Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients

André N.A. Gonçalves; Priscilla R. Costa; Mateus V. Thomazella; Carolina A. Correia; Mariana P. Marmorato; Juliana Z.C. Dias; Cassia G.T. Silveira; Alvino Maestri; Natalia B. Cerqueira; Carlos H.V. Moreira; Renata Buccheri; Alvina C. Félix; Felipe M. Martins; Vanessa E. Maso; Frederico M. Ferreira; José D.A. Araújo; Amanda P. Vasconcelos; Patrícia Gonzalez-Dias; Adam Nicolas Pelletier; Rafick Pierre Sékaly; Otavio Cabral-Marques; Jordana G.A. Coelho-dos-Reis; Daniela Ferreira; Esper G. Kallas; Helder I. Nakaya

doi:10.1002/jmv.70099

Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients

André N.A. Gonçalves
, Priscilla R. Costa
, Mateus V. Thomazella
, Carolina A. Correia
, Mariana P. Marmorato
, Juliana Z.C. Dias
, Cassia G.T. Silveira
, Alvino Maestri
, Natalia B. Cerqueira
, Carlos H.V. Moreira
, Renata Buccheri
, Alvina C. Félix
, Felipe M. Martins
, Vanessa E. Maso
, Frederico M. Ferreira
, José D.A. Araújo
, Amanda P. Vasconcelos
, Patrícia Gonzalez-Dias
, Adam Nicolas Pelletier
, Rafick Pierre Sékaly

Otavio Cabral-Marques, Jordana G.A. Coelho-dos-Reis, Daniela Ferreira, Esper G. Kallas, Helder I. Nakaya

NIHR Oxford Biomedical Research Centre
Universidade de São Paulo
Instituto de Infectologia Emílio Ribas
MONTREAL
Emory University
DO′R Institute for Research
Universidade Federal de Minas Gerais
Hospital Israelita Albert Einstein

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

3 Citations (Scopus)

Abstract

In the 2018 yellow fever (YF) outbreak in Brazil, we generated new transcriptomic data and combined it with clinical and immunological data to decode the pathogenesis of YF. Analyzing 79 patients, we found distinct gene expression patterns between acute YF, other viral infections, and the milder YF-17D vaccine infection. We identified a critical role for low-density, immature neutrophils in severe outcomes, marked by the downregulation of genes essential for neutrophil migration and maturation, such as PADI4, CSF3R, and ICAM1, in deceased patients. Our study also revealed complex interactions among inflammation-related genes, including increased CXCL10 and IL1R2 expression and decreased IL-1b expression in the acute phase. The diminished expression of HLA class II genes indicates impaired antigen presentation. These findings highlight the delicate balance of immune responses in YF pathogenesis and lay the groundwork for future therapeutic and diagnostic advancements.

Original language	English
Article number	e70099
Journal	Journal of Medical Virology
Volume	96
Issue number	12
DOIs	https://doi.org/10.1002/jmv.70099
Publication status	Published - 1 Dec 2024
Externally published	Yes

UN SDGs

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

SDG 3 Good Health and Well-being

Keywords

PBMC transcriptome
system biology analysis
yellow fever infection

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10.1002/jmv.70099

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Gonçalves, A. N. A., Costa, P. R., Thomazella, M. V., Correia, C. A., Marmorato, M. P., Dias, J. Z. C., Silveira, C. G. T., Maestri, A., Cerqueira, N. B., Moreira, C. H. V., Buccheri, R., Félix, A. C., Martins, F. M., Maso, V. E., Ferreira, F. M., Araújo, J. D. A., Vasconcelos, A. P., Gonzalez-Dias, P., Pelletier, A. N., ... Nakaya, H. I. (2024). Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients. Journal of Medical Virology, 96(12), Article e70099. https://doi.org/10.1002/jmv.70099

@article{8828b2f69f674de69d937c6611430609,

title = "Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients",

abstract = "In the 2018 yellow fever (YF) outbreak in Brazil, we generated new transcriptomic data and combined it with clinical and immunological data to decode the pathogenesis of YF. Analyzing 79 patients, we found distinct gene expression patterns between acute YF, other viral infections, and the milder YF-17D vaccine infection. We identified a critical role for low-density, immature neutrophils in severe outcomes, marked by the downregulation of genes essential for neutrophil migration and maturation, such as PADI4, CSF3R, and ICAM1, in deceased patients. Our study also revealed complex interactions among inflammation-related genes, including increased CXCL10 and IL1R2 expression and decreased IL-1b expression in the acute phase. The diminished expression of HLA class II genes indicates impaired antigen presentation. These findings highlight the delicate balance of immune responses in YF pathogenesis and lay the groundwork for future therapeutic and diagnostic advancements.",

keywords = "PBMC transcriptome, system biology analysis, yellow fever infection",

