Stable CD4 expression and local immune activation in the ectocervical mucosa of HIV-infected women

Journal of Immunology

Volumn 191, Issue 7, 2013, Pages 3948-3954

  Hirbod, Taha ^a   Kimani, Joshua ^b   Tjernlund, Annelie ^a   Cheruiyot, Juliana ^b   Petrova, Anna ^a   Ball, Terry B ^c,d   Mugo, Nelly ^b   Jaoko, Walter ^b   Plummer, Francis A ^c,d   Kaul, Rupert ^e   Broliden, Kristina ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF NAIROBI   (Kenya)

^c UNIVERSITY OF MANITOBA   (Canada)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; CD3 ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR CCR5; GAMMA INTERFERON; HORMONE; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 3; INTERLEUKIN 22; INTERLEUKIN 6; LANGERIN; MANNOSE RECEPTOR; MESSENGER RNA;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CD4 LYMPHOCYTE COUNT; CELL SPECIFICITY; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE DURATION; ETHNIC GROUP; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IMMUNOSTIMULATION; INFECTION RISK; INTESTINE MUCOSA; KENYA; KENYAN; NONHUMAN; PRIORITY JOURNAL; PROSTITUTION; PROTEIN DEPLETION; RISK ASSESSMENT; SEXUAL BEHAVIOR; UPREGULATION; UTERINE CERVIX BIOPSY; UTERINE CERVIX MUCOSA; VIRUS CELL INTERACTION; VIRUS LOAD;

ADULT; ANTIGENS, CD4; BIOLOGICAL MARKERS; CD4 LYMPHOCYTE COUNT; CERVIX UTERI; CYTOKINES; FEMALE; GENE EXPRESSION; HIV INFECTIONS; HIV-1; HUMANS; MIDDLE AGED; MUCOUS MEMBRANE; SEX WORKERS; YOUNG ADULT;

EID: 84885129867     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301220     Document Type: Article

References (41)

