Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells
Introduction: Diet-induced obesity has been shown to decrease the abundance of Turicibacter, a genus known to play a role in the serotonin signaling system, which is associated with colorectal tumorigenesis, making the presence of Turicibacter potentially influential in the protection of intestinal...
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| Format: | Article |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Pharmacology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphar.2023.1203087/full |
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| author | Ting-Chun Lin Anand Soorneedi Yingxue Guan Ying Tang Eleanor Shi Matthew D. Moore Zhenhua Liu Zhenhua Liu |
| author_facet | Ting-Chun Lin Anand Soorneedi Yingxue Guan Ying Tang Eleanor Shi Matthew D. Moore Zhenhua Liu Zhenhua Liu |
| author_sort | Ting-Chun Lin |
| collection | DOAJ |
| description | Introduction: Diet-induced obesity has been shown to decrease the abundance of Turicibacter, a genus known to play a role in the serotonin signaling system, which is associated with colorectal tumorigenesis, making the presence of Turicibacter potentially influential in the protection of intestinal tumorigenesis. Recently, Antrodia camphorata (AC), a medicinal fungus native to Taiwan, has emerged as a promising candidate for complementary and alternative cancer therapy. Small molecules and polysaccharides derived from AC have been reported to possess health-promoting effects, including anti-cancer properties.Methods: Bacterial culture followed with cell culture were used in this study to determine the role of Turicibacter in colorectal tumorigenesis and to explore the anti-cancer mechanism of AC with Turicibacter fermentation.Results:Turicibacter fermentation and the addition of AC polysaccharide led to a significant increase in the production of nutrients and metabolites, including α-ketoglutaric acid and lactic acid (p < 0.05). Treatment of Turicibacter fermented AC polysaccharide was more effective in inhibiting serotonin signaling-related genes, including Tph1, Htr1d, Htr2a, Htr2b, and Htr2c (p < 0.05), and Wnt-signaling related protein and downstream gene expressions, such as phospho-GSK-3β, active β-catenin, c-Myc, Ccnd1, and Axin2 (p < 0.05). Additionally, it triggered the highest generation of reactive oxygen species (ROS), which activated PI3K/Akt and MAPK/Erk signaling and resulted in cleaved caspase-3 expression. In comparison, the treatment of AC polysaccharide without Turicibacter fermentation displayed a lesser effect.Discussion: Our findings suggest that AC polysaccharide effectively suppresses the tumorigenic serotonin and Wnt-signaling pathways, and promotes ROS-mediated apoptosis in Caco-2 cells. These processes are further enhanced by Turicibacter fermentation. |
| first_indexed | 2024-03-12T14:29:58Z |
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| institution | Directory Open Access Journal |
| issn | 1663-9812 |
| language | English |
| last_indexed | 2024-03-12T14:29:58Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Pharmacology |
| spelling | doaj.art-04076a55c0f1423fae96bf0ec08accc32023-08-17T13:37:43ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122023-08-011410.3389/fphar.2023.12030871203087Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cellsTing-Chun Lin0Anand Soorneedi1Yingxue Guan2Ying Tang3Eleanor Shi4Matthew D. Moore5Zhenhua Liu6Zhenhua Liu7Department of Nutrition, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, United StatesDepartment of Food Science, University of Massachusetts, Amherst, MA, United StatesDepartment of Nutrition, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, United StatesDepartment of Nutrition, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, United StatesChobanian and Avedisian School of Medicine, Boston University, Boston, MA, United StatesDepartment of Food Science, University of Massachusetts, Amherst, MA, United StatesDepartment of Nutrition, School of Public Health and Health Sciences, University of Massachusetts, Amherst, MA, United StatesUMass Cancer Center, University of Massachusetts Chan Medical School, Worcester, MA, United StatesIntroduction: Diet-induced obesity has been shown to decrease the abundance of Turicibacter, a genus known to play a role in the serotonin signaling system, which is associated with colorectal tumorigenesis, making the presence of Turicibacter potentially influential in the protection of intestinal tumorigenesis. Recently, Antrodia camphorata (AC), a medicinal fungus native to Taiwan, has emerged as a promising candidate for complementary and alternative cancer therapy. Small molecules and polysaccharides derived from AC have been reported to possess health-promoting effects, including anti-cancer properties.Methods: Bacterial culture followed with cell culture were used in this study to determine the role of Turicibacter in colorectal tumorigenesis and to explore the anti-cancer mechanism of AC with Turicibacter fermentation.Results:Turicibacter fermentation and the addition of AC polysaccharide led to a significant increase in the production of nutrients and metabolites, including α-ketoglutaric acid and lactic acid (p < 0.05). Treatment of Turicibacter fermented AC polysaccharide was more effective in inhibiting serotonin signaling-related genes, including Tph1, Htr1d, Htr2a, Htr2b, and Htr2c (p < 0.05), and Wnt-signaling related protein and downstream gene expressions, such as phospho-GSK-3β, active β-catenin, c-Myc, Ccnd1, and Axin2 (p < 0.05). Additionally, it triggered the highest generation of reactive oxygen species (ROS), which activated PI3K/Akt and MAPK/Erk signaling and resulted in cleaved caspase-3 expression. In comparison, the treatment of AC polysaccharide without Turicibacter fermentation displayed a lesser effect.Discussion: Our findings suggest that AC polysaccharide effectively suppresses the tumorigenic serotonin and Wnt-signaling pathways, and promotes ROS-mediated apoptosis in Caco-2 cells. These processes are further enhanced by Turicibacter fermentation.https://www.frontiersin.org/articles/10.3389/fphar.2023.1203087/fullmushroom polysaccharidemicrobiomeTuricibacterserotoninWnt/βcatenin signalingreactive oxygen species |
| spellingShingle | Ting-Chun Lin Anand Soorneedi Yingxue Guan Ying Tang Eleanor Shi Matthew D. Moore Zhenhua Liu Zhenhua Liu Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells Frontiers in Pharmacology mushroom polysaccharide microbiome Turicibacter serotonin Wnt/βcatenin signaling reactive oxygen species |
| title | Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells |
| title_full | Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells |
| title_fullStr | Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells |
| title_full_unstemmed | Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells |
| title_short | Turicibacter fermentation enhances the inhibitory effects of Antrodia camphorata supplementation on tumorigenic serotonin and Wnt pathways and promotes ROS-mediated apoptosis of Caco-2 cells |
| title_sort | turicibacter fermentation enhances the inhibitory effects of antrodia camphorata supplementation on tumorigenic serotonin and wnt pathways and promotes ros mediated apoptosis of caco 2 cells |
| topic | mushroom polysaccharide microbiome Turicibacter serotonin Wnt/βcatenin signaling reactive oxygen species |
| url | https://www.frontiersin.org/articles/10.3389/fphar.2023.1203087/full |
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