Enhancing anti-tumor immunity through liposomal oxaliplatin and localized immunotherapy via STING activation

The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and adaptive immunity. Recent evidence suggests that chemotherapy-induced DNA damage can directly induce dendritic cell (DC) maturation and recruit...

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Veröffentlicht in:	Journal of controlled release Jg. 357; S. 531 - 544
Hauptverfasser:	Gu, Zili, Hao, Yang, Schomann, Timo, Ossendorp, Ferry, ten Dijke, Peter, Cruz, Luis J.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	Netherlands Elsevier B.V 01.05.2023
Schlagworte:	agonists antigens antineoplastic activity Antineoplastic Agents - therapeutic use Cancer cell death colorectal neoplasms Colorectal Neoplasms - drug therapy crosslinking dendritic cells DNA DNA damage Humans Immunochemotherapy immunogenicity immunosuppression immunotherapy Immunotherapy - methods interferons Liposomes macrophages Nanomedicine Oxaliplatin phagocytosis phenotype remission STING T-lymphocytes Immunochemotherapy CRT DL MHC HMGB1 DAMPs BSA OLP Oxaliplatin TAMs CFMDA IC50 cGAS Nanomedicine EE DSPC IL H&E Tregs eLP DAPI ICD TME IR780-LP TAA UPLC STING OXA CTL mPEG2000-DSPE Liposomes ATP dsDNA Cancer DC
ISSN:	0168-3659, 1873-4995, 1873-4995
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Abstract	The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and adaptive immunity. Recent evidence suggests that chemotherapy-induced DNA damage can directly induce dendritic cell (DC) maturation and recruitment, which synergizes with STING activation to enhance anti-tumor effects. As an immunogenic cell death (ICD) inducer, oxaliplatin generates massive double-stranded DNA (dsDNA) crosslinks, release of tumor-associated antigens and promoting the “eat me” signal. STING activation improves antigen immunogenicity, which can promote T cell activation and infiltration. In this study, we developed liposomes encapsulating oxaliplatin and combine this formulation with a STING agonist (ADU-S100) for treating colorectal cancer. The liposomes efficiently inhibited the proliferation of tumor cells while induced ICD in CT26 colorectal cancer cells, which enhanced dendritic cell maturation and phagocytosis in vitro. The liposome-based immunochemotherapy exhibited the strongest efficacy, resulting in complete remission upon tumor inoculation. Mechanistic studies showed this potent anti-cancer effect was related to the significant recruitment of infiltrating CD8 and CD4 T cells, reduction of suppressive Treg cells, and a shift in the phenotype of tumor-associated suppressive macrophages that promote cancer to immune stimulating macrophages. Thus, our study demonstrated the potential of combining oxaliplatin-loaded liposomes with a STING agonist to reduce tumor growth by regulating the immunosuppressive state in the tumor. [Display omitted] •First combination of oxaliplatin and ADU-S100 for cancer treatment•Enhanced anti-tumor efficiency by regulate tumor microenvironment•Orchestrated immune response on both innate and adaptive immunity
AbstractList	The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and adaptive immunity. Recent evidence suggests that chemotherapy-induced DNA damage can directly induce dendritic cell (DC) maturation and recruitment, which synergizes with STING activation to enhance anti-tumor effects. As an immunogenic cell death (ICD) inducer, oxaliplatin generates massive double-stranded DNA (dsDNA) crosslinks, release of tumor-associated antigens and promoting the "eat me" signal. STING activation improves antigen immunogenicity, which can promote T cell activation and infiltration. In this study, we developed liposomes encapsulating oxaliplatin and combine this formulation with a STING agonist (ADU-S100) for treating colorectal cancer. The liposomes efficiently inhibited the proliferation of tumor cells while induced ICD in CT26 colorectal cancer cells, which enhanced dendritic cell maturation and phagocytosis in vitro. The liposome-based immunochemotherapy exhibited the strongest efficacy, resulting in complete remission upon tumor inoculation. Mechanistic studies showed this potent anti-cancer effect was related to the significant recruitment of infiltrating CD8 and CD4 T cells, reduction of suppressive Treg cells, and a shift in the phenotype of tumor-associated suppressive macrophages that promote cancer to immune stimulating macrophages. Thus, our study demonstrated the potential of combining oxaliplatin-loaded liposomes with a STING agonist to reduce tumor growth by regulating the immunosuppressive state in the tumor. The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and adaptive immunity. Recent evidence suggests that chemotherapy-induced DNA damage can directly induce dendritic cell (DC) maturation and recruitment, which synergizes with STING activation to enhance anti-tumor effects. As an immunogenic cell death (ICD) inducer, oxaliplatin generates massive double-stranded DNA (dsDNA) crosslinks, release of tumor-associated antigens and promoting the “eat me” signal. STING activation improves antigen immunogenicity, which can promote T cell activation and infiltration. In this study, we developed liposomes encapsulating oxaliplatin and combine this formulation with a STING agonist (ADU-S100) for treating colorectal cancer. The liposomes efficiently inhibited the proliferation of tumor cells while induced ICD in CT26 colorectal cancer cells, which enhanced dendritic cell maturation and phagocytosis in vitro. The liposome-based immunochemotherapy exhibited the strongest efficacy, resulting in complete remission upon tumor inoculation. Mechanistic studies showed this potent anti-cancer effect was related to the significant recruitment of infiltrating CD8 and CD4 T cells, reduction of suppressive Treg cells, and a shift in the phenotype of tumor-associated suppressive macrophages that promote cancer to immune stimulating macrophages. Thus, our