Antibodies are not required to a protective immune response against dengue virus elicited in a mouse encephalitis model

Virology

Volumn 487, Issue , 2016, Pages 41-49

  Amorim, Jaime Henrique ^a   dos Santos Alves, Rúbens Prince ^a   Bizerra, Raíza ^a   Araújo Pereira, Sara ^a   Ramos Pereira, Lennon ^a   Nascimento Fabris, Denicar Lina ^a   Santos, Robert Andreata ^a   Romano, Camila Malta ^a   de Souza Ferreira, Luís Carlos ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Antibodies; Dengue; Immune response; Nonstructural proteins; T lymphocytes

Indexed keywords

ANTIBODY; GAMMA INTERFERON; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5; ANTISERUM; VIRUS ANTIBODY; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ARTICLE; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 2; ENCEPHALITIS; EXPERIMENTAL MODEL; HUMORAL IMMUNITY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T CELL DEPLETION; VIRUS STRAIN; VIRUS SURVIVAL; AEDES; ANIMAL; CELL LINE; DENGUE VIRUS; DISEASE MODEL; ENCEPHALITIS, VIRAL; IMMUNOLOGY; LYMPHOCYTE DEPLETION; PASSIVE IMMUNIZATION; RHESUS MONKEY; VIROLOGY;

AEDES; ANIMALS; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; DENGUE; DENGUE VIRUS; DISEASE MODELS, ANIMAL; ENCEPHALITIS, VIRAL; IMMUNE SERA; IMMUNITY, CELLULAR; IMMUNIZATION, PASSIVE; LYMPHOCYTE DEPLETION; MACACA MULATTA; MALE; MICE; MICE, INBRED BALB C; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84944937839     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.10.006     Document Type: Article

References (51)

