Modulation of TLR9 response in a mouse model of herpes simplex virus encephalitis

Antiviral Research

Volumn 96, Issue 3, 2012, Pages 414-421

  Boivin, Nicolas ^a   Menasria, Rafik ^a   Piret, Jocelyne ^a   Boivin, Guy ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Agonist and antagonist; Encephalitis; Herpes; Mouse; Toll like receptors

Indexed keywords

INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; OLIGODEOXYNUCLEOTIDE 1585; OLIGODEOXYNUCLEOTIDE 1826; OLIGODEOXYNUCLEOTIDE 2088; OLIGODEOXYNUCLEOTIDE 2395; OLIGODEOXYNUCLEOTIDE DERIVATIVE; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CYTOKINE PRODUCTION; HERPES SIMPLEX ENCEPHALITIS; MOUSE; NONHUMAN; POST TREATMENT SURVIVAL; PRIORITY JOURNAL; SINGLE DRUG DOSE; VERO CELL; VIRUS LOAD;

ANIMALS; ANTIVIRAL AGENTS; BRAIN; CHEMOKINES; DNA, VIRAL; ENCEPHALITIS, HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED BALB C; NEUTRALIZATION TESTS; OLIGODEOXYRIBONUCLEOTIDES; POLY I-C; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 9; VIRAL LOAD;

HERPES; HUMAN HERPESVIRUS 1; MUS; SIMPLEXVIRUS;

EID: 84869142278     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2012.09.022     Document Type: Article

References (57)

