CD8+ T cell immune response in immunocompetent mice during Zika virus infection

Journal of Virology

Volumn 91, Issue 22, 2017, Pages

  Huang, Huarong ^a,b   Li, Shihua ^a   Zhang, Yongli ^d   Han, Xiaojuan ^a,b   Jia, Baoqian ^a   Liu, Hongtao ^a,b   Liu, Dandan ^a,b   Tan, Shuguang ^a   Wang, Qihui ^a   Bi, Yuhai ^a   Liu, William J ^d   Hou, Baidong ^c   Gao, George Fu ^a,b,d,e   Zhang, Fuping ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

^d CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^e INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

CD8+ T cell; Central nervous system; Cross protection; Immunocompetent mouse model; ZIKV

Indexed keywords

CYTOKINE; EPITOPE; TETRAMER; ZIKA VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; CD8+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CROSS PROTECTION; DENGUE; FEMALE; IMMUNE RESPONSE; IMMUNOCOMPETENCE; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; VIRUS DETECTION; ZIKA FEVER; ADOPTIVE TRANSFER; ANIMAL; CELLULAR IMMUNITY; CHLOROCEBUS AETHIOPS; HAMSTER; IMMUNOLOGY; PATHOLOGY; VERO CELL LINE; ZIKA VIRUS;

ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CERCOPITHECUS AETHIOPS; CRICETINAE; EPITOPES, T-LYMPHOCYTE; IMMUNITY, CELLULAR; MICE; VERO CELLS; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85032283066     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00900-17     Document Type: Article

References (36)

