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Article: Late-life isoleucine restriction promotes physiological and molecular signatures of healthy aging.

Yeh, Chung-Yang / Chini, Lucas C S / Davidson, Jessica W / Garcia, Gonzalo G / Gallagher, Meredith S / Freichels, Isaac T / Calubag, Mariah F / Rodgers, Allison C / Green, Cara L / Babygirija, Reji / Sonsalla, Michelle M / Pak, Heidi H / Trautman, Michaela / Hacker, Timothy A / Miller, Richard A / Simcox, Judith / Lamming, Dudley W

bioRxiv : the preprint server for biology

2024

Abstract: In defiance of the paradigm that calories from all sources are equivalent, we and others have shown that dietary protein is a dominant regulator of healthy aging. The restriction of protein or the branched-chain amino acid isoleucine promotes healthspan ... ...

Abstract	In defiance of the paradigm that calories from all sources are equivalent, we and others have shown that dietary protein is a dominant regulator of healthy aging. The restriction of protein or the branched-chain amino acid isoleucine promotes healthspan and extends lifespan when initiated in young or adult mice. However, many interventions are less efficacious or even deleterious when initiated in aged animals. Here, we investigate the physiological, metabolic, and molecular consequences of consuming a diet with a 67% reduction of all amino acids (Low AA), or of isoleucine alone (Low Ile), in male and female C57BL/6J.Nia mice starting at 20 months of age. We find that both diet regimens effectively reduce adiposity and improve glucose tolerance, which were benefits that were not mediated by reduced calorie intake. Both diets improve specific aspects of frailty, slow multiple molecular indicators of aging rate, and rejuvenate the aging heart and liver at the molecular level. These results demonstrate that Low AA and Low Ile diets can drive youthful physiological and molecular signatures, and support the possibility that these dietary interventions could help to promote healthy aging in older adults.
Language	English
Publishing date	2024-01-09
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.02.06.527311
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Article: FGF21 has a sex-specific role in calorie-restriction-induced beiging of white adipose tissue in mice.

Calubag, Mariah F / Ademi, Ismail / Yeh, Chung-Yang / Babygirija, Reji / Pak, Heidi H / Bhoopat, Alyssa M / Kasza, Ildiko / Green, Cara L / Sonsalla, Michelle M / Lamming, Dudley W

Aging Biology

2023 Volume 1

Abstract: Calorie restriction (CR) promotes healthspan and extends the lifespan of diverse organisms, including mice, and there is intense interest in understanding the molecular mechanisms by which CR functions. Some studies have demonstrated that CR induces ... ...

Abstract	Calorie restriction (CR) promotes healthspan and extends the lifespan of diverse organisms, including mice, and there is intense interest in understanding the molecular mechanisms by which CR functions. Some studies have demonstrated that CR induces fibroblast growth factor 21 (FGF21), a hormone that regulates energy balance and that when overexpressed, promotes metabolic health and longevity in mice, but the role of FGF21 in the response to CR has not been fully investigated. We directly examined the role of FGF21 in the physiological and metabolic response to a CR diet by feeding
Language	English
Publishing date	2023-05-22
Publishing country	United States
Document type	Journal Article
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Article: Protein restriction slows the development and progression of Alzheimer's disease in mice.

Research square

2024

Abstract: Dietary protein is a critical regulator of metabolic health and aging. Low protein diets are associated with healthy aging in humans, and many independent groups of researchers have shown that dietary protein restriction (PR) extends the lifespan and ... ...

