Zika virus infection induces RNAi-mediated antiviral immunity in human neural progenitors and brain organoids

The re-emergence of Zika virus (ZIKV) in the Western Hemisphere has resulted in global public health crisis since 2015. ZIKV preferentially infects and targets human neural progenitor cells (hNPCs) and causes fetal microcephaly upon maternal infection. hNPCs not only play critical roles during fetal...

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Published inCell research Vol. 29; no. 4; pp. 265 - 273
Main Authors Xu, Yan-Peng, Qiu, Yang, Zhang, Boya, Chen, Guilai, Chen, Qi, Wang, Miao, Mo, Fan, Xu, Jiuyue, Wu, Jin, Zhang, Rong-Rong, Cheng, Meng-Li, Zhang, Na-Na, Lyu, Bao, Zhu, Wen-Liang, Wu, Meng-Hua, Ye, Qing, Zhang, Da, Man, Jiang-Hong, Li, Xiao-Feng, Cui, Jie, Xu, Zhiheng, Hu, Baoyang, Zhou, Xi, Qin, Cheng-Feng
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.04.2019
Nature Publishing Group
Subjects
45/100
45/91
631/1647
631/250/262
631/532/2182
82/51
Ablation
Animals
Antibiotics
Antiviral drugs
Biomedical and Life Sciences
Brain
Brain - immunology
Brain - pathology
Cell Biology
Cell Line
Cells (biology)
Enoxacin
Enoxacin - pharmacology
Fetuses
Humans
Immunity
Immunity, Innate
Infections
Life Sciences
Microcephaly
Neural stem cells
Neural Stem Cells - immunology
Neural Stem Cells - pathology
Organoids
Organoids - immunology
Organoids - pathology
Phenotypes
Progenitor cells
Public health
RNA Interference
RNA, Viral - immunology
RNA-mediated interference
Somatic cells
Vector-borne diseases
Viral infections
Virus Replication
Viruses
Western Hemisphere
Zika virus
Zika Virus - genetics
Zika Virus - immunology
Zika Virus - physiology
Zika Virus Infection - immunology
Online AccessGet full text

