Medroxyprogesterone acetate regulates HIV-1 uptake and transcytosis but not replication in primary genital epithelial cells, resulting in enhanced T-cell infection

Journal of Infectious Diseases

Volumn 211, Issue 11, 2015, Pages 1745-1756

  Ferreira, Victor H ^a,b   Dizzell, Sara ^a,b   Nazli, Aisha ^a,b   Kafka, Jessica K ^a,b   Mueller, Kristen ^a,b   Nguyen, Philip V ^a,b   Tremblay, Michel J ^d   Cochrane, Alan ^c   Kaushic, Charu ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

Author keywords

female sex hormones; genital epithelial cells; HIV replication; HIV transmission; HIV 1; hormonal contraceptives; inflammation; medroxyprogesterone acetate; transcytosis

Indexed keywords

CHEMOKINE; EOTAXIN 2; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; MEDROXYPROGESTERONE ACETATE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROGESTERONE; RANTES; TUMOR NECROSIS FACTOR ALPHA; CONTRACEPTIVE AGENT; CYTOKINE;

ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOCYTOSIS; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSCYTOSIS; UPREGULATION; VIRUS REPLICATION; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; UTERUS; VIROLOGY; VIRUS ENTRY;

CELLS, CULTURED; CONTRACEPTIVE AGENTS, FEMALE; CYTOKINES; ENDOCYTOSIS; EPITHELIAL CELLS; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; MEDROXYPROGESTERONE ACETATE; PROGESTERONE; T-LYMPHOCYTES; UP-REGULATION; UTERUS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84930430131     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu832     Document Type: Article

References (45)