author = "Gon{\c c}alves, \{Andr{\'e} N.A.\} and Costa, \{Priscilla R.\} and Thomazella, \{Mateus V.\} and Correia, \{Carolina A.\} and Marmorato, \{Mariana P.\} and Dias, \{Juliana Z.C.\} and Silveira, \{Cassia G.T.\} and Alvino Maestri and Cerqueira, \{Natalia B.\} and Moreira, \{Carlos H.V.\} and Renata Buccheri and F{\'e}lix, \{Alvina C.\} and Martins, \{Felipe M.\} and Maso, \{Vanessa E.\} and Ferreira, \{Frederico M.\} and Ara{\'u}jo, \{Jos{\'e} D.A.\} and Vasconcelos, \{Amanda P.\} and Patr{\'i}cia Gonzalez-Dias and Pelletier, \{Adam Nicolas\} and S{\'e}kaly, \{Rafick Pierre\} and Otavio Cabral-Marques and Coelho-dos-Reis, \{Jordana G.A.\} and Daniela Ferreira and Kallas, \{Esper G.\} and Nakaya, \{Helder I.\}",

year = "2024",

month = dec,

day = "1",

doi = "10.1002/jmv.70099",

language = "English",

volume = "96",

journal = "Journal of Medical Virology",

issn = "0146-6615",

publisher = "John Wiley and Sons Inc",

number = "12",

}

Gonçalves, ANA, Costa, PR, Thomazella, MV, Correia, CA, Marmorato, MP, Dias, JZC, Silveira, CGT, Maestri, A, Cerqueira, NB, Moreira, CHV, Buccheri, R, Félix, AC, Martins, FM, Maso, VE, Ferreira, FM, Araújo, JDA, Vasconcelos, AP, Gonzalez-Dias, P, Pelletier, AN, Sékaly, RP, Cabral-Marques, O, Coelho-dos-Reis, JGA, Ferreira, D, Kallas, EG & Nakaya, HI 2024, 'Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients', Journal of Medical Virology, vol. 96, no. 12, e70099. https://doi.org/10.1002/jmv.70099

TY - JOUR

T1 - Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients

AU - Gonçalves, André N.A.

AU - Costa, Priscilla R.

AU - Thomazella, Mateus V.

AU - Correia, Carolina A.

AU - Marmorato, Mariana P.

AU - Dias, Juliana Z.C.

AU - Silveira, Cassia G.T.

AU - Maestri, Alvino

AU - Cerqueira, Natalia B.

AU - Moreira, Carlos H.V.

AU - Buccheri, Renata

AU - Félix, Alvina C.

AU - Martins, Felipe M.

AU - Maso, Vanessa E.

AU - Ferreira, Frederico M.

AU - Araújo, José D.A.

AU - Vasconcelos, Amanda P.

AU - Gonzalez-Dias, Patrícia

AU - Pelletier, Adam Nicolas

AU - Sékaly, Rafick Pierre

AU - Cabral-Marques, Otavio

AU - Coelho-dos-Reis, Jordana G.A.

AU - Ferreira, Daniela

AU - Kallas, Esper G.

AU - Nakaya, Helder I.

PY - 2024/12/1

Y1 - 2024/12/1

N2 - In the 2018 yellow fever (YF) outbreak in Brazil, we generated new transcriptomic data and combined it with clinical and immunological data to decode the pathogenesis of YF. Analyzing 79 patients, we found distinct gene expression patterns between acute YF, other viral infections, and the milder YF-17D vaccine infection. We identified a critical role for low-density, immature neutrophils in severe outcomes, marked by the downregulation of genes essential for neutrophil migration and maturation, such as PADI4, CSF3R, and ICAM1, in deceased patients. Our study also revealed complex interactions among inflammation-related genes, including increased CXCL10 and IL1R2 expression and decreased IL-1b expression in the acute phase. The diminished expression of HLA class II genes indicates impaired antigen presentation. These findings highlight the delicate balance of immune responses in YF pathogenesis and lay the groundwork for future therapeutic and diagnostic advancements.

AB - In the 2018 yellow fever (YF) outbreak in Brazil, we generated new transcriptomic data and combined it with clinical and immunological data to decode the pathogenesis of YF. Analyzing 79 patients, we found distinct gene expression patterns between acute YF, other viral infections, and the milder YF-17D vaccine infection. We identified a critical role for low-density, immature neutrophils in severe outcomes, marked by the downregulation of genes essential for neutrophil migration and maturation, such as PADI4, CSF3R, and ICAM1, in deceased patients. Our study also revealed complex interactions among inflammation-related genes, including increased CXCL10 and IL1R2 expression and decreased IL-1b expression in the acute phase. The diminished expression of HLA class II genes indicates impaired antigen presentation. These findings highlight the delicate balance of immune responses in YF pathogenesis and lay the groundwork for future therapeutic and diagnostic advancements.

KW - PBMC transcriptome

KW - system biology analysis

KW - yellow fever infection

U2 - 10.1002/jmv.70099

DO - 10.1002/jmv.70099

M3 - Article

SN - 0146-6615

VL - 96

JO - Journal of Medical Virology

JF - Journal of Medical Virology

IS - 12

M1 - e70099

ER -

Systems Immunology Approaches to Understanding Immune Responses in Acute Infection of Yellow Fever Patients

Abstract

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Keywords

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