Induction of Innate Immune Responses in the Female Genital Tract: Friend or Foe of HIV-1 Infection?

American Journal of Reproductive Immunology

Volumn 65, Issue 3, 2011, Pages 344-351

  Firoz Mian, M ^a   Ashkar, Ali A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Antiviral immunity; HIV 1; Mucosal innate immunity; TLR ligand; Type I IFNs

Indexed keywords

ANTIVIRUS AGENT; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMIDAZOQUINOLINE DERIVATIVE; INTERFERON; LOXORIBINE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR AGONIST;

COMPREHENSION; FEMALE; FEMALE GENITAL SYSTEM; HETEROSEXUALITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNITY; INNATE IMMUNITY; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS INFECTION; VIRUS REPLICATION;

ANTIVIRAL AGENTS; FEMALE; GENITALIA, FEMALE; HERPES SIMPLEX; HERPESVIRUS 2, HUMAN; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTERFERONS; MUCOUS MEMBRANE; TOLL-LIKE RECEPTORS;

EID: 79551647083     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2010.00945.x     Document Type: Review

References (78)

1. UNAIDS: Report on AIDS Epidemic. July 2008.
2. Royce RA, Sena A, Cates W Jr, Cohen MS: Sexual transmission of HIV. N Engl J Med 1997; 336:1072-1078.
3. Polgreen PM, Xiang J, Chang Q, Stapleton JT: GB virus type C/hepatitis G virus: a non-pathogenic flavivirus associated with prolonged survival in HIV-infected individuals. Microbes Infect 2003; 5:1255-1261.
4. Watt G, Kantipong P, de Souza M, Chanbancherd P, Jongsakul K, Ruangweerayud R, Loomis-Price LD, Polonis V, Myint KS, Birx DL, Brown AE, Krishna S: HIV-1 suppression during acute scrub-typhus infection. Lancet 2000; 356:475-479.
5. Watt G, Kantipong P, Jongsakul K: Decrease in human immunodeficiency virus type 1 load during acute dengue fever. Clin Infect Dis 2003; 36:1067-1069.
6. Moss WJ, Ryon JJ, Monze M, Cutts F, Quinn TC, Griffin DE: Suppression of human immunodeficiency virus replication during acute measles. J Infect Dis 2002; 185:1035-1042.
7. Fleming DT, Wasserheit JN: From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999; 75:3-17.
8. Cohen MS: HIV and sexually transmitted diseases: lethal synergy. Top HIV Med 2004; 12:104-107.
9. Hester RA, Kennedy SB: Candida infection as a risk factor for HIV transmission. J Womens Health (Larchmt) 2003; 12:487-494.
10. Wasserheit JN: Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 19:61-77.
11. de Jong MA, de Witte L, Taylor ME, Geijtenbeek TB: Herpes simplex virus type 2 enhances HIV-1 susceptibility by affecting Langerhans cell function. J Immunol 2010; 185:1633-1641.
12. 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.
13. Rebbapragada A, Wachihi C, Pettengell C, Sunderji S, Huibner S, Jaoko W, Ball B, Fowke K, Mazzulli T, Plummer FA, Kaul R: Negative mucosal synergy between Herpes simplex type 2 and HIV in the female genital tract. AIDS 2007; 21:589-598.
14. King AE, Critchley HO, Kelly RW: Presence of secretory leukocyte protease inhibitor in human endometrium and first trimester decidua suggests an antibacterial protective role. Mol Hum Reprod 2000; 6:191-196.
15. King AE, Fleming DC, Critchley HO, Kelly RW: Differential expression of the natural antimicrobials, beta-defensins 3 and 4, in human endometrium. J Reprod Immunol 2003; 59:1-16.
16. Ganz T, Lehrer RI: Defensins. Pharmacol Ther 1995; 66:191-205.
17. Ghosh M, Fahey JV, Shen Z, Lahey T, Cu-Uvin S, Wu Z, Mayer K, Wright PF, Kappes JC, Ochsenbauer C, Wira CR: Anti-HIV activity in cervical-vaginal secretions from HIV-positive and -negative women correlate with innate antimicrobial levels and IgG antibodies. PLoS ONE 2010; 5:e11366.
