Acetylation-dependent regulation of PD-L1 nuclear translocation dictates the efficacy of anti-PD-1 immunotherapy

Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mech...

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Published inNature cell biology Vol. 22; no. 9; pp. 1064 - 1075
Main Authors Gao, Yang, Nihira, Naoe Taira, Bu, Xia, Chu, Chen, Zhang, Jinfang, Kolodziejczyk, Aleksandra, Fan, Yizeng, Chan, Ngai Ting, Ma, Leina, Liu, Jing, Wang, Dong, Dai, Xiaoming, Liu, Huadong, Ono, Masaya, Nakanishi, Akira, Inuzuka, Hiroyuki, North, Brian J., Huang, Yu-Han, Sharma, Samanta, Geng, Yan, Xu, Wei, Liu, X. Shirley, Li, Lei, Miki, Yoshio, Sicinski, Piotr, Freeman, Gordon J., Wei, Wenyi
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.09.2020
Nature Publishing Group
Subjects
13/1
13/106
13/109
13/31
13/95
14/19
38/23
38/91
631/250/580
631/67/1059/2325
631/80/458/1275
692/699/67
82
82/58
82/83
96
Acetylation
Animals
Apoptosis
B7-H1 Antigen - metabolism
Biomedical and Life Sciences
Cancer Research
Cell Biology
Cell death
Cell Line
Cell Line, Tumor
Cell Nucleus - metabolism
Cellular proteins
CTLA-4 protein
Cytotoxicity
Deacetylation
Developmental Biology
E1A-Associated p300 Protein - metabolism
Endocytosis
Gene expression
Gene Expression - physiology
Genes
HDAC2 protein
Health aspects
HEK293 Cells
Histone deacetylase
Humans
Immune checkpoint
Immune system
Immunotherapy
Immunotherapy - methods
Life Sciences
Localization
Lymphocytes
Lymphocytes T
MCF-7 Cells
Medical research
Medicine, Experimental
Mice
Neoplasms - metabolism
Nuclear transport
PD-1 protein
PD-L1 protein
Programmed Cell Death 1 Receptor - metabolism
Protein Processing, Post-Translational - physiology
Proteins
RAW 264.7 Cells
Stem Cells
Translocation
Translocation (Genetics)
Tumors
United States
Online AccessGet full text

