Dectin-1 Activation by a Natural Product β-Glucan Converts Immunosuppressive Macrophages into an M1-like Phenotype

Tumor-associated macrophages (TAM) with an alternatively activated phenotype have been linked to tumor-elicited inflammation, immunosuppression, and resistance to chemotherapies in cancer, thus representing an attractive target for an effective cancer immunotherapy. In this study, we demonstrate tha...

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Vydáno v:	The Journal of immunology (1950) Ročník 195; číslo 10; s. 5055
Hlavní autoři:	Liu, Min, Luo, Fengling, Ding, Chuanlin, Albeituni, Sabrin, Hu, Xiaoling, Ma, Yunfeng, Cai, Yihua, McNally, Lacey, Sanders, Mary Ann, Jain, Dharamvir, Kloecker, Goetz, Bousamra, 2nd, Michael, Zhang, Huang-ge, Higashi, Richard M, Lane, Andrew N, Fan, Teresa W-M, Yan, Jun
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States 15.11.2015
Témata:	Animals beta-Glucans - chemistry beta-Glucans - pharmacology CARD Signaling Adaptor Proteins - genetics CARD Signaling Adaptor Proteins - immunology Cell Line, Tumor Fungal Polysaccharides - chemistry Fungal Polysaccharides - pharmacology Lectins, C-Type - immunology Macrophages - immunology Macrophages - metabolism MAP Kinase Signaling System - drug effects MAP Kinase Signaling System - genetics MAP Kinase Signaling System - immunology Mice Mice, Knockout Neoplasms, Experimental - drug therapy Neoplasms, Experimental - genetics Neoplasms, Experimental - immunology Neoplasms, Experimental - pathology Saccharomyces cerevisiae - chemistry
ISSN:	1550-6606, 1550-6606
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Abstract	Tumor-associated macrophages (TAM) with an alternatively activated phenotype have been linked to tumor-elicited inflammation, immunosuppression, and resistance to chemotherapies in cancer, thus representing an attractive target for an effective cancer immunotherapy. In this study, we demonstrate that particulate yeast-derived β-glucan, a natural polysaccharide compound, converts polarized alternatively activated macrophages or immunosuppressive TAM into a classically activated phenotype with potent immunostimulating activity. This process is associated with macrophage metabolic reprograming with enhanced glycolysis, Krebs cycle, and glutamine utilization. In addition, particulate β-glucan converts immunosuppressive TAM via the C-type lectin receptor dectin-1-induced spleen tyrosine kinase-Card9-Erk pathway. Further in vivo studies show that oral particulate β-glucan treatment significantly delays tumor growth, which is associated with in vivo TAM phenotype conversion and enhanced effector T cell activation. Mice injected with particulate β-glucan-treated TAM mixed with tumor cells have significantly reduced tumor burden with less blood vascular vessels compared with those with TAM plus tumor cell injection. In addition, macrophage depletion significantly reduced the therapeutic efficacy of particulate β-glucan in tumor-bearing mice. These findings have established a new paradigm for macrophage polarization and immunosuppressive TAM conversion and shed light on the action mode of β-glucan treatment in cancer.
AbstractList	Tumor-associated macrophages (TAM) with an alternatively activated phenotype have been linked to tumor-elicited inflammation, immunosuppression, and resistance to chemotherapies in cancer, thus representing an attractive target for an effective cancer immunotherapy. In this study, we demonstrate that particulate yeast-derived β-glucan, a natural polysaccharide compound, converts polarized alternatively activated macrophages or immunosuppressive TAM into a classically activated phenotype with potent immunostimulating activity. This process is associated with macrophage metabolic reprograming with enhanced glycolysis, Krebs cycle, and glutamine utilization. In addition, particulate β-glucan converts immunosuppressive TAM via the C-type lectin receptor dectin-1-induced spleen tyrosine kinase-Card9-Erk pathway. Further in vivo studies show that oral particulate β-glucan treatment significantly delays tumor growth, which is associated with in vivo TAM phenotype conversion and enhanced effector T cell activation. Mice injected with particulate β-glucan-treated TAM mixed with tumor cells have significantly reduced tumor burden with less blood vascular vessels compared with those with TAM plus tumor cell injection. In addition, macrophage depletion significantly reduced the therapeutic efficacy of particulate β-glucan in tumor-bearing mice. These findings have established a new paradigm for macrophage polarization and immunosuppressive TAM conversion and shed light on the action mode of β-glucan treatment in cancer. Tumor-associated macrophages (TAM) with an alternatively activated phenotype have been linked to tumor-elicited inflammation, immunosuppression, and resistance to chemotherapies in cancer, thus representing an attractive target for an effective cancer immunotherapy. In this study, we demonstrate that particulate yeast-derived β-glucan, a natural polysaccharide compound, converts polarized alternatively activated macrophages or immunosuppressive TAM into a classically activated phenotype with potent immunostimulating activity. This process is associated with macrophage metabolic reprograming with enhanced glycolysis, Krebs cycle, and glutamine utilization. In addition, particulate β-glucan converts immunosuppressive TAM via the C-type lectin receptor dectin-1-induced spleen tyrosine kinase-Card9-Erk pathway. Further in vivo studies show that oral particulate β-glucan treatment significantly delays tumor growth, which is associated with in vivo TAM phenotype conversion and enhanced effector T cell activation. Mice injected with particulate β-glucan-treated TAM mixed with tumor cells have significantly reduced tumor burden with less blood vascular vessels compared with those with TAM plus tumor cell injection. In addition, macrophage depletion significantly reduced the therapeutic efficacy of particulate β-glucan in tumor-bearing mice. These findings have established a new paradigm for macrophage polarization and immunosuppressive TAM conversion and shed light on the action mode of β-glucan treatment in cancer.Tumor-associated macrophages (TAM) with an alternatively activated phenotype have been linked to tumor-elicited inflammation, immunosuppression, and resistance to chemotherapies in cancer, thus representing an attractive target for an effective cancer immunotherapy. In this study, we demonstrate that particulate yeast-derived β-glucan, a natural polysaccharide compound, converts polarized alternatively activated macrophages or immunosuppressive TAM into a classically activated phenotype with potent immunostimulating activity. This process is associated with macrophage metabolic reprograming with enhanced glycolysis, Krebs cycle, and glutamine utilization. In addition, particulate β-glucan converts immunosuppressive TAM via the C-type lectin receptor dectin-1-induced spleen tyrosine kinase-Card9-Erk pathway. Further in vivo studies show that oral particulate β-glucan treatment significantly delays tumor growth, which is associated with in vivo TAM phenotype conversion and enhanced effector T cell activation. Mice injected with particulate β-glucan-treated TAM mixed with tumor cells have significantly reduced tumor burden with less blood vascular vessels compared with those with TAM plus tumor cell injection. In addition, macrophage depletion significantly reduced the therapeutic efficacy of particulate β-glucan in tumor-bearing mice. These findings have established a new paradigm for macrophage polarization and immunosuppressive TAM conversion and shed light on the action mode of β-glucan treatment in cancer.
