Animal Models of Zika Virus Infection during Pregnancy
Abstract
:1. Introduction
2. Mouse Models
2.1. Type I Interferon Receptor Deficient Mouse Models
2.2. Immunocompetent Mouse Models
2.3. Effects of Type I IFN Signaling on Fetal Resorption
2.4. Gestational Stage Effects
2.5. Summary
3. Development of ZIKV Countermeasures in Pregnant Mice
3.1. Vaccines
3.2. Antibody Treatment
4. Non-human Primate (NHP) Models
4.1. Maternal Syndrome in NHPs
4.2. Fetal Infection and CZS in NHPs
4.3. Countermeasure Studies in NHPs
5. Other Models
6. Conclusions
Funding
Conflicts of Interest
References
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Dam | Sire | ZIKV Strain(s) | Route of Infection(s) | Phenotypes | References |
---|---|---|---|---|---|
C57BL/6 + anti-Ifnar1 Ab | C57BL/6 | H/PF/2013 (Genbank: KJ776791.2) | SC | IUGR | [19,24] |
C57BL/6 + anti-Ifnar1 Ab | C57BL/6 | Mouse-adapted Dakar 41525 (Genbank: MG758786) | SC or IVAG | Placental injury, viral RNA in placenta/fetal heads | [25,26,27] |
Ifnar1−/− | C57BL/6 | H/PF/2013 (Genbank: KJ776791.2) | SC | Fetal resorption, IUGR, pallor, placental injury | [19] |
Ifnar1−/− | C57BL/6 | FSS13025 (Genbank: KU955593) | IVAG | Fetal resorption, IUGR | [23] |
C57BL/6 | C57BL/6 | FSS13025 (Genbank: KU955593) | IVAG | IUGR | [23] |
C57BL/6 | C57BL/6 | SZ01 (Genbank: KU866423) | IP/Intra-ventricular | Brain malformations | [28] |
C57BL/6 | C57BL/6 | MEX1-44 or MR-766 (Genbank: DQ859059) | Lateral ventricle of fetal brain | Reduced cortical neural progenitor cells, brain malformations, microcephaly | [29,30] |
C57BL/6 | C57BL/6 | Brazilian clinical isolate | IV | No clinical signs in pups, no virus detected | [31] |
SJL | SJL | Brazilian clinical isolate | IV | IUGR, brain malformations, ocular abnormalities | [31] |
ICR | ICR | SZ01 (Genbank: KU866423) | Lateral ventricle of fetal brain | Reduced brain size, brain malformations | [32,33] |
Irf3−/−Irf7−/− | Irf3−/−Irf7−/− | FSS13025 (Genbank: KU955593) | IVAG | IUGR | [23] |
AG129 | AG129 | Malaysia P6-740 (Genbank: KX377336) | SC | Viral RNA in placenta and fetal heads, reduced weight and head length | [34] |
C57BL/6 | C57BL/6 | PRVABC59 (Genbank: KU501215) | IV | Fetal resorption, little to no viral RNA in placenta and fetal heads | [35] |
CD1 | CD1 | FSS13025 (Genbank: KU955593), Brazil Paraíba 2015 (Genbank: KX280026), PRVABC59 (Genbank: KU501215), 1968 Nigeria (Genbank: HQ234500) | IU | Viral RNA in uterine horn, placenta, fetal head, increase in number of aborted fetuses | [36] |
CD1 | CD1 | 1968 Nigeria (Genbank: HQ234500) | IP | No viral RNA in placenta or fetal heads | [36] |
hSTAT2 KI | hSTAT2 KI or C57BL/6 | Mouse-adapted Dakar 41525 (Genbank: MG758786) and Parent Dakar 41525 (Genbank: MG758785) | SC | Viral RNA in placenta and fetal heads | [37] |
SJL | SJL | PA 259459 | IV | Viral RNA in fetal heads, Sofosbuvir protected fetuses | [38] |
C57BL/6 or FVB/NJ | C57BL/6 or FVB/NJ | HS-2015-BA-01 (Bahia, Brazil) (Genbank: KX520666) | IV (External jugular) | Fetal and maternal viral RNA; fetal pathology including pericardial edema and abnormal fore and hind limbs | [39] |
