TLR3 mediated innate immune response in mice brain following infection with Chikungunya virus

Virus Research

Volumn 189, Issue , 2014, Pages 194-205

  Priya, Raj ^a   Patro, I K ^b   Parida, M M ^a  

^a Defence Research/Devt Establishment   (India)

^b JIWAJI UNIVERSITY   (India)

Author keywords

Chikungunya; Innate immune response; Neuropathogenesis; TLR

Indexed keywords

BETA INTERFERON; CHIKUNGUNYA ALPHAVIRUS VACCINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INACTIVATED VIRUS VACCINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 4; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; IMMUNOLOGICAL ADJUVANT; TLR3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; BRAIN NERVE CELL; CEREBELLUM; CHIKUNGUNYA; CHIKUNGUNYA ALPHAVIRUS; CONTROLLED STUDY; CXCL 10 GENE; CYTOKINE PRODUCTION; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; IFN BETA GENE; IL 4 GENE; IL 6 GENE; IMMUNOHISTOCHEMISTRY; IMMUNOSTIMULATION; INNATE IMMUNITY; ISG 15 GENE; MALE; MCP 1 GENE; MOUSE; MX 2 GENE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OAS 3 GENE; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TICAM 1 GENE; TLR3 GENE; TRAF 6 GENE; UPREGULATION; VIRAL CLEARANCE; VIRUS MUTATION; VIRUS NEUTRALIZATION; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TITRATION; ANIMAL; BAGG ALBINO MOUSE; BRAIN; HUMAN; IMMUNOLOGY; NEWBORN; PATHOLOGY; SURVIVAL; VIROLOGY; VIRUS LOAD;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANIMALS, NEWBORN; BRAIN; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; FEMALE; GENE EXPRESSION PROFILING; HUMANS; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; MALE; MICE, INBRED BALB C; POLY I-C; SURVIVAL ANALYSIS; TOLL-LIKE RECEPTOR 3; VIRAL LOAD;

EID: 84905981118     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2014.05.010     Document Type: Article

References (59)

