Productive HIV-1 infection of human cervical tissue ex vivo is associated with the secretory phase of the menstrual cycle

Mucosal Immunology

Volumn 6, Issue 6, 2013, Pages 1081-1090

  Saba, E ^a,b   Origoni, M ^a,b   Taccagni, G ^a   Ferrari, D ^a   Doglioni, C ^a   Nava, A ^a   Lisco, A ^c,d   Grivel, J C ^c   Margolis, L ^c   Poli, G ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOMETRIUM ATROPHY; EX VIVO STUDY; EXPLANT; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; INFECTION SENSITIVITY; MACROPHAGE; MENSTRUAL CYCLE; PRIORITY JOURNAL; VIRUS REPLICATION;

ADULT; AGED; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CERVIX UTERI; CHEMOKINE CCL3; CHEMOKINE CCL5; DNA, VIRAL; FEMALE; HIV CORE PROTEIN P24; HIV INFECTIONS; HIV-1; HUMANS; LUTEAL PHASE; MACROPHAGES; MIDDLE AGED; ORGAN CULTURE TECHNIQUES; VIRULENCE;

EID: 84886031967     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2013.2     Document Type: Article

References (50)

1. Lisco, A. et al. Semen of HIV-1-infected individuals: Local shedding of herpesviruses and reprogrammed cytokine network. J. Infect. Dis. 205, 97-105 (2012).
2. Grivel, J.C., Shattock, R.J. & Margolis, L.B. Selective transmission of R5 HIV-1 variants: Where is the gatekeeper? J. Transl. Med. 9 (Suppl 1), S6 (2011).
3. Abdool Karim, Q. et al. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 329, 1168-1174 (2010).
4. Quinones-Mateu, M.E. & Vanham, G. HIV microbicides: Where are we now? Curr. HIV Res. 10, 1-2 (2012).
5. Sugaya, M., Lore, K., Koup, R.A., Douek, D.C. & Blauvelt, A. HIV-infected Langerhans cells preferentially transmit virus to proliferating autologous CD4+ memory T cells located within Langerhans cell-T cell clusters. J. Immunol. 172, 2219-2224 (2004).
6. Shen, R. et al. Macrophages in vaginal but not intestinal mucosa are monocyte-like and permissive to human immunodeficiency virus type 1 infection. J. Virol. 83, 3258-3267 (2009).
7. Duncan, C.J. & Sattentau, Q.J. Viral determinants of HIV-1 macrophage tropism. Viruses 3, 2255-2279 (2011).
8. Wira, C.R., Fahey, J.V., Sentman, C.L., Pioli, P.A. & Shen, L. Innate and adaptive immunity in female genital tract: Cellular responses and interactions. Immunol. Rev. 206, 306-335 (2005).
9. Sun, L. et al. Human beta-defensins suppress human immunodeficiency virus infection: Potential role in mucosal protection. J. Virol. 79, 14318-14329 (2005).
10. Wira, C.R., Patel, M.V., Ghosh, M., Mukura, L. & Fahey, J.V. Innate immunity in the human female reproductive tract: Endocrine regulation of endogenous antimicrobial protection against HIV and other sexually transmitted infections. Am. J. Reprod. Immunol. 65, 196-211 (2011).
11. Keller, M.J. et al. PRO 2000 elicits a decline in genital tract immune mediators without compromising intrinsic antimicrobial activity. AIDS 21, 467-476 (2007).
12. Wira, C.R. & Fahey, J.V. A new strategy to understand how HIV infects women: Identification of a window of vulnerability during the menstrual cycle. AIDS 22, 1909-1917 (2008).
13. 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. 63, 544-565 (2010).
14. Hel, Z., Stringer, E. & Mestecky, J. Sex steroid hormones, hormonal contraception, and the immunobiology of human immunodeficiency virus-1 infection. Endocr. Rev. 31, 79-97 (2010).
15. Wicherek, L. et al. The characterization of the subpopulation of suppressive B7H4(+) macrophages and the subpopulation of CD25(+) CD4(+) and FOXP3(+) regulatory T-cells in decidua during the secretory cycle phase, Arias Stella reaction, and spontaneous abortion-A preliminary report. Am. J. Reprod. Immunol. 61, 303-312 (2009).
16. Chao, K.H., Wu, M.Y., Chen, M.J., Hung, C.C. & Ho, H.N. Impact of the menstrual cycle on immunologic markers in HIV-infected Taiwanese women. Taiwan J. Obstet. Gynecol. 45, 42-47 (2006).
17. Vishwanathan, S.A. et al. High susceptibility to repeated, low-dose, vaginal SHIV exposure late in the luteal phase of the menstrual cycle of pigtail macaques. J. Acquir. Immune Defic. Syndr. 57, 261-264 (2011).
18. Poonia, B. et al. Cyclic changes in the vaginal epithelium of normal rhesus macaques. J. Endocrinol. 190, 829-835 (2006).
19. Heffron, R. et al. Use of hormonal contraceptives and risk of HIV-1 transmission: A prospective cohort study. Lancet Infect. Dis. 12, 19-26 (2012).
20. Tebit, D.M., Ndembi, N., Weinberg, A. & Quinones-Mateu, M.E. Mucosal transmission of human immunodeficiency virus. Curr. HIV Res. 10, 3-8 (2012).
21. Greenhead, P. et al. Parameters of human immunodeficiency virus infection of human cervical tissue and inhibition by vaginal virucides. J. Virol. 74, 5577-5586 (2000).
22. Saba, E. et al. HIV-1 sexual transmission: Early events of HIV-1 infection of human cervico-vaginal tissue in an optimized ex vivo model. Mucosal Immunol. 3, 280-290 (2010).
