Probing Molecular Insights into Zika Virus–Host Interactions
Abstract
:1. Introduction
1.1. The Zika Virus (ZIKV): An Emerging Public Health Threat
1.2. The Organization of Zika Virus
1.3. The Infectious Cycle of ZIKV and Human Transmission
1.4. A Brief History of ZIKV
1.5. What Has Been Learned from the Recent ZIKV Break?
2. Cellular Targets and Viral Entry
2.1. Cellular Targets
2.2. The Cellular Receptors for ZIKV Entry
3. Cellular and Immune Responses to ZIKV Infection
4. Viral Counteraction to Host Antiviral Responses and ZIKV-Induced Cytopathic Effects
4.1. Viral Counteraction to Host Antiviral Responses
4.2. ZIKV-Induced Cytopathic Effects
4.3. The Structural Proteins
4.4. The Non-Structural Proteins
5. Concluding Remarks
Acknowledgments
Conflicts of Interest
Abbreviations
ADE | Antibody-dependent enhancement |
CPE | Cytotoxic effect |
CNS | Central nerve system |
DC | Dendritic cell |
DENV | Dengue virus |
dsRNA | Double stranded RNA |
ER | Endoplasmic reticulum |
HAVcr-1 | Hepatitis A virus cellular receptor 1 |
hEC | Human epithelial cell |
hNPC | Human neural progenitor cell |
hBMEC | Human brain microvascular endothelial cell |
GBS | Guillain–Barré syndrome |
IFN | Interferon |
iPSC | Induced pluripotent stem cell |
IRF3 | Interferon regulatory factor 3 |
ISGS | Interferon stimulated genes |
JEV | Japanese Encephalitis Virus |
NPCs | Neural progenitor stem cells |
PAMP | Pathogen-associated molecular pattern |
PR | Protease |
PRRs | Pattern recognition receptors |
RdRP | RNA-dependent RNA polymerase |
RLRs | RIG-I like receptors |
sfRNA | Subgenomic flavivirus RNA |
TGN | Trans-Golgi network |
TLR3 | Toll-like receptor 3 |
TOR | Target of rapamycin |
WHO | World health organization |
WNV | West Nile Virus |
ZIKV | Zika virus |
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ZIKV Strain | Model Used | Host/Location/Year | Microcephaly-Like Phenotypes | Reference |
---|---|---|---|---|
Human fetal tissue or organoid models | ||||
MR766 | Human brain-specific organoids | Rhesus monkey/Uganda/1947 | Increased cell death and reduced proliferation, resulting in decreased neuronal cell-layer volume resembling microcephaly. | [40] |
MR766 | Human neurospheres and organoids | Rhesus monkey/Uganda/1947 | Growth impairment of neurospheres and organoids | [43] |
MR766 | Human cerebral organoids | Rhesus monkey/Uganda/1947 | Reduction of organoid growth and volume reminiscent of microcephaly via induction of TLR3 | [57] |
FSS 13025 | Human brain-specific organoids | Human/Cambodia/2010 | Increased cell death and reduced proliferation, resulting in decreased neuronal cell-layer volume resembling microcephaly. | [40] |
ZIKV(BR) | Human organoids | Human/Brazil/2015 | Reduction of proliferative zones and disrupted cortical layers; induction of apoptosis, autophagy and impaired neurodevelopment | [59] |
KU527068 | Aborted human fetal brain | Human/Brazil/2016 | Microcephaly with calcification in the fetal brain and placenta | [32] |
FB_GWUH | Aborted human fetal brain | Human/USA/2016 | Fetal brain abnormalities with diffuse cerebral cortical thinning | [39] |
Mouse models | ||||
PF/2013/KD507 | Mouse | Human/French Polynesia/2013 | Fetal demise or intrauterine growth restriction | [33] |
ZIKV(BR) | Mouse | Human/Brazil/2015 | Intrauterine growth restriction, including signs of microcephaly and vertical transmission | [59] |
SZ01 | Mouse vertical transmission | Human/Samoa/2016 | Infection of radial glia cells of dorsal ventricular zone of the fetuses resulting in reduced cavity of lateral ventricles and decreased cortical surface area | [40] |
SZ01 | Embryonic mouse brain | Human/Samoa/2016 | Cell cycle arrest, apoptosis, and inhibition of NPC differentiation, resulting in cortical thinning and microcephaly | [61] |
