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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

Electrically-evoked isometric contractions of the triceps surae were recorded in situ in semistarved and refed rats and in their respective controls. Force characteristics and kinetics of contraction and relaxation were determined. (A) The average phasic traces of refed rats and their controls are depicted, illustrating muscle contraction followed by complete relaxation. The kinetics values (time to peak and time for half-relaxation from the peak) are highlighted in green (control) and in red (refed). (B) Absolute phasic and tetanic tensions, (C) specific phasic and tetanic tensions, (D) kinetics of contraction and relaxation, (E) force-frequency relationships, and (F) muscle fatigue were determined as described in the text. 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; ***P ≤ 0.001; ns, not significant, comparing SS or RF to their respective control.
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Figure 1: Electrically-evoked isometric contractions of the triceps surae were recorded in situ in semistarved and refed rats and in their respective controls. Force characteristics and kinetics of contraction and relaxation were determined. (A) The average phasic traces of refed rats and their controls are depicted, illustrating muscle contraction followed by complete relaxation. The kinetics values (time to peak and time for half-relaxation from the peak) are highlighted in green (control) and in red (refed). (B) Absolute phasic and tetanic tensions, (C) specific phasic and tetanic tensions, (D) kinetics of contraction and relaxation, (E) force-frequency relationships, and (F) muscle fatigue were determined as described in the text. 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; ***P ≤ 0.001; ns, not significant, comparing SS or RF to their respective control.

Mentions: Phasic twitches were recorded after electrical stimulation of the triceps surae from rats after semistarvation for 2 weeks and after refeeding for 1 week. As illustrated in Figure 1A for the CRF and RF groups, the electrical stimulation of the triceps triggered its contraction (rising phase), followed by its complete relaxation (descending phase), allowing to determine phasic tensions (Figures 1B,C), and kinetics of contraction and relaxation (Figure 1D). Then, the stimulation frequency was gradually increased from 10 to 100 Hz and the strongest contraction was used for determining the tetanic tension (Figures 1B,C).


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)

Electrically-evoked isometric contractions of the triceps surae were recorded in situ in semistarved and refed rats and in their respective controls. Force characteristics and kinetics of contraction and relaxation were determined. (A) The average phasic traces of refed rats and their controls are depicted, illustrating muscle contraction followed by complete relaxation. The kinetics values (time to peak and time for half-relaxation from the peak) are highlighted in green (control) and in red (refed). (B) Absolute phasic and tetanic tensions, (C) specific phasic and tetanic tensions, (D) kinetics of contraction and relaxation, (E) force-frequency relationships, and (F) muscle fatigue were determined as described in the text. 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; ***P ≤ 0.001; 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 1: Electrically-evoked isometric contractions of the triceps surae were recorded in situ in semistarved and refed rats and in their respective controls. Force characteristics and kinetics of contraction and relaxation were determined. (A) The average phasic traces of refed rats and their controls are depicted, illustrating muscle contraction followed by complete relaxation. The kinetics values (time to peak and time for half-relaxation from the peak) are highlighted in green (control) and in red (refed). (B) Absolute phasic and tetanic tensions, (C) specific phasic and tetanic tensions, (D) kinetics of contraction and relaxation, (E) force-frequency relationships, and (F) muscle fatigue were determined as described in the text. 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; ***P ≤ 0.001; ns, not significant, comparing SS or RF to their respective control.
Mentions: Phasic twitches were recorded after electrical stimulation of the triceps surae from rats after semistarvation for 2 weeks and after refeeding for 1 week. As illustrated in Figure 1A for the CRF and RF groups, the electrical stimulation of the triceps triggered its contraction (rising phase), followed by its complete relaxation (descending phase), allowing to determine phasic tensions (Figures 1B,C), and kinetics of contraction and relaxation (Figure 1D). Then, the stimulation frequency was gradually increased from 10 to 100 Hz and the strongest contraction was used for determining the tetanic tension (Figures 1B,C).

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