Lifelong calorie restriction affects indicators of colonic health in aging C57Bl/6J mice

Dieuwertje E.G. Kok, Fenni Rusli, Benthe van der Lugt, Carolien Lute, Luca Laghi, Stefano Salvioli, Gianfranco Picone, Claudio Franceschi, Hauke Smidt, Jacques Vervoort, Ellen Kampman, Michael Müller, Wilma T. Steegenga

Research output: Contribution to journalArticleAcademicpeer-review

5 Citations (Scopus)

Abstract

Diminished colonic health is associated with various age-related pathologies. Calorie restriction (CR) is an effective strategy to increase healthy lifespan, although underlying mechanisms are not fully elucidated. Here, we report the effects of lifelong CR on indicators of colonic health in aging C57Bl/6J mice. Compared to an ad libitum control and moderate-fat diet, 30% energy reduction was associated with attenuated immune- and inflammation-related gene expression in the colon. Furthermore, expression of genes involved in lipid metabolism was higher upon CR, which may point towards efficient regulation of energy metabolism. The relative abundance of bacteria considered beneficial to colonic health, such as Bifidobacterium and Lactobacillus, increased in the mice exposed to CR for 28 months as compared to the other diet groups. We found lower plasma levels of interleukin-6 and lower levels of various metabolites, among which are bile acids, in the colonic luminal content of CR-exposed mice as compared to the other diet groups. Switching from CR to an ad libitum moderate-fat diet at old age (24 months) revealed remarkable phenotypic plasticity in terms of gene expression, microbiota composition and metabolite levels, although expression of a subset of genes remained CR-associated. This study demonstrated in a comprehensive way that CR affects indicators of colonic health in aging mice. Our findings provide unique leads for further studies that need to address optimal and feasible strategies for prolonged energy deprivation, which may contribute to healthy aging.
Original languageEnglish
Pages (from-to)152-164
JournalJournal of Nutritional Biochemistry
Volume56
DOIs
Publication statusPublished - 1 Jun 2018

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Nutrition
Aging of materials
Health
Diet
Metabolites
Gene Expression
Gene expression
Genes
Fats
Bifidobacterium
Microbiota
Lactobacillus
Pathology
Bile Acids and Salts
Lipid Metabolism
Energy Metabolism
Plasticity
Interleukin-6
Bacteria
Colon

Keywords

  • Aging
  • Calorie restriction
  • Colonic health
  • Gene expression
  • Gut microbiota
  • Metabolites

Cite this

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title = "Lifelong calorie restriction affects indicators of colonic health in aging C57Bl/6J mice",
abstract = "Diminished colonic health is associated with various age-related pathologies. Calorie restriction (CR) is an effective strategy to increase healthy lifespan, although underlying mechanisms are not fully elucidated. Here, we report the effects of lifelong CR on indicators of colonic health in aging C57Bl/6J mice. Compared to an ad libitum control and moderate-fat diet, 30{\%} energy reduction was associated with attenuated immune- and inflammation-related gene expression in the colon. Furthermore, expression of genes involved in lipid metabolism was higher upon CR, which may point towards efficient regulation of energy metabolism. The relative abundance of bacteria considered beneficial to colonic health, such as Bifidobacterium and Lactobacillus, increased in the mice exposed to CR for 28 months as compared to the other diet groups. We found lower plasma levels of interleukin-6 and lower levels of various metabolites, among which are bile acids, in the colonic luminal content of CR-exposed mice as compared to the other diet groups. Switching from CR to an ad libitum moderate-fat diet at old age (24 months) revealed remarkable phenotypic plasticity in terms of gene expression, microbiota composition and metabolite levels, although expression of a subset of genes remained CR-associated. This study demonstrated in a comprehensive way that CR affects indicators of colonic health in aging mice. Our findings provide unique leads for further studies that need to address optimal and feasible strategies for prolonged energy deprivation, which may contribute to healthy aging.",
keywords = "Aging, Calorie restriction, Colonic health, Gene expression, Gut microbiota, Metabolites",
author = "Kok, {Dieuwertje E.G.} and Fenni Rusli and {van der Lugt}, Benthe and Carolien Lute and Luca Laghi and Stefano Salvioli and Gianfranco Picone and Claudio Franceschi and Hauke Smidt and Jacques Vervoort and Ellen Kampman and Michael M{\"u}ller and Steegenga, {Wilma T.}",
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Lifelong calorie restriction affects indicators of colonic health in aging C57Bl/6J mice. / Kok, Dieuwertje E.G.; Rusli, Fenni; van der Lugt, Benthe; Lute, Carolien; Laghi, Luca; Salvioli, Stefano; Picone, Gianfranco; Franceschi, Claudio; Smidt, Hauke; Vervoort, Jacques; Kampman, Ellen; Müller, Michael; Steegenga, Wilma T.

