Co-delivery of IOX1 and doxorubicin for antibody-independent cancer chemo-immunotherapy

Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-c...

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Published inNature communications Vol. 12; no. 1; pp. 2425 - 17
Main Authors Liu, Jing, Zhao, Zhihao, Qiu, Nasha, Zhou, Quan, Wang, Guowei, Jiang, Haiping, Piao, Ying, Zhou, Zhuxian, Tang, Jianbin, Shen, Youqing
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 23.04.2021
Nature Publishing Group
Nature Portfolio
Subjects
13/109
13/2
13/21
13/31
14
14/1
14/19
14/63
38/88
38/90
59/5
631/67/1059/2325
631/67/1059/99
631/67/1504/1885
631/67/322
631/67/580
64/60
8-Hydroxyquinoline
82/80
Animals
Antibodies
Antibodies - immunology
Antineoplastic Combined Chemotherapy Protocols - therapeutic use
Apoptosis
B7-H1 Antigen - antagonists & inhibitors
B7-H1 Antigen - immunology
B7-H1 Antigen - metabolism
Cancer
Cell death
Cell Line, Tumor
Cell Survival - drug effects
Cell Survival - immunology
Chemotherapy
Doxorubicin
Doxorubicin - administration & dosage
Doxorubicin - pharmacology
Glycoproteins
HCT116 Cells
Histones
Humanities and Social Sciences
Humans
Hydroxyquinoline
Hydroxyquinolines - administration & dosage
Hydroxyquinolines - chemistry
Hydroxyquinolines - pharmacology
Immune checkpoint
Immunogenicity
Immunological memory
Immunology
Immunosuppressive agents
Immunotherapy
Immunotherapy - methods
Infiltration
Inhibitors
Lung cancer
Lymphocytes
Lymphocytes T
MCF-7 Cells
Metastases
Mice
Mice, Inbred BALB C
Mice, Nude
Mortality
multidisciplinary
Neoplasms - immunology
Neoplasms - metabolism
Neoplasms - therapy
Neoplasms, Experimental - immunology
Neoplasms, Experimental - metabolism
Neoplasms, Experimental - therapy
NIH 3T3 Cells
PD-1 protein
PD-L1 protein
Programmed Cell Death 1 Receptor - antagonists & inhibitors
Programmed Cell Death 1 Receptor - immunology
Programmed Cell Death 1 Receptor - metabolism
Science
Science (multidisciplinary)
T-Lymphocytes - drug effects
T-Lymphocytes - immunology
T-Lymphocytes - metabolism
Tumor Burden - drug effects
Tumor Burden - immunology
Tumors
β-Catenin
Online AccessGet full text

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Abstract Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-carboxy-8-hydroxyquinoline (IOX1), which inhibits tumour histone demethylase Jumonji domain-containing 1A (JMJD1A) and thus downregulates its downstream β-catenin and subsequent PD-L1, providing an antibody-independent paradigm interrupting the PD-1/PD-L1 checkpoint. Synergistically, IOX1 inhibits cancer cells’ P-glycoproteins (P-gp) through the JMJD1A/β-catenin/P-gp pathway and greatly enhances doxorubicin (DOX)-induced immune-stimulatory immunogenic cell death. As a result, the IOX1 and DOX combination greatly promotes T cell infiltration and activity and significantly reduces tumour immunosuppressive factors. Their liposomal combination reduces the growth of various murine tumours, including subcutaneous, orthotopic, and lung metastasis tumours, and offers a long-term immunological memory function against tumour rechallenging. This work provides a small molecule-based potent cancer chemo-immunotherapy. Some chemotherapeutic drugs, such as doxorubicin, induce immunogenic cell death (ICD) and promote anti-tumor immune responses. Here the authors report that the histone demethylase inhibitor 5-carboxy-8-hydroxyquinoline (IOX1) reduces the expression of PD-L1 in cancer cells and enhances doxorubicin-induced ICD, promoting T cell infiltration and reducing tumor growth in preclinical models.
AbstractList Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-carboxy-8-hydroxyquinoline (IOX1), which inhibits tumour histone demethylase Jumonji domain-containing 1A (JMJD1A) and thus downregulates its downstream β-catenin and subsequent PD-L1, providing an antibody-independent paradigm interrupting the PD-1/PD-L1 checkpoint. Synergistically, IOX1 inhibits cancer cells’ P-glycoproteins (P-gp) through the JMJD1A/β-catenin/P-gp pathway and greatly enhances doxorubicin (DOX)-induced immune-stimulatory immunogenic cell death. As a result, the IOX1 and DOX combination greatly promotes T cell infiltration and activity and significantly reduces tumour immunosuppressive factors. Their liposomal combination reduces the growth of various murine tumours, including subcutaneous, orthotopic, and lung metastasis tumours, and offers a long-term immunological memory function against tumour rechallenging. This work provides a small molecule-based potent cancer chemo-immunotherapy. Some chemotherapeutic drugs, such as doxorubicin, induce immunogenic cell death (ICD) and promote anti-tumor immune responses. Here the authors report that the histone demethylase inhibitor 5-carboxy-8-hydroxyquinoline (IOX1) reduces the expression of PD-L1 in cancer cells and enhances doxorubicin-induced ICD, promoting T cell infiltration and reducing tumor growth in preclinical models.
Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-carboxy-8-hydroxyquinoline (IOX1), which inhibits tumour histone demethylase Jumonji domain-containing 1A (JMJD1A) and thus downregulates its downstream β-catenin and subsequent PD-L1, providing an antibody-independent paradigm interrupting the PD-1/PD-L1 checkpoint. Synergistically, IOX1 inhibits cancer cells’ P-glycoproteins (P-gp) through the JMJD1A/β-catenin/P-gp pathway and greatly enhances doxorubicin (DOX)-induced immune-stimulatory immunogenic cell death. As a result, the IOX1 and DOX combination greatly promotes T cell infiltration and activity and significantly reduces tumour immunosuppressive factors. Their liposomal combination reduces the growth of various murine tumours, including subcutaneous, orthotopic, and lung metastasis tumours, and offers a long-term immunological memory function against tumour rechallenging. This work provides a small molecule-based potent cancer chemo-immunotherapy.
Some chemotherapeutic drugs, such as doxorubicin, induce immunogenic cell death (ICD) and promote anti-tumor immune responses. Here the authors report that the histone demethylase inhibitor 5-carboxy-8-hydroxyquinoline (IOX1) reduces the expression of PD-L1 in cancer cells and enhances doxorubicin-induced ICD, promoting T cell infiltration and reducing tumor growth in preclinical models.
Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-carboxy-8-hydroxyquinoline (IOX1), which inhibits tumour histone demethylase Jumonji domain-containing 1A (JMJD1A) and thus downregulates its downstream β-catenin and subsequent PD-L1, providing an antibody-independent paradigm interrupting the PD-1/PD-L1 checkpoint. Synergistically, IOX1 inhibits cancer cells' P-glycoproteins (P-gp) through the JMJD1A/β-catenin/P-gp pathway and greatly enhances doxorubicin (DOX)-induced immune-stimulatory immunogenic cell death. As a result, the IOX1 and DOX combination greatly promotes T cell infiltration and activity and significantly reduces tumour immunosuppressive factors. Their liposomal combination reduces the growth of various murine tumours, including subcutaneous, orthotopic, and lung metastasis tumours, and offers a long-term immunological memory function against tumour rechallenging. This work provides a small molecule-based potent cancer chemo-immunotherapy.Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-carboxy-8-hydroxyquinoline (IOX1), which inhibits tumour histone demethylase Jumonji domain-containing 1A (JMJD1A) and thus downregulates its downstream β-catenin and subsequent PD-L1, providing an antibody-independent paradigm interrupting the PD-1/PD-L1 checkpoint. Synergistically, IOX1 inhibits cancer cells' P-glycoproteins (P-gp) through the JMJD1A/β-catenin/P-gp pathway and greatly enhances doxorubicin (DOX)-induced immune-stimulatory immunogenic cell death. As a result, the IOX1 and DOX combination greatly promotes T cell infiltration and activity and significantly reduces tumour immunosuppressive factors. Their liposomal combination reduces the growth of various murine tumours, including subcutaneous, orthotopic, and lung metastasis tumours, and offers a long-term immunological memory function against tumour rechallenging. This work provides a small molecule-based potent cancer chemo-immunotherapy.
Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune checkpoint, which reverses T cell dysfunction/exhaustion and shows success in treating cancer. Here, we report a histone demethylase inhibitor, 5-carboxy-8-hydroxyquinoline (IOX1), which inhibits tumour histone demethylase Jumonji domain-containing 1A (JMJD1A) and thus downregulates its downstream β-catenin and subsequent PD-L1, providing an antibody-independent paradigm interrupting the PD-1/PD-L1 checkpoint. Synergistically, IOX1 inhibits cancer cells’ P-glycoproteins (P-gp) through the JMJD1A/β-catenin/P-gp pathway and greatly enhances doxorubicin (DOX)-induced immune-stimulatory immunogenic cell death. As a result, the IOX1 and DOX combination greatly promotes T cell infiltration and activity and significantly reduces tumour immunosuppressive factors. Their liposomal combination reduces the growth of various murine tumours, including subcutaneous, orthotopic, and lung metastasis tumours, and offers a long-term immunological memory function against tumour rechallenging. This work provides a small molecule-based potent cancer chemo-immunotherapy.Some chemotherapeutic drugs, such as doxorubicin, induce immunogenic cell death (ICD) and promote anti-tumor immune responses. Here the authors report that the histone demethylase inhibitor 5-carboxy-8-hydroxyquinoline (IOX1) reduces the expression of PD-L1 in cancer cells and enhances doxorubicin-induced ICD, promoting T cell infiltration and reducing tumor growth in preclinical models.
