ArticleCell stem cell2017
Zika-Virus-Encoded NS2A Disrupts Mammalian Cortical Neurogenesis by Degrading Adherens Junction Proteins.
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Article in Cell stem cell, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 133 papers.
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133citing papers in PubMed
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133 citing papers in PubMed, 213 citations in OpenAlex.
- Review
- Article
- New developments and applications of human organoids.Nature reviews. Molecular cell biology · 2026Review
- Breaking barriers and beyond: Mechanisms and pathological implications of Zika virus traversal across blood-tissue interfaces.Virologica Sinica · 2026Review
- Human organoids as 3D in vitro platforms for drug discovery: opportunities and challenges.Nature reviews. Drug discovery · 2026Review
- ZIKV envelope protein is a strong blocker of early directional differentiation in the neural lineage.Communications biology · 2026Article
- Comparison of human cerebral organoids infected with wild-type Zika versus attenuated DN-2 virus strains uncovers differences in host immune responses.Cell communication and signaling : CCS · 2025Article
- Hiding in plain sight: Genomic and phenotypic characterization of mosquito-borne Bussuquara virus.PLoS neglected tropical diseases · 2025Article
- An immunocompetent mouse model revealed that congenital Zika virus infection disrupted hippocampal function by activating autophagy.Emerging microbes & infections · 2025Article
- Metabolic functions for molecular chaperones and stress proteins in microcephaly.Cellular and molecular life sciences : CMLS · 2025Review
- Contribution of rare coding variants to microcephaly in individuals with neurodevelopmental disorders.Genome medicine · 2025Article
- Zika virus non-structural protein NS2A mediated endoplasmic reticulum stress through interacting with Sarco/endoplasmic reticulum CaJournal of virology · 2025Article
- Zika virus disrupts steroidogenesis and impairs spermatogenesis by stalling the translation of CYP17A1 mRNA.Nature communications · 2025Article
- Harnessing ZIKV NS2A RNA for alleviating acute hepatitis and cytokine release storm by targeting translation machinery.Hepatology (Baltimore, Md.) · 2025Article
- Functional Roles and Host Interactions ofPathogens (Basel, Switzerland) · 2025Review
- Article
- The Critical Role of YAP/BMP/ID1 Axis on Simulated Microgravity-Induced Neural Tube Defects in Human Brain Organoids.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025Article
- West Nile virus unmasked: from gene variability to future challenges.Frontiers in cellular and infection microbiology · 2025Review
- Article
- An Overview of Zika Virus and Zika Virus Induced Neuropathies.International journal of molecular sciences · 2024Review
73 more citing papers are in PubMed but not listed here.
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Authors and funding
33 authors at 10 institutions in 2 countries.
Ki-Jun YoonInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Guang SongDepartment of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Xuyu QianInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Bioengineering Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Jianbo PanDepartment of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Dan XuInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China; College of Biological Science and Engineering, Institute of Life Sciences, Fuzhou University, Fuzhou 350116, China.
Hee-Sool RhoDepartment of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Nam-Shik KimInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Christa HabelaDepartment of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Lily ZhengThe Human Genetic Pre-doctoral Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Fadi JacobInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Feiran ZhangDepartment of Human Genetics, Emory University School of Medicine, Atlanta, GA 30322, USA.
Emily M LeeDepartment of Biological Science, Florida State University, Tallahassee, FL 32306, USA.
Wei-Kai HuangInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Graduate Program in Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Francisca Rojas RingelingInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Human Genetic Pre-doctoral Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Caroline VissersInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Biochemistry, Cellular and Molecular Biology Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Cui LiInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Ling YuanInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Koeun KangInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Sunghan KimInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Junghoon YeoInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Yichen ChengDepartment of Biological Science, Florida State University, Tallahassee, FL 32306, USA.
Sheng LiuDepartment of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Zhexing WenDepartment of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA 30322, USA; Department of Cell Biology, Emory University School of Medicine, Atlanta, GA 30322, USA.
Cheng-Feng QinDepartment of Virology, State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China.
Qingfeng WuInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Kimberly M ChristianDepartment of Neuroscience, Mahoney Institute for Neurosciences, Perelman School for Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Hengli TangDepartment of Biological Science, Florida State University, Tallahassee, FL 32306, USA.
Peng JinDepartment of Human Genetics, Emory University School of Medicine, Atlanta, GA 30322, USA.
Zhiheng XuInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Jiang QianDepartment of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Heng ZhuDepartment of Pharmacology and Molecular Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Hongjun SongInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Bioengineering Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Human Genetic Pre-doctoral Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Graduate Program in Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Biochemistry, Cellular and Molecular Biology Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neuroscience, Mahoney Institute for Neurosciences, Perelman School for Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Regenerative Medicine, Perelman School for Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; The Epigenetics Institute, Perelman School for Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Guo-Li MingInstitute for Cell Engineering, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Bioengineering Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Graduate Program in Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; The Biochemistry, Cellular and Molecular Biology Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Department of Neuroscience, Mahoney Institute for Neurosciences, Perelman School for Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Regenerative Medicine, Perelman School for Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: gming@mail.med.upenn.edu.