1. Sharma A, Lal SK. 2017. Zika virus: transmission, detection, control, and prevention. Front Microbiol 8:110. https://doi.org/10.3389/fmicb.2017.01602.
2. Dick GW, Kitchen SF, Haddow AJ. 1952. Zika virus I Isolations and serological specificity. Trans R Soc Trop Med Hyg 46:509-20. https://doi.org/10.1016/0035-9203(52)90042-4.
3. Mlakar J, Korva M, Tul N, Popovic M, Poljsak-Prijatelj M, Mraz J, Kolenc M, Resman Rus K, Vesnaver Vipotnik T, Fabjan Vodusek V, Vizjak A, Pizem J, Petrovec M, Avsic Zupanc T. 2016. Zika virus associated with microcephaly. N Engl J Med 374:951-958. https://doi.org/10.1056/NEJMoa1600651.
4. Lucchese G, Kanduc D. 2016. Zika virus and autoimmunity: from microcephaly to Guillain-Barre syndrome, and beyond. Autoimmun Rev 15: 801-808. https://doi.org/10.1016/j.autrev.2016.03.020.
5. Elong Ngono A, Vizcarra EA, Tang WW, Sheets N, Joo Y, Kim K, Gorman MJ, Diamond MS, Shresta S. 2017. Mapping and role of the CD8+ T cell response during primary Zika virus infection in mice. Cell Host Microbe 21:35-46. https://doi.org/10.1016/j.chom.2016.12.010.
6. Lazear HM, Govero J, Smith AM, Platt DJ, Fernandez E, Miner JJ, Diamond MS. 2016. A mouse model of Zika virus pathogenesis. Cell Host Microbe 19:720-730. https://doi.org/10.1016/j.chom.2016.03.010.
7. Manangeeswaran M, Ireland DD, Verthelyi D. 2016. Zika (PRVABC59) infection is associated with T cell infiltration and neurodegeneration in CNS of immunocompetent neonatal C57Bl/6 mice. PLoS Pathog 12: e1006004. https://doi.org/10.1371/journal.ppat.1006004.
8. Winkler CW, Myers LM, Woods TA, Messer RJ, Carmody AB, McNally KL, Scott DP, Hasenkrug KJ, Best SM, Peterson KE. 2017. Adaptive immune responses to Zika virus are important for controlling virus infection and preventing infection in brain and testes. J Immunol 198:3526-3535. https://doi.org/10.4049/jimmunol.1601949.
9. Pardy RD, Rajah MM, Condotta SA, Taylor NG, Sagan SM, Richer MJ. 2017. Analysis of the T cell response to Zika virus and identification of a novel CD8+ T cell epitope in immunocompetent mice. PLoS Pathog 13: e1006184. https://doi.org/10.1371/journal.ppat.1006184.
10. Zust R, Toh YX, Valdes I, Cerny D, Heinrich J, Hermida L, Marcos E, Guillen G, Kalinke U, Shi PY, Fink K. 2014. Type I interferon signals in macrophages and dendritic cells control dengue virus infection: implications for a new mouse model to test dengue vaccines. J Virol 88:7276-7285. https://doi.org/10.1128/JVI.03827-13.
11. Wen J, Tang WW, Sheets N, Ellison J, Sette A, Kim K, Shresta S. 2017. Identification of Zika virus epitopes reveals immunodominant and protective roles for dengue virus cross-reactive CD8+ T cells. Nat Microbiol 2:17036. https://doi.org/10.1038/nmicrobiol.2017.36.
12. Hastings AK, Erickson JJ, Schuster JE, Boyd KL, Tollefson SJ, Johnson M, Gilchuk P, Joyce S, Williams JV. 2015. Role of type I interferon signaling in human metapneumovirus pathogenesis and control of viral replication. J Virol 89:4405-4420. https://doi.org/10.1128/JVI.03275-14.
13. Pinto AK, Daffis S, Brien JD, Gainey MD, Yokoyama WM, Sheehan KC, Murphy KM, Schreiber RD, Diamond MS. 2011. A temporal role of type I interferon signaling in CD8+ T cell maturation during acute West Nile virus infection. PLoS Pathog 7:e1002407. https://doi.org/10.1371/journal.ppat.1002407.
14. Contreras D, Arumugaswami V. 2016. Zika virus infectious cell culture system and the in vitro prophylactic effect of interferons. J Vis Exp https://doi.org/10.3791/54767.
15. Bowen JR, Quicke KM, Maddur MS, O'Neal JT, McDonald CE, Fedorova NB, Puri V, Shabman RS, Pulendran B, Suthar MS. 2017. Zika virus antagonizes type I interferon responses during infection of human dendritic cells. PLoS Pathog 13:e1006164. https://doi.org/10.1371/ journal.ppat.1006164.
16. McDermott DS, Varga SM. 2011. Quantifying antigen-specific CD4 T cells during a viral infection: CD4 T cell responses are larger than we think. J Immunol 187:5568-5576. https://doi.org/10.4049/jimmunol.1102104.
17. Rai D, Pham NL, Harty JT, Badovinac VP. 2009. Tracking the total CD8 T cell response to infection reveals substantial discordance in magnitude and kinetics between inbred and outbred hosts. J Immunol 183: 7672-7681. https://doi.org/10.4049/jimmunol.0902874.