CAM/2010AndVEN/2016 | Neonatal mouse brain | Human/Cambodia/2010 Human/Venezuela/2016 | Neonatal ZIKV infection of VEN/2016 leads to more severe microcephaly than CAM/2010. VEN/2016 strain infection leads to stronger immune response, more severe calcification, more neuronal death and abolished oligodendrocyte development, but less activation of microglial cells. | [62] |
Primary Cell | Receptor | References | |
---|---|---|---|
Brain | |||
Neural progenitor cells (NPCs) | AXL, TLR3 | [80,84,85] | |
Astroglial cells | AXL | [36,81,86,87,88] | |
Microglial cells | AXL | [81] | |
Placenta | |||
Hofbauer cells | AXL, Tyro3, TIM1 | [67,68,83] | |
Trophoblasts | AXL, Tyro3, TIM1, TLR3, TLR8 | [67,68,83] | |
Endothelial cells | AXL, Tyro3, TIM1 | [33,83] | |
Skin | |||
Dermal fibroblasts | AXL, TIM-1, TYRO3, TLR3, RIG-I, MDA5 | [64,89] | |
Epidermal keratinocytes | AXL, TIM-1, TYRO3, TLR3, RIG-I, MDA5 | [64] | |
Immune cells | |||
Immature dendritic cells | DC-SIGN | [64,65] | |
Dendritic cells | DC-SIGN | [66] | |
CD14+ monocytes | Unknown | [90,91,92] | |
CD14+CD16+ monocytes | Unknown | [91] | |
Testis | |||
Sertoli cell | AXL | [28,93,94] | |
Spermatozoa | Tyro3 | [95,96] | |
Kidney | |||
Renal mesangial cell | Unknown | [97] | |
Glomerular podocytes | Unknown | ||
Renal Glomerular Endothelial Cell | Unknown | ||
Retina | |||
Retinal pericytes | Tyro3, AXL | [1,98] | |
Retinal microvascular endothelial cells | Tyro3, AXL | ||
Permissive human cell lines | |||
Cell line | Origins | Permissiveness | References |
SK-N-SH | Brain/Bone marrow | ** | [99] |
SH-SY5Y | Nerve | ** | [100] |
SF268 | CNS in brain | *** | [42,70] |
HBMEC | Brain | *** | [69,94] |
SNB19 | CNS in brain | *** | [42] |
Huh-7 | Liver | *** | [70] |
HFF-1 | Skin | *** | [64] |
A549 | Lung | *** | [100,101] |
HOBIT | Osteoblast-like Cells | *** | [102] |
Cellular Antiviral Responses to Zika Infection | |||
Cellular Response | Cellular Protein Involved | Molecular Actions and Consequences | References |
Pro-inflammatory CD8+ T-cell immune response | Cytokines: IL-1β, IL-6, MIP1α; chemokines: IP-10, RANTES | T-cell mediated polyfunctional immune responses with releases of antiviral cytokines and chemokines | [65,103,118,119] |
CD14+ monocytes and macrophages immune response | CXCL9, CXCL10, CXCL11, CCL5, IL-15 | CD14+ monocytes prime NK cell activities during ZIKV infection | [92] |
Humoral immune response | IgM, IgG | Production of neutralizing and protective antibodies to ZIKV | [120,121,122] |
Cellular innate immune response: TLR3-mediated response | TLR3, IRF3, TBK1, type I IFNs, and IFNβ | An early response that triggers IRF3 and recognizes ZIKV dsRNA in cytoplasm leading to activation of type I IFNs and IFNβ production | [57,64,65] |
Cellular innate immune response: RIG-1/MDA5-mediated response | RIG-1, MDA5, IRF-3, NFkB, type I IFNs, and IFNβ | Late responses that recognize ZIKV dsRNA and contribute to activation of type I IFNs and IFNβ production | [64,65] |
Type I and type III interferon activation | OAS2, ISG15, MX1 | Production of IFNβ as part of the cellular antiviral responses | [64] |
Viral Counteraction | |||
Viral response | Viral protein involved | Molecular actions and consequences | References |
Counteraction to activation of type 1 IFNs and IFNβ production | NS1, NS2A, NS2B, NS4A, NS4B and NS5 | Targeting RIG-1 pathway | [123,124,125] |
Inhibition of IFNβ production | NS1, NS4A, NS4B, NS5 | NS4A and NS5 inhibit IRF3 and NFkB; NS1 inhibits IRF3 IFNβ production through binding to TBK1 | [49] |
Inhibition of the JAK/STAT pathway | NS5, PR | NS5 binds to STAT2 for its proteasomal degradation; PR inhibits JAK1 kinase | [115,126,127] |
Selective activation of type II IFN signaling | NS5 | NS5 promotes the formation of STAT1/STAT1 homodimers and activates type II IFN for viral replication | [123] |
Induction of cellular autophagy | prM, M, NS1, NS2A, NS4A | In a yeast study, these ZIKV proteins induced cellular autophagy as indicated by formation of cytoplasmic puncta | [9] |
