Functional failure of TLR3 and its signaling components contribute to herpes simplex encephalitis

Journal of Neuroimmunology

Volumn 316, Issue , 2018, Pages 65-73

  Mielcarska, Matylda Barbara ^a   Bossowska Nowicka, Magdalena ^a   Toka, Felix Ngosa ^a,b  

^a WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^b Ross University School of Veterinary Medicine   (Saint Kitts and Nevis)

Author keywords

HSE; HSV 1; HSV 2; Innate immunity; TLR3

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; HERPES SIMPLEX VACCINE; I KAPPA B KINASE EPSILON; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1 RECEPTOR; MEMBRANE PROTEIN; PROTEIN KINASE; PROTEIN TBK1; PROTEIN UNC93B; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UNCLASSIFIED DRUG; TLR3 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL FEATURE; CYTOKINE PRODUCTION; HERPES SIMPLEX ENCEPHALITIS; HUMAN; INFECTION SENSITIVITY; INNATE IMMUNITY; LYSOSOME; MYELOID DENDRITIC CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; VIRUS REACTIVATION; VIRUS REPLICATION; IMMUNOLOGY; METABOLISM;

ENCEPHALITIS, HERPES SIMPLEX; HUMANS; IMMUNITY, INNATE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 85039778097     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2017.12.011     Document Type: Review

References (110)

1. Abel, L., Plancoulaine, S., Jouanguy, E., Zhang, S.Y., Mahfoufi, N., Nicolas, N., Sancho-Shimizu, V., Alcaïs, A., Guo, Y., Cardon, A., Boucherit, S., Obach, D., Clozel, T., Lorenzo, L., Amsallem, D., Berquin, P., Blanc, T., Bost-Bru, C., Chabrier, S., Chabrol, B., Cheuret, E., Dulac, O., Evrard, P., Héron, B., Lazaro, L., Mancini, J., Pedespan, J.M., Rivier, F., Vallée, L., Lebon, P., Rozenberg, F., Casanova, J.L., Tardieu, M., Age-dependent Mendelian predisposition to herpes simplex virus type 1 encephalitis in childhood. J. Pediatr. 157 (2010), 623–629.
2. Akira, S., Takeda, K., Kaisho, T., Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2 (2001), 675–680.
3. Akula, S.M., Naranatt, P.P., Walia, N.S., Wang, F.Z., Fegley, B., Chandran, B., Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) infection of human fibroblast cells occurs through endocytosis. J. Virol. 77 (2003), 7978–7990.
4. Aldea, S., Joly, L.M., Roujeau, T., Oswald, A.M., Devaux, B., Postoperative herpes simplex virus encephalitis after neurosurgery: case report and review of the literature. Clin. Infect. Dis. 36 (2003), e96–9.
5. Alexopoulou, L., Holt, A.C., Medzhitov, R., Flavell, R.A., Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413 (2001), 732–738.
6. Algahtani, H., Shirah, B., Hmoud, M., Subahi, A., Nosocomial herpes simplex encephalitis: a challenging diagnosis. J. Infect. Public Health 10 (2016), 343–347.
7. Altan, M., Burtness, B., EGFR-directed antibodies increase the risk of severe infection in cancer patients. BMC Med., 13, 2015, 37.
8. Andersen, L.L., Mørk, N., Reinert, L.S., Kofod-Olsen, E., Narita, R., Jørgensen, S.E., Skipper, K.A., Höning, K., Gad, H.H., Østergaard, L., Ørntoft, T.F., Hornung, V., Paludan, S.R., Mikkelsen, J.G., Fujita, T., Christiansen, M., Hartmann, R., Mogensen, T.H., Functional IRF3 deficiency in a patient with herpes simplex encephalitis. J. Exp. Med. 212 (2015), 1371–1379.
9. Anderson, K.V., Jürgens, G., Nüsslein-Volhard, C., Establishment of dorsal-ventral polarity in the Drosophila embryo; genetic studies on the role of the Toll gene product. Cell 42 (1985), 779–789.
