Defining levels of dengue virus serotype-specific neutralizing antibodies induced by a live attenuated tetravalent dengue vaccine (TAK-003)

The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new seroty...

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Published inPLoS neglected tropical diseases Vol. 15; no. 3; p. e0009258
Main Authors White, Laura J., Young, Ellen F., Stoops, Mark J., Henein, Sandra R., Adams, Elizabeth C., Baric, Ralph S., de Silva, Aravinda M.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.03.2021
Public Library of Science (PLoS)
Subjects
Adult
Amino acids
Animals
Antibodies
Antibodies, Neutralizing - blood
Antibodies, Viral - blood
Antigens
Attenuation
Biology and Life Sciences
Chlorocebus aethiops
Clinical trials
Dengue
Dengue fever
Dengue Vaccines - immunology
Dengue Virus - immunology
Dengue viruses
Disease control
Epitopes - immunology
Fc receptors
Fetal calf serum
Genetic aspects
Genotype & phenotype
Glutamine
Haplorhini
Human diseases
Humans
Identification and classification
Immunity
Immunological research
Infections
Medicine and Health Sciences
Penicillin
Receptors
Research and Analysis Methods
Serogroup
Serotypes
Serum
Streptomycin
Target cells
Tropical diseases
Vaccination
Vaccines
Vector-borne diseases
Vero Cells
Viral antibodies
Viruses
Thailand
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Abstract The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes. Trial Registration: ClinicalTrials.gov NCT02425098 .
AbstractList The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes.
The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes. Trial Registration: ClinicalTrials.gov NCT02425098.
The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes. Trial Registration: ClinicalTrials.gov NCT02425098 . The licensed tetravalent dengue vaccine Dengvaxia is indicated for individuals with previous exposure to dengue. In subjects with no past dengue infection, vaccine trials showed low efficacy against some serotypes and increased risk of severe disease upon post-vaccination infection. The development of tetravalent dengue vaccines has been guided by neutralizing antibodies to each serotype as a measure of safe and effective immunity. However, the absolute level of neutralizing antibodies to each serotype has proven to be an unreliable correlate of protection. Recent studies suggest that a better correlate may be levels of antibodies to epitopes that are unique to each serotype and are independently stimulated by each vaccine component, rather than total quantity of neutralizing antibodies. Here, we mapped the antibody specificity induced by the Takeda tetravalent dengue vaccine TAK-003 in monkeys and humans with no prior immunity to dengue. The vaccine induces high levels of dengue serotype 2 specific neutralizing antibodies that map to known protective epitopes. In contrast, the dengue serotype 1, 3 and 4 specific responses are lower and predominantly consist of cross-reactive antibodies binding to antigenic regions conserved between serotypes. It remains to be determined whether these cross-reactive antibodies, most likely induced by the serotype 2 component, contribute to long-term protection after vaccination.
The ability of some DENV serotype cross-reactive antibodies to promote the entry of heterologous serotypes into Fc receptor-bearing target cells is widely supported as the initiating event that culminates in severe disease [9,10]. There are several DENV vaccines under development, including two live attenuated tetravalent DENV vaccines (TAK-003 developed by Takeda Vaccines Inc. and TV-003 developed by the US National Institutes of Health) currently in phase III clinical trials and one live attenuated tetravalent vaccine, Dengvaxia, developed by Sanofi Pasteur that has been licensed for use in children with pre-existing immunity to DENV [17–19]. Vero cells were maintained in Dulbecco’s modified Eagle’s medium-F12 (DMEM-F12) at 37°C. All growth and maintenance media used were supplemented with 5% fetal bovine serum (FBS), 100 U/mL penicillin, 100 mg/mL streptomycin, 0.1 mM non-essential amino acids (Gibco), and 2 mM glutamine. Source of human serum samples Subjects in the Phase 2 clinical trial DEN-205 were randomly assigned 1:1 to receive a single dose of either TDV or HD- TDV on Day 1 of the trial.
The ability of some DENV serotype cross-reactive antibodies to promote the entry of heterologous serotypes into Fc receptor-bearing target cells is widely supported as the initiating event that culminates in severe disease [9,10]. There are several DENV vaccines under development, including two live attenuated tetravalent DENV vaccines (TAK-003 developed by Takeda Vaccines Inc. and TV-003 developed by the US National Institutes of Health) currently in phase III clinical trials and one live attenuated tetravalent vaccine, Dengvaxia, developed by Sanofi Pasteur that has been licensed for use in children with pre-existing immunity to DENV [17–19]. Vero cells were maintained in Dulbecco’s modified Eagle’s medium-F12 (DMEM-F12) at 37°C. All growth and maintenance media used were supplemented with 5% fetal bovine serum (FBS), 100 U/mL penicillin, 100 mg/mL streptomycin, 0.1 mM non-essential amino acids (Gibco), and 2 mM glutamine. Source of human serum samples Subjects in the Phase 2 clinical trial DEN-205 were randomly assigned 1:1 to receive a single dose of either TDV or HD- TDV on Day 1 of the trial.