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Abstract Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mechanisms of the immune checkpoint pathways are not completely understood. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interactions with components of the endocytosis and nucleocytoplasmic transport pathways, regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune-response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune-response-related genes and, as a consequence, enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune-response gene expression, and thereby advocate targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade. Gao et al. uncover p300-induced acetylation and HDAC2-mediated deacetylation of PD-L1, which modulate its nuclear translocation to affect the expression of immune genes and the efficacy of anti-PD-1 therapy.
AbstractList Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mechanisms of the immune checkpoint pathways are not completely understood. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interactions with components of the endocytosis and nucleocytoplasmic transport pathways, regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune-response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune-response-related genes and, as a consequence, enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune-response gene expression, and thereby advocate targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade.
Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mechanisms of the immune checkpoint pathways are not completely understood. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interactions with components of the endocytosis and nucleocytoplasmic transport pathways, regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune-response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune-response-related genes and, as a consequence, enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune-response gene expression, and thereby advocate targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade.Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mechanisms of the immune checkpoint pathways are not completely understood. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interactions with components of the endocytosis and nucleocytoplasmic transport pathways, regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune-response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune-response-related genes and, as a consequence, enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune-response gene expression, and thereby advocate targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade.
Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mechanisms of the immune checkpoint pathways are not completely understood. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interactions with components of the endocytosis and nucleocytoplasmic transport pathways, regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune-response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune-response-related genes and, as a consequence, enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune-response gene expression, and thereby advocate targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade. Gao et al. uncover p300-induced acetylation and HDAC2-mediated deacetylation of PD-L1, which modulate its nuclear translocation to affect the expression of immune genes and the efficacy of anti-PD-1 therapy.
Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting that the mechanisms of the immune checkpoint pathways are not completely understood. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interactions with components of the endocytosis and nucleocytoplasmic transport pathways, regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune-response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune-response-related genes and, as a consequence, enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune-response gene expression, and thereby advocate targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade.Gao et al. uncover p300-induced acetylation and HDAC2-mediated deacetylation of PD-L1, which modulate its nuclear translocation to affect the expression of immune genes and the efficacy of anti-PD-1 therapy.
Immunotherapies targeting programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown impressive clinical outcomes for multiple tumours. However, only a subset of patients achieves durable responses, suggesting incompletely understood mechanisms of the immune checkpoint pathways. Here, we report that PD-L1 translocates from the plasma membrane into the nucleus through interaction with components of endocytosis and nucleocytoplasmic transport pathways, which is regulated by p300-mediated acetylation and HDAC2-dependent deacetylation of PD-L1. Moreover, PD-L1 deficiency leads to compromised expression of multiple immune response-related genes. Genetically or pharmacologically modulating PD-L1 acetylation blocks its nuclear translocation, reprograms the expression of immune response-related genes and consequently enhances the anti-tumour response to PD-1 blockade. Thus, our results reveal an acetylation-dependent regulation of PD-L1 nuclear localization that governs immune response gene expression, thereby advocating for targeting PD-L1 translocation to enhance the efficacy of PD-1/PD-L1 blockade.
Audience Academic
Author Sicinski, Piotr
Kolodziejczyk, Aleksandra
Liu, X. Shirley
Inuzuka, Hiroyuki
Wang, Dong
Geng, Yan
Ma, Leina
North, Brian J.
Xu, Wei
Huang, Yu-Han
Miki, Yoshio
Zhang, Jinfang
Bu, Xia
Liu, Huadong
Sharma, Samanta
Chan, Ngai Ting
Nakanishi, Akira
Fan, Yizeng
Liu, Jing
Nihira, Naoe Taira
Chu, Chen
Gao, Yang
Freeman, Gordon J.
Ono, Masaya
Wei, Wenyi
Dai, Xiaoming
Li, Lei
AuthorAffiliation 4 Division of Pediatric Dentistry, Department of Oral Health and Development Sciences, Tohoku University Graduate School of Dentistry, Sendai 980-8575, Japan
7 Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA
12 Division of Genetics and Genomics, Boston Children’s Hospital, Boston, MA 02115, USA
6 Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA
9 Center for Mitochondrial Biology and Medicine, The Key Laboratory of Biomedical Information Engineering of Ministry of Education, School of Life Science and Technology and Frontier Institute of Science and Technology, Xi’an Jiaotong University, Xi’ an, 710049, China
13 Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA
11 Department of Biomedical Informatics, Harvard Medical School, Boston, MA 02215, USA
3 Department of Molecular Genetics, Medical Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, J
AuthorAffiliation_xml – name: 1 Department of Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA 02115, USA
– name: 7 Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA 02115, USA
– name: 6 Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, MA 02215, USA
– name: 10 Department of Clinical Proteomics National Cancer Center Research Institute, Tokyo 104-0045, Japan
– name: 4 Division of Pediatric Dentistry, Department of Oral Health and Development Sciences, Tohoku University Graduate School of Dentistry, Sendai 980-8575, Japan
– name: 12 Division of Genetics and Genomics, Boston Children’s Hospital, Boston, MA 02115, USA
– name: 8 McArdle Laboratory for Cancer Research, University of Wisconsin-Madison, Madison, Wisconsin 53705, USA
– name: 3 Department of Molecular Genetics, Medical Research Institute, Tokyo Medical and Dental University, Tokyo 113-8510, Japan
– name: 14 These authors contributed equally to this work
– name: 2 Department of Urology, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, 710061, China
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  surname: Kolodziejczyk
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  givenname: Yizeng
  surname: Fan
  fullname: Fan, Yizeng
  organization: Department of Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Department of Urology, The First Affiliated Hospital of Xi’an Jiaotong University
– sequence: 8
  givenname: Ngai Ting
  surname: Chan
  fullname: Chan, Ngai Ting
  organization: McArdle Laboratory for Cancer Research, University of Wisconsin-Madison
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  givenname: Leina
  surname: Ma
  fullname: Ma, Leina
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– sequence: 10
  givenname: Jing
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  organization: Department of Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32839551$$D View this record in MEDLINE/PubMed
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Y. Gao, N.T.N. and X.B. designed and performed the experiments with assistance from J.Z., C.C., Y.F., Y-H.H., L.M. A.K., X.D., S.S., Y. Geng, D.W., H.I., B.J.N. and L.L.; N.T.N., M.O., A.N. and J.L. performed the mass spectrometry analysis, A.K., W.X. and N.T.C. did the ChIP experiments; H.L., A.N. and M.O. analyzed the data; C.C and X.S.L helped the bioinformatic analysis. Y.M., P.S., G.J.F. and W.W. guided and supervised the study. N.T.N., Y. Gao, J.Z. and W.W. wrote the manuscript. All authors commented on the manuscript.
Author contributions
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– reference: 32839550 - Nat Cell Biol. 2020 Sep;22(9):1031-1032. doi: 10.1038/s41556-020-0568-y
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Snippet Immunotherapies that target programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have...
Immunotherapies targeting programmed cell death protein 1 (PD-1) and its ligand PD-L1 as well as cytotoxic T-lymphocyte-associated protein 4 (CTLA4) have shown...
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StartPage 1064
SubjectTerms 13/1
13/106
13/109
13/31
13/95
14/19
38/23
38/91
631/250/580
631/67/1059/2325
631/80/458/1275
692/699/67
82
82/58
82/83
96
Acetylation
Animals
Apoptosis
B7-H1 Antigen - metabolism
Biomedical and Life Sciences
Cancer Research
Cell Biology
Cell death
Cell Line
Cell Line, Tumor
Cell Nucleus - metabolism
Cellular proteins
CTLA-4 protein
Cytotoxicity
Deacetylation
Developmental Biology
E1A-Associated p300 Protein - metabolism
Endocytosis
Gene expression
Gene Expression - physiology
Genes
HDAC2 protein
Health aspects
HEK293 Cells
Histone deacetylase
Humans
Immune checkpoint
Immune system
Immunotherapy
Immunotherapy - methods
Life Sciences
Localization
Lymphocytes
Lymphocytes T
MCF-7 Cells
Medical research
Medicine, Experimental
Mice
Neoplasms - metabolism
Nuclear transport
PD-1 protein
PD-L1 protein
Programmed Cell Death 1 Receptor - metabolism
Protein Processing, Post-Translational - physiology
Proteins
RAW 264.7 Cells
Stem Cells
Translocation
Translocation (Genetics)
Tumors
Title Acetylation-dependent regulation of PD-L1 nuclear translocation dictates the efficacy of anti-PD-1 immunotherapy
URI https://link.springer.com/article/10.1038/s41556-020-0562-4
https://www.ncbi.nlm.nih.gov/pubmed/32839551
https://www.proquest.com/docview/2439756064
https://www.proquest.com/docview/2437121228
https://pubmed.ncbi.nlm.nih.gov/PMC7484128
Volume 22
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