Abstract	Dietary protein is a critical regulator of metabolic health and aging. Low protein diets are associated with healthy aging in humans, and many independent groups of researchers have shown that dietary protein restriction (PR) extends the lifespan and healthspan of mice. Here, we examined the effect of PR on metabolic health and the development and progression of Alzheimer's disease (AD) in the 3xTg mouse model of AD. We found that PR has metabolic benefits for 3xTg mice and non-transgenic controls of both sexes, promoting leanness and glycemic control in 3xTg mice and rescuing the glucose intolerance of 3xTg females. We found that PR induces sex-specific alterations in circulating metabolites and in the brain metabolome and lipidome, downregulating sphingolipid subclasses including ceramides, glucosylceramides, and sphingomyelins in 3xTg females. Consumption of a PR diet starting at 6 months of age reduced AD pathology in conjunction with reduced mTORC1 activity, increased autophagy, and had cognitive benefits for 3xTg mice. Finally, PR improved the survival of 3xTg mice. Our results demonstrate that PR slows the progression of AD at molecular and pathological levels, preserves cognition in this mouse model of AD, and suggests that PR or pharmaceutical interventions that mimic the effects of this diet may hold promise as a treatment for AD.
Language	English
Publishing date	2024-04-24
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-3342413/v2
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Article ; Online: The Second Annual Symposium of the Midwest Aging Consortium: The Future of Aging Research in the Midwestern United States.

Green, Cara L / Englund, Davis A / Das, Srijit / Herrerias, Mariana M / Yousefzadeh, Matthew J / Grant, Rogan A / Clark, Josef / Pak, Heidi H / Liu, Peiduo / Bai, Hua / Prahlad, Veena / Lamming, Dudley W / Chusyd, Daniella E

The journals of gerontology. Series A, Biological sciences and medical sciences

2021 Volume 76, Issue 12, Page(s) 2156–2161

Abstract: While the average human life span continues to increase, there is little evidence that this is leading to a contemporaneous increase in "healthy years" experienced by our aging population. Consequently, many scientists focus their research on ... ...

Abstract	While the average human life span continues to increase, there is little evidence that this is leading to a contemporaneous increase in "healthy years" experienced by our aging population. Consequently, many scientists focus their research on understanding the process of aging and trialing interventions that can promote healthspan. The 2021 Midwest Aging Consortium consensus statement is to develop and further the understanding of aging and age-related disease using the wealth of expertise across universities in the Midwestern United States. This report summarizes the cutting-edge research covered in a virtual symposium held by a consortium of researchers in the Midwestern United States, spanning topics such as senescence biomarkers, serotonin-induced DNA protection, immune system development, multisystem impacts of aging, neural decline following severe infection, the unique transcriptional impact of calorie restriction of different fat depots, the pivotal role of fasting in calorie restriction, the impact of peroxisome dysfunction, and the influence of early life trauma on health. The symposium speakers presented data from studies conducted in a variety of common laboratory animals as well as less-common species, including Caenorhabditis elegans, Drosophila, mice, rhesus macaques, elephants, and humans. The consensus of the symposium speakers is that this consortium highlights the strength of aging research in the Midwestern United States as well as the benefits of a collaborative and diverse approach to geroscience.
MeSH term(s)	Aging ; Animals ; Biomedical Research/trends ; Caloric Restriction ; Geroscience/trends ; Humans ; Longevity ; Macaca mulatta ; Models, Animal
Language	English
Publishing date	2021-07-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1223643-3
ISSN	1758-535X ; 1079-5006
ISSN (online)	1758-535X
ISSN	1079-5006
DOI	10.1093/gerona/glab210
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Article ; Online: Dietary restriction of isoleucine increases healthspan and lifespan of genetically heterogeneous mice.

Cell metabolism

2023 Volume 35, Issue 11, Page(s) 1976–1995.e6

Abstract: Low-protein diets promote health and longevity in diverse species. Restriction of the branched-chain amino acids (BCAAs) leucine, isoleucine, and valine recapitulates many of these benefits in young C57BL/6J mice. Restriction of dietary isoleucine (IleR) ...