1. Amorim J.H., Bizerra R., dos Santos Alves R.P., Nascimento Fabris D.L., de Souza Ferreira L.C. Dengue virus models based on mice as experimental hosts. Future Virol. 2015, 10:835-844. 10.2217/fvl.15.48.
2. Amorim J.H., Pereira Bizerra R.S., dos Santos Alves R.P., Sbrogio-Almeida M.E., Levi J.E., Capurro M.L., de Souza Ferreira L.C. A genetic and pathologic study of a DENV2 clinical isolate capable of inducing encephalitis and hematological disturbances in immunocompetent mice. PLoS One 2012, 7:e44984. 10.1371/journal.pone.0044984.
3. Bäck A.T., Lundkvist A. Dengue viruses-an overview. Infect. Ecol. Epidemiol. 2013, 3:1-21. 10.3402/iee.v3i0.19839.
4. Bashyam H.S., Green S., Rothman A.L. Dengue virus-reactive CD8+ T cells display quantitative and qualitative differences in their response to variant epitopes of heterologous viral serotypes. J. Immunol. 2006, 176:2817-2824.
5. Bhatt S., Gething P.W., Brady O.J., Messina J.P., Farlow A.W., Moyes C.L., Drake J.M., Brownstein J.S., Hoen A.G., Sankoh O., Myers M.F., George D.B., Jaenisch T., Wint G.R.W., Simmons C.P., Scott T.W., Farrar J.J., Hay S.I. The global distribution and burden of dengue. Nature 2013, 496:504-507. 10.1038/nature12060.
6. Blaney J.E.J., Matro J.M., Murphy B.R., Whitehead S.S. Recombinant, live-attenuated tetravalent dengue virus vaccine formulations induce a balanced, broad, and protective neutralizing antibody response against each of the four serotypes in rhesus monkeys. J. Virol. 2005, 79:5516-5528. 10.1128/JVI.79.9.5516-5528.2005.
7. Brien J.D., Uhrlaub J.L., Nikolich-Zugich J. West Nile virus-specific CD4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are sufficient for antiviral protection. J. Immunol. 2008, 181:8568-8575.
8. Chevalier G., Suberbielle E., Monnet C., Duplan V., Martin-Blondel G., Farrugia F., Le Masson G., Liblau R., Gonzalez-Dunia D. Neurons are MHC class I-dependent targets for CD8 T cells upon neurotropic viral infection. PLoS Pathog. 2011, 7:e1002393. 10.1371/journal.ppat.1002393.
9. Chiang C.-Y., Huang M.-H., Hsieh C.-H., Chen M.-Y., Liu H.-H., Tsai J.-P., Li Y.-S., Chang C.-Y., Liu S.-J., Chong P., Leng C.-H., Chen H.-W. Dengue-1 envelope protein domain III along with PELC and CpG oligodeoxynucleotides synergistically enhances immune responses. PLoS Negl. Trop. Dis. 2012, 6:e1645. 10.1371/journal.pntd.0001645.
10. Cockburn J.J.B., Navarro Sanchez M.E., Goncalvez A.P., Zaitseva E., Stura E.A., Kikuti C.M., Duquerroy S., Dussart P., Chernomordik L.V., Lai C.-J., Rey F.A. Structural insights into the neutralization mechanism of a higher primate antibody against dengue virus. EMBO J. 2012, 31:767-779. 10.1038/emboj.2011.439.
11. Gao G., Wang Q., Dai Z., Calcedo R., Sun X., Li G., Wilson J.M. Adenovirus-based vaccines generate cytotoxic T lymphocytes to epitopes of NS1 from dengue virus that are present in all major serotypes. Hum. Gene Ther. 2008, 19:927-936. 10.1089/hum.2008.011.
12. Gehrmann J., Matsumoto Y., Kreutzberg G.W. Microglia: intrinsic immuneffector cell of the brain. Brain Res. Rev. 1995, 20:269-287. 10.1016/0165-0173(94)00015-H.
13. Gil L., López C., Blanco A., Lazo L., Martín J., Valdés I., Romero Y., Figueroa Y., Guillén G., Hermida L. The cellular immune response plays an important role in protecting against dengue virus in the mouse encephalitis model. Viral Immunol. 2009, 22:23-30. 10.1089/vim.2008.0063.
14. Guirakhoo F., Arroyo J., Pugachev K.V., Miller C., Zhang Z.X., Weltzin R., Georgakopoulos K., Catalan J., Ocran S., Soike K., Ratterree M., Monath T.P. Construction, safety, and immunogenicity in nonhuman primates of a chimeric yellow fever-dengue virus tetravalent vaccine. J. Virol. 2001, 75:7290-7304. 10.1128/JVI.75.16.7290-7304.2001.
15. Guirakhoo F., Pugachev K., Zhang Z., Myers G., Levenbook I., Draper K., Lang J., Ocran S., Mitchell F., Parsons M., Brown N., Brandler S., Fournier C., Barrere B., Rizvi F., Travassos A., Nichols R., Trent D., Monath T. Safety and efficacy of chimeric yellow fever-dengue virus tetravalent vaccine formulations in nonhuman primates. J. Virol. 2004, 78:4761-4775.
16. Guirakhoo F., Weltzin R., Chambers T.J., Zhang Z.X., Soike K., Ratterree M., Arroyo J., Georgakopoulos K., Catalan J., Monath T.P. Recombinant chimeric yellow fever-dengue type 2 virus is immunogenic and protective in nonhuman primates. J. Virol. 2000, 74:5477-5485.
17. Guy B., Saville M., Lang J. Development of Sanofi Pasteur tetravalent dengue vaccine. Hum. Vaccin 2010, 6. doi:10.4161.hv.6.9.12739.
