mRNA vaccines against SARS-CoV-2 induce divergent antigen-specific T-cell responses in patients with lung cancer

BackgroundThe severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy...

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Published inJournal for immunotherapy of cancer Vol. 12; no. 1; p. e007922
Main Authors Song, No-Joon, Chakravarthy, Karthik B, Jeon, Hyeongseon, Bolyard, Chelsea, Reynolds, Kelsi, Weller, Kevin P, Reisinger, Sarah, Wang, Yi, Li, Anqi, Jiang, Sizun, Ma, Qin, Barouch, Dan H, Rubinstein, Mark P, Shields, Peter G, Oltz, Eugene M, Chung, Dongjun, Li, Zihai
Format Journal Article
LanguageEnglish
Published England BMJ Publishing Group Ltd 04.01.2024
BMJ Publishing Group LTD
BMJ Publishing Group
SeriesOriginal research
Subjects
Antibodies
Antigens
Cancer therapies
CD4-Positive T-Lymphocytes
CD8-Positive T-Lymphocytes
Cells
Clinical/Translational Cancer Immunotherapy
COVID-19
COVID-19 vaccines
Data analysis
Flow cytometry
Immunotherapy
Infections
Lung cancer
Lymphocytes
mRNA vaccines
Pandemics
Patients
Peptides
Severe acute respiratory syndrome coronavirus 2
Software
CD8-Positive T-Lymphocytes
COVID-19
CD4-Positive T-Lymphocytes
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Abstract BackgroundThe severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy of booster vaccination in patients with late-stage lung cancer on immune-modulating agents including anti-programmed cell death protein 1(PD-1)/programmed death-ligand 1 (PD-L1) has not yet been elucidated.MethodsWe assessed T-cell responses using a modified activation-induced marker assay, coupled with high-dimension flow cytometry analyses. Peripheral blood mononuclear cells (PBMCs) were stimulated with various viral peptides and antigen-specific T-cell responses were evaluated using flow cytometry.ResultsBooster vaccines induced CD8+ T-cell response against the ancestral SARS-CoV-2 strain and Omicron variant in both non-cancer subjects and patients with lung cancer, but only a marginal induction was detected for CD4+ T cells. Importantly, antigen-specific T cells from patients with lung cancer showed distinct subpopulation dynamics with varying degrees of differentiation compared with non-cancer subjects, with evidence of dysfunction. Notably, female-biased T-cell responses were observed.ConclusionWe conclude that patients with lung cancer on immunotherapy show a substantial qualitative deviation from non-cancer subjects in their T-cell response to mRNA vaccines, highlighting the need for heightened protective measures for patients with cancer to minimize the risk of breakthrough infection with the Omicron and other future variants.
AbstractList BackgroundThe severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy of booster vaccination in patients with late-stage lung cancer on immune-modulating agents including anti-programmed cell death protein 1(PD-1)/programmed death-ligand 1 (PD-L1) has not yet been elucidated.MethodsWe assessed T-cell responses using a modified activation-induced marker assay, coupled with high-dimension flow cytometry analyses. Peripheral blood mononuclear cells (PBMCs) were stimulated with various viral peptides and antigen-specific T-cell responses were evaluated using flow cytometry.ResultsBooster vaccines induced CD8+ T-cell response against the ancestral SARS-CoV-2 strain and Omicron variant in both non-cancer subjects and patients with lung cancer, but only a marginal induction was detected for CD4+ T cells. Importantly, antigen-specific T cells from patients with lung cancer showed distinct subpopulation dynamics with varying degrees of differentiation compared with non-cancer subjects, with evidence of dysfunction. Notably, female-biased T-cell responses were observed.ConclusionWe conclude that patients with lung cancer on immunotherapy show a substantial qualitative deviation from non-cancer subjects in their T-cell response to mRNA vaccines, highlighting the need for heightened protective measures for patients with cancer to minimize the risk of breakthrough infection with the Omicron and other future variants.