Abstract	Low-protein diets promote health and longevity in diverse species. Restriction of the branched-chain amino acids (BCAAs) leucine, isoleucine, and valine recapitulates many of these benefits in young C57BL/6J mice. Restriction of dietary isoleucine (IleR) is sufficient to promote metabolic health and is required for many benefits of a low-protein diet in C57BL/6J males. Here, we test the hypothesis that IleR will promote healthy aging in genetically heterogeneous adult UM-HET3 mice. We find that IleR improves metabolic health in young and old HET3 mice, promoting leanness and glycemic control in both sexes, and reprograms hepatic metabolism in a sex-specific manner. IleR reduces frailty and extends the lifespan of male and female mice, but to a greater degree in males. Our results demonstrate that IleR increases healthspan and longevity in genetically diverse mice and suggests that IleR, or pharmaceuticals that mimic this effect, may have potential as a geroprotective intervention.
MeSH term(s)	Male ; Female ; Animals ; Mice ; Isoleucine/pharmacology ; Longevity ; Health Promotion ; Mice, Inbred C57BL ; Amino Acids, Branched-Chain/metabolism
Chemical Substances	Isoleucine (04Y7590D77) ; Amino Acids, Branched-Chain
Language	English
Publishing date	2023-11-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2176834-1
ISSN	1932-7420 ; 1550-4131
ISSN (online)	1932-7420
ISSN	1550-4131
DOI	10.1016/j.cmet.2023.10.005
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Article ; Online: Fasting drives the metabolic, molecular and geroprotective effects of a calorie-restricted diet in mice.

Pak, Heidi H / Haws, Spencer A / Green, Cara L / Koller, Mikaela / Lavarias, Mitchell T / Richardson, Nicole E / Yang, Shany E / Dumas, Sabrina N / Sonsalla, Michelle / Bray, Lindsey / Johnson, Michelle / Barnes, Stephen / Darley-Usmar, Victor / Zhang, Jianhua / Yen, Chi-Liang Eric / Denu, John M / Lamming, Dudley W

Nature metabolism

2021 Volume 3, Issue 10, Page(s) 1327–1341

Abstract: Calorie restriction (CR) promotes healthy ageing in diverse species. Recently, it has been shown that fasting for a portion of each day has metabolic benefits and promotes lifespan. These findings complicate the interpretation of rodent CR studies, in ... ...

Abstract	Calorie restriction (CR) promotes healthy ageing in diverse species. Recently, it has been shown that fasting for a portion of each day has metabolic benefits and promotes lifespan. These findings complicate the interpretation of rodent CR studies, in which animals typically eat only once per day and rapidly consume their food, which collaterally imposes fasting. Here we show that a prolonged fast is necessary for key metabolic, molecular and geroprotective effects of a CR diet. Using a series of feeding regimens, we dissect the effects of calories and fasting, and proceed to demonstrate that fasting alone recapitulates many of the physiological and molecular effects of CR. Our results shed new light on how both when and how much we eat regulate metabolic health and longevity, and demonstrate that daily prolonged fasting, and not solely reduced caloric intake, is likely responsible for the metabolic and geroprotective benefits of a CR diet.
MeSH term(s)	Aging/metabolism ; Animals ; Caloric Restriction ; Longevity/physiology ; Mice
Language	English
Publishing date	2021-10-18
Publishing country	Germany
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	2522-5812
ISSN (online)	2522-5812
DOI	10.1038/s42255-021-00466-9
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Article ; Online: Sex and genetic background define the metabolic, physiologic, and molecular response to protein restriction.

Green, Cara L / Pak, Heidi H / Richardson, Nicole E / Flores, Victoria / Yu, Deyang / Tomasiewicz, Jay L / Dumas, Sabrina N / Kredell, Katherine / Fan, Jesse W / Kirsh, Charlie / Chaiyakul, Krittisak / Murphy, Michaela E / Babygirija, Reji / Barrett-Wilt, Gregory A / Rabinowitz, Joshua / Ong, Irene M / Jang, Cholsoon / Simcox, Judith / Lamming, Dudley W

Cell metabolism

2022 Volume 34, Issue 2, Page(s) 209–226.e5

Abstract: Low-protein diets promote metabolic health in humans and rodents. Despite evidence that sex and genetic background are key factors in the response to diet, most protein intake studies examine only a single strain and sex of mice. Using multiple strains ... ...