study demonstrated the potential of combining oxaliplatin-loaded liposomes with a STING agonist to reduce tumor growth by regulating the immunosuppressive state in the tumor. [Display omitted] •First combination of oxaliplatin and ADU-S100 for cancer treatment•Enhanced anti-tumor efficiency by regulate tumor microenvironment•Orchestrated immune response on both innate and adaptive immunity The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and adaptive immunity. Recent evidence suggests that chemotherapy-induced DNA damage can directly induce dendritic cell (DC) maturation and recruitment, which synergizes with STING activation to enhance anti-tumor effects. As an immunogenic cell death (ICD) inducer, oxaliplatin generates massive double-stranded DNA (dsDNA) crosslinks, release of tumor-associated antigens and promoting the "eat me" signal. STING activation improves antigen immunogenicity, which can promote T cell activation and infiltration. In this study, we developed liposomes encapsulating oxaliplatin and combine this formulation with a STING agonist (ADU-S100) for treating colorectal cancer. The liposomes efficiently inhibited the proliferation of tumor cells while induced ICD in CT26 colorectal cancer cells, which enhanced dendritic cell maturation and phagocytosis in vitro. The liposome-based immunochemotherapy exhibited the strongest efficacy, resulting in complete remission upon tumor inoculation. Mechanistic studies showed this potent anti-cancer effect was related to the significant recruitment of infiltrating CD8 and CD4 T cells, reduction of suppressive Treg cells, and a shift in the phenotype of tumor-associated suppressive macrophages that promote cancer to immune stimulating macrophages. Thus, our study demonstrated the potential of combining oxaliplatin-loaded liposomes with a STING agonist to reduce tumor growth by regulating the immunosuppressive state in the tumor.The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and adaptive immunity. Recent evidence suggests that chemotherapy-induced DNA damage can directly induce dendritic cell (DC) maturation and recruitment, which synergizes with STING activation to enhance anti-tumor effects. As an immunogenic cell death (ICD) inducer, oxaliplatin generates massive double-stranded DNA (dsDNA) crosslinks, release of tumor-associated antigens and promoting the "eat me" signal. STING activation improves antigen immunogenicity, which can promote T cell activation and infiltration. In this study, we developed liposomes encapsulating oxaliplatin and combine this formulation with a STING agonist (ADU-S100) for treating colorectal cancer. The liposomes efficiently inhibited the proliferation of tumor cells while induced ICD in CT26 colorectal cancer cells, which enhanced dendritic cell maturation and phagocytosis in vitro. The liposome-based immunochemotherapy exhibited the strongest efficacy, resulting in complete remission upon tumor inoculation. Mechanistic studies showed this potent anti-cancer effect was related to the significant recruitment of infiltrating CD8 and CD4 T cells, reduction of suppressive Treg cells, and a shift in the phenotype of tumor-associated suppressive macrophages that promote cancer to immune stimulating macrophages. Thus, our study demonstrated the potential of combining oxaliplatin-loaded liposomes with a STING agonist to reduce tumor growth by regulating the immunosuppressive state in the tumor.
Author	Cruz, Luis J. Gu, Zili Ossendorp, Ferry Hao, Yang Schomann, Timo ten Dijke, Peter
Author_xml	– sequence: 1 givenname: Zili surname: Gu fullname: Gu, Zili organization: Department of Radiology, Leiden University Medical Center, the Netherlands – sequence: 2 givenname: Yang surname: Hao fullname: Hao, Yang organization: Department of Radiology, Leiden University Medical Center, the Netherlands – sequence: 3 givenname: Timo surname: Schomann fullname: Schomann, Timo organization: Department of Radiology, Leiden University Medical Center, the Netherlands – sequence: 4 givenname: Ferry surname: Ossendorp fullname: Ossendorp, Ferry organization: Department of Immunology, Leiden University Medical Center, the Netherlands – sequence: 5 givenname: Peter surname: ten Dijke fullname: ten Dijke, Peter email: P.ten_Dijke@lumc.nl organization: Oncode Institute, Department of Cell and Chemical Biology, Leiden University Medical Center, the Netherlands – sequence: 6 givenname: Luis J. surname: Cruz fullname: Cruz, Luis J. email: l.j.cruz_ricondo@lumc.nl organization: Department of Radiology, Leiden University Medical Center, the Netherlands
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/37030544$$D View this record in MEDLINE/PubMed
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Keywords	Immunochemotherapy CRT DL MHC HMGB1 DAMPs BSA OLP Oxaliplatin TAMs CFMDA IC50 cGAS Nanomedicine EE DSPC IL H&E Tregs eLP DAPI ICD TME IR780-LP TAA UPLC STING OXA CTL mPEG2000-DSPE Liposomes ATP dsDNA Cancer DC
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Snippet	The cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) pathway is a promising approach for anti-cancer immunotherapy by bridging innate and...
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SubjectTerms	agonists antigens antineoplastic activity Antineoplastic Agents - therapeutic use Cancer cell death colorectal neoplasms Colorectal Neoplasms - drug therapy crosslinking dendritic cells DNA DNA damage Humans Immunochemotherapy immunogenicity immunosuppression immunotherapy Immunotherapy - methods interferons Liposomes macrophages Nanomedicine Oxaliplatin phagocytosis phenotype remission STING T-lymphocytes
Title	Enhancing anti-tumor immunity through liposomal oxaliplatin and localized immunotherapy via STING activation
URI	https://dx.doi.org/10.1016/j.jconrel.2023.04.011 https://www.ncbi.nlm.nih.gov/pubmed/37030544 https://www.proquest.com/docview/2798714311 https://www.proquest.com/docview/2834232817
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