Viral immunogenicity determines epidemiological fitness in a cohort of DENV-1 infection in Brazil

Tauyne Menegaldo Pinheiro; Mânlio Tasso de Oliveira Mota; Aripuanã Sakurada Aranha Watanabe; Joice Matos Biselli-Périco; Betânia Paiva Drumond; Milene Rocha Ribeiro; Danila Vedovello; João Pessoa Araújo; Paulo Filemon Paolucci Pimenta; Bárbara Aparecida Chaves; Mayara Marques Carneiro da Silva; Izabella Cristina Andrade Batista; Michelle Premazzi Papa; Lana Monteiro Meuren; Carolina Gonçalves de Oliveira Lucas; Flavio Lemos Matassoli; Laura Helena Vega Gonzales Gil; Adriana Bozzi; Carlos Eduardo Calzavara-Silva; Luciana Barros de Arruda; Danielle da Glória de Souza; Mauro Martins Teixeira; Nikos Vasilakis; Maurício Lacerda Nogueira

doi:10.1371/journal.pntd.0006525

Viral immunogenicity determines epidemiological fitness in a cohort of DENV-1 infection in Brazil

Tauyne Menegaldo Pinheiro, Mânlio Tasso de Oliveira Mota, Aripuanã Sakurada Aranha Watanabe, Joice Matos Biselli-Périco, Betânia Paiva Drumond, Milene Rocha Ribeiro, Danila Vedovello, João Pessoa Araújo, Paulo Filemon Paolucci Pimenta, Bárbara Aparecida Chaves, Mayara Marques Carneiro da Silva, Izabella Cristina Andrade Batista, Michelle Premazzi Papa, Lana Monteiro Meuren, Carolina Gonçalves de Oliveira Lucas, Flavio Lemos Matassoli, Laura Helena Vega Gonzales Gil, Adriana Bozzi, Carlos Eduardo Calzavara-Silva, Luciana Barros de ArrudaDanielle da Glória de Souza, Mauro Martins Teixeira, Nikos Vasilakis, Maurício Lacerda Nogueira

Pathology

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18 Scopus citations

Abstract

The dynamics of dengue virus (DENV) circulation depends on serotype, genotype and lineage replacement and turnover. In São José do Rio Preto, Brazil, we observed that the L6 lineage of DENV-1 (genotype V) remained the dominant circulating lineage even after the introduction of the L1 lineage. We investigated viral fitness and immunogenicity of the L1 and L6 lineages and which factors interfered with the dynamics of DENV epidemics. The results showed a more efficient replicative fitness of L1 over L6 in mosquitoes and in human and non-human primate cell lines. Infections by the L6 lineage were associated with reduced antigenicity, weak B and T cell stimulation and weak host immune system interactions, which were associated with higher viremia. Our data, therefore, demonstrate that reduced viral immunogenicity and consequent greater viremia determined the increased epidemiological fitness of DENV-1 L6 lineage in São José do Rio Preto.

Original language	English (US)
Article number	e0006525
Journal	PLoS neglected tropical diseases
Volume	12
Issue number	5
DOIs	https://doi.org/10.1371/journal.pntd.0006525
State	Published - May 29 2018

ASJC Scopus subject areas

Public Health, Environmental and Occupational Health
Infectious Diseases

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Pinheiro, T. M., Mota, M. T. D. O., Watanabe, A. S. A., Biselli-Périco, J. M., Drumond, B. P., Ribeiro, M. R., Vedovello, D., Araújo, J. P., Pimenta, P. F. P., Chaves, B. A., Silva, M. M. C. D., Batista, I. C. A., Papa, M. P., Meuren, L. M., Lucas, C. G. D. O., Matassoli, F. L., Gil, L. H. V. G., Bozzi, A., Calzavara-Silva, C. E., ... Nogueira, M. L. (2018). Viral immunogenicity determines epidemiological fitness in a cohort of DENV-1 infection in Brazil. PLoS neglected tropical diseases, 12(5), Article e0006525. https://doi.org/10.1371/journal.pntd.0006525

