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Open Access 01-06-2017 | Review

Molecular and cellular insights into Zika virus-related neuropathies

Authors: Kai Zhou, Long Wang, Di Yu, Hesuyuan Huang, Hong Ji, Xuming Mo

Published in: Journal of NeuroVirology | Issue 3/2017

Abstract

Zika virus (ZIKV), a relatively elusive Aedes mosquito-transmitted flavivirus, had been brought into spotlight until recent widespread outbreaks accompanied by unexpectedly severe clinical neuropathies, including fetal microcephaly and Guillain–Barré syndrome (GBS) in the adult. In this review, we focus on the underlying cellular and molecular mechanisms by which vertically transmitted microorganisms reach the fetus and trigger neuropathies.

Abbink P, Larocca RA, De La Barrera RA, Bricault CA, Moseley ET, Boyd M, Kirilova M, Li Z, Ng’ang’a D, Nanayakkara O et al (2016) Protective efficacy of multiple vaccine platforms against Zika virus challenge in rhesus monkeys. Science 353:1129–1132CrossRefPubMedPubMedCentral

Adams Waldorf, K.M., Stencel-Baerenwald, J.E., Kapur, R.P., Studholme, C., Boldenow, E., Vornhagen, J., Baldessari, A., Dighe, M.K., Thiel, J., Merillat, S., et al. (2016). Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate. Nat Med

Barba-Spaeth G, Dejnirattisai W, Rouvinski A, Vaney MC, Medits I, Sharma A, Simon-Loriere E, Sakuntabhai A, Cao-Lormeau VM, Haouz A et al (2016) Structural basis of potent Zika-dengue virus antibody cross-neutralization. Nature 536:48–53CrossRefPubMed

Barkovich AJ, Guerrini R, Kuzniecky RI, Jackson GD, Dobyns WB (2012) A developmental and genetic classification for malformations of cortical development: update 2012. Brain 135:1348–1369CrossRefPubMedPubMedCentral

Baronti C, Piorkowski G, Charrel RN, Boubis L, Leparc-Goffart I, de Lamballerie X (2014) Complete coding sequence of zika virus from a French polynesia outbreak in 2013. Genome Announc 2

Bell TM, Field EJ, Narang HK (1971) Zika virus infection of the central nervous system of mice. Arch Gesamte Virusforsch 35:183–193CrossRefPubMed

Brasil, P., and Nielsen-Saines, K. (2016). More pieces to the microcephaly-Zika virus puzzle in Brazil. The Lancet Infectious diseases

Brasil P, Calvet GA, Siqueira AM, Wakimoto M, de Sequeira PC, Nobre A, Quintana Mde S, Mendonca MC, Lupi O, de Souza RV et al (2016a) Zika virus outbreak in Rio de Janeiro, Brazil: clinical characterization, epidemiological and Virological aspects. PLoS Negl Trop Dis 10:e0004636CrossRefPubMedPubMedCentral

Brasil, P., Pereira, J.P., Jr., Raja Gabaglia, C., Damasceno, L., Wakimoto, M., Ribeiro Nogueira, R.M., Carvalho de Sequeira, P., Machado Siqueira, A., Abreu de Carvalho, L.M., Cotrim da Cunha, D., et al. (2016b). Zika virus infection in pregnant women in Rio de Janeiro—preliminary Report. The New England journal of medicine

Broutet N, Krauer F, Riesen M, Khalakdina A, Almiron M, Aldighieri S, Espinal M, Low N, Dye C (2016) Zika virus as a cause of neurologic disorders. N Engl J Med 374:1506–1509CrossRefPubMed

Budday S, Steinmann P, Kuhl E (2015) Physical biology of human brain development. Front Cell Neurosci 9:257CrossRefPubMedPubMedCentral

Calvet G, Aguiar RS, Melo AS, Sampaio SA, de Filippis I, Fabri A, Araujo ES, de Sequeira PC, de Mendonca MC, de Oliveira L et al (2016) Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect Dis 16:653–660CrossRefPubMed

Carteaux G, Maquart M, Bedet A, Contou D, Brugieres P, Fourati S, Cleret de Langavant L, de Broucker T, Brun-Buisson C, Leparc-Goffart I et al (2016) Zika virus associated with meningoencephalitis. N Engl J Med 374:1595–1596CrossRefPubMed

Coyne CB, Lazear HM (2016) Zika virus—reigniting the TORCH. Nat Rev Microbiol 14:707–715CrossRefPubMed

