Zika Virus Infection during Pregnancy in Mice Causes Placental Damage and Fetal Demise

Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1−/−) c...

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Published in	Cell Vol. 165; no. 5; pp. 1081 - 1091
Main Authors	Miner, Jonathan J., Cao, Bin, Govero, Jennifer, Smith, Amber M., Fernandez, Estefania, Cabrera, Omar H., Garber, Charise, Noll, Michelle, Klein, Robyn S., Noguchi, Kevin K., Mysorekar, Indira U., Diamond, Michael S.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 19.05.2016
Subjects	abortion (animals) animal models Animals antibodies Apoptosis brain Brain - embryology Brain - pathology Brain - virology congenital abnormalities Disease Models, Animal Female females fetal death Fetal Diseases - pathology Fetal Diseases - virology fetus heterozygosity humans interferons Male males Mice Mice, Inbred C57BL pathogenesis placenta Placenta Diseases - pathology Placenta Diseases - virology Pregnancy Pregnancy Complications, Infectious - pathology Pregnancy Complications, Infectious - virology pregnant women Receptor, Interferon alpha-beta - genetics Receptor, Interferon alpha-beta - metabolism RNA, Viral - isolation & purification vaccines Zika virus Zika Virus - physiology Zika Virus Infection - pathology Zika Virus Infection - virology
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Abstract	Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1−/−) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. [Display omitted] •Establishment of an in utero transmission model of ZIKV infection•ZIKV infects placental cells and results in intrauterine growth restriction•ZIKV infection and injury of the fetal brain is observed•ZIKV infection of fetuses can occur by a trans-placental route Zika virus infection of mice early in pregnancy results in infection of the placenta and fetal brain, causing a fetal syndrome that resembles the intrauterine growth restriction and spontaneous abortion observed in ZIKV-infected pregnant women.
AbstractList	Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1−/−) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1(-/-)) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1(-/-)) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations.Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1(-/-)) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling ( Ifnar1 −/− ) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1 super(-/-)) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse models of placental and fetal disease associated with in utero transmission of ZIKV. Female mice lacking type I interferon signaling (Ifnar1−/−) crossed to wild-type (WT) males produced heterozygous fetuses resembling the immune status of human fetuses. Maternal inoculation at embryonic day 6.5 (E6.5) or E7.5 resulted in fetal demise that was associated with ZIKV infection of the placenta and fetal brain. We identified ZIKV within trophoblasts of the maternal and fetal placenta, consistent with a trans-placental infection route. Antibody blockade of Ifnar1 signaling in WT pregnant mice enhanced ZIKV trans-placental infection although it did not result in fetal death. These models will facilitate the study of ZIKV pathogenesis, in utero transmission, and testing of therapies and vaccines to prevent congenital malformations. [Display omitted] •Establishment of an in utero transmission model of ZIKV infection•ZIKV infects placental cells and results in intrauterine growth restriction•ZIKV infection and injury of the fetal brain is observed•ZIKV infection of fetuses can occur by a trans-placental route Zika virus infection of mice early in pregnancy results in infection of the placenta and fetal brain, causing a fetal syndrome that resembles the intrauterine growth restriction and spontaneous abortion observed in ZIKV-infected pregnant women.
Author	Garber, Charise Cao, Bin Fernandez, Estefania Miner, Jonathan J. Noguchi, Kevin K. Diamond, Michael S. Klein, Robyn S. Cabrera, Omar H. Noll, Michelle Mysorekar, Indira U. Govero, Jennifer Smith, Amber M.
AuthorAffiliation	5 Department of Obstetrics and Gynecology, Washington University School of Medicine, Saint Louis, MO 63110 7 The Center for Human Immunology and Immunotherapy Programs, Washington University School of Medicine, Saint Louis, MO 63110 4 Department of Pathology and Immunology, Washington University School of Medicine, Saint Louis, MO 63110 6 Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO 63110 1 Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110 3 Department of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110 2 Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, MO 63110
AuthorAffiliation_xml	– name: 6 Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO 63110 – name: 7 The Center for Human Immunology and Immunotherapy Programs, Washington University School of Medicine, Saint Louis, MO 63110 – name: 2 Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, MO 63110 – name: 3 Department of Molecular Microbiology, Washington University School of Medicine, Saint Louis, MO 63110 – name: 1 Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110 – name: 4 Department of Pathology and Immunology, Washington University School of Medicine, Saint Louis, MO 63110 – name: 5 Department of Obstetrics and Gynecology, Washington University School of Medicine, Saint Louis, MO 63110
Author_xml	– sequence: 1 givenname: Jonathan J. surname: Miner fullname: Miner, Jonathan J. organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 2 givenname: Bin surname: Cao fullname: Cao, Bin organization: Department of Obstetrics and Gynecology, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 3 givenname: Jennifer surname: Govero fullname: Govero, Jennifer organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 4 givenname: Amber M. surname: Smith fullname: Smith, Amber M. organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 5 givenname: Estefania surname: Fernandez fullname: Fernandez, Estefania organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 6 givenname: Omar H. surname: Cabrera fullname: Cabrera, Omar H. organization: Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 7 givenname: Charise surname: Garber fullname: Garber, Charise organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 8 givenname: Michelle surname: Noll fullname: Noll, Michelle organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 9 givenname: Robyn S. surname: Klein fullname: Klein, Robyn S. organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 10 givenname: Kevin K. surname: Noguchi fullname: Noguchi, Kevin K. organization: Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 11 givenname: Indira U. surname: Mysorekar fullname: Mysorekar, Indira U. email: mysorekari@wudosis.wustl.edu organization: Department of Pathology and Immunology, Washington University School of Medicine, Saint Louis, MO 63110, USA – sequence: 12 givenname: Michael S. surname: Diamond fullname: Diamond, Michael S. email: diamond@borcim.wustl.edu organization: Department of Medicine, Washington University School of Medicine, Saint Louis, MO 63110, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/27180225$$D View this record in MEDLINE/PubMed
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Snippet	Zika virus (ZIKV) infection in pregnant women causes intrauterine growth restriction, spontaneous abortion, and microcephaly. Here, we describe two mouse...
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SubjectTerms	abortion (animals) animal models Animals antibodies Apoptosis brain Brain - embryology Brain - pathology Brain - virology congenital abnormalities Disease Models, Animal Female females fetal death Fetal Diseases - pathology Fetal Diseases - virology fetus heterozygosity humans interferons Male males Mice Mice, Inbred C57BL pathogenesis placenta Placenta Diseases - pathology Placenta Diseases - virology Pregnancy Pregnancy Complications, Infectious - pathology Pregnancy Complications, Infectious - virology pregnant women Receptor, Interferon alpha-beta - genetics Receptor, Interferon alpha-beta - metabolism RNA, Viral - isolation & purification vaccines Zika virus Zika Virus - physiology Zika Virus Infection - pathology Zika Virus Infection - virology
Title	Zika Virus Infection during Pregnancy in Mice Causes Placental Damage and Fetal Demise
URI	https://dx.doi.org/10.1016/j.cell.2016.05.008 https://www.ncbi.nlm.nih.gov/pubmed/27180225 https://www.proquest.com/docview/1790462560 https://www.proquest.com/docview/1808643541 https://www.proquest.com/docview/2000229455 https://pubmed.ncbi.nlm.nih.gov/PMC4874881
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