Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding
Weight regain after caloric restriction results in accelerated fat storage in adipose tissue. This catch-up fat phenomenon is postulated to result partly from suppressed skeletal muscle thermogenesis, but the underlying mechanisms are elusive. We investigated whether the reduced rate of skeletal mus...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2015-09-01
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| Series: | Frontiers in Physiology |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fphys.2015.00254/full |
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| author | Paula Bresciani M. De Andrade Laurence A Neff Miriam K Strosova Denis eArsenijevic Ophélie ePatthey-Vuadens Ophélie ePatthey-Vuadens Leonardo eScapozza Jean-Pierre eMontani Urs T Ruegg Abdul G Dulloo Olivier M Dorchies Olivier M Dorchies |
| author_facet | Paula Bresciani M. De Andrade Laurence A Neff Miriam K Strosova Denis eArsenijevic Ophélie ePatthey-Vuadens Ophélie ePatthey-Vuadens Leonardo eScapozza Jean-Pierre eMontani Urs T Ruegg Abdul G Dulloo Olivier M Dorchies Olivier M Dorchies |
| author_sort | Paula Bresciani M. De Andrade |
| collection | DOAJ |
| description | Weight regain after caloric restriction results in accelerated fat storage in adipose tissue. This catch-up fat phenomenon is postulated to result partly from suppressed skeletal muscle thermogenesis, but the underlying mechanisms are elusive. We investigated whether the reduced rate of skeletal muscle contraction-relaxation cycle that occurs after caloric restriction persists during weight recovery and could contribute to catch-up fat. Using a rat model of semistarvation-refeeding, in which fat recovery is driven by suppressed thermogenesis, we show that contraction and relaxation of leg muscles are slower after both semistarvation and refeeding. These effects are associated with (i) higher expression of muscle deiodinase type 3 (DIO3) which inactivates tri-iodothyronine (T3), and lower expression of T3-activating enzyme, deiodinase type 2 (DIO2), (ii) slower net formation of T3 from its T4 precursor in muscles, and (iii) accumulation of slow fibers at the expense of fast fibers. These semistarvation-induced changes persisted during recovery and correlated with impaired expression of transcription factors involved in slow-twitch muscle development.We conclude that diminished muscle thermogenesis following caloric restriction results from reduced muscle T3 levels, alteration in muscle-specific transcription factors, and fast-to-slow fiber shift causing slower contractility. Energy-sparing effects persist during weight recovery and likely contribute to catch-up fat. |
| first_indexed | 2024-12-13T04:59:51Z |
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| id | doaj.art-09f1a1c50b91414b95b2f80de284c89f |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-13T04:59:51Z |
| publishDate | 2015-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-09f1a1c50b91414b95b2f80de284c89f2022-12-21T23:58:49ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2015-09-01610.3389/fphys.2015.00254140969Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeedingPaula Bresciani M. De Andrade0Laurence A Neff1Miriam K Strosova2Denis eArsenijevic3Ophélie ePatthey-Vuadens4Ophélie ePatthey-Vuadens5Leonardo eScapozza6Jean-Pierre eMontani7Urs T Ruegg8Abdul G Dulloo9Olivier M Dorchies10Olivier M Dorchies11University of FribourgUniversity of Geneva, University of LausanneUniversity of Geneva, University of LausanneUniversity of FribourgUniversity of Geneva, University of LausanneUniversity of Geneva, University of LausanneUniversity of Geneva, University of LausanneUniversity of FribourgUniversity of Geneva, University of LausanneUniversity of FribourgUniversity of Geneva, University of LausanneUniversity of Geneva, University of LausanneWeight regain after caloric restriction results in accelerated fat storage in adipose tissue. This catch-up fat phenomenon is postulated to result partly from suppressed skeletal muscle thermogenesis, but the underlying mechanisms are elusive. We investigated whether the reduced rate of skeletal muscle contraction-relaxation cycle that occurs after caloric restriction persists during weight recovery and could contribute to catch-up fat. Using a rat model of semistarvation-refeeding, in which fat recovery is driven by suppressed thermogenesis, we show that contraction and relaxation of leg muscles are slower after both semistarvation and refeeding. These effects are associated with (i) higher expression of muscle deiodinase type 3 (DIO3) which inactivates tri-iodothyronine (T3), and lower expression of T3-activating enzyme, deiodinase type 2 (DIO2), (ii) slower net formation of T3 from its T4 precursor in muscles, and (iii) accumulation of slow fibers at the expense of fast fibers. These semistarvation-induced changes persisted during recovery and correlated with impaired expression of transcription factors involved in slow-twitch muscle development.We conclude that diminished muscle thermogenesis following caloric restriction results from reduced muscle T3 levels, alteration in muscle-specific transcription factors, and fast-to-slow fiber shift causing slower contractility. Energy-sparing effects persist during weight recovery and likely contribute to catch-up fat.http://journal.frontiersin.org/Journal/10.3389/fphys.2015.00254/fullObesityThermogenesisratskeletal muscledeiodinaseweight regain |
| spellingShingle | Paula Bresciani M. De Andrade Laurence A Neff Miriam K Strosova Denis eArsenijevic Ophélie ePatthey-Vuadens Ophélie ePatthey-Vuadens Leonardo eScapozza Jean-Pierre eMontani Urs T Ruegg Abdul G Dulloo Olivier M Dorchies Olivier M Dorchies Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding Frontiers in Physiology Obesity Thermogenesis rat skeletal muscle deiodinase weight regain |
| title | Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding |
| title_full | Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding |
| title_fullStr | Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding |
| title_full_unstemmed | Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding |
| title_short | Caloric restriction induces energy-sparing alterations in skeletal muscle contraction, fiber composition and local thyroid hormone metabolism that persist during catch-up fat upon refeeding |
| title_sort | caloric restriction induces energy sparing alterations in skeletal muscle contraction fiber composition and local thyroid hormone metabolism that persist during catch up fat upon refeeding |
| topic | Obesity Thermogenesis rat skeletal muscle deiodinase weight regain |
| url | http://journal.frontiersin.org/Journal/10.3389/fphys.2015.00254/full |
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