Pinheiro, TM, Mota, MTDO, Watanabe, ASA, Biselli-Périco, JM, Drumond, BP, Ribeiro, MR, Vedovello, D, Araújo, JP, Pimenta, PFP, Chaves, BA, Silva, MMCD, Batista, ICA, Papa, MP, Meuren, LM, Lucas, CGDO, Matassoli, FL, Gil, LHVG, Bozzi, A, Calzavara-Silva, CE, Arruda, LBD, Souza, DDGD, Teixeira, MM, Vasilakis, N & Nogueira, ML 2018, 'Viral immunogenicity determines epidemiological fitness in a cohort of DENV-1 infection in Brazil', PLoS neglected tropical diseases, vol. 12, no. 5, e0006525. https://doi.org/10.1371/journal.pntd.0006525

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abstract = "The dynamics of dengue virus (DENV) circulation depends on serotype, genotype and lineage replacement and turnover. In S{\~a}o Jos{\'e} do Rio Preto, Brazil, we observed that the L6 lineage of DENV-1 (genotype V) remained the dominant circulating lineage even after the introduction of the L1 lineage. We investigated viral fitness and immunogenicity of the L1 and L6 lineages and which factors interfered with the dynamics of DENV epidemics. The results showed a more efficient replicative fitness of L1 over L6 in mosquitoes and in human and non-human primate cell lines. Infections by the L6 lineage were associated with reduced antigenicity, weak B and T cell stimulation and weak host immune system interactions, which were associated with higher viremia. Our data, therefore, demonstrate that reduced viral immunogenicity and consequent greater viremia determined the increased epidemiological fitness of DENV-1 L6 lineage in S{\~a}o Jos{\'e} do Rio Preto.",

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AU - Mota, Mânlio Tasso de Oliveira

AU - Watanabe, Aripuanã Sakurada Aranha

AU - Biselli-Périco, Joice Matos

AU - Drumond, Betânia Paiva

AU - Ribeiro, Milene Rocha

AU - Vedovello, Danila

AU - Araújo, João Pessoa

AU - Pimenta, Paulo Filemon Paolucci

AU - Chaves, Bárbara Aparecida

AU - Silva, Mayara Marques Carneiro da

AU - Batista, Izabella Cristina Andrade

AU - Papa, Michelle Premazzi

AU - Meuren, Lana Monteiro

AU - Lucas, Carolina Gonçalves de Oliveira

AU - Matassoli, Flavio Lemos

AU - Gil, Laura Helena Vega Gonzales

AU - Bozzi, Adriana

AU - Calzavara-Silva, Carlos Eduardo

AU - Arruda, Luciana Barros de

AU - Souza, Danielle da Glória de

AU - Teixeira, Mauro Martins

AU - Vasilakis, Nikos

AU - Nogueira, Maurício Lacerda

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N2 - The dynamics of dengue virus (DENV) circulation depends on serotype, genotype and lineage replacement and turnover. In São José do Rio Preto, Brazil, we observed that the L6 lineage of DENV-1 (genotype V) remained the dominant circulating lineage even after the introduction of the L1 lineage. We investigated viral fitness and immunogenicity of the L1 and L6 lineages and which factors interfered with the dynamics of DENV epidemics. The results showed a more efficient replicative fitness of L1 over L6 in mosquitoes and in human and non-human primate cell lines. Infections by the L6 lineage were associated with reduced antigenicity, weak B and T cell stimulation and weak host immune system interactions, which were associated with higher viremia. Our data, therefore, demonstrate that reduced viral immunogenicity and consequent greater viremia determined the increased epidemiological fitness of DENV-1 L6 lineage in São José do Rio Preto.

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Viral immunogenicity determines epidemiological fitness in a cohort of DENV-1 infection in Brazil

Abstract

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