Author	Luo, Fengling Albeituni, Sabrin Hu, Xiaoling Cai, Yihua Sanders, Mary Ann Zhang, Huang-ge McNally, Lacey Higashi, Richard M Liu, Min Kloecker, Goetz Jain, Dharamvir Ding, Chuanlin Lane, Andrew N Ma, Yunfeng Bousamra, 2nd, Michael Fan, Teresa W-M Yan, Jun
Author_xml	– sequence: 1 givenname: Min orcidid: 0000-0001-7095-1344 surname: Liu fullname: Liu, Min organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202; Department of Immunology, Wuhan University School of Medicine, Wuhan 430072, China – sequence: 2 givenname: Fengling surname: Luo fullname: Luo, Fengling organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202; Department of Immunology, Wuhan University School of Medicine, Wuhan 430072, China – sequence: 3 givenname: Chuanlin surname: Ding fullname: Ding, Chuanlin organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 4 givenname: Sabrin surname: Albeituni fullname: Albeituni, Sabrin organization: Department of Microbiology and Immunology, University of Louisville School of Medicine, Louisville, KY 40202 – sequence: 5 givenname: Xiaoling surname: Hu fullname: Hu, Xiaoling organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 6 givenname: Yunfeng surname: Ma fullname: Ma, Yunfeng organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 7 givenname: Yihua surname: Cai fullname: Cai, Yihua organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 8 givenname: Lacey surname: McNally fullname: McNally, Lacey organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 9 givenname: Mary Ann surname: Sanders fullname: Sanders, Mary Ann organization: Department of Pathology, University of Louisville School of Medicine, Louisville, KY 40202 – sequence: 10 givenname: Dharamvir orcidid: 0000-0003-3482-8001 surname: Jain fullname: Jain, Dharamvir organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 11 givenname: Goetz surname: Kloecker fullname: Kloecker, Goetz organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202 – sequence: 12 givenname: Michael surname: Bousamra, 2nd fullname: Bousamra, 2nd, Michael organization: Department of Cardiovascular Thoracic Surgery, University of Louisville, Louisville, KY 40202 – sequence: 13 givenname: Huang-ge surname: Zhang fullname: Zhang, Huang-ge organization: Department of Microbiology and Immunology, University of Louisville School of Medicine, Louisville, KY 40202 – sequence: 14 givenname: Richard M surname: Higashi fullname: Higashi, Richard M organization: Department of Chemistry, University of Louisville, Louisville, KY 40202; and – sequence: 15 givenname: Andrew N orcidid: 0000-0003-1121-5106 surname: Lane fullname: Lane, Andrew N organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202; Department of Chemistry, University of Louisville, Louisville, KY 40202; and Center for Regulatory and Environmental Analytical Metabolomics, University of Louisville, Louisville, KY 40202 – sequence: 16 givenname: Teresa W-M surname: Fan fullname: Fan, Teresa W-M organization: Department of Chemistry, University of Louisville, Louisville, KY 40202; and Center for Regulatory and Environmental Analytical Metabolomics, University of Louisville, Louisville, KY 40202 – sequence: 17 givenname: Jun surname: Yan fullname: Yan, Jun email: jun.yan@louisville.edu organization: Division of Hematology/Oncology, Department of Medicine, James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202; Department of Microbiology and Immunology, University of Louisville School of Medicine, Louisville, KY 40202; jun.yan@louisville.edu
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Snippet	Tumor-associated macrophages (TAM) with an alternatively activated phenotype have been linked to tumor-elicited inflammation, immunosuppression, and resistance...
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SubjectTerms	Animals beta-Glucans - chemistry beta-Glucans - pharmacology CARD Signaling Adaptor Proteins - genetics CARD Signaling Adaptor Proteins - immunology Cell Line, Tumor Fungal Polysaccharides - chemistry Fungal Polysaccharides - pharmacology Lectins, C-Type - immunology Macrophages - immunology Macrophages - metabolism MAP Kinase Signaling System - drug effects MAP Kinase Signaling System - genetics MAP Kinase Signaling System - immunology Mice Mice, Knockout Neoplasms, Experimental - drug therapy Neoplasms, Experimental - genetics Neoplasms, Experimental - immunology Neoplasms, Experimental - pathology Saccharomyces cerevisiae - chemistry
Title	Dectin-1 Activation by a Natural Product β-Glucan Converts Immunosuppressive Macrophages into an M1-like Phenotype
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