1. Hladik F, McElrath MJ. Setting the stage: host invasion by HIV. Nat Rev Immunol 2008; 8:447-57.
2. Asin SN, Fanger MW, Wildt-Perinic D, Ware PL, Wira CR, Howell AL. Transmission of HIV-1 by primary human uterine epithelial cells and stromal fibroblasts. J Infect Dis 2004; 190:236-45.
3. Asin SN, Wildt-Perinic D, Mason SI, Howell AL, Wira CR, FangerMW. Human immunodeficiency virus type 1 infection of human uterine epithelial cells: viral shedding and cell contact-mediated infectivity. J Infect Dis 2003; 187:1522-33.
4. Tan X, Pearce-Pratt R, Phillips DM. Productive infection of a cervical epithelial cell line with human immunodeficiency virus: implications for sexual transmission. J Virol 1993; 67:6447-52.
5. Micsenyi AM, Zony C, Alvarez RA, Durham ND, Chen BK, Klotman ME. Postintegration HIV-1 infection of cervical epithelial cells mediates contact-dependent productive infection of T cells. J Infect Dis 2013; 208:1756-67.
6. Dezzutti CS, Guenthner PC, Cummins JE Jr, et al. Cervical and prostate primary epithelial cells are not productively infected but sequester human immunodeficiency virus type 1. J Infect Dis 2001; 183:1204-13.
7. Greenhead P, Hayes P, Watts PS, Laing KG, Griffin GE, Shattock RJ. Parameters of human immunodeficiency virus infection of human cervical tissue and inhibition by vaginal virucides. J Virol 2000; 74:5577-86.
8. Wu Z, Chen Z, Phillips DM. Human genital epithelial cells capture cellfree human immunodeficiency virus type 1 and transmit the virus to CD4+ cells: implications for mechanisms of sexual transmission. J Infect Dis 2003; 188:1473-82.
9. Bomsel M. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat Med 1997; 3:42-7.
10. Bobardt MD, Chatterji U, Selvarajah S, et al. Cell-free human immunodeficiency virus type 1 transcytosis through primary genital epithelial cells. J Virol 2007; 81:395-405.
11. Carreno MP, Krieff C, Irinopoulou T, Kazatchkine MD, Belec L. Enhanced transcytosis of R5-tropic human immunodeficiency virus across tight monolayer of polarized human endometrial cells under pro-inflammatory conditions. Cytokine 2002; 20:289-94.
12. Gupta S, Gach JS, Becerra JC, et al. The neonatal Fc receptor (FcRn) enhances human immunodeficiency virus type 1 (HIV-1) transcytosis across epithelial cells. PLoS Pathog 2013; 9:e1003776.
13. Hocini H, Becquart P, Bouhlal H, et al. Active and selective transcytosis of cell-free human immunodeficiency virus through a tight polarized monolayer of human endometrial cells. J Virol 2001; 75:5370-4.
14. Stoddard E, Ni H, Cannon G, et al. gp340 promotes transcytosis of human immunodeficiency virus type 1 in genital tract-derived cell lines and primary endocervical tissue. J Virol 2009; 83:8596-603.
15. Haase AT. Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu Rev Med 2011; 62:127-39.
16. Li Q, Estes JD, Schlievert PM, et al. Glycerol monolaurate prevents mucosal SIV transmission. Nature 2009; 458:1034-8.
17. Miller CJ, Vogel P, Alexander NJ, Sutjipto S, Hendrickx AG, Marx PA. Localization of SIV in the genital tract of chronically infected female rhesus macaques. Am J Pathol 1992; 141:655-60.
18. Stieh DJ, Maric D, Kelley ZL, et al. Vaginal challenge with an SIV-based dual reporter system reveals that infection can occur throughout the upper and lower female reproductive tract. PLoS Pathog 2014; 10: e1004440.
19. Pudney J, Quayle AJ, Anderson DJ. Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation zone. Biol Reprod 2005; 73:1253-63.
20. Carias AM, McCoombe S, McRavenM, et al. Defining the interaction of HIV-1 with the mucosal barriers of the female reproductive tract. J Virol 2013; 87:11388-400.
21. Population Division, Department of Economic and Social Affairs, United Nations.World contraceptive use 2003. New York: United Nations, 2004
22. 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.
23. Heffron R, Donnell D, Rees H, et al. Use of hormonal contraceptives and risk of HIV-1 transmission: a prospective cohort study. Lancet Infect Dis 2012; 12:19-26.
24. Marx PA, Spira AI, Gettie A, et al. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat Med 1996; 2:1084-9.
25. Gillgrass AE, Ashkar AA, Rosenthal KL, Kaushic C Prolonged exposure to progesterone prevents induction of protective mucosal responses following intravaginal immunization with attenuated herpes simplex virus type 2. J Virol 2003; 77:9845-51.
26. MacDonald EM, Savoy A, Gillgrass A, et al. Susceptibility of human female primary genital epithelial cells to herpes simplex virus, type-2 and the effect of TLR3 ligand and sex hormones on infection. Biol Reprod 2007; 77:1049-59.
27. Kaushic C, Nazli A, Ferreira VH, Kafka JK. Primary human epithelial cell culture system for studying interactions between female upper genital tract and sexually transmitted viruses, HSV-2 and HIV-1. Methods 2011; 55:114-21.
28. Nazli A, Chan O, Dobson-Belaire WN, et al. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 2010; 6:e1000852.
29. Vidricaire G, Gauthier S, Tremblay MJ. HIV-1 infection of trophoblasts is independent of gp120/CD4 Interactions but relies on heparan sulfate proteoglycans. J Infect Dis 2007; 195:1461-71.
30. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 2006; 10:839-50.
31. Parry S, Zhang J, Koi H, Arechavaleta-Velasco F, Elovitz MA. Transcytosis of Human immunodeficiency virus 1 across the placenta is enhanced by treatment with tumour necrosis factor alpha. J Gen Virol 2006; 87(Pt 8):2269-78.
32. Kimpton J, Emerman M. Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene. J Virol 1992; 66:2232-9.
33. Wong RW, Balachandran A, Ostrowski MA, Cochrane A. Digoxin suppresses HIV-1 replication by altering viral RNA processing. PLoS Pathog 2013; 9:e1003241.
34. Vidricaire G, Tremblay MJ. Rab5 and Rab7, but not ARF6, govern the early events of HIV-1 infection in polarized human placental cells. J Immunol 2005; 175:6517-30.
35. Doitsh G, Cavrois M, Lassen KG, et al. Abortive HIV infection mediates CD4T cell depletion and inflammation in human lymphoid tissue. Cell 2010; 143:789-801.
36. Stricker R, Eberhart R, Chevailler MC, Quinn FA, Bischof P, Stricker R. Establishment of detailed reference values for luteinizing hormone, follicle stimulating hormone, estradiol, and progesterone during different phases of the menstrual cycle on the Abbott ARCHITECT analyzer. Clin Chem Lab Med 2006; 44:883-7.
37. Halpern V, Combes SL, Dorflinger LJ, Weiner DH, Archer DF. Pharmacokinetics of subcutaneous depot medroxyprogesterone acetate injected in the upper arm. Contraception 2014; 89:31-5.
38. BerlierW, Bourlet T, Lawrence P, et al. Selective sequestration of X4 isolates by human genital epithelial cells: Implication for virus tropism selection process during sexual transmission of HIV. J Med Virol 2005; 77:465-74.
39. Nazli A, Kafka JK, Ferreira VH, et al. HIV-1 gp120 induces TLR2- and TLR4-mediated innate immune activation in human female genital epithelium. J Immunol 2013; 191:4246-58.
40. Rancez M, Couedel-Courteille A, Cheynier R. Chemokines at mucosal barriers and their impact on HIV infection. Cytokine Growth Factor Rev 2012; 23:233-43.
41. Morrison C, Fichorova RN, Mauck C, et al. Cervical inflammation and immunity associated with hormonal contraception, pregnancy, and HIV-1 seroconversion. J Acquir Immune Defic Syndr 2014; 66: 109-17.
42. Huijbregts RP, Michel KG, Hel Z. Effect of progestins on immunity: medroxyprogesterone but not norethisterone or levonorgestrel suppresses the function of T cells and pDCs. Contraception 2014; 90:123-9.
43. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P. Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 1995; 270:1811-5.
44. Schall TJ. Biology of the RANTES/SIS cytokine family. Cytokine 1991; 3:165-83.
45. Mitchell CM, McLemore L, Westerberg K, et al. Long-term effect of depot medroxyprogesterone acetate on vaginal microbiota, epithelial thickness and HIV target cells. J Infect Dis 2014; 210:651-5.