Attenuation of the influenza virus sickness behavior in mice deficient in Toll-like receptor 3

Brain, Behavior, and Immunity

Volumn 24, Issue 2, 2010, Pages 306-315

  Majde, Jeannine A ^a   Kapás, Levente ^b   Bohnet, Stewart G ^a   De, Alok ^c   Krueger, James M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MISSOURI KANSAS CITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acute phase response; Body weight changes; DsRNA; Hypothermia; Influenza; Locomotor activity; Sickness behavior; Sleep changes; Toll like receptor 3; Virus

Indexed keywords

DOUBLE STRANDED RNA; TOLL LIKE RECEPTOR 3; VIRUS RNA;

ACUTE PHASE RESPONSE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; FLU LIKE SYNDROME; HYPOTHERMIA; INFLUENZA VIRUS A; KNOCKOUT MOUSE; LOCOMOTION; MALE; MOUSE; NONHUMAN; NONREM SLEEP; PRIORITY JOURNAL; STRAIN DIFFERENCE; VIRUS IMMUNITY; WEIGHT CHANGE; WEIGHT REDUCTION; WILD TYPE;

ANIMALS; BEHAVIOR, ANIMAL; BODY TEMPERATURE; BODY WEIGHT; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; INFLUENZA A VIRUS, H1N1 SUBTYPE; MALE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; ORTHOMYXOVIRIDAE INFECTIONS; SLEEP; SLEEP STAGES; TOLL-LIKE RECEPTOR 3;

EID: 72649102955     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.10.011     Document Type: Article

References (75)

