Specific cannabinoids revive adaptive immunity by reversing immune evasion mechanisms in metastatic tumours
Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through s...
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| Published in | Frontiers in immunology Vol. 13; p. 982082 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Media S.A
22.02.2023
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 1664-3224 1664-3224 |
| DOI | 10.3389/fimmu.2022.982082 |
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| Abstract | Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through several mechanisms; one of the most frequently observed involves the loss of expression or mutation of genes composing the MHC-I antigen presentation machinery (APM) that yields tumours invisible to Cytotoxic T lymphocytes, the key component of the adaptive cellular immune response. Fascinating ethnographic and experimental findings indicate that cannabinoids inhibit the growth and progression of several categories of cancer; however, the mechanisms underlying these observations remain clouded in uncertainty. Here, we screened a library of cannabinoid compounds and found molecular selectivity amongst specific cannabinoids, where related molecules such as Δ9-tetrahydrocannabinol, cannabidiol, and cannabigerol can reverse the metastatic immune escape phenotype
in vitro
by inducing MHC-I cell surface expression in a wide variety of metastatic tumours that subsequently sensitizing tumours to T lymphocyte recognition. Remarkably, H3K27Ac ChIPseq analysis established that cannabigerol and gamma interferon induce overlapping epigenetic signatures and key gene pathways in metastatic tumours related to cellular senescence, as well as APM genes involved in revealing metastatic tumours to the adaptive immune response. Overall, the data suggest that specific cannabinoids may have utility in cancer immunotherapy regimens by overcoming immune escape and augmenting cancer immune surveillance in metastatic disease. Finally, the fundamental discovery of the ability of cannabinoids to alter epigenetic programs may help elucidate many of the pleiotropic medicinal effects of cannabinoids on human physiology. |
|---|---|
| AbstractList | Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through several mechanisms; one of the most frequently observed involves the loss of expression or mutation of genes composing the MHC-I antigen presentation machinery (APM) that yields tumours invisible to Cytotoxic T lymphocytes, the key component of the adaptive cellular immune response. Fascinating ethnographic and experimental findings indicate that cannabinoids inhibit the growth and progression of several categories of cancer; however, the mechanisms underlying these observations remain clouded in uncertainty. Here, we screened a library of cannabinoid compounds and found molecular selectivity amongst specific cannabinoids, where related molecules such as Δ9-tetrahydrocannabinol, cannabidiol, and cannabigerol can reverse the metastatic immune escape phenotype
in vitro
by inducing MHC-I cell surface expression in a wide variety of metastatic tumours that subsequently sensitizing tumours to T lymphocyte recognition. Remarkably, H3K27Ac ChIPseq analysis established that cannabigerol and gamma interferon induce overlapping epigenetic signatures and key gene pathways in metastatic tumours related to cellular senescence, as well as APM genes involved in revealing metastatic tumours to the adaptive immune response. Overall, the data suggest that specific cannabinoids may have utility in cancer immunotherapy regimens by overcoming immune escape and augmenting cancer immune surveillance in metastatic disease. Finally, the fundamental discovery of the ability of cannabinoids to alter epigenetic programs may help elucidate many of the pleiotropic medicinal effects of cannabinoids on human physiology. Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through several mechanisms; one of the most frequently observed involves the loss of expression or mutation of genes composing the MHC-I antigen presentation machinery (APM) that yields tumours invisible to Cytotoxic T lymphocytes, the key component of the adaptive cellular immune response. Fascinating ethnographic and experimental findings indicate that cannabinoids inhibit the growth and progression of several categories of cancer; however, the mechanisms underlying these observations remain clouded in uncertainty. Here, we screened a library of cannabinoid compounds and found molecular selectivity amongst specific cannabinoids, where related molecules such as Δ9-tetrahydrocannabinol, cannabidiol, and cannabigerol can reverse the metastatic immune escape phenotype in vitro by inducing MHC-I cell surface expression in a wide variety of metastatic tumours that subsequently sensitizing tumours to T lymphocyte recognition. Remarkably, H3K27Ac ChIPseq analysis established that cannabigerol and gamma interferon induce overlapping epigenetic signatures and key gene pathways in metastatic tumours related to cellular senescence, as well as APM genes involved in revealing metastatic tumours to the adaptive immune response. Overall, the data suggest that specific cannabinoids may have utility in cancer immunotherapy regimens by overcoming immune escape and augmenting cancer immune surveillance in metastatic disease. Finally, the fundamental discovery of the ability of cannabinoids to alter epigenetic programs may help elucidate many of the pleiotropic medicinal effects of cannabinoids on human physiology.Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through several mechanisms; one of the most frequently observed involves the loss of expression or mutation of genes composing the MHC-I antigen presentation machinery (APM) that yields tumours invisible to Cytotoxic T lymphocytes, the key component of the adaptive cellular immune response. Fascinating ethnographic and experimental findings indicate that cannabinoids inhibit the growth and progression of several categories of cancer; however, the mechanisms underlying these observations remain clouded in uncertainty. Here, we screened a library of cannabinoid compounds and found molecular selectivity amongst specific cannabinoids, where related molecules such as Δ9-tetrahydrocannabinol, cannabidiol, and cannabigerol can reverse the metastatic immune escape phenotype in vitro by inducing MHC-I cell surface expression in a wide variety of metastatic tumours that subsequently sensitizing tumours to T lymphocyte recognition. Remarkably, H3K27Ac ChIPseq analysis established that cannabigerol and gamma interferon induce overlapping epigenetic signatures and key gene pathways in metastatic tumours related to cellular senescence, as well as APM genes involved in revealing metastatic tumours to the adaptive immune response. Overall, the data suggest that specific cannabinoids may have utility in cancer immunotherapy regimens by overcoming immune escape and augmenting cancer immune surveillance in metastatic disease. Finally, the fundamental discovery of the ability of cannabinoids to alter epigenetic programs may help elucidate many of the pleiotropic medicinal effects of cannabinoids on human physiology. Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through several mechanisms; one of the most frequently observed involves the loss of expression or mutation of genes composing the MHC-I antigen presentation machinery (APM) that yields tumours invisible to Cytotoxic T lymphocytes, the key component of the adaptive cellular immune response. Fascinating ethnographic and experimental findings indicate that cannabinoids inhibit the growth and progression of several categories of cancer; however, the mechanisms underlying these observations remain clouded in uncertainty. Here, we screened a library of cannabinoid compounds and found molecular selectivity amongst specific cannabinoids, where related molecules such as Δ9-tetrahydrocannabinol, cannabidiol, and cannabigerol can reverse the metastatic immune escape phenotype by inducing MHC-I cell surface expression in a wide variety of metastatic tumours that subsequently sensitizing tumours to T lymphocyte recognition. Remarkably, H3K27Ac ChIPseq analysis established that cannabigerol and gamma interferon induce overlapping epigenetic signatures and key gene pathways in metastatic tumours related to cellular senescence, as well as APM genes involved in revealing metastatic tumours to the adaptive immune response. Overall, the