A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses

PLoS Pathogens

Volumn 13, Issue 3, 2017, Pages

  Tripathi, Shashank ^a   Balasubramaniam, Vinod R M T ^a   Brown, Julia A ^a   Mena, Ignacio ^a   Grant, Alesha ^a   Bardina, Susana V ^a   Maringer, Kevin ^a,b   Schwarz, Megan C ^a   Maestre, Ana M ^a   Sourisseau, Marion ^a   Albrecht, Randy A ^a   Krammer, Florian ^a   Evans, Matthew J ^a   Fernandez Sesma, Ana ^a   Lim, Jean K ^a   García Sastre, Adolfo ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR3; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 22; INTERLEUKIN 4; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; NONSTRUCTURAL PROTEIN 5; RANTES; STAT2 PROTEIN; TUMOR NECROSIS FACTOR; VIRUS RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL INFILTRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE EXPRESSION; GONAD; IMMUNE RESPONSE; INFLAMMATION; LETHALITY; MALE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPATIOTEMPORAL ANALYSIS; STRAIN DIFFERENCE; VIRUS GENOME; VIRUS PATHOGENESIS; VIRUS PLAQUE; VIRUS REPLICATION; VIRUS STRAIN; VISCERA; ZIKA VIRUS; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOGENICITY; VIROLOGY; ZIKA FEVER;

ANIMALS; DISEASE MODELS, ANIMAL; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85016448472     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006258     Document Type: Article

References (44)

