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Annual Review of Virology

Volume 6, 2019

Update on the Animal Models and Underlying Mechanisms for ZIKV-Induced Microcephaly

Abstract

The circulation of Zika virus (ZIKV) in nearly 80 countries and territories poses a significant global threat to public health. ZIKV is causally linked to severe developmental defects in the brain, recognized as congenital Zika syndrome (CZS), which includes microcephaly and other serious congenital neurological complications. Since the World Health Organization declared the ZIKV outbreak a public health emergency of international concern, remarkable progress has been made in the generation of different ZIKV infection animal models to gain insight into cellular targets and pathogenesis and to explore the associated underlying mechanisms. Here we focus on summarizing our current understanding of the effects of ZIKV on mammalian brain development in different developmental stages and discuss the potential underlying mechanisms of ZIKV-induced CZS, as well as future perspectives.

Keyword(s): mechanism, microcephaly, mouse model, neuropathogenesis, Zika virus
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/content/journals/10.1146/annurev-virology-092818-015740
2019-09-29
2024-04-19
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Literature Cited

  1. 1. 
    Dick GW, Kitchen SF, Haddow AJ 1952. Zika virus. I. Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46:509–20
     [Google Scholar]
  2. 2. 
    Melo AS, Aguiar RS, Amorim MM, Arruda MB, Melo FO et al. 2016. Congenital Zika virus infection: beyond neonatal microcephaly. JAMA Neurol 73:1407–16
     [Google Scholar]
  3. 3. 
    Oliveira Melo AS, Malinger G, Ximenes R, Szejnfeld PO, Alves Sampaio S, Bispo de Filippis AM 2016. Zika virus intrauterine infection causes fetal brain abnormality and microcephaly: tip of the iceberg?. Ultrasound Obstet. Gynecol. 47:6–7
     [Google Scholar]
  4. 4. 
    Pierson TC, Diamond MS. 2013. Flaviviruses. Fields Virology DM Knipe, PM Howley 746–94 Philadelphia: Wolters Kluwer
     [Google Scholar]
  5. 5. 
    Garcia-Blanco MA, Vasudevan SG, Bradrick SS, Nicchitta C 2016. Flavivirus RNA transactions from viral entry to genome replication. Antiviral Res. 134:244–49
     [Google Scholar]
  6. 6. 
    Foy BD, Kobylinski KC, Chilson Foy JL, Blitvich BJ, Travassos da Rosa A et al. 2011. Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg. Infect. Dis. 17:880–82
     [Google Scholar]
  7. 7. 
    Musso D, Roche C, Robin E, Nhan T, Teissier A, Cao-Lormeau VM 2015. Potential sexual transmission of Zika virus. Emerg. Infect. Dis. 21:359–61
     [Google Scholar]
  8. 8. 
    Brasil P, Pereira JP, Moreira ME, Nogueira RMR, Damasceno L et al. 2016. Zika virus infection in pregnant women in Rio de Janeiro. N. Engl. J. Med. 375:2321–34
     [Google Scholar]
  9. 9. 
    Chan JF, Choi GK, Yip CC, Cheng VC, Yuen KY 2016. Zika fever and congenital Zika syndrome: an unexpected emerging arboviral disease. J. Infect. 72:507–24
     [Google Scholar]
  10. 10. 
    Slavov SN, Otaguiri KK, Kashima S, Covas DT 2016. Overview of Zika virus (ZIKV) infection in regards to the Brazilian epidemic. Braz. J. Med. Biol. Res. 49:e5420
     [Google Scholar]
  11. 11. 
    Mlakar J, Korva M, Tul N, Popovic M, Poljsak-Prijatelj M et al. 2016. Zika virus associated with microcephaly. N. Engl. J. Med. 374:951–58
     [Google Scholar]
  12. 12. 
    Liu ZY, Shi WF, Qin CF 2019. The evolution of Zika virus from Asia to the Americas. Nat. Rev. Microbiol. 17:131–39
     [Google Scholar]
  13. 13. 
    Mecharles S, Herrmann C, Poullain P, Tran TH, Deschamps N et al. 2016. Acute myelitis due to Zika virus infection. Lancet 387:1481
     [Google Scholar]
  14. 14. 
    Carteaux G, Maquart M, Bedet A, Contou D, Brugieres P et al. 2016. Zika virus associated with meningoencephalitis. N. Engl. J. Med. 374:1595–97
     [Google Scholar]
  15. 15. 
    Styczynski AR, Malta JMAS, Krow-Lucal ER, Percio J, Nobrega ME et al. 2017. Increased rates of Guillain-Barré syndrome associated with Zika virus outbreak in the Salvador metropolitan area, Brazil. PLOS Negl. Trop. Dis. 11:e0005869
     [Google Scholar]
  16. 16. 
