Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats

Attenuating acetylcholinesterase and insulin/insulin-like growth factor-1 signaling in the hippocampus is associated with Alzheimer’s disease (AD) development. Fucoidan and carrageenan are brown and red algae, respectively, with potent antibacterial, anti-inflammatory, antioxidant and antiviral acti...

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Main Authors: Ting Zhang, Xuangao Wu, Heng Yuan, Shaokai Huang, Sunmin Park
Format: Article
Language:English
Published: MDPI AG 2022-07-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/15/2301
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author Ting Zhang
Xuangao Wu
Heng Yuan
Shaokai Huang
Sunmin Park
author_facet Ting Zhang
Xuangao Wu
Heng Yuan
Shaokai Huang
Sunmin Park
author_sort Ting Zhang
collection DOAJ
description Attenuating acetylcholinesterase and insulin/insulin-like growth factor-1 signaling in the hippocampus is associated with Alzheimer’s disease (AD) development. Fucoidan and carrageenan are brown and red algae, respectively, with potent antibacterial, anti-inflammatory, antioxidant and antiviral activities. This study examined how low-molecular-weight (MW) and high-MW fucoidan and λ-carrageenan would improve memory impairment in Alzheimer’s disease-induced rats caused by an infusion of toxic amyloid-β(Aβ). Fucoidan and λ-carrageenan were dissected into low-MW by <i>Luteolibacter algae</i> and <i>Pseudoalteromonas carrageenovora</i>. Rats receiving an Aβ(25–35) infusion in the CA1 region of the hippocampus were fed dextrin (AD-Con), 1% high-MW fucoidan (AD-F-H), 1% low-MW fucoidan (AD-F-L), 1% high-MW λ-carrageenan (AD-C-H), and 1% low-MW λ-carrageenan (AD-C-L) for six weeks. Rats to receive saline infusion (Normal-Con) had an AD-Con diet. The AD-F-L group showed an improved memory function, which manifested as an enhanced Y-maze spontaneous alternation test, water maze, and passive avoidance tests, similar to the Normal-Con group. AD-F-L also potentiated hippocampal insulin signaling and increased the expression of ciliary neurotrophic factor (CNTF) and brain-derived neurotrophic factor (BDNF) in the hippocampus. AD-C-L improved the memory function mainly by increasing the BDNF content. AD-F-H and AD-C-H did not improve the memory function. Compared to AD-Con, the ascending order of AD-C-H, AD-F-H, AD-C-L, and AD-F-L increased insulin signaling by enhancing the pSTAT3→pAkt→pGSK-3β pathway. AD-F-L improved glucose tolerance the most. Compared to AD-CON, the AD-F-L treatment increased the serum acetate concentrations and compensated for the defect of cerebral glucose metabolism. AD-Con increased <i>Clostridium</i>, <i>Terrisporobacter</i> and <i>Sporofaciens</i> compared to Normal-Con, and AD-F-L and AD-C-L increased <i>Akkermentia</i>. In conclusion, AD-F-L and AD-C-L alleviated the memory function in the rats with induced AD symptoms by modulating.
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spelling doaj.art-ae04834103444ba392294cc543d1df0b2023-12-03T12:31:59ZengMDPI AGCells2073-44092022-07-011115230110.3390/cells11152301Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused RatsTing Zhang0Xuangao Wu1Heng Yuan2Shaokai Huang3Sunmin Park4Department of Bioconvergence System, Hoseo University, Asan 31499, KoreaDepartment of Bioconvergence System, Hoseo University, Asan 31499, KoreaDepartment of Bioconvergence System, Hoseo University, Asan 31499, KoreaDepartment of Bioconvergence System, Hoseo University, Asan 31499, KoreaDepartment of Bioconvergence System, Hoseo University, Asan 31499, KoreaAttenuating acetylcholinesterase and insulin/insulin-like growth factor-1 signaling in the hippocampus is associated with Alzheimer’s disease (AD) development. Fucoidan and carrageenan are brown and red algae, respectively, with potent antibacterial, anti-inflammatory, antioxidant and antiviral activities. This study examined how low-molecular-weight (MW) and high-MW fucoidan and λ-carrageenan would improve memory impairment in Alzheimer’s disease-induced rats caused by an infusion of toxic amyloid-β(Aβ). Fucoidan and λ-carrageenan were dissected into low-MW by <i>Luteolibacter algae</i> and <i>Pseudoalteromonas carrageenovora</i>. Rats receiving an Aβ(25–35) infusion in the CA1 region of the hippocampus were fed dextrin (AD-Con), 1% high-MW fucoidan (AD-F-H), 1% low-MW fucoidan (AD-F-L), 1% high-MW λ-carrageenan (AD-C-H), and 1% low-MW λ-carrageenan (AD-C-L) for six weeks. Rats to receive saline infusion (Normal-Con) had an AD-Con diet. The AD-F-L group showed an improved memory function, which manifested as an enhanced Y-maze spontaneous alternation test, water maze, and passive avoidance tests, similar to the Normal-Con group. AD-F-L also potentiated hippocampal insulin signaling and increased the expression of ciliary neurotrophic factor (CNTF) and brain-derived neurotrophic factor (BDNF) in the hippocampus. AD-C-L improved the memory function mainly by increasing the BDNF content. AD-F-H and AD-C-H did not improve the memory function. Compared to AD-Con, the ascending order of AD-C-H, AD-F-H, AD-C-L, and AD-F-L increased insulin signaling by enhancing the pSTAT3→pAkt→pGSK-3β pathway. AD-F-L improved glucose tolerance the most. Compared to AD-CON, the AD-F-L treatment increased the serum acetate concentrations and compensated for the defect of cerebral glucose metabolism. AD-Con increased <i>Clostridium</i>, <i>Terrisporobacter</i> and <i>Sporofaciens</i> compared to Normal-Con, and AD-F-L and AD-C-L increased <i>Akkermentia</i>. In conclusion, AD-F-L and AD-C-L alleviated the memory function in the rats with induced AD symptoms by modulating.https://www.mdpi.com/2073-4409/11/15/2301fucoidanλ-carrageenanAlzheimer’s diseaseshort-chain fatty acidsfermentation
spellingShingle Ting Zhang
Xuangao Wu
Heng Yuan
Shaokai Huang
Sunmin Park
Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats
Cells
fucoidan
λ-carrageenan
Alzheimer’s disease
short-chain fatty acids
fermentation
title Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats
title_full Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats
title_fullStr Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats
title_full_unstemmed Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats
title_short Mitigation of Memory Impairment with Fermented Fucoidan and λ-Carrageenan Supplementation through Modulating the Gut Microbiota and Their Metagenome Function in Hippocampal Amyloid-β Infused Rats
title_sort mitigation of memory impairment with fermented fucoidan and λ carrageenan supplementation through modulating the gut microbiota and their metagenome function in hippocampal amyloid β infused rats
topic fucoidan
λ-carrageenan
Alzheimer’s disease
short-chain fatty acids
fermentation
url https://www.mdpi.com/2073-4409/11/15/2301
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