{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T15:44:12Z","timestamp":1777563852140,"version":"3.51.4"},"reference-count":58,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2020,6,2]],"date-time":"2020-06-02T00:00:00Z","timestamp":1591056000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100006827","name":"Florida Department of Health","doi-asserted-by":"publisher","award":["7ZK09"],"award-info":[{"award-number":["7ZK09"]}],"id":[{"id":"10.13039\/100006827","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["DA036154"],"award-info":[{"award-number":["DA036154"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Here, we used a mouse model with defective autophagy to further decipher the role of Beclin1 in the infection and disease of Zika virus (ZIKV)-R103451. Hemizygous (Becn1+\/\u2212) and wild-type (Becn1+\/+) pregnant mice were transiently immunocompromised using the anti-interferon alpha\/beta receptor subunit 1 monoclonal antibody MAR1-5A3. Despite a low mortality rate among the infected dams, 25% of Becn1+\/\u2212 offspring were smaller in size and had smaller, underdeveloped brains. This phenotype became apparent after 2-to 3-weeks post-birth. Furthermore, the smaller-sized pups showed a decrease in the mRNA expression levels of insulin-like growth factor (IGF)-1 and the expression levels of several microcephaly associated genes, when compared to their typical-sized siblings. Neuronal loss was also noticeable in brain tissues that were removed postmortem. Further analysis with murine mixed glia, derived from ZIKV-infected Becn1+\/\u2212 and Becn1+\/+ pups, showed greater infectivity in glia derived from the Becn1+\/\u2212 genotype, along with a significant increase in pro-inflammatory molecules. In the present study, we identified a link by which defective autophagy is causally related to increased inflammatory molecules, reduced growth factor, decreased expression of microcephaly-associated genes, and increased neuronal loss. Specifically, we showed that a reduced expression of Beclin1 aggravated the consequences of ZIKV infection on brain development and qualifies Becn1 as a susceptibility gene of ZIKV congenital syndrome.<\/jats:p>","DOI":"10.3390\/v12060608","type":"journal-article","created":{"date-parts":[[2020,6,3]],"date-time":"2020-06-03T04:12:09Z","timestamp":1591157529000},"page":"608","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Reduced-Beclin1-Expressing Mice Infected with Zika-R103451 and Viral-Associated Pathology during Pregnancy"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2795-5689","authenticated-orcid":false,"given":"Mohan Kumar Muthu","family":"Karuppan","sequence":"first","affiliation":[{"name":"Department of Immunology and Nanomedicine, Herbert Wertheim College of Medicine, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6816-8892","authenticated-orcid":false,"given":"Chet Raj","family":"Ojha","sequence":"additional","affiliation":[{"name":"Department of Immunology and Nanomedicine, Herbert Wertheim College of Medicine, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Myosotys","family":"Rodriguez","sequence":"additional","affiliation":[{"name":"Department of Immunology and Nanomedicine, Herbert Wertheim College of Medicine, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0606-9792","authenticated-orcid":false,"given":"Jessica","family":"Lapierre","sequence":"additional","affiliation":[{"name":"Department of Immunology and Nanomedicine, Herbert Wertheim College of Medicine, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6977-4707","authenticated-orcid":false,"given":"M. Javad","family":"Aman","sequence":"additional","affiliation":[{"name":"Integrated Biotherapeutics, Rockville, MD 20850, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fatah","family":"Kashanchi","sequence":"additional","affiliation":[{"name":"National Center for Biodefense and Infectious Diseases, George Mason University, Manassas, VA 20110, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4475-2119","authenticated-orcid":false,"given":"Michal","family":"Toborek","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, University of Miami Miller School of Medicine, Miami, FL 33136, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Madhavan","family":"Nair","sequence":"additional","affiliation":[{"name":"Department of Immunology and Nanomedicine, Herbert Wertheim College of Medicine, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nazira","family":"El-Hage","sequence":"additional","affiliation":[{"name":"Department of Immunology and Nanomedicine, Herbert Wertheim College of Medicine, Florida International University, Miami, FL 33199, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,6,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1356","DOI":"10.1016\/S1473-3099(16)30318-8","article-title":"Association between Zika virus infection and microcephaly in Brazil, January to May, 2016: Preliminary report of a case-control study","volume":"16","author":"Rodrigues","year":"2016","journal-title":"Lancet Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"191","DOI":"10.2471\/BLT.16.178608","article-title":"Risk of microcephaly after Zika virus infection in Brazil, 2015 to 2016","volume":"95","author":"Jaenisch","year":"2017","journal-title":"Bull. World Health Organ."