    Munoz LS, Barreras P, Pardo CA 2016. Zika virus-associated neurological disease in the adult: Guillain-Barré syndrome, encephalitis, and myelitis. Semin. Reprod. Med. 34:273–79
     [Google Scholar]
  17. 17. 
    Heymann DL, Hodgson A, Sall AA, Freedman DO, Staples JE et al. 2016. Zika virus and microcephaly: Why is this situation a PHEIC?. Lancet 387:719–21
     [Google Scholar]
  18. 18. 
    Marrs C, Olson G, Saade G, Hankins G, Wen T et al. 2016. Zika virus and pregnancy: a review of the literature and clinical considerations. Am. J. Perinatol. 33:625–39
     [Google Scholar]
  19. 19. 
    Mahmood S, Ahmad W, Hassan MJ 2011. Autosomal recessive primary microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum. Orphanet. J. Rare Dis. 6:39
     [Google Scholar]
  20. 20. 
    McDonell LM, Warman Chardon J, Schwartzentruber J, Foster D, Beaulieu CL et al. 2014. The utility of exome sequencing for genetic diagnosis in a familial microcephaly epilepsy syndrome. BMC Neurol 14:22
     [Google Scholar]
  21. 21. 
    Chen J, Ingham N, Clare S, Raisen C, Vancollie VE et al. 2013. Mcph1-deficient mice reveal a role for MCPH1 in otitis media. PLOS ONE 8:e58156
     [Google Scholar]
  22. 22. 
    Tanaka AJ, Cho MT, Millan F, Juusola J, Retterer K et al. 2015. Mutations in SPATA5 are associated with microcephaly, intellectual disability, seizures, and hearing loss. Am. J. Hum. Genet. 97:457–64
     [Google Scholar]
  23. 23. 
    Pomar L, Malinger G, Benoist G, Carles G, Ville Y et al. 2017. Association between Zika virus and fetopathy: a prospective cohort study in French Guiana. Ultrasound Obstet. Gynecol. 49:729
     [Google Scholar]
  24. 24. 
    Azar SR, Rossi SL, Haller SH, Yun R, Huang JH et al. 2018. ZIKV demonstrates minimal pathologic effects and mosquito infectivity in viremic cynomolgus macaques. Viruses 10:661
     [Google Scholar]
  25. 25. 
    Wen Z, Song H, Ming GL 2017. How does Zika virus cause microcephaly?. Genes Dev 31:849
     [Google Scholar]
  26. 26. 
    Caine EA, Jagger BW, Diamond MS 2018. Animal models of Zika virus infection during pregnancy. Viruses 10:598
     [Google Scholar]
  27. 27. 
    Pena LJ, Guarines KM, Duarte Silva AJ, Sales Leal LR, Mendes Felix D et al. 2018. In vitro and in vivo models for studying Zika virus biology. J. Gen. Virol. 99:1529–50
     [Google Scholar]
  28. 28. 
    Morrison TE, Diamond MS. 2017. Animal models of Zika virus infection, pathogenesis, and immunity. J. Virol. 91:e00009–17
     [Google Scholar]
  29. 29. 
    Siddharthan V, Van Wettere AJ, Li R, Miao J, Wang Z et al. 2017. Zika virus infection of adult and fetal STAT2 knock-out hamsters. Virology 507:89–95
     [Google Scholar]
  30. 30. 
    Kumar M, Krause KK, Azouz F, Nakano E, Nerurkar VR 2017. A guinea pig model of Zika virus infection. Virol. J. 14:75
     [Google Scholar]
  31. 31. 
    Goodfellow FT, Tesla B, Simchick G, Zhao Q, Hodge T et al. 2016. Zika virus induced mortality and microcephaly in chicken embryos. Stem Cells Dev 25:1691–97
     [Google Scholar]
  32. 32. 
    Malmlov A, Bantle C, Aboellail T, Wagner K, Campbell CL et al. 2019. Experimental Zika virus infection of Jamaican fruit bats (Artibeus jamaicensis) and possible entry of virus into brain via activated microglial cells. PLOS Negl. Trop. Dis. 13:2e0007071
     [Google Scholar]
  33. 33. 
    Zhang NN, Zhang L, Deng YQ, Feng Y, Ma F et al. 2019. Zika virus infection in Tupaia belangeri causes dermatological manifestations and confers protection against secondary infection. J. Virol. 93:8e01982–18
     [Google Scholar]
  34. 34. 
    Calvet G, Aguiar RS, Melo AS, Sampaio SA, de Filippis I et al. 2016. Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect. Dis. 16:653–60
     [Google Scholar]
  35. 35. 
    Driggers RW, Ho CY, Korhonen EM, Kuivanen S, Jaaskelainen AJ et al. 2016. Zika virus infection with prolonged maternal viremia and fetal brain abnormalities. N. Engl. J. Med. 374:222142–51
     [Google Scholar]
  36. 36. 
