Dampened antiviral immunity to intravaginal exposure to RNA viral pathogens allows enhanced viral replication

Journal of Experimental Medicine

Volumn 213, Issue 13, 2016, Pages 2913-2929

  Khan, Shahzada ^a   Woodruff, Erik M ^a   Trapecar, Martin ^a   Fontaine, Krystal A ^a   Ezaki, Ashley ^a   Borbet, Timothy C ^a,c   Ott, Melanie ^a,b   Sanjabi, Shomyseh ^a,b  

^a GLADSTONE INSTITUTE OF VIROLOGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARENAVIRUS INFECTION; ARTICLE; CD8+ T LYMPHOCYTE; CELL MATURATION; FEMALE; IMMUNITY; INNATE IMMUNITY; INTERFERON INDUCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEXUAL TRANSMISSION; T LYMPHOCYTE ACTIVATION; VAGINA MUCOSA; VAGINA TISSUE; VAGINITIS; VIRUS REPLICATION; VIRUS TRANSMISSION; ZIKA FEVER; ANIMAL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTIC CHORIOMENINGITIS; PATHOLOGY; PHYSIOLOGY; VAGINA; VIROLOGY; ZIKA VIRUS;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; IMMUNITY, INNATE; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, KNOCKOUT; VAGINA; VIRUS REPLICATION; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85008467258     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20161289     Document Type: Article

References (58)

1. Ashkar, A.A., X.D. Yao, N. Gill, D. Sajic, A.J. Patrick, and K.L. Rosenthal. 2004. 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. 190:1841-1849. http://dx.doi.org/10.1086/425079
2. Barouch, D.H., K. Ghneim, W.J. Bosche, Y. Li, B. Berkemeier, M. Hull, S. Bhattacharyya, M. Cameron, J. Liu, K. Smith, et al. 2016. Rapid inflammasome activation following mucosal SIV infection of Rhesus monkeys. Cell. 165:656-667. http://dx.doi.org/10.1016/j.cell.2016.03.021
3. Barton, L.L., M.B. Mets, and C.L. Beauchamp. 2002. Lymphocytic choriomeningitis virus: emerging fetal teratogen. Am. J. Obstet. Gynecol. 187:1715-1716. http://dx.doi.org/10.1067/mob.2002.126297
4. Belkaid, Y., and S. Naik. 2013. Compartmentalized and systemic control of tissue immunity by commensals. Nat. Immunol. 14:646-653. http://dx.doi.org/10.1038/ni.2604
5. Black, C.A., L.C. Rohan, M. Cost, S.C. Watkins, R. Draviam, S. Alber, and R.P. Edwards. 2000. Vaginal mucosa serves as an inductive site for tolerance. J. Immunol. 165:5077-5083. http://dx.doi.org/10.4049/jimmunol.165.9.5077
6. Brooks, J.T., A. Friedman, R.E. Kachur, M. LaFlam, P.J. Peters, and D.J. Jamieson. 2016. Update: Interim guidance for prevention of sexual transmission of Zika virus -United States, July 2016. MMWR Morb. Mortal. Wkly. Rep. 65:745-747. http://dx.doi.org/10.15585/mmwr.mm6529e2
7. Byers, S.L., M.V. Wiles, S.L. Dunn, and R.A. Taft. 2012. Mouse estrous cycle identification tool and images. PLoS One. 7:e35538. http://dx.doi.org/10.1371/journal.pone.0035538
8. Casey, K.A., K.A. Fraser, J.M. Schenkel, A. Moran, M.C. Abt, L.K. Beura, P.J. Lucas, D. Artis, E.J. Wherry, K. Hogquist, et al. 2012. Antigenindependent differentiation and maintenance of effector-like resident memory T cells in tissues. J. Immunol. 188:4866-4875. http://dx.doi.org/10.4049/jimmunol.1200402
9. Christie, A., G.J. Davies-Wayne, T. Cordier-Lassalle, D.J. Blackley, A.S. Laney, D.E. Williams, S.A. Shinde, M. Badio, T. Lo, S.E. Mate, et al. Centers for Disease Control and Prevention. 2015. Possible sexual transmission of Ebola virus-Liberia, 2015. MMWR Morb. Mortal. Wkly. Rep. 64:479-481.