Rag1−/− + anti-Ifnar1 Ab | Rag1−/− (+/− anti-Ifnar1 Ab | Brazil Paraíba 2015 (Genbank: KX280026) | IP | Vertical transmission, viral RNA in fetus, placenta, maternal tissues | [40] |
Ifnar1−/− | Rag1−/− (+/− anti-Ifnar1 Ab | Brazil Paraíba 2015 (Genbank: KX280026) | IP | Sexual transmission (male-to-female), viral RNA in placenta and uterus | [40] |
AG129 | AG129 | PRVABC59 (Genbank: KU501215) | SC, IVAG, Sexual | Infectious ZIKV in maternal brain, uterus, ovary, and fetus through all route of infection | [41] |
C57BL/6 | C57BL/6 | SMGC-1 (Genbank: KX266255) | IU (via laparotomy) | Ocular pathology, microcephaly, neuronal loss, hind limb paralysis, spontaneous abortions | [42] |
Swiss-Webster + anti-Ifnar1 Ab | Swiss-Webster | HN16 (Genbank: KY328289) | SC | Growth restriction in pups, decreased brain weight, viral RNA in brain and spinal cord of fetuses | [43] |
ICR | ICR | GZ01 (Genbank: KU820898), FSS13025 (Genbank: KU955593) | Fetus and pup intra-ventricular | ZIKV induced microcephaly, loss of neurons, neutralizing antibody protected pups from microcephaly | [44,45] |
Ifnar1−/− | C57BL/6 | Brazil Paraíba 2015 (Genbank: KX280026) | SC | Fetal resorption, viral RNA in fetus and placenta, microcephaly | [46] |
C57BL/6 + anti-Ifnar1 Ab | C57BL/6 | 2015 Paraíba (Genbank: KX280026) | SC | Viral RNA in placenta (decidua and junctional zone) and fetal heads, maternal brain, spleen | [46] |
Ifnlr1−/− + anti-Ifnar1 Ab | C57BL/6 or Ifnlr1−/− | 2015 Paraíba (Genbank: KX280026) | SC | Viral RNA in placenta (decidua and junctional zone) and fetal heads, maternal brain, spleen | [46] |
C57BL/6 | C57BL/6 | SZ01 (Genbank: KU866423) | IA | Decrease in brain volume and cortical thickness of fetuses, paralysis and motor function deficits in pups | [47] |
C57BL/6 | C57BL/6 | ZIKA-SMGC-1 (Genbank KX266255) | IU | Pups developed microcephaly, ocular defects, paralysis | [42] |
C57BL/6 (H-2b) + anti-Ifnar1 Ab | Balb/c (H-2d) | PRVABC59 (Genbank: KU501215) and MR766 (Genbank: DQ859059) | SC | Viral RNA in fetal tissue and maternal serum, spleen, liver, and brain | [48] |
Balb/c + anti-Ifnar1 Ab | Balb/c | GZ01 (Genbank: KU820898) and FSS13025 (Genbank: KU955593) | SC | Viral RNA in fetal head and placenta, hemorrhagic uterus | [49] |
Ifnar1−/−Ifngr1−/− (AG6) | Ifnar1−/−Ifngr1−/− (AG6) | SZ-WIV01 (KU963796) | IP | In utero death | [50] |
Ifnar1−/− | C57BL/6 | Brazil Paraiba 2015 (Genbank: KX280026) | SC | Fetal resorption | [25,26] |
Ifnar1−/− | C57BL/6 | FSS13025 (Genbank: KU955593) | SC or IV | Fetal resorption, decreased fetal size | [51] |
C57BL/6 + anti-Ifnar1 Ab | C57BL/6 | FSS13025 (Genbank: KU955593) | IV | Viral RNA in fetal tissue, placenta, maternal serum, brain, and spleen | [51] |
Atg161HM + anti-Ifnar1 Ab | Atg161HM | Brazil Paraiba 2015 (Genbank: KX280026) | SC | Reduction in viral RNA in placenta and fetus compared to WT controls | [52] |
Cyp 19 Cre+ Atg16L1fl/fl + anti-Ifnar1 Ab | Cyp 19 Cre+ Atg16L1fl/fl | Brazil Paraiba 2015 (Genbank: KX280026) | SC | Restricted ZIKV infection in placenta compared to controls | [52] |
A129 | A129 | PRVABC59 (Genbank: KU501215) | SC | Viral RNA in placenta, fetal head, maternal brain, reduced fetal weight | [53] |