18. Ghosh M, Shen Z, Fahey JV, Cu-Uvin S, Mayer K, Wira CR: Trappin-2/Elafin: a novel innate anti-human immunodeficiency virus-1 molecule of the human female reproductive tract. Immunology 2010; 129:207-219.
19. Hladik F, McElrath MJ: Setting the stage: host invasion by HIV. Nat Rev Immunol 2008; 8:447-457.
20. 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; 206:306-335.
21. Wira CR, Grant-Tschudy KS, Crane-Godreau MA: Epithelial cells in the female reproductive tract: a central role as sentinels of immune protection. Am J Reprod Immunol 2005; 53:65-76.
22. Quayle AJ: The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J Reprod Immunol 2002; 57:61-79.
23. Wira CR, Fahey JV, Ghosh M, Patel MV, Hickey DK, Ochiel DO: 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 2010; 63:544-565.
24. Ochiel DO, Fahey JV, Ghosh M, Haddad SN, Wira CR: Innate immunity in the female reproductive tract: role of sex hormones in regulating uterine epithelial cell protection against pathogens. Curr Womens Health Rev 2008; 4:102-117.
25. Smith SM, Mefford M, Sodora D, Klase Z, Singh M, Alexander N, Hess D, Marx PA: Topical estrogen protects against SIV vaginal transmission without evidence of systemic effect. AIDS 2004; 18:1637-1643.
26. Stringer EM, Kaseba C, Levy J, Sinkala M, Goldenberg RL, Chi BH, Matongo I, Vermund SH, Mwanahamuntu M, Stringer JS: A randomized trial of the intrauterine contraceptive device vs hormonal contraception in women who are infected with the human immunodeficiency virus. Am J Obstet Gynecol 2007; 197:144, e141-148.
27. de Jong MA, de Witte L, Oudhoff MJ, Gringhuis SI, Gallay P, Geijtenbeek TB: TNF-alpha and TLR agonists increase susceptibility to HIV-1 transmission by human Langerhans cells ex vivo. J Clin Invest 2008; 118:3440-3452.
28. Kaul R, Pettengell C, Sheth PM, Sunderji S, Biringer A, MacDonald K, Walmsley S, Rebbapragada A: The genital tract immune milieu: an important determinant of HIV susceptibility and secondary transmission. J Reprod Immunol 2008; 77:32-40.
29. Kwant-Mitchell A, Ashkar AA, Rosenthal KL: Mucosal innate and adaptive immune responses against herpes simplex virus type 2 in a humanized mouse model. J Virol 2009; 83:10664-10676.
30. Martinson JA, Tenorio AR, Montoya CJ, Al-Harthi L, Gichinga CN, Krieg AM, Baum LL, Landay AL: Impact of class A, B and C CpG-oligodeoxynucleotides on in vitro activation of innate immune cells in human immunodeficiency virus-1 infected individuals. Immunology 2007; 120:526-535.
31. Nazli A, Yao XD, Smieja M, Rosenthal KL, Ashkar AA, Kaushic C: Differential induction of innate anti-viral responses by TLR ligands against Herpes simplex virus, type 2, infection in primary genital epithelium of women. Antiviral Res 2009; 81:103-112.
32. Schaefer TM, Desouza K, Fahey JV, Beagley KW, Wira CR: Toll-like receptor (TLR) expression and TLR-mediated cytokine/chemokine production by human uterine epithelial cells. Immunology 2004; 112:428-436.
33. Lester RT, Yao XD, Ball TB, McKinnon LR, Kaul R, Wachihi C, Jaoko W, Plummer FA, Rosenthal KL: Toll-like receptor expression and responsiveness are increased in viraemic HIV-1 infection. AIDS 2008; 22:685-694.
34. Hart KM, Murphy AJ, Barrett KT, Wira CR, Guyre PM, Pioli PA: Functional expression of pattern recognition receptors in tissues of the human female reproductive tract. J Reprod Immunol 2009; 80:33-40.
35. Akira S, Uematsu S, Takeuchi O: Pathogen recognition and innate immunity. Cell 2006; 124:783-801.
