A Zika virus mutation enhances transmission potential and confers escape from protective dengue virus immunity
Abstract
Zika virus (ZIKV) and dengue virus (DENV) are arthropod-borne pathogenic flaviviruses that co-circulate in many countries. To understand some of the pressures that influence ZIKV evolution, we mimic the natural transmission cycle by repeating serial passaging of ZIKV through cultured mosquito cells and either DENV-naive or DENV-immune mice. Compared with wild-type ZIKV, the strains passaged under both conditions exhibit increased pathogenesis in DENV-immune mice. Application of reverse genetics identifies an isoleucine-to-valine mutation (I39V) in the NS2B proteins of both passaged strains that confers enhanced fitness and escape from pre-existing DENV immunity. Introduction of I39V or I39T, a naturally occurring homologous mutation detected in recent ZIKV isolates, increases the replication of wild-type ZIKV in human neuronal precursor cells and laboratory-raised mosquitoes. Our data indicate that ZIKV strains with enhanced transmissibility and pathogenicity can emerge in DENV-naive or -immune settings, and that NS2B-I39 mutants may represent ZIKV variants of interest.
- Authors:
-
[2]
- La Jolla Institute for Immunology, CA (United States); Univ. de Guadalajara (Mexico)
- La Jolla Institute for Immunology, CA (United States)
- University of Texas Medical Branch, Galveston, TX (United States)
- Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrative Bioimaging Division
- Univ. of California, San Diego, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
- OSTI Identifier:
- 1893119
- Grant/Contract Number:
- AC02-05CH11231; R01 AI153500; R01 AI163188; R56 AI148635; U01 AI151810; R01 NS106387; R01 AI134907; R43 AI145617; UL1 TR001439
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Cell Reports
- Additional Journal Information:
- Journal Volume: 39; Journal Issue: 2; Journal ID: ISSN 2211-1247
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Flavivirus evolution; zika virus; dengue virus; mouse-adapted virus; cross-protective immunity; viral pathogenesis; viral transmission; viral variants
Citation Formats
Regla-Nava, Jose Angel, Wang, Ying-Ting, Fontes-Garfias, Camila R., Liu, Yang, Syed, Thasneem, Susantono, Mercylia, Gonzalez, Andrew, Viramontes, Karla M., Verma, Shailendra Kumar, Kim, Kenneth, Landeras-Bueno, Sara, Huang, Chun-Teng, Prigozhin, Daniil M., Gleeson, Joseph G., Terskikh, Alexey V., Shi, Pei-Yong, and Shresta, Sujan. A Zika virus mutation enhances transmission potential and confers escape from protective dengue virus immunity. United States: N. p., 2022.
Web. doi:10.1016/j.celrep.2022.110655.
Regla-Nava, Jose Angel, Wang, Ying-Ting, Fontes-Garfias, Camila R., Liu, Yang, Syed, Thasneem, Susantono, Mercylia, Gonzalez, Andrew, Viramontes, Karla M., Verma, Shailendra Kumar, Kim, Kenneth, Landeras-Bueno, Sara, Huang, Chun-Teng, Prigozhin, Daniil M., Gleeson, Joseph G., Terskikh, Alexey V., Shi, Pei-Yong, & Shresta, Sujan. A Zika virus mutation enhances transmission potential and confers escape from protective dengue virus immunity. United States. https://doi.org/10.1016/j.celrep.2022.110655
Regla-Nava, Jose Angel, Wang, Ying-Ting, Fontes-Garfias, Camila R., Liu, Yang, Syed, Thasneem, Susantono, Mercylia, Gonzalez, Andrew, Viramontes, Karla M., Verma, Shailendra Kumar, Kim, Kenneth, Landeras-Bueno, Sara, Huang, Chun-Teng, Prigozhin, Daniil M., Gleeson, Joseph G., Terskikh, Alexey V., Shi, Pei-Yong, and Shresta, Sujan. Wed .
"A Zika virus mutation enhances transmission potential and confers escape from protective dengue virus immunity". United States. https://doi.org/10.1016/j.celrep.2022.110655. https://www.osti.gov/servlets/purl/1893119.
@article{osti_1893119,
title = {A Zika virus mutation enhances transmission potential and confers escape from protective dengue virus immunity},
author = {Regla-Nava, Jose Angel and Wang, Ying-Ting and Fontes-Garfias, Camila R. and Liu, Yang and Syed, Thasneem and Susantono, Mercylia and Gonzalez, Andrew and Viramontes, Karla M. and Verma, Shailendra Kumar and Kim, Kenneth and Landeras-Bueno, Sara and Huang, Chun-Teng and Prigozhin, Daniil M. and Gleeson, Joseph G. and Terskikh, Alexey V. and Shi, Pei-Yong and Shresta, Sujan},
abstractNote = {Zika virus (ZIKV) and dengue virus (DENV) are arthropod-borne pathogenic flaviviruses that co-circulate in many countries. To understand some of the pressures that influence ZIKV evolution, we mimic the natural transmission cycle by repeating serial passaging of ZIKV through cultured mosquito cells and either DENV-naive or DENV-immune mice. Compared with wild-type ZIKV, the strains passaged under both conditions exhibit increased pathogenesis in DENV-immune mice. Application of reverse genetics identifies an isoleucine-to-valine mutation (I39V) in the NS2B proteins of both passaged strains that confers enhanced fitness and escape from pre-existing DENV immunity. Introduction of I39V or I39T, a naturally occurring homologous mutation detected in recent ZIKV isolates, increases the replication of wild-type ZIKV in human neuronal precursor cells and laboratory-raised mosquitoes. Our data indicate that ZIKV strains with enhanced transmissibility and pathogenicity can emerge in DENV-naive or -immune settings, and that NS2B-I39 mutants may represent ZIKV variants of interest.},
doi = {10.1016/j.celrep.2022.110655},
journal = {Cell Reports},
number = 2,
volume = 39,
place = {United States},
year = {Wed Apr 13 00:00:00 EDT 2022},
month = {Wed Apr 13 00:00:00 EDT 2022}
}
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