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1513","DOI":"10.1056\/NEJMoa1605564","article-title":"Guillain-Barre Syndrome Associated with Zika Virus Infection in Colombia","volume":"375","author":"Parra","year":"2016","journal-title":"N. Engl. J. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"951","DOI":"10.1056\/NEJMoa1600651","article-title":"Zika Virus Associated with Microcephaly","volume":"374","author":"Mlakar","year":"2016","journal-title":"N. Engl. J. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"26","DOI":"10.5858\/arpa.2016-0382-RA","article-title":"Zika Virus Infection in Pregnancy, Microcephaly, and Maternal and Fetal Health: What We Think, What We Know, and What We Think We Know","volume":"14","author":"Alvarado","year":"2017","journal-title":"Arch. Pathol. Lab. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1016\/0035-9203(52)90042-4","article-title":"Zika virus. I. Isolations and serological specificity","volume":"46","author":"Dick","year":"1952","journal-title":"Trans. R. Soc. Trop Med. Hyg."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"547986","DOI":"10.1155\/2014\/547986","article-title":"Molecular and cellular basis of autosomal recessive primary microcephaly","volume":"2014","author":"Barbelanne","year":"2014","journal-title":"Biomed. Res. Int."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.stem.2016.04.017","article-title":"Zika Virus Disrupts Neural Progenitor Development and Leads to Microcephaly in Mice","volume":"19","author":"Li","year":"2016","journal-title":"Cell Stem Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/j.stem.2016.02.016","article-title":"Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth","volume":"18","author":"Tang","year":"2016","journal-title":"Cell Stem Cell"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"8610","DOI":"10.1093\/nar\/gkw765","article-title":"Molecular signatures associated with ZIKV exposure in human cortical neural progenitors","volume":"44","author":"Zhang","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Faheem, M., Naseer, M.I., Rasool, M., Chaudhary, A.G., Kumosani, T.A., Ilyas, A.M., Pushparaj, P., Ahmed, F., Algahtani, H.A., and Al-Qahtani, M.H. (2015). Molecular genetics of human primary microcephaly: An overview. BMC Med. Genom., 8.","DOI":"10.1186\/1755-8794-8-S1-S4"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1002\/wdev.89","article-title":"Genetic causes of microcephaly and lessons for neuronal development","volume":"2","author":"Gilmore","year":"2013","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1002\/ana.24839","article-title":"Immune activation in amniotic fluid from Zika virus-associated microcephaly","volume":"81","author":"Ornelas","year":"2017","journal-title":"Ann. Neurol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Ojha, C.R., Rodriguez, M., Karuppan, M.K.M., Lapierre, J., Kashanchi, F., and El-Hage, N. (2019). Toll-like receptor 3 regulates Zika virus infection and associated host inflammatory response in primary human astrocytes. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0208543"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.4161\/auto.7.11.17661","article-title":"A comprehensive glossary of autophagy-related molecules and processes (2nd edition)","volume":"7","author":"Klionsky","year":"2011","journal-title":"Autophagy"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1007\/s11481-018-9788-3","article-title":"Critical Role of Beclin1 in HIV Tat and Morphine-Induced Inflammation and Calcium Release in Glial Cells from Autophagy Deficient Mouse","volume":"13","author":"Lapierre","year":"2018","journal-title":"J. Neuroimmune Pharm."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"672","DOI":"10.1038\/45257","article-title":"Induction of autophagy and inhibition of tumorigenesis by beclin 1","volume":"9","author":"Liang","year":"1999","journal-title":"Nature"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4778","DOI":"10.1038\/s41598-018-23078-y","article-title":"Author Correction: Intranasal drug delivery of small interfering RNA targeting Beclin1 encapsulated with polyethylenimine (PEI) in mouse brain to achieve HIV attenuation","volume":"8","author":"Rodriguez","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1016\/S0306-4522(00)00461-9","article-title":"Synergistic neurotoxicity of opioids and human immunodeficiency virus-1 Tat protein in striatal neurons in vitro","volume":"102","author":"Gurwell","year":"2001","journal-title":"Neuroscience"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"13924","DOI":"10.1128\/JVI.79.22.13924-13933.2005","article-title":"NS1 protein secretion during the acute phase of West Nile virus infection","volume":"79","author":"Macdonald","year":"2005","journal-title":"J. Virol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1016\/j.bbrc.2008.02.055","article-title":"TMEM74, a lysosome and autophagosome protein, regulates autophagy","volume":"369","author":"Yu","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Tripathi, S., Balasubramaniam, V.R., Brown, J.A., Mena, I., Grant, A., Bardina, S.V., Maringer, K., Schwarz, M.C., Maestre, A.M., and Sourisseau, M. (2017). A novel Zika virus mouse model reveals strain specific differences in virus pathogenesis and host inflammatory immune responses. