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Differential effects of a six-day immobilization on newborn rat soleus muscles at two developmental stages
F Picquet1, L Stevens, G S Butler-Browne
1Laboratoire de Plasticité Neuromusculaire, Université des Sciences et Technologies de Lille, Villeneuve D'Ascq, France.
Insights
Six-day limb immobilization during rat postnatal development alters soleus muscle maturation. Immobilization during polyneuronal innervation delays maturation, while during monosynaptic innervation, it promotes a fast muscle fiber phenotype.
Area of Science:
- Developmental biology
- Muscle physiology
- Neuroscience
Background:
- Postnatal muscle development involves significant changes in innervation and fiber type composition.
- Disuse, such as immobilization, is known to induce substantial alterations in muscle structure and function.
- The soleus muscle, a postural slow muscle, is particularly sensitive to changes in activity levels.
Purpose of the Study:
- To investigate the impact of short-term immobilization on soleus muscle development during distinct postnatal innervation stages.
- To determine how immobilization affects myosin heavy chain (MyHC) isoform expression and functional properties at different developmental time points.
Main Methods:
- Soleus muscle immobilization in a shortened position in rats at two critical postnatal periods (6–12 days and 17–23 days).
- Histochemical analysis using ATPase staining.
- Myosin heavy chain (MyHC) isoform identification via SDS-PAGE and monoclonal antibodies.
- Assessment of functional properties using calcium/strontium activation curves of skinned fiber bundles.
Main Results:
- Immobilization from 6–12 days (polyneuronal innervation) increased type IIC fibers, MyHC neo expression, and calcium affinity, delaying maturation.
- Immobilization from 17–23 days (monosynaptic innervation) increased calcium affinity, decreased MyHC neo, and induced expression of the fast MyHC IIB isoform.
- Control muscles showed a natural maturation with increased adult MyHCs (I and IIA) and decreased MyHC neo and calcium affinity.
Conclusions:
- Immobilization during early postnatal development (polyneuronal innervation) hinders normal soleus muscle maturation.
- Immobilization during later postnatal development (monosynaptic innervation) drives the soleus muscle towards a fast phenotype through altered MyHC expression.
- These findings highlight the critical role of innervation state in mediating muscle response to disuse during development.
Abstract:
Our objective was to determine the effects of a six-day immobilization on the musculoskeletal system of the rat during postnatal development at two key periods when the states of innervation are known to be different. This work was undertaken on the soleus muscle since it is well known that postural slow muscles show marked changes after a period of disuse. Thus, the soleus muscle was immobilized in a shortened position either when the innervation was polyneuronal or monosynaptic, respectively from 6 to 12 and from 17 to 23 days. The muscle modifications were followed by ATPase staining and myosin heavy chain (MyHC) isoform identification using monoclonal antibodies and SDS-PAGE. The functional properties of skinned fibre bundles were established by calcium/strontium (Ca/Sr) activation characteristics. In control muscles the maturation was characterized by a progressive increase of adult MyHCs (I and IIA) concomitant with a decrease in both the MyHC neo and the Ca affinity. Between 6 to 12 days, immobilization of the limb induced an increase in histochemical type IIC fibres. Using antibodies we identified new fibre types, classified as a function of their MyHC isoform co-expression. We observed an increase in expression of both MyHC neo and Ca affinity. From 17 to 23 days, the immobilization induced an increase in Ca affinity and marked changes in the MyHC isoform composition: disappearance of MyHC neo and expression of the fast MyHC IIB isoform, which in normal conditions is never expressed in the soleus muscle. We conclude that an immobilization imposed during polyneuronal innervation delays the postnatal maturation of the soleus muscle, whereas when the immobilization is performed under monosynaptic innervation the muscle evolves towards a fast phenotype using a default pathway for MyHC expression.