1. Ahmad-Nejad P., Hacker H., Rutz M., Bauer S., Vabulas R.M., Wagner H. Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur. J. Immunol. 2002, 32:1958-1968.
2. 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 2001, 413:732-738.
3. Aravalli R.N., Hu S., Rowen T.N., Palmquist J.M., Lokensgard J.R. Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J. Immunol. 2005, 175:4189-4193.
4. Ashkar A.A., Bauer S., Mitchell W.J., Vieira J., Rosenthal K.L. 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.
5. Ashkar A.A., Rosenthal K.L. Toll-like receptor 9, CpG DNA and innate immunity. Curr. Mol. Med. 2002, 2:545-556.
6. Ashkar A.A., Yao X.D., Gill N., Sajic D., Patrick A.J., Rosenthal K.L. 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.
7. Bernstein D.I., Harrison C.J., Tomai M.A., Miller R.L. Daily or weekly therapy with resiquimod (R-848) reduces genital recurrences in herpes simplex virus-infected guinea pigs during and after treatment. J. Infect. Dis. 2001, 183:844-849.
8. Boivin G., Goyette N., Sergerie Y., Keays S., Booth T. Longitudinal evaluation of herpes simplex virus DNA load during episodes of herpes labialis. J. Clin. Virol. 2006, 37:248-251.
9. Boivin N., Sergerie Y., Rivest S., Boivin G. Effect of pretreatment with toll-like receptor agonists in a mouse model of herpes simplex virus type 1 encephalitis. J. Infect. Dis. 2008, 198:664-672.
10. Doyle S., Vaidya S., O'Connell R., Dadgostar H., Dempsey P., Wu T., Rao G., Sun R., Haberland M., Modlin R., Cheng G. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 2002, 17:251-263.
11. Doyle S.E., O'Connell R., Vaidya S.A., Chow E.K., Yee K., Cheng G. Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J. Immunol. 2003, 170:3565-3571.
12. Gaajetaan G.R., Geelen T.H., Grauls G.E., Bruggeman C.A., Stassen F.R. CpG and poly(I:C) stimulation of dendritic cells and fibroblasts limits herpes simplex virus type 1 infection in an IFNbeta-dependent and -independent way. Antiviral Res. 2012, 93:39-47.
13. Getts D.R., Terry R.L., Getts M.T., Muller M., Rana S., Shrestha B., Radford J., Van Rooijen N., Campbell I.L., King N.J. Ly6c+ inflammatory monocytes are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J. Exp. Med. 2008, 205:2319-2337.
14. Gill N., Deacon P.M., Lichty B., Mossman K.L., Ashkar A.A. 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.
15. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., Diamond M.S., Colonna M. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 2006, 103:8459-8464.
16. Glass W.G., Hickey M.J., Hardison J.L., Liu M.T., Manning J.E., Lane T.E. Antibody targeting of the CC chemokine ligand 5 results in diminished leukocyte infiltration into the central nervous system and reduced neurologic disease in a viral model of multiple sclerosis. J. Immunol. 2004, 172:4018-4025.
17. Herbst-Kralovetz M.M., Pyles R.B. Quantification of poly(I:C)-mediated protection against genital herpes simplex virus type 2 infection. J. Virol. 2006, 80:9988-9997.
18. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., Taniguchi T. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777.
19. Jacquemont B., Roizman B. RNA synthesis in cells infected with herpes simplex virus. X. Properties of viral symmetric transcripts and of double-stranded RNA prepared from them. J. Virol. 1975, 15:707-713.
20. Janssens S., Beyaert R. A universal role for MyD88 in TLR/IL-1R-mediated signaling. Trends Biochem. Sci. 2002, 27:474-482.
21. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., Otsu K., Tsujimura T., Koh C.S., Reis e Sousa C., Matsuura Y., Fujita T., Akira S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
22. Kawai T., Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 2010, 11:373-384.
23. Klinman D.M. Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat. Rev. Immunol. 2004, 4:249-258.
24. Klinman D.M., Yi A.K., Beaucage S.L., Conover J., Krieg A.M. CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc. Natl. Acad. Sci. USA 1996, 93:2879-2883.
25. Krieg A.M. Therapeutic potential of Toll-like receptor 9 activation. Nat. Rev. Drug Discov. 2006, 5:471-484.
26. Krieg A.M., Wu T., Weeratna R., Efler S.M., Love-Homan L., Yang L., Yi A.K., Short D., Davis H.L. Sequence motifs in adenoviral DNA block immune activation by stimulatory CpG motifs. Proc. Natl. Acad. Sci. USA 1998, 95:12631-12636.
27. Krieg A.M., Yi A.K., Matson S., Waldschmidt T.J., Bishop G.A., Teasdale R., Koretzky G.A., Klinman D.M. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 1995, 374:546-549.
28. Krug A., Luker G.D., Barchet W., Leib D.A., Akira S., Colonna M. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 2004, 103:1433-1437.
29. Krug A., Rothenfusser S., Hornung V., Jahrsdorfer B., Blackwell S., Ballas Z.K., Endres S., Krieg A.M., Hartmann G. Identification of CpG oligonucleotide sequences with high induction of IFN-alpha/beta in plasmacytoid dendritic cells. Eur. J. Immunol. 2001, 31:2154-2163.
30. Kurt-Jones E.A., Chan M., Zhou S., Wang J., Reed G., Bronson R., Arnold M.M., Knipe D.M., Finberg R.W. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc. Natl. Acad. Sci. USA 2004, 101:1315-1320.
31. Latz E., Schoenemeyer A., Visintin A., Fitzgerald K.A., Monks B.G., Knetter C.F., Lien E., Nilsen N.J., Espevik T., Golenbock D.T. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 2004, 5:190-198.
