Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies

Crisanta Serrano-Collazo; Erick X. Pérez-Guzmán; Petraleigh Pantoja; Mariah A. Hassert; Idia V. Rodríguez; Luis Giavedoniid; Vida Hodara; Laura Parodi; Lorna Cruz; Teresa Arana; Melween I. Martínez; Laura White; James D. Brien; Aravinda de Silva; Amelia K. Pinto; Carlos A. Sariol

doi:10.1371/journal.pntd.0008285

Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies

Crisanta Serrano-Collazo, Erick X. Pérez-Guzmán, Petraleigh Pantoja, Mariah A. Hassert, Idia V. Rodríguez, Luis Giavedoniid, Vida Hodara, Laura Parodi, Lorna Cruz, Teresa Arana, Melween I. Martínez, Laura White, James D. Brien, Aravinda de Silva, Amelia K. Pinto, Carlos A. Sariol

Research output: Contribution to journal › Article › peer-review

18 Scopus citations

Abstract

Little is known about the contribution of virus-specific and cross-reacting antibodies (Abs) or the cellular immune response generated by a primary dengue (DENV) infection on the course of a secondary zika (ZIKV) infection in vivo. Here we show that the length of time between DENV/ZIKV infections has a qualitative impact on controlling early ZIKV replication. Depletion of DENV2-specific Abs in sera confirmed that those type-specific Abs do not contribute to ZIKV control. We show that the magnitude and durability of the neutralizing antibodies (nAbs) induced by a secondary ZIKV infection is modest compared to the response induced after a secondary heterologous DENV infection. Our in vivo results are showing a complex interplay between the cellular and innate immune responses characterized by a high frequency of plasmacytoid dendritic cells (pDC) correlating with an increase in the frequency of DENV antigen specific T cells and a significant control of ZIKV replication which is time dependent. Taken together, our results suggest that early after ZIKV infection other mechanisms such as the innate and cellular immune responses may play a predomi-nant role in controlling ZIKV replication. Regardless of the time elapsed between infections there was no evidence of in vivo antibody-dependent enhancement (ADE) of ZIKV by DENV immunity. These findings have pivotal implications while interpreting ZIKV pathogenesis in flavivirus-experimented populations, diagnostic results interpretation and vaccine designs and schedules among others.

Original language	English
Article number	e0008285
Pages (from-to)	1-28
Number of pages	28
Journal	PLoS Neglected Tropical Diseases
Volume	14
Issue number	5
DOIs	https://doi.org/10.1371/journal.pntd.0008285
State	Published - May 2020

Bibliographical note

Publisher Copyright:
© 2020 Serrano-Collazo et al.

Funding

This work received support by Grants 2 P40 OD012217 and 2U42OD021458-15 to MIM and CAS (ORIP, OD, NIH), and R25GM061838 to C.S.-C. Also, partial support was provided by Grant K22AI104794 to JDB (NIAID) and partially used resources that were supported by the Southwest National Primate Research Center grant P51 OD011133 from the Office of Research Infrastructure Programs, National Institutes of Health to LDG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Funders	Funder number
NIH Office of Research Infrastructure Programs
Southwest National Primate Research Center	P51 OD011133
National Institutes of Health (NIH)	R25GM061838
National Institutes of Health (NIH)
NIH Office of the Director	U42OD021458
NIH Office of the Director
National Institute of Allergy and Infectious Diseases	K22AI104794
National Institute of Allergy and Infectious Diseases

ASJC Scopus subject areas

Public Health, Environmental and Occupational Health
Infectious Diseases

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pntd.0008285

Cite this

Serrano-Collazo, C., Pérez-Guzmán, E. X., Pantoja, P., Hassert, M. A., Rodríguez, I. V., Giavedoniid, L., Hodara, V., Parodi, L., Cruz, L., Arana, T., Martínez, M. I., White, L., Brien, J. D., de Silva, A., Pinto, A. K., & Sariol, C. A. (2020). Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies. PLoS Neglected Tropical Diseases, 14(5), 1-28. Article e0008285. https://doi.org/10.1371/journal.pntd.0008285

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title = "Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies",

abstract = "Little is known about the contribution of virus-specific and cross-reacting antibodies (Abs) or the cellular immune response generated by a primary dengue (DENV) infection on the course of a secondary zika (ZIKV) infection in vivo. Here we show that the length of time between DENV/ZIKV infections has a qualitative impact on controlling early ZIKV replication. Depletion of DENV2-specific Abs in sera confirmed that those type-specific Abs do not contribute to ZIKV control. We show that the magnitude and durability of the neutralizing antibodies (nAbs) induced by a secondary ZIKV infection is modest compared to the response induced after a secondary heterologous DENV infection. Our in vivo results are showing a complex interplay between the cellular and innate immune responses characterized by a high frequency of plasmacytoid dendritic cells (pDC) correlating with an increase in the frequency of DENV antigen specific T cells and a significant control of ZIKV replication which is time dependent. Taken together, our results suggest that early after ZIKV infection other mechanisms such as the innate and cellular immune responses may play a predomi-nant role in controlling ZIKV replication. Regardless of the time elapsed between infections there was no evidence of in vivo antibody-dependent enhancement (ADE) of ZIKV by DENV immunity. These findings have pivotal implications while interpreting ZIKV pathogenesis in flavivirus-experimented populations, diagnostic results interpretation and vaccine designs and schedules among others.",