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006258"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1016\/j.chom.2016.03.010","article-title":"A Mouse Model of Zika Virus Pathogenesis","volume":"19","author":"Lazear","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1038\/cr.2016.58","article-title":"Vertical transmission of Zika virus targeting the radial glial cells affects cortex development of offspring mice","volume":"26","author":"Wu","year":"2016","journal-title":"Cell Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/S0079-6123(01)32113-1","article-title":"Glial cells as targets of viral infection in the human central nervous system","volume":"132","author":"Schweighardt","year":"2001","journal-title":"Prog. Brain Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"201","DOI":"10.3389\/fmicb.2012.00201","article-title":"Viral CNS infections: Role of glial pattern recognition receptors in neuroinflammation","volume":"3","author":"Furr","year":"2012","journal-title":"Front. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1128\/JCM.40.02.376-381.2002","article-title":"Enzyme-linked immunosorbent assay specific to Dengue virus type 1 nonstructural protein NS1 reveals circulation of the antigen in the blood during the acute phase of disease in patients experiencing primary or secondary infections","volume":"40","author":"Alcon","year":"2002","journal-title":"J. Clin. Microbiol"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1165","DOI":"10.1086\/343813","article-title":"High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever","volume":"186","author":"Libraty","year":"2002","journal-title":"J. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.1084\/jem.20170957","article-title":"Inhibition of autophagy limits vertical transmission of Zika virus in pregnant mice","volume":"214","author":"Cao","year":"2017","journal-title":"J. Exp. Med."},{"key":"ref_30","first-page":"4114","article-title":"The African Zika virus MR-766 is more virulent and causes more severe brain damage than current Asian lineage and dengue virus","volume":"144","author":"Shao","year":"2017","journal-title":"Development"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e00292-17","DOI":"10.1128\/mSphere.00292-17","article-title":"Phenotypic Differences between Asian and African Lineage Zika Viruses in Human Neural Progenitor Cells","volume":"2","author":"Anfasa","year":"2017","journal-title":"mSphere"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s12250-018-0078-2","article-title":"The Asian Lineage of Zika Virus: Transmission and Evolution in Asia and the Americas","volume":"34","author":"Hu","year":"2019","journal-title":"Virol. Sin."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e00113","DOI":"10.1128\/JVI.00113-19","article-title":"Envelope Protein Glycosylation Mediates Zika Virus Pathogenesis","volume":"93","author":"Carbaugh","year":"2019","journal-title":"J. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Ferdin, J., Goricar, K., Dolzan, V., Plemenitas, A., Martin, J.N., Peterlin, B.M., Deeks, S.G., and Lenassi, M. (2018). Viral protein Nef is detected in plasma of half of HIV-infected adults with undetectable plasma HIV RNA. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0191613"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e273","DOI":"10.1002\/wdev.273","article-title":"Potential mechanisms of Zika-linked microcephaly","volume":"6","author":"Merfeld","year":"2017","journal-title":"Wiley Interdiscip Rev. Dev. Biol"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1038\/ng.682","article-title":"WDR62 is associated with the spindle pole and is mutated in human microcephaly","volume":"42","author":"Nicholas","year":"2010","journal-title":"Nat. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1038\/ng.683","article-title":"Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture","volume":"42","author":"Yu","year":"2010","journal-title":"Nat. Genet."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3885","DOI":"10.1038\/ncomms4885","article-title":"Microcephaly disease gene Wdr62 regulates mitotic progression of embryonic neural stem cells and brain size","volume":"5","author":"Chen","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1007\/s00439-015-1619-5","article-title":"A novel homozygous splicing mutation of CASC5 causes primary microcephaly in a large Pakistani family","volume":"135","author":"Szczepanski","year":"2016","journal-title":"Hum. Genet."