data suggest that specific cannabinoids may have utility in cancer immunotherapy regimens by overcoming immune escape and augmenting cancer immune surveillance in metastatic disease. Finally, the fundamental discovery of the ability of cannabinoids to alter epigenetic programs may help elucidate many of the pleiotropic medicinal effects of cannabinoids on human physiology. Emerging cancers are sculpted by neo-Darwinian selection for superior growth and survival but minimal immunogenicity; consequently, metastatic cancers often evolve common genetic and epigenetic signatures to elude immune surveillance. Immune subversion by metastatic tumours can be achieved through several mechanisms; one of the most frequently observed involves the loss of expression or mutation of genes composing the MHC-I antigen presentation machinery (APM) that yields tumours invisible to Cytotoxic T lymphocytes, the key component of the adaptive cellular immune response. Fascinating ethnographic and experimental findings indicate that cannabinoids inhibit the growth and progression of several categories of cancer; however, the mechanisms underlying these observations remain clouded in uncertainty. Here, we screened a library of cannabinoid compounds and found molecular selectivity amongst specific cannabinoids, where related molecules such as Δ9-tetrahydrocannabinol, cannabidiol, and cannabigerol can reverse the metastatic immune escape phenotype in vitro by inducing MHC-I cell surface expression in a wide variety of metastatic tumours that subsequently sensitizing tumours to T lymphocyte recognition. Remarkably, H3K27Ac ChIPseq analysis established that cannabigerol and gamma interferon induce overlapping epigenetic signatures and key gene pathways in metastatic tumours related to cellular senescence, as well as APM genes involved in revealing metastatic tumours to the adaptive immune response. Overall, the data suggest that specific cannabinoids may have utility in cancer immunotherapy regimens by overcoming immune escape and augmenting cancer immune surveillance in metastatic disease. Finally, the fundamental discovery of the ability of cannabinoids to alter epigenetic programs may help elucidate many of the pleiotropic medicinal effects of cannabinoids on human physiology. |
| Author | Pfeifer, Cheryl G. Andersen, Raymond J. Eyford, Brett A. Jefferies, Wilfred A. Nohara, Lilian L. Garcia, Nicolas H. Munro, Lonna Wood, Christi Gray, Patrick W. Tjoelker, Larry Dada, Sarah Saranchova, Iryna Garrovillas, Emmanuel Al Haddad, Eliana Morova, Tunc Dreier, Carola Kari, Suresh Ellis, Samantha L. S. Lack, Nathan A. Caspani, Giorgia |
| AuthorAffiliation | 12 Department of Urological Science, University of British Columbia , Vancouver, BC , Canada 11 Department of Zoology, University of British Columbia , Vancouver, BC , Canada 5 Department of Microbiology and Immunology, University of British Columbia , Vancouver, BC , Canada 10 Department of Chemistry, University of British Columbia , Vancouver, BC , Canada 8 Pascal Biosciences , Seattle, WA , United States 7 Biotechnology - Biomedical Science and Technology (BST), University of Applied Sciences , Mannheim , Germany 6 Department of Medical Genetics, University of British Columbia , Vancouver, BC , Canada 9 School of Medicine, Koç University , Istanbul , Türkiye 4 The Djavad Mowafaghian Centre for Brain Health, University of British Columbia , Vancouver, BC , Canada 2 Vancouver Prostate Centre, Vancouver Coastal Health Research Institute , Vancouver, BC , Canada 3 Centre for Blood Research, University of British Columbia , Vancouver, BC , Canada 1 Michael Smith Laboratories, University of British |
| AuthorAffiliation_xml | – name: 8 Pascal Biosciences , Seattle, WA , United States – name: 2 Vancouver Prostate Centre, Vancouver Coastal Health Research Institute , Vancouver, BC , Canada – name: 10 Department of Chemistry, University of British Columbia , Vancouver, BC , Canada – name: 12 Department of Urological Science, University of British Columbia , Vancouver, BC , Canada – name: 4 The Djavad Mowafaghian Centre for Brain Health, University of British Columbia , Vancouver, BC , Canada – name: 3 Centre for Blood Research, University of British Columbia , Vancouver, BC , Canada – name: 7 Biotechnology - Biomedical Science and Technology (BST), University of Applied Sciences , Mannheim , Germany – name: 11 Department of Zoology, University of British Columbia , Vancouver, BC , Canada – name: 1 Michael Smith Laboratories, University of British Columbia , Vancouver, BC , Canada – name: 5 Department of Microbiology and Immunology, University of British Columbia , Vancouver, BC , Canada – name: 6 Department of Medical Genetics, University of British Columbia , Vancouver, BC , Canada – name: 9 School of Medicine, Koç University , Istanbul , Türkiye |