10. Audry, M., Ciancanelli, M., Yang, K., Cobat, A., Chang, H.H., Sancho-Shimizu, V., Lorenzo, L., Niehues, T., Reichenbach, J., Li, X.X., Israel, A., Abel, L., Casanova, J.L., Zhang, S.Y., Jouanguy, E., Puel, A., NEMO is a key component of NF-κB- and IRF-3-dependent TLR3-mediated immunity to herpes simplex virus. J. Allergy Clin. Immunol. 128 (2011), 610–617.
11. Awasthi, S., Huang, J., Shaw, C., Friedman, H.M., Blocking herpes simplex virus 2 glycoprotein E immune evasion as an approach to enhance efficacy of a trivalent subunit antigen vaccine for genital herpes. J. Virol. 88 (2014), 8421–8432.
12. Baines, J.D., Herpes simplex virus capsid assembly and DNA packaging: a present and future antiviral drug target. Trends Microbiol. 19 (2011), 606–613.
13. Barreiro, L.B., Ben-Ali, M., Quach, H., Laval, G., Patin, E., Pickrell, J.K., Bouchier, C., Tichit, M., Neyrolles, O., Gicquel, B., Kidd, J.R., Kidd, K.K., Alcaïs, A., Ragimbeau, J., Pellegrini, S., Abel, L., Casanova, J.L., Quintana-Murci, L., Evolutionary dynamics of human Toll-like receptors and their different contributions to host defense. PLoS Genet., 5, 2009, e1000562.
14. Barton, G.M., Kagan, J.C., A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9 (2009), 535–542.
15. Blasius, A.L., Beutler, B., Intracellular toll-like receptors. Immunity 32 (2010), 305–315.
16. Bonnard, M., Mirtsos, C., Suzuki, S., Graham, K., Huang, J., Ng, M., Itié A., Wakeham, A., Shahinian, A., Henzel, W.J., Elia, A.J., Shillinglaw, W., Mak, T.W., Cao, Z., Yeh, W.C., Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription. EMBO J. 19 (2000), 4976–4985.
17. Brinkmann, M.M., Spooner, E., Hoebe, K., Beutler, B., Ploegh, H.L., Kim, Y.M., The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J. Cell Biol. 177 (2007), 265–275.
18. Bsibsi, M., Ravid, R., Gveric, D., Van Noort, J.M., Broad expression of Toll-like receptors in the human central nervous system. J. Neuropathol. Exp. Neurol. 61 (2002), 1013–1021.
19. Bsibsi, M., Persoon-Deen, C., Verwer, R.W., Meeuwsen, S., Ravid, R., Van Noort, J.M., Toll-like receptor 3 on adult human astrocytes triggers production of neuroprotective mediators. Glia 53 (2006), 688–695.
20. Buckley, R.H., Molecular defects in human severe combined immunodeficiency and approaches to immune reconstitution. Annu. Rev. Immunol. 22 (2004), 625–655.
21. Casrouge, A., Zhang, S.Y., Eidenschenk, C., Jouanguy, E., Puel, A., Yang, K., Alcais, A., Picard, C., Mahfoufi, N., Nicolas, N., Lorenzo, L., Plancoulaine, S., Sénéchal, B., Geissmann, F., Tabeta, K., Hoebe, K., Du, X., Miller, R.L., Héron, B., Mignot, C., de Villemeur, T.B., Lebon, P., Dulac, O., Rozenberg, F., Beutler, B., Tardieu, M., Abel, L., Casanova, J.L., Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 314 (2006), 308–312.
22. Chattopadhyay, S., Sen, G.C., Tyrosine phosphorylation in Toll-like receptor signaling. Cytokine Growth Factor Rev. 25 (2014), 533–541.
23. Cheung, P., Banfield, B.W., Tufaro, F., Brefeldin A arrests the maturation and egress of herpes simplex virus particles during infection. J. Virol. 65 (1991), 1893–1904.
24. Chow, F.C., Glaser, C.A., Sheriff, H., Xia, D., Messenger, S., Whitley, R., Venkatesan, A., Use of clinical and neuroimaging characteristics to distinguish temporal lobe herpes simplex encephalitis from its mimics. Clin. Infect. Dis. 60 (2015), 1377–1383.