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.dnarep.2013.04.017","article-title":"DNA damage response in microcephaly development of MCPH1 mouse model","volume":"12","author":"Zhou","year":"2013","journal-title":"DNA Repair (Amsterdam)"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1128\/CMR.00014-16","article-title":"Emerging Role of Zika Virus in Adverse Fetal and Neonatal Outcomes","volume":"29","author":"Panchaud","year":"2016","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1016\/j.devcel.2011.12.027","article-title":"A Dual Role for UVRAG in Maintaining Chromosomal Stability Independent of Autophagy","volume":"22","author":"Zhao","year":"2012","journal-title":"Dev. Cell"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1101\/gad.1545107","article-title":"Autophagy suppresses tumor progression by limiting chromosomal instability","volume":"21","author":"Mathew","year":"2007","journal-title":"Genes Dev."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Kadir, R., Harel, T., Markus, B., Perez, Y., Bakhrat, A., Cohen, I., Volodarsky, M., Feintsein-Linial, M., Chervinski, E., and Zlotogora, J. (2016). ALFY-Controlled DVL3 Autophagy Regulates Wnt Signaling, Determining Human Brain Size. PLoS Genet., 12.","DOI":"10.1371\/journal.pgen.1005919"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1186\/s12974-019-1443-2","article-title":"The role of microglia in viral encephalitis: A review","volume":"16","author":"Chen","year":"2019","journal-title":"J. Neuroinflamm."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.chom.2018.05.022","article-title":"Inflammation-Induced, STING-Dependent Autophagy Restricts Zika Virus Infection in the Drosophila Brain","volume":"24","author":"Liu","year":"2018","journal-title":"Cell Host Microbe"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1016\/j.stem.2016.07.019","article-title":"Zika Virus NS4A and NS4B Proteins Deregulate Akt-mTOR Signaling in Human Fetal Neural Stem Cells to Inhibit Neurogenesis and Induce Autophagy","volume":"19","author":"Liang","year":"2016","journal-title":"Cell Stem Cell"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"2340","DOI":"10.3389\/fimmu.2018.02340","article-title":"Complementary Mechanisms Potentially Involved in the Pathology of Zika Virus","volume":"9","author":"Ojha","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Peng, H., Liu, B., Yves, T.D., He, Y., Wang, S., Tang, H., Ren, H., Zhao, P., Qi, Z., and Qin, Z. (2018). Zika Virus Induces Autophagy in Human Umbilical Vein Endothelial Cells. Viruses, 10.","DOI":"10.3390\/v10050259"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.virusres.2017.09.006","article-title":"Role of autophagy in Zika virus infection and pathogenesis","volume":"254","author":"Chiramel","year":"2018","journal-title":"Virus Res."},{"key":"ref_51","first-page":"703","article-title":"Treatment of dwarfism with recombinant human insulin-like growth factor-1","volume":"106","author":"Ranke","year":"2009","journal-title":"Dtsch. Arztebl. Int."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"263","DOI":"10.3389\/fendo.2019.00263","article-title":"Roles of Type 1 Insulin-Like Growth Factor (IGF) Receptor and IGF-II in Growth Regulation: Evidence From a Patient Carrying Both an 11p Paternal Duplication and 15q Deletion","volume":"10","author":"Giabicani","year":"2019","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/0896-6273(95)90216-3","article-title":"Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons","volume":"14","author":"Beck","year":"1995","journal-title":"Neuron"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1017\/S0012162206001605","article-title":"Cerebrospinal fluid insulin-like growth factors IGF-1 and IGF-2 in infantile autism","volume":"48","author":"Riikonen","year":"2006","journal-title":"Dev. Med. Child. Neurol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Riikonen, R. (2017). Insulin-Like Growth Factors in the Pathogenesis of Neurological Diseases in Children. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18102056"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Das, G., Shravage, B.V., and Baehrecke, E.H. (2012). Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb. Perspect. Biol.","DOI":"10.1101\/cshperspect.a008813"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2158","DOI":"10.3389\/fmicb.2019.02158","article-title":"Selective Disruption of the Blood-Brain Barrier by Zika Virus","volume":"10","author":"Leda","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1016\/j.cell.2010.02.016","article-title":"Mechanisms underlying inflammation in neurodegeneration","volume":"140","author":"Glass","year":"2010","journal-title":"Cell"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/6\/608\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:35:03Z","timestamp":1760175303000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/12\/6\/608"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,2]]},"references-count":58,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,6]]}},"alternative-id":["v12060608"],"URL":"https:\/\/doi.org\/10.3390\/v12060608","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,2]]}}}