10. D'Ortenzio, E., S. Matheron, Y. Yazdanpanah, X. de Lamballerie, B. Hubert, G. Piorkowski, M. Maquart, D. Descamps, F. Damond, and I. Leparc-Goffart. 2016. Evidence of sexual transmission of Zika virus. N. Engl. J. Med. 374:2195-2198. http://dx.doi.org/10.1056/NEJMc1604449
11. Erlebacher, A. 2013. Mechanisms of T cell tolerance towards the allogeneic fetus. Nat. Rev. Immunol. 13:23-33. http://dx.doi.org/10.1038/nri3361
12. Fukao, T., and S. Koyasu. 2000. Expression of functional IL-2 receptors on mature splenic dendritic cells. Eur. J. Immunol. 30:1453-1457. http://dx.doi.org/10.1002/(SICI)1521-4141(200005)30:5<1453::AID-IMMU1453>3.0.CO;2-W
13. Fung-Leung, W.P., M.W. Schilham, A. Rahemtulla, T.M. Kündig, M. Vollenweider, J. Potter, W. van Ewijk, and T.W. Mak. 1991. CD8 is needed for development of cytotoxic T but not helper T cells. Cell. 65:443-449. http://dx.doi.org/10.1016/0092-8674(91)90462-8
14. Gill, N., P.M. Deacon, B. Lichty, K.L. Mossman, and A.A. Ashkar. 2006. 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. 80:9943-9950. http://dx.doi.org/10.1128/JVI.01036-06
15. Grant, A., S.S. Ponia, S. Tripathi, V. Balasubramaniam, L. Miorin, M. Sourisseau, M.C. Schwarz, M.P. Sánchez-Seco, M.J. Evans, S.M. Best, and A. García-Sastre. 2016. Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe. 19:882-890. http://dx.doi.org/10.1016/j.chom.2016.05.009
16. Granucci, F., D.M. Andrews, M.A. Degli-Esposti, and P. Ricciardi-Castagnoli. 2002. IL-2 mediates adjuvant effect of dendritic cells. Trends Immunol. 23:169-171. http://dx.doi.org/10.1016/S1471-4906(02)02187-7
17. Griffith, J.W., C.L. Sokol, and A.D. Luster. 2014. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32:659-702. http://dx.doi.org/10.1146/annurev-immunol-032713-120145
18. Harrower, J., T. Kiedrzynski, S. Baker, A. Upton, F. Rahnama, J. Sherwood, Q.S. Huang, A. Todd, and D. Pulford. 2016. Sexual transmission of Zika virus and persistence in semen, New Zealand, 2016. Emerg. Infect. Dis. 22:1855-1857. http://dx.doi.org/10.3201/eid2210.160951
19. Herbst-Kralovetz, M.M., and R.B. Pyles. 2006. Quantification of poly(I:C)-mediated protection against genital herpes simplex virus type 2 infection. J. Virol. 80:9988-9997. http://dx.doi.org/10.1128/JVI.01099-06
20. Hsia, E., M.J. Johnston, R.J. Houlden, W.H. Chern, and H.E. Hofland. 2008. Effects of topically applied acitretin in reconstructed human epidermis and the rhino mouse. J. Invest. Dermatol. 128:125-130. http://dx.doi.org/10.1038/sj.jid.5700968
21. Iversen, M.B., L.S. Reinert, M.K. Thomsen, I. Bagdonaite, R. Nandakumar, N. Cheshenko, T. Prabakaran, S.Y. Vakhrushev, M. Krzyzowska, S.K. Kratholm, et al. 2016. An innate antiviral pathway acting before interferons at epithelial surfaces. Nat. Immunol. 17:150-158. http://dx.doi.org/10.1038/ni.3319
22. Iwasaki, A. 2007. Mucosal dendritic cells. Annu. Rev. Immunol. 25:381-418. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141634
23. Iwasaki, A. 2010. Antiviral immune responses in the genital tract: clues for vaccines. Nat. Rev. Immunol. 10:699-711. http://dx.doi.org/10.1038/nri2836
24. Iwasaki, A., and R. Medzhitov. 2015. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16:343-353. http://dx.doi.org/10.1038/ni.3123
25. Kumamoto, Y., and A. Iwasaki. 2012. Unique features of antiviral immune system of the vaginal mucosa. Curr. Opin. Immunol. 24:411-416. http://dx.doi.org/10.1016/j.coi.2012.05.006
26. Lazear, H.M., and M.S. Diamond. 2016. Zika virus: New clinical syndromes and its emergence in the Western hemisphere. J. Virol. 90:4864-4875. http://dx.doi.org/10.1128/JVI.00252-16