25. De Bouteiller, O., Merck, E., Hasan, U.A., Hubac, S., Benguigui, B., Trinchieri, G., Bates, E.E., Caux, C., Recognition of double-stranded RNA by human Toll-like receptor 3 and downstream receptor signaling requires multimerization and acidic pH. J. Biol. Chem. 280 (2005), 38133–38145.
26. De Tiège, X., Rozenberg, F., Héron, B., The spectrum of herpes simplex encephalitis in children. Eur. J. Paediatr. Neurol. 12 (2008), 72–81.
27. Dupuis, S., Jouanguy, E., Al-Hajjar, S., Fieschi, C., Al-Mohsen, I.Z., Al-Jumaah, S., Yang, K., Chapgier, A., Eidenschenk, C., Eid, P., Al, Ghonaium A., Tufenkeji, H., Frayha, H., Al-Gazlan, S., Al-Rayes, H., Schreiber, R.D., Gresser, I., Casanova, J.L., Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat. Genet. 33 (2003), 388–391.
28. Fitzgerald, K.A., McWhirter, S.M., Faia, K.L., Rowe, D.C., Latz, E., Golenbock, D.T., Coyle, A.J., Liao, S.M., Maniatis, T., IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4 (2003), 491–496.
29. Garcia-Cattaneo, A., Gobert, F.X., Müller, M., Toscano, F., Flores, M., Lescure, A., Del Nery, E., Benaroch, P., Cleavage of Toll-like receptor 3 by cathepsins B and H is essential for signaling. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 9053–9058.
30. Gnann, J.W., Whitley, R.J., Herpes simplex encephalitis: an update. Curr. Infect. Dis. Rep., 19, 2017, 13.
31. Gnann, J.W., Sköldenberg, B., Hart, J., Aurelius, E., Schliamser, S., Studahl, M., Eriksson, B.M., Hanley, D., Aoki, F., Jackson, A.C., Griffiths, P., Miedzinski, L., Hanfelt-Goade, D., Hinthorn, D., Ahlm, C., Aksamit, A., Cruz-Flores, S., Dale, I., Cloud, G., Jester, P., Whitley, R.J., Herpes simplex encephalitis: lack of clinical benefit of long-term valacyclovir therapy. Clin. Infect. Dis. 61 (2015), 683–691.
32. Greene, W., Gao, S.J., Actin dynamics regulate multiple endosomal steps during Kaposi's sarcoma-associated herpesvirus entry and trafficking in endothelial cells. PLoS Pathog., 5, 2009, e1000512.
33. Griffin, D.E., Encephalitis, myelitis, and neuritis. Mandell, G.L., Bennett, J.E., Dolin, R., (eds.) Mandell, Bennett, & Dolin: Principles and Practice of Infectious Diseases, 6th Edition, 2005, Churchill Livingstone, New York, 1144–1150.
34. Guo, Y., Audry, M., Ciancanelli, M., Alsina, L., Azevedo, J., Herman, M., Anguiano, E., Sancho-Shimizu, V., Lorenzo, L., Pauwels, E., Philippe, P.B., Pérez de Diego, R., Cardon, A., Vogt, G., Picard, C., Andrianirina, Z.Z., Rozenberg, F., Lebon, P., Plancoulaine, S., Tardieu, M., Doireau, V., Jouanguy, E., Chaussabel, D., Geissmann, F., Abel, L., Casanova, J.L., Zhang, S.Y., Herpes simplex virus encephalitis in a patient with complete TLR3 deficiency: TLR3 is otherwise redundant in protective immunity. J. Exp. Med. 208 (2011), 2083–2098.
35. Harley, C.A., Dasgupta, A., Wilson, D.W., Characterization of herpes simplex virus-containing organelles by subcellular fractionation: role for organelle acidification in assembly of infectious particles. J. Virol. 75 (2001), 1236–1251.
36. Hemmi, H., Takeuchi, O., Sato, S., Yamamoto, M., Kaisho, T., Sanjo, H., Kawai, T., Hoshino, K., Takeda, K., Akira, S., The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199 (2004), 1641–1650.