    Hazin AN, Poretti A, Di Cavalcanti Souza Cruz D, Tenorio M, van der Linden A et al. 2016. Computed tomographic findings in microcephaly associated with Zika virus. N. Engl. J. Med. 374:2193–95
     [Google Scholar]
  37. 37. 
    de Fatima Vasco Aragao M, van der Linden V, Brainer-Lima AM, Coeli RR, Rocha MA et al. 2016. Clinical features and neuroimaging (CT and MRI) findings in presumed Zika virus related congenital infection and microcephaly: retrospective case series study. BMJ 353:i1901
     [Google Scholar]
  38. 38. 
    Chimelli L, Avvad-Portari E. 2018. Congenital Zika virus infection: a neuropathological review. Childs Nerv. Syst. 34:95–99
     [Google Scholar]
  39. 39. 
    Tang H, Hammack C, Ogden SC, Wen Z, Qian X et al. 2016. Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18:587–90
     [Google Scholar]
  40. 40. 
    Garcez PP, Loiola EC, Madeiro da Costa R, Higa LM, Trindade P et al. 2016. Zika virus impairs growth in human neurospheres and brain organoids. Science 352:816–18
     [Google Scholar]
  41. 41. 
    Qian XY, Nguyen HN, Jacob F, Song HJ, Ming GL 2017. Using brain organoids to understand Zika virus-induced microcephaly. Development 144:952–57
     [Google Scholar]
  42. 42. 
    Qian XY, Nguyen HN, Song MM, Hadiono C, Ogden SC et al. 2016. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165:1238–54
     [Google Scholar]
  43. 43. 
    Lum FM, Low DK, Fan Y, Tan JJ, Lee B et al. 2017. Zika virus infects human fetal brain microglia and induces inflammation. Clin. Infect. Dis. 64:914–20
     [Google Scholar]
  44. 44. 
    Cumberworth SL, Barrie JA, Cunningham ME, de Figueiredo DPG, Schultz V et al. 2017. Zika virus tropism and interactions in myelinating neural cell cultures: CNS cells and myelin are preferentially affected. Acta Neuropathol. Commun. 5:50
     [Google Scholar]
  45. 45. 
    Dong S, Liang Q. 2018. Recent advances in animal models of Zika virus infection. Virol. Sin. 33:125–30
     [Google Scholar]
  46. 46. 
    Winkler CW, Peterson KE. 2017. Using immunocompromised mice to identify mechanisms of Zika virus transmission and pathogenesis. Immunology 153:443–54
     [Google Scholar]
  47. 47. 
    Lazear HM, Govero J, Smith AM, Platt DJ, Fernandez E et al. 2016. A mouse model of Zika virus pathogenesis. Cell Host Microbe 19:720–30
     [Google Scholar]
  48. 48. 
    Rossi SL, Tesh RB, Azar SR, Muruato AE, Hanley KA et al. 2016. Characterization of a novel murine model to study Zika virus. Am. J. Trop. Med. Hyg. 94:1362–69
     [Google Scholar]
  49. 49. 
    Bell TM, Field EJ, Narang HK 1971. Zika virus infection of the central nervous system of mice. Arch. Gesamte Virusforsch. 35:183–93
     [Google Scholar]
  50. 50. 
    Li C, Xu D, Ye Q, Hong S, Jiang Y et al. 2016. Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19:120–26
     [Google Scholar]
  51. 51. 
    Wu KY, Zuo GL, Li XF, Ye Q, Deng YQ et al. 2016. Vertical transmission of Zika virus targeting the radial glial cells affects cortex development of offspring mice. Cell Res 26:645–54
     [Google Scholar]
  52. 52. 
    Oh Y, Zhang F, Wang Y, Lee EM, Choi IY et al. 2017. Zika virus directly infects peripheral neurons and induces cell death. Nat. Neurosci. 20:1209–12
     [Google Scholar]
  53. 53. 
    Li C, Wang Q, Jiang Y, Ye Q, Xu D et al. 2018. Disruption of glial cell development by Zika virus contributes to severe microcephalic newborn mice. Cell Discov 4:43
     [Google Scholar]
  54. 54. 
    Shao Q, Herrlinger S, Yang SL, Lai F, Moore JM et al. 2016. Zika virus infection disrupts neurovascular development and results in postnatal microcephaly with brain damage. Development 143:4127–36
     [Google Scholar]
  55. 55. 
    Schaub B, Monthieux A, Najioullah F, Adenet C, Muller F, Cesaire R 2017. Persistent maternal Zika viremia: a marker of fetal infection. Ultrasound Obstet. Gynecol. 49:658–60
     [Google Scholar]
  56. 56. 
