The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies

Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1 + CD8 + T cells relative to that of PD-1 + regulatory T...

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Published inNature immunology Vol. 21; no. 11; pp. 1346 - 1358
Main Authors Kumagai, Shogo, Togashi, Yosuke, Kamada, Takahiro, Sugiyama, Eri, Nishinakamura, Hitomi, Takeuchi, Yoshiko, Vitaly, Kochin, Itahashi, Kota, Maeda, Yuka, Matsui, Shigeyuki, Shibahara, Takuma, Yamashita, Yasuho, Irie, Takuma, Tsuge, Ayaka, Fukuoka, Shota, Kawazoe, Akihito, Udagawa, Hibiki, Kirita, Keisuke, Aokage, Keiju, Ishii, Genichiro, Kuwata, Takeshi, Nakama, Kenta, Kawazu, Masahito, Ueno, Toshihide, Yamazaki, Naoya, Goto, Koichi, Tsuboi, Masahiro, Mano, Hiroyuki, Doi, Toshihiko, Shitara, Kohei, Nishikawa, Hiroyoshi
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.11.2020
Nature Publishing Group
Subjects
631/250/580
631/67/580
Antigens - chemistry
Antigens - immunology
Apoptosis
Biomarkers
Biomarkers, Tumor
Biomedical and Life Sciences
Biomedicine
CD28 Antigens - metabolism
CD8 antigen
CD8-Positive T-Lymphocytes - immunology
CD8-Positive T-Lymphocytes - metabolism
Cell death
Cellular proteins
Effector cells
Enzymes
Gene expression
Gene Expression Regulation - drug effects
Genetic aspects
Health aspects
Humans
Immune checkpoint
Immune Checkpoint Inhibitors - pharmacology
Immune Checkpoint Inhibitors - therapeutic use
Immunology
Immunomodulation
Immunoregulation
Immunosuppression
Immunotherapy
Infectious Diseases
Lymphocyte Activation - immunology
Lymphocytes
Lymphocytes T
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - metabolism
Molecular Targeted Therapy
Neoplasm Metastasis
Neoplasm Staging
Neoplasms - drug therapy
Neoplasms - etiology
Neoplasms - metabolism
Neoplasms - mortality
PD-1 protein
PD-L1 protein
Peptides - chemistry
Peptides - immunology
Prognosis
Programmed Cell Death 1 Receptor - antagonists & inhibitors
Programmed Cell Death 1 Receptor - genetics
Programmed Cell Death 1 Receptor - metabolism
Reactive Oxygen Species - metabolism
Receptors, Antigen, T-Cell - metabolism
Regulation
Signal Transduction
T-Lymphocytes, Regulatory - drug effects
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - metabolism
Treatment Outcome
Tumor microenvironment
Tumor Microenvironment - immunology
Tumors
Japan
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Abstract Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1 + CD8 + T cells relative to that of PD-1 + regulatory T (T reg ) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8 + T cells and T reg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1 + CD8 + T cells and enhanced PD-1 + T reg cell–mediated immunosuppression. A profound reactivation of effector PD-1 + CD8 + T cells rather than PD-1 + T reg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies. Checkpoint blockade is effective in only a subset of patients; therefore, biomarkers that can predict efficacy would be clinically highly valuable. Nishkawa and colleagues develop a biomarker based on PD-1 positivity of effector and regulatory T cells in the tumor microenvironment that accurately predicts the effectiveness of checkpoint blockade in patients.
AbstractList Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1 + CD8 + T cells relative to that of PD-1 + regulatory T (T reg ) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8 + T cells and T reg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1 + CD8 + T cells and enhanced PD-1 + T reg cell–mediated immunosuppression. A profound reactivation of effector PD-1 + CD8 + T cells rather than PD-1 + T reg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies. Checkpoint blockade is effective in only a subset of patients; therefore, biomarkers that can predict efficacy would be clinically highly valuable. Nishkawa and colleagues develop a biomarker based on PD-1 positivity of effector and regulatory T cells in the tumor microenvironment that accurately predicts the effectiveness of checkpoint blockade in patients.
Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1+CD8+ T cells relative to that of PD-1+ regulatory T (Treg) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8+ T cells and Treg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1+CD8+ T cells and enhanced PD-1+ Treg cell–mediated immunosuppression. A profound reactivation of effector PD-1+CD8+ T cells rather than PD-1+ Treg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies.Checkpoint blockade is effective in only a subset of patients; therefore, biomarkers that can predict efficacy would be clinically highly valuable. Nishkawa and colleagues develop a biomarker based on PD-1 positivity of effector and regulatory T cells in the tumor microenvironment that accurately predicts the effectiveness of checkpoint blockade in patients.
Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1+CD8+ T cells relative to that of PD-1+ regulatory T (Treg) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8+ T cells and Treg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1+CD8+ T cells and enhanced PD-1+ Treg cell-mediated immunosuppression. A profound reactivation of effector PD-1+CD8+ T cells rather than PD-1+ Treg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies.Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1+CD8+ T cells relative to that of PD-1+ regulatory T (Treg) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8+ T cells and Treg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1+CD8+ T cells and enhanced PD-1+ Treg cell-mediated immunosuppression. A profound reactivation of effector PD-1+CD8+ T cells rather than PD-1+ Treg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies.
Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1.sup.+CD8.sup.+ T cells relative to that of PD-1.sup.+ regulatory T (T.sub.reg) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8.sup.+ T cells and T.sub.reg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1.sup.+CD8.sup.+ T cells and enhanced PD-1.sup.+ T.sub.reg cell-mediated immunosuppression. A profound reactivation of effector PD-1.sup.+CD8.sup.+ T cells rather than PD-1.sup.+ T.sub.reg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies. Checkpoint blockade is effective in only a subset of patients; therefore, biomarkers that can predict efficacy would be clinically highly valuable. Nishkawa and colleagues develop a biomarker based on PD-1 positivity of effector and regulatory T cells in the tumor microenvironment that accurately predicts the effectiveness of checkpoint blockade in patients.
Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1 CD8 T cells relative to that of PD-1 regulatory T (T ) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8 T cells and T cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1 CD8 T cells and enhanced PD-1 T cell-mediated immunosuppression. A profound reactivation of effector PD-1 CD8 T cells rather than PD-1 T cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies.
Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive of clinical efficacy are urgently required. Here, we show that the frequency of PD-1.sup.+CD8.sup.+ T cells relative to that of PD-1.sup.+ regulatory T (T.sub.reg) cells in the tumor microenvironment can predict the clinical efficacy of programmed cell death protein 1 (PD-1) blockade therapies and is superior to other predictors, including PD ligand 1 (PD-L1) expression or tumor mutational burden. PD-1 expression by CD8.sup.+ T cells and T.sub.reg cells negatively impacts effector and immunosuppressive functions, respectively. PD-1 blockade induces both recovery of dysfunctional PD-1.sup.+CD8.sup.+ T cells and enhanced PD-1.sup.+ T.sub.reg cell-mediated immunosuppression. A profound reactivation of effector PD-1.sup.+CD8.sup.+ T cells rather than PD-1.sup.+ T.sub.reg cells by PD-1 blockade is necessary for tumor regression. These findings provide a promising predictive biomarker for PD-1 blockade therapies.
Audience Academic
Author Itahashi, Kota
Kawazoe, Akihito
Togashi, Yosuke
Nishinakamura, Hitomi
Fukuoka, Shota
Kuwata, Takeshi
Kirita, Keisuke
Nakama, Kenta
Sugiyama, Eri
Tsuboi, Masahiro
Shibahara, Takuma
Doi, Toshihiko
Takeuchi, Yoshiko
Yamashita, Yasuho
Kumagai, Shogo
Udagawa, Hibiki
Aokage, Keiju
Matsui, Shigeyuki
Kawazu, Masahito
Irie, Takuma
Maeda, Yuka
Mano, Hiroyuki
Shitara, Kohei
Tsuge, Ayaka
Ueno, Toshihide
Goto, Koichi
Vitaly, Kochin
Kamada, Takahiro
Yamazaki, Naoya
Nishikawa, Hiroyoshi
Ishii, Genichiro
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/32868929$$D View this record in MEDLINE/PubMed
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Snippet Immune checkpoint blockade has provided a paradigm shift in cancer therapy, but the success of this approach is very variable; therefore, biomarkers predictive...
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SubjectTerms 631/250/580
631/67/580
Antigens - chemistry
Antigens - immunology
Apoptosis
Biomarkers
Biomarkers, Tumor
Biomedical and Life Sciences
Biomedicine
CD28 Antigens - metabolism
CD8 antigen
CD8-Positive T-Lymphocytes - immunology
CD8-Positive T-Lymphocytes - metabolism
Cell death
Cellular proteins
Effector cells
Enzymes
Gene expression
Gene Expression Regulation - drug effects
Genetic aspects
Health aspects
Humans
Immune checkpoint
Immune Checkpoint Inhibitors - pharmacology
Immune Checkpoint Inhibitors - therapeutic use
Immunology
Immunomodulation
Immunoregulation
Immunosuppression
Immunotherapy
Infectious Diseases
Lymphocyte Activation - immunology
Lymphocytes
Lymphocytes T
Lymphocytes, Tumor-Infiltrating - immunology
Lymphocytes, Tumor-Infiltrating - metabolism
Molecular Targeted Therapy
Neoplasm Metastasis
Neoplasm Staging
Neoplasms - drug therapy
Neoplasms - etiology
Neoplasms - metabolism
Neoplasms - mortality
PD-1 protein
PD-L1 protein
Peptides - chemistry
Peptides - immunology
Prognosis
Programmed Cell Death 1 Receptor - antagonists & inhibitors
Programmed Cell Death 1 Receptor - genetics
Programmed Cell Death 1 Receptor - metabolism
Reactive Oxygen Species - metabolism
Receptors, Antigen, T-Cell - metabolism
Regulation
Signal Transduction
T-Lymphocytes, Regulatory - drug effects
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - metabolism
Treatment Outcome
Tumor microenvironment
Tumor Microenvironment - immunology
Tumors
Title The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies
URI https://link.springer.com/article/10.1038/s41590-020-0769-3
https://www.ncbi.nlm.nih.gov/pubmed/32868929
https://www.proquest.com/docview/2475061487
https://www.proquest.com/docview/2439624212
Volume 21
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