36. Beutler B, Jiang Z, Georgel P, Crozat K, Croker B, Rutschmann S, Du X, Hoebe K: Genetic analysis of host resistance: toll-like receptor signaling and immunity at large. Annu Rev Immunol 2006; 24:353-389.
37. Iwasaki A, Medzhitov R: Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004; 5:987-995.
38. Ashkar AA, Bauer S, Mitchell WJ, Vieira J, Rosenthal KL: Local delivery of CpG oligodeoxynucleotides induces rapid changes in the genital mucosa and inhibits replication, but not entry, of herpes simplex virus type 2. J Virol 2003; 77:8948-8956.
39. Harandi AM, Eriksson K, Holmgren J: A protective role of locally administered immunostimulatory CpG oligodeoxynucleotide in a mouse model of genital herpes infection. J Virol 2003; 77:953-962.
40. Shen H, Iwasaki A: A crucial role for plasmacytoid dendritic cells in antiviral protection by CpG ODN-based vaginal microbicide. J Clin Invest 2006; 116:2237-2243.
41. Sajic D, Ashkar AA, Patrick AJ, McCluskie MJ, Davis HL, Levine KL, Holl R, Rosenthal KL: Parameters of CpG oligodeoxynucleotide-induced protection against intravaginal HSV-2 challenge. J Med Virol 2003; 71:561-568.
42. Sato A, Linehan MM, Iwasaki A: Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc Natl Acad Sci U S A 2006; 103:17343-17348.
43. Ashkar AA, Yao XD, Gill N, Sajic D, Patrick AJ, Rosenthal KL: Toll-like receptor (TLR)-3, but not TLR4, agonist protects against genital herpes infection in the absence of inflammation seen with CpG DNA. J Infect Dis 2004; 190:1841-1849.
44. Duerst RJ, Morrison LA: Innate immunity to herpes simplex virus type 2. Viral Immunol 2003; 16:475-490.
45. Herbst-Kralovetz MM, Pyles RB: Quantification of poly(I:C)-mediated protection against genital herpes simplex virus type 2 infection. J Virol 2006; 80:9988-9997.
46. Ogawa Y, Kawamura T, Kimura T, Ito M, Blauvelt A, Shimada S: Gram-positive bacteria enhance HIV-1 susceptibility in Langerhans cells, but not in dendritic cells, via Toll-like receptor activation. Blood 2009; 113:5157-5166.
47. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, Kluger C, Salazar AM, Colonna M, Steinman RM: Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med 2009; 206:1589-1602.
48. Brichacek B, Vanpouille C, Kiselyeva Y, Biancotto A, Merbah M, Hirsch I, Lisco A, Grivel JC, Margolis L: Contrasting roles for TLR ligands in HIV-1 pathogenesis. PLoS ONE 2010; 5:e12831.
49. Funderburg N, Luciano AA, Jiang W, Rodriguez B, Sieg SF, Lederman MM: Toll-like receptor ligands induce human T cell activation and death, a model for HIV pathogenesis. PLoS ONE 2008; 3:e1915.
50. Pichlmair A, Reise Sousa C: Innate recognition of viruses. Immunity 2007; 27:370-383.
51. Iwasaki A: Antiviral immune responses in the genital tract: clues for vaccines. Nat Rev Immunol 2010; 10:699-711.
52. Trinchieri G: Type I interferon: friend or foe? J Exp Med 2010; 207:2053-2063.
53. Iwasaki A, Medzhitov R: Regulation of adaptive immunity by the innate immune system. Science 2010; 327:291-295.
54. Kanneganti TD, Lamkanfi M, Nunez G: Intracellular NOD-like receptors in host defense and disease. Immunity 2007; 27:549-559.
55. Thompson JM, Iwasaki A: Toll-like receptors regulation of viral infection and disease. Adv Drug Deliv Rev 2008; 60:786-794.
56. Donnelly RP, Kotenko SV: Interferon-lambda: a new addition to an old family. J Interferon Cytokine Res 2010; 30:555-564.
57. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP: IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003; 4:69-77.
58. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR: Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 2006; 80:4501-4509.