1. Lazear HM, Diamond MS, Zika Virus: New Clinical Syndromes and Its Emergence in the Western Hemisphere. J Virol. 2016;90(10):4864–75. doi: 10.1128/JVI.00252-1626962217
2. Ramos da Silva S, Gao SJ, Zika virus: An update on epidemiology, pathology, molecular biology, and animal model. J Med Virol. 2016;88(8):1291–6. doi: 10.1002/jmv.2456327124623
3. Weaver SC, Costa F, Garcia-Blanco MA, Ko AI, Ribeiro GS, Saade G, et al. Zika virus: History, emergence, biology, and prospects for control. Antiviral Res. 2016;130:69–80. doi: 10.1016/j.antiviral.2016.03.01026996139
4. Dick GW, Kitchen SF, Haddow AJ, Zika virus. I. Isolations and serological specificity. Trans R Soc Trop Med Hyg. 1952;46(5):509–20. 12995440
5. Costello A, Dua T, Duran P, Gulmezoglu M, Oladapo OT, Perea W, et al. Defining the syndrome associated with congenital Zika virus infection. Bull World Health Organ. 2016;94(6):406–A. doi: 10.2471/BLT.16.17699027274588
6. Faye O, Freire CC, Iamarino A, Faye O, de Oliveira JV, Diallo M, et al. Molecular evolution of Zika virus during its emergence in the 20(th) century. PLoS Negl Trop Dis. 2014;8(1):e2636. doi: 10.1371/journal.pntd.000263624421913
7. Pettersson JH, Eldholm V, Seligman SJ, Lundkvist A, Falconar AK, Gaunt MW, et al. How Did Zika Virus Emerge in the Pacific Islands and Latin America?MBio. 2016;7(5).
8. Ramos da Silva S, Gao SJ, Zika virus update II: Recent development of animal models-Proofs of association with human pathogenesis. J Med Virol. 2016;88(10):1657–8. doi: 10.1002/jmv.2458227208545
9. Ming GL, Tang H, Song H, Advances in Zika Virus Research: Stem Cell Models, Challenges, and Opportunities. Cell Stem Cell. 2016;19(6):690–702. doi: 10.1016/j.stem.2016.11.01427912090
10. Bayer A, Lennemann NJ, Ouyang Y, Bramley JC, Morosky S, Marques ET, Jr.et al. Type III Interferons Produced by Human Placental Trophoblasts Confer Protection against Zika Virus Infection. Cell Host Microbe. 2016;19(5):705–12. doi: 10.1016/j.chom.2016.03.00827066743
11. Quicke KM, Bowen JR, Johnson EL, McDonald CE, Ma H, O'Neal JT, et al. Zika Virus Infects Human Placental Macrophages. Cell Host Microbe. 2016;20(1):83–90. doi: 10.1016/j.chom.2016.05.01527247001
12. Dick GW, Zika virus. II. Pathogenicity and physical properties. Trans R Soc Trop Med Hyg. 1952;46(5):521–34. 12995441
13. Bell TM, Field EJ, Narang HK, Zika virus infection of the central nervous system of mice. Arch Gesamte Virusforsch. 1971;35(2):183–93. 5002906
14. Dowall SD, Graham VA, Rayner E, Atkinson B, Hall G, Watson RJ, et al. A Susceptible Mouse Model for Zika Virus Infection. PLoS Negl Trop Dis. 2016;10(5):e0004658. doi: 10.1371/journal.pntd.000465827149521
15. Dudley DM, Aliota MT, Mohr EL, Weiler AM, Lehrer-Brey G, Weisgrau KL, et al. A rhesus macaque model of Asian-lineage Zika virus infection. Nat Commun. 2016;7:12204. doi: 10.1038/ncomms1220427352279
16. Goodfellow FT, Tesla B, Simchick G, Zhao Q, Hodge T, Brindley MA, et al. Zika Virus Induced Mortality and Microcephaly in Chicken Embryos. Stem Cells Dev. 2016;25(22):1691–7. doi: 10.1089/scd.2016.023127627457
17. Lazear HM, Govero J, Smith AM, Platt DJ, Fernandez E, Miner JJ, et al. A Mouse Model of Zika Virus Pathogenesis. Cell Host Microbe. 2016;19(5):720–30. doi: 10.1016/j.chom.2016.03.01027066744
18. Aliota MT, Caine EA, Walker EC, Larkin KE, Camacho E, Osorio JE, Characterization of Lethal Zika Virus Infection in AG129 Mice. PLoS Negl Trop Dis. 2016;10(4):e0004682. doi: 10.1371/journal.pntd.000468227093158
19. Rossi SL, Tesh RB, Azar SR, Muruato AE, Hanley KA, Auguste AJ, et al. Characterization of a Novel Murine Model to Study Zika Virus. Am J Trop Med Hyg. 2016;94(6):1362–9. doi: 10.4269/ajtmh.16-011127022155
20. Kim K, Shresta S, Neuroteratogenic Viruses and Lessons for Zika Virus Models. Trends Microbiol. 2016;24(8):622–36. doi: 10.1016/j.tim.2016.06.00227387029
21. Cugola FR, Fernandes IR, Russo FB, Freitas BC, Dias JL, Guimaraes KP, et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature. 2016;534(7606):267–71. doi: 10.1038/nature1829627279226
22. Govero J, Esakky P, Scheaffer SM, Fernandez E, Drury A, Platt DJ, et al. Zika virus infection damages the testes in mice. Nature. 2016.
23. Li C, Xu D, Ye Q, Hong S, Jiang Y, Liu X, et al. Zika Virus Disrupts Neural Progenitor Development and Leads to Microcephaly in Mice. Cell Stem Cell. 2016;19(1):120–6. doi: 10.1016/j.stem.2016.04.01727179424
