17β-estradiol protects primary macrophages against HIV infection through induction of interferon-alpha

Viral Immunology

Volumn 27, Issue 4, 2014, Pages 140-150

  Tasker, Carley ^a   Ding, Jian ^a   Schmolke, Mirco ^b   Rivera Medina, Amariliz ^c   García Sastre, Adolfo ^b   Chang, Theresa L ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; ESTRADIOL; NEUTRALIZING ANTIBODY; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INNATE IMMUNITY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; NORMAL HUMAN; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; RNA TRANSCRIPTION; UPREGULATION; VIRUS ATTACHMENT; VIRUS ENTRY; ANIMAL; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; FEMALE; HOST PATHOGEN INTERACTION; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY;

ANIMALS; CELLS, CULTURED; ESTRADIOL; FEMALE; HIV; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-ALPHA; MACROPHAGES; MALE; MICE, INBRED C57BL; REVERSE TRANSCRIPTION;

EID: 84900550691     PISSN: 08828245     EISSN: 15578976     Source Type: Journal    
DOI: 10.1089/vim.2013.0120     Document Type: Article

References (54)

1. Baca-Regen L, Heinzinger N, Stevenson M, and Gendelman HE. Alpha interferon-induced antiretroviral activities: restriction of viral nucleic acid synthesis and progeny virion production in human immunodeficiency virus type 1-infected monocytes. J Virol 1994; 68: 7559-7565.
2. Berger G, Durand S, Fargier G, et al. APOBEC3A is a specific inhibitor of the early phases of HIV-1 infection in myeloid cells. PLoS Pathog 2011; 7: e1002221.
3. Biswas DK, Singh S, Shi Q, Pardee AB, and Iglehart JD. Crossroads of estrogen receptor and NF-kappaB signaling. Sci STKE 2005;pe27.
4. CalippeB, Douin-EchinardV, Delpy L, et al. 17Beta-estradiol promotes TLR4-triggered proinflammatory mediator production through direct estrogen receptor alpha signaling in macrophages in vivo. J Immunol 2010; 185: 1169-1176.
5. Chadwick CC, Chippari S, Matelan E, et al. Identification of pathway-selective estrogen receptor ligands that inhibit NF-kappaB transcriptional activity. Proc Natl Acad Sci U S A 2005; 102: 2543-2548.
6. Chang TL, Vargas J Jr, DelPortillo A, and Klotman ME. Dual role of alpha-defensin-1 in anti-HIV-1 innate immunity. J Clin Invest 2005; 115: 765-773.
7. Cheney KM, and McKnight A. Interferon-alpha mediates restriction of human immunodeficiency virus type-1 replication in primary human macrophages at an early stage of replication. PLoS One 2010; 5: e13521.
8. Connor RI, Sheridan KE, Ceradini D, Choe S, and Landau NR. Change in coreceptor use coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 1997; 185: 621-628.
9. Doehle BP, Chang K, Rustagi A, McNevin J, McElrath MJ, and Gale M Jr. Vpu mediates depletion of interferon regulatory factor 3 during HIV infection by a lysosomedependent mechanism. J Virol 2012; 86: 8367-8374.
10. Doehle BP, Hladik F, McNevin JP, McElrath MJ, and Gale M Jr. Human immunodeficiency virus type 1 mediates global disruption of innate antiviral signaling and immune defenses within infected cells. J Virol 2009; 83: 10395-10405.
11. Escribese MM, Kraus T, Rhee E, Fernandez-Sesma A, Lopez CB, and Moran TM. Estrogen inhibits dendritic cell maturation to RNA viruses. Blood 2008; 112: 4574-4584.
12. Goila-Gaur R, and Strebel K. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 2008; 5: 51.
13. Goujon C, and Malim MH. Characterization of the alpha interferon-induced postentry block to HIV-1 infection in primary human macrophages and T cells. J Virol 2010; 84: 9254-9266.