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy of booster vaccination in patients with late-stage lung cancer on immune-modulating agents including anti-programmed cell death protein 1(PD-1)/programmed death-ligand 1 (PD-L1) has not yet been elucidated.BACKGROUNDThe severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy of booster vaccination in patients with late-stage lung cancer on immune-modulating agents including anti-programmed cell death protein 1(PD-1)/programmed death-ligand 1 (PD-L1) has not yet been elucidated.We assessed T-cell responses using a modified activation-induced marker assay, coupled with high-dimension flow cytometry analyses. Peripheral blood mononuclear cells (PBMCs) were stimulated with various viral peptides and antigen-specific T-cell responses were evaluated using flow cytometry.METHODSWe assessed T-cell responses using a modified activation-induced marker assay, coupled with high-dimension flow cytometry analyses. Peripheral blood mononuclear cells (PBMCs) were stimulated with various viral peptides and antigen-specific T-cell responses were evaluated using flow cytometry.Booster vaccines induced CD8+ T-cell response against the ancestral SARS-CoV-2 strain and Omicron variant in both non-cancer subjects and patients with lung cancer, but only a marginal induction was detected for CD4+ T cells. Importantly, antigen-specific T cells from patients with lung cancer showed distinct subpopulation dynamics with varying degrees of differentiation compared with non-cancer subjects, with evidence of dysfunction. Notably, female-biased T-cell responses were observed.RESULTSBooster vaccines induced CD8+ T-cell response against the ancestral SARS-CoV-2 strain and Omicron variant in both non-cancer subjects and patients with lung cancer, but only a marginal induction was detected for CD4+ T cells. Importantly, antigen-specific T cells from patients with lung cancer showed distinct subpopulation dynamics with varying degrees of differentiation compared with non-cancer subjects, with evidence of dysfunction. Notably, female-biased T-cell responses were observed.We conclude that patients with lung cancer on immunotherapy show a substantial qualitative deviation from non-cancer subjects in their T-cell response to mRNA vaccines, highlighting the need for heightened protective measures for patients with cancer to minimize the risk of breakthrough infection with the Omicron and other future variants.CONCLUSIONWe conclude that patients with lung cancer on immunotherapy show a substantial qualitative deviation from non-cancer subjects in their T-cell response to mRNA vaccines, highlighting the need for heightened protective measures for patients with cancer to minimize the risk of breakthrough infection with the Omicron and other future variants.
Background The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy of booster vaccination in patients with late-stage lung cancer on immune-modulating agents including anti-programmed cell death protein 1(PD-1)/programmed death-ligand 1 (PD-L1) has not yet been elucidated.Methods We assessed T-cell responses using a modified activation-induced marker assay, coupled with high-dimension flow cytometry analyses. Peripheral blood mononuclear cells (PBMCs) were stimulated with various viral peptides and antigen-specific T-cell responses were evaluated using flow cytometry.Results Booster vaccines induced CD8+ T-cell response against the ancestral SARS-CoV-2 strain and Omicron variant in both non-cancer subjects and patients with lung cancer, but only a marginal induction was detected for CD4+ T cells. Importantly, antigen-specific T cells from patients with lung cancer showed distinct subpopulation dynamics with varying degrees of differentiation compared with non-cancer subjects, with evidence of dysfunction. Notably, female-biased T-cell responses were observed.Conclusion We conclude that patients with lung cancer on immunotherapy show a substantial qualitative deviation from non-cancer subjects in their T-cell response to mRNA vaccines, highlighting the need for heightened protective measures for patients with cancer to minimize the risk of breakthrough infection with the Omicron and other future variants.