    Zhang F, Wang HJ, Wang Q, Liu ZY, Yuan L et al. 2017. American strain of Zika virus causes more severe microcephaly than an old Asian strain in neonatal mice. EBioMedicine 25:95–105
     [Google Scholar]
  57. 57. 
    Wu YH, Tseng CK, Lin CK, Wei CK, Lee JC, Young KC 2018. ICR suckling mouse model of Zika virus infection for disease modeling and drug validation. PLOS Negl. Trop. Dis. 12:e0006848
     [Google Scholar]
  58. 58. 
    Huang WC, Abraham R, Shim BS, Choe H, Page DT 2016. Zika virus infection during the period of maximal brain growth causes microcephaly and corticospinal neuron apoptosis in wild type mice. Sci. Rep. 6:34793
     [Google Scholar]
  59. 59. 
    Nem de Oliveira Souza I, Frost PS, Franca JV, Nascimento-Viana JB, Neris RLS et al. 2018. Acute and chronic neurological consequences of early-life Zika virus infection in mice. Sci. Transl. Med. 10:eaar2749
     [Google Scholar]
  60. 60. 
    Pessoa A, van der Linden V, Yeargin-Allsopp M, Carvalho M, Ribeiro EM et al. 2018. Motor abnormalities and epilepsy in infants and children with evidence of congenital Zika virus infection. Pediatrics 141:S167–79
     [Google Scholar]
  61. 61. 
    Brown AM, McFarlin DE. 1981. Relapsing experimental allergic encephalomyelitis in the SJL/J mouse. Lab. Invest. 45:278–84
     [Google Scholar]
  62. 62. 
    Hutchings PR, Varey AM, Cooke A 1986. Immunological defects in SJL mice. Immunology 59:445–50
     [Google Scholar]
  63. 63. 
    Cugola FR, Fernandes IR, Russo FB, Freitas BC, Dias JL et al. 2016. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534:267–71
     [Google Scholar]
  64. 64. 
    Li C, Deng YQ, Wang S, Ma F, Aliyari R et al. 2017. 25-Hydroxycholesterol protects host against Zika virus infection and its associated microcephaly in a mouse model. Immunity 46:446–56
     [Google Scholar]
  65. 65. 
    Wang S, Hong S, Deng YQ, Ye Q, Zhao LZ et al. 2017. Transfer of convalescent serum to pregnant mice prevents Zika virus infection and microcephaly in offspring. Cell Res 27:158–60
     [Google Scholar]
  66. 66. 
    Li C, Gao F, Yu L, Wang R, Jiang Y et al. 2018. A single injection of human neutralizing antibody protects against Zika virus infection and microcephaly in developing mouse embryos. Cell Rep 23:1424–34
     [Google Scholar]
  67. 67. 
    Manzini MC, Walsh CA. 2011. What disorders of cortical development tell us about the cortex: One plus one does not always make two. Curr. Opin. Genet. Dev. 21:333–39
     [Google Scholar]
  68. 68. 
    Thornton GK, Woods CG. 2009. Primary microcephaly: Do all roads lead to Rome?. Trends Genet 25:501–10
     [Google Scholar]
  69. 69. 
    Kriegstein A, Alvarez-Buylla A. 2009. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32:149–84
     [Google Scholar]
  70. 70. 
    de Noronha L, Zanluca C, Azevedo MLV, Luz KG, dos Santos CND 2016. Zika virus damages the human placental barrier and presents marked fetal neurotropism. Mem. Inst. Oswaldo Cruz 111:287–93
     [Google Scholar]
  71. 71. 
    Retallack H, Di Lullo E, Arias C, Knopp KA, Laurie MT et al. 2016. Zika virus cell tropism in the developing human brain and inhibition by azithromycin. PNAS 113:14408–13
     [Google Scholar]
  72. 72. 
    Fernandes NC, Nogueira JS, Ressio RA, Cirqueira CS, Kimura LM et al. 2017. Experimental Zika virus infection induces spinal cord injury and encephalitis in newborn Swiss mice. Exp. Toxicol. Pathol. 69:63–71
     [Google Scholar]
  73. 73. 
    De Sousa JR, Azevedo RSS, Martins FAJ, Araujo MTF, Moutinho ERC et al. 2018. Correlation between apoptosis and in situ immune response in fatal cases of microcephaly caused by Zika virus. Am. J. Pathol. 188:2644–52
     [Google Scholar]
  74. 74. 
    Shi Y, Li S, Wu Q, Sun L, Zhang J et al. 2018. Vertical transmission of the Zika virus causes neurological disorders in mouse offspring. Sci. Rep. 8:3541
     [Google Scholar]
  75. 75. 
    Yuan L, Huang XY, Liu ZY, Zhang F, Zhu XL et al. 2017. A single mutation in the prM protein of Zika virus contributes to fetal microcephaly. Science 358:933–36
     [Google Scholar]
  76. 76. 