37. Herman, M., Ciancanelli, M., Ou, Y.H., Lorenzo, L., Klaudel-Dreszler, M., Pauwels, E., Sancho-Shimizu, V., Pérez de Diego, R., Abhyankar, A., Israelsson, E., Guo, Y., Cardon, A., Rozenberg, F., Lebon, P., Tardieu, M., Heropolitanska-Pliszka, E., Chaussabel, D., White, M.A., Abel, L., Zhang, S.Y., Casanova, J.L., Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex encephalitis of childhood. J. Exp. Med. 209 (2012), 1567–1582.
38. Hoebe, K., Beutler, B., TRAF3: a new component of the TLR-signaling apparatus. Trends Mol. Med. 12 (2006), 187–189.
39. Hollinshead, M., Johns, H.L., Sayers, C.L., Gonzalez-Lopez, C., Smith, G.L., Elliott, G., Endocytic tubules regulated by Rab GTPases 5 and 11 are used for envelopment of herpes simplex virus. EMBO J. 31 (2012), 4204–4220.
40. Honda, K., Taniguchi, T., IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6 (2006), 644–658.
41. Jacobs, B.L., Langland, J.O., When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219 (1996), 339–349.
42. Jiang, Z., Mark, T.W., Sen, G., Li, X., Toll-like receptor 3-mediated activation of NF-kappaB and IRF3 diverges at Toll-IL-1 receptor domain-containing adapter inducing IFN-beta. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 3533–3538.
43. Johnston, C., Koelle, D.M., Wald, A., HSV-2: in pursuit of a vaccine. J. Clin. Invest. 121 (2011), 4600–4609.
44. Johnston, C., Gottlieb, S.L., Wald, A., Status of vaccine research and development of vaccines for herpes simplex virus. Vaccine 34 (2016), 2948–2952.
45. Kim, Y.M., Brinkmann, M.M., Paquet, M.E., Ploegh, H.L., UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452 (2008), 234–238.
46. Krishnan, J., Selvarajoo, K., Tsuchiya, M., Lee, G., Choi, S., Toll-like receptor signal transduction. Exp. Mol. Med. 39 (2007), 421–438.
47. Lafaille, F.G., Pessach, I.M., Zhang, S.Y., Ciancanelli, M.J., Herman, M., Abhyankar, A., Ying, S.W., Keros, S., Goldstein, P.A., Mostoslavsky, G., Ordovas-Montanes, J., Jouanguy, E., Plancoulaine, S., Tu, E., Elkabetz, Y., Al-Muhsen, S., Tardieu, M., Schlaeger, T.M., Daley, G.Q., Abel, L., Casanova, J.L., Studer, L., Notarangelo, L.D., Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 491 (2012), 769–773.
48. Lalani, A.I., Moore, C.R., Luo, C., Kreider, B.Z., Liu, Y., Morse, H.C. 3rd, Xie, P., Myeloid cell TRAF3 regulates immune responses and inhibits inflammation and tumor development in mice. J. Immunol. 194 (2015), 334–348.
49. Lee, B.L., Barton, G.M., Trafficking of endosomal Toll-like receptors. Trends Cell Biol. 24 (2014), 360–369.
50. Lellouch-Tubiana, A., Fohlen, M., Robain, O., Rozenberg, F., Immunocytochemical characterization of long-term persistent immune activation in human brain after herpes simplex encephalitis. Neuropathol. Appl. Neurobiol. 26 (2000), 285–294.
51. Li, K., Chen, Z., Kato, N., Gale, M. Jr., Lemon, S.M., Distinct poly(I–C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J. Biol. Chem. 280 (2005), 16739–16747.
52. Lim, H.K., Seppänen, M., Hautala, T., Ciancanelli, M.J., Itan, Y., Lafaille, F.G., Dell, W., Lorenzo, L., Byun, M., Pauwels, E., Rönnelid, Y., Cai, X., Boucherit, S., Jouanguy, E., Paetau, A., Lebon, P., Rozenberg, F., Tardieu, M., Abel, L., Yildiran, A., Vergison, A., Roivainen, R., Etzioni, A., Tienari, P.J., Casanova, J.L., Zhang, S.Y., TLR3 deficiency in herpes simplex encephalitis: high allelic heterogeneity and recurrence risk. Neurology 83 (2014), 1888–1897.