Abstract	Low-protein diets promote metabolic health in humans and rodents. Despite evidence that sex and genetic background are key factors in the response to diet, most protein intake studies examine only a single strain and sex of mice. Using multiple strains and both sexes of mice, we find that improvements in metabolic health in response to reduced dietary protein strongly depend on sex and strain. While some phenotypes were conserved across strains and sexes, including increased glucose tolerance and energy expenditure, we observed high variability in adiposity, insulin sensitivity, and circulating hormones. Using a multi-omics approach, we identified mega-clusters of differentially expressed hepatic genes, metabolites, and lipids associated with each phenotype, providing molecular insight into the differential response to protein restriction. Our results highlight the importance of sex and genetic background in the response to dietary protein level, and the potential importance of a personalized medicine approach to dietary interventions.
MeSH term(s)	Animals ; Diet, Protein-Restricted ; Energy Metabolism/genetics ; Female ; Fibroblast Growth Factors/metabolism ; Genetic Background ; Insulin Resistance/genetics ; Liver/metabolism ; Male ; Mice
Chemical Substances	Fibroblast Growth Factors (62031-54-3)
Language	English
Publishing date	2022-02-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2176834-1
ISSN	1932-7420 ; 1550-4131
ISSN (online)	1932-7420
ISSN	1550-4131
DOI	10.1016/j.cmet.2021.12.018
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Article ; Online: The Metabolic Response to a Low Amino Acid Diet is Independent of Diet-Induced Shifts in the Composition of the Gut Microbiome.

Pak, Heidi H / Cummings, Nicole E / Green, Cara L / Brinkman, Jacqueline A / Yu, Deyang / Tomasiewicz, Jay L / Yang, Shany E / Boyle, Colin / Konon, Elizabeth N / Ong, Irene M / Lamming, Dudley W

Scientific reports

2019 Volume 9, Issue 1, Page(s) 67

Abstract: Obesity and type 2 diabetes are increasing in prevalence around the world, and there is a clear need for new and effective strategies to promote metabolic health. A low protein (LP) diet improves metabolic health in both rodents and humans, but the ... ...

Abstract	Obesity and type 2 diabetes are increasing in prevalence around the world, and there is a clear need for new and effective strategies to promote metabolic health. A low protein (LP) diet improves metabolic health in both rodents and humans, but the mechanisms that underlie this effect remain unknown. The gut microbiome has recently emerged as a potent regulator of host metabolism and the response to diet. Here, we demonstrate that a LP diet significantly alters the taxonomic composition of the gut microbiome at the phylum level, altering the relative abundance of Actinobacteria, Bacteroidetes, and Firmicutes. Transcriptional profiling suggested that any impact of the microbiome on liver metabolism was likely independent of the microbiome-farnesoid X receptor (FXR) axis. We therefore tested the ability of a LP diet to improve metabolic health following antibiotic ablation of the gut microbiota. We found that a LP diet promotes leanness, increases energy expenditure, and improves glycemic control equally well in mice treated with antibiotics as in untreated control animals. Our results demonstrate that the beneficial effects of a LP diet on glucose homeostasis, energy balance, and body composition are unlikely to be mediated by diet-induced changes in the taxonomic composition of the gut microbiome.
MeSH term(s)	Amino Acids/metabolism ; Animals ; Biota ; Diet/methods ; Gene Expression Profiling ; Intestines/microbiology ; Metabolism ; Mice
Chemical Substances	Amino Acids
Language	English
Publishing date	2019-01-11
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-018-37177-3
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Article ; Online: Lifelong restriction of dietary branched-chain amino acids has sex-specific benefits for frailty and lifespan in mice.

Nature aging

2021 Volume 1, Issue 1, Page(s) 73–86

Abstract: Protein restricted (PR) diets promote health and longevity in many species. While the precise components of a PR diet that mediate the beneficial effects to longevity have not been defined, we recently showed that many metabolic effects of PR can be ... ...