Cugola FR, Fernandes IR, Russo FB, Freitas BC, Dias JL, Guimaraes KP, Benazzato C, Almeida N, Pignatari GC, Romero S et al (2016) The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534:267–271PubMedPubMedCentral

Dang J, Tiwari SK, Lichinchi G, Qin Y, Patil VS, Eroshkin AM, Rana TM (2016) Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19:258–265CrossRefPubMed

de Fatima Vasco Aragao M, van der Linden V, Brainer-Lima AM, Coeli RR, Rocha MA, Sobral da Silva P, Durce Costa Gomes de Carvalho M, van der Linden A, Cesario de Holanda A, Valenca MM (2016) Clinical features and neuroimaging (CT and MRI) findings in presumed Zika virus related congenital infection and microcephaly: retrospective case series study. BMJ 353:i1901CrossRefPubMedPubMedCentral

Diamond MS, Pierson TC (2015) Molecular insight into dengue virus pathogenesis and its implications for disease control. Cell 162:488–492CrossRefPubMedPubMedCentral

D’Ortenzio E, Matheron S, Yazdanpanah Y, de Lamballerie X, Hubert B, Piorkowski G, Maquart M, Descamps D, Damond F, Leparc-Goffart I (2016) Evidence of sexual transmission of Zika Virus. N Engl J Med 374:2195–2198CrossRefPubMed

Dowd, K.A., Ko, S.Y., Morabito, K.M., Yang, E.S., Pelc, R.S., DeMaso, C.R., Castilho, L.R., Abbink, P., Boyd, M., Nityanandam, R., et al. (2016). Rapid development of a DNA vaccine for Zika virus. Science

Faria NR, Azevedo Rdo S, Kraemer MU, Souza R, Cunha MS, Hill SC, Theze J, Bonsall MB, Bowden TA, Rissanen I et al (2016) Zika virus in the Americas: early epidemiological and genetic findings. Science 352:345–349CrossRefPubMedPubMedCentral

Garcez PP, Loiola EC, Madeiro da Costa R, Higa LM, Trindade P, Delvecchio R, Nascimento JM, Brindeiro R, Tanuri A, Rehen SK (2016) Zika virus impairs growth in human neurospheres and brain organoids. Science 352:816–818CrossRefPubMed

Haddow AD, Schuh AJ, Yasuda CY, Kasper MR, Heang V, Huy R, Guzman H, Tesh RB, Weaver SC (2012) Genetic characterization of Zika virus strains: geographic expansion of the Asian lineage. PLoS Negl Trop Dis 6:e1477CrossRefPubMedPubMedCentral

Hamel R, Dejarnacphélie, Wichit S, Ekchariyawat P, Neyret A, Luplertlop N, Perera-Lecoin M, Surasombatpattana P, Talignani L, Thomas F, Cao-Lormeau V-M, Choumet V, Briant L, Desprès P, Amara A, Yssel H, Missé D, Diamond MS (2015) Biology of Zika virus infection in human skin cells. J Virol 89(17):8880–8896

Hayes EB (2009) Zika virus outside Africa. Emerg Infect Dis 15:1347–1350CrossRefPubMedPubMedCentral

Heymann DL, Hodgson A, Sall AA, Freedman DO, Staples JE, Althabe F, Baruah K, Mahmud G, Kandun N, Vasconcelos PF et al (2016) Zika virus and microcephaly: why is this situation a PHEIC? Lancet 387:719–721CrossRefPubMed

Hills SL, Russell K, Hennessey M, Williams C, Oster AM, Fischer M, Mead P (2016) Transmission of Zika virus through sexual contact with travelers to areas of ongoing transmission—continental United States, 2016. MMWR Morb Mortal Wkly Rep 65:215–216CrossRefPubMed

Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184CrossRefPubMedPubMedCentral

Kuno G, Chang GJ (2007) Full-length sequencing and genomic characterization of Bagaza, Kedougou, and Zika viruses. Arch Virol 152:687–696CrossRefPubMed

Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR (2008) Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg Infect Dis 14:1232–1239CrossRefPubMedPubMedCentral

Lazear HM, Diamond MS (2016) Zika virus: new clinical syndromes and its emergence in the Western hemisphere. J Virol 90:4864–4875CrossRefPubMedPubMedCentral

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 19:720–730CrossRefPubMedPubMedCentral

Lee DY (2015) Roles of mTOR signaling in brain development. Exp Neurobiol 24:177–185CrossRefPubMedPubMedCentral