53. Liu, L., Botos, I., Wang, Y., Leonard, J.N., Shiloach, J., Segal, D.M., Davies, D.R., Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 320 (2008), 379–381.
54. Lo Presti, A., Weil, A.G., Niazi, T.N., Bhatia, S., Herpes simplex reactivation or postinfectious inflammatory response after epilepsy surgery: case report and review of the literature. Surg. Neurol. Int., 6, 2015, 47.
55. Long, D., Skoberne, M., Gierahn, T.M., Larson, S., Price, J.A., Clemens, V., Baccari, A.E., Cohane, K.P., Garvie, D., Siber, G.R., Flechtner, J.B., Identification of novel virus-specific antigens by CD4 + and CD8 + T cells from asymptomatic HSV-2 seropositive and seronegative donors. Virology 464-465 (2014), 296–311.
56. Maraş Genç H., Uyur Yalçın, E., Sayan, M., Bayhan, A., Öncel, S., Arısoy, E.S., Kara, B., Clinical outcomes in children with herpes simplex encephalitis receiving steroid therapy. J. Clin. Virol. 80 (2016), 87–92.
57. McWhirter, S.M., Fitzgerald, K.A., Rosains, J., Rowe, D.C., Golenbock, D.T., Maniatis, T., IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 233–238.
58. Medzhitov, R., Preston-Hurlburt, P., Janeway, C.A. Jr., A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388 (1997), 394–397.
59. Menachery, V.D., Pasieka, T.J., Leib, D.A., Interferon regulatory factor 3-dependent pathways are critical for control of herpes simplex virus type 1 central nervous system infection. J. Virol. 84 (2010), 9685–9694.
60. Meylan, E., Tschopp, J., Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol. Cell 22 (2006), 561–569.
61. Meylan, E., Burns, K., Hofmann, K., Blancheteau, V., Martinon, F., Kelliher, M., Tschopp, J., RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat. Immunol. 5 (2004), 503–507.
62. Modi, S., Mahajan, A., Dharaiya, D., Varelas, P., Mitsias, P., Burden of herpes simplex virus encephalitis in the United States. J. Neurol. 264 (2017), 1204–1208.
63. Moore, C.R., Liu, Y., Shao, C., Covey, L.R., Morse, H.C. 3rd, Xie, P., Specific deletion of TRAF3 in B lymphocytes leads to B-lymphoma development in mice. Leukemia 26 (2012), 1122–1127.
64. Mørk, N., Kofod-Olsen, E., Sørensen, K.B., Bach, E., Ørntoft, T.F., Østergaard, L., Paludan, S.R., Christiansen, M., Mogensen, T.H., Mutations in the TLR3 signaling pathway and beyond in adult patients with herpes simplex encephalitis. Genes Immun. 16 (2015), 552–566.
65. Muzio, M., Polentarutti, N., Bosisio, D., Manoj Kumar, P.P., Mantovani, A., Toll-like receptor family and signalling pathway. Biochem. Soc. Trans. 28 (2000), 563–566.
66. Oganesyan, G., Saha, S.K., Guo, B., He, J.Q., Shahangian, A., Zarnegar, B., Perry, A., Cheng, G., Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 439 (2006), 208–211.
67. Önnheim K., Ekblad M., Görander S., Bergström T., Liljeqvist J., 2016, Vaccination with the secreted glycoprotein G of herpes simplex virus 2 induces protective immunity after genital infection. Viruses 8, 110.
68. Paludan, S.R., Bowie, A.G., Horan, K.A., Fitzgerald, K.A., Recognition of herpesviruses by the innate immune system. Nat. Rev. Immunol. 11 (2011), 143–154.
69. Peltier, D.C., Simms, A., Farmer, J.R., Miller, D.J., Human neuronal cells possess functional cytoplasmic and TLR-mediated innate immune pathways influenced by phosphatidylinositol-3 kinase signaling. J. Immunol. 184 (2010), 7010–7021.
70. Pérez de Diego, R., Rodriguez-Gallego, C., Chapter 34 – other TLR pathway defects. Sullivan, K.E., Stiehm, E.R., (eds.) Stiehm's Immune Deficiencies, 2014, Elsevier, 692.
