Limits...
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.

De Andrade PB, Neff LA, Strosova MK, Arsenijevic D, Patthey-Vuadens O, Scapozza L, Montani JP, Ruegg UT, Dulloo AG, Dorchies OM - Front Physiol (2015)

Bottom Line: 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.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.These energy-sparing effects persist during weight recovery and contribute to catch-up fat.

View Article: PubMed Central - PubMed

Affiliation: Department of Medicine, Physiology, University of Fribourg Fribourg, Switzerland.

ABSTRACT
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. These energy-sparing effects persist during weight recovery and contribute to catch-up fat.

No MeSH data available.


Related in: MedlinePlus

The distribution of fiber types in gastrocnemius muscles of semistarved and refed rats and their respective controls was determined based on the expression of myosin heavy chain (MyHC) isoforms. Muscle sections were incubated with monoclonal antibodies to specific MyHC isoforms and fluorescent secondary antibodies. The extracellular matrix was stained with a fluorescent lectin in order to help demarcating the muscle fibers. (A) Example of MyHC 1 labeling in the gastrocnemius of a control rat, revealing the slow-twitch, type I fibers (green) and the counterstained extracellular matrix (red). A similar procedure was employed for staining type IIA and type IIB fibers using anti-MyHC 2A and anti-MyHC 2B, respectively. The positive fibers were expressed as the percentage of the total number of fibers. Approximately 1900 fibers were counted on every section. Bar: 100 μm. (B) Distribution of fiber types in the experimental groups. The fibers that were not of type I, IIA, or IIB were identified as type IIX. (C) Ratio of type I to type IIB fibers. SS, semistarved rats; CSS, control of semistarved rats; RF, refed rats; CRF, control of refed rats. n = 8–10; Mann-Whitney test; *P ≤ 0.05; **P ≤ 0.01; ns, not significant, comparing SS or RF to their respective control.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4584973&req=5

Figure 2: The distribution of fiber types in gastrocnemius muscles of semistarved and refed rats and their respective controls was determined based on the expression of myosin heavy chain (MyHC) isoforms. Muscle sections were incubated with monoclonal antibodies to specific MyHC isoforms and fluorescent secondary antibodies. The extracellular matrix was stained with a fluorescent lectin in order to help demarcating the muscle fibers. (A) Example of MyHC 1 labeling in the gastrocnemius of a control rat, revealing the slow-twitch, type I fibers (green) and the counterstained extracellular matrix (red). A similar procedure was employed for staining type IIA and type IIB fibers using anti-MyHC 2A and anti-MyHC 2B, respectively. The positive fibers were expressed as the percentage of the total number of fibers. Approximately 1900 fibers were counted on every section. Bar: 100 μm. (B) Distribution of fiber types in the experimental groups. The fibers that were not of type I, IIA, or IIB were identified as type IIX. (C) Ratio of type I to type IIB fibers. SS, semistarved rats; CSS, control of semistarved rats; RF, refed rats; CRF, control of refed rats. n = 8–10; Mann-Whitney test; *P ≤ 0.05; **P ≤ 0.01; ns, not significant, comparing SS or RF to their respective control.

Mentions: In order to elucidate the reasons for the slower kinetics of contraction and relaxation, we performed exhaustive fiber typing by labeling the MyHC with isoform-specific antibodies. Figure 2A illustrates the labeling of MyHC type 1. We found that the fibers positive for MyHC 1 were more abundant in the oxidative regions of gastrocnemius muscles after semistarvation, compared to the CSS control rats (+31.5%; P ≤ 0.01). MyHC 1 is characteristic for the type I, slow-twitch fibers (Figure 2B). An augmented proportion of type I fibers partly persisted in the gastrocnemius of RF rats (+13.4%), without reaching statistical significance. The accumulation of the type I fibers occurred not only at the expense of the type IIA fibers but also of type IIB fibers and to a lesser extent, of type IIX fibers, demonstrating an overall conversion of fast fibers into slower fibers. As a result, the ratio of type I to IIA fibers was moderately increased (+~51%) but the ratio of type I to IIB fibers was more than doubled (+127%) in the gastrocnemius from SS rats and remained ~78% higher in the RF rats, compared to their respective controls (Figure 2C). The fiber typing data supported our findings on the slower contraction and relaxation kinetics.


