Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice
IntroductionCognitive decline is a common consequence of aging. Dietary patterns that lack fibers and are high in saturated fats worsen cognitive impairment by triggering pro-inflammatory pathways and metabolic dysfunctions. Emerging evidence highlights the neurocognitive benefits of fiber-rich diet...
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Nutrition |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnut.2024.1322201/full |
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| author | Saurabh Kadyan Gwoncheol Park Nathaniel Hochuli Katelyn Miller Bo Wang Ravinder Nagpal |
| author_facet | Saurabh Kadyan Gwoncheol Park Nathaniel Hochuli Katelyn Miller Bo Wang Ravinder Nagpal |
| author_sort | Saurabh Kadyan |
| collection | DOAJ |
| description | IntroductionCognitive decline is a common consequence of aging. Dietary patterns that lack fibers and are high in saturated fats worsen cognitive impairment by triggering pro-inflammatory pathways and metabolic dysfunctions. Emerging evidence highlights the neurocognitive benefits of fiber-rich diets and the crucial role of gut-microbiome-brain signaling. However, the mechanisms of this diet-microbiome-brain regulation remain largely unclear.MethodsAccordingly, we herein investigated the unexplored neuroprotective mechanisms of dietary pulses-derived resistant starch (RS) in improving aging-associated neurocognitive function in an aged (60-weeks old) murine model carrying a human microbiome.Results and discussionFollowing 20-weeks dietary regimen which included a western-style diet without (control; CTL) or with 5% w/w fortification with RS from pinto beans (PTB), black-eyed-peas (BEP), lentils (LEN), chickpeas (CKP), or inulin fiber (INU), we find that RS, particularly from LEN, ameliorate the cognitive impairments induced by western diet. Mechanistically, RS-mediated improvements in neurocognitive assessments are attributed to positive remodeling of the gut microbiome-metabolome arrays, which include increased short-chain fatty acids and reduced branched-chain amino acids levels. This microbiome-metabolite-brain signaling cascade represses neuroinflammation, cellular senescence, and serum leptin/insulin levels, while enhancing lipid metabolism through improved hepatic function. Altogether, the data demonstrate the prebiotic effects of RS in improving neurocognitive function via modulating the gut-brain axis. |
| first_indexed | 2024-03-08T09:59:43Z |
| format | Article |
| id | doaj.art-4850c61659e4479393529dc4a1dc346a |
| institution | Directory Open Access Journal |
| issn | 2296-861X |
| language | English |
| last_indexed | 2024-03-08T09:59:43Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Nutrition |
| spelling | doaj.art-4850c61659e4479393529dc4a1dc346a2024-01-29T12:18:32ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2024-01-011110.3389/fnut.2024.13222011322201Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged miceSaurabh Kadyan0Gwoncheol Park1Nathaniel Hochuli2Katelyn Miller3Bo Wang4Ravinder Nagpal5The Gut Biome Lab, Department of Health, Nutrition, and Food Sciences, College of Education, Health, and Human Sciences, Florida State University, Tallahassee, FL, United StatesThe Gut Biome Lab, Department of Health, Nutrition, and Food Sciences, College of Education, Health, and Human Sciences, Florida State University, Tallahassee, FL, United StatesThe Gut Biome Lab, Department of Health, Nutrition, and Food Sciences, College of Education, Health, and Human Sciences, Florida State University, Tallahassee, FL, United StatesThe Gut Biome Lab, Department of Health, Nutrition, and Food Sciences, College of Education, Health, and Human Sciences, Florida State University, Tallahassee, FL, United StatesDepartment of Biomedical and Chemical Engineering and Sciences, Florida Institute of Technology, Melbourne, FL, United StatesThe Gut Biome Lab, Department of Health, Nutrition, and Food Sciences, College of Education, Health, and Human Sciences, Florida State University, Tallahassee, FL, United StatesIntroductionCognitive decline is a common consequence of aging. Dietary patterns that lack fibers and are high in saturated fats worsen cognitive impairment by triggering pro-inflammatory pathways and metabolic dysfunctions. Emerging evidence highlights the neurocognitive benefits of fiber-rich diets and the crucial role of gut-microbiome-brain signaling. However, the mechanisms of this diet-microbiome-brain regulation remain largely unclear.MethodsAccordingly, we herein investigated the unexplored neuroprotective mechanisms of dietary pulses-derived resistant starch (RS) in improving aging-associated neurocognitive function in an aged (60-weeks old) murine model carrying a human microbiome.Results and discussionFollowing 20-weeks dietary regimen which included a western-style diet without (control; CTL) or with 5% w/w fortification with RS from pinto beans (PTB), black-eyed-peas (BEP), lentils (LEN), chickpeas (CKP), or inulin fiber (INU), we find that RS, particularly from LEN, ameliorate the cognitive impairments induced by western diet. Mechanistically, RS-mediated improvements in neurocognitive assessments are attributed to positive remodeling of the gut microbiome-metabolome arrays, which include increased short-chain fatty acids and reduced branched-chain amino acids levels. This microbiome-metabolite-brain signaling cascade represses neuroinflammation, cellular senescence, and serum leptin/insulin levels, while enhancing lipid metabolism through improved hepatic function. Altogether, the data demonstrate the prebiotic effects of RS in improving neurocognitive function via modulating the gut-brain axis.https://www.frontiersin.org/articles/10.3389/fnut.2024.1322201/fullmicrobiotaplant polysaccharidesmetabolic diseasesagingneuroinflammation |
| spellingShingle | Saurabh Kadyan Gwoncheol Park Nathaniel Hochuli Katelyn Miller Bo Wang Ravinder Nagpal Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice Frontiers in Nutrition microbiota plant polysaccharides metabolic diseases aging neuroinflammation |
| title | Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice |
| title_full | Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice |
| title_fullStr | Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice |
| title_full_unstemmed | Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice |
| title_short | Resistant starches from dietary pulses improve neurocognitive health via gut-microbiome-brain axis in aged mice |
| title_sort | resistant starches from dietary pulses improve neurocognitive health via gut microbiome brain axis in aged mice |
| topic | microbiota plant polysaccharides metabolic diseases aging neuroinflammation |
| url | https://www.frontiersin.org/articles/10.3389/fnut.2024.1322201/full |
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