In: Journal of Nutritional Biochemistry, Vol. 56, 01.06.2018, p. 152-164.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Lifelong calorie restriction affects indicators of colonic health in aging C57Bl/6J mice

AU - Kok, Dieuwertje E.G.

AU - Rusli, Fenni

AU - van der Lugt, Benthe

AU - Lute, Carolien

AU - Laghi, Luca

AU - Salvioli, Stefano

AU - Picone, Gianfranco

AU - Franceschi, Claudio

AU - Smidt, Hauke

AU - Vervoort, Jacques

AU - Kampman, Ellen

AU - Müller, Michael

AU - Steegenga, Wilma T.

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N2 - Diminished colonic health is associated with various age-related pathologies. Calorie restriction (CR) is an effective strategy to increase healthy lifespan, although underlying mechanisms are not fully elucidated. Here, we report the effects of lifelong CR on indicators of colonic health in aging C57Bl/6J mice. Compared to an ad libitum control and moderate-fat diet, 30% energy reduction was associated with attenuated immune- and inflammation-related gene expression in the colon. Furthermore, expression of genes involved in lipid metabolism was higher upon CR, which may point towards efficient regulation of energy metabolism. The relative abundance of bacteria considered beneficial to colonic health, such as Bifidobacterium and Lactobacillus, increased in the mice exposed to CR for 28 months as compared to the other diet groups. We found lower plasma levels of interleukin-6 and lower levels of various metabolites, among which are bile acids, in the colonic luminal content of CR-exposed mice as compared to the other diet groups. Switching from CR to an ad libitum moderate-fat diet at old age (24 months) revealed remarkable phenotypic plasticity in terms of gene expression, microbiota composition and metabolite levels, although expression of a subset of genes remained CR-associated. This study demonstrated in a comprehensive way that CR affects indicators of colonic health in aging mice. Our findings provide unique leads for further studies that need to address optimal and feasible strategies for prolonged energy deprivation, which may contribute to healthy aging.

AB - Diminished colonic health is associated with various age-related pathologies. Calorie restriction (CR) is an effective strategy to increase healthy lifespan, although underlying mechanisms are not fully elucidated. Here, we report the effects of lifelong CR on indicators of colonic health in aging C57Bl/6J mice. Compared to an ad libitum control and moderate-fat diet, 30% energy reduction was associated with attenuated immune- and inflammation-related gene expression in the colon. Furthermore, expression of genes involved in lipid metabolism was higher upon CR, which may point towards efficient regulation of energy metabolism. The relative abundance of bacteria considered beneficial to colonic health, such as Bifidobacterium and Lactobacillus, increased in the mice exposed to CR for 28 months as compared to the other diet groups. We found lower plasma levels of interleukin-6 and lower levels of various metabolites, among which are bile acids, in the colonic luminal content of CR-exposed mice as compared to the other diet groups. Switching from CR to an ad libitum moderate-fat diet at old age (24 months) revealed remarkable phenotypic plasticity in terms of gene expression, microbiota composition and metabolite levels, although expression of a subset of genes remained CR-associated. This study demonstrated in a comprehensive way that CR affects indicators of colonic health in aging mice. Our findings provide unique leads for further studies that need to address optimal and feasible strategies for prolonged energy deprivation, which may contribute to healthy aging.

KW - Aging

KW - Calorie restriction

KW - Colonic health

KW - Gene expression

KW - Gut microbiota

KW - Metabolites

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DO - 10.1016/j.jnutbio.2018.01.001

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SP - 152

EP - 164

JO - Journal of Nutritional Biochemistry

JF - Journal of Nutritional Biochemistry

SN - 0955-2863

ER -