Zika Virus Depletes Neural Progenitors in Human Cerebral Organoids through Activation of the Innate Immune Receptor TLR3

Cell Stem Cell

Volumn 19, Issue 2, 2016, Pages 258-265

  Dang, Jason ^a,b   Tiwari, Shashi Kant ^a   Lichinchi, Gianluigi ^a,c   Qin, Yue ^a   Patil, Veena S ^a   Eroshkin, Alexey M ^c   Rana, Tariq M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

microcephaly; organoids; Toll like receptors; Zika virus

Indexed keywords

TOLL LIKE RECEPTOR 3; RNA; TLR3 PROTEIN, HUMAN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; AXON; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN REGION; CELL FATE; CEREBRAL ORGANOID; CONTROLLED STUDY; FETUS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; INNATE IMMUNITY; MICROCEPHALY; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; TRANSCRIPTOMICS; ZIKA FEVER; ZIKA VIRUS; ANIMAL; BRAIN; CELL DIFFERENTIATION; CYTOPLASM; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; PHYSIOLOGY; VIROLOGY;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CEREBRUM; FETUS; HUMANS; IMMUNITY, INNATE; MICE; NEURAL STEM CELLS; NEUROGENESIS; ORGANOIDS; RNA; TOLL-LIKE RECEPTOR 3; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 84971557656     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.04.014     Document Type: Article

References (32)

