Adipose tissue NAD⁺ biosynthesis is required for regulating adaptive thermogenesis and whole-body energy homeostasis in mice
Nicotinamide adenine dinucleotide (NAD⁺) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD⁺ metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we g...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 116; no. 47; pp. 23822 - 23828 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
19.11.2019
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Nicotinamide adenine dinucleotide (NAD⁺) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD⁺ metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase (Nampt) knockout (ANKO) and brown adipocyte-specific Nampt knockout (BANKO) mice because NAMPT is the rate-limiting NAD⁺ biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT andWAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD⁺–SIRT1–caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD⁺ synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found NAMPT expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD⁺ biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. |
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| AbstractList | Nicotinamide adenine dinucleotide (NAD
+
) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD
+
metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase (
Nampt
) knockout (ANKO) and brown adipocyte-specific
Nampt
knockout (BANKO) mice because NAMPT is the rate-limiting NAD
+
biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT and WAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD
+
–SIRT1–caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD
+
synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found
NAMPT
expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD
+
biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. Nicotinamide adenine dinucleotide (NAD+) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD+ metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase (Nampt) knockout (ANKO) and brown adipocyte-specific Nampt knockout (BANKO) mice because NAMPT is the rate-limiting NAD+ biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT and WAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD+–SIRT1–caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD+ synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found NAMPT expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD+ biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. Nicotinamide adenine dinucleotide (NAD⁺) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD⁺ metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase (Nampt) knockout (ANKO) and brown adipocyte-specific Nampt knockout (BANKO) mice because NAMPT is the rate-limiting NAD⁺ biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT andWAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD⁺–SIRT1–caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD⁺ synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found NAMPT expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD⁺ biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. Nicotinamide adenine dinucleotide (NAD+) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD+ metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase (Nampt) knockout (ANKO) and brown adipocyte-specific Nampt knockout (BANKO) mice because NAMPT is the rate-limiting NAD+ biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT and WAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD+-SIRT1-caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD+ synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found NAMPT expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD+ biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism.Nicotinamide adenine dinucleotide (NAD+) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD+ metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase (Nampt) knockout (ANKO) and brown adipocyte-specific Nampt knockout (BANKO) mice because NAMPT is the rate-limiting NAD+ biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT and WAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD+-SIRT1-caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD+ synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found NAMPT expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD+ biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. Nicotinamide adenine dinucleotide (NAD ) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase ( ) knockout (ANKO) and brown adipocyte-specific knockout (BANKO) mice because NAMPT is the rate-limiting NAD biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT and WAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD -SIRT1-caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. Thermogenesis is a fundamental aspect of energy homeostasis. Here, we present evidence that adipose tissue NAD + metabolism is essential for thermogenesis. We found cold exposure activates NAD + biosynthesis mediated by a rate-limiting enzyme, NAMPT, in mouse and human brown adipose tissue (BAT). Loss of NAMPT impairs the gene programs involved in thermogenesis and mitochondrial function in BAT. Mice lacking NAMPT in both BAT and white adipose tissue (WAT) but not in BAT alone have impaired thermogenic responses to cold exposure, fasting, and β-adrenergic stimulation. In WAT, NAMPT deletion decreases adrenergic-mediated lipolysis through inactivation of caveolin-1, which likely impairs whole-body thermogenesis. Nicotinamide mononucleotide administration normalized these metabolic derangements. These findings demonstrate the importance of adipose tissue NAD + biology in energy metabolism. Nicotinamide adenine dinucleotide (NAD + ) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of brown and white adipose tissue (BAT and WAT) NAD + metabolism in regulating whole-body thermogenesis and energy metabolism. Accordingly, we generated and analyzed adipocyte-specific nicotinamide phosphoribosyltransferase ( Nampt ) knockout (ANKO) and brown adipocyte-specific Nampt knockout (BANKO) mice because NAMPT is the rate-limiting NAD + biosynthetic enzyme. We found ANKO mice, which lack NAMPT in both BAT and WAT, had impaired gene programs involved in thermogenesis and mitochondrial function in BAT and a blunted thermogenic (rectal temperature, BAT temperature, and whole-body oxygen consumption) response to acute cold exposure, prolonged fasting, and administration of β-adrenergic agonists (norepinephrine and CL-316243). In addition, the absence of NAMPT in WAT markedly reduced adrenergic-mediated lipolytic activity, likely through inactivation of the NAD + –SIRT1–caveolin-1 axis, which limits an important fuel source fatty acid for BAT thermogenesis. These metabolic abnormalities were rescued by treatment with nicotinamide mononucleotide (NMN), which bypasses the block in NAD + synthesis induced by NAMPT deficiency. Although BANKO mice, which lack NAMPT in BAT only, had BAT cellular alterations similar to the ANKO mice, BANKO mice had normal thermogenic and lipolytic responses. We also found NAMPT expression in supraclavicular adipose tissue (where human BAT is localized) obtained from human subjects increased during cold exposure, suggesting our finding in rodents could apply to people. These results demonstrate that adipose NAMPT-mediated NAD + biosynthesis is essential for regulating adaptive thermogenesis, lipolysis, and whole-body energy metabolism. |
| Author | Gunawardana, Subhadra C. Rensing, Nicholas Klein, Samuel Wozniak, David F. Franczyk, Michael P. Qi, Nathan Sasaki, Yo Yoshino, Jun Porter, Lane C. Wong, Michael Stromsdorfer, Kelly L. Piston, David W. Chondronikola, Maria Yamaguchi, Shintaro |
| Author_xml | – sequence: 1 givenname: Shintaro surname: Yamaguchi fullname: Yamaguchi, Shintaro – sequence: 2 givenname: Michael P. surname: Franczyk fullname: Franczyk, Michael P. – sequence: 3 givenname: Maria surname: Chondronikola fullname: Chondronikola, Maria – sequence: 4 givenname: Nathan surname: Qi fullname: Qi, Nathan – sequence: 5 givenname: Subhadra C. surname: Gunawardana fullname: Gunawardana, Subhadra C. – sequence: 6 givenname: Kelly L. surname: Stromsdorfer fullname: Stromsdorfer, Kelly L. – sequence: 7 givenname: Lane C. surname: Porter fullname: Porter, Lane C. – sequence: 8 givenname: David F. surname: Wozniak fullname: Wozniak, David F. – sequence: 9 givenname: Yo surname: Sasaki fullname: Sasaki, Yo – sequence: 10 givenname: Nicholas surname: Rensing fullname: Rensing, Nicholas – sequence: 11 givenname: Michael surname: Wong fullname: Wong, Michael – sequence: 12 givenname: David W. surname: Piston fullname: Piston, David W. – sequence: 13 givenname: Samuel surname: Klein fullname: Klein, Samuel – sequence: 14 givenname: Jun surname: Yoshino fullname: Yoshino, Jun |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31694884$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright National Academy of Sciences Nov 19, 2019 2019 |
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| Issue | 47 |
| Keywords | NAD adipose tissue thermogenesis lipolysis energy metabolism |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Edited by William Lee Kraus, The University of Texas Southwestern Medical Center at Dallas, Dallas, TX, and accepted by Editorial Board Member David J. Mangelsdorf October 16, 2019 (received for review June 10, 2019) Author contributions: N.Q., D.F.W., N.R., M.W., D.W.P., S.K., and J.Y. designed research; S.Y., M.P.F., M.C., N.Q., S.C.G., K.L.S., L.C.P., D.F.W., Y.S., N.R., M.W., D.W.P., S.K., and J.Y. performed research; J.Y. contributed new reagents/analytic tools; S.Y., M.P.F., M.C., N.Q., Y.S., N.R., M.W., D.W.P., and J.Y. analyzed data; and S.Y., M.P.F., M.C., N.Q., S.C.G., K.L.S., L.C.P., D.F.W., Y.S., N.R., M.W., D.W.P., S.K., and J.Y. wrote the paper. 1S.Y. and M.P.F. contributed equally to this work. |
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| Snippet | Nicotinamide adenine dinucleotide (NAD⁺) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of... Nicotinamide adenine dinucleotide (NAD + ) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance... Nicotinamide adenine dinucleotide (NAD ) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of... Nicotinamide adenine dinucleotide (NAD+) is a critical coenzyme for cellular energy metabolism. The aim of the present study was to determine the importance of... Thermogenesis is a fundamental aspect of energy homeostasis. Here, we present evidence that adipose tissue NAD + metabolism is essential for thermogenesis. We... |
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| SubjectTerms | Abnormalities Adaptation, Physiological Adenine Adipocytes Adipose tissue Adipose Tissue, Brown - enzymology Adipose Tissue, Brown - metabolism Animals Biological Sciences Biosynthesis Body temperature Caveolin Caveolin 1 - antagonists & inhibitors Caveolin-1 Clavicle Cold Temperature Cytokines - genetics Deactivation Energy balance Energy Metabolism Fasting Fatty acids Homeostasis Humans Inactivation Lipolysis Metabolism Mice Mice, Knockout Mitochondria NAD NAD - biosynthesis Nicotinamide Nicotinamide adenine dinucleotide Nicotinamide Mononucleotide - administration & dosage Nicotinamide phosphoribosyltransferase Nicotinamide Phosphoribosyltransferase - genetics Norepinephrine Oxygen consumption Phosphoribosyltransferase Rodents SIRT1 protein Sympathomimetics Thermogenesis |
| Title | Adipose tissue NAD⁺ biosynthesis is required for regulating adaptive thermogenesis and whole-body energy homeostasis in mice |
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