Pre- and peri-implantation Zika virus infection impairs fetal development by targeting trophectoderm cells

Lei Tan, Lauretta A. Lacko, Ting Zhou, Delia Tomoiaga, Romulo Hurtado, Tuo Zhang, Ana Sevilla, Aaron Zhong, Christopher E Mason, Scott Noggle, Todd Evans, Heidi Stuhlmann (), Robert E. Schwartz () and Shuibing Chen ()
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Lei Tan: Weill Cornell Medical College
Lauretta A. Lacko: Weill Cornell Medical College
Ting Zhou: Weill Cornell Medical College
Delia Tomoiaga: Weill Cornell Medical College
Romulo Hurtado: Weill Cornell Medical College
Tuo Zhang: Weill Cornell Medical College
Ana Sevilla: New York Stem Cell Foundation
Aaron Zhong: Sloan Kettering Institute
Christopher E Mason: Weill Cornell Medical College
Scott Noggle: New York Stem Cell Foundation
Todd Evans: Weill Cornell Medical College
Heidi Stuhlmann: Weill Cornell Medical College
Robert E. Schwartz: Weill Cornell Medical College
Shuibing Chen: Weill Cornell Medical College

Nature Communications, 2019, vol. 10, issue 1, 1-12

Abstract: Abstract Zika virus (ZIKV) infection results in an increased risk of spontaneous abortion and poor intrauterine growth although the underlying mechanisms remain undetermined. Little is known about the impact of ZIKV infection during the earliest stages of pregnancy, at pre- and peri-implantation, because most current ZIKV pregnancy studies have focused on post-implantation stages. Here, we demonstrate that trophectoderm cells of pre-implantation human and mouse embryos can be infected with ZIKV, and propagate virus causing neural progenitor cell death. These findings are corroborated by the dose-dependent nature of ZIKV susceptibility of hESC-derived trophectoderm cells. Single blastocyst RNA-seq reveals key transcriptional changes upon ZIKV infection, including nervous system development, prior to commitment to the neural lineage. The pregnancy rate of mice is >50% lower in pre-implantation infection than infection at E4.5, demonstrating that pre-implantation ZIKV infection leads to miscarriage. Cumulatively, these data elucidate a previously unappreciated association of pre- and peri-implantation ZIKV infection and microcephaly.

Date: 2019
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DOI: 10.1038/s41467-019-12063-2

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