Nicotinamide Riboside Augments the Aged Human Skeletal Muscle NAD+ Metabolome and Induces Transcriptomic and Anti-inflammatory Signatures
Nicotinamide adenine dinucleotide (NAD+) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether...
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| Published in | Cell reports (Cambridge) Vol. 28; no. 7; pp. 1717 - 1728.e6 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
13.08.2019
Cell Press Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Nicotinamide adenine dinucleotide (NAD+) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD+ metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD+ metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR.
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•NR supplementation in aged subjects augments the skeletal muscle NAD+ metabolome•NR supplementation does not affect skeletal muscle mitochondrial bioenergetics•NR supplementation reduces levels of circulating inflammatory cytokines
Elhassan et al. show that oral nicotinamide riboside increases the NAD+ metabolome in aged human skeletal muscle, without apparently altering mitochondrial bioenergetics. Measures of muscle and whole-body metabolism are also unchanged. Nicotinamide riboside reduces the levels of circulating inflammatory cytokines. Studies in relevant human disease models are warranted. |
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| AbstractList | Nicotinamide adenine dinucleotide (NAD+) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD+ metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD+ metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR.
[Display omitted]
•NR supplementation in aged subjects augments the skeletal muscle NAD+ metabolome•NR supplementation does not affect skeletal muscle mitochondrial bioenergetics•NR supplementation reduces levels of circulating inflammatory cytokines
Elhassan et al. show that oral nicotinamide riboside increases the NAD+ metabolome in aged human skeletal muscle, without apparently altering mitochondrial bioenergetics. Measures of muscle and whole-body metabolism are also unchanged. Nicotinamide riboside reduces the levels of circulating inflammatory cytokines. Studies in relevant human disease models are warranted. Nicotinamide adenine dinucleotide (NAD ) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR. Nicotinamide adenine dinucleotide (NAD + ) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD + metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD + metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR. • NR supplementation in aged subjects augments the skeletal muscle NAD + metabolome • NR supplementation does not affect skeletal muscle mitochondrial bioenergetics • NR supplementation reduces levels of circulating inflammatory cytokines Elhassan et al. show that oral nicotinamide riboside increases the NAD + metabolome in aged human skeletal muscle, without apparently altering mitochondrial bioenergetics. Measures of muscle and whole-body metabolism are also unchanged. Nicotinamide riboside reduces the levels of circulating inflammatory cytokines. Studies in relevant human disease models are warranted. Nicotinamide adenine dinucleotide (NAD+) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD+ metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD+ metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR. : Elhassan et al. show that oral nicotinamide riboside increases the NAD+ metabolome in aged human skeletal muscle, without apparently altering mitochondrial bioenergetics. Measures of muscle and whole-body metabolism are also unchanged. Nicotinamide riboside reduces the levels of circulating inflammatory cytokines. Studies in relevant human disease models are warranted. Keywords: nicotinamide adenine dinucleotide, metabolism, aging, inflammation, cell adhesion Nicotinamide adenine dinucleotide (NAD+) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD+ metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD+ metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR.Nicotinamide adenine dinucleotide (NAD+) is modulated by conditions of metabolic stress and has been reported to decline with aging in preclinical models, but human data are sparse. Nicotinamide riboside (NR) supplementation ameliorates metabolic dysfunction in rodents. We aimed to establish whether oral NR supplementation in aged participants can increase the skeletal muscle NAD+ metabolome and if it can alter muscle mitochondrial bioenergetics. We supplemented 12 aged men with 1 g NR per day for 21 days in a placebo-controlled, randomized, double-blind, crossover trial. Targeted metabolomics showed that NR elevated the muscle NAD+ metabolome, evident by increased nicotinic acid adenine dinucleotide and nicotinamide clearance products. Muscle RNA sequencing revealed NR-mediated downregulation of energy metabolism and mitochondria pathways, without altering mitochondrial bioenergetics. NR also depressed levels of circulating inflammatory cytokines. Our data establish that oral NR is available to aged human muscle and identify anti-inflammatory effects of NR. |
| Author | Tennant, Daniel A. Cartwright, David M. Lavery, Gareth G. Oakey, Lucy Manolopoulos, Konstantinos N. Kluckova, Katarina Jenkinson, Ned Akerman, Ildem Wallis, Gareth A. Philp, Andrew Wilson, Martin Garten, Antje Lucas, Samuel J.E. Seabright, Alex Elhassan, Yasir S. Doig, Craig L. Burley, Claire V. Fletcher, Rachel S. Lai, Yu-Chiang Schmidt, Mark S. Nightingale, Peter Brenner, Charles |