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.

De Andrade PB, Neff LA, Strosova MK, Arsenijevic D, Patthey-Vuadens O, Scapozza L, Montani JP, Ruegg UT, Dulloo AG, Dorchies OM - Front Physiol (2015)

The distribution of fiber types in gastrocnemius muscles of semistarved and refed rats and their respective controls was determined based on the expression of myosin heavy chain (MyHC) isoforms. Muscle sections were incubated with monoclonal antibodies to specific MyHC isoforms and fluorescent secondary antibodies. The extracellular matrix was stained with a fluorescent lectin in order to help demarcating the muscle fibers. (A) Example of MyHC 1 labeling in the gastrocnemius of a control rat, revealing the slow-twitch, type I fibers (green) and the counterstained extracellular matrix (red). A similar procedure was employed for staining type IIA and type IIB fibers using anti-MyHC 2A and anti-MyHC 2B, respectively. The positive fibers were expressed as the percentage of the total number of fibers. Approximately 1900 fibers were counted on every section. Bar: 100 μm. (B) Distribution of fiber types in the experimental groups. The fibers that were not of type I, IIA, or IIB were identified as type IIX. (C) Ratio of type I to type IIB fibers. SS, semistarved rats; CSS, control of semistarved rats; RF, refed rats; CRF, control of refed rats. n = 8–10; Mann-Whitney test; *P ≤ 0.05; **P ≤ 0.01; ns, not significant, comparing SS or RF to their respective control.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4584973&req=5

Figure 2: The distribution of fiber types in gastrocnemius muscles of semistarved and refed rats and their respective controls was determined based on the expression of myosin heavy chain (MyHC) isoforms. Muscle sections were incubated with monoclonal antibodies to specific MyHC isoforms and fluorescent secondary antibodies. The extracellular matrix was stained with a fluorescent lectin in order to help demarcating the muscle fibers. (A) Example of MyHC 1 labeling in the gastrocnemius of a control rat, revealing the slow-twitch, type I fibers (green) and the counterstained extracellular matrix (red). A similar procedure was employed for staining type IIA and type IIB fibers using anti-MyHC 2A and anti-MyHC 2B, respectively. The positive fibers were expressed as the percentage of the total number of fibers. Approximately 1900 fibers were counted on every section. Bar: 100 μm. (B) Distribution of fiber types in the experimental groups. The fibers that were not of type I, IIA, or IIB were identified as type IIX. (C) Ratio of type I to type IIB fibers. SS, semistarved rats; CSS, control of semistarved rats; RF, refed rats; CRF, control of refed rats. n = 8–10; Mann-Whitney test; *P ≤ 0.05; **P ≤ 0.01; ns, not significant, comparing SS or RF to their respective control.
Mentions: In order to elucidate the reasons for the slower kinetics of contraction and relaxation, we performed exhaustive fiber typing by labeling the MyHC with isoform-specific antibodies. Figure 2A illustrates the labeling of MyHC type 1. We found that the fibers positive for MyHC 1 were more abundant in the oxidative regions of gastrocnemius muscles after semistarvation, compared to the CSS control rats (+31.5%; P ≤ 0.01). MyHC 1 is characteristic for the type I, slow-twitch fibers (Figure 2B). An augmented proportion of type I fibers partly persisted in the gastrocnemius of RF rats (+13.4%), without reaching statistical significance. The accumulation of the type I fibers occurred not only at the expense of the type IIA fibers but also of type IIB fibers and to a lesser extent, of type IIX fibers, demonstrating an overall conversion of fast fibers into slower fibers. As a result, the ratio of type I to IIA fibers was moderately increased (+~51%) but the ratio of type I to IIB fibers was more than doubled (+127%) in the gastrocnemius from SS rats and remained ~78% higher in the RF rats, compared to their respective controls (Figure 2C). The fiber typing data supported our findings on the slower contraction and relaxation kinetics.

Bottom Line: 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.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.These energy-sparing effects persist during weight recovery and contribute to catch-up fat.

View Article: PubMed Central - PubMed

Affiliation: Department of Medicine, Physiology, University of Fribourg Fribourg, Switzerland.

ABSTRACT
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. These energy-sparing effects persist during weight recovery and contribute to catch-up fat.

No MeSH data available.


Related in: MedlinePlus