14. Gupta S, Kumar N, Singhal N, Manektala U, Jain S, and Sodhani P. Cytohormonal and morphological alterations in cervicovaginal smears of postmenopausal women on hormone replacement therapy. Diagn Cytopathol 2006; 34: 676-681.
15. Harkonen PL, and Vaananen HK. Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann N Y Acad Sci 2006; 1089: 218-227.
16. Harman AN, Lai J, Turville S, et al. HIV infection of dendritic cells subverts the IFN induction pathway via IRF- 1 and inhibits type 1 IFN production. Blood 2011; 118: 298-308.
17. 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.
18. Heffron R, Mugo N, Ngure K, et al. Hormonal contraceptive use and risk of HIV-1 disease progression. Aids 2013; 27: 261-267.
19. Hel Z, Stringer E, and Mestecky J. Sex steroid hormones, hormonal contraception, and the immunobiology of human immunodeficiency virus-1 infection. Endocr Rev 2010; 31: 79-97.
20. Hrecka K, Hao C, Gierszewska M, et al. Vpx relieves inhibition of HIV-1 infection of macrophages mediated by the SAMHD1 protein. Nature 2011; 474: 658-661.
21. Hubacher D, Mavranezouli I, and McGinn E. Unintended pregnancy in sub-Saharan Africa: magnitude of the problem and potential role of contraceptive implants to alleviate it. Contraception 2008; 78: 73-78.
22. Kanda N, and Watanabe S. 17beta-estradiol inhibits the production of interferon-induced protein of 10 kDa by human keratinocytes. J Invest Dermatol 2003; 120: 411-419.
23. Karpuzoglu-Sahin E, Hissong BD, and Ansar Ahmed S. Interferon-gamma levels are upregulated by 17-betaestradiol and diethylstilbestrol. J Reprod Immunol 2001; 52: 113-127.
24. Kramer PR, Kramer SF, and Guan G. 17 beta-estradiol regulates cytokine release through modulation of CD16 expression in monocytes and monocyte-derived macrophages. Arthritis Rheum 2004; 50: 1967-1975.
25. Lengi AJ, Phillips RA, Karpuzoglu E, and Ahmed SA. Estrogen selectively regulates chemokines in murine splenocytes. J Leukoc Biol 2007; 81: 1065-1074.
26. Li X, Xu Y, Ma L, Sun L, Fu G, and Hou Y. 17betaestradiol enhances the response of plasmacytoid dendritic cell to CpG. PLoS One 20009; 4: e8412.
27. Liu X, Mosoian A, Li-Yun Chang T, et al. Gonococcal lipooligosaccharide suppresses HIV infection in human primary macrophages through induction of innate immunity. J Infect Dis 2006; 194: 751-759.
28. Lutalo T, Musoke R, Polis C, et al. Effects of hormonal contraceptive use on HIV acquisition in women and transmission to men among HIV-discordant couples, Rakai, Uganda, Abstract #563, 19th Conference on Retroviruses and Opportunistic Infections, Seattle, WA, 2012.
29. Malim MH, and Bieniasz PD. HIV Restriction Factors and Mechanisms of Evasion. Cold Spring Harb Perspect Med 2012; 2: a006940.
30. Marx PA, Spira AI, Gettie A, et al. Progesterone implants enhance SIV vaginal transmission and early virus load. Nat Med 1996; 2: 1084-1089.
31. McCoy S, Zheng W, Montgomery ET, et al. Oral and injectable contraception use and risk of HIV acquisition among women: MIRA study, p. 20LB, 19th Conference on Retroviruses and Opportunistic Infections, Seattle, WA, 2012.
32. Messingham KA, Heinrich SA, and Kovacs EJ. Estrogen restores cellular immunity in injured male mice via suppression of interleukin-6 production. J Leukoc Biol 2001; 70: 887-895.
33. Molander U, Milsom I, Ekelund P, Mellstrom D, and Eriksson O. Effect of oral oestriol on vaginal flora and cytology and urogenital symptoms in the post-menopause. Maturitas 1990; 12: 113-120.