Li C, Xu D, Ye Q, Hong S, Jiang Y, Liu X, Zhang N, Shi L, Qin CF, Xu Z (2016a) Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19:120–126CrossRefPubMed

Li, H., Saucedo-Cuevas, L., Regla-Nava, J.A., Chai, G., Sheets, N., Tang, W., Terskikh, A.V., Shresta, S., and Gleeson, J.G. (2016b). Zika virus infects neural progenitors in the adult mouse brain and alters proliferation. Cell stem cell

Liang, Q., Luo, Z., Zeng, J., Chen, W., Foo, S.S., Lee, S.A., Ge, J., Wang, S., Goldman, S.A., Zlokovic, B.V., 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

Luethy LN, Erickson AK, Jesudhasan PR, Ikizler M, Dermody TS, Pfeiffer JK (2016) Comparison of three neurotropic viruses reveals differences in viral dissemination to the central nervous system. Virology 487:1–10CrossRefPubMed

Malkki H (2016a) CNS infections: mouse studies confirm the link between Zika virus infection and microcephaly. Nat Rev Neurol 12:369CrossRefPubMed

Malkki H (2016b) CNS infections: Zika virus infection could trigger Guillain-Barre syndrome. Nat Rev Neurol 12:187CrossRefPubMed

Mansuy JM, Pasquier C, Daudin M, Chapuy-Regaud S, Moinard N, Chevreau C, Izopet J, Mengelle C, Bujan L (2016) Zika virus in semen of a patient returning from a non-epidemic area. Lancet Infect Dis 16:894–895CrossRefPubMed

Martines RB, Bhatnagar J, Keating MK, Silva-Flannery L, Muehlenbachs A, Gary J, Goldsmith C, Hale G, Ritter J, Rollin D et al (2016) Notes from the field: evidence of Zika virus infection in brain and placental tissues from two congenitally infected newborns and two fetal losses—Brazil, 2015. MMWR Morb Mortal Wkly Rep 65:159–160CrossRefPubMed

Miner JJ, Cao B, Govero J, Smith AM, Fernandez E, Cabrera OH, Garber C, Noll M, Klein RS, Noguchi KK et al (2016a) Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cel l 165:1081–1091CrossRef

Miner, J.J., Sene, A., Richner, J.M., Smith, A.M., Santeford, A., Ban, N., Weger-Lucarelli, J., Manzella, F., Ruckert, C., Govero, J., et al. (2016b). Zika virus infection in mice causes panuveitis with shedding of virus in tears. Cell Rep

Mlakar J, Korva M, Tul N, Popovic M, Poljsak-Prijatelj M, Mraz J, Kolenc M, Resman Rus K, Vesnaver Vipotnik T, Fabjan Vodusek V et al (2016) Zika virus associated with microcephaly. N Engl J Med 374:951–958CrossRefPubMed

Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427–437CrossRefPubMed

Mukhopadhyay S, Kuhn RJ, Rossmann MG (2005) A structural perspective of the flavivirus life cycle. Nat Rev Microbiol 3:13–22CrossRefPubMed

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 18:591–596CrossRefPubMedPubMedCentral

Parra, B., Lizarazo, J., Jimenez-Arango, J.A., Zea-Vera, A.F., Gonzalez-Manrique, G., Vargas, J., Angarita, J.A., Zuniga, G., Lopez-Gonzalez, R., Beltran, C.L., et al. (2016). Guillain-Barre Syndrome associated with Zika virus infection in Colombia. The New England journal of medicine

Pastula DM, Smith DE, Beckham JD, Tyler KL (2016) Four emerging arboviral diseases in North America: Jamestown Canyon, Powassan, chikungunya, and Zika virus diseases. J Neurovirol 22:257–260CrossRefPubMedPubMedCentral

Perera-Lecoin M, Meertens L, Carnec X, Amara A (2013) Flavivirus entry receptors: an update. Viruses 6:69–88CrossRefPubMedPubMedCentral

Petersen E, Wilson ME, Touch S, McCloskey B, Mwaba P, Bates M, Dar O, Mattes F, Kidd M, Ippolito G et al (2016) Rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases 44:11–15CrossRef

Pierson, T.C., and Graham, B.S. (2016). Zika virus: immunity and vaccine development. Cell

Prisant, N., Bujan, L., Benichou, H., Hayot, P.H., Pavili, L., Lurel, S., Herrmann, C., Janky, E., and Joguet, G. (2016). Zika virus in the female genital tract. The Lancet Infectious diseases