    Yoon KJ, Song G, Qian X, Pan J, Xu D et al. 2017. Zika-virus-encoded NS2A disrupts mammalian cortical neurogenesis by degrading adherens junction proteins. Cell Stem Cell 21:349–58.e6
     [Google Scholar]
  77. 77. 
    Li HD, Saucedo-Cuevas L, Regla-Nava JA, Chai GL, Sheets N et al. 2016. Zika virus infects neural progenitors in the adult mouse brain and alters proliferation. Cell Stem Cell 19:593–98
     [Google Scholar]
  78. 78. 
    Marthiens V, Rujano MA, Pennetier C, Tessier S, Paul-Gilloteaux P, Basto R 2013. Centrosome amplification causes microcephaly. Nat. Cell Biol. 15:731–40
     [Google Scholar]
  79. 79. 
    Souza BS, Sampaio GL, Pereira CS, Campos GS, Sardi SI et al. 2016. Zika virus infection induces mitosis abnormalities and apoptotic cell death of human neural progenitor cells. Sci. Rep. 6:39775
     [Google Scholar]
  80. 80. 
    Gabriel E, Ramani A, Karow U, Gottardo M, Natarajan K et al. 2017. Recent Zika virus isolates induce premature differentiation of neural progenitors in human brain organoids. Cell Stem Cell 20:397–406.e5
     [Google Scholar]
  81. 81. 
    Onorati M, Li Z, Liu FC, Sousa AMM, Nakagawa N et al. 2016. Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Rep 16:2576–92
     [Google Scholar]
  82. 82. 
    Wolf B, Diop F, Ferraris P, Wichit S, Busso C et al. 2017. Zika virus causes supernumerary foci with centriolar proteins and impaired spindle positioning. Open Biol 7:160231
     [Google Scholar]
  83. 83. 
    Chavali PL, Stojic L, Meredith LW, Joseph N, Nahorski MS et al. 2017. Neurodevelopmental protein Musashi-1 interacts with the Zika genome and promotes viral replication. Science 357:83–88
     [Google Scholar]
  84. 84. 
    Goodfellow FT, Willard KA, Wu X, Scoville S, Stice SL, Brindley MA 2018. Strain-dependent consequences of Zika virus infection and differential impact on neural development. Viruses 10:550
     [Google Scholar]
  85. 85. 
    Liang Q, Luo Z, Zeng J, Chen W, Foo SS et al. 2016. Zika virus NS4A and NS4B proteins deregulate Akt-mTOR signaling in human fetal neural stem cells to inhibit neurogenesis and induce autophagy. Cell Stem Cell 19:663–71
     [Google Scholar]
  86. 86. 
    Martinot AJ, Abbink P, Afacan O, Prohl AK, Bronson R et al. 2018. Fetal neuropathology in Zika virus-infected pregnant female rhesus monkeys. Cell 173:1111–22.e10
     [Google Scholar]
  87. 87. 
    Ghouzzi VE, Bianchi FT, Molineris I, Mounce BC, Berto GE et al. 2016. ZIKA virus elicits P53 activation and genotoxic stress in human neural progenitors similar to mutations involved in severe forms of genetic microcephaly and p53. Cell Death Dis 7:e2440
     [Google Scholar]
  88. 88. 
    Zhang F, Hammack C, Ogden SC, Cheng Y, Lee EM et al. 2016. Molecular signatures associated with ZIKV exposure in human cortical neural progenitors. Nucleic Acids Res 44:8610–20
     [Google Scholar]
  89. 89. 
    Xu M, Lee EM, Wen Z, Cheng Y, Huang WK et al. 2016. Identification of small-molecule inhibitors of Zika virus infection and induced neural cell death via a drug repurposing screen. Nat. Med. 22:1101–7
     [Google Scholar]
  90. 90. 
    Tan Z, Zhang W, Sun J, Fu Z, Ke X et al. 2018. ZIKV infection activates the IRE1-XBP1 and ATF6 pathways of unfolded protein response in neural cells. J. Neuroinflamm. 15:275
     [Google Scholar]
  91. 91. 
    Chang YF, Jiang YS, Li C, Wang Q, Zhang F et al. 2019. Dissecting of the gene networks affected by Zika virus infection in a mouse microcephaly model. Genom. Proteom. Bioinform In press
    [Google Scholar]
  92. 92. 
    Lin S, Yang S, He J, Guest JD, Ma Z et al. 2019. Zika virus NS5 protein antagonizes type I interferon production via blocking TBK1 activation. Virology 527:180–87
     [Google Scholar]
  93. 93. 
    Grant A, Ponia SS, Tripathi S, Balasubramaniam V, Miorin L et al. 2016. Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe 19:882–90
     [Google Scholar]
  94. 94. 
