Dengue immune sera enhance Zika virus infection in human peripheral blood monocytes through Fc gamma receptors

Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific antibodies can enhance Zika virus (ZIKV) infectivity, and vice versa. To examine the mechanisms of ADE of ZIKV infection in primary human cells,...

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Published inPloS one Vol. 13; no. 7; p. e0200478
Main Authors Li, Min, Zhao, Lingzhai, Zhang, Chao, Wang, Xin, Hong, Wenxin, Sun, Jin, Liu, Ran, Yu, Lei, Wang, Jianhua, Zhang, Fuchun, Jin, Xia
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 25.07.2018
Public Library of Science (PLoS)
Subjects
Adolescent
Adult
Aged
Antibodies
Antibodies, Viral - blood
Antibodies, Viral - immunology
Antibody-Dependent Enhancement - immunology
Antisera
Biology and Life Sciences
Blood
CD14 antigen
CD16 antigen
Cross Reactions - immunology
Dendritic cells
Dendritic Cells - immunology
Dengue
Dengue - blood
Dengue - immunology
Dengue - virology
Dengue fever
Dengue virus
Dengue Virus - immunology
Fc receptors
Female
Glycoproteins
Guillain-Barre syndrome
Humans
Immune Sera - immunology
Immune serum
Immunoglobulins
Immunology
Infections
Infectivity
Laboratories
Leukemia
Leukocytes (mononuclear)
Lymphocytes
Lymphocytes B
Lymphocytes T
Male
Medicine and Health Sciences
Microcephaly
Middle Aged
Monocytes
Monocytes - immunology
Neutralization
Neutralization Tests
Pathogenesis
Peripheral blood mononuclear cells
Receptors
Receptors, IgG - blood
Receptors, IgG - immunology
Research and Analysis Methods
Tumor cell lines
Vector-borne diseases
Viral diseases
Virology
Viruses
Young Adult
Zika virus
Zika Virus - immunology
Zika Virus - pathogenicity
Zika virus infection
Zika Virus Infection - immunology
Zika Virus Infection - virology
Brazil
Beijing China
China
French Polynesia
Online AccessGet full text
ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0200478