ArticleNumber 2425
Author Zhou, Quan
Liu, Jing
Jiang, Haiping
Qiu, Nasha
Wang, Guowei
Piao, Ying
Shen, Youqing
Zhao, Zhihao
Zhou, Zhuxian
Tang, Jianbin
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  givenname: Zhihao
  surname: Zhao
  fullname: Zhao, Zhihao
  organization: Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou Global Scientific and Technological Innovation Center
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  givenname: Nasha
  surname: Qiu
  fullname: Qiu, Nasha
  organization: Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University
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  givenname: Quan
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  organization: Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University
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  givenname: Haiping
  surname: Jiang
  fullname: Jiang, Haiping
  organization: Department of Medical Oncology, The First Affiliated Hospital, School of Medicine, Zhejiang University
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  givenname: Ying
  surname: Piao
  fullname: Piao, Ying
  organization: Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou Global Scientific and Technological Innovation Center
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  givenname: Zhuxian
  orcidid: 0000-0002-7104-9915
  surname: Zhou
  fullname: Zhou, Zhuxian
  organization: Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou Global Scientific and Technological Innovation Center
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  orcidid: 0000-0003-1837-7976
  surname: Shen
  fullname: Shen, Youqing
  email: shenyq@zju.edu.cn
  organization: Zhejiang Key Laboratory of Smart Biomaterials and Key Laboratory of Biomass Chemical Engineering of Ministry of Education, College of Chemical and Biological Engineering, Zhejiang University, Hangzhou Global Scientific and Technological Innovation Center
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33893275$$D View this record in MEDLINE/PubMed
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  ident: 22407_CR65
  publication-title: Nat. Med.
  doi: 10.1038/nm863
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Snippet Anti-programmed cell death-1 (PD-1)/programmed cell death-ligand 1 (PD-L1) antibodies are currently used in the clinic to interupt the PD-1/PD-L1 immune...
Some chemotherapeutic drugs, such as doxorubicin, induce immunogenic cell death (ICD) and promote anti-tumor immune responses. Here the authors report that the...
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StartPage 2425
SubjectTerms 13/109
13/2
13/21
13/31
14
14/1
14/19
14/63
38/88
38/90
59/5
631/67/1059/2325
631/67/1059/99
631/67/1504/1885
631/67/322
631/67/580
64/60
8-Hydroxyquinoline
82/80
Animals
Antibodies
Antibodies - immunology
Antineoplastic Combined Chemotherapy Protocols - therapeutic use
Apoptosis
B7-H1 Antigen - antagonists & inhibitors
B7-H1 Antigen - immunology
B7-H1 Antigen - metabolism
Cancer
Cell death
Cell Line, Tumor
Cell Survival - drug effects
Cell Survival - immunology
Chemotherapy
Doxorubicin
Doxorubicin - administration & dosage
Doxorubicin - pharmacology
Glycoproteins
HCT116 Cells
Histones
Humanities and Social Sciences
Humans
Hydroxyquinoline
Hydroxyquinolines - administration & dosage
Hydroxyquinolines - chemistry
Hydroxyquinolines - pharmacology
Immune checkpoint
Immunogenicity
Immunological memory
Immunology
Immunosuppressive agents
Immunotherapy
Immunotherapy - methods
Infiltration
Inhibitors
Lung cancer
Lymphocytes
Lymphocytes T
MCF-7 Cells
Metastases
Mice
Mice, Inbred BALB C
Mice, Nude
Mortality
multidisciplinary
Neoplasms - immunology
Neoplasms - metabolism
Neoplasms - therapy
Neoplasms, Experimental - immunology
Neoplasms, Experimental - metabolism
Neoplasms, Experimental - therapy
NIH 3T3 Cells
PD-1 protein
PD-L1 protein
Programmed Cell Death 1 Receptor - antagonists & inhibitors
Programmed Cell Death 1 Receptor - immunology
Programmed Cell Death 1 Receptor - metabolism
Science
Science (multidisciplinary)
T-Lymphocytes - drug effects
T-Lymphocytes - immunology
T-Lymphocytes - metabolism
Tumor Burden - drug effects
Tumor Burden - immunology
Tumors
β-Catenin
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  providerName: Springer Nature
Title Co-delivery of IOX1 and doxorubicin for antibody-independent cancer chemo-immunotherapy
URI https://link.springer.com/article/10.1038/s41467-021-22407-6
https://www.ncbi.nlm.nih.gov/pubmed/33893275
https://www.proquest.com/docview/2517102578
https://www.proquest.com/docview/2518220921
https://pubmed.ncbi.nlm.nih.gov/PMC8065121
https://doaj.org/article/9c13235dc1e945df90f7c6920d76d06e
Volume 12
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