Abstract	Protein restricted (PR) diets promote health and longevity in many species. While the precise components of a PR diet that mediate the beneficial effects to longevity have not been defined, we recently showed that many metabolic effects of PR can be attributed to reduced dietary levels of the branched-chain amino acids (BCAAs) leucine, isoleucine, and valine. Here, we demonstrate that restricting dietary BCAAs increases the survival of two different progeroid mouse models, delays frailty and promotes the metabolic health of wild-type C57BL/6J mice when started in midlife, and leads to a 30% increase in lifespan and a reduction in frailty in male, but not female, wild-type mice when fed lifelong. Our results demonstrate that restricting dietary BCAAs can increase healthspan and longevity in mice, and suggest that reducing dietary BCAAs may hold potential as a translatable intervention to promote healthy aging.
MeSH term(s)	Female ; Male ; Animals ; Mice ; Amino Acids, Branched-Chain/metabolism ; Longevity ; Frailty/prevention & control ; Health Promotion ; Mice, Inbred C57BL ; Diet
Chemical Substances	Amino Acids, Branched-Chain
Language	English
Publishing date	2021-01-14
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2662-8465
ISSN (online)	2662-8465
DOI	10.1038/s43587-020-00006-2
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Article ; Online: The adverse metabolic effects of branched-chain amino acids are mediated by isoleucine and valine.

Yu, Deyang / Richardson, Nicole E / Green, Cara L / Spicer, Alexandra B / Murphy, Michaela E / Flores, Victoria / Jang, Cholsoon / Kasza, Ildiko / Nikodemova, Maria / Wakai, Matthew H / Tomasiewicz, Jay L / Yang, Shany E / Miller, Blake R / Pak, Heidi H / Brinkman, Jacqueline A / Rojas, Jennifer M / Quinn, William J / Cheng, Eunhae P / Konon, Elizabeth N /

Haider, Lexington R / Finke, Megan / Sonsalla, Michelle / Alexander, Caroline M / Rabinowitz, Joshua D / Baur, Joseph A / Malecki, Kristen C / Lamming, Dudley W

Cell metabolism

2021 Volume 33, Issue 5, Page(s) 905–922.e6

Abstract: Low-protein diets promote metabolic health in rodents and humans, and the benefits of low-protein diets are recapitulated by specifically reducing dietary levels of the three branched-chain amino acids (BCAAs), leucine, isoleucine, and valine. Here, we ... ...

Abstract	Low-protein diets promote metabolic health in rodents and humans, and the benefits of low-protein diets are recapitulated by specifically reducing dietary levels of the three branched-chain amino acids (BCAAs), leucine, isoleucine, and valine. Here, we demonstrate that each BCAA has distinct metabolic effects. A low isoleucine diet reprograms liver and adipose metabolism, increasing hepatic insulin sensitivity and ketogenesis and increasing energy expenditure, activating the FGF21-UCP1 axis. Reducing valine induces similar but more modest metabolic effects, whereas these effects are absent with low leucine. Reducing isoleucine or valine rapidly restores metabolic health to diet-induced obese mice. Finally, we demonstrate that variation in dietary isoleucine levels helps explain body mass index differences in humans. Our results reveal isoleucine as a key regulator of metabolic health and the adverse metabolic response to dietary BCAAs and suggest reducing dietary isoleucine as a new approach to treating and preventing obesity and diabetes.
MeSH term(s)	Adipose Tissue, White/metabolism ; Amino Acids, Branched-Chain/metabolism ; Animals ; Body Mass Index ; Diet/veterinary ; Energy Metabolism ; Fibroblast Growth Factors/deficiency ; Fibroblast Growth Factors/genetics ; Fibroblast Growth Factors/metabolism ; Humans ; Isoleucine/metabolism ; Liver/metabolism ; Male ; Mechanistic Target of Rapamycin Complex 1/metabolism ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Obesity/metabolism ; Obesity/pathology ; Protein Serine-Threonine Kinases/metabolism ; Uncoupling Protein 1/genetics ; Uncoupling Protein 1/metabolism ; Valine/metabolism
Chemical Substances	Amino Acids, Branched-Chain ; Uncoupling Protein 1 ; fibroblast growth factor 21 ; Isoleucine (04Y7590D77) ; Fibroblast Growth Factors (62031-54-3) ; Eif2ak4 protein, mouse (EC 2.7.11.1) ; Mechanistic Target of Rapamycin Complex 1 (EC 2.7.11.1) ; Protein Serine-Threonine Kinases (EC 2.7.11.1) ; Valine (HG18B9YRS7)
Language	English
Publishing date	2021-04-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2176834-1
ISSN	1932-7420 ; 1550-4131
ISSN (online)	1932-7420
ISSN	1550-4131
DOI	10.1016/j.cmet.2021.03.025
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