Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data

Objective: The invasion of dengue virus (DENV)-2 Cosmopolitan genotype into the Philippines, where the Asian II genotype previously circulated challenges the principle of dengue serotype-specific immunity. Assessment of antibodies in this population may provide a mechanistic basis for how new genoty...

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Main Authors: Jean Claude Balingit, Mark Pierre S. Dimamay, Ryosuke Suzuki, Mami Matsuda, Dalouny Xayavong, Mya Myat Ngwe Tun, Ronald R. Matias, Filipinas F. Natividad, Meng Ling Moi, Yuki Takamatsu, Richard Culleton, Corazon C. Buerano, Kouichi Morita
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:International Journal of Infectious Diseases
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1201971223007865
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author Jean Claude Balingit
Mark Pierre S. Dimamay
Ryosuke Suzuki
Mami Matsuda
Dalouny Xayavong
Mya Myat Ngwe Tun
Ronald R. Matias
Filipinas F. Natividad
Meng Ling Moi
Yuki Takamatsu
Richard Culleton
Corazon C. Buerano
Kouichi Morita
author_facet Jean Claude Balingit
Mark Pierre S. Dimamay
Ryosuke Suzuki
Mami Matsuda
Dalouny Xayavong
Mya Myat Ngwe Tun
Ronald R. Matias
Filipinas F. Natividad
Meng Ling Moi
Yuki Takamatsu
Richard Culleton
Corazon C. Buerano
Kouichi Morita
author_sort Jean Claude Balingit
collection DOAJ
description Objective: The invasion of dengue virus (DENV)-2 Cosmopolitan genotype into the Philippines, where the Asian II genotype previously circulated challenges the principle of dengue serotype-specific immunity. Assessment of antibodies in this population may provide a mechanistic basis for how new genotypes emerge in dengue-endemic areas. Methods: We evaluated the neutralizing antibody (nAb) and antibody-dependent enhancement (ADE) responses against the two genotypes using archived serum samples collected from 333 patients with confirmed dengue in Metro Manila, Philippines, before, during, and after the introduction of the Cosmopolitan genotype. We quantified nAb titers in baby hamster kidney (BHK-21) cells with or without the Fcγ receptor IIA (FcγRIIA) to detect the capacity of virus-antibody complexes to neutralize or enhance DENV. Results: The nAb potency of the archived serum samples against the two genotypes was greatly affected by the presence of FcγRIIA. We found significant differences in nAb titers between the two genotypes in BHK-21 cells with FcγRIIA (P <0.0001). The archived serum samples were incapable of fully neutralizing the Cosmopolitan genotype, but instead strongly promoted its ADE compared to the Asian II genotype (P <0.0001). Conclusion: These results reinforce the role of pre-existing immunity in driving genotype shifts. Our finding that specific genotypes exhibit differing susceptibilities to ADE by cross-reactive antibodies may have implications for dengue vaccine development.
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spelling doaj.art-5aae5d98353844eb8392fb0a563ef7462024-01-13T04:43:24ZengElsevierInternational Journal of Infectious Diseases1201-97122024-02-011395968Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological dataJean Claude Balingit0Mark Pierre S. Dimamay1Ryosuke Suzuki2Mami Matsuda3Dalouny Xayavong4Mya Myat Ngwe Tun5Ronald R. Matias6Filipinas F. Natividad7Meng Ling Moi8Yuki Takamatsu9Richard Culleton10Corazon C. Buerano11Kouichi Morita12Department of Tropical Viral Vaccine Development, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; Department of Virology, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, JapanResearch and Biotechnology Group, St. Luke's Medical Center, Quezon City, Metro Manila, PhilippinesDepartment of Virology II, National Institute of Infectious Diseases, Gakuen, Musashi-murayama, Tokyo, JapanDepartment of Virology II, National Institute of Infectious Diseases, Gakuen, Musashi-murayama, Tokyo, JapanDepartment of Virology, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, JapanDepartment of Tropical Viral Vaccine Development, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; Department of Virology, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, JapanResearch and Biotechnology Group, St. Luke's Medical Center, Quezon City, Metro Manila, PhilippinesNational Ethics Committee, Philippine Council for Health Research and Development, Department of Science and Technology (DOST), Saliksik Building, DOST Compound, Bicutan, Taguig City, Metro Manila, PhilippinesDepartment of Developmental Medical Sciences, School of International Health, University of Tokyo, Bunkyo-ku, Tokyo, JapanDepartment of Tropical Viral Vaccine Development, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; Department of Virology, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, JapanDivision of Molecular Parasitology, Proteo-Science Center, Ehime University, Shitsukawa, Ehime, JapanDepartment of Tropical Viral Vaccine Development, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; Research and Biotechnology Group, St. Luke's Medical Center, Quezon City, Metro Manila, PhilippinesDepartment of Tropical Viral Vaccine Development, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; Department of Virology, Institute of Tropical Medicine, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; DEJIMA Infectious Disease Research Alliance, Nagasaki University, Sakamoto, Nagasaki City, Nagasaki, Japan; Corresponding author:Objective: The invasion of dengue virus (DENV)-2 Cosmopolitan genotype into the Philippines, where the Asian II genotype previously circulated challenges the principle of dengue serotype-specific immunity. Assessment of antibodies in this population may provide a mechanistic basis for how new genotypes emerge in dengue-endemic areas. Methods: We evaluated the neutralizing antibody (nAb) and antibody-dependent enhancement (ADE) responses against the two genotypes using archived serum samples collected from 333 patients with confirmed dengue in Metro Manila, Philippines, before, during, and after the introduction of the Cosmopolitan genotype. We quantified nAb titers in baby hamster kidney (BHK-21) cells with or without the Fcγ receptor IIA (FcγRIIA) to detect the capacity of virus-antibody complexes to neutralize or enhance DENV. Results: The nAb potency of the archived serum samples against the two genotypes was greatly affected by the presence of FcγRIIA. We found significant differences in nAb titers between the two genotypes in BHK-21 cells with FcγRIIA (P <0.0001). The archived serum samples were incapable of fully neutralizing the Cosmopolitan genotype, but instead strongly promoted its ADE compared to the Asian II genotype (P <0.0001). Conclusion: These results reinforce the role of pre-existing immunity in driving genotype shifts. Our finding that specific genotypes exhibit differing susceptibilities to ADE by cross-reactive antibodies may have implications for dengue vaccine development.http://www.sciencedirect.com/science/article/pii/S1201971223007865DengueAntibody-dependent enhancementGenotype shiftNeutralizing antibodiesPre-existing immunity
spellingShingle Jean Claude Balingit
Mark Pierre S. Dimamay
Ryosuke Suzuki
Mami Matsuda
Dalouny Xayavong
Mya Myat Ngwe Tun
Ronald R. Matias
Filipinas F. Natividad
Meng Ling Moi
Yuki Takamatsu
Richard Culleton
Corazon C. Buerano
Kouichi Morita
Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data
International Journal of Infectious Diseases
Dengue
Antibody-dependent enhancement
Genotype shift
Neutralizing antibodies
Pre-existing immunity
title Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data
title_full Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data
title_fullStr Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data
title_full_unstemmed Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data
title_short Role of pre-existing immunity in driving the dengue virus serotype 2 genotype shift in the Philippines: A retrospective analysis of serological data
title_sort role of pre existing immunity in driving the dengue virus serotype 2 genotype shift in the philippines a retrospective analysis of serological data
topic Dengue
Antibody-dependent enhancement
Genotype shift
Neutralizing antibodies
Pre-existing immunity
url http://www.sciencedirect.com/science/article/pii/S1201971223007865
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