The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes. Trial Registration: ClinicalTrials.gov NCT02425098.The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes. Trial Registration: ClinicalTrials.gov NCT02425098.
The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of DENV vaccines is difficult because immunity to a single serotype increases risk of severe disease during a second infection with a new serotype. Leading vaccines are based on tetravalent formulations to induce simultaneous and balanced protective immunity to all 4 serotypes. TAK-003 is a tetravalent live attenuated dengue vaccine candidate developed by Takeda Vaccines Inc, which is currently being evaluated in phase 3 efficacy trials. Here, we use antibody depletion methods and chimeric, epitope transplant DENVs to characterize the specificity of neutralizing antibodies in dengue-naïve adults and non-human primates immunized with TAK-003. Our results demonstrate that TAK-003 induced high levels of DENV2 neutralizing antibodies that recognized unique (type-specific) epitopes on DENV2. In contrast, most vaccinated subjects developed lower levels of DENV1, DENV3 and DENV4 neutralizing antibodies that mainly targeted epitopes that were conserved (cross-reactive) between serotypes. Trial Registration: ClinicalTrials.gov NCT02425098 .
Audience Academic
Author Adams, Elizabeth C.
Stoops, Mark J.
Baric, Ralph S.
White, Laura J.
Henein, Sandra R.
de Silva, Aravinda M.
Young, Ellen F.
AuthorAffiliation La Jolla Institute for Allergy and Immunology, UNITED STATES
2 Department of Epidemiology, The University of North Carolina at Chapel Hill School of Public Health, Chapel Hill, NC, United States of America
1 Department of Microbiology and Immunology, The University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC, United States of America
AuthorAffiliation_xml – name: 1 Department of Microbiology and Immunology, The University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, NC, United States of America
– name: 2 Department of Epidemiology, The University of North Carolina at Chapel Hill School of Public Health, Chapel Hill, NC, United States of America
– name: La Jolla Institute for Allergy and Immunology, UNITED STATES
Author_xml – sequence: 1
  givenname: Laura J.
  orcidid: 0000-0002-1859-4981
  surname: White
  fullname: White, Laura J.
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  orcidid: 0000-0001-6520-0490
  surname: Young
  fullname: Young, Ellen F.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33711074$$D View this record in MEDLINE/PubMed
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Copyright COPYRIGHT 2021 Public Library of Science
2021 White et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2021 White et al 2021 White et al
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– notice: 2021 White et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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DocumentTitleAlternate Unbalanced immunity following tetravalent dengue vaccination
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I have read the journal’s policy and the authors of this manuscript have the following competing interests: RB and AdS have served as consultants for dengue vaccine developers and they are inventors on patents filed by the University of North Carolina at Chapel Hill related to dengue vaccines.
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Snippet The four dengue virus serotypes (DENV1-4) infect several hundred million people each year living in tropical and sub-tropical regions. Clinical development of...
The ability of some DENV serotype cross-reactive antibodies to promote the entry of heterologous serotypes into Fc receptor-bearing target cells is widely...
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SubjectTerms Adult
Amino acids
Animals
Antibodies
Antibodies, Neutralizing - blood
Antibodies, Viral - blood
Antigens
Attenuation
Biology and Life Sciences
Chlorocebus aethiops
Clinical trials
Dengue
Dengue fever
Dengue Vaccines - immunology
Dengue Virus - immunology
Dengue viruses
Disease control
Epitopes - immunology
Fc receptors
Fetal calf serum
Genetic aspects
Genotype & phenotype
Glutamine
Haplorhini
Human diseases
Humans
Identification and classification
Immunity
Immunological research
Infections
Medicine and Health Sciences
Penicillin
Receptors
Research and Analysis Methods
Serogroup
Serotypes
Serum
Streptomycin
Target cells
Tropical diseases
Vaccination
Vaccines
Vector-borne diseases
Vero Cells
Viral antibodies
Viruses
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Title Defining levels of dengue virus serotype-specific neutralizing antibodies induced by a live attenuated tetravalent dengue vaccine (TAK-003)
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