Zika Virus Infects Intermediate Progenitor Cells and Post-mitotic Committed Neurons in Human Fetal Brain Tissues

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Lin, Ming Yi ^a   Wang, Yi Ling ^a   Wu, Wan Lin ^a   Wolseley, Victoria ^a   Tsai, Ming Ting ^a   Radic, Vladimir ^a   Thornton, Matthew E ^a   Grubbs, Brendan H ^a   Chow, Robert H ^a   Huang, I Chueh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; EMBRYOLOGY; FEMALE; FETUS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; MICROCEPHALY; MITOSIS; NERVE CELL; PATHOLOGY; PREGNANCY; STEM CELL; TISSUE CULTURE TECHNIQUE; VIROLOGY; ZIKA FEVER; ZIKA VIRUS;

BRAIN; FEMALE; FETUS; HUMANS; IMMUNITY, INNATE; MICROCEPHALY; MITOSIS; NEURONS; PREGNANCY; STEM CELLS; TISSUE CULTURE TECHNIQUES; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85042933241     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-13980-2     Document Type: Article

References (51)

1. Mlakar, J. et al. Zika Virus Associated with Microcephaly. N Engl J Med 374, 951–958 (2016)
2. Dick, G. W., Kitchen, S. F. & Haddow, A. J. Zika virus. I. Isolations and serological specificity. Trans R Soc Trop Med Hyg 46, 509–520 (1952)
3. Macnamara, F. N. Zika virus: a report on three cases of human infection during an epidemic of jaundice in Nigeria. Trans R Soc Trop Med Hyg 48, 139–145 (1954)
4. Lazear, H. M. & Diamond, M. S. Zika Virus: New Clinical Syndromes and Its Emergence in the Western Hemisphere. J Virol 90, 4864–4875 (2016)
5. Faye, O. et al. Molecular evolution of Zika virus during its emergence in the 20(th) century. PLoS Negl Trop Dis 8, e2636 (2014)
6. Faria, N. R. et al. Zika virus in the Americas: Early epidemiological and genetic findings. Science 352, 345–349 (2016)
7. Sirohi, D. et al. The 3.8 A resolution cryo-EM structure of Zika virus. Science 352, 467–470 (2016)
8. Lazear, H. M. et al. A Mouse Model of Zika Virus Pathogenesis. Cell Host Microbe 19, 720–730 (2016)
9. Sapparapu, G. et al. Neutralizing human antibodies prevent Zika virus replication and fetal disease in mice. Nature 540, 443–447 (2016)
10. Zhao, H. et al. Structural Basis of Zika Virus-Specific Antibody Protection. Cell 166, 1016–1027 (2016)
11. Calvet, G. et al. Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect Dis 16, 653–660 (2016)
12. Brasil, P. et al. Zika Virus Infection in Pregnant Women in Rio de Janeiro - Preliminary Report. N Engl J Med (2016)
13. Driggers, R. W. et al. Zika Virus Infection with Prolonged Maternal Viremia and Fetal Brain Abnormalities. N Engl J Med 374, 2142–2151 (2016)
14. Lodato, S., Shetty, A. S. & Arlotta, P. Cerebral cortex assembly: generating and reprogramming projection neuron diversity. Trends Neurosci 38, 117–125 (2015)
15. Bystron, I., Blakemore, C. & Rakic, P. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9, 110–122 (2008)
16. Kriegstein, A. & Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32, 149–184 (2009)
17. Ellis, P. et al. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 26, 148–165 (2004)
18. Pontious, A., Kowalczyk, T., Englund, C. & Hevner, R. F. Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci 30, 24–32 (2008)
19. Haubensak, W., Attardo, A., Denk, W. & Huttner, W. B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 101, 3196–3201 (2004)
20. Miyata, T. et al. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133–3145 (2004)
21. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7, 136–144 (2004)
22. Vasistha, N. A. et al. Cortical and Clonal Contribution of Tbr2 Expressing Progenitors in the Developing Mouse Brain. Cereb Cortex 25, 3290–3302 (2015)
23. Kowalczyk, T. et al. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex 19, 2439–2450 (2009)
24. Englund, C. et al. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25, 247–251 (2005)
