Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance

Inflammatory bowel disease (IBD) often coexists with depression, posing considerable challenges for treatment. This study aimed to investigate the therapeutic potential of fucoidan, a compound derived from Laminaria japonica, in a dextran sulfate sodium (DSS)-induced model of IBD with comorbid depre...

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Main Authors: Zi-Wei Ye, Zhong-Yu Yuan, Jun Wang, Hua Li, Cheng-Fu Li, Guang-Hui Xu, Li-Tao Yi, Wei-Feng Huang
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:Journal of Functional Foods
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1756464623005510
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author Zi-Wei Ye
Zhong-Yu Yuan
Jun Wang
Hua Li
Cheng-Fu Li
Guang-Hui Xu
Li-Tao Yi
Wei-Feng Huang
author_facet Zi-Wei Ye
Zhong-Yu Yuan
Jun Wang
Hua Li
Cheng-Fu Li
Guang-Hui Xu
Li-Tao Yi
Wei-Feng Huang
author_sort Zi-Wei Ye
collection DOAJ
description Inflammatory bowel disease (IBD) often coexists with depression, posing considerable challenges for treatment. This study aimed to investigate the therapeutic potential of fucoidan, a compound derived from Laminaria japonica, in a dextran sulfate sodium (DSS)-induced model of IBD with comorbid depression. The administration of fucoidan demonstrated significant therapeutic efficacy, as it reduced disease activity, increased sucrose preference, and decreased immobility time, suggesting benefits for both IBD and depression. Fucoidan had a noteworthy impact on the gut microbiota, characterized by an increase in the abundance of Firmicutes and Lactobacillus. Additionally, it strengthened the integrity of the colonic barrier by upregulating tight junction proteins (ZO-1, Occludin, and Claudin-1) and reduced colonic inflammation via the TLR4/NF-κB pathway. Fucoidan also exhibited the ability to suppress peripheral inflammation and lower stress response hormone levels, particularly corticosterone. Furthermore, fucoidan reduced the number of microglia, as well as decreasing cytokines such as interleukin-1 beta (IL-1β) and tumor necrosis factor alpha (TNF-α) levels, indicating a decrease in neuroinflammation in IBD-afflicted mice. In conclusion, fucoidan effectively mitigates IBD comorbid with depression by modulating the gut microbiota-brain axis. These findings offer promise for fucoidan as a natural compound to manage both IBD and associated depressive symptoms.
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spelling doaj.art-53cbcc275bf94e34b4e9c82b09b9dece2024-01-14T05:37:19ZengElsevierJournal of Functional Foods1756-46462024-01-01112105951Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balanceZi-Wei Ye0Zhong-Yu Yuan1Jun Wang2Hua Li3Cheng-Fu Li4Guang-Hui Xu5Li-Tao Yi6Wei-Feng Huang7Department of Gastroenterology and Hepatology, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen 361003, Fujian Province, PR China; Department of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR ChinaDepartment of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR ChinaDepartment of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR ChinaDepartment of Gastroenterology and Hepatology, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen 361003, Fujian Province, PR ChinaXiamen Hospital of Traditional Chinese Medicine, Xiamen 361009, Fujian Province, PR ChinaXiamen Medicine Research Institute, Xiamen 361008, Fujian Province, PR China; Corresponding authors at: Xiamen Medicine Research Institute, Xiamen 361008, Fujian province, PR China (G.-H. Xu). Department of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR China (L.-T. Yi). Department of Gastroenterology and Hepatology, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen 361003, Fujian Province, PR China (W.-F. Huang).Department of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR China; Institute of Pharmaceutical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR China; Fujian Provincial Key Laboratory of Biochemical Technology, Huaqiao University, Xiamen 361021, Fujian Province, PR China; Corresponding authors at: Xiamen Medicine Research Institute, Xiamen 361008, Fujian province, PR China (G.-H. Xu). Department of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR China (L.-T. Yi). Department of Gastroenterology and Hepatology, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen 361003, Fujian Province, PR China (W.-F. Huang).Department of Gastroenterology and Hepatology, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen 361003, Fujian Province, PR China; The School of Clinical Medicine, Fujian Medical University, Fuzhou 350004, Fujian Province, PR China; Corresponding authors at: Xiamen Medicine Research Institute, Xiamen 361008, Fujian province, PR China (G.-H. Xu). Department of Chemical and Pharmaceutical Engineering, College of Chemical Engineering, Huaqiao University, Xiamen 361021, Fujian Province, PR China (L.-T. Yi). Department of Gastroenterology and Hepatology, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen 361003, Fujian Province, PR China (W.-F. Huang).Inflammatory bowel disease (IBD) often coexists with depression, posing considerable challenges for treatment. This study aimed to investigate the therapeutic potential of fucoidan, a compound derived from Laminaria japonica, in a dextran sulfate sodium (DSS)-induced model of IBD with comorbid depression. The administration of fucoidan demonstrated significant therapeutic efficacy, as it reduced disease activity, increased sucrose preference, and decreased immobility time, suggesting benefits for both IBD and depression. Fucoidan had a noteworthy impact on the gut microbiota, characterized by an increase in the abundance of Firmicutes and Lactobacillus. Additionally, it strengthened the integrity of the colonic barrier by upregulating tight junction proteins (ZO-1, Occludin, and Claudin-1) and reduced colonic inflammation via the TLR4/NF-κB pathway. Fucoidan also exhibited the ability to suppress peripheral inflammation and lower stress response hormone levels, particularly corticosterone. Furthermore, fucoidan reduced the number of microglia, as well as decreasing cytokines such as interleukin-1 beta (IL-1β) and tumor necrosis factor alpha (TNF-α) levels, indicating a decrease in neuroinflammation in IBD-afflicted mice. In conclusion, fucoidan effectively mitigates IBD comorbid with depression by modulating the gut microbiota-brain axis. These findings offer promise for fucoidan as a natural compound to manage both IBD and associated depressive symptoms.http://www.sciencedirect.com/science/article/pii/S1756464623005510FucoidanInflammatory bowel disease (IBD)DepressionGut microbiotaBrainInflammation
spellingShingle Zi-Wei Ye
Zhong-Yu Yuan
Jun Wang
Hua Li
Cheng-Fu Li
Guang-Hui Xu
Li-Tao Yi
Wei-Feng Huang
Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance
Journal of Functional Foods
Fucoidan
Inflammatory bowel disease (IBD)
Depression
Gut microbiota
Brain
Inflammation
title Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance
title_full Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance
title_fullStr Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance
title_full_unstemmed Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance
title_short Fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota-brain axis balance
title_sort fucoidan attenuates chronic colitis and behavioral deficits by reshaping gut microbiota brain axis balance
topic Fucoidan
Inflammatory bowel disease (IBD)
Depression
Gut microbiota
Brain
Inflammation
url http://www.sciencedirect.com/science/article/pii/S1756464623005510
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