Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression

During solid tumor progression, the tumor microenvironment (TME) evolves into a highly immunosuppressive milieu. Key players in the immunosuppressive environment are regulatory myeloid cells, including myeloid-derived suppressor cells (MDSCs) and tumor-associated macrophages (TAMs), which are recrui...

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Main Authors: Iris Wyrobnik, Miryam Steinberg, Anat Gelfand, Ronen Rosenblum, Yara Eid Mutlak, Liron Sulimani, Shiri Procaccia, Yishai Ofran, Hila Novak-Kotzer, David Meiri
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Language:English
Published: Taylor & Francis Group 2023-12-01
Series:OncoImmunology
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Online Access:https://www.tandfonline.com/doi/10.1080/2162402X.2023.2219164
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author Iris Wyrobnik
Miryam Steinberg
Anat Gelfand
Ronen Rosenblum
Yara Eid Mutlak
Liron Sulimani
Shiri Procaccia
Yishai Ofran
Hila Novak-Kotzer
David Meiri
author_facet Iris Wyrobnik
Miryam Steinberg
Anat Gelfand
Ronen Rosenblum
Yara Eid Mutlak
Liron Sulimani
Shiri Procaccia
Yishai Ofran
Hila Novak-Kotzer
David Meiri
author_sort Iris Wyrobnik
collection DOAJ
description During solid tumor progression, the tumor microenvironment (TME) evolves into a highly immunosuppressive milieu. Key players in the immunosuppressive environment are regulatory myeloid cells, including myeloid-derived suppressor cells (MDSCs) and tumor-associated macrophages (TAMs), which are recruited and activated via tumor-secreted cytokines such as colony-stimulating factor 1 (CSF-1). Therefore, the depletion of tumor-secreted cytokines is a leading anticancer strategy. Here, we found that CSF-1 secretion by melanoma cells is decreased following treatment with Cannabis extracts. Cannabigerol (CBG) was identified as the bioactive cannabinoid responsible for the effects. Conditioned media from cells treated with pure CBG or the high-CBG extract reduced the expansion and macrophage transition of the monocytic-MDSC subpopulation. Treated MO-MDSCs also expressed lower levels of iNOS, leading to restored CD8+ T-cell activation. Tumor-bearing mice treated with CBG presented reduced tumor progression, lower TAM frequencies and reduced TAM/M1 ratio. A combination of CBG and αPD-L1 was more effective in reducing tumor progression, enhancing survival and increasing the infiltration of activated cytotoxic T-cells than each treatment separately. We show a novel mechanism for CBG in modulating the TME and enhancing immune checkpoint blockade therapy, underlining its promising therapeutic potential for the treatment of a variety of tumors with elevated CSF-1 expression.
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spelling doaj-art-39ec33dd04e2407db267ecc7cf92338a2025-08-20T02:01:29ZengTaylor & Francis GroupOncoImmunology2162-402X2023-12-0112110.1080/2162402X.2023.2219164Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progressionIris Wyrobnik0Miryam Steinberg1Anat Gelfand2Ronen Rosenblum3Yara Eid Mutlak4Liron Sulimani5Shiri Procaccia6Yishai Ofran7Hila Novak-Kotzer8David Meiri9The Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Kleifeld Laboratory, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelDepartment of Hematology, Shaare Zedek Medical Center and Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelThe Laboratory of Cancer Biology and Cannabinoid Research, Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelDuring solid tumor progression, the tumor microenvironment (TME) evolves into a highly immunosuppressive milieu. Key players in the immunosuppressive environment are regulatory myeloid cells, including myeloid-derived suppressor cells (MDSCs) and tumor-associated macrophages (TAMs), which are recruited and activated via tumor-secreted cytokines such as colony-stimulating factor 1 (CSF-1). Therefore, the depletion of tumor-secreted cytokines is a leading anticancer strategy. Here, we found that CSF-1 secretion by melanoma cells is decreased following treatment with Cannabis extracts. Cannabigerol (CBG) was identified as the bioactive cannabinoid responsible for the effects. Conditioned media from cells treated with pure CBG or the high-CBG extract reduced the expansion and macrophage transition of the monocytic-MDSC subpopulation. Treated MO-MDSCs also expressed lower levels of iNOS, leading to restored CD8+ T-cell activation. Tumor-bearing mice treated with CBG presented reduced tumor progression, lower TAM frequencies and reduced TAM/M1 ratio. A combination of CBG and αPD-L1 was more effective in reducing tumor progression, enhancing survival and increasing the infiltration of activated cytotoxic T-cells than each treatment separately. We show a novel mechanism for CBG in modulating the TME and enhancing immune checkpoint blockade therapy, underlining its promising therapeutic potential for the treatment of a variety of tumors with elevated CSF-1 expression.https://www.tandfonline.com/doi/10.1080/2162402X.2023.2219164Tumor MicroenvironmentRegulatory Myeloid CellsCSF-1 (M-CSF)MDSCTAMCannabis
spellingShingle Iris Wyrobnik
Miryam Steinberg
Anat Gelfand
Ronen Rosenblum
Yara Eid Mutlak
Liron Sulimani
Shiri Procaccia
Yishai Ofran
Hila Novak-Kotzer
David Meiri
Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
OncoImmunology
Tumor Microenvironment
Regulatory Myeloid Cells
CSF-1 (M-CSF)
MDSC
TAM
Cannabis
title Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
title_full Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
title_fullStr Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
title_full_unstemmed Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
title_short Decreased melanoma CSF-1 secretion by Cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
title_sort decreased melanoma csf 1 secretion by cannabigerol treatment reprograms regulatory myeloid cells and reduces tumor progression
topic Tumor Microenvironment
Regulatory Myeloid Cells
CSF-1 (M-CSF)
MDSC
TAM
Cannabis
url https://www.tandfonline.com/doi/10.1080/2162402X.2023.2219164
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