1. Akira S., and Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunol. Lett. 85 (2003) 85-95
2. Allen I.C., Scull M.A., Moore C.B., Holl E.K., Elvania-TeKippe E., Taxman D.J., Guthrie E.H., Pickles R.J., and Ting J.P.Y. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunology 30 (2009) 556-565
3. Amadori M. The role of IFN-alpha as homeostatic agent in the inflammatory response: a balance between danger and response?. J. Interferon Cytokine Res. 27 (2007) 181-190
4. Baas T., Baskin C.R., Diamond D.L., Garcia-Sastre A., Bielefeldt-Ohmann H., Tumpey T.M., Thomas M.J., Carter V.S., Teal T.H., Van Hoeven N., Proll S., Jacobs J.M., Caldwell Z.R., Gritsenko M.A., Hukkanen R.R., Camp II D.G., Smith R.D., and Katze M.G. Integrated molecular signature of disease: analysis of influenza virus-infected macaques through functional genomics and proteomics. J. Virol. 80 (2006) 10813-10828
5. Boehme K.W., and Compton T. Innate sensing of viruses by toll-like receptors. J. Virol. 78 (2004) 7867-7873
6. Bose S., and Banerjee A.K. Innate immune response against nonsegmented negative strand RNA viruses. J. Interferon Cytokine Res. 23 (2003) 401-412
7. Carpentier P.A., Williams B.R., and Miller S.D. Distinct roles of protein kinase R and toll-like receptor 3 in the activation of astrocytes by viral stimuli. Glia 55 (2007) 239-252
8. Carter W.A., and De Clercq E. Viral infection and host defense. Science 186 (1974) 1172-1178
9. Chen L., Duricka D., Nelson S., Mukherjee S., Bohnet S.G., Taishi P., Majde J.A., and Krueger J.M. Influenza virus-induced sleep responses in mice with targeted disruptions in neuronal or inducible nitric oxide synthases. J. Appl. Physiol. 97 (2004) 17-28
10. Conn C.A., McClellan J.L., Maassab H.F., Smitka C.W., Majde J.A., and Kluger M.J. Cytokines and the acute phase response to influenza virus in mice. Am. J. Physiol. 268 (1995) R78-R84
11. Cunningham C., Campion S., Teeling J., Felton L., and Perry V.H. The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C). Brain Behav. Immun. 21 (2007) 490-502
12. Diebold S.S., Kaisho T., Hemmi H., Akira S., and Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303 (2004) 1529-1531
13. Diebold S.S., Massacrier C., Akira S., Paturel C., Morel Y., and Reis e Sousa C. Nucleic acid agonists for Toll-like receptor 7 are defined by the presence of uridine ribonucleotides. Eur. J. Immunol. 36 (2006) 3256-3267
14. Dogusan Z., Garcia M., Flamez D., Alexopoulou L., Goldman M., Gysemans C., Mathieu C., Libert C., Eizirik D.L., and Rasschaert J. Double-stranded RNA induces pancreatic b-cell apoptosis by activation of the Toll-like receptor 3 and interferon regulatory factor 3 pathways. Diabetes 57 (2008) 1236-1245
15. Edelmann K.H., Richardson-Burns S., Alexopoulou L., Tyler K.L., Flavell R.A., and Oldstone M.B. Does Toll-like receptor 3 play a biological role in virus infections?. Virology 322 (2004) 231-238
16. Eisenacher K., Steinberg C., Reindl W., and Krug A. The role of viral nucleic acid recognition in dendritic cells for innate and adaptive antiviral immunity. Immunobiology 212 (2008) 701-714
17. Fang J., Bredow S., Taishi P., Majde J.A., and Krueger J.M. Synthetic influenza viral double-stranded RNA induces an acute phase response in rabbits. J. Med. Virol. 57 (1999) 198-203
18. Fang J., Sanborn C.K., Renegar K.B., Majde J.A., and Krueger J.M. Influenza viral infections enhance sleep in mice. Proc. Soc. Exp. Biol. Med. 210 (1995) 242-252
19. Fernandez-Sesma A., Marukian S., Ebersole B.J., Kaminski D., Park M.S., Yuen T., Sealfon S.C., Garcia-Sastre A., and Moran T.M. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 80 (2006) 6295-6304
20. Gandhi R., Hayley S., Gibb J., Merali Z., and Anisman H. Influence of poly I:C on sickness behaviors, plasma cytokines, corticosterone and central monoamine activity: moderation by social stressors. Brain Behav. Immun. 21 (2007) 477-489
21. Gantier M.P., and Williams B.R.G. The response of mammalian cells to double-stranded RNA. Cytokine Growth Factor Rev. 18 (2007) 363-371
22. Garcia-Sastre A. Identification and characterization of viral antagonists of type I interferon in negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283 (2004) 249-280
23. Geiser F. Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66 (2004) 239-274
24. Guillot L., Le Goffic R., Bloch S., Escriou N., Akira S., Chignard M., and Si-Tahar M. Involvement of Toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J. Biol. Chem. 280 (2005) 5571-5580
25. Guo Z., Chen L.M., Zeng H., Gomez J.A., Plowden J., Fujita T., Katz J.M., Donis R.O., and Sambhara S. NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am. J. Respir. Cell Mol. Biol. 36 (2007) 263-269