Induction of cellular autophagy | NS4A, NS4B | Inhibit Akt-mediated mTOR pathway through Tor1/TSC1 and Tip41 | [9,111] |
Protein | Primary Function | Main Phenotypes | References |
---|---|---|---|
Structural Proteins | |||
anaC | Anchored capsid protein | In the fission yeast cells, it restricts cellular growth and affects cell cycling. It also induces cellular oxidative stress leading to cell death. | [9] |
C | Capsid protein | In the fission yeast cells, it restricts cellular growth. It also induces cellular oxidative stress leading to cell death; in hNPCs, it induces ribosomal stress and apoptosis. | [9,130] |
prM | Precursor membrane protein | In the fission yeast cells, it restricts cellular growth and affects cell cycling. It also induces cellular oxidative stress and autophagy leading to cell death; a single prM mutation contributes to fetal microcephaly | [9,131] |
M | Membrane protein | In the fission yeast cells, it restricts cellular growth and affects cell cycling. It also induces cellular oxidative stress and autophagy, leading to cell death. | [9] |
Pr | Cleaved product from prM | Unknown | |
E | Envelope protein | A putative cytopathic factor based on a yeast study. E protein facilitates viral entry. A single residue in the αB helix of the E protein is critical for Zika virus thermostability, and interaction with the host cell membrane. | [9,132] |
Non-structural Proteins | |||
NS1 | Viral replication, pathogenesis and immune evasion | In the fission yeast cells, it induces cellular oxidative stress and autophagy leading to cell death; An essential role in viral replication and immune evasion. It presents on the cell surface and presents as a dimer within cells, and as a hexamer once being secreted. NS1-mediated CPEs in mammalian cells have not yet been established. | [47,48,49,133] |
NS2A | Unknown | In the fission yeast cells, it induces cellular oxidative stress and autophagy leading to cell death; ZIKV-encoded NS2A disrupts mammalian cortical neurogenesis by degrading adherens junction (AJ) proteins, leading to reduced proliferation and premature differentiation of radial glial cells and aberrant positioning of newborn neurons. | [131] |
NS2B | Protease cofactor | In fission yeast cells, it restricts cellular growth. Forms a protease complex with NS3; a putative cytopathic factor based on a yeast study | [9,134] |
NS3 | Protease and helicase | NS3-mediated CPEs in mammalian cells have not yet been established. | [131] |
NS4A | Viral RNA synthesis and viral morphogenesis | In the fission yeast cells, it restricts cellular growth and affects cell cycling. It also induces cellular oxidative stress and autophagy leading to cell death. It induces autophagy by inhibiting Atk-mediated TOR pathway through Tor1/TSC1 and Tip41 in both yeast and mammalian cells. | [9,111] |
2K | A signal peptide | Viral RNA synthesis and viral morphogenesis. 2K-mediated CPEs have not yet been established. | [9,11,12] |
NS4B | Viral RNA synthesis and viral morphogenesis | Synergistic to NS4A on inhibiting Akt-mediated TOR pathway | [111] |
NS5 | Methyltrasferase; RNA-dependent polymerase | NS5-mediated CPEs in mammalian cells have not yet been established. | [128] |
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Lee, I.; Bos, S.; Li, G.; Wang, S.; Gadea, G.; Desprès, P.; Zhao, R.Y. Probing Molecular Insights into Zika Virus–Host Interactions. Viruses 2018, 10, 233. https://doi.org/10.3390/v10050233
Lee I, Bos S, Li G, Wang S, Gadea G, Desprès P, Zhao RY. Probing Molecular Insights into Zika Virus–Host Interactions. Viruses. 2018; 10(5):233. https://doi.org/10.3390/v10050233
Chicago/Turabian StyleLee, Ina, Sandra Bos, Ge Li, Shusheng Wang, Gilles Gadea, Philippe Desprès, and Richard Y. Zhao. 2018. "Probing Molecular Insights into Zika Virus–Host Interactions" Viruses 10, no. 5: 233. https://doi.org/10.3390/v10050233