34. Morrison CS, Skoler-Karpoff S, Kwok C. Hormonal contraception and the risk of HIV acquisition among women in South Africa. Aids 2012; 26: 497-504.
35. Mosoian A, Teixeira A, Burns CS, et al. Prothymosin-alpha inhibits HIV-1 via Toll-like receptor 4-mediated type I interferon induction. Proc Natl Acad Sci U S A 2010; 107: 10178-10183.
36. Nilsson K, Risberg B, and Heimer G. The vaginal epithelium in the postmenopause-cytology, histology and pH as methods of assessment. Maturitas 1995; 21: 51-56.
37. Okumura A, Alce T, Lubyova B, Ezelle H, Strebel K, and Pitha PM. HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 2008; 373: 85-97.
38. Pask AJ, McInnes KJ, Webb DR, and Short RV. Topical oestrogen keratinises the human foreskin and may help prevent HIV infection. PLoS One 2008; 3: e2308.
39. Peng G, Lei KJ, Jin W, Greenwell-Wild T, and Wahl SM. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J Exp Med 2006; 203: 41-46.
40. Plummer FA, Simonsen JN, Cameron DW, et al. Cofactors in male-female sexual transmission of human immunodeficiency virus type J Infect Dis 1991; 163: 233-239.
41. Rodriguez-Garcia M, Biswas N, Patel MV, et al. Estradiol reduces susceptibility of CD4 + T cells and macrophages to HIV-infection. PLoS One 2013; 8: e62069.
42. Rollenhagen C, and Asin SN. Enhanced HIV-1 replication in ex vivo ectocervical tissues from post-menopausal women correlates with increased inflammatory responses. Mucosal Immunol 2011; 4: 671-681.
43. Shen R, Richter HE, and Smith PD. Early HIV-1 target cells in human vaginal and ectocervical mucosa. Am J Reprod Immunol 2011; 65: 261-267.
44. Sikoski P, Register TC, Lees CJ, et al. Effects of two novel selective estrogen receptor modulators, raloxifene, tamoxifen, and ethinyl estradiol on the uterus, vagina and breast in ovariectomized cynomolgus monkeys (Macaca fascicularis). Am J Obstet Gynecol 2007; 196: 75 e71-77.
45. Smith SM, Baskin GB, and Marx PA. Estrogen protects against vaginal transmission of simian immunodeficiency virus. J Infect Dis 2000; 182: 708-715.
46. Straub RH. The complex role of estrogens in inflammation. Endocr Rev 2007; 28: 521-574.
47. Szotek EL, Narasipura SD, and Al-Harthi L. 17beta-Estradiol inhibits HIV-1 by inducing a complex formation between beta-catenin and estrogen receptor alpha on the HIV promoter to suppress HIV transcription. Virology 2013; 443: 375-383.
48. Tourgeman DE, Gentzchein E, Stanczyk FZ, and Paulson RJ. Serum and tissue hormone levels of vaginally and orally administered estradiol. Am J Obstet Gynecol 1999; 180: 1480-1483.
49. Trunova N, Tsai L, Tung S, et al. Progestin-based contraceptive suppresses cellular immune responses in SHIVinfected rhesus macaques. Virology 2006; 352: 169-177.
50. Wand H, and Ramjee G. The effects of injectable hormonal contraceptives on HIV seroconversion and on sexually transmitted infections. Aids 2012; 26: 375-380.
51. Wei P, Garber ME, Fang SM, . Fischer WH, and Jones KA. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 1998; 92: 451-462.
52. Wie SH, Du P, Luong TQ, et al. HIV Downregulates Interferon-Stimulated Genes in Primary Macrophages. J Interferon Cytokine Res 2013; 33: 90-95.
53. Zack JA, Arrigo SJ, Weitsman SR, et al. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990; 61: 213-222.
54. Zheng YH, Jeang KT, and Tokunaga K. Host restriction factors in retroviral infection: promises in virus-host interaction. Retrovirology 2012; 9: 112.