Previous exposure to dengue virus is associated with increased Zika virus burden at the maternal-fetal interface in rhesus macaques

Crooks, Chelsea M.; Weiler, Andrea M.; Rybarczyk, Sierra; Bliss, Mason I.; Jaeger, Anna S.; Murphy, Megan E.; Simmons, Heather A.; Mejía, Andrés; Fritsch, Michael K.; Hayes, Jennifer; Eickhoff, Jens; Mitzey, Ann M.; Razo, Elaina; Braun, Katarina M.; Brown, Elizabeth; Yamamoto, Keisuke; Shepherd, Phoenix M.; Possell, Amber; Weaver, Kara; Antony, Kathleen M.; Morgan, Terry K.; Newman, Christina M.; Dudley, Dawn M.; Schultz-Darken, Nancy; Peterson, Eric J.; Katzelnick, Leah C.; Balmaseda, Ángel; Harris, Eva; O’Connor, David H.; Mohr, Emma L.; Golos, Thaddeus G.; Friedrich, Thomas C.; Aliota, Matthew T.

doi:10.1371/journal.pntd.0009641

Cited by 20 publications

(20 citation statements)

References 72 publications

(95 reference statements)

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“…Conversely, it is possible that in the presence of a weak neutralizing response antibodies can enhance a viral infection as has been demonstrated with multiple viruses [14,15]. Indeed, ADE has been reported for several human viral diseases including RSV, Measles, Dengue fever and Zika [39,40], in addition to diseases caused by other members of the coronavirus family, including FIPV, and SARS--CoV-1 [41,42]. Since the limited options available for prevention and treatment of SARS-2 are primarily antibody-based, questions of whether SARS-2 infection can be enhanced by these antibodies is an important consideration [43][44][45][46].…”

Section: Discussionmentioning

confidence: 99%

Anti-SARS-CoV-2 IgG and IgA antibodies in COVID-19 convalescent plasma do not enhance viral infection

et al. 2022

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The novel coronavirus, SARS-CoV-2 that causes COVID-19 has resulted in the death of nearly 4 million people within the last 18 months. While preventive vaccination, and monoclonal antibody therapies have been rapidly developed and deployed, early in the pandemic the use of COVID-19 convalescent plasma (CCP) was a common means of passive immunization with a theoretical risk of antibody-dependent enhancement (ADE) of viral infection. Though vaccines elicit a strong and protective immune response and transfusion of CCP with high titers of neutralization activity are correlated with better clinical outcomes, the question of whether antibodies in CCP can enhance infection of SARS-CoV-2 has not been directly addressed. In this study, we analyzed for and observed passive transfer of neutralization activity with CCP transfusion. Furthermore, to specifically understand if antibodies against the spike protein (S) enhance infection, we measured the anti-S IgG, IgA, and IgM responses and adapted retroviral-pseudotypes to measure virus neutralization with target cells expressing the ACE2 virus receptor and the Fc alpha receptor (FcαR) or Fc gamma receptor IIA (FcγRIIA). Whereas neutralizing activity of CCP correlated best with higher titers of anti-S IgG antibodies, the neutralizing titer was not affected when Fc receptors were present on target cells. These observations support the absence of antibody-dependent enhancement of infection (ADE) by IgG and IgA isotypes found in CCP. The results presented, therefore, not only supports the therapeutic use of currently available antibody-based treatment, including the continuation of CCP transfusion strategies, but also the use of various vaccine platforms in a prophylactic approach.

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Section: Discussionmentioning

confidence: 99%

Anti-SARS-CoV-2 IgG and IgA antibodies in COVID-19 convalescent plasma do not enhance viral infection

et al. 2022

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“…Thus, this setting could foster severe dengue cases due to antibody-dependent enhancement, occurring when DENV infection follows a first DENV infection by a heterologous serotype or a first ZIKV infection ( Katzelnick et al , 2020 ). The idea that preexisting DENV immunity may have a pathologic role in ZIKV infection, particularly congenital ZIKV infection is notable ( Ausderau et al, 2021 ;Bardina et al, 2017 ;Crooks et al, 2021 ;Zimmerman et al, 2018 ). However, the impact on clinical outcomes in pregnancy is uncertain and likely complex, with one ecological study indicating that prior DENV outbreaks may be followed by increased or decreased risk for microcephaly cases ( Carvalho et al , 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Susceptibility to endemic Aedes‐borne viruses among pregnant women in Risaralda, Colombia

Cardona-Ospina¹,

Trujillo²,

Jiménez-Posada³

et al. 2022

International Journal of Infectious Diseases

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“…Therefore, FcRn-mediated transplacental transcytosis of ZIKV immune complexes might be an additional mechanism contributing to transplacental transmission of ZIKV in the second and third trimester of pregnancy, while in the first trimester, ZIKV can infect multiple proliferating placental cells [ 53 ]. The reason why increased fetal pathology has not been observed in DENV immune pregnant NHP that got infected with ZIKV could be that these NHP were infected in the first trimester of pregnancy when maternal IgG is not yet transported efficiently across the placenta [ 11 , 12 , 54 ].…”

Section: Discussionmentioning

confidence: 99%

Transplacental Zika virus transmission in ex vivo perfused human placentas

et al. 2022

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A Zika virus (ZIKV) infection during pregnancy can result in severe birth defects such as microcephaly. To date, it is incompletely understood how ZIKV can cross the human placenta. Furthermore, results from studies in pregnant mice and non-human primates are conflicting regarding the role of cross-reactive dengue virus (DENV) antibodies on transplacental ZIKV transmission. Elucidating how ZIKV can cross the placenta and which risk factors contribute to this is important for risk assessment and for potential intervention strategies for transplacental ZIKV transmission. In this study we use an ex vivo human placental perfusion model to study transplacental ZIKV transmission and the effect that cross-reactive DENV antibodies have on this transmission. By using this model, we demonstrate that DENV antibodies significantly increase ZIKV uptake in perfused human placentas and that this increased uptake is neonatal Fc-receptor-dependent. Furthermore, we show that cross-reactive DENV antibodies enhance ZIKV infection in term human placental explants and in primary fetal macrophages but not in primary trophoblasts. Our data supports the hypothesis that presence of cross-reactive DENV antibodies could be an important risk factor for transplacental ZIKV transmission. Furthermore, we demonstrate that the ex vivo placental perfusion model is a relevant and animal friendly model to study transplacental pathogen transmission.

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Previous exposure to dengue virus is associated with increased Zika virus burden at the maternal-fetal interface in rhesus macaques

Cited by 20 publications

References 72 publications

Anti-SARS-CoV-2 IgG and IgA antibodies in COVID-19 convalescent plasma do not enhance viral infection

Anti-SARS-CoV-2 IgG and IgA antibodies in COVID-19 convalescent plasma do not enhance viral infection

Susceptibility to endemic Aedes‐borne viruses among pregnant women in Risaralda, Colombia

Transplacental Zika virus transmission in ex vivo perfused human placentas

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