Short-term periodic restricted feeding elicits metabolome-microbiome signatures with sex dimorphic persistence in primate intervention.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 Feb 2024
Historique:
received: 02 08 2023
accepted: 18 01 2024
medline: 6 2 2024
pubmed: 6 2 2024
entrez: 5 2 2024
Statut: epublish

Résumé

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.

Identifiants

pubmed: 38316796
doi: 10.1038/s41467-024-45359-z
pii: 10.1038/s41467-024-45359-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1088

Informations de copyright

© 2024. This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply.

Références

Le Couteur, D. G., Raubenheimer, D., Solon-Biet, S., de Cabo, R. & Simpson, S. J. Does diet influence aging? Evidence from animal studies. J. Intern. Med. https://doi.org/10.1111/joim.13530 (2022).
de Cabo, R., Carmona-Gutierrez, D., Bernier, M., Hall, M. N. & Madeo, F. The search for antiaging interventions: from elixirs to fasting regimens. Cell 157, 1515–1526 (2014).
doi: 10.1016/j.cell.2014.05.031 pubmed: 24949965 pmcid: 4254402
Mitchell, S. J. et al. Daily fasting improves health and survival in male mice independent of diet composition and calories. Cell Metab. 29, 221–228 e223 (2019).
doi: 10.1016/j.cmet.2018.08.011 pubmed: 30197301
Pak, H. H. et al. Fasting drives the metabolic, molecular and geroprotective effects of a calorie-restricted diet in mice. Nat. Metab. 3, 1327–1341 (2021).
doi: 10.1038/s42255-021-00466-9 pubmed: 34663973 pmcid: 8544824
Longo, V. D. & Mattson, M. P. Fasting: molecular mechanisms and clinical applications. Cell Metab. 19, 181–192 (2014).
doi: 10.1016/j.cmet.2013.12.008 pubmed: 24440038 pmcid: 3946160
Liu, D. et al. Calorie restriction with or without time-restricted eating in weight loss. N. Engl. J. Med. 386, 1495–1504 (2022).
doi: 10.1056/NEJMoa2114833 pubmed: 35443107
de Cabo, R. & Mattson, M. P. Effects of intermittent fasting on health, aging, and disease. N. Engl. J. Med. 381, 2541–2551 (2019).
doi: 10.1056/NEJMra1905136 pubmed: 31881139
Mattson, M. P. et al. Meal frequency and timing in health and disease. Proc. Natl Acad. Sci. USA 111, 16647–16653 (2014).
doi: 10.1073/pnas.1413965111 pubmed: 25404320 pmcid: 4250148
Diaz-Ruiz, A. et al. Diet composition influences the metabolic benefits of short cycles of very low caloric intake. Nat. Commun. 12, 6463 (2021).
doi: 10.1038/s41467-021-26654-5 pubmed: 34753921 pmcid: 8578605
Longo, V. D. & Panda, S. Fasting, circadian rhythms, and time-restricted feeding in healthy lifespan. Cell Metab. 23, 1048–1059 (2016).
doi: 10.1016/j.cmet.2016.06.001 pubmed: 27304506 pmcid: 5388543
Soty, M., Gautier-Stein, A., Rajas, F. & Mithieux, G. Gut-brain glucose signaling in energy homeostasis. Cell Metab. 25, 1231–1242 (2017).
doi: 10.1016/j.cmet.2017.04.032 pubmed: 28591631
Stekovic, S. et al. Alternate day fasting improves physiological and molecular markers of aging in healthy, non-obese humans. Cell Metab. 30, 462–476 e466 (2019).
doi: 10.1016/j.cmet.2019.07.016 pubmed: 31471173
Mattison, J. A. et al. Caloric restriction improves health and survival of rhesus monkeys. Nat. Commun. 8, 14063 (2017).
doi: 10.1038/ncomms14063 pubmed: 28094793 pmcid: 5247583
Colman, R. J. et al. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science 325, 201–204 (2009).
doi: 10.1126/science.1173635 pubmed: 19590001 pmcid: 2812811
von Schwartzenberg, R. J. et al. Caloric restriction disrupts the microbiota and colonization resistance. Nature 595, 272–277 (2021).
doi: 10.1038/s41586-021-03663-4
David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).
doi: 10.1038/nature12820 pubmed: 24336217
Bisanz, J. E., Upadhyay, V., Turnbaugh, J. A., Ly, K. & Turnbaugh, P. J. Meta-analysis reveals reproducible gut microbiome alterations in response to a high-fat diet. Cell Host Microbe 26, 265–272 e264 (2019).
doi: 10.1016/j.chom.2019.06.013 pubmed: 31324413 pmcid: 6708278
Bruggner, R. V., Bodenmiller, B., Dill, D. L., Tibshirani, R. J. & Nolan, G. P. Automated identification of stratifying signatures in cellular subpopulations. Proc. Natl Acad. Sci. USA 111, E2770–E2777 (2014).
doi: 10.1073/pnas.1408792111 pubmed: 24979804 pmcid: 4084463
Douglas, G. M. et al. PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol. 38, 685–688 (2020).
doi: 10.1038/s41587-020-0548-6 pubmed: 32483366 pmcid: 7365738
Woo, V. & Alenghat, T. Epigenetic regulation by gut microbiota. Gut Microbes 14, 2022407 (2022).
doi: 10.1080/19490976.2021.2022407 pubmed: 35000562 pmcid: 8744890
Spadaro, O. et al. Caloric restriction in humans reveals immunometabolic regulators of health span. Science 375, 671–677 (2022).
doi: 10.1126/science.abg7292 pubmed: 35143297 pmcid: 10061495
Tang, D. et al. Dietary restriction improves repopulation but impairs lymphoid differentiation capacity of hematopoietic stem cells in early aging. J. Exp. Med. 213, 535–553 (2016).
doi: 10.1084/jem.20151100 pubmed: 26951333 pmcid: 4821645
Yanai, H. et al. Male rat leukocyte population dynamics predict a window for intervention in aging. eLife 11, e76808 (2022).
doi: 10.7554/eLife.76808 pubmed: 35507394 pmcid: 9150891
Healey, G. R., Murphy, R., Brough, L., Butts, C. A. & Coad, J. Interindividual variability in gut microbiota and host response to dietary interventions. Nutr. Rev. 75, 1059–1080 (2017).
doi: 10.1093/nutrit/nux062 pubmed: 29190368
Ghosh, T. S., Shanahan, F. & O’Toole, P. W. The gut microbiome as a modulator of healthy ageing. Nat. Rev. Gastroenterol. Hepatol. 19, 565–584 (2022).
doi: 10.1038/s41575-022-00605-x pubmed: 35468952 pmcid: 9035980
Clarke, S. F. et al. The gut microbiota and its relationship to diet and obesity: new insights. Gut Microbes 3, 186–202 (2012).
doi: 10.4161/gmic.20168 pubmed: 22572830 pmcid: 3427212
Barcena, C. et al. Healthspan and lifespan extension by fecal microbiota transplantation into progeroid mice. Nat. Med. 25, 1234–1242 (2019).
doi: 10.1038/s41591-019-0504-5 pubmed: 31332389
Castaner, O. et al. The gut microbiome profile in obesity: a systematic review. Int J. Endocrinol. 2018, 4095789 (2018).
pubmed: 29849617 pmcid: 5933040
Froy, O., Chapnik, N. & Miskin, R. Effect of intermittent fasting on circadian rhythms in mice depends on feeding time. Mech. Ageing Dev. 130, 154–160 (2009).
doi: 10.1016/j.mad.2008.10.006 pubmed: 19041664
Voigt, R. M., Forsyth, C. B., Green, S. J., Engen, P. A. & Keshavarzian, A. Circadian rhythm and the gut microbiome. Int. Rev. Neurobiol. 131, 193–205 (2016).
doi: 10.1016/bs.irn.2016.07.002 pubmed: 27793218
Aon, M. A. et al. Untangling determinants of enhanced health and lifespan through a multi-omics approach in mice. Cell Metab. 32, 100–116 e104 (2020).
doi: 10.1016/j.cmet.2020.04.018 pubmed: 32413334 pmcid: 8214079
Wongkittichote, P., Ah Mew, N. & Chapman, K. A. Propionyl-CoA carboxylase—a review. Mol. Genet. Metab. 122, 145–152 (2017).
doi: 10.1016/j.ymgme.2017.10.002 pubmed: 29033250 pmcid: 5725275
Basolo, A. et al. Effects of underfeeding and oral vancomycin on gut microbiome and nutrient absorption in humans. Nat. Med. 26, 589–598 (2020).
doi: 10.1038/s41591-020-0801-z pubmed: 32235930