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Abstract Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific antibodies can enhance Zika virus (ZIKV) infectivity, and vice versa. To examine the mechanisms of ADE of ZIKV infection in primary human cells, we assessed 40 serum samples obtained from convalescent DENV-1 or DENV-3 infected subjects. All sera tested exhibited high binding potency, while modest or none neutralization activities against ZIKV. Primary CD14+ monocytes, rather than B and T cells in peripheral blood mononuclear cells (PBMCs), were found to be the mediators of the enhancement of ZIKV infectivity by DENV immune sera. Monocyte-derived immature dendritic cells (DCs), but not mature DCs were highly permissive to ZIKV infection, whereas neither immature nor mature DCs could mediate enhanced ZIKV infection in the presence of DENV immune sera. In addition, antibody blocking of either FcγRI (CD64), or FcγRII (CD32), or FcγRIII (CD16) resulted in diminished ADE of ZIKV infection. Our findings provide an improved understanding of the pathogenesis of ZIKV infection, and inform rational vaccine design.
AbstractList Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific antibodies can enhance Zika virus (ZIKV) infectivity, and vice versa. To examine the mechanisms of ADE of ZIKV infection in primary human cells, we assessed 40 serum samples obtained from convalescent DENV-1 or DENV-3 infected subjects. All sera tested exhibited high binding potency, while modest or none neutralization activities against ZIKV. Primary CD14+ monocytes, rather than B and T cells in peripheral blood mononuclear cells (PBMCs), were found to be the mediators of the enhancement of ZIKV infectivity by DENV immune sera. Monocyte-derived immature dendritic cells (DCs), but not mature DCs were highly permissive to ZIKV infection, whereas neither immature nor mature DCs could mediate enhanced ZIKV infection in the presence of DENV immune sera. In addition, antibody blocking of either FcγRI (CD64), or FcγRII (CD32), or FcγRIII (CD16) resulted in diminished ADE of ZIKV infection. Our findings provide an improved understanding of the pathogenesis of ZIKV infection, and inform rational vaccine design.
Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific antibodies can enhance Zika virus (ZIKV) infectivity, and vice versa. To examine the mechanisms of ADE of ZIKV infection in primary human cells, we assessed 40 serum samples obtained from convalescent DENV-1 or DENV-3 infected subjects. All sera tested exhibited high binding potency, while modest or none neutralization activities against ZIKV. Primary CD14+ monocytes, rather than B and T cells in peripheral blood mononuclear cells (PBMCs), were found to be the mediators of the enhancement of ZIKV infectivity by DENV immune sera. Monocyte-derived immature dendritic cells (DCs), but not mature DCs were highly permissive to ZIKV infection, whereas neither immature nor mature DCs could mediate enhanced ZIKV infection in the presence of DENV immune sera. In addition, antibody blocking of either Fc[gamma]RI (CD64), or Fc[gamma]RII (CD32), or Fc[gamma]RIII (CD16) resulted in diminished ADE of ZIKV infection. Our findings provide an improved understanding of the pathogenesis of ZIKV infection, and inform rational vaccine design.
Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific antibodies can enhance Zika virus (ZIKV) infectivity, and vice versa. To examine the mechanisms of ADE of ZIKV infection in primary human cells, we assessed 40 serum samples obtained from convalescent DENV-1 or DENV-3 infected subjects. All sera tested exhibited high binding potency, while modest or none neutralization activities against ZIKV. Primary CD14+ monocytes, rather than B and T cells in peripheral blood mononuclear cells (PBMCs), were found to be the mediators of the enhancement of ZIKV infectivity by DENV immune sera. Monocyte-derived immature dendritic cells (DCs), but not mature DCs were highly permissive to ZIKV infection, whereas neither immature nor mature DCs could mediate enhanced ZIKV infection in the presence of DENV immune sera. In addition, antibody blocking of either FcγRI (CD64), or FcγRII (CD32), or FcγRIII (CD16) resulted in diminished ADE of ZIKV infection. Our findings provide an improved understanding of the pathogenesis of ZIKV infection, and inform rational vaccine design.Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific antibodies can enhance Zika virus (ZIKV) infectivity, and vice versa. To examine the mechanisms of ADE of ZIKV infection in primary human cells, we assessed 40 serum samples obtained from convalescent DENV-1 or DENV-3 infected subjects. All sera tested exhibited high binding potency, while modest or none neutralization activities against ZIKV. Primary CD14+ monocytes, rather than B and T cells in peripheral blood mononuclear cells (PBMCs), were found to be the mediators of the enhancement of ZIKV infectivity by DENV immune sera. Monocyte-derived immature dendritic cells (DCs), but not mature DCs were highly permissive to ZIKV infection, whereas neither immature nor mature DCs could mediate enhanced ZIKV infection in the presence of DENV immune sera. In addition, antibody blocking of either FcγRI (CD64), or FcγRII (CD32), or FcγRIII (CD16) resulted in diminished ADE of ZIKV infection. Our findings provide an improved understanding of the pathogenesis of ZIKV infection, and inform rational vaccine design.
Audience Academic
Author Li, Min
Sun, Jin
Wang, Jianhua
Zhang, Chao
Zhang, Fuchun
Wang, Xin
Zhao, Lingzhai
Liu, Ran
Hong, Wenxin
Jin, Xia
Yu, Lei
AuthorAffiliation 2 University of Chinese Academy of Sciences, Beijing, China
4 School of Life Sciences, Shanghai University, Shanghai, China
1 CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences (CAS), Shanghai, China
3 Guangzhou Eighth People’s Hospital, Guangzhou Medical University, Guangzhou, China
University of Hong Kong, HONG KONG
AuthorAffiliation_xml – name: 1 CAS Key Laboratory of Molecular Virology and Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences (CAS), Shanghai, China
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Snippet Antibody dependent enhancement (ADE) has most often been associated with dengue virus (DENV). Studies using leukemia cell lines suggest that DENV specific...
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StartPage e0200478
SubjectTerms Adolescent
Adult
Aged
Antibodies
Antibodies, Viral - blood
Antibodies, Viral - immunology
Antibody-Dependent Enhancement - immunology
Antisera
Biology and Life Sciences
Blood
CD14 antigen
CD16 antigen
Cross Reactions - immunology
Dendritic cells
Dendritic Cells - immunology
Dengue
Dengue - blood
Dengue - immunology
Dengue - virology
Dengue fever
Dengue virus
Dengue Virus - immunology
Fc receptors
Female
Glycoproteins
Guillain-Barre syndrome
Humans
Immune Sera - immunology
Immune serum
Immunoglobulins
Immunology
Infections
Infectivity
Laboratories
Leukemia
Leukocytes (mononuclear)
Lymphocytes
Lymphocytes B
Lymphocytes T
Male
Medicine and Health Sciences
Microcephaly
Middle Aged
Monocytes
Monocytes - immunology
Neutralization
Neutralization Tests
Pathogenesis
Peripheral blood mononuclear cells
Receptors
Receptors, IgG - blood
Receptors, IgG - immunology
Research and Analysis Methods
Tumor cell lines
Vector-borne diseases
Viral diseases
Virology
Viruses
Young Adult
Zika virus
Zika Virus - immunology
Zika Virus - pathogenicity
Zika virus infection
Zika Virus Infection - immunology
Zika Virus Infection - virology
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Title Dengue immune sera enhance Zika virus infection in human peripheral blood monocytes through Fc gamma receptors
URI https://www.ncbi.nlm.nih.gov/pubmed/30044839
https://www.proquest.com/docview/2082089210
https://www.proquest.com/docview/2076902893
https://pubmed.ncbi.nlm.nih.gov/PMC6059439
https://doaj.org/article/4f086cfd5501411d802dbe21dc85d6e1
http://dx.doi.org/10.1371/journal.pone.0200478
Volume 13
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