    Dang J, Tiwari SK, Lichinchi G, Qin Y, Patil VS et al. 2016. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19:258–65
     [Google Scholar]
  95. 95. 
    Tsou WI, Nguyen KQ, Calarese DA, Garforth SJ, Antes AL et al. 2014. Receptor tyrosine kinases, TYRO3, AXL, and MER, demonstrate distinct patterns and complex regulation of ligand-induced activation. J. Biol. Chem. 289:25750–63
     [Google Scholar]
  96. 96. 
    Hamel R, Dejarnac O, Wichit S, Ekchariyawat P, Neyret A et al. 2015. Biology of Zika virus infection in human skin cells. J. Virol. 89:8880–96
     [Google Scholar]
  97. 97. 
    Nowakowski TJ, Pollen AA, Di Lullo E, Sandoval-Espinosa C, Bershteyn M, Kriegstein AR 2016. Expression analysis highlights AXL as a candidate Zika virus entry receptor in neural stem cells. Cell Stem Cell 18:591–96
     [Google Scholar]
  98. 98. 
    Wells MF, Salick MR, Wiskow O, Ho DJ, Worringer KA et al. 2016. Genetic ablation of AXL does not protect human neural progenitor cells and cerebral organoids from Zika virus infection. Cell Stem Cell 19:703–08
     [Google Scholar]
  99. 99. 
    Miner JJ, Sene A, Richner JM, Smith AM, Santeford A et al. 2016. Zika virus infection in mice causes panuveitis with shedding of virus in tears. Cell Rep 16:3208–18
     [Google Scholar]
  100. 100. 
    Wang ZY, Wang Z, Zhen ZD, Feng KH, Guo J et al. 2017. Axl is not an indispensable factor for Zika virus infection in mice. J. Gen. Virol. 98:2061–68
     [Google Scholar]
  101. 101. 
    Meertens L, Labeau A, Dejarnac O, Cipriani S, Sinigaglia L et al. 2017. Axl mediates ZIKA virus entry in human glial cells and modulates innate immune responses. Cell Rep 18:324–33
     [Google Scholar]
  102. 102. 
    Zhu Z, Chan JF, Tee KM, Choi GK, Lau SK et al. 2016. Comparative genomic analysis of pre-epidemic and epidemic Zika virus strains for virological factors potentially associated with the rapidly expanding epidemic. Emerg. Microbes Infect. 5:e22
     [Google Scholar]
  103. 103. 
    Lin MY, Wang YL, Wu WL, Wolseley V, Tsai MT et al. 2017. Zika virus infects intermediate progenitor cells and post-mitotic committed neurons in human fetal brain tissues. Sci. Rep. 7:14883
     [Google Scholar]
  104. 104. 
    Herculano-Houzel S. 2014. The glia/neuron ratio: how it varies uniformly across brain structures and species and what that means for brain physiology and evolution. Glia 62:1377–91
     [Google Scholar]
  105. 105. 
    Rowitch DH, Kriegstein AR. 2010. Developmental genetics of vertebrate glial-cell specification. Nature 468:214–22
     [Google Scholar]
  106. 106. 
    Zhang Y, Sloan SA, Clarke LE, Caneda C, Plaza CA et al. 2016. Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron 89:37–53
     [Google Scholar]
  107. 107. 
    Miner JJ, Cao B, Govero J, Smith AM, Fernandez E et al. 2016. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165:1081–91
     [Google Scholar]
  108. 108. 
    Deleted in proof
  109. 109. 
    Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–20
     [Google Scholar]
  110. 110. 
    Xu D, Zhang F, Wang Y, Sun Y, Xu Z 2014. Microcephaly-associated protein WDR62 regulates neurogenesis through JNK1 in the developing neocortex. Cell Rep 6:104–16
     [Google Scholar]
  111. 111. 
    Jayaraman D, Kodani A, Gonzalez DM, Mancias JD, Mochida GH et al. 2016. Microcephaly proteins Wdr62 and Aspm define a mother centriole complex regulating centriole biogenesis, apical complex, and cell fate. Neuron 92:813–28
     [Google Scholar]
  112. 112. 
    Rosenfeld AB, Doobin DJ, Warren AL, Racaniello VR, Vallee RB 2017. Replication of early and recent Zika virus isolates throughout mouse brain development. PNAS 114:12273–78
     [Google Scholar]
  113. 113. 
    Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B 2008. Neocortical glial cell numbers in human brains. Neurobiol. Aging 29:1754–62
     [Google Scholar]
  114. 114. 
    Reemst K, Noctor SC, Lucassen PJ, Hol EM 2016. The indispensable roles of microglia and astrocytes during brain development. Front. Hum. Neurosci. 10:566
     [Google Scholar]
  115. 115. 