32. LeBlanc R.A., Pesnicak L., Cabral E.S., Godleski M., Straus S.E. Lack of interleukin-6 (IL-6) enhances susceptibility to infection but does not alter latency or reactivation of herpes simplex virus type 1 in IL-6 knockout mice. J. Virol. 1999, 73:8145-8151.
33. Lima G.K., Zolini G.P., Mansur D.S., Freire Lima B.H., Wischhoff U., Astigarraga R.G., Dias M.F., das Gracas Almeida Silva M., Bela S.R., do Valle Antonelli L.R., Arantes R.M., Gazzinelli R.T., Bafica A., Kroon E.G., Campos M.A. Toll-like receptor (TLR) 2 and TLR9 expressed in trigeminal ganglia are critical to viral control during herpes simplex virus 1 infection. Am. J. Pathol. 2010, 177:2433-2445.
34. Lund J., Sato A., Akira S., Medzhitov R., Iwasaki A. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 2003, 198:513-520.
35. Malmgaard L., Melchjorsen J., Bowie A.G., Mogensen S.C., Paludan S.R. Viral activation of macrophages through TLR-dependent and -independent pathways. J. Immunol. 2004, 173:6890-6898.
36. Marques C.P., Hu S., Sheng W., Lokensgard J.R. Microglial cells initiate vigorous yet non-protective immune responses during HSV-1 brain infection. Virus Res. 2006, 121:1-10.
37. Marshall J.D., Fearon K.L., Higgins D., Hessel E.M., Kanzler H., Abbate C., Yee P., Gregorio J., Cruz T.D., Lizcano J.O., Zolotorev A., McClure H.M., Brasky K.M., Murthy K.K., Coffman R.L., Nest G.V. Superior activity of the type C class of ISS in vitro and in vivo across multiple species. DNA Cell Biol. 2005, 24:63-72.
38. Matsumoto M., Funami K., Tanabe M., Oshiumi H., Shingai M., Seto Y., Yamamoto A., Seya T. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 2003, 171:3154-3162.
39. McCluskie M.J., Cartier J.L., Patrick A.J., Sajic D., Weeratna R.D., Rosenthal K.L., Davis H.L. Treatment of intravaginal HSV-2 infection in mice. a comparison of CpG oligodeoxynucleotides and resiquimod (R-848). Antiviral Res. 2006, 69:77-85.
40. Melchjorsen J. Sensing herpes: more than toll. Rev. Med. Virol. 2012, 22:106-121.
41. Paul R., Koedel U., Winkler F., Kieseier B.C., Fontana A., Kopf M., Hartung H.P., Pfister H.W. Lack of IL-6 augments inflammatory response but decreases vascular permeability in bacterial meningitis. Brain 2003, 126:1873-1882.
42. Peter M., Bode K., Lipford G.B., Eberle F., Heeg K., Dalpke A.H. Characterization of suppressive oligodeoxynucleotides that inhibit Toll-like receptor-9-mediated activation of innate immunity. Immunology 2008, 123:118-128.
43. Pyles R.B., Higgins D., Chalk C., Zalar A., Eiden J., Brown C., Van Nest G., Stanberry L.R. Use of immunostimulatory sequence-containing oligonucleotides as topical therapy for genital herpes simplex virus type 2 infection. J. Virol. 2002, 76:11387-11396.
44. Rutz M., Metzger J., Gellert T., Luppa P., Lipford G.B., Wagner H., Bauer S. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 2004, 34:2541-2550.
45. Sarangi P.P., Kim B., Kurt-Jones E., Rouse B.T. Innate recognition network driving herpes simplex virus-induced corneal immunopathology: role of the toll pathway in early inflammatory events in stromal keratitis. J. Virol. 2007, 81:11128-11138.
46. Sergerie Y., Boivin G., Gosselin D., Rivest S. Delayed but not early glucocorticoid treatment protects the host during experimental herpes simplex virus encephalitis in mice. J. Infect. Dis. 2007, 195:817-825.
47. Stamatovic S.M., Shakui P., Keep R.F., Moore B.B., Kunkel S.L., Van Rooijen N., Andjelkovic A.V. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J. Cereb. Blood Flow Metab. 2005, 25:593-606.
48. Stunz L.L., Lenert P., Peckham D., Yi A.K., Haxhinasto S., Chang M., Krieg A.M., Ashman R.F. Inhibitory oligonucleotides specifically block effects of stimulatory CpG oligonucleotides in B cells. Eur. J. Immunol. 2002, 32:1212-1222.
49. Sun R., Sun L., Bao M., Zhang Y., Wang L., Wu X., Hu D., Liu Y., Yu Y., Wang L. A human microsatellite DNA-mimicking oligodeoxynucleotide with CCT repeats negatively regulates TLR7/9-mediated innate immune responses via selected TLR pathways. Clin. Immunol. 2010, 134:262-276.
50. Takeda K., Akira S. Toll-like receptors in innate immunity. Int. Immunol. 2005, 17:1-14.
51. Takeda S., Miyazaki D., Sasaki S., Yamamoto Y., Terasaka Y., Yakura K., Yamagami S., Ebihara N., Inoue Y. Roles played by toll-like receptor-9 in corneal endothelial cells after herpes simplex virus type 1 infection. Invest. Ophthalmol. Vis. Sci. 2011, 52:6729-6736.
52. Takeuchi O., Akira S. MyD88 as a bottle neck in Toll/IL-1 signaling. Curr. Top. Microbiol. Immunol. 2002, 270:155-167.
53. Tyler K.L. Update on herpes simplex encephalitis. Rev. Neurol Dis. 2004, 1:169-178.
54. Vilela M.C., Mansur D.S., Lacerda-Queiroz N., Rodrigues D.H., Lima G.K., Arantes R.M., Kroon E.G., da Silva Campos M.A., Teixeira M.M., Teixeira A.L. The chemokine CCL5 is essential for leukocyte recruitment in a model of severe Herpes simplex encephalitis. Ann. NY Acad. Sci. 2009, 1153:256-263.
55. Whitley R.J., Kimberlin D.W. Herpes simplex encephalitis: children and adolescents. Semin. Pediatr. Infect. Dis. 2005, 16:17-23.
56. Wilkins C., Gale M. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 2010, 22:41-47.
57. Yang G., Wan M., Zhang Y., Sun L., Sun R., Hu D., Zhou X., Wang L., Wu X., Wang L., Yu Y. Inhibition of a C-rich oligodeoxynucleotide on activation of immune cells in vitro and enhancement of antibody response in mice. Immunology 2010, 131:501-512.