71. Pérez de Diego, R., Sancho-Shimizu, V., Lorenzo, L., Puel, A., Plancoulaine, S., Picard, C., Herman, M., Cardon, A., Durandy, A., Bustamante, J., Vallabhapurapu, S., Bravo, J., Warnatz, K., Chaix, Y., Cascarrigny, F., Lebon, P., Rozenberg, F., Karin, M., Tardieu, M., Al-Muhsen, S., Jouanguy, E., Zhang, S.Y., Abel, L., Casanova, J.L., Human TRAF3 adaptor molecule deficiency leads to impaired Toll-like receptor 3 response and susceptibility to herpes simplex encephalitis. Immunity 33 (2010), 400–411.
72. Perry, A.K., Chow, E.K., Goodnough, J.B., Yeh, W.C., Cheng, G., Differential requirement for TANK-binding kinase-1 in type I interferon responses to toll-like receptor activation and viral infection. J. Exp. Med. 199 (2004), 1651–1658.
73. Purves, D., Augustine, G.J., Fitzpatrick, D., Katz, L.C., LaMantia, A.S., McNamara, J.O., Williams, S.M., Chapter 1 – neuroglial cells. Neuroscience, 2nd Edition, 2001, Sinauer Associates, Sunderland (MA).
74. Qi, R., Singh, D., Kao, C.C., Proteolytic processing regulates Toll-like receptor 3 stability and endosomal localization. J. Biol. Chem. 287 (2012), 32617–32629.
75. Reinert, L.S., Harder, L., Holm, C.K., Iversen, M.B., Horan, K.A., Dagnæs-Hansen, F., Ulhøi, B.P., Holm, T.H., Mogensen, T.H., Owens, T., Nyengaard, J.R., Thomsen, A.R., Paludan, S.R., TLR3 deficiency renders astrocytes permissive to herpes simplex virus infection and facilitates establishment of CNS infection in mice. J. Clin. Invest. 122 (2012), 1368–1376.
76. Reinert, L.S., Lopušná K., Winther, H., Sun, C., Thomsen, M.K., Nandakumar, R., Mogensen, T.H., Meyer, M., Vægter, C., Nyengaard, J.R., Fitzgerald, K.A., Paludan, S.R., Sensing of HSV-1 by the cGAS–STING pathway in microglia orchestrates antiviral defence in the CNS. Nat. Commun., 7, 2016, 13348.
77. Riancho, J., Delgado-Alvarado, M., Sedano, M.J., Polo, J.M., Berciano, J., Herpes simplex encephalitis: clinical presentation, neurological sequelae and new prognostic factors. Ten years of experience. Neurol. Sci. 34 (2013), 1879–1881.
78. Rozenberg, F., Deback, C., Agut, C., Herpes simplex encephalitis: from virus to therapy. Infect. Disord. Drug Targets 11 (2011), 235–250.
79. Samuel, C.E., Antiviral actions of interferons. Clin. Microbiol. Rev. 14 (2001), 778–809.
80. Sancho-Shimizu, V., Pérez de Diego, R., Jouanguy, E., Zhang, S.Y., Casanova, J.L., Inborn errors of anti-viral interferon immunity in humans. Curr. Opin. Virol. 1 (2011), 487–496.
81. Sancho-Shimizu, V., Pérez de Diego, R., Lorenzo, L., Halwani, R., Alangari, A., Israelsson, E., Fabrega, S., Cardon, A., Maluenda, J., Tatematsu, M., Mahvelati, F., Herman, M., Ciancanelli, M., Guo, Y., AlSum, Z., Alkhamis, N., Al-Makadma, A.S., Ghadiri, A., Boucherit, S., Plancoulaine, S., Picard, C., Rozenberg, F., Tardieu, M., Lebon, P., Jouanguy, E., Rezaei, N., Seya, T., Matsumoto, M., Chaussabel, D., Puel, A., Zhang, S.Y., Abel, L., Al-Muhsen, S., Casanova, J.L., Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J. Clin. Invest. 121 (2011), 4889–4902.
82. Sarkar, S.N., Smith, H.L., Rowe, T.M., Sen, G.S., Double-stranded RNA signaling by Toll-like receptor 3 requires specific tyrosine residues in its cytoplasmic domain. J. Biol. Chem. 278 (2003), 4393–4396.