    Molofsky AV, Krencik R, Ullian EM, Tsai HH, Deneen B et al. 2012. Astrocytes and disease: a neurodevelopmental perspective. Genes Dev 26:891–907
     [Google Scholar]
  116. 116. 
    Zuchero JB, Barres BA. 2015. Glia in mammalian development and disease. Development 142:3805–9
     [Google Scholar]
  117. 117. 
    Lindqvist R, Mundt F, Gilthorpe JD, Wolfel S, Gekara NO et al. 2016. Fast type I interferon response protects astrocytes from flavivirus infection and virus-induced cytopathic effects. J. Neuroinflamm. 13:277
     [Google Scholar]
  118. 118. 
    Hamel R, Ferraris P, Wichit S, Diop F, Talignani L et al. 2017. African and Asian Zika virus strains differentially induce early antiviral responses in primary human astrocytes. Infect. Genet. Evol. 49:134–37
     [Google Scholar]
  119. 119. 
    Mesci P, Macia A, LaRock CN, Tejwani L, Fernandes IR et al. 2018. Modeling neuro-immune interactions during Zika virus infection. Hum. Mol. Genet. 27:41–52
     [Google Scholar]
  120. 120. 
    Kozak RA, Majer A, Biondi MJ, Medina SJ, Goneau LW et al. 2017. MicroRNA and mRNA dysregulation in astrocytes infected with Zika virus. Viruses 9:297
     [Google Scholar]
  121. 121. 
    Chen J, Yang YF, Yang Y, Zou P, Chen J et al. 2018. AXL promotes Zika virus infection in astrocytes by antagonizing type I interferon signalling. Nat. Microbiol. 3:302–9
     [Google Scholar]
  122. 122. 
    Khaiboullina SF, Uppal T, Sarkar R, Gorzalski A, St Jeor S, Verma SC 2017. ZIKV infection regulates inflammasomes pathway for replication in monocytes. Sci. Rep. 7:16050
     [Google Scholar]
  123. 123. 
    Tricarico PM, Caracciolo I, Crovella S, D'Agaro P 2017. Zika virus induces inflammasome activation in the glial cell line U87-MG. Biochem. Biophys. Res. Commun. 492:597–602
     [Google Scholar]
  124. 124. 
    Hu B, Huo Y, Yang L, Chen G, Luo M et al. 2017. ZIKV infection effects changes in gene splicing, isoform composition and lncRNA expression in human neural progenitor cells. Virol. J. 14:217
     [Google Scholar]
  125. 125. 
    Zhang H, Chang Y, Zhang L, Kim SN, Otaegi G et al. 2019. Upregulation of microRNA miR-9 is associated with microcephaly and Zika virus infection in mice. Mol. Neurobiol. 56:4072–85
     [Google Scholar]
  126. 126. 
    Bhagat R, Prajapati B, Narwal S, Agnihotri N, Adlakha YK et al. 2018. Zika virus E protein alters the properties of human fetal neural stem cells by modulating microRNA circuitry. Cell Death Differ 25:1837–54
     [Google Scholar]
  127. 127. 
    Nguyen SM, Antony KM, Dudley DM, Kohn S, Simmons HA et al. 2017. Highly efficient maternal-fetal Zika virus transmission in pregnant rhesus macaques. PLOS Pathog 13:e1006378
     [Google Scholar]
  128. 128. 
    Dudley DM, Aliota MT, Mohr EL, Weiler AM, Lehrer-Brey G et al. 2016. A rhesus macaque model of Asian-lineage Zika virus infection. Nat. Commun. 7:12204
     [Google Scholar]
  129. 129. 
    Bleeker FE, Molenaar RJ, Leenstra S 2012. Recent advances in the molecular understanding of glioblastoma. J. Neurooncol. 108:11–27
     [Google Scholar]
  130. 130. 
    Cheshier SH, Kalani MY, Lim M, Ailles L, Huhn SL, Weissman IL 2009. A neurosurgeon's guide to stem cells, cancer stem cells, and brain tumor stem cells. Neurosurgery 65:237–50
     [Google Scholar]
  131. 131. 
    Chen Q, Wu J, Ye Q, Ma F, Zhu Q et al. 2018. Treatment of human glioblastoma with a live attenuated Zika virus vaccine candidate. mBio 9:e01683–18
     [Google Scholar]
  132. 132. 
    Zhu Z, Gorman MJ, McKenzie LD, Chai JN, Hubert CG et al. 2017. Zika virus has oncolytic activity against glioblastoma stem cells. J. Exp. Med. 214:2843–57
     [Google Scholar]
  133. 133. 
    Lubin JA, Zhang RR, Kuo JS 2018. Zika virus has oncolytic activity against glioblastoma stem cells. Neurosurgery 82:E113–14
     [Google Scholar]
  134. 134. 
