Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention
Abstract Dietary restriction has shown benefits in physiological, metabolic, and molecular signatures associated with aging but is a difficult lifestyle to maintain for most individuals. In mice, a less restrictive diet that allows for cyclical periods of reduced calories mitigates aging phenotypes,...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-45359-z |
| _version_ | 1797274060330106880 |
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| author | Hagai Yanai Bongsoo Park Hyunwook Koh Hyo Jung Jang Kelli L. Vaughan Mayuri Tanaka-Yano Miguel Aon Madison Blanton Ilhem Messaoudi Alberto Diaz-Ruiz Julie A. Mattison Isabel Beerman |
| author_facet | Hagai Yanai Bongsoo Park Hyunwook Koh Hyo Jung Jang Kelli L. Vaughan Mayuri Tanaka-Yano Miguel Aon Madison Blanton Ilhem Messaoudi Alberto Diaz-Ruiz Julie A. Mattison Isabel Beerman |
| author_sort | Hagai Yanai |
| collection | DOAJ |
| description | Abstract Dietary restriction has shown benefits in physiological, metabolic, and molecular signatures associated with aging but is a difficult lifestyle to maintain for most individuals. In mice, a less restrictive diet that allows for cyclical periods of reduced calories mitigates aging phenotypes, yet the effects of such an intervention in a genetically heterogenous, higher-order mammal has not been examined. Here, using middle-aged rhesus macaques matched for age and sex, we show that a regimen of 4 days of low-calorie intake followed by 10 days of ad libitum feeding (4:10 diet) performed in repeating cycles over 12 weeks led to significant loss of weight and fat percentage, despite the free access to food for most of the study duration. We show the 4-day restriction period is sufficient to drive alterations to the serum metabolome characterized by substantial differences in lipid classes. These phenotypes were paralleled by changes in the gut microbiome of restricted monkeys that highlight the involvement of a microbiome-metabolome axis. This regimen shows promising phenotypes, with some sex-dimorphic responses, including residual memory of the diet. As many calorie restriction interventions are difficult to sustain, we propose that this short-term diet may be easier to adhere to and have benefits directly relevant to human aging. |
| first_indexed | 2024-03-07T14:52:58Z |
| format | Article |
| id | doaj.art-db9957647c4c41dba19b324fff38ec43 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-07T14:52:58Z |
| publishDate | 2024-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-db9957647c4c41dba19b324fff38ec432024-03-05T19:37:42ZengNature PortfolioNature Communications2041-17232024-02-0115111110.1038/s41467-024-45359-zShort-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate interventionHagai Yanai0Bongsoo Park1Hyunwook Koh2Hyo Jung Jang3Kelli L. Vaughan4Mayuri Tanaka-Yano5Miguel Aon6Madison Blanton7Ilhem Messaoudi8Alberto Diaz-Ruiz9Julie A. Mattison10Isabel Beerman11Translational Gerontology Branch, National Institute on Aging, NIHTranslational Gerontology Branch, National Institute on Aging, NIHDepartment of Applied Mathematics & Statistics, The State University of New York, Korea (SUNY Korea)Department of Applied Mathematics & Statistics, The State University of New York, Korea (SUNY Korea)Translational Gerontology Branch, National Institute on Aging, NIHTranslational Gerontology Branch, National Institute on Aging, NIHTranslational Gerontology Branch, National Institute on Aging, NIHDepartment of Microbiology, Immunology and Molecular Genetics, College of Medicine, University of KentuckyDepartment of Microbiology, Immunology and Molecular Genetics, College of Medicine, University of KentuckyLaboratory of Cellular and Molecular Gerontology, Precision Nutrition and Aging Program, Institute IMDEA Food (CEI UAM+CSIC)Translational Gerontology Branch, National Institute on Aging, NIHTranslational Gerontology Branch, National Institute on Aging, NIHAbstract Dietary restriction has shown benefits in physiological, metabolic, and molecular signatures associated with aging but is a difficult lifestyle to maintain for most individuals. In mice, a less restrictive diet that allows for cyclical periods of reduced calories mitigates aging phenotypes, yet the effects of such an intervention in a genetically heterogenous, higher-order mammal has not been examined. Here, using middle-aged rhesus macaques matched for age and sex, we show that a regimen of 4 days of low-calorie intake followed by 10 days of ad libitum feeding (4:10 diet) performed in repeating cycles over 12 weeks led to significant loss of weight and fat percentage, despite the free access to food for most of the study duration. We show the 4-day restriction period is sufficient to drive alterations to the serum metabolome characterized by substantial differences in lipid classes. These phenotypes were paralleled by changes in the gut microbiome of restricted monkeys that highlight the involvement of a microbiome-metabolome axis. This regimen shows promising phenotypes, with some sex-dimorphic responses, including residual memory of the diet. As many calorie restriction interventions are difficult to sustain, we propose that this short-term diet may be easier to adhere to and have benefits directly relevant to human aging.https://doi.org/10.1038/s41467-024-45359-z |
| spellingShingle | Hagai Yanai Bongsoo Park Hyunwook Koh Hyo Jung Jang Kelli L. Vaughan Mayuri Tanaka-Yano Miguel Aon Madison Blanton Ilhem Messaoudi Alberto Diaz-Ruiz Julie A. Mattison Isabel Beerman Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention Nature Communications |
| title | Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention |
| title_full | Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention |
| title_fullStr | Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention |
| title_full_unstemmed | Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention |
| title_short | Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention |
| title_sort | short term periodic restricted feeding elicits metabolome microbiome signatures with sex dimorphic persistence in primate intervention |
| url | https://doi.org/10.1038/s41467-024-45359-z |
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