1. Abere B., Wikan N., Ubol S., Auewarakul P., Paemanee A., Kittisenachai S., Roytrakul S., Smith D.R. Proteomic analysis of chikungunya virus in infected microglia cells. PloS ONE 2012, 7:e34800.
2. Abraham R., Mudaliar P., Padmanabhan A., Sreekumar E. Induction of cytopathogenicity in human glioblastoma cells by Chikungunya virus. PLoS ONE 2012, 10.1371/journal.pone.0075854.
3. Brehin A.C., Casademont I., Frenkiel M.P., Julier C., Sakuntabhai A., Despres P. The large form of human 2',5'-Oligoadenylate Synthetase (OAS3) exerts antiviral effect against Chikungunya virus. Virology 2009, 384:216-222.
4. Caskey M., Lefebvre F., Filali-Mouhim A., Cameron M.J., Goulet J.P., Haddad E.K., Breton G., Trumpfheller C., Pollak S., Shimeliovich I., Duque-Alarcon A., Pan L., Nelkenbaum A., Salazar A.M., Schlesinger S.J., Steinman R.M., Sékaly R.P. Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. J. Exp. Med. 2011, 208:2357-2366.
5. Chandak N.H., Kashyap R.S., Kabra D., Karandikar P., Saha S.S., Morey S.H., Purohit H.J., Taori G.M., Daginawala H.F. Neurological complications of Chikungunya virus infection. Neurol. India 2009, 57:177-180.
6. Chatterjee S.N., Sarkar J.K. Electron microscopic studies of suckling mouse brain cells infected with Chikungunya virus. Indian J. Exp. Biol. 1965, 3:227-234.
7. Couderc T., Chretien F., Schilte C., Disson O., Brigitte M., Guivel-Benhassine F., Touret Y., Barau G., Cayet N., Schuffenecker I., Desprès P., Arenzana-Seisdedos F., Michault A., Albert M.L., Lecuit M. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog. 2008, 4:e29.
8. Dhanwani R., Khan M., Bhaskar A.S., Singh R., Patro I.K., Rao P.V., Parida M.M. Characterization of Chikungunya virus infection in human neuroblastoma SH-SY5Y cells: role of apoptosis in neuronal cell death. Virus Res. 2012, 163:563-572.
9. Dixit E., Boulant S., Zhang Y., Lee A.S., Odendal l.C., Shum B., Hacohen N., Chen Z.J., Whelan S.P., Fransen M., Nibert M.L., Superti-Furga G., Kagan J.C. Peroxisomes are signaling platforms for antiviral innate immunity. Cell 2010, 141:668-681.
10. Economopoulou A., Dominguez M., Helynck B., Sissoko D., Wichmann O., Quenel P., Germonneau P., Quatresous I. Atypical Chikungunya virus infections: clinical manifestations, mortality and risk factors for severe disease during the 2005-2006 outbreak on Reunion. Epidemiol. Infect. 2009, 137:534-541.
11. Ernould S., Walters H., Alessandri J.L., Llanas B., Jaffar M.C., Robin S., Attali T., Ramful D., Combes J.C. Aspects pediatriques de l'epidemie De Chikungunya 2005-2006 a Saint-Denis, ile de la Réunion. Arch. Pediatr. 2008, 15:253-262.
12. Gad H.H., Paulous S., Belarbi E., Diancourt L., Drosten C.K., Kümmerer B.M., Plate A.E., Caro V., Despr P. The E2-E166K substitution restores Chikungunya virus growth in OAS3 expressing cells by acting on viral entry. Virology 2012, 434:27-37.
13. Griffin D., Levine B., Tyor W., Ubol S., Despres P. The role of antibody in recovery from alphavirus encephalitis. Immunol. Rev. 1997, 159:155-161.
14. Grivard P., Le Roux K., Laurent P., Fianu A., Perrau J., Gigan J., Hoarau G., Grondin N., Staikowsky F., Favier F., Michault A. Molecular and serological diagnostic of Chikungunya virus infection. Pathol. Biol. 2007, 55:490-494.
15. Guidotti L.G., Chisari F.V. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu. Rev. Immunol. 2001, 19:65-91.
16. Hausmann J., Pagenstecher A., Baur K., Richter K., Rziha H.J., Staeheli P. CD8 T cells require gamma interferon to clear borna disease virus from the brain and prevent immune system-mediated neuronal damage. J. Virol. 2005, 79:13509-13518.
17. Her Z., Malleret B., Chan B., Ong E.K., Wong S.C., Kwek D.J., Tolou H., Lin R.T., Tambyah P.A., Rénia L., Ng L.F. Active infection of human blood monocytes by Chikungunya virus triggers an innate immune response. J. Immunol. 2010, 184:5903-5913.
18. Hoarau J.J., Bandjee M.C.J., Trotot P.K., Das T., Li-Pat-Yuen G., Dassa B., Denizot M., Guichard E., Ribera A., Henni T., Tallet F., Moiton M.P., Gauzère B.A., Bruniquet S., Bandjee Z.J., Morbidelli P., Martigny G., Jolivet M., Gay F., Grandadam M., Tolou H., Vieillard V., Debré P., Brigitte Autran B., Gasque P. Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response. J. Immunol. 2010, 184(10):5914-5927.
19. Jin H.K., Yoshimatsu K., Takada A., Ogino M., Asano A., Arikawa J., Watanabe T. Mouse Mx2 protein inhibits hantavirus but not influenza virus replication. Arch. Virol. 2001, 146:41-49.