Qian X, Nguyen HN, Song MM, Hadiono C, Ogden SC, Hammack C, Yao B, Hamersky GR, Jacob F, Zhong C et al (2016) Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165:1238–1254CrossRefPubMedPubMedCentral

Quicke KM, Bowen JR, Johnson EL, McDonald CE, Ma H, O’Neal JT, Rajakumar A, Wrammert J, Rimawi BH, Pulendran B et al (2016) Zika virus infects human placental macrophages. Cell Host Microbe 20:83–90CrossRefPubMed

Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR (2016) Zika virus and birth defects—reviewing the evidence for causality. N Engl J Med 374:1981–1987CrossRefPubMed

Sarno, M., Sacramento, G.A., Khouri, R., do Rosario, M.S., Costa, F., Archanjo, G., Santos, L.A., Nery, N., Jr., Vasilakis, N., Ko, A.I., et al. (2016). Zika virus infection and stillbirths: a case of hydrops fetalis, hydranencephaly and fetal demise. PLoS Negl Trop Dis 10, e0004517.

Sips GJ, Wilschut J, Smit JM (2012) Neuroinvasive flavivirus infections. Rev Med Virol 22:69–87CrossRefPubMed

Sun, J., Wu, Zhong, H., Guan, D., Zhang, H., Tan, Q., and Ke, C. (2016). Presence of Zika virus in conjunctival fluid. JAMA Ophthalmol

Suter MA, Aagaard KM (2016) Disease watch: Zika virus—placental passage and permissivity for infection. Nat Rev Endocrinol 12:437–438CrossRefPubMed

Suthar MS, Diamond MS, Gale M Jr (2013) West Nile virus infection and immunity. Nat Rev Microbiol 11:115–128CrossRefPubMed

Tabata, T., Petitt, M., Puerta-Guardo, H., Michlmayr, D., Wang, C., Fang-Hoover, J., Harris, E., and Pereira, L. (2016). Zika virus targets different primary human placental cells, suggesting two routes for vertical transmission. Cell host & microbe

Takei N, Nawa H (2014) mTOR signaling and its roles in normal and abnormal brain development. Front Mol Neurosci 7:28CrossRefPubMedPubMedCentral

Tang H, Hammack C, Ogden SC, Wen Z, Qian X, Li Y, Yao B, Shin J, Zhang F, Lee EM et al (2016) Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18:587–590CrossRefPubMedPubMedCentral

van den Berg B, Walgaard C, Drenthen J, Fokke C, Jacobs BC, van Doorn PA (2014) Guillain-Barre syndrome: pathogenesis, diagnosis, treatment and prognosis. Nat Rev Neurol 10:469–482CrossRefPubMed

Wang L, Valderramos SG, Wu A, Ouyang S, Li C, Brasil P, Bonaldo M, Coates T, Nielsen-Saines K, Jiang T et al (2016) From mosquitos to humans: genetic evolution of Zika virus. Cell Host Microbe 19:561–565CrossRefPubMed

Wikan N, Smith DR (2016) Zika virus: history of a newly emerging arbovirus. Lancet Infect Dis 16:e119–e126CrossRefPubMed

Wilsch-Brauninger M, Florio M, Huttner WB (2016) Neocortex expansion in development and evolution—from cell biology to single genes. Curr Opin Neurobiol 39:122–132CrossRefPubMed

Wollnik B (2010) A common mechanism for microcephaly. Nat Genet 42:923–924CrossRefPubMed

Woodworth MB, Custo Greig L, Kriegstein AR, Macklis JD (2012) SnapShot: cortical development. Cell 151(918–918):e911

Wu KY, Zuo GL, Li XF, Ye Q, Deng YQ, Huang XY, Cao WC, Qin CF, Luo ZG (2016) Vertical transmission of Zika virus targeting the radial glial cells affects cortex development of offspring mice. Cell Res 26:645–654CrossRefPubMedPubMedCentral

Title: Molecular and cellular insights into Zika virus-related neuropathies
Authors: Kai Zhou
Long Wang
Di Yu
Hesuyuan Huang
Hong Ji
Xuming Mo
Publication date: 01-06-2017
Publisher: Springer International Publishing
Published in: Journal of NeuroVirology / Issue 3/2017
Print ISSN: 1355-0284
Electronic ISSN: 1538-2443
DOI: https://doi.org/10.1007/s13365-017-0514-3

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Molecular and cellular insights into Zika virus-related neuropathies

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

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