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Abstract The re-emergence of Zika virus (ZIKV) in the Western Hemisphere has resulted in global public health crisis since 2015. ZIKV preferentially infects and targets human neural progenitor cells (hNPCs) and causes fetal microcephaly upon maternal infection. hNPCs not only play critical roles during fetal brain development, but also persist in adult brain throughout life. Yet the mechanism of innate antiviral immunity in hNPCs remains largely unknown. Here, we show that ZIKV infection triggers the abundant production of virus-derived small interfering RNAs in hNPCs, but not in the more differentiated progenies or somatic cells. Ablation of key RNAi machinery components significantly enhances ZIKV replication in hNPCs. Furthermore, enoxacin, a broad-spectrum antibiotic that is known as an RNAi enhancer, exerts potent anti-ZIKV activity in hNPCs and other RNAi-competent cells. Strikingly, enoxacin treatment completely prevents ZIKV infection and circumvents ZIKV-induced microcephalic phenotypes in brain organoid models that recapitulate human fetal brain development. Our findings highlight the physiological importance of RNAi-mediated antiviral immunity during the early stage of human brain development, uncovering a novel strategy to combat human congenital viral infections through enhancing RNAi.
AbstractList The re-emergence of Zika virus (ZIKV) in the Western Hemisphere has resulted in global public health crisis since 2015. ZIKV preferentially infects and targets human neural progenitor cells (hNPCs) and causes fetal microcephaly upon maternal infection. hNPCs not only play critical roles during fetal brain development, but also persist in adult brain throughout life. Yet the mechanism of innate antiviral immunity in hNPCs remains largely unknown. Here, we show that ZIKV infection triggers the abundant production of virus-derived small interfering RNAs in hNPCs, but not in the more differentiated progenies or somatic cells. Ablation of key RNAi machinery components significantly enhances ZIKV replication in hNPCs. Furthermore, enoxacin, a broad-spectrum antibiotic that is known as an RNAi enhancer, exerts potent anti-ZIKV activity in hNPCs and other RNAi-competent cells. Strikingly, enoxacin treatment completely prevents ZIKV infection and circumvents ZIKV-induced microcephalic phenotypes in brain organoid models that recapitulate human fetal brain development. Our findings highlight the physiological importance of RNAi-mediated antiviral immunity during the early stage of human brain development, uncovering a novel strategy to combat human congenital viral infections through enhancing RNAi.
The re-emergence of Zika virus (ZIKV) in the Western Hemisphere has resulted in global public health crisis since 2015. ZIKV preferentially infects and targets human neural progenitor cells (hNPCs) and causes fetal microcephaly upon maternal infection. hNPCs not only play critical roles during fetal brain development, but also persist in adult brain throughout life. Yet the mechanism of innate antiviral immunity in hNPCs remains largely unknown. Here, we show that ZIKV infection triggers the abundant production of virus-derived small interfering RNAs in hNPCs, but not in the more differentiated progenies or somatic cells. Ablation of key RNAi machinery components significantly enhances ZIKV replication in hNPCs. Furthermore, enoxacin, a broad-spectrum antibiotic that is known as an RNAi enhancer, exerts potent anti-ZIKV activity in hNPCs and other RNAi-competent cells. Strikingly, enoxacin treatment completely prevents ZIKV infection and circumvents ZIKV-induced microcephalic phenotypes in brain organoid models that recapitulate human fetal brain development. Our findings highlight the physiological importance of RNAi-mediated antiviral immunity during the early stage of human brain development, uncovering a novel strategy to combat human congenital viral infections through enhancing RNAi.The re-emergence of Zika virus (ZIKV) in the Western Hemisphere has resulted in global public health crisis since 2015. ZIKV preferentially infects and targets human neural progenitor cells (hNPCs) and causes fetal microcephaly upon maternal infection. hNPCs not only play critical roles during fetal brain development, but also persist in adult brain throughout life. Yet the mechanism of innate antiviral immunity in hNPCs remains largely unknown. Here, we show that ZIKV infection triggers the abundant production of virus-derived small interfering RNAs in hNPCs, but not in the more differentiated progenies or somatic cells. Ablation of key RNAi machinery components significantly enhances ZIKV replication in hNPCs. Furthermore, enoxacin, a broad-spectrum antibiotic that is known as an RNAi enhancer, exerts potent anti-ZIKV activity in hNPCs and other RNAi-competent cells. Strikingly, enoxacin treatment completely prevents ZIKV infection and circumvents ZIKV-induced microcephalic phenotypes in brain organoid models that recapitulate human fetal brain development. Our findings highlight the physiological importance of RNAi-mediated antiviral immunity during the early stage of human brain development, uncovering a novel strategy to combat human congenital viral infections through enhancing RNAi.
Author Cheng, Meng-Li
Wang, Miao
Xu, Jiuyue
Zhu, Wen-Liang
Zhang, Da
Chen, Qi
Cui, Jie
Ye, Qing
Qin, Cheng-Feng
Qiu, Yang
Zhang, Boya
Hu, Baoyang
Wu, Meng-Hua
Chen, Guilai
Li, Xiao-Feng
Xu, Yan-Peng
Mo, Fan
Xu, Zhiheng
Zhou, Xi
Lyu, Bao
Zhang, Rong-Rong
Zhang, Na-Na
Wu, Jin
Man, Jiang-Hong
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30814679$$D View this record in MEDLINE/PubMed
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Copyright IBCB, SIBS, CAS 2019
2019© IBCB, SIBS, CAS 2019
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Snippet The re-emergence of Zika virus (ZIKV) in the Western Hemisphere has resulted in global public health crisis since 2015. ZIKV preferentially infects and targets...
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springer
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SubjectTerms 45/100
45/91
631/1647
631/250/262
631/532/2182
82/51
Ablation
Animals
Antibiotics
Antiviral drugs
Biomedical and Life Sciences
Brain
Brain - immunology
Brain - pathology
Cell Biology
Cell Line
Cells (biology)
Enoxacin
Enoxacin - pharmacology
Fetuses
Humans
Immunity
Immunity, Innate
Infections
Life Sciences
Microcephaly
Neural stem cells
Neural Stem Cells - immunology
Neural Stem Cells - pathology
Organoids
Organoids - immunology
Organoids - pathology
Phenotypes
Progenitor cells
Public health
RNA Interference
RNA, Viral - immunology
RNA-mediated interference
Somatic cells
Vector-borne diseases
Viral infections
Virus Replication
Viruses
Western Hemisphere
Zika virus
Zika Virus - genetics
Zika Virus - immunology
Zika Virus - physiology
Zika Virus Infection - immunology
Title Zika virus infection induces RNAi-mediated antiviral immunity in human neural progenitors and brain organoids
URI https://link.springer.com/article/10.1038/s41422-019-0152-9
https://www.ncbi.nlm.nih.gov/pubmed/30814679
https://www.proquest.com/docview/2201693789
https://www.proquest.com/docview/2187034691
https://pubmed.ncbi.nlm.nih.gov/PMC6461993
Volume 29
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