Auteurs

Hagai Yanai (H)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA.

Bongsoo Park (B)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA.

Hyunwook Koh (H)

Department of Applied Mathematics & Statistics, The State University of New York, Korea (SUNY Korea), Incheon, South Korea.

Hyo Jung Jang (HJ)

Department of Applied Mathematics & Statistics, The State University of New York, Korea (SUNY Korea), Incheon, South Korea.

Kelli L Vaughan (KL)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA.

Mayuri Tanaka-Yano (M)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA.

Miguel Aon (M)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA.

Madison Blanton (M)

Department of Microbiology, Immunology and Molecular Genetics, College of Medicine, University of Kentucky, Lexington, KY, USA.

Ilhem Messaoudi (I)

Department of Microbiology, Immunology and Molecular Genetics, College of Medicine, University of Kentucky, Lexington, KY, USA.

Alberto Diaz-Ruiz (A)

Laboratory of Cellular and Molecular Gerontology, Precision Nutrition and Aging Program, Institute IMDEA Food (CEI UAM+CSIC), Madrid, Spain.
CIBER Physiopathology of Obesity and Nutrition (CIBERobn), Madrid, Spain.

Julie A Mattison (JA)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA.

Isabel Beerman (I)

Translational Gerontology Branch, National Institute on Aging, NIH, Baltimore, MD, USA. isabel.beerman@nih.gov.

Classifications MeSH