Journal of Clinical Immunology

, Volume 30, Issue 1, pp 90–98 | Cite as

Chemokine Expression Patterns in the Systemic and Genital Tract Compartments are Associated with HIV-1 Infection in Women from Benin

  • Julie Lajoie
  • Johanne Poudrier
  • Marguerite Massinga Loembe
  • Fernand Guédou
  • François Leblond
  • Annie-Claude Labbé
  • Michel Alary
  • Michel Roger
Article

Abstract

Introduction

Understanding the genital mucosal immunity and the factors involved in linking innate to adaptive immunity is crucial for the design of efficient preventive strategies against human immunodeficiency virus (HIV)-1.

Methods

Levels of both genital mucosal and blood chemokines were compared between 58 HIV-1-uninfected and 50 HIV-1-infected female commercial sex workers (CSWs) as well as 53 HIV-1-uninfected non-CSW control women at low risk for exposure, recruited in Cotonou, Benin.

Results

HIV-1-infected CSWs had significantly higher blood and genital levels of monocyte chemotactic protein (MCP-3/CCL7) and monokine induced by gamma interferon (MIG/CXCL9) compared with those in both the HIV-1-uninfected CSW and non-CSW groups. In the HIV-1-infected group, levels of MCP-3 and MIG were significantly higher in the genital mucosa than in the blood. However, the blood levels of macrophage inflammatory protein (MIP-1a/CCL3) and MIP-1b/CCL4 were higher in HIV-1-uninfected CSWs compared with those in the other groups.

Conclusion

Increased production of chemokines in the genital tract may favour the recruitment of HIV-1 target cells causing a mucosal environment that promotes viral replication and dissemination, whereas higher expression of β-chemokines at the systemic level is associated with protection from HIV-1 infection.