26. Haller O., Staeheli P., and Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie 89 (2007) 812-818
27. Hashimoto M., Furuyashiki M., Kaseya R., Fukada Y., Akimaru M., Aoyama K., Okuno T., Tamura T., Kirikae T., Kirikae F., Eiraku N., Morioka H., Fujimoto Y., Fukase K., Takashige K., Moriya Y., Kusumoto S., and Suda Y. Evidence of immunostimulating lipoprotein existing in the natural lipoteichoic acid fraction. Infect. Immun. 75 (2007) 1926-1932
28. Hidaka F., Matsuo S., Muta T., Takeshige K., Mizukami T., and Nunoi H. A missense mutation of the Toll-like receptor 3 gene in a patient with influenza-associated encephalopathy. Clin. Immunol. 119 (2006) 188-194
29. Ishizaki Y., Takemoto M., Kira R., Kusuhara K., Torisu H., Sakai Y., Sanefuji M., Yukaya N., and Hara T. Association of toll-like receptor 3 gene polymorphism with subacute sclerosing panencephalitis. J. Neurovirol. 14 (2008) 486-491
30. Jhaveri K.A., Trammell R.A., and Toth L.A. Effect of environmental temperature on sleep, locomotor activity, core body temperature and immune responses of C57BL/6J mice. Brain Behav. Immun. 21 (2007) 975-987
31. Kapas L., Bohnet S.G., Traynor T.R., Majde J.A., Szentirmai E., Magrath P., Taishi P., and Krueger J.M. Spontaneous and influenza virus-induced sleep are altered in TNFa double-receptor deficient mice. J. Appl. Physiol. 105 (2008) 1187-1198
32. Kariko K., Bhuyan P., Capodici J., and Weissman D. Small interfering RNAs mediate sequence-independent gene suppression and induce immune activation by signaling through Toll-like receptor 3. J. Immunol. 172 (2004) 6545-6549
33. Kariko K., Ni H., Capodici J., Lamphier M., and Weissman D. MRNA is an endogenous ligand for Toll-like receptor 3. J. Biol. Chem. 279 (2004) 12542-12550
34. 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., and Akira S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441 (2006) 101-105
35. Kawai T., and Akira S. Pathogen recognition with Toll-like receptors. Curr. Opin. Immunol. 17 (2005) 338-344
36. Kawai T., and Akira S. Innate immune recognition of viral infection. Nat. Immunol. 7 (2006) 131-137
37. Kimura-Takeuchi M., Majde J.A., Toth L.A., and Krueger J.M. The role of double-stranded RNA in the induction of the acute phase response in an abortive influenza viral infection. J. Infect. Dis. 166 (1992) 1266-1275
38. Klein M.S., Conn C.A., and Kluger M.J. Behavioral thermoregulation in mice inoculated with influenza virus. Physiol. Behav. 52 (1992) 1133-1139
39. Kozak W., Poli V., Soszynski D., Conn C.A., Leon L.R., and Kluger M.J. Sickness behavior in mice deficient in interleukin-6 during turpentine abscess and influenza pneumonitis. Am. J. Physiol. 272 (1997) R621-R630
40. Kozak W., Zheng H., Conn C.A., Soszynski D., Van der Ploeg L.H.T., and Kluger M.J. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1b deficient mice. Am. J. Physiol. 269 (1995) R969-R977
41. Le Goffic R., Balloy V., Lagranderie M., Alexopoulou L., Escriou N., Flavell R., Chignard M., and Si-Tahar M. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus induced acute pneumonia. PLoS Pathog. 2 (2006) e53
42. Le Goffic R., Pothlichet J., Vitour D., Fujita T., Meurs E., Chignard M., and Si-Tahar M. Influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J. Immunol. 178 (2007) 3368-3372
43. Leavy O. Sensing viruses. Nat. Rev. Immunol. 6 (2006) 492
44. Lee K.H., Youn J.W., Kim H.J., and Seong B.L. Identification and characterization of mutations in the high growth vaccine strain of influenza virus. Arch. Virol. 146 (2001) 369-377
45. Leon L.R. Hypothermia in systemic inflammation: role of cytokines. Front. Biosci. 9 (2004) 1877-1888
46. Levy D.E., and Garcia-Sastre A. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev. 12 (2001) 143-156
47. Leyva-Grado V., Churchill L., Wu M., Williams T.J., Majde J.A., Taishi P., and Krueger J.M. Influenza virus- and cytokine-immunoreactive cells in the murine olfactory and central autonomic nervous systems before and after illness onset. J. Neuroimmunol. 211 (2009) 73-83
48. Majde J.A. Viral double-stranded RNA, cytokines and the flu. J. Interferon Cytokine Res. 20 (2000) 259-272
49. Majde J.A., Bohnet S.G., Ellis G.A., Churchill L., Leyva-Grado V., Wu M., Szentirmai E., Rehman A., and Krueger J.M. Detection of mouse-adapted human influenza virus in the olfactory bulb of mice within hours after intranasal infection. J. Neurovirol. 13 (2007) 399-409
50. Majde J.A., Brown R.K., Jones M.W., Dieffenbach C.W., Maitra N., Krueger J.M., Cady A.B., Smitka C.W., and Maassab H.F. Detection of toxic viral-associated double-stranded RNA (dsRNA) in influenza-infected lung. Microb. Pathogen. 10 (1991) 105-115