27. Lazear, H.M., J. Govero, A.M. Smith, D.J. Platt, E. Fernandez, J.J. Miner, and M.S. Diamond. 2016. A mouse model of Zika virus pathogenesis. Cell Host Microbe. 19:720-730. http://dx.doi.org/10.1016/j.chom.2016.03.010
28. Lessler, J., L.H. Chaisson, L.M. Kucirka, Q. Bi, K. Grantz, H. Salje, A.C. Carcelen, C.T. Ott, J.S. Sheffield, N.M. Ferguson, et al. 2016. Assessing the global threat from Zika virus. Science. 353:aaf8160. http://dx.doi.org/10.1126/science.aaf8160
29. Li, P., P. Kaiser, H.W. Lampiris, P. Kim, S.A. Yukl, D.V. Havlir, W.C. Greene, and J.K. Wong. 2016. Stimulating the RIG-I pathway to kill cells in the latent HIV reservoir following viral reactivation. Nat. Med. 22:807-811. http://dx.doi.org/10.1038/nm.4124
30. Madsen, L., N. Labrecque, J. Engberg, A. Dierich, A. Svejgaard, C. Benoist, D. Mathis, and L. Fugger. 1999. Mice lacking all conventional MHC class II genes. Proc. Natl. Acad. Sci. USA. 96:10338-10343. http://dx.doi.org/10.1073/pnas.96.18.10338
31. Mahlakõiv, T., P. Hernandez, K. Gronke, A. Diefenbach, and P. Staeheli. 2015. Leukocyte-derived IFN-α/β and epithelial IFN-γ constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLoS Pathog. 11:e1004782. http://dx.doi.org/10.1371/journal.ppat.1004782
32. Marks, E., M.A. Tam, and N.Y. Lycke. 2010. The female lower genital tract is a privileged compartment with IL-10 producing dendritic cells and poor Th1 immunity following Chlamydia trachomatis infection. PLoS Pathog. 6:e1001179. http://dx.doi.org/10.1371/journal.ppat.1001179
33. McCausland, M.M., and S. Crotty. 2008. Quantitative PCR technique for detecting lymphocytic choriomeningitis virus in vivo. J. Virol. Methods. 147:167-176. http://dx.doi.org/10.1016/j.jviromet.2007.08.025
34. Moldenhauer, L.M., K.R. Diener, D.M. Thring, M.P. Brown, J.D. Hayball, and S.A. Robertson. 2009. Cross-presentation of male seminal fluid antigens elicits T cell activation to initiate the female immune response to pregnancy. J. Immunol. 182:8080-8093. http://dx.doi.org/10.4049/jimmunol.0804018
35. Mombaerts, P., J. Iacomini, R.S. Johnson, K. Herrup, S. Tonegawa, and V.E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 68:869-877. http://dx.doi.org/10.1016/0092-8674(92)90030-G
36. Munoz-Suano, A., A.B. Hamilton, and A.G. Betz. 2011. Gimme shelter: the immune system during pregnancy. Immunol. Rev. 241:20-38. http://dx.doi.org/10.1111/j.1600-065X.2011.01002.x
37. Musso, D., C. Roche, E. Robin, T. Nhan, A. Teissier, and V.M. Cao-Lormeau. 2015. Potential sexual transmission of Zika virus. Emerg. Infect. Dis. 21:359-361. http://dx.doi.org/10.3201/eid2102.141363
38. Nurkkala, M., I. Nordström, E. Telemo, and K. Eriksson. 2007. MHC expression and chemokine production in the murine vagina following intra-vaginal administration of ligands to toll-like receptors 3, 7 and 9. J. Reprod. Immunol. 73:148-157. http://dx.doi.org/10.1016/j.jri.2006.09.001
39. Ochiel, D.O., M. Ghosh, J.V. Fahey, P.M. Guyre, and C.R. Wira. 2010. Human uterine epithelial cell secretions regulate dendritic cell differentiation and responses to TLR ligands. J. Leukoc. Biol. 88:435-444. http://dx.doi.org/10.1189/jlb.1009700
40. Oh, J.E., B.C. Kim, D.H. Chang, M. Kwon, S.Y. Lee, D. Kang, J.Y. Kim, I. Hwang, J.W. Yu, S. Nakae, and H.K. Lee. 2016. Dysbiosis-induced IL-33 contributes to impaired antiviral immunity in the genital mucosa. Proc. Natl. Acad. Sci. USA. 113:E762-E771. http://dx.doi.org/10.1073/pnas.1518589113
41. Olson, M.R., D.S. McDermott, and S.M. Varga. 2012. The initial draining lymph node primes the bulk of the CD8 T cell response and influences memory T cell trafficking after a systemic viral infection. PLoS Pathog. 8:e1003054. http://dx.doi.org/10.1371/journal.ppat.1003054