1. Bin, J.M., Han, D., Lai Wing Sun, K., Croteau, L.P., Dumontier, E., Cloutier, J.F., Kania, A., Kennedy, T.E., Complete Loss of Netrin-1 Results in Embryonic Lethality and Severe Axon Guidance Defects without Increased Neural Cell Death. Cell Rep. 12 (2015), 1099–1106.
2. Calvet, G., Aguiar, R.S., Melo, A.S.O., Sampaio, S.A., de Filippis, I., Fabri, A., Araujo, E.S.M., de Sequeira, P.C., de Mendonça, M.C.L., de Oliveira, L., et al. Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect. Dis., 2016, 10.1016/S1473-3099(16)00095-5 in press. Published online February 17, 2016.
3. Cameron, J.S., Alexopoulou, L., Sloane, J.A., DiBernardo, A.B., Ma, Y., Kosaras, B., Flavell, R., Strittmatter, S.M., Volpe, J., Sidman, R., Vartanian, T., Toll-like receptor 3 is a potent negative regulator of axonal growth in mammals. J. Neurosci. 27 (2007), 13033–13041.
4. Camp, J.G., Badsha, F., Florio, M., Kanton, S., Gerber, T., Wilsch-Bräuninger, M., Lewitus, E., Sykes, A., Hevers, W., Lancaster, M., et al. Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. Proc. Natl. Acad. Sci. USA 112 (2015), 15672–15677.
5. Chumley, M.J., Catchpole, T., Silvany, R.E., Kernie, S.G., Henkemeyer, M., EphB receptors regulate stem/progenitor cell proliferation, migration, and polarity during hippocampal neurogenesis. J. Neurosci. 27 (2007), 13481–13490.
6. De Miranda, J., Yaddanapudi, K., Hornig, M., Villar, G., Serge, R., Lipkin, W.I., Induction of Toll-like receptor 3-mediated immunity during gestation inhibits cortical neurogenesis and causes behavioral disturbances. MBio, 1, 2010, 10.
7. Driggers, R.W., Ho, C.Y., Korhonen, E.M., Kuivanen, S., Jääskeläinen, A.J., Smura, T., Rosenberg, A., Hill, D.A., DeBiasi, R.L., Vezina, G., et al. Zika Virus Infection with Prolonged Maternal Viremia and Fetal Brain Abnormalities. N. Engl. J. Med., 2016, 10.1056/NEJMoa1601824 in press. Published online March 30.
8. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., Sasai, Y., Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3 (2008), 519–532.
9. Furne, C., Rama, N., Corset, V., Chédotal, A., Mehlen, P., Netrin-1 is a survival factor during commissural neuron navigation. Proc. Natl. Acad. Sci. USA 105 (2008), 14465–14470.
10. Hamel, R., Dejarnac, O., Wichit, S., Ekchariyawat, P., Neyret, A., Luplertlop, N., Perera-Lecoin, M., Surasombatpattana, P., Talignani, L., Thomas, F., et al. Biology of Zika Virus Infection in Human Skin Cells. J. Virol. 89 (2015), 8880–8896.
11. Kang, H.J., Kawasawa, Y.I., Cheng, F., Zhu, Y., Xu, X., Li, M., Sousa, A.M., Pletikos, M., Meyer, K.A., Sedmak, G., et al. Spatio-temporal transcriptome of the human brain. Nature 478 (2011), 483–489.
12. Katakowski, M., Zhang, Z., deCarvalho, A.C., Chopp, M., EphB2 induces proliferation and promotes a neuronal fate in adult subventricular neural precursor cells. Neurosci. Lett. 385 (2005), 204–209.
13. Koehler, K.R., Hashino, E., 3D mouse embryonic stem cell culture for generating inner ear organoids. Nat. Protoc. 9 (2014), 1229–1244.
14. Lancaster, M.A., Knoblich, J.A., Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 345, 2014, 1247125.
15. Lancaster, M.A., Renner, M., Martin, C.A., Wenzel, D., Bicknell, L.S., Hurles, M.E., Homfray, T., Penninger, J.M., Jackson, A.P., Knoblich, J.A., Cerebral organoids model human brain development and microcephaly. Nature 501 (2013), 373–379.
16. Lathia, J.D., Okun, E., Tang, S.C., Griffioen, K., Cheng, A., Mughal, M.R., Laryea, G., Selvaraj, P.K., ffrench-Constant, C., Magnus, T., et al. Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J. Neurosci. 28 (2008), 13978–13984.
17. Lazear, H.M., Govero, J., Smith, A.M., Platt, D.J., Fernandez, E., Miner, J.J., Diamond, M.S., A Mouse Model of Zika Virus Pathogenesis. Cell Host Microbe, 2016, 10.1016/j.chom.2016.03.010 in press. Published online April 5, 2016.
18. Mariani, J., Coppola, G., Zhang, P., Abyzov, A., Provini, L., Tomasini, L., Amenduni, M., Szekely, A., Palejev, D., Wilson, M., et al. FOXG1-Dependent Dysregulation of GABA/Glutamate Neuron Differentiation in Autism Spectrum Disorders. Cell 162 (2015), 375–390.
19. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., et al. Zika Virus Associated with Microcephaly. N. Engl. J. Med. 374 (2016), 951–958.
20. Nowakowski, T.J., Pollen, A.A., Di Lullo, E., Sandoval-Espinosa, C., Bershteyn, M., Kriegstein, A.R., Expression Analysis Highlights AXL as a Candidate Zika Virus Entry Receptor in Neural Stem Cells. Cell Stem Cell 18 (2016), 591–596.
21. Okun, E., Griffioen, K., Barak, B., Roberts, N.J., Castro, K., Pita, M.A., Cheng, A., Mughal, M.R., Wan, R., Ashery, U., Mattson, M.P., Toll-like receptor 3 inhibits memory retention and constrains adult hippocampal neurogenesis. Proc. Natl. Acad. Sci. USA 107 (2010), 15625–15630.
22. Okun, E., Griffioen, K.J., Mattson, M.P., Toll-like receptor signaling in neural plasticity and disease. Trends Neurosci. 34 (2011), 269–281.
23. Ozmadenci, D., Féraud, O., Markossian, S., Kress, E., Ducarouge, B., Gibert, B., Ge, J., Durand, I., Gadot, N., Plateroti, M., et al. Netrin-1 regulates somatic cell reprogramming and pluripotency maintenance. Nat. Commun., 6, 2015, 7398.
24. Petersen, E., Wilson, M.E., Touch, S., McCloskey, B., Mwaba, P., Bates, M., Dar, O., Mattes, F., Kidd, M., Ippolito, G., et al. Rapid Spread of Zika Virus in The Americas - Implications for Public Health Preparedness for Mass Gatherings at the 2016 Brazil Olympic Games. Int. J. Infect. Dis. 44 (2016), 11–15.
25. Poliak, S., Morales, D., Croteau, L.P., Krawchuk, D., Palmesino, E., Morton, S., Cloutier, J.F., Charron, F., Dalva, M.B., Ackerman, S.L., et al. Synergistic integration of Netrin and ephrin axon guidance signals by spinal motor neurons. eLife, 4, 2015, 4.
26. Rossi, S.L., Tesh, R.B., Azar, S.R., Muruato, A.E., Hanley, K.A., Auguste, A.J., Langsjoen, R.M., Paessler, S., Vasilakis, N., Weaver, S.C., Characterization of a Novel Murine Model to Study Zika Virus. Am. J. Trop. Med. Hyg., 2016, 10.4269/ajtmh.16-0111 in press. Published online March 28, 2016.
27. Shiose, S., Chen, Y., Okano, K., Roy, S., Kohno, H., Tang, J., Pearlman, E., Maeda, T., Palczewski, K., Maeda, A., Toll-like receptor 3 is required for development of retinopathy caused by impaired all-trans-retinal clearance in mice. J. Biol. Chem. 286 (2011), 15543–15555.
28. Sips, G.J., Wilschut, J., Smit, J.M., Neuroinvasive flavivirus infections. Rev. Med. Virol. 22 (2012), 69–87.
29. Tang, H., Hammack, C., Ogden, S.C., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E.M., et al. Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth. Cell Stem Cell 18 (2016), 587–590.
30. Tsai, Y.T., Chang, S.Y., Lee, C.N., Kao, C.L., Human TLR3 recognizes dengue virus and modulates viral replication in vitro. Cell. Microbiol. 11 (2009), 604–615.
31. Yaddanapudi, K., De Miranda, J., Hornig, M., Lipkin, W.I., Toll-like receptor 3 regulates neural stem cell proliferation by modulating the Sonic Hedgehog pathway. PLoS ONE, 6, 2011, e26766.
32. Yamanaka, S., Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10 (2012), 678–684.