Keywords

Africa chemokine female genital tract HIV immunity mucosal and systemic 

References

  1. 1.
    Haynes BF, Shattock RJ. Critical issues in mucosal immunity for HIV-1 vaccine development. J Allergy Clin Immunol. 2008;122:3–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Padian NS, van der Straten A, Ramjee G, Chipato T, de Bruyn G, Blanchard K, et al. Diaphragm and lubricant gel for prevention of HIV acquisition in Southern African women: a randomised controlled trial. Lancet. 2007;370:251–61.CrossRefPubMedGoogle Scholar
  3. 3.
    Hel Z, McGhee JR, Mestecky J. HIV infection: first battle decides the war. Trends Immunol. 2006;27:274–81.CrossRefPubMedGoogle Scholar
  4. 4.
    Glass WG, Rosenberg HF, Murphy PM. Chemokine regulation of inflammation during acute viral infection. Curr Opin Allergy Clin Immunol. 2003;3:467–73.CrossRefPubMedGoogle Scholar
  5. 5.
    Colobran R, Adreani P, Ashhab Y, Llano A, Esté JA, Dominguez O, et al. Multiple products derived from two CCL4 loci: high incidence of a new polymorphism in HIV positive patients. J Immunol. 2005;174:5655–64.PubMedGoogle Scholar
  6. 6.
    Gonzalez E, Kulkarni H, Bolivar H, Mangano A, Sanchez R, Catano G, et al. The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science. 2005;307:1434–40.CrossRefPubMedGoogle Scholar
  7. 7.
    Iqbal SM, Ball TB, Kimani J, Thottingal P, Embree JE, Fowke KR, et al. Elevated T cell counts and RANTES expression in the genital mucosa of HIV-1-resistant Kenyan commercial sex workers. J Infect Dis. 2005;192:728–38.CrossRefPubMedGoogle Scholar
  8. 8.
    Hirbod T, Nilsson J, Andersson S, Uberti-Foppa C, Ferrari D, Maghi M, et al. Upregulation of interferon-α and RANTES in the cervix of HIV-1 seronegative women with high-risk behavior. J Acquir Immune Defic Syndr. 2006;43:137–43.CrossRefPubMedGoogle Scholar
  9. 9.
    Kaul R, Rebbapragada A, Hirbod T, Wachihi C, Ball TB, Plummer FA, et al. Genital levels of soluble immune factors with anti-HIV activity may correlate with increased HIV susceptibility. AIDS. 2008;22:2049–51.CrossRefPubMedGoogle Scholar
  10. 10.
    Campbell GR, Spector SA. CCL2 increases X4-tropic HIV-1 entry into resting CD4+ T Cells. J Biol Chem. 2008;283:30745–53.CrossRefPubMedGoogle Scholar
  11. 11.
    Brainard DM, Tager AM, Misdraji J, Frahm N, Lichterfeld M, Draeneret R, et al. Decreased CXCR3+ CD8 T cells in advanced human immunodeficiency virus infection suggest that a homing defect contributes to cytotoxic T-lymphocyte dysfunction. J Virol. 2007;81:8439–50.CrossRefPubMedGoogle Scholar
  12. 12.
    Lajoie J, Poudrier J, Massinga-Loembe M, Guédou F, Agossa-Gbenafa C, Labbé AC, et al. Differences in immunoregulatory cytokine expression patterns in the systemic and genital tract compartments of HIV-1 infected commercial sex workers in Benin. Mucosal Immunol. 2008;1:309–16.CrossRefPubMedGoogle Scholar
  13. 13.
    Gumbi PP, Nkwanyana NN, Bere A, Burgers WA, Gray CM, Williamson AC, et al. Impact of inflammation on cervical human immunodeficiency virus (HIV-1)-specific DC8 T-cell responses in the female genital tract during chronic HIV infection. J Virol. 2008;82:8529–36.CrossRefPubMedGoogle Scholar
  14. 14.
    Wira CR, Fahey JV, Sentman CL, Pioli PA, Shen L. Innate and adaptive immunity in female genital tract: cellular responses and interactions. Immunol Rev. 2005;206:306–35.CrossRefPubMedGoogle Scholar
  15. 15.
    Sugaya M, Loré K, Koup RA, Douek DC, 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. 2004;172:2219–24.PubMedGoogle Scholar
  16. 16.
    Sharkey DJ, Macpherson AM, Tremellen KP, Robertson SA. Seminal plasma differentially regulates inflammatory cytokine gene expression in human cervical and vaginal epithelial cells. Mol Hum Reprod. 2007;13:491–501.CrossRefPubMedGoogle Scholar
  17. 17.
    Cohen CR, Plummer FA, Mugo N, Maclean L, Shen C, Bukosi EA, et al. Increased interleukin-10 in the endocervical secretions of women with non-ulcerative sexually transmitted diseases: a mechanism for enhanced HIV-1 transmission? AIDS. 1999;13:327–32.CrossRefPubMedGoogle Scholar
  18. 18.
    Boulton IC, Gray-Owen SD. Neisserial binding to CEACAM-1 arrests the activation and proliferation of CD4+ T lymphocytes. Nat Immunol. 2002;3:229–36.CrossRefPubMedGoogle Scholar
  19. 19.
    Fichorova RN, Desai PJ, Gibson FC, Genco CA. Distinct proinflammatory host responses to Neisseria Gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect Immun. 2001;69:5840–8.CrossRefPubMedGoogle Scholar
  20. 20.
    Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS. 2006;20:73–83.CrossRefPubMedGoogle Scholar
  21. 21.
    Rebbapragada A, Wachihi C, Pettengell C, Sunderji S, Huibner S, Jaoko W, et al. Negative mucosal synergy between herpes simplex type 2 and HIV in the female genital tract. AIDS. 2007;21:589–98.CrossRefPubMedGoogle Scholar
  22. 22.
    Kaul R, Plummer FA, Kimani J, Dong T, Kiama P, Rostron T, et al. HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1-resistant prostitutes in Nairobi. J Immunol. 2000;164:1602–11.PubMedGoogle Scholar
  23. 23.
    Kaul R, Trabattoni D, Bwayo JJ, Arienti D, Zagliani A, Mwanji FM, et al. HIV-1-specific mucosal IgA in a cohort of HIV-1-resistant Kenyan sex workers. AIDS. 1999;13:23–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Devito C, Hinkula J, Kaul R, Kimani J, Kiama P, Lopalco L, et al. Cross-clade HIV-1-specific neutralizing IgA in mucosal and systemic compartments of HIV-1-exposed, persistently seronegative subjects. J Acquir Immune Defic Syndr. 2002;30:413–20.PubMedGoogle Scholar
  25. 25.
    Suresh P, Wanchu A, Bhatnagar A, Sachdeva RK, Sharma M. Spontaneous and antigen-induced chemokine production in exposed but uninfected partners of HIV type 1-infected individuals in North India. AIDS Res Hum Retroviruses. 2007;23:261–8.CrossRefPubMedGoogle Scholar
  26. 26.
    Schall TJ, Bacon K, Camp RD, Kaspari JW, Goeddel DV. Human macrophage inflammatory protein alpha (MIP-1 alpha) and MIP-1 beta chemokines attract distinct populations of lymphocytes. J Exp Med. 1993;177:1821–6.CrossRefPubMedGoogle Scholar
  27. 27.
    Lillard JW, Singh UP, Boyaka PN, Singh S, Taub DD, McGhee JR. MIP-1 alpha and MIP-1 beta differentially mediate mucosal and systemic adaptive immunity. Blood. 2003;101:807–14.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Julie Lajoie
    • 1
    • 2
  • Johanne Poudrier
    • 1
    • 2
  • Marguerite Massinga Loembe
    • 3
    • 4
  • Fernand Guédou
    • 4
  • François Leblond
    • 5
  • Annie-Claude Labbé
    • 5
  • Michel Alary
    • 4
  • Michel Roger
    • 1
    • 2
  1. 1.Laboratoire d’immunogénétiqueCentre de Recherche du Centre Hospitalier de l’Université de Montréal (CRCHUM)MontrealCanada
  2. 2.Département de Microbiologie et ImmunologieHôpital Notre-Dame du Centre Hospitalier de l’Université de Montréal (CHUM)MontréalCanada
  3. 3.Laboratory of ImmunologyInstitute of Tropical MedicineAntwerpBelgium
  4. 4.Unité de Recherche en Santé des PopulationsCentre hospitalier affilié universitaire de Québec and Université LavalQuébecCanada
  5. 5.Département de Microbiologie de l’hôpital Maisonneuve-RosemontMontréalCanada

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