83. Sarkar, S.N., Peters, K.L., Elco, C.P., Sakamoto, S., Pal, S., Sen, G.C., Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat. Struct. Mol. Biol. 11 (2004), 1060–1067.
84. Sarkar, S.N., Elco, C.P., Peters, K.L., Chattopadhyay, S., Sen, G.C., Two tyrosine residues of Toll-like receptor 3 trigger different steps of NF-kappa B activation. J. Biol. Chem. 282 (2007), 3423–3427.
85. Sasai, M., Oshiumi, H., Matsumoto, M., Inoue, N., Fujita, F., Nakanishi, M., Seya, T., Cutting edge: NF-kappaB-activating kinase-associated protein 1 participates in TLR3/Toll-IL-1 homology domain-containing adapter molecule-1-mediated IFN regulatory factor 3 activation. J. Immunol. 174 (2005), 27–30.
86. Sharma, V., Mobeen, F., Prakash, T., Comparative genomics of herpesviridae family to look for potential signatures of human infecting strains. Int. J. Genomics, 2016, 2016, 9543274.
87. Shin, H., Iwasaki, A., A vaccine strategy protects against genital herpes by establishing local memory T cells. Nature 491 (2012), 463–467.
88. Shin, H., Iwasaki, A., Generating protective immunity against genital herpes. Trends Immunol. 34 (2013), 487–494.
89. Sironi, M., Peri, A.M., Cagliani, R., Forni, D., Riva, S., Biasin, M., Clerici, M., Gori, A., TLR3 mutations in adult patients with herpes simplex virus and varicella-zoster virus encephalitis. J. Infect. Dis. 215 (2017), 1430–1434.
90. Stanfield, B., Kousoulas, K.G., Herpes simplex vaccines: prospects of live-attenuated HSV vaccines to combat genital and ocular infections. Curr. Clin. Microbiol. Rep. 2 (2015), 125–136.
91. Sun, X., Shi, L., Zhang, H., Li, R., Liang, R., Liu, Z., Effects of Toll-like receptor 3 on herpes simplex virus type-1-infected mouse neural stem cells. Can. J. Microbiol. 61 (2015), 201–208.
92. Tabeta, K., Hoebe, K., Janssen, E.M., Du, X., Georgel, P., Crozat, K., Mudd, S., Mann, N., Sovath, S., Goode, J., Shamel, L., Herskovits, A.A., Portnoy, D.A., Cooke, M., Tarantino, L.M., Wiltshire, T., Steinberg, B.E., Grinstein, S., Beutler, B., The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 7 (2006), 156–164.
93. Takaoka, A., Wang, Z., Choi, M.K., Yanai, H., Negishi, H., Ban, T., Lu, Y., Miyagishi, M., Kodama, T., Honda, K., Ohba, Y., Taniguchi, T., DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448 (2007), 501–505.
94. Toscano, F., Estornes, Y., Virard, F., Garcia-Cattaneo, A., Pierrot, A., Vanbervliet, B., Bonnin, M., Ciancanelli, M.J., Zhang, S.Y., Funami, K., Seya, T., Matsumoto, M., Pin, J.J., Casanova, J.L., Renno, T., Lebecque, S., Cleaved/associated TLR3 represents the primary form of the signaling receptor. J. Immunol. 190 (2013), 764–773.
95. Tsai, S.Y., Segovia, J.A., Chang, T.H., Shil, N.K., Pokharel, S.M., Kannan, T.R., Baseman, J.B., Defrêne, J., Pagé N., Cesaro, A., Tessier, P.A., Bose, S., Regulation of TLR3 activation by S100A9. J. Immunol. 195 (2015), 4426–4437.
96. Turcotte, S., Letellier, J., Lippé R., Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J. Virol. 79 (2005), 8847–8860.
97. Upton, J.W., Chan, F.K., Staying alive: cell death in anti-viral immunity. Mol. Cell 54 (2014), 273–280.
98. Wald, A., Corey, L., Chapter 36 – persistence in the population: epidemiology, transmission. Arvin, A., Campadelli-Fiume, G., Mocarski, E., Moore, P.S., Roizman, B., Whitley, R.J., Yamanishi, K., (eds.) Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis, 2007, Cambridge University Press, Cambridge.