1. + T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J. Virol. 77:11708-11717.
2. + T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200:761-770.
3. Marchetti, G., C. Tincati, and G. Silvestri. 2013. Microbial translocation in the pathogenesis of HIV infection and AIDS. Clin. Microbiol. Rev. 26:2-18.
4. Brenchley, J. M., D. A. Price, T. W. Schacker, T. E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, D. Altmann, et al. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12:1365-1371.
5. Kamat, B. R., and P. G. Isaacson. 1987. The immunocytochemical distribution of leukocytic subpopulations in human endometrium. Am. J. Pathol. 127:66-73.
6. Poppe, W. A., M. Drijkoningen, P. S. Ide, J. M. Lauweryns, and F. A. Van Assche. 1998. Lymphocytes and dendritic cells in the normal uterine cervix: an immunohistochemical study. Eur. J. Obstet. Gynecol. Reprod. Biol. 81:277-282.
7. Hladik, F., P. Sakchalathorn, L. Ballweber, G. Lentz, M. Fialkow, D. Eschenbach, and M. J. McElrath. 2007. Initial events in establishing vaginal entry and infection by human immunodeficiency virus type-1. Immunity 26:257-270.
8. Hirbod, T., T. Kaldensjö, and K. Broliden. 2011. In situ distribution of HIV-binding CCR5 and C-type lectin receptors in the human endocervical mucosa. PLoS ONE 6:e25551.
9. Hirbod, T., T. Kaldensjö, L. Lopalco, E. Klareskog, S. Andersson, C. Uberti-Foppa, D. Ferrari, M. Manghi, J. Andersson, K. Loré, and K. Broliden. 2009. Abundant and superficial expression of C-type lectin receptors in ectocervix of women at risk of HIV infection. J. Acquir. Immune Defic. Syndr. 51:239-247.
10. Kaldensjö, T., P. Petersson, A. Tolf, G. Morgan, K. Broliden, and T. Hirbod. 2011. Detection of intraepithelial and stromal Langerin and CCR5 positive cells in the human endometrium: potential targets for HIV infection. PLoS ONE 6:e21344.
11. + Th1 phenotype. J. Immunol. 163:2306-2313.
12. + T cell subset coexpressing multiple markers of HIV susceptibility. J. Immunol. 187:6032-6042.
13. Prakash, M., M. S. Kapembwa, F. Gotch, and S. Patterson. 2002. Oral contraceptive use induces upregulation of the CCR5 chemokine receptor on CD4+ T cells in the cervical epithelium of healthy women. J. Reprod. Immunol. 54:117-131.
14. Zhang, Y. J., T. Dragic, Y. Cao, L. Kostrikis, D. S. Kwon, D. R. Littman, V. N. KewalRamani, and J. P. Moore. 1998. Use of coreceptors other than CCR5 by non-syncytium-inducing adult and pediatric isolates of human immunodeficiency virus type 1 is rare in vitro. J. Virol. 72:9337-9344.
15. de Witte, L., A. Nabatov, M. Pion, D. Fluitsma, M. A. de Jong, T. de Gruijl, V. Piguet, Y. van Kooyk, and T. B. Geijtenbeek. 2007. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat. Med. 13:367-371.
16. Geijtenbeek, T. B., D. S. Kwon, R. Torensma, S. J. van Vliet, G. C. van Duijnhoven, J. Middel, I. L. Cornelissen, H. S. Nottet, V. N. KewalRamani, D. R. Littman, et al. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587-597.
17. Nguyen, D. G., and J. E. Hildreth. 2003. Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages. Eur. J. Immunol. 33:483-493.
18. Kaushic, C., V. H. Ferreira, J. K. Kafka, and A. Nazli. 2010. HIV infection in the female genital tract: discrete influence of the local mucosal microenvironment. Am. J. Reprod. Immunol. 63:566-575.
19. + cell counts in women with acute HIV-1 infection. J. Infect. Dis. 198:710-714.
20. Roberts, L., J. A. Passmore, K. Mlisana, C. Williamson, F. Little, L. M. Bebell, G. Walzl, M. R. Abrahams, Z. Woodman, Q. Abdool Karim, and S. S. Abdool Karim. 2012. Genital tract inflammation during early HIV-1 infection predicts higher plasma viral load set point in women. J. Infect. Dis. 205:194-203.
21. Mitchell, C., J. Hitti, K. Paul, K. Agnew, S. E. Cohn, A. E. Luque, and R. Coombs. 2011. Cervicovaginal shedding of HIV type 1 is related to genital tract inflammation independent of changes in vaginal microbiota. AIDS Res. Hum. Retroviruses 27:35-39.
22. Introini, A., C. Vanpouille, A. Lisco, J. C. Grivel, and L. Margolis. 2013. Interleukin-7 facilitates HIV-1 transmission to cervico-vaginal tissue ex vivo. PLoS Pathog. 9:e1003148.
