Antigenic evolution of dengue viruses over 20 years

Katzelnick, Leah C.; Escoto, Ana Coello; Huang, Angkana T.; García‐Carreras, Bernardo; Chowdhury, Nayeem; Berry, Irina Maljkovic; Chavez, Chris; Buchy, Philippe; Duong, Veasna; Dussart, Philippe; Gromowski, Gregory D.; Macareo, Louis; Thaisomboonsuk, Butsaya; Fernandez, Stefan; Smith, Derek J.; Jarman, Richard G.; Whitehead, Stephen S.; Salje, Henrik; Cummings, Derek A. T.

doi:10.1126/science.abk0058

Cited by 52 publications

(85 citation statements)

References 49 publications

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“…However, differences in susceptibility to heterotypic immunity have also been linked to clade replacements, suggesting antigenic selection may have a role in DENV evolution [49,50]. In support of this hypothesis, we recently showed that antigenic traits of DENV have changed over time and are associated with both epidemic dynamics and genotype replacement [22]. The genetic determinants of antigenic differences identified in our study here will enable formal inferences into these evolutionary processes.…”

Section: Plos Pathogenssupporting

confidence: 76%

“…To identify associations of antigenic signal with specific substitutions across all DENV proteins, we leveraged a dataset of paired whole genome sequences and neutralizing antibody titers that includes 348 DENV1-4 strains co-circulating in Bangkok, Thailand over two decades (1994 to 2014, S1 Fig) [22]. Viruses were placed onto a 3-dimensional antigenic map using antigenic cartography, a method which fits the Euclidean distance between virus-serum pairs on a map to the difference in titer measurements across a panel of reference sera [3].…”

Section: Plos Pathogensmentioning

confidence: 99%

“…Our study utilized whole genome sequences and 3-dimensional antigenic map coordinates of 348 DENV previously characterized by Katzelnick et al [22]. In brief, 1,944 isolated viruses were derived from serum specimens collected from acute illnesses admitted to the Queen Sirikit National Institute of Child Health (QSNICH) in Bangkok, Thailand, mostly between 1994 and 2014.…”

Section: Datamentioning

confidence: 99%

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Beneath the surface: Amino acid variation underlying two decades of dengue virus antigenic dynamics in Bangkok, Thailand

Huang

Salje²,

Escoto³

et al. 2022

PLoS Pathog

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Neutralizing antibodies are important correlates of protection against dengue. Yet, determinants of variation in neutralization across strains within the four dengue virus serotypes (DENV1-4) is imperfectly understood. Studies focus on structural DENV proteins, especially the envelope (E), the primary target of anti-DENV antibodies. Although changes in immune recognition (antigenicity) are often attributed to variation in epitope residues, viral processes influencing conformation and epitope accessibility also affect neutralizability, suggesting possible modulating roles of nonstructural proteins. We estimated effects of residue changes in all 10 DENV proteins on antigenic distances between 348 DENV collected from individuals living in Bangkok, Thailand (1994-2014). Antigenic distances were derived from response of each virus to a panel of twenty non-human primate antisera. Across 100 estimations, excluding 10% of virus pairs each time, 77 of 295 positions with residue variability in E consistently conferred antigenic effects; 52 were within ±3 sites of known binding sites of neutralizing human monoclonal antibodies, exceeding expectations from random assignments of effects to sites (p = 0.037). Effects were also identified for 16 sites on the stem/anchor of E which were only recently shown to become exposed under physiological conditions. For all proteins, except nonstructural protein 2A (NS2A), root-mean-squared-error (RMSE) in predicting distances between pairs held out in each estimation did not outperform sequences of equal length derived from all proteins or E, suggesting that antigenic signals present were likely through linkage with E. Adjusted for E, we identified 62/219 sites embedding the excess signals in NS2A. Concatenating these sites to E additionally explained 3.4% to 4.0% of observed variance in antigenic distances from when E alone (50.5% to 50.8%); RMSE outperformed concatenating E with sites from any protein of the virus (ΔRMSE, 95%IQR: 0.01, 0.05). Our results support examining antigenic determinants beyond the DENV surface.

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Section: Plos Pathogenssupporting

confidence: 76%

Section: Plos Pathogensmentioning

confidence: 99%

Section: Datamentioning

confidence: 99%

See 1 more Smart Citation

Beneath the surface: Amino acid variation underlying two decades of dengue virus antigenic dynamics in Bangkok, Thailand

Huang

Salje²,

Escoto³

et al. 2022

PLoS Pathog

Self Cite

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“…At time of infection, clear vector-associated risk factors-including habits of mosquito net use, larvicide use, and mosquito coil use-demonstrated no association with DENV infection status either. Though vector-driven selection has a significant role in overall transmission potential 34 , epidemic years may be more intensely driven by changes in serotype or genotype that underpin viral evasion of existing host immunity 13 . In our global predictor model, patient age and upper/middle vs. lower socioeconomic status were negatively correlated with DENV positivity, highlighting the preponderance of infections in children and those in poorer income brackets (Table S6).…”

Section: Regional Active Surveillance In the 2019 Cambodia Dengue Epi...mentioning

confidence: 99%

Climate, demography, immunology, and virology combine to drive two decades of dengue virus dynamics in Cambodia

Brook

Yek

et al. 2022

Preprint

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The year 2019 witnessed the highest number of dengue cases ever reported globally. We analyzed epidemiological, serological, and phylogenomic data to investigate the drivers of the 2019 epidemic in Cambodia. Using epidemiological models fit to a 19-year national dataset, we identified an overall trend of declining annual force of infection (FOI) for dengue virus (DENV) in Cambodia, interspersed with FOI spikes corresponding to epidemic year caseloads that exceeded demographic predictions. We constructed time-resolved phylogenetic trees with 105 DENV genomes sequenced from the 2019 Cambodian epidemic, paired with historical Southeast Asian data, to document the first-recorded introduction of DENV-2 Cosmopolitan genotype into Cambodia. This introduction yielded highly localized transmission and decreased genomic diversity when compared to endemic DENV-1, supporting the hypothesis of epidemic invasion. Introduction of this genetically distinct lineage into a population with limited prior immunity-paired with a spike in FOI-was a key driver of the 2019 Cambodian epidemic.

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“…A recent study of data from Thailand revealed that as dengue virus evolves to evade host immunity, major epidemics result when a serotype strain becomes more antigenically similar to other serotypes than its own. 3 The force of the invading strain can result in a selective sweep, reducing viral diversity with a subsequent drop in cases. Chen and colleagues added spatial random effects to account for the introduction of new dengue serotypes, and population immunity was labelled annual anomaly in the model.…”

mentioning

confidence: 99%