Anticancer effects of ikarugamycin and astemizole identified in a screen for stimulators of cellular immune responses.


Journal

Journal for immunotherapy of cancer
ISSN: 2051-1426
Titre abrégé: J Immunother Cancer
Pays: England
ID NLM: 101620585

Informations de publication

Date de publication:
Jul 2023
Historique:
accepted: 21 06 2023
medline: 10 7 2023
pubmed: 8 7 2023
entrez: 7 7 2023
Statut: ppublish

Résumé

Most immunotherapies approved for clinical use rely on the use of recombinant proteins and cell-based approaches, rendering their manufacturing expensive and logistics onerous. The identification of novel small molecule immunotherapeutic agents might overcome such limitations. For immunopharmacological screening campaigns, we built an artificial miniature immune system in which dendritic cells (DCs) derived from immature precursors present MHC (major histocompatibility complex) class I-restricted antigen to a T-cell hybridoma that then secretes interleukin-2 (IL-2). The screening of three drug libraries relevant to known signaling pathways, FDA (Food and Drug Administration)-approved drugs and neuroendocrine factors yielded two major hits, astemizole and ikarugamycin. Mechanistically, ikarugamycin turned out to act on DCs to inhibit hexokinase 2, hence stimulating their antigen presenting potential. In contrast, astemizole acts as a histamine H1 receptor (H1R1) antagonist to activate T cells in a non-specific, DC-independent fashion. Astemizole induced the production of IL-2 and interferon-γ (IFN-γ) by CD4 These findings underscore the potential utility of this screening system for the identification of immunostimulatory drugs with anticancer effects.

Sections du résumé

BACKGROUND BACKGROUND
Most immunotherapies approved for clinical use rely on the use of recombinant proteins and cell-based approaches, rendering their manufacturing expensive and logistics onerous. The identification of novel small molecule immunotherapeutic agents might overcome such limitations.
METHOD METHODS
For immunopharmacological screening campaigns, we built an artificial miniature immune system in which dendritic cells (DCs) derived from immature precursors present MHC (major histocompatibility complex) class I-restricted antigen to a T-cell hybridoma that then secretes interleukin-2 (IL-2).
RESULTS RESULTS
The screening of three drug libraries relevant to known signaling pathways, FDA (Food and Drug Administration)-approved drugs and neuroendocrine factors yielded two major hits, astemizole and ikarugamycin. Mechanistically, ikarugamycin turned out to act on DCs to inhibit hexokinase 2, hence stimulating their antigen presenting potential. In contrast, astemizole acts as a histamine H1 receptor (H1R1) antagonist to activate T cells in a non-specific, DC-independent fashion. Astemizole induced the production of IL-2 and interferon-γ (IFN-γ) by CD4
CONCLUSIONS CONCLUSIONS
These findings underscore the potential utility of this screening system for the identification of immunostimulatory drugs with anticancer effects.

Identifiants

pubmed: 37419511
pii: jitc-2023-006785
doi: 10.1136/jitc-2023-006785
pmc: PMC10347457
pii:
doi:

Substances chimiques

Interleukin-2 0
Astemizole 7HU6337315
ikarugamycin 36531-78-9
Oxaliplatin 04ZR38536J
Histocompatibility Antigens Class I 0
Interferon-gamma 82115-62-6

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : European Research Council
ID : 101052444
Pays : International

Informations de copyright

© Author(s) (or their employer(s)) 2023. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Déclaration de conflit d'intérêts

Competing interests: OK is a co-founder of Samsara Therapeutics. GK has been holding research contracts with Daiichi Sankyo, Eleor, Kaleido, Lytix Pharma, PharmaMar, Osasuna Therapeutics, Samsara Therapeutics, Sanofi, Tollys, and Vascage. GK has been consulting for Reithera. GK is on the Board of Directors of the Bristol Myers Squibb Foundation France. GK is a scientific co-founder of everImmune, Osasuna Therapeutics, Samsara Therapeutics and Therafast Bio. GK is the inventor of patents covering therapeutic targeting of aging, cancer, cystic fibrosis and metabolic disorders. GK’s wife, Laurence Zitvogel, has held research contracts with 9 Meters Biopharma, Daiichi Sankyo, Pilege, was on the Board of Directors of Transgene, is a co-founder of everImmune, and holds patents covering the treatment of cancer and the therapeutic manipulation of the microbiota. GK’s brother, Romano Kroemer, was an employee of Sanofi and now consults for Boehringer-Ingelheim.

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Auteurs

Shuai Zhang (S)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.
Department of Respiratory and Critical Care Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.
Faculté de Médecine, Université de Paris Saclay, Kremlin Bicêtre, France.

Liwei Zhao (L)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.

Mengfei Guo (M)

Department of Respiratory and Critical Care Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.

Peng Liu (P)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.

Sijing Li (S)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.
Faculté de Médecine, Université de Paris Saclay, Kremlin Bicêtre, France.

Wei Xie (W)

Cell death and Inflammation Unit, VIB-UGent Center for Inflammation Research, Ghent, Belgium.
Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium.

Ai-Ling Tian (AL)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.

Jonathan G Pol (JG)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.

Hui Chen (H)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.
Faculté de Médecine, Université de Paris Saclay, Kremlin Bicêtre, France.

Hui Pan (H)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.
Faculté de Médecine, Université de Paris Saclay, Kremlin Bicêtre, France.

Misha Mao (M)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.
Faculté de Médecine, Université de Paris Saclay, Kremlin Bicêtre, France.
Surgical Oncology Department, Sir Run Run Shaw Hospital, Zhejiang University, Hangzhou, Zhejiang, China.

Yumei Li (Y)

Department of Respiratory and Critical Care Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.

Laurence Zitvogel (L)

INSERM U1015, Equipe labellisée par la Ligue contre le cancer, Gustave Roussy, Villjuif, France.
ClinicObiome, Gustave-Roussy, Villejuif, France.

Yang Jin (Y)

Department of Respiratory and Critical Care Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China captain.olsen@gmail.com kroemer@orange.fr whuhjy@126.com.

Oliver Kepp (O)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France captain.olsen@gmail.com kroemer@orange.fr whuhjy@126.com.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.

Guido Kroemer (G)

Metabolomics and Cell Biology Platforms, Gustave Roussy, Villejuif, France captain.olsen@gmail.com kroemer@orange.fr whuhjy@126.com.
Centre de Recherche des Cordeliers, Equipe labellisée par la Ligue contre le cancer, Université Paris Cité, Sorbonne Université, Inserm U1138, Institut Universitaire de France, Paris, France.
Institut du Cancer Paris CARPEM, Department of Biology, Hôpital Européen Georges Pompidou, AP-HP, Paris, France.

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