59. Ank N, West H, Paludan SR: IFN-lambda: novel antiviral cytokines. J Interferon Cytokine Res 2006; 26:373-379.
60. Onoguchi K, Yoneyama M, Takemura A, Akira S, Taniguchi T, Namiki H, Fujita T: Viral infections activate types I and III interferon genes through a common mechanism. J Biol Chem 2007; 282:7576-7581.
61. Yang K, Puel A, Zhang S, Eidenschenk C, Ku CL, Casrouge A, Picard C, von Bernuth H, Senechal B, Plancoulaine S, Al-Hajjar S, Al-Ghonaium A, Marodi L, Davidson D, Speert D, Roifman C, Garty BZ, Ozinsky A, Barrat FJ, Coffman RL, Miller RL, Li X, Lebon P, Rodriguez-Gallego C, Chapel H, Geissmann F, Jouanguy E, Casanova JL: Human TLR-7-, -8-, and -9-mediated induction of IFN-alpha/beta and -lambda Is IRAK-4 dependent and redundant for protective immunity to viruses. Immunity 2005; 23:465-478.
62. Akira S, Takeda K: Toll-like receptor signalling. Nat Rev Immunol 2004; 4:499-511.
63. Kawai T, Akira S: Innate immune recognition of viral infection. Nat Immunol 2006; 7:131-137.
64. Kawai T, Akira S: The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 2010; 11:373-384.
65. Marie I, Durbin JE, Levy DE: Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J 1998; 17:6660-6669.
66. Tailor P, Tamura T, Kong HJ, Kubota T, Kubota M, Borghi P, Gabriele L, Ozato K: The feedback phase of type I interferon induction in dendritic cells requires interferon regulatory factor 8. Immunity 2007; 27:228-239.
67. Gill N, Deacon PM, Lichty B, Mossman KL, Ashkar AA: Induction of innate immunity against herpes simplex virus type 2 infection via local delivery of Toll-like receptor ligands correlates with beta interferon production. J Virol 2006; 80:9943-9950.
68. Svensson A, Bellner L, Magnusson M, Eriksson K: Role of IFN-alpha/beta signaling in the prevention of genital herpes virus type 2 infection. J Reprod Immunol 2007; 74:114-123.
69. Boasso A, Hardy AW, Anderson SA, Dolan MJ, Shearer GM: HIV-induced type I interferon and tryptophan catabolism drive T cell dysfunction despite phenotypic activation. PLoS ONE 2008; 3:e2961.
70. Muller-Trutwin M, Hosmalin A: Role for plasmacytoid dendritic cells in anti-HIV innate immunity. Immunol Cell Biol 2005; 83:578-583.
71. Fitzgerald-Bocarsly P, Jacobs ES: Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J Leukoc Biol 2010; 87:609-620.
72. Ghosh M, Schaefer TM, Fahey JV, Wright JA, Wira CR: Antiviral responses of human Fallopian tube epithelial cells to toll-like receptor 3 agonist poly(I:C). Fertil Steril 2008; 89:1497-1506.
73. Schlaepfer E, Audige A, Joller H, Speck RF: TLR7/8 triggering exerts opposing effects in acute versus latent HIV infection. J Immunol 2006; 176:2888-2895.
74. Schlaepfer E, Speck RF: Anti-HIV activity mediated by natural killer and CD8+ cells after toll-like receptor 7/8 triggering. PLoS ONE 2008; 3:e1999.
75. Doehle BP, Hladik F, McNevin JP, McElrath MJ, 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.
76. Brand S, Beigel F, Olszak T, Zitzmann K, Eichhorst ST, Otte JM, Diebold J, Diepolder H, Adler B, Auernhammer CJ, Goke B, Dambacher J: IL-28A and IL-29 mediate antiproliferative and antiviral signals in intestinal epithelial cells and murine CMV infection increases colonic IL-28A expression. Am J Physiol Gastrointest Liver Physiol 2005; 289:G960-G968.
77. Hou W, Wang X, Ye L, Zhou L, Yang ZQ, Riedel E, Ho WZ: Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J Virol 2009; 83:3834-3842.
78. Yan N, Regalado-Magdos AD, Stiggelbout B, Lee-Kirsch MA, Lieberman J: The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 2010; 11:1005-1013.