51. Majde J.A., Guha-Thakurta N., Chen Z., Bredow S., and Krueger J.M. Spontaneous release of stable viral double-stranded RNA into the extracellular medium by influenza virus-infected MDCK epithelial cells: implications for the viral acute phase response. Arch. Virol. 143 (1998) 2371-2380
52. Marcus P.I. Interferon induction by viruses: one molecule of dsRNA as the threshold for interferon induction. Interferon 5 (1983) 115-180
53. Matskevich A.A., and Moelling K. Dicer is involved in protection against influenza A virus infection. J. Gen. Virol. 88 (2007) 2627-2635
54. Matsumoto M., Funami K., Oshiumi H., and Seya T. Toll-like receptor 3: a link between toll-like receptor, interferon and viruses. Microbiol. Immunol. 48 (2004) 147-154
55. Miettinen M., Sareneva T., Julkunen I., and Matikainen S. IFNs activate toll-like receptor gene expression in viral infections. Genes Immun. 2 (2001) 349-355
56. Phipps-Yonas H., Seto J., Sealfon S.C., Moran T.M., and Fernandez-Sesma A. Interferon-b pretreatment of conventional and plasmacytoid human dendritic cells enhances their activation by influenza virus. PLoS Pathog. 4 (2008) e1000193
57. Pichlmair A., and Reis e Sousa C. Innate recognition of viruses. Immunology 27 (2007) 370-383
58. Pichlmair A., Schulz O., Tan C.P., Naslund T.I., Liljestrom P., Weber F., and Reis e Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314 (2006) 997-1001
59. Reading P.C., Morey L.S., Crouch E.C., and Anders E.M. Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J. Virol. 71 (1997) 8204-8212
60. Reading P.C., Tate M.D., Pickett D.L., and Brooks A.G. Glycosylation as a target for recognition of influenza viruses by the innate immune system. Adv. Exp. Med. Biol. 598 (2007) 279-292
61. + T cells and augments their antigen-specific responses upon their adoptive transfer into naive recipient mice. Vaccine 27 (2009) 549-557
62. Sancho-Shimizu V., Zhang S.Y., Abel L., Tardieu M., Rozenberg F., Jouanguy E., and Casanova J.L. Genetic susceptibility to herpes simplex virus 1 encephalitis in mice and humans. Curr. Opin. Allergy Clin. Immunol. 7 (2007) 495-505
63. Schroder M., and Bowie A.G. TLR3 in antiviral immunity: key player or bystander?. Trends Immunol. 26 (2005) 462-468
64. Seya T., and Matsumoto M. The extrinsic RNA-sensing pathway for adjuvant immunotherapy of cancer. Cancer Immunol. Immunother. 58 (2009) 1175-1184
65. Toth L.A., Rehg J.E., and Webster R.G. Strain differences in sleep and other pathophysiological sequelae of influenza virus infection in naive and immunized mice. J. Neuroimmunol. 58 (1995) 89-99
66. Traynor T.R., Majde J.A., Bohnet S.G., and Krueger J.M. Sleep and body temperature responses in an acute viral infection model are altered in interferon type I receptor-deficient mice. Brain Behav. Immun. 20 (2006) 290-299
67. Traynor T.R., Majde J.A., Bohnet S.G., and Krueger J.M. Interferon type I receptor-deficient mice have altered disease symptoms in response to influenza virus. Brain Behav. Immun. 21 (2007) 311-322
68. Ueta M. Innate immunity of the ocular surface and ocular surface inflammatory disorders. Cornea 27 Suppl. 1 (2008) S31-S40
69. Vercammen E., Staal J., and Beyaert R. Sensing of viral infection and activation of innate immunity by Toll-like receptor 3. Clin. Microbiol. Rev. 21 (2008) 13-25
70. Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., and Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 10 (2004) 1366-1373
71. Wang Z., Xiang L., Shao J., and Yuan Z. The 3′ CCACCA sequence of tRNAAla(UGC) is the motif that is important in inducing Th1-like immune response, and this motif can be recognized by Toll-like receptor 3. Clin. Vaccine Immunol. 13 (2006) 733-739
72. Weber F., Wagner V., Rasmussen S.B., Hartmann R., and Paludan S.R. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 80 (2006) 5059-5064
73. Zhang S.Y., Boisson-Dupuis S., Chapgier A., Yang K., Bustamante J., Puel A., Picard C., Abel L., Jouanguy E., and 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
74. Zhang S.Y., Jouanguy E., Sancho-Shimizu V., von Bernuth H., Yang K., Abel L., Picard C., Puel A., and Casanova J.L. Human Toll-like receptor-dependent induction of interferons in protective immunity to viruses. Immunol. Rev. 220 (2007) 225-236
75. 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., Heron B., Vallee L., Quintana-Murci L., Hovnanian A., Rozenberg F., Vivier E., Geissmann F., Tardieu M., Abel L., and Casanova J.L. TLR3 deficiency in patients with herpes simplex encephalitis. Science 317 (2007) 1522-1527