| Author_xml | – sequence: 1 givenname: Sarah surname: Dada fullname: Dada, Sarah – sequence: 2 givenname: Samantha L. S. surname: Ellis fullname: Ellis, Samantha L. S. – sequence: 3 givenname: Christi surname: Wood fullname: Wood, Christi – sequence: 4 givenname: Lilian L. surname: Nohara fullname: Nohara, Lilian L. – sequence: 5 givenname: Carola surname: Dreier fullname: Dreier, Carola – sequence: 6 givenname: Nicolas H. surname: Garcia fullname: Garcia, Nicolas H. – sequence: 7 givenname: Iryna surname: Saranchova fullname: Saranchova, Iryna – sequence: 8 givenname: Lonna surname: Munro fullname: Munro, Lonna – sequence: 9 givenname: Cheryl G. surname: Pfeifer fullname: Pfeifer, Cheryl G. – sequence: 10 givenname: Brett A. surname: Eyford fullname: Eyford, Brett A. – sequence: 11 givenname: Suresh surname: Kari fullname: Kari, Suresh – sequence: 12 givenname: Emmanuel surname: Garrovillas fullname: Garrovillas, Emmanuel – sequence: 13 givenname: Giorgia surname: Caspani fullname: Caspani, Giorgia – sequence: 14 givenname: Eliana surname: Al Haddad fullname: Al Haddad, Eliana – sequence: 15 givenname: Patrick W. surname: Gray fullname: Gray, Patrick W. – sequence: 16 givenname: Tunc surname: Morova fullname: Morova, Tunc – sequence: 17 givenname: Nathan A. surname: Lack fullname: Lack, Nathan A. – sequence: 18 givenname: Raymond J. surname: Andersen fullname: Andersen, Raymond J. – sequence: 19 givenname: Larry surname: Tjoelker fullname: Tjoelker, Larry – sequence: 20 givenname: Wilfred A. surname: Jefferies fullname: Jefferies, Wilfred A. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36923728$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2023 Dada, Ellis, Wood, Nohara, Dreier, Garcia, Saranchova, Munro, Pfeifer, Eyford, Kari, Garrovillas, Caspani, Al Haddad, Gray, Morova, Lack, Andersen, Tjoelker and Jefferies. Copyright © 2023 Dada, Ellis, Wood, Nohara, Dreier, Garcia, Saranchova, Munro, Pfeifer, Eyford, Kari, Garrovillas, Caspani, Al Haddad, Gray, Morova, Lack, Andersen, Tjoelker and Jefferies 2023 Dada, Ellis, Wood, Nohara, Dreier, Garcia, Saranchova, Munro, Pfeifer, Eyford, Kari, Garrovillas, Caspani, Al Haddad, Gray, Morova, Lack, Andersen, Tjoelker and Jefferies |
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| Keywords | major histocompatibility class I metastatic cancers immune edited cytolytic T lymphocyte MHC cannabinoids CTL immune escape |
| Language | English |
| License | Copyright © 2023 Dada, Ellis, Wood, Nohara, Dreier, Garcia, Saranchova, Munro, Pfeifer, Eyford, Kari, Garrovillas, Caspani, Al Haddad, Gray, Morova, Lack, Andersen, Tjoelker and Jefferies. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present addresses: Sarah Dada, Michael Smith Genome Sciences Centre, Vancouver, BC, Canada; Bioinformatics Graduate Program, Faculty of Science, University of British Columbia, Vancouver, BC, Canada Edited by: Adriana Albini, MultiMedica Holding SpA (IRCCS), Italy Reviewed by: Bruno Miguel Fonseca, University of Porto, Portugal; Douglas Mc Clain Noonan, University of Insubria, Italy These authors share first authorship This article was submitted to Cancer Immunity and Immunotherapy, a section of the journal Frontiers in Immunology |
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| SubjectTerms | Adaptive Immunity cannabinoids Cannabinoids - pharmacology CTL cytolytic T lymphocyte Humans immune escape Immune Evasion Immunology major histocompatibility class I MHC Neoplasms |
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| Title | Specific cannabinoids revive adaptive immunity by reversing immune evasion mechanisms in metastatic tumours |
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