25. Soltani, M. H. et al. Microtubule-associated protein 2, a marker of neuronal differentiation, induces mitotic defects, inhibits growth of melanoma cells, and predicts metastatic potential of cutaneous melanoma. Am J Pathol 166, 1841–1850 (2005)
26. Britanova, O. et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57, 378–392 (2008)
27. Roessmann, U. & Gambetti, P. Astrocytes in the developing human brain. An immunohistochemical study. Acta Neuropathol 70, 308–313 (1986)
28. Messam, C. A., Hou, J., Berman, J. W. & Major, E. O. Analysis of the temporal expression of nestin in human fetal brain derived neuronal and glial progenitor cells. Brain Res Dev Brain Res 134, 87–92 (2002)
29. Wilkinson, M., Hume, R., Strange, R. & Bell, J. E. Glial and neuronal differentiation in the human fetal brain 9-23 weeks of gestation. Neuropathol Appl Neurobiol 16, 193–204 (1990)
30. Jakovcevski, I., Filipovic, R., Mo, Z., Rakic, S. & Zecevic, N. Oligodendrocyte development and the onset of myelination in the human fetal brain. Front Neuroanat 3, 5 (2009)
31. Semple, B. D., Blomgren, K., Gimlin, K., Ferriero, D. M. & Noble-Haeusslein, L. J. Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol 106–107, 1–16 (2013)
32. Tang, H. et al. Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth. Cell Stem Cell 18, 587–590 (2016)
33. Liang, Q. et al. 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 (2016)
34. Cugola, F. R. et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534, 267–271 (2016)
35. Qian, X. et al. Brain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure. Cell 165, 1238–1254 (2016)
36. Garcez, P. P. et al. Zika virus impairs growth in human neurospheres and brain organoids. Science 352, 816–818 (2016)
37. Chin, M. H., Pellegrini, M., Plath, K. & Lowry, W. E. Molecular analyses of human induced pluripotent stem cells and embryonic stem cells. Cell Stem Cell 7, 263–269 (2010)
38. Onorati, M. et al. Zika Virus Disrupts Phospho-TBK1 Localization and Mitosis in Human Neuroepithelial Stem Cells and Radial Glia. Cell Rep 16, 2576–2592 (2016)
39. Paridaen, J. T. & Huttner, W. B. Neurogenesis during development of the vertebrate central nervous system. EMBO Rep 15, 351–364 (2014)
40. Lui, J. H., Hansen, D. V. & Kriegstein, A. R. Development and evolution of the human neocortex. Cell 146, 18–36 (2011)
41. Casper, K. B. & McCarthy, K. D. GFAP-positive progenitor cells produce neurons and oligodendrocytes throughout the CNS. Mol Cell Neurosci 31, 676–684 (2006)
42. Howard, B. M. et al. Radial glia cells in the developing human brain. Neuroscientist 14, 459–473 (2008)
43. Cunningham, C. L., Martinez-Cerdeno, V. & Noctor, S. C. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J Neurosci 33, 4216–4233 (2013)
44. Borsini, A., Zunszain, P. A., Thuret, S. & Pariante, C. M. The role of inflammatory cytokines as key modulators of neurogenesis. Trends Neurosci 38, 145–157 (2015)
45. Rowitch, D. H. & Kriegstein, A. R. Developmental genetics of vertebrate glial-cell specification. Nature 468, 214–222 (2010)
46. Baala, L. et al. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat Genet 39, 454–456 (2007)
47. Avirutnan, P. et al. Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog 3, e183 (2007)
48. Ray, B., Chopra, N., Long, J. M. & Lahiri, D. K. Human primary mixed brain cultures: preparation, differentiation, characterization and application to neuroscience research. Mol Brain 7, 63 (2014)
49. Ho, P. P., Young, A. L. & Truehaft, M. Plaque formation with influenza viruses in dog kidney cells. J Gen Virol 33, 143–145 (1976)
50. Malewicz, B. & Jenkin, H. M. Development of dengue virus plaques under serum-free overlay medium. J Clin Microbiol 9, 609–614 (1979)
51. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25, 402–408 (2001)