24. Ma W, Li S, Ma S, Jia L, Zhang F, Zhang Y, et al. Zika Virus Causes Testis Damage and Leads to Male Infertility in Mice. Cell. 2016;167(6):1511–24 e10. doi: 10.1016/j.cell.2016.11.01627884405
25. Manangeeswaran M, Ireland DD, Verthelyi D, Zika (PRVABC59) Infection Is Associated with T cell Infiltration and Neurodegeneration in CNS of Immunocompetent Neonatal C57Bl/6 Mice. PLoS Pathog. 2016;12(11):e1006004. doi: 10.1371/journal.ppat.100600427855206
26. Miner JJ, Cao B, Govero J, Smith AM, Fernandez E, Cabrera OH, et al. Zika Virus Infection during Pregnancy in Mice Causes Placental Damage and Fetal Demise. Cell. 2016;165(5):1081–91. doi: 10.1016/j.cell.2016.05.00827180225
27. Wu KY, Zuo GL, Li XF, Ye Q, Deng YQ, Huang XY, et al. Vertical transmission of Zika virus targeting the radial glial cells affects cortex development of offspring mice. Cell Res. 2016;26(6):645–54. doi: 10.1038/cr.2016.5827174054
28. Yockey LJ, Varela L, Rakib T, Khoury-Hanold W, Fink SL, Stutz B, et al. Vaginal Exposure to Zika Virus during Pregnancy Leads to Fetal Brain Infection. Cell. 2016;166(5):1247–56 e4. doi: 10.1016/j.cell.2016.08.00427565347
29. Grant A, Ponia SS, Tripathi S, Balasubramaniam V, Miorin L, Sourisseau M, et al. Zika Virus Targets Human STAT2 to Inhibit Type I Interferon Signaling. Cell Host Microbe. 2016;19(6):882–90. doi: 10.1016/j.chom.2016.05.00927212660
30. Kumar A, Hou S, Airo AM, Limonta D, Mancinelli V, Branton W, et al. Zika virus inhibits type-I interferon production and downstream signaling. EMBO Rep. 2016;17(12):1766–75. doi: 10.15252/embr.20164262727797853
31. Schneider WM, Chevillotte MD, Rice CM, Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 2014;32:513–45. doi: 10.1146/annurev-immunol-032713-12023124555472
32. Haddow AD, Schuh AJ, Yasuda CY, Kasper MR, Heang V, Huy R, et al. Genetic characterization of Zika virus strains: geographic expansion of the Asian lineage. PLoS Negl Trop Dis. 2012;6(2):e1477. doi: 10.1371/journal.pntd.000147722389730
33. Ramos HJ, Lanteri MC, Blahnik G, Negash A, Suthar MS, Brassil MM, et al. IL-1beta signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS Pathog. 2012;8(11):e1003039. doi: 10.1371/journal.ppat.100303923209411
34. Verbist KC, Klonowski KD, Functions of IL-15 in anti-viral immunity: multiplicity and variety. Cytokine. 2012;59(3):467–78. doi: 10.1016/j.cyto.2012.05.02022704694
35. Li H, Saucedo-Cuevas L, Regla-Nava JA, Chai G, Sheets N, Tang W, et al. Zika Virus Infects Neural Progenitors in the Adult Mouse Brain and Alters Proliferation. Cell Stem Cell. 2016;19(5):593–8. doi: 10.1016/j.stem.2016.08.00527545505
36. Way JH, Bowen ET, Platt GS, Comparative studies of some African arboviruses in cell culture and in mice. J Gen Virol. 1976;30(1):123–30. doi: 10.1099/0022-1317-30-1-1231245842
37. Qian X, Nguyen HN, Song MM, Hadiono C, Ogden SC, Hammack C, et al. Brain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure. Cell. 2016;165(5):1238–54. doi: 10.1016/j.cell.2016.04.03227118425
38. Tang H, Hammack C, Ogden SC, Wen Z, Qian X, Li Y, et al. Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth. Cell Stem Cell. 2016;18(5):587–90. doi: 10.1016/j.stem.2016.02.01626952870
39. Zhang F, Hammack C, Ogden SC, Cheng Y, Lee EM, Wen Z, et al. Molecular signatures associated with ZIKV exposure in human cortical neural progenitors. Nucleic Acids Res. 2016;44(18):8610–20. doi: 10.1093/nar/gkw76527580721
40. Simonin Y, Loustalot F, Desmetz C, Foulongne V, Constant O, Fournier-Wirth C, et al. Zika Virus Strains Potentially Display Different Infectious Profiles in Human Neural Cells. EBioMedicine. 2016;12:161–9. doi: 10.1016/j.ebiom.2016.09.02027688094
41. Morrison J, Aguirre S, Fernandez-Sesma A, Innate immunity evasion by Dengue virus. Viruses. 2012;4(3):397–413. doi: 10.3390/v403039722590678
42. Tsetsarkin KA, Chen R, Sherman MB, Weaver SC, Chikungunya virus: evolution and genetic determinants of emergence. Curr Opin Virol. 2011;1(4):310–7. doi: 10.1016/j.coviro.2011.07.00421966353
43. Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, et al. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis. 2008;14(8):1232–9. doi: 10.3201/eid1408.08028718680646
44. Biancotto A, Wank A, Perl S, Cook W, Olnes MJ, Dagur PK, et al. Baseline levels and temporal stability of 27 multiplexed serum cytokine concentrations in healthy subjects. PLoS One. 2013;8(12):e76091. doi: 10.1371/journal.pone.007609124348989