Johns Hopkins University · USJohns Hopkins Medicine · USEmory University · USFlorida State University · USChinese Academy of Sciences · CNInstitute of Genetics and Developmental Biology · CNCalifornia Institute for Regenerative Medicine · USFuzhou University · CNUniversity of Pennsylvania · USWuhan Institute of Virology · CN
Funding
MEDICAL SCIENTIST TRAINING PROGRAMT32GM007309 · NIGMS · JOHNS HOPKINS UNIVERSITY · PI COX, ANDREA L · 1985 to 2019
$43.2MChild Neurologist Career Development Program (CNCDP)K12NS098482 · NINDS · HUGO W. MOSER RES INST KENNEDY KRIEGER · PI SCHLAGGAR, BRADLEY L · 2016 to 2025
$26.2MBIOCHEMISTRY, CELLULAR AND MOLECULAR BIOLOGY PROGRAMT32GM007445 · NIGMS · JOHNS HOPKINS UNIVERSITY · PI GREEN, RACHEL · 1985 to 2021
$24.1MRole of CACNA1C - a shared risk gene in neuropsychiatric disordersU19MH106434 · NIMH · UNIVERSITY OF PENNSYLVANIA · PI GAGE, FRED H · 2016 to 2020
$13.8MPredoctoral Training Program in Human GeneticsT32GM007814 · NIGMS · JOHNS HOPKINS UNIVERSITY · PI VALLE, DAVID · 1985 to 2021
$10.6MMolecular Basis of rCGG-Mediated NeurodegenerationR01NS051630 · NINDS · EMORY UNIVERSITY · PI NELSON, DAVID LOREN · 2006 to 2023
$9.8MModeling Zika virus pathogenesis and potential intervention during neural development using a human brain organoid systemU19AI131130 · NIAID · UNIVERSITY OF PENNSYLVANIA · PI WEN, ZHEXING · 2017 to 2021
$7.7MFunctional roles of genetic risk factors for brain disorders in neurogenesis and neurodevelopmentR35NS097370 · NINDS · UNIVERSITY OF PENNSYLVANIA · PI MING, GUO-LI · 2017 to 2024
$6.7MTranslational models of neurodevelopmental epigenetics and disease using human iPSCsP01NS097206 · NINDS · UNIVERSITY OF PENNSYLVANIA · PI SONG, HONGJUN · 2016 to 2020
$4.3MResearch Education Program for Residents and Fellows in Neurology - PorrasR25NS065729 · NINDS · JOHNS HOPKINS UNIVERSITY · PI HILLIS, ARGYE E. · 2009 to 2024
$3.3MCalcium signaling in neuronal navigationR01NS048271 · NINDS · JOHNS HOPKINS UNIVERSITY · PI MING, GUO-LI · 2004 to 2014
$3.2MLocal circuitry mechanisms regulating adult hippocampal neurogenesisR37NS047344 · NINDS · UNIVERSITY OF PENNSYLVANIA · PI SONG, HONGJUN · 2013 to 2019
$2.9MNIAID NIH HHS R21 AI119530NIAID NIH HHS U19 AI131130NIEHS NIH HHS R21 ES021957NIGMS NIH HHS R01 GM111514NIGMS NIH HHS T32 GM007309NIGMS NIH HHS T32 GM007445NIGMS NIH HHS T32 GM007814NIMH NIH HHS R01 MH105128NIMH NIH HHS R21 MH087874NIMH NIH HHS R33 MH087874NIMH NIH HHS U19 MH106434NINDS NIH HHS K12 NS098482NINDS NIH HHS P01 NS097206NINDS NIH HHS R01 NS048271NINDS NIH HHS R01 NS051630NINDS NIH HHS R21 NS095348NINDS NIH HHS R25 NS065729NINDS NIH HHS R35 NS097370NINDS NIH HHS R37 NS047344NINDS NIH HHS R56 NS047344
Abstract
Zika virus (ZIKV) directly infects neural progenitors and impairs their proliferation. How ZIKV interacts with the host molecular machinery to impact neurogenesis in vivo is not well understood. Here, by systematically introducing individual proteins encoded by ZIKV into the embryonic mouse cortex, we show that expression of ZIKV-NS2A, but not Dengue virus (DENV)-NS2A, leads to reduced proliferation and premature differentiation of radial glial cells and aberrant positioning of newborn neurons. Mechanistically, in vitro mapping of protein-interactomes and biochemical analysis suggest interactions between ZIKA-NS2A and multiple adherens junction complex (AJ) components. Functionally, ZIKV-NS2A, but not DENV-NS2A, destabilizes the AJ complex, resulting in impaired AJ formation and aberrant radial glial fiber scaffolding in the embryonic mouse cortex. Similarly, ZIKA-NS2A, but not DENV-NS2A, reduces radial glial cell proliferation and causes AJ deficits in human forebrain organoids. Together, our results reveal pathogenic mechanisms underlying ZIKV infection in the developing mammalian brain.
Indexed as
NeurogenesisProteolysisAdherens JunctionsAnimalsCell DifferentiationCell ProliferationCerebral CortexHEK293 CellsHumansMammalsMembrane ProteinsMiceNeurogliaProtein BindingProtein Interaction MappingViral Nonstructural ProteinsMembrane ProteinsViral Nonstructural Proteinsadherens junctioncortical neurogenesisflavivirushuman organoidhuman protein microarraymicrocephalyneural stem cellneuronal migrationradial glial cellZika virus
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