23. Nazli, A., O. Chan, W. N. Dobson-Belaire, M. Ouellet, M. J. Tremblay, S. D. Gray-Owen, A. L. Arsenault, and C. Kaushic. 2010. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog. 6:e1000852.
24. Fowke, K. R., N. J. Nagelkerke, J. Kimani, J. N. Simonsen, A. O. Anzala, J. J. Bwayo, K. S. MacDonald, E. N. Ngugi, and F. A. Plummer. 1996. Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 348:1347-1351.
25. Hasselrot, K., J. Cheruiyot, J. Kimani, T. B. Ball, R. Kaul, and T. Hirbod. 2012. Feasibility and safety of cervical biopsy sampling for mucosal immune studies in female sex workers from Nairobi, Kenya. PLoS One 7:e47570.
26. Embree, J. E., S. Njenga, P. Datta, N. J. Nagelkerke, J. O. Ndinya-Achola, Z. Mohammed, S. Ramdahin, J. J. Bwayo, and F. A. Plummer. 2000. Risk factors for postnatal mother-child transmission of HIV-1. AIDS 14:2535-2541.
27. Hobbs, M. M., M. J. Steiner, K. D. Rich, M. F. Gallo, L. Warner, and M. Macaluso. 2010. Vaginal swab specimen processing methods influence performance of rapid semen detection tests: a cautionary tale. Contraception 82:291-295.
28. Hirbod, T., R. C. Bailey, K. Agot, S. Moses, J. Ndinya-Achola, R. Murugu, J. Andersson, J. Nilsson, and K. Broliden. 2010. Abundant expression of HIV target cells and C-type lectin receptors in the foreskin tissue of young Kenyan men. Am. J. Pathol. 176:2798-2805.
29. Brismar Wendel, S., T. Kaldensjö, P. Peterson, S. Andersson, K. Broliden, and T. Hirbod. 2010. Slumbering mucosal immune response in the cervix of human papillomavirus DNA-positive and -negative women. Int. J. Oncol. 37:1565-1573.
30. (-ΔΔC (T)) Method. Methods 25:402-408.
31. Lajoie, J., J. Juno, A. Burgener, S. Rahman, K. Mogk, C. Wachihi, J. Mwanjewe, F. A. Plummer, J. Kimani, T. B. Ball, and K. R. Fowke. 2012. A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Mucosal Immunol. 5:277-287.
32. Mukura, L. R., M. Ghosh, J. V. Fahey, S. Cu-Uvin, and C. R. Wira. 2012. Genital tract viral load in HIV type 1-positive women correlates with specific cytokine levels in cervical-vaginal secretions but is not a determinant of infectious virus or anti-HIV activity. AIDS Res. Hum. Retroviruses 28:1533-1539.
33. Nkwanyana, N. N., P. P. Gumbi, L. Roberts, L. Denny, W. Hanekom, A. Soares, B. Allan, A. L. Williamson, D. Coetzee, A. J. Olivier, et al. 2009. Impact of human immunodeficiency virus 1 infection and inflammation on the composition and yield of cervical mononuclear cells in the female genital tract. Immunology 128(Suppl. 1):e746-e757.
34. + T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
35. + T cell depletion and viral replication in SIV infection. Science 280:427-431.
36. + regulatory T cells. J. Infect. Dis. 199:1318-1322.
37. + T cell compartment and reduced expression of HIV-dependent host factors. J. Infect. Dis. 202(Suppl. 3):S339-S344.
38. Chege, D., Y. Chai, S. Huibner, T. Kain, C. Wachihi, M. Kimani, S. Barasa, L. R. McKinnon, F. K. Muriuki, A. Kariri, et al. 2012. Blunted IL17/IL22 and pro-inflammatory cytokine responses in the genital tract and blood of HIV-exposed, seronegative female sex workers in Kenya. PLoS One 7:e43670.
39. Meditz, A. L., M. K. Haas, J. M. Folkvord, K. Melander, R. Young, M. McCarter, S. Mawhinney, T. B. Campbell, Y. Lie, E. Coakley, et al. 2011. HLA-DR+CD38+ CD4+ T lymphocytes have elevated CCR5 expression and produce the majority of R5-tropic HIV-1 RNA in vivo. J. Virol. 85:10189-10200.
40. Baeten, J. M., E. Kahle, J. R. Lingappa, R. W. Coombs, S. Delany-Moretlwe, E. Nakku-Joloba, N. R. Mugo, A. Wald, L. Corey, D. Donnell, et al. 2011. Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci. Transl. Med. 3:77ra29.
41. Jaspan, H. B., L. Liebenberg, W. Hanekom, W. Burgers, D. Coetzee, A. L. Williamson, F. Little, L. Myer, R. W. Coombs, D. Sodora, and J. A. Passmore. 2011. Immune activation in the female genital tract during HIV infection predicts mucosal CD4 depletion and HIV shedding. J. Infect. Dis. 204:1550-1556.