    Xavier-Neto J, Carvalho M, Pascoalino BD, Cardoso AC, Costa AM et al. 2017. Hydrocephalus and arthrogryposis in an immunocompetent mouse model of ZIKA teratogeny: a developmental study. PLOS Negl. Trop. Dis. 11:e0005363
     [Google Scholar]
  135. 135. 
    Richner JM, Jagger BW, Shan C, Fontes CR, Dowd KA et al. 2017. Vaccine mediated protection against Zika virus-induced congenital disease. Cell 170:273–83.e12
     [Google Scholar]
  136. 136. 
    Cui L, Zou P, Chen E, Yao H, Zheng H et al. 2017. Visual and motor deficits in grown-up mice with congenital Zika virus infection. EBioMedicine 20:193–201
     [Google Scholar]
  137. 137. 
    Gorman MJ, Caine EA, Zaitsev K, Begley MC, Weger-Lucarelli J et al. 2018. An immunocompetent mouse model of Zika virus infection. Cell Host Microbe 23:672–85.e6
     [Google Scholar]
  138. 138. 
    Manangeeswaran M, Kielczewski JL, Sen HN, Xu BYC, Ireland DDC et al. 2018. ZIKA virus infection causes persistent chorioretinal lesions. Emerg. Microbes Infect. 7:1–15
     [Google Scholar]
  139. 139. 
    Smith DR, Hollidge B, Daye S, Zeng X, Blancett C et al. 2017. Neuropathogenesis of Zika virus in a highly susceptible immunocompetent mouse model after antibody blockade of type I interferon. PLOS Negl. Trop. Dis. 11:e0005296
     [Google Scholar]
  140. 140. 
    Dowall SD, Graham VA, Rayner E, Atkinson B, Hall G et al. 2016. A susceptible mouse model for Zika virus infection. PLOS Negl. Trop. Dis. 10:e0004658
     [Google Scholar]
  141. 141. 
    Muthumani K, Griffin BD, Agarwal S, Kudchodkar SB, Reuschel EL et al. 2016. In vivo protection against ZIKV infection and pathogenesis through passive antibody transfer and active immunisation with a prMEnv DNA vaccine. NPJ Vaccines 1:16021
     [Google Scholar]
  142. 142. 
    Xie XP, Kum DPB, Xia HJ, Luo HL, Shan C et al. 2018. A single-dose live-attenuated Zika virus vaccine with controlled infection rounds that protects against vertical transmission. Cell Host Microbe 24:487–99.e5
     [Google Scholar]
  143. 143. 
    Sumathy K, Kulkarni B, Gondu RK, Ponnuru SK, Bonguram N et al. 2017. Protective efficacy of Zika vaccine in AG129 mouse model. Sci. Rep. 7:46375
     [Google Scholar]
  144. 144. 
    Espinosa D, Mendy J, Manayani D, Vang L, Wang C et al. 2018. Passive transfer of immune sera induced by a Zika virus-like particle vaccine protects AG129 mice against lethal Zika virus challenge. EBioMedicine 27:61–70
     [Google Scholar]
  145. 145. 
    Salvo MA, Kingstad-Bakke B, Salas-Quinchucua C, Camacho E, Osorio JE 2018. Zika virus like particles elicit protective antibodies in mice. PLOS Negl. Trop. Dis. 12:e0006210
     [Google Scholar]
  146. 146. 
    Simanjuntak Y, Liang JJ, Chen SY, Li JK, Lee YL et al. 2018. Ebselen alleviates testicular pathology in mice with Zika virus infection and prevents its sexual transmission. PLOS Pathog 14:e1006854
     [Google Scholar]
  147. 147. 
    Tang WW, Young MP, Mamidi A, Regla-Nava JA, Kim K, Shresta S 2016. A mouse model of Zika virus sexual transmission and vaginal viral replication. Cell Rep 17:3091–98
     [Google Scholar]
  148. 148. 
    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
     [Google Scholar]
  149. 149. 
    Kamiyama N, Soma R, Hidano S, Watanabe K, Umekita H et al. 2017. Ribavirin inhibits Zika virus (ZIKV) replication in vitro and suppresses viremia in ZIKV-infected STAT1-deficient mice. Antivir. Res. 146:1–11
     [Google Scholar]
  150. 150. 
    Bailey MJ, Duehr J, Dulin H, Broecker F, Brown JA et al. 2018. Human antibodies targeting Zika virus NS1 provide protection against disease in a mouse model. Nat. Commun. 9:4560
     [Google Scholar]
/content/journals/10.1146/annurev-virology-092818-015740
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Update on the Animal Models and Underlying Mechanisms for ZIKV-Induced Microcephaly
Annual Review of Virology 6, 459 (2019); https://doi.org/10.1146/annurev-virology-092818-015740
/content/journals/10.1146/annurev-virology-092818-015740
/content/journals/10.1146/annurev-virology-092818-015740
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