99. Wang, X., Majumdar, T., Kessler, P., Ozhegov, E., Zhang, Y., Chattopadhyay, S., Barik, S., Sen, G.C., STING requires the adaptor TRIF to trigger innate immune responses to microbial infection. Cell Host Microbe 20 (2016), 329–341.
100. Whitley, R.J., Kimberlin, D.W., Herpes simplex encephalitis: children and adolescents. Semin. Pediatr. Infect. Dis. 16 (2005), 17–23.
101. Whitley, R.J., Kimberlin, D.W., Prober, C.G., Chapter 32 – Pathogenesis and disease. Arvin, A., Campadelli-Fiume, G., Mocarski, E., Moore, P.S., Roizman, B., Whitley, R.J., Yamanishi, K., (eds.) Human Herpesviruses. Biology, Therapy, and Immunoprophylaxis, 2007, Cambridge University Press, Cambridge.
102. Widener, R.W., Whitley, R.J., Chapter 11 – Herpes simplex virus. Tselis, A.C., Booss, J., (eds.) Handbook of Clinical Neurology Neurovirology, Vol 123, 2014, 251–263.
103. Xie, P., Stunz, L.L., Larison, K.D., Yang, B., Bishop, G.A., TRAF3 is a critical regulator of B cell homeostasis in secondary lymphoid organs. Immunity 27 (2007), 253–267.
104. Yamamoto, M., Sato, S., Hemmi, H., Hoshino, K., Kaisho, T., Sanjo, H., Takeuchi, O., Sugiyama, M., Okabe, M., Takeda, K., Akira, S., Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301 (2003), 640–643.
105. Zapata, J.M., Llobet, D., Krajewska, M., Lefebvre, S., Kress, C.L., Reed, J.C., Lymphocyte-specific TRAF3 transgenic mice have enhanced humoral responses and develop plasmacytosis, autoimmunity, inflammation, and cancer. Blood 113 (2009), 4595–4603.
106. Zerboni, L., Che, X., Reichelt, M., Qiao, Y., Gu, H., Arvin, A., Herpes simplex virus 1 tropism for human sensory ganglion neurons in the severe combined immunodeficiency mouse model of neuropathogenesis. J. Virol. 87 (2013), 2791–2802.
107. Zhang, S.Y., Jouanguy, E., Ugolini, S., Smahi, A., Elain, G., Romero, P., Segal, D., Sancho-Shimizu, V., Lorenzo, L., Puel, A., Picard, C., Chapgier, A., Plancoulaine, S., Titeux, M., Cognet, C., von Bernuth, H., Ku, C.L., Casrouge, A., Zhang, X.X., Barreiro, L., Leonard, J., Hamilton, C., Lebon, P., Héron, B., Vallée, L., Quintana-Murci, L., Hovnanian, A., Rozenberg, F., Vivier, E., Geissmann, F., Tardieu, M., Abel, L., Casanova, J.L., TLR3 deficiency in patients with herpes simplex encephalitis. Science 317 (2007), 1522–1527.
108. Zhang, S.Y., Boisson-Dupuis, S., Chapgier, A., Yang, K., Bustamante, J., Puel, A., Picard, C., Abel, L., Jouanguy, E., Casanova, J.L., Inborn errors of interferon (IFN)-mediated immunity in humans: insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense. Immunol. Rev. 226 (2008), 29–40.
109. Zhang, S.Y., Herman, M., Ciancanelli, M.J., Pérez de Diego, R., Sancho-Shimizu, V., Abel, L., Casanova, J.L., TLR3 immunity to infection in mice and humans. Curr. Opin. Immunol. 25 (2013), 19–33.
110. Zhang, P., Xie, L., Balliet, J.W., Casimiro, D.R., Yao, F., A herpes simplex virus 2 (HSV-2) glycoprotein D-expressing nonreplicating dominant-negative HSV-2 virus vaccine is superior to a gD2 subunit vaccine against HSV-2 genital infection in guinea pigs. PLoS One, 9, 2014, e101373.