18. Guzman M.G., Halstead S.B., Artsob H., Buchy P., Farrar J., Gubler D.J., Hunsperger E., Kroeger A., Margolis H.S., Martínez E., Nathan M.B., Pelegrino J.L., Simmons C., Yoksan S., Peeling R.W. Dengue: a continuing global threat. Nat. Rev. Microbiol 2010, 8:S7-S16. 10.1038/nrmicro2460.
19. Guzman M.G., Harris E. Dengue. Lancet 2015, 385:453-465. 10.1016/S0140-6736(14)60572-9.
20. Han Y.W., Singh S.K., Eo S.K. The roles and perspectives of toll-like receptors and CD4(+) helper T cell subsets in acute viral encephalitis. Immune Netw. 2012, 12:48-57. 10.4110/in.2012.12.2.48.
21. Horstick O., Martinez E., Guzman M.G., Martin J.L.S., Ranzinger S.R. WHO dengue case classification 2009 and its usefulness in practice: an expert consensus in the Americas. Pathog. Glob. Health 2015, 109:19-25. 2047773215Y0000000003. 10.1179/2047773215Y.0000000003.
22. Knickelbein J.E., Khanna K.M., Yee M.B., Baty C.J., Kinchington P.R., Hendricks R.L. Noncytotoxic lytic granule-mediated CD8+ T cell inhibition of HSV-1 reactivation from neuronal latency. Science 2008, 322:268-271. 10.1126/science.1164164.
23. Kurane I., Innis B.L., Nimmannitya S., Nisalak A., Meager A., Janus J., Ennis F.A. Activation of T lymphocytes in dengue virus infections. High levels of soluble interleukin 2 receptor, soluble CD4, soluble CD8, interleukin 2, and interferon-gamma in sera of children with dengue. J. Clin. Investig. 1991, 88:1473-1480. 10.1172/JCI115457.
24. Liu T., Chambers T.J. Yellow fever virus encephalitis: properties of the brain-associated T-cell response during virus clearance in normal and gamma interferon-deficient mice and requirement for CD4+ lymphocytes. J. Virol. 2001, 75:2107-2118. 10.1128/JVI.75.5.2107-2118.2001.
25. Liu T., Khanna K.M., Carriere B.N., Hendricks R.L. Gamma interferon can prevent herpes simplex virus type 1 reactivation from latency in sensory neurons. J. Virol. 2001, 75:11178-11184. 10.1128/JVI.75.22.11178-11184.2001.
26. Lok S.-M., Kostyuchenko V., Nybakken G.E., Holdaway H.A., Battisti A.J., Sukupolvi-Petty S., Sedlak D., Fremont D.H., Chipman P.R., Roehrig J.T., Diamond M.S., Kuhn R.J., Rossmann M.G. Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nat. Struct. Mol. Biol. 2008, 15:312-317. 10.1038/nsmb.1382.
27. Lundegaard C., Lamberth K., Harndahl M., Buus S., Lund O., Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res. 2008, 36:W509-W512. 10.1093/nar/gkn202.
28. Luria-Perez R., Cedillo-Barron L., Santos-Argumedo L., Ortiz-Navarrete V.F., Ocaña-Mondragon A., Gonzalez-Bonilla C.R. A fusogenic peptide expressed on the surface of Salmonella enterica elicits CTL responses to a dengue virus epitope. Vaccine 2007, 25:5071-5085. 10.1016/j.vaccine.2007.03.047.
29. Moutaftsi M., Peters B., Pasquetto V., Tscharke D.C., Sidney J., Bui H.-H., Grey H., Sette A. A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat. Biotechnol. 2006, 24:817-819. 10.1038/nbt1215.
30. Murali-Krishna K., Ravi V., Manjunath R. Protection of adult but not newborn mice against lethal intracerebral challenge with Japanese encephalitis virus by adoptively transferred virus-specific cytotoxic T lymphocytes: requirement for L3T4+ T cells. J. Gen. Virol. 1996, 77(Pt 4):705-714.
31. Murgue B., Roche C., Chungue E., Deparis X. Prospective study of the duration and magnitude of viraemia in children hospitalised during the 1996-1997 dengue-2 outbreak in French Polynesia. J. Med. Virol. 2000, 60:432-438.
32. Pierson T.C., Kuhn R.J. Capturing a virus while it catches its breath. Structure 2012, 20:200-202. 10.1016/j.str.2012.01.014.
33. Rivino L., Kumaran E.A., Thein T.-L., Too C.T., Hao Gan V.C., Hanson B.J., Wilder-Smith A., Bertoletti A., Gascoigne N.R.J., Lye D.C., Leo Y.S., Akbar A.N., Kemeny D.M., MacAry P.A. Virus-specific T lymphocytes home to the skin during natural dengue infection. Sci. Transl. Med. 2015, 7:278ra35. 10.1126/scitranslmed.aaa0526.
34. Rivino L., Kumaran E.A.P., Jovanovic V., Nadua K., Teo E.W., Pang S.W., Teo G.H., Gan V.C.H., Lye D.C., Leo Y.S., Hanson B.J., Smith K.G.C., Bertoletti A., Kemeny D.M., MacAry P.A. Differential targeting of viral components by CD4+ versus CD8+ T lymphocytes in dengue virus infection. J. Virol 2013, 87:2693-2706. 10.1128/JVI.02675-12.
35. Roehrig J.T., Hombach J., Barrett A.D.T. Guidelines for plaque-reduction neutralization testing of human antibodies to dengue viruses. Viral Immunol. 2008, 21:123-132. 10.1089/vim.2008.0007.
