TL, Busch JL, Sheridan BS, Harvey SA, Hendricks RL. 2008. Medroxyprogesterone acetate inhibits CD8 T cell viral-specific effector function and induces herpes simplex virus type 1 reactivation. J. Immunol. 181:969-975.
33. Vicetti Miguel RD, Hendricks RL, Aguirre AJ, Melan MA, Harvey SA, Terry-Allison T, St Leger AJ, Thomson AW, Cherpes TL. 2012. Dendritic cell activation and memory cell development are impaired among mice administered medroxyprogesterone acetate prior to mucosal herpes simplex virus type 1 infection. J. Immunol. 189:3449-3461.
34. Heimbeck I, Hofer TP, Eder C, Wright AK, Frankenberger M, Marei A, Boghdadi G, Scherberich J, Ziegler-Heitbrock L. 2010. Standardized single-platform assay for human monocyte subpopulations: lower monocytes in females. Cytometry A 77:823-830.
35. Hughes GC, Martin D, Zhang K, Hudkins KL, Alpers CE, Clark EA, Elkon KB. 2009. Decrease in glomerulonephritis and Th1-associated autoantibody production after progesterone treatment in NZB/NZW mice. Arthritis Rheum. 60:1775-1784.
36. McNeill AM, Zhang C, Stanczyk FZ, Duckles SP, Krause DN. 2002. Estrogen increases endothelial nitric oxide synthase via estrogen receptors in rat cerebral blood vessels: effect preserved after concurrent treatment with medroxyprogesterone acetate or progesterone. Stroke 33:1685-1691.
37. Palmieri D, Halverson DO, Ouatas T, Horak CE, Salerno M, Johnson J, Figg WD, Hollingshead M, Hursting S, Berrigan D, Steinberg SM, Merino MJ, Steeg PS. 2005. Medroxyprogesterone acetate elevation of Nm23-H1 metastasis suppressor expression in hormone receptornegative breast cancer. J. Natl. Cancer Inst. 97:632-642.
38. Hernandez-Pando R, de la Luz SM, Orozco H, Arriaga K, Pavon L, Al-Nakhli SA, Rook GA. 1998. The effects of androstenediol and dehydroepiandrosterone on the course and cytokine profile of tuberculosis in BALB/c mice. Immunology 95:234-241.
39. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, Siegel JN, Braun MM. 2001. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N. Engl. J. Med. 345:1098-1104.
40. Higgins DM, Sanchez-Campillo J, Rosas-Taraco AG, Lee EJ, Orme IM, Gonzalez-Juarrero M. 2009. Lack of IL-10 alters inflammatory and immune responses during pulmonary Mycobacterium tuberculosis infection. Tuberculosis (Edinb.) 89:149-157.
41. Welsh KJ, Abbott AN, Hwang SA, Indrigo J, Armitige LY, Blackburn MR, Hunter RL, Jr, Actor JK. 2008. A role for tumour necrosis factor-alpha, complement C5 and interleukin-6 in the initiation and development of the mycobacterial cord factor trehalose 6,6=- dimycolate induced granulomatous response. Microbiology 154:1813-1824.
42. Curtis MM, Way SS. 2009. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126:177-185.
43. Scriba TJ, Kalsdorf B, Abrahams DA, Isaacs F, Hofmeister J, Black G, Hassan HY, Wilkinson RJ, Walzl G, Gelderbloem SJ, Mahomed H, Hussey GD, Hanekom WA. 2008. Distinct, specific IL-17- and IL-22-producing CD4 T cell subsets contribute to the human antimycobacterial immune response. J. Immunol. 180:1962-1970.
44. Djoba Siawaya JF, Chegou NN, van den Heuvel MM, Diacon AH, Beyers N, van Helden P, Walzl G. 2009. Differential cytokine/ chemokines and KL-6 profiles in patients with different forms of tuberculosis. Cytokine 47:132-136.
45. Dandona P, Aljada A, Garg R, Mohanty P. 1999. Increase in plasma interleukin-10 following hydrocortisone injection. J. Clin. Endocrinol. Metab. 84:1141-1144.
46. Allie N, Alexopoulou L, Quesniaux VJ, Fick L, Kranidioti K, Kollias G, Ryffel B, Jacobs M. 2008. Protective role of membrane tumour necrosis factor in the host's resistance to mycobacterial infection. Immunology 125:522-534.
47. Tumes DJ, Cormie J, Calvert MG, Stewart K, Nassenstein C, Braun A, Foster PS, Dent LA. 2007. Strain-dependent resistance to allergeninduced lung pathophysiology in mice correlates with rate of apoptosis of lung-derived eosinophils. J. Leukoc. Biol. 81:1362-1373.