20. Khan M., Dhanwani R., Rao P.V., Parida M. Subunit vaccine formulations based on recombinant envelope proteins of Chikungunya virus elicit balanced Th1/Th2 response and virus-neutralizing antibodies in mice. Virus Res. 2012, 167:236-246.
21. Khan M., Dhanwani R., Kumar J.S., Rao P.V.L., Parida M. Comparative evaluation of the diagnostic potential of recombinant envelope proteins and native cell culture purified viral antigens of Chikungunya virus. J. Med. Virol. 2013, 10.1002/jmv.23752.
22. Kim D., Niewiesk S. Synergistic induction of interferon a through TLR-3 and TLR-9 agonists identifies CD21 as interferon a receptor for the B cell response. PLoS Pathog. 2013, 9:e1003233.
23. Kumar J.S., Khan M., Gupta G., Bhoopati M., Rao P.V.L., Parida M.M. Production, characterization, and application of monoclonal antibodies specific to recombinant (E2) structural protein in antigen-capture ELISA for clinical diagnosis of Chikungunya virus. Viral. Immunol. 2012, 25(2):153-160.
24. Lee J., Chan S.L., Mattson M.P. Adverse effect of a presenilin-1 mutation in microglia results in enhanced nitric oxide and inflammatory cytokine responses to immune challenge in the brain. Neuromolecular Med. 2002, 2:29-45.
25. Lemant J., Boisson V., Winer A., Thibault L., Andre H., Tixier F., Lemercier M., Antok E., Cresta M.P., Grivard P., Besnard M., Rollot O., Favier F., Huerre M., Campinos J.L., Michault A. Serious acute Chikungunya virus infection requiring intensive care during the Reunion Island outbreak in 2005-2006. Crit. Care Med. 2008, 36:2536-2541.
26. Lenschow D.J., Lai C., Frias-Staheli N., Giannakopoulos N.V., Lutz A., Wolff T., Osiak A., Levine B., Schmidt R.E., García-Sastre A., Leib D.A., Pekosz A., Knobeloch K.P., Horak I., Virgin H.W. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1371-1376.
27. Li Y.G., Siripanyaphinyo U., Tumkosit U., Noranate N., Nuegoonpipat A., Pan Y., Kameoka M., Kurosu T., Ikuta K., Takeda N., Anantapreecha S. Poly I: C, an agonist of toll like receptor-3, inhibits replication of the Chikungunya virus in BEAS-2B cells. Virol. J. 2012, 9:114.
28. T Method. Methods 2011, 25:402-408.
29. Matthews A.E., Weiss S.R., Shlomchik M.J., Hannum L.G., Gombold J.L., Paterson Y. Antibody is required for clearance of infectious murine hepatitis virus A59 from the central nervous system, but not in the liver. J. Immunol. 2001, 167:5254-5263.
30. Morrison T.E., Whitmore A.C., Shabman R.S., Lidbury B.A., Mahalingam S., Heise M.T. Characterization of Ross River virus tropism and virus-induced inflammation in a mouse model of viral arthritis and myositis. J. Virol. 2006, 80:737-749.
31. Ng L.F., Chow A., Sun Y.J., Kwek D.J., Lim P.L., Dimatatac F., Ng L.C., Ooi E.E., Choo K.H., Her Z., Leo Y.S. IL-1beta, IL-6 and RANTES as biomarkers of Chikungunya severity. PLoS ONE 2009, 4(1):e4261.
32. Nouranifar R.K., Ali M., Nath J. The earliest manifestation of focal encephalitis on diffusion-weighted MRI. Clin. Imaging 2003, 27:316-320.
33. Oshiumi H., Matsumoto M., Funami K., Akazawa T., Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 2003, 4:161-167.
34. Pathak S., Webb H.E. Possible mechanisms for the transport of Semliki forest virus into and within mouse brain. An electron-microscopic study. J. Neurol. Sci. 1974, 23:175-184.
35. Patterson C.E., Lawrence D.M., Echols L.A., Rall G.F. Immune-mediated protection from measles virus-induced central nervous system disease is noncytolytic and gamma interferon dependent. J. Virol. 2002, 76:4497-4506.
36. Pialoux G., Gaüzère B.A., Jauréguiberry S., Strobel M. Chikungunya, an epidemic arbovirosis. Lancet Infect. Dis. 2007, 7:319-327.
37. Powers A.M., Logue C.H. Changing patterns of Chikungunya virus: reemergence of a zoonotic arbovirus. J. Gen. Virol. 2007, 88:2363-2377.
38. Precious S.W., Webb H.E., Bowen E.T. Isolation and persistence of Chikungunya virus in cultures of mouse brain cells. J. Gen. Virol. 1974, 23:271-279.
39. Priya R., Dhanwani R., Patro I.K., Rao P.V., Parida M.M. Differential regulation of TLR mediated innate immune response of mouse neuronal cells following infection with novel ECSA genotype of Chikungunya virus with and without E1:A226V mutation. Infect. Genet. Evol. 2013, 20:396-406.
40. Rampal S.M., Meena H. Neurological complications in Chikungunya fever. J. Assoc. Physicians India 2007, 55:765-769.