36. Romano C.M., Lauck M., Salvador F.S., Lima C.R., Villas-Boas L.S., Araújo E.S.A., Levi J.E., Pannuti C.S., O'Connor D., Kallas E.G. Inter- and intra-host viral diversity in a large seasonal DENV2 outbreak. PLoS One 2013, 8:e70318. 10.1371/journal.pone.0070318.
37. Sabchareon A., Wallace D., Sirivichayakul C., Limkittikul K., Chanthavanich P., Suvannadabba S., Jiwariyavej V., Dulyachai W., Pengsaa K., Wartel T.A., Moureau A., Saville M., Bouckenooghe A., Viviani S., Tornieporth N.G., Lang J. Protective efficacy of the recombinant, live-attenuated, CYD tetravalent dengue vaccine in Thai schoolchildren: a randomised, controlled phase 2b trial. Lancet 2012, 380:1559-1567. 10.1016/S0140-6736(12)61428-7.
38. Sabin A.B. Research on dengue during World War II. Am. J. Trop. Med. Hyg. 1952, 1:30-50.
39. Sitati E.M., Diamond M.S. CD4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J. Virol. 2006, 80:12060-12069. 10.1128/JVI.01650-06.
40. Teoh E.P., Kukkaro P., Teo E.W., Lim A.P.C., Tan T.T., Yip A., Schul W., Aung M., Kostyuchenko V.A., Leo Y.S., Chan S.H., Smith K.G.C., Chan A.H.Y., Zou G., Ooi E.E., Kemeny D.M., Tan G.K., Ng J.K.W., Ng M.L., Alonso S., Fisher D., Shi P.-Y., Hanson B.J., Lok S.-M., MacAry P.A. The structural basis for serotype-specific neutralization of dengue virus by a human antibody. Sci. Transl. Med. 2012, 4:139ra83. 10.1126/scitranslmed.3003888.
41. Vaughn D.W., Green S., Kalayanarooj S., Innis B.L., Nimmannitya S., Suntayakorn S., Endy T.P., Raengsakulrach B., Rothman A.L., Ennis F.A., Nisalak A. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J. Infect. Dis. 2000, 18:2-9. 10.1086/315215.
42. Villar L., Dayan G.H., Arredondo-García J.L., Rivera D.M., Cunha R., Deseda C., Reynales H., Costa M.S., Morales-Ramírez J.O., Carrasquilla G., Rey L.C., Dietze R., Luz K., Rivas E., Montoya M.C.M., Supelano M.C., Zambrano B., Langevin E., Boaz M., Tornieporth N., Saville M., Noriega F. Efficacy of a tetravalent dengue vaccine in children in Latin America. N. Engl. J. Med. 2014, 372. 141103114505002. 10.1056/NEJMoa1411037.
43. Wang P., Sidney J., Dow C., Mothé B., Sette A., Peters B. A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach. PLoS Comput. Biol. 2008, 4:e1000048. 10.1371/journal.pcbi.1000048.
44. Weiskopf D., Angelo M.A., Bangs D.J., Sidney J., Paul S., Peters B., de Silva A.D., Lindow J.C., Diehl S.A., Whitehead S., Durbin A., Kirkpatrick B., Sette A. The human CD8+ T cell responses induced by a live attenuated tetravalent dengue vaccine are directed against highly conserved epitopes. J. Virol. 2015, 89:120-128. 10.1128/JVI.02129-14.
45. Weiskopf D., Bangs D.J., Sidney J., Kolla R.V., De Silva A.D., de Silva A.M., Crotty S., Peters B., Sette A. Dengue virus infection elicits highly polarized CX3CR1+ cytotoxic CD4+ T cells associated with protective immunity. Proc. Natl. Acad. Sci. USA 2015, 112:E4256-E4263. 10.1073/pnas.1505956112.
46. Whitehead S.S., Blaney J.E., Durbin A.P., Murphy B.R. Prospects for a dengue virus vaccine. Nat. Rev. Microbiol. 2007, 5:518-528. 10.1038/nrmicro1690.
47. Yauch L.E., Prestwood T.R., May M.M., Morar M.M., Zellweger R.M., Peters B., Sette A., Shresta S. CD4+ T cells are not required for the induction of dengue virus-specific CD8+ T cell or antibody responses but contribute to protection after vaccination. J. Immunol. 2010, 185:5405-5416. 10.4049/jimmunol.1001709.
48. Yoshida T., Omatsu T., Saito A., Katakai Y., Iwasaki Y., Kurosawa T., Hamano M., Higashino A., Nakamura S., Takasaki T., Yasutomi Y., Kurane I., Akari H. Dynamics of cellular immune responses in the acute phase of dengue virus infection. Arch. Virol. 2013, 158:1209-1220. 10.1007/s00705-013-1618-6.
49. Yun N.E., Peng B.-H., Bertke A.S., Borisevich V., Smith J.K., Smith J.N., Poussard A.L., Salazar M., Judy B.M., Zacks M.A., Estes D.M., Paessler S. CD4+ T cells provide protection against acute lethal encephalitis caused by Venezuelan equine encephalitis virus. Vaccine 2009, 27:4064-4073. 10.1016/j.vaccine.2009.04.015.
50. Zellweger R.M., Miller R., Eddy W.E., White L.J., Johnston R.E., Shresta S. Role of humoral versus cellular responses induced by a protective dengue vaccine candidate. PLoS Pathog. 2013, 9:e1003723. 10.1371/journal.ppat.1003723.
51. Zhang Z.-S., Yan Y.-S., Weng Y.-W., Huang H.-L., Li S.-Q., He S., Zhang J.-M. High-level expression of recombinant dengue virus type 2 envelope domain III protein and induction of neutralizing antibodies in BALB/C mice. J. Virol. Methods 2007, 143:125-131. 10.1016/j.jviromet.2007.02.012.