23. Thompson, K.A., Cherry, C.L., Bell, J.E. & McLean, C.A. Brain cell reservoirs of latent virus in presymptomatic HIV-infected individuals. Am. J. Pathol. 179, 1623-1629 (2011).
24. Alexaki, A., Liu, Y. Wigdahl, B. Cellular reservoirs of HIV-1 and their role in viral persistence. Curr. HIV Res. 6, 388-400 (2008).
25. Vicenzi, E. et al. Divergent regulation of HIV-1 replication in PBMC of infected individuals by CC chemokines: Suppression by RANTES, MIP-1alpha, and MCP-3, and enhancement by MCP-1. J. Leukoc. Biol. 68, 405-412 (2000).
26. Fantuzzi, L. et al. Endogenous CCL2 (monocyte chemotactic protein-1) modulates human immunodeficiency virus type-1 replication and affects cytoskeleton organization in human monocyte-derived macrophages. Blood 102, 2334-2337 (2003).
27. Shen, R., Richter, H.E. & Smith, P.D. Early HIV-1 target cells in human vaginal and ectocervical mucosa. Am. J. Reprod. Immunol. 65, 261-267 (2011).
28. Pohlmann, S., Baribaud, F. & Doms, R.W. DC-SIGN and DC-SIGNR: Helping hands for HIV. Trends Immunol. 22, 643-646 (2001).
29. Geijtenbeek, T.B. & van Kooyk, Y. DC-SIGN: A novel HIV receptor on DCs that mediates HIV-1 transmission. Curr. Top. Microbiol. Immunol. 276, 31-54 (2003).
30. Gringhuis, S.I. et al. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 11, 419-426 (2010).
31. Berzi, A. et al. A glycomimetic compound inhibits DC-SIGN-mediated HIV infection in cellular and cervical explant models. AIDS 26, 127-137 (2012).
32. Lehner, T. The role of CCR5 chemokine ligands and antibodies to CCR5 coreceptors in preventing HIV infection. Trends Immunol. 23, 347-351 (2002).
33. Iqbal, S.M. et al. Elevated T cell counts and RANTES expression in the genital mucosa of HIV-1-resistant Kenyan commercial sex workers. J. Infect. Dis. 192, 728-738 (2005).
34. Swingler, S. et al. HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat. Med. 5, 997-1003 (1999).
35. Dai, L. & Stevenson,M. A novel motif in HIV-1 Nef that regulates MIP-1beta chemokine release in macrophages. J. Virol. 84, 8327-8331 (2010).
36. D'Aversa, T.G., Yu, K.O. & Berman, J.W. Expression of chemokines by human fetal microglia after treatment with the human immunodeficiency virus type 1 protein Tat. J. Neurovirol. 10, 86-97 (2004).
37. Choe, W., Volsky, D.J. & Potash, M.J. Induction of rapid and extensive beta-chemokine synthesis in macrophages by human immunodeficiency virus type 1 and gp120, independently of their coreceptor phenotype. J. Virol. 75, 10738-10745 (2001).
38. Sheffield, J.S., Wendel, G.D. Jr., McIntire, D.D. & Norgard, M.V. The effect of progesterone levels and pregnancy on HIV-1 coreceptor expression. Reprod. Sci. 16, 20-31 (2009).
39. Meditz, A.L. et al. CCR5 expression is elevated on endocervical CD4+ T cells in healthy postmenopausal women. J. Acquir. Immune Defic. Syndr. 59, 221-228 (2012).
40. Salle, B. et al. Infection of macaques after vaginal exposure to cell-Associated simian immunodeficiency virus. J. Infect. Dis. 202, 337-344 (2010).
41. Ma, Z., Lu, F.X., Torten, M. & Miller, C.J. The number and distribution of immune cells in the cervicovaginal mucosa remain constant throughout the menstrual cycle of rhesus macaques. Clin. Immunol. 100, 240-249 (2001).
42. Ghosh, M. et al. Anti-HIV activity in cervical-vaginal secretions from HIVpositive and -negative women correlate with innate antimicrobial levels and IgG antibodies. PloS One 5, e11366 (2010).
43. Han, J.H. et al. Modulation of human beta-defensin-2 expression by 17beta-estradiol and progesterone in vaginal epithelial cells. Cytokine 49, 209-214 (2010).
44. Weinberg, A., Quinones-Mateu, M.E. & Lederman, M.M. Role of human beta-defensins in HIV infection. Adv. Dent. Res. 19, 42-48 (2006).
45. Grivel, J.C. & Margolis, L. Use of human tissue explants to study human infectious agents. Nat. Protoc. 4, 256-269 (2009).
46. Koup, R.A., Ho, D.D., Poli, G. & Fauci, A.S. Isolation and quantitation ofHIV in peripheral blood. Curr. Protoc. Immunol. Chapter 12, 12.2, 1-11 (2001).
47. Glushakova, S., Baibakov, B., Margolis, L.B. & Zimmerberg, J. Infection of human tonsil histocultures: A model for HIV pathogenesis. Nat. Med. 1, 1320-1322 (1995).
48. Vicenzi, E., Panina-Bodignon, P., Vallanti, G., Di Lucia, P. & Poli, G. Restricted replication of primary HIV-1 isolates using both CCR5 and CXCR4 in Th2 but not in Th1 CD4(+) T cells. J. Leukoc. Biol. 72, 913-920 (2002).
49. Collin, M. & Gordon, S. The kinetics of human immunodeficiency virus reverse transcription are slower in primary human macrophages than in a lymphoid cell line. Virology 200, 114-120 (1994).
50. Biancotto, A. et al. A highly sensitive and dynamic immunofluorescent cytometric bead assay for the detection of HIV-1 p24. J. Virol. Methods 157, 98-101 (2009).