18. Groom JR, Luster AD. 2011. CXCR3 in T cell function. Exp Cell Res 317:620-631. https://doi.org/10.1016/j.yexcr.2010.12.017.
19. Wang Q, Yang Y, Zheng H, Bi Y, Song J, Li L, Gu D, Wang P, Li S, Liu S, Zhao Y, Liu L, Gao G, Liu Y. 2016. Genetic and biological characterization of Zika virus from human cases imported through Shenzhen Port. Chin Sci Bull 61:2463-2474. https://doi.org/10.1360/N972015-00990.
20. Diamond MS. 2003. Evasion of innate and adaptive immunity by flaviviruses. Immunol Cell Biol 81:196-206. https://doi.org/10.1046/j.1440-1711.2003.01157.x.
21. Yauch LE, Prestwood TR, May MM, Morar MM, Zellweger RM, Peters B, Sette A, Shresta S. 2010. 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 185:5405-5416. https:// doi.org/10.4049/jimmunol.1001709.
22. Harrison SC. 2016. Immunogenic cross-talk between dengue and Zika viruses. Nat Immunol 17:1010-1012. https://doi.org/10.1038/ni.3539.
23. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A, Bianchi S, Vanzetta F, Minola A, Jaconi S, Mele F, Foglierini M, Pedotti M, Simonelli L, Dowall S, Atkinson B, Percivalle E, Simmons CP, Varani L, Blum J, Baldanti F, Cameroni E, Hewson R, Harris E, Lanzavecchia A, Sallusto F, Corti D. 2016. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science 353:823-826. https://doi.org/10.1126/science.aaf8505.
24. Yauch LE, Zellweger RM, Kotturi MF, Qutubuddin A, Sidney J, Peters B, Prestwood TR, Sette A, Shresta S. 2009. A protective role for dengue virus-specific CD8+ T cells. J Immunol 182:4865-4873. https://doi.org/ 10.4049/jimmunol.0801974.
25. Kaech SM, Wherry EJ, Ahmed R. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2:251-262. https://doi.org/10.1038/nri778.
26. Krzych U, Dalai S, Zarling S, Pichugin A. 2012. Memory CD8 T cells specific for plasmodia liver-stage antigens maintain protracted protection against malaria. Front Immunol 3:370. https://doi.org/10.3389/ fimmu.2012.00370.
27. Moseman EA, McGavern DB. 2013. The great balancing act: regulation and fate of antiviral T-cell interactions. Immunol Rev 255:110-124. https://doi.org/10.1111/imr.12093.
28. Ransohoff RM, Engelhardt B. 2012. The anatomical and cellular basis of immune surveillance in the central nervous system. Nat Rev Immunol 12:623-635. https://doi.org/10.1038/nri3265.
29. Malkki H. 2016. CNS infections: Zika virus infection could trigger Guillain-Barre syndrome. Nat Rev Neurol 12:187. https://doi.org/10.1038/ nrneurol.2016.30.
30. Hou HQ, Miao J, Feng XD, Han M, Song XJ, Guo L. 2014. Changes in lymphocyte subsets in patients with Guillain-Barre syndrome treated with immunoglobulin. BMC Neurol 14:202. https://doi.org/10.1186/ s12883-014-0202-3.
31. Aliota MT, Caine EA, Walker EC, Larkin KE, Camacho E, Osorio JE. 2016. Characterization of lethal Zika virus infection in AG129 mice. PLoS Negl Trop Dis 10:e0004682. https://doi.org/10.1371/journal.pntd.0004682.
32. Rossi SL, Tesh RB, Azar SR, Muruato AE, Hanley KA, Auguste AJ, Langsjoen RM, Paessler S, Vasilakis N, Weaver SC. 2016. Characterization of a novel murine model to study Zika virus. Am J Trop Med Hyg 94: 1362-1369. https://doi.org/10.4269/ajtmh.16-0111.
33. Korn T, Kallies A. 2017. T cell responses in the central nervous system. Nat Rev Immunol 17:179-194. https://doi.org/10.1038/nri.2016.144.
34. Cupovic J, Onder L, Gil-Cruz C, Weiler E, Caviezel-Firner S, Perez-Shibayama C, Rulicke T, Bechmann I, Ludewig B. 2016. Central nervous system stromal cells control local CD8+ T cell responses during virusinduced neuroinflammation. Immunity 44:622-633. https://doi.org/10.1016/j.immuni.2015.12.022.
35. Wang Q, Yang H, Liu X, Dai L, Ma T, Qi J, Wong G, Peng R, Liu S, Li J, Li S, Song J, Liu J, He J, Yuan H, Xiong Y, Liao Y, Yang J, Tong Z, Griffin BD, Bi Y, Liang M, Xu X, Qin C, Cheng G, Zhang X, Wang P, Qiu X, Kobinger G, Shi Y, Yan J, Gao GF. 2016. Molecular determinants of human neutralizing antibodies isolated from a patient infected with Zika virus. Sci Transl Med 8:369ra179. https://doi.org/10.1126/scitranslmed.aai8336.
36. Liu J, Wu B, Zhang S, Tan S, Sun Y, Chen Z, Qin Y, Sun M, Shi G, Wu Y, Liu N, Ning K, Ma Y, Gao B, Yan J, Zhu F, Wang H, Gao GF. 2013. Conserved epitopes dominate cross-CD8+ T-cell responses against influenza A H1N1 virus among Asian populations. Eur J Immunol 43: 2055-2069. https://doi.org/10.1002/eji.201343417.