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA (mRNA) vaccination against ancestral strain spike protein can induce intact T-cell immunity against the Omicron variant, but efficacy of booster vaccination in patients with late-stage lung cancer on immune-modulating agents including anti-programmed cell death protein 1(PD-1)/programmed death-ligand 1 (PD-L1) has not yet been elucidated. We assessed T-cell responses using a modified activation-induced marker assay, coupled with high-dimension flow cytometry analyses. Peripheral blood mononuclear cells (PBMCs) were stimulated with various viral peptides and antigen-specific T-cell responses were evaluated using flow cytometry. Booster vaccines induced CD8 T-cell response against the ancestral SARS-CoV-2 strain and Omicron variant in both non-cancer subjects and patients with lung cancer, but only a marginal induction was detected for CD4 T cells. Importantly, antigen-specific T cells from patients with lung cancer showed distinct subpopulation dynamics with varying degrees of differentiation compared with non-cancer subjects, with evidence of dysfunction. Notably, female-biased T-cell responses were observed. We conclude that patients with lung cancer on immunotherapy show a substantial qualitative deviation from non-cancer subjects in their T-cell response to mRNA vaccines, highlighting the need for heightened protective measures for patients with cancer to minimize the risk of breakthrough infection with the Omicron and other future variants.
Author Chakravarthy, Karthik B
Jeon, Hyeongseon
Jiang, Sizun
Chung, Dongjun
Li, Anqi
Song, No-Joon
Bolyard, Chelsea
Ma, Qin
Li, Zihai
Wang, Yi
Reynolds, Kelsi
Barouch, Dan H
Shields, Peter G
Oltz, Eugene M
Reisinger, Sarah
Weller, Kevin P
Rubinstein, Mark P
AuthorAffiliation 3 The Ohio State University Wexner Medical Center , Columbus , Ohio , USA
1 Pelotonia Institute for Immuno-Oncology , The Ohio State University Comprehensive Cancer Center Arthur G James Cancer Hospital and Richard J Solove Research Institute , Columbus , Ohio , USA
5 Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center , Harvard Medical School , Boston , Massachusetts , USA
6 Division of Medical Oncology, Department of Internal Medicine , The Ohio State University College of Medicine , Columbus , Ohio , USA
2 Department of Biomedical Informatics , The Ohio State University College of Medicine , Columbus , Ohio , USA
4 Department of Pathology , Stanford University , Stanford , California , USA
7 Department of Microbial Infection and Immunity , The Ohio State University , Columbus , Ohio , USA
AuthorAffiliation_xml – name: 1 Pelotonia Institute for Immuno-Oncology , The Ohio State University Comprehensive Cancer Center Arthur G James Cancer Hospital and Richard J Solove Research Institute , Columbus , Ohio , USA
– name: 7 Department of Microbial Infection and Immunity , The Ohio State University , Columbus , Ohio , USA
– name: 5 Center for Virology and Vaccine Research, Beth Israel Deaconess Medical Center , Harvard Medical School , Boston , Massachusetts , USA
– name: 6 Division of Medical Oncology, Department of Internal Medicine , The Ohio State University College of Medicine , Columbus , Ohio , USA
– name: 4 Department of Pathology , Stanford University , Stanford , California , USA
– name: 3 The Ohio State University Wexner Medical Center , Columbus , Ohio , USA
– name: 2 Department of Biomedical Informatics , The Ohio State University College of Medicine , Columbus , Ohio , USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/38177076$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords CD8-Positive T-Lymphocytes
COVID-19
CD4-Positive T-Lymphocytes
Language English
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PublicationTitle Journal for immunotherapy of cancer
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Snippet BackgroundThe severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity....
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity. Messenger RNA...
Background The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Omicron variant is highly transmissible and evades pre-established immunity....
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SubjectTerms Antibodies
Antigens
Cancer therapies
CD4-Positive T-Lymphocytes
CD8-Positive T-Lymphocytes
Cells
Clinical/Translational Cancer Immunotherapy
COVID-19
COVID-19 vaccines
Data analysis
Flow cytometry
Immunotherapy
Infections
Lung cancer
Lymphocytes
mRNA vaccines
Pandemics
Patients
Peptides
Severe acute respiratory syndrome coronavirus 2
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Title mRNA vaccines against SARS-CoV-2 induce divergent antigen-specific T-cell responses in patients with lung cancer
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Volume 12
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