author = "Crisanta Serrano-Collazo and P{\'e}rez-Guzm{\'a}n, \{Erick X.\} and Petraleigh Pantoja and Hassert, \{Mariah A.\} and Rodr{\'i}guez, \{Idia V.\} and Luis Giavedoniid and Vida Hodara and Laura Parodi and Lorna Cruz and Teresa Arana and Mart{\'i}nez, \{Melween I.\} and Laura White and Brien, \{James D.\} and \{de Silva\}, Aravinda and Pinto, \{Amelia K.\} and Sariol, \{Carlos A.\}",

note = "Publisher Copyright: {\textcopyright} 2020 Serrano-Collazo et al.",

year = "2020",

month = may,

doi = "10.1371/journal.pntd.0008285",

language = "English",

volume = "14",

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Serrano-Collazo, C, Pérez-Guzmán, EX, Pantoja, P, Hassert, MA, Rodríguez, IV, Giavedoniid, L, Hodara, V, Parodi, L, Cruz, L, Arana, T, Martínez, MI, White, L, Brien, JD, de Silva, A, Pinto, AK & Sariol, CA 2020, 'Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies', PLoS Neglected Tropical Diseases, vol. 14, no. 5, e0008285, pp. 1-28. https://doi.org/10.1371/journal.pntd.0008285

Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies. / Serrano-Collazo, Crisanta; Pérez-Guzmán, Erick X.; Pantoja, Petraleigh et al.
In: PLoS Neglected Tropical Diseases, Vol. 14, No. 5, e0008285, 05.2020, p. 1-28.

Research output: Contribution to journal › Article › peer-review

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AU - Serrano-Collazo, Crisanta

AU - Pérez-Guzmán, Erick X.

AU - Pantoja, Petraleigh

AU - Hassert, Mariah A.

AU - Rodríguez, Idia V.

AU - Giavedoniid, Luis

AU - Hodara, Vida

AU - Parodi, Laura

AU - Cruz, Lorna

AU - Arana, Teresa

AU - Martínez, Melween I.

AU - White, Laura

AU - Brien, James D.

AU - de Silva, Aravinda

AU - Pinto, Amelia K.

AU - Sariol, Carlos A.

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N2 - Little is known about the contribution of virus-specific and cross-reacting antibodies (Abs) or the cellular immune response generated by a primary dengue (DENV) infection on the course of a secondary zika (ZIKV) infection in vivo. Here we show that the length of time between DENV/ZIKV infections has a qualitative impact on controlling early ZIKV replication. Depletion of DENV2-specific Abs in sera confirmed that those type-specific Abs do not contribute to ZIKV control. We show that the magnitude and durability of the neutralizing antibodies (nAbs) induced by a secondary ZIKV infection is modest compared to the response induced after a secondary heterologous DENV infection. Our in vivo results are showing a complex interplay between the cellular and innate immune responses characterized by a high frequency of plasmacytoid dendritic cells (pDC) correlating with an increase in the frequency of DENV antigen specific T cells and a significant control of ZIKV replication which is time dependent. Taken together, our results suggest that early after ZIKV infection other mechanisms such as the innate and cellular immune responses may play a predomi-nant role in controlling ZIKV replication. Regardless of the time elapsed between infections there was no evidence of in vivo antibody-dependent enhancement (ADE) of ZIKV by DENV immunity. These findings have pivotal implications while interpreting ZIKV pathogenesis in flavivirus-experimented populations, diagnostic results interpretation and vaccine designs and schedules among others.

AB - Little is known about the contribution of virus-specific and cross-reacting antibodies (Abs) or the cellular immune response generated by a primary dengue (DENV) infection on the course of a secondary zika (ZIKV) infection in vivo. Here we show that the length of time between DENV/ZIKV infections has a qualitative impact on controlling early ZIKV replication. Depletion of DENV2-specific Abs in sera confirmed that those type-specific Abs do not contribute to ZIKV control. We show that the magnitude and durability of the neutralizing antibodies (nAbs) induced by a secondary ZIKV infection is modest compared to the response induced after a secondary heterologous DENV infection. Our in vivo results are showing a complex interplay between the cellular and innate immune responses characterized by a high frequency of plasmacytoid dendritic cells (pDC) correlating with an increase in the frequency of DENV antigen specific T cells and a significant control of ZIKV replication which is time dependent. Taken together, our results suggest that early after ZIKV infection other mechanisms such as the innate and cellular immune responses may play a predomi-nant role in controlling ZIKV replication. Regardless of the time elapsed between infections there was no evidence of in vivo antibody-dependent enhancement (ADE) of ZIKV by DENV immunity. These findings have pivotal implications while interpreting ZIKV pathogenesis in flavivirus-experimented populations, diagnostic results interpretation and vaccine designs and schedules among others.

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Effective control of early zika virus replication by dengue immunity is associated to the length of time between the 2 infections but not mediated by antibodies

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

UN SDGs

Access to Document

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