Model | ZIKV Strain | Route | Dose | Time Infected | Number NHPs Infected | Phenotypes | References |
---|---|---|---|---|---|---|---|
Rhesus macaque | H/PF/2013 (GenBank: KJ776791.2) | SC | 104 PFU | GD: 31 or 38 | 2 | Persistent viremia | [71] |
Rhesus macaque | H/PF/2013 (GenBank: KJ776791.2) | SC | 104 PFU | GD: 31, 38, 104, or 199 | 4 | Persistent viremia, viral RNA in fetus | [72] |
Rhesus macaque | PRVABC59 (Genbank: KU501215.1) | SC | 105 FFU | GD: 31, 51, 114, or 115 | 5 | Viral RNA in fetus, placenta damage, decreased oxygen permeability, villous calcification, stromal proliferation, fibrin deposition, subtle fetal brain abnormalities in 2 of 5 animals (second and third trimester) | [86] |
Rhesus macaque | Brazil ZKV2015 (GenBank: KU497555.1) | SC | 103 PFU | GD: 42–98 | 9 | Persistent viremia, fetal neuropathology, fetal loss, smaller brain size, brain lesions, apoptosis of neuroprogenitor cells, placental pathology | [75] |
Rhesus macaque | PRVABC59 (Genbank: KU501215.1)-Barcoded | SC | 104 PFU | GD: 35 | 1 | Persistent viremia | [76] |
Rhesus macaque | Rio U-1/2016 (Genbank: KU926309) | SC | 104 PFU | GD: 44–124 | 11 | Virus in the amniotic fluid (AF); and in utero fetal deaths | [73] |
Rhesus macaque | Brazil SPH2015 (GenBank: KU321639.1 | IA | 105 PFU | GD: 41, 50, 64, or 90 | 4 | Fetal demise, high viral RNA levels in fetal and placental tissues, including brain; fetuses carried to near term and euthanized displayed no gross microcephaly, but had brain calcifications and reduced neural precursor cells | [84] |
Pigtail macaque | Cambodia FSS13025 (GenBank: KU955593.1) | SC | 5 × 107 PFU | GD: 119 | 1 | Ultrasound lag in growth biparietal diameter, fetal brain lesions, viral RNA in fetal brain, liver, placenta | [70] |
Pigtail macaque | Cambodia FSS13025 (GenBank: KU955593.1) | SC | 5 × 107 PFU | GD: 82 or 119 3 | 2 | Ependymal injury in posterior lateral ventricles, fused ventricular surfaces, periventricular gliosis, white matter GFAP+ gliosis, axonal spheroids, deficient fetal neuronal progenitor cells, loss of non-cortical volume in fetal brain (silent pathology) | [80] |
Pigtail macaque | Brazil Fortaleza 2015 (GenBank: KX811222.1) | SC 1 | 5 × 107 PFU | GD: 60–63 | 3 | Ependymal injury in posterior lateral ventricles, fused ventricular surfaces, periventricular gliosis, white matter GFAP+ gliosis, axonal spheroids, deficient fetal neuronal progenitor cells, loss of non-cortical volume in fetal brain (silent pathology) | [80] |
Marmoset | Brazil SPH2015 (GenBank: KU321639.1) | IM 2 | 2.5 × 105 PFU | GD: 68 or 79 | 2 | Fetal demise, abortion, viral RNA in placenta and fetus | [77] |
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Caine, E.A.; Jagger, B.W.; Diamond, M.S. Animal Models of Zika Virus Infection during Pregnancy. Viruses 2018, 10, 598. https://doi.org/10.3390/v10110598
Caine EA, Jagger BW, Diamond MS. Animal Models of Zika Virus Infection during Pregnancy. Viruses. 2018; 10(11):598. https://doi.org/10.3390/v10110598
Chicago/Turabian StyleCaine, Elizabeth A., Brett W. Jagger, and Michael S. Diamond. 2018. "Animal Models of Zika Virus Infection during Pregnancy" Viruses 10, no. 11: 598. https://doi.org/10.3390/v10110598