41. Robin S., Ramful D., Le Seach F., Jaffar-Bandjee M.C., Rigou G., Alessandri J.L. Neurologic manifestations of pediatric chikungunya infection. J. Child Neurol. 2008, 23:1028-1035.
42. Rodriguez M., Zoecklein L.J., Howe C.L., Pavelko K.D., Gamez J.D., Nakane S., Papke L.M. Gamma interferon is critical for neuronal viral clearance and protection in a susceptible mouse strain following early intracranial Theiler's murine encephalomyelitis virus infection. J. Virol. 2003, 77:12252-12265.
43. Santosh S.R., Parida M.M., Dash P.K., Pateriya A., Pattnaik B., Pradhan H.K., Tripathi N.K., Ambuj S., Gupta N., Saxena P., Rao P.V.L. Development and evaluation of SYBR Green I-based one-step real-time RT-PCR assay for detection and quantification of Chikungunya virus. J. Clin. Virol. 2007, 39:188-193.
44. Santhosh S.R., Dash P.K., Parida M.M., Khan M., Tiwari M., Rao P.V.L. Comparative full genome analysis revealed E1: A226V shift in 2007 Indian Chikungunya virus isolates. Virus Res. 2008, 135:36-41.
45. Schilte C., Couderc T., Chretien F., Sourisseau M., Gangneux N., Guivel-Benhassine F., Kraxner A., Tschopp J., Higgs S., Michault A., Arenzana-Seisdedos F., Colonna M., Peduto L., Schwartz O., Lecuit M., Albert M.L. Type I IFN controls Chikungunya virus via its action on nonhematopoietic cells. J. Exp. Med. 2010, 207:429-442.
46. Schoggins J.W., Wilson S.J., Panis M., Murphy M.Y., Jones C.T., Bieniasz P., Rice C.M. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472:481-485.
47. Sharma A., Maheshwari R.K. Oligonucleotide array analysis of Toll-like receptors and associated signaling genes in Venezuelan equine encephalitis virus infected mouse brain. J. Gen. Virol. 2009, 90:1836-1847.
48. Sissoko D., Malvy D., Ezzedine K., Renault P., Moscetti F., Ledrans M., Pierre V. Post-epidemic Chikungunya disease on Reunion Island: course of rheumatic manifestations and associated factors over a 15-month period. PLoS Negl. Trop. Dis. 2009, 3:e389.
49. Soilu-Hanninen M., Eralinna J.P., Hukkanen V., Roytta M., Salmi A.A., Bieniasz P., Rice C.M. Semliki Forest virus infects mouse brain endothelial cells and causes blood-brain barrier damage. J. Virol. 1994, 68:6291-6298.
50. Stephen E.L., Sammons M.L., Pannier W.L., Baron S., Spertzel R.O. Effect of a nuclease-resistant derivative of polyriboinosinic-polyribocytidylic acid complex on yellow fever in rhesus monkeys (Macaca mulatta). J. Infect. Dis. 1977, 136:122-126.
51. Tiwari M., Parida M.M., Santhosh S.R., Khan M., Dash P.K., Rao P.V.L. Assessment of immunogenic potential of Vero adapted formalin inactivated vaccine derived from novel ECSA genotype of Chikungunya virus. Vaccine 2009, 27(18):2513-2522.
52. Tournebize P., Charlin C., Lagrange M. Neurological manifestations in Chikungunya: about 23 cases collected in Reunion Island. Rev. Neurol. (Paris) 2009, 165:48-51.
53. Wauquier N., Becquart P., Nkoghe D., Padilla C., Ndjoyi-Mbiguino A., Leroy E.M. The acute phase of chikungunya virus infection in humans is associated with strong innate immunity and T CD8 cell activation. J. Infect. Dis. 2011, 204:115-123.
54. Werneke S., Schilte C., Rohatgi A., Monte K.J., Michault A., Arenzana-Seisdedos F., Vanlandingham D.L., Higgs S., Fontanet A. ISG15 is critical in the control of Chikungunya virus infection independent of UbE1L mediated conjugation. PLoS Pathogen. 2011, 10.1371/journal.ppat.1002322.
55. White L.K., Sali T., Alvarado D., Gatti E., Pierre P., Streblow D., Defilippis V.R. Chikungunya virus induces IPS-1-dependent innate immune activation and protein kinase R-independent translational shutoff. J. Virol. 2011, 85:606-620.
56. Yamada K., Takasaki T., Nawa M., Kurane I. Virus isolation as one of the diagnostic methods for dengue virus infection. J. Clin. Virol. 2002, 24:203-209.
57. 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., Casanova J.L. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007, 317:1522-1527.
58. Zhao J., Wohlford-Lenane C., Zhao J., Fleming E., Thomas E., Lane T.E., McCray P.B., Perlman S. Intranasal treatment with poly (I·C) protects aged mice from lethal respiratory virus infections. J. Virol. 2012, 88(21):11416-11424.
59. Ziegler S.A., Lu L., da Rosa A.P., Xiao S.Y., Tesh R.B. An animal model for studying the pathogenesis of Chikungunya virus infection. Am. J. Trop. Med. Hyg. 2008, 79:133-139.