| AuthorAffiliation | 6 Centre for Human Brain Health, University of Birmingham, Birmingham, UK 2 Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK 3 MRC-Arthritis Research UK Centre for Musculoskeletal Ageing Research, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK 4 Department of Biochemistry, Carver College of Medicine, University of Iowa, Iowa City, IA, USA 8 Institute of Translational Medicine, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK 9 Diabetes and Metabolism Division, Garvan Institute of Medical Research, Sydney, NSW, Australia 7 School of Psychology, University of Birmingham, Birmingham, UK 10 Faculty of Medicine, St. Vincent’s Clinical School, Sydney, UNSW, Australia 5 School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK 1 Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK |
| AuthorAffiliation_xml | – name: 4 Department of Biochemistry, Carver College of Medicine, University of Iowa, Iowa City, IA, USA – name: 2 Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham, UK – name: 7 School of Psychology, University of Birmingham, Birmingham, UK – name: 1 Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – name: 9 Diabetes and Metabolism Division, Garvan Institute of Medical Research, Sydney, NSW, Australia – name: 8 Institute of Translational Medicine, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK – name: 5 School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – name: 10 Faculty of Medicine, St. Vincent’s Clinical School, Sydney, UNSW, Australia – name: 3 MRC-Arthritis Research UK Centre for Musculoskeletal Ageing Research, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK – name: 6 Centre for Human Brain Health, University of Birmingham, Birmingham, UK |
| Author_xml | – sequence: 1 givenname: Yasir S. surname: Elhassan fullname: Elhassan, Yasir S. organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 2 givenname: Katarina surname: Kluckova fullname: Kluckova, Katarina organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 3 givenname: Rachel S. surname: Fletcher fullname: Fletcher, Rachel S. organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 4 givenname: Mark S. surname: Schmidt fullname: Schmidt, Mark S. organization: Department of Biochemistry, Carver College of Medicine, University of Iowa, Iowa City, IA, USA – sequence: 5 givenname: Antje surname: Garten fullname: Garten, Antje organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 6 givenname: Craig L. surname: Doig fullname: Doig, Craig L. organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 7 givenname: David M. surname: Cartwright fullname: Cartwright, David M. organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 8 givenname: Lucy surname: Oakey fullname: Oakey, Lucy organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 9 givenname: Claire V. surname: Burley fullname: Burley, Claire V. organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 10 givenname: Ned surname: Jenkinson fullname: Jenkinson, Ned organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 11 givenname: Martin surname: Wilson fullname: Wilson, Martin organization: Centre for Human Brain Health, University of Birmingham, Birmingham, UK – sequence: 12 givenname: Samuel J.E. surname: Lucas fullname: Lucas, Samuel J.E. organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 13 givenname: Ildem surname: Akerman fullname: Akerman, Ildem organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 14 givenname: Alex surname: Seabright fullname: Seabright, Alex organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 15 givenname: Yu-Chiang surname: Lai fullname: Lai, Yu-Chiang organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 16 givenname: Daniel A. surname: Tennant fullname: Tennant, Daniel A. organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 17 givenname: Peter surname: Nightingale fullname: Nightingale, Peter organization: Institute of Translational Medicine, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK – sequence: 18 givenname: Gareth A. surname: Wallis fullname: Wallis, Gareth A. organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 19 givenname: Konstantinos N. surname: Manolopoulos fullname: Manolopoulos, Konstantinos N. organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK – sequence: 20 givenname: Charles surname: Brenner fullname: Brenner, Charles organization: Department of Biochemistry, Carver College of Medicine, University of Iowa, Iowa City, IA, USA – sequence: 21 givenname: Andrew surname: Philp fullname: Philp, Andrew organization: School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK – sequence: 22 givenname: Gareth G. surname: Lavery fullname: Lavery, Gareth G. email: g.g.lavery@bham.ac.uk organization: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31412242$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Aged Aged, 80 and over aging Aging - drug effects Aging - metabolism Anti-Inflammatory Agents - blood cell adhesion Cross-Sectional Studies Cytokines - blood Cytokines - drug effects Double-Blind Method Humans inflammation Male metabolism Metabolome - drug effects Muscle, Skeletal - drug effects Muscle, Skeletal - metabolism NAD - metabolism Niacinamide - analogs & derivatives Niacinamide - pharmacology nicotinamide adenine dinucleotide Pyridinium Compounds Transcriptome - drug effects |
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| Title | Nicotinamide Riboside Augments the Aged Human Skeletal Muscle NAD+ Metabolome and Induces Transcriptomic and Anti-inflammatory Signatures |
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