42. Perez-Lopez, A., J. Behnsen, S.P. Nuccio, and M. Raffatellu. 2016. Mucosal immunity to pathogenic intestinal bacteria. Nat. Rev. Immunol. 16:135-148. http://dx.doi.org/10.1038/nri.2015.17
43. Pircher, H., D. Moskophidis, U. Rohrer, K. Bürki, H. Hengartner, and R.M. Zinkernagel. 1990. Viral escape by selection of cytotoxic T cell-resistant virus variants in vivo. Nature. 346:629-633. http://dx.doi.org/10.1038/346629a0
44. Rossi, S.L., R.B. Tesh, S.R. Azar, A.E. Muruato, K.A. Hanley, A.J. Auguste, R.M. Langsjoen, S. Paessler, N. Vasilakis, and S.C. Weaver. 2016. Characterization of a novel murine model to study Zika virus. Am. J. Trop. Med. Hyg. 94:1362-1369. http://dx.doi.org/10.4269/ajtmh.16-0111
45. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity. 13:539-548. http://dx.doi.org/10.1016/S1074-7613(00)00053-4
46. + T cells. Nat. Immunol. 14:509-513. http://dx.doi.org/10.1038/ni.2568
47. Stary, G., A. Olive, A.F. Radovic-Moreno, D. Gondek, D. Alvarez, P.A. Basto, M. Perro, V.D. Vrbanac, A.M. Tager, J. Shi, et al. 2015. A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells. Science. 348:aaa8205. http://dx.doi.org/10.1126/science.aaa8205
48. Suvas, P.K., H.M. Dech, F. Sambira, J. Zeng, and T.M. Onami. 2007. Systemic and mucosal infection program protective memory CD8 T cells in the vaginal mucosa. J. Immunol. 179:8122-8127. http://dx.doi.org/10.4049/jimmunol.179.12.8122
49. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell. 140:805-820. http://dx.doi.org/10.1016/j.cell.2010.01.022
50. Trinchieri, G. 2010. Type I interferon: friend or foe? J. Exp. Med. 207:2053-2063. http://dx.doi.org/10.1084/jem.20101664
51. Turmel, J.M., P. Abgueguen, B. Hubert, Y.M. Vandamme, M. Maquart, H. Le Guillou-Guillemette, and I. Leparc-Goffart. 2016. Late sexual transmission of Zika virus related to persistence in the semen. Lancet. 387:2501. http://dx.doi.org/10.1016/S0140-6736(16)30775-9
52. Warning, J.C., S.A. McCracken, and J.M. Morris. 2011. A balancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction. 141:715-724. http://dx.doi.org/10.1530/REP-10-0360
53. Wira, C.R., M. Rodriguez-Garcia, and M.V. Patel. 2015. The role of sex hormones in immune protection of the female reproductive tract. Nat. Rev. Immunol. 15:217-230. http://dx.doi.org/10.1038/nri3819
54. Wuest, S.C., J.H. Edwan, J.F. Martin, S. Han, J.S. Perry, C.M. Cartagena, E. Matsuura, D. Maric, T.A. Waldmann, and B. Bielekova. 2011. A role for interleukin-2 trans-presentation in dendritic cell-mediated T cell activation in humans, as revealed by daclizumab therapy. Nat. Med. 17:604-609. http://dx.doi.org/10.1038/nm.2365
55. Yiu, Z.Z., R.B. Warren, U. Mrowietz, and C.E. Griffiths. 2015. Safety of conventional systemic therapies for psoriasis on reproductive potential and outcomes. J. Dermatolog. Treat. 26:329-334. http://dx.doi.org/10.3109/09546634.2014.991673
56. Yockey, L.J., L. Varela, T. Rakib, W. Khoury-Hanold, S.L. Fink, B. Stutz, K. Szigeti-Buck, A. Van den Pol, B.D. Lindenbach, T.L. Horvath, and A. Iwasaki. 2016. Vaginal exposure to Zika virus during pregnancy leads to fetal brain infection. Cell. 166:1247-1256.e4. http://dx.doi.org/10.1016/j.cell.2016.08.004
57. Zhao, X., E. Deak, K. Soderberg, M. Linehan, D. Spezzano, J. Zhu, D.M. Knipe, and A. Iwasaki. 2003. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J. Exp. Med. 197:153-162. http://dx.doi.org/10.1084/jem.20021109
58. Zhou, X., S. Ramachandran, M. Mann, and D.L. Popkin. 2012. Role of lymphocytic choriomeningitis virus (LCMV) in understanding viral immunology: past, present and future. Viruses. 4:2650-2669. http://dx.doi.org/10.3390/v4112650