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Changes in responsiveness to extracellular ATP in chick skeletal muscle during development and upon denervation
D G Wells1, M J Zawisa, R I Hume
1Department of Biology, University of Michigan, Ann Arbor 48109-1048, USA.
Insights
Developing chick skeletal muscles initially contract in response to adenosine 5'-triphosphate (ATP) but lose this sensitivity as they mature. Denervation, however, can restore ATP responsiveness, suggesting motor neuron regulation.
Area of Science:
- Developmental Biology
- Neuroscience
- Muscle Physiology
Background:
- Developing skeletal muscles exhibit sensitivity to extracellular adenosine 5'-triphosphate (ATP).
- ATP is known to depolarize skeletal muscle cells.
- Understanding the regulation of muscle responsiveness is crucial for developmental studies.
Purpose of the Study:
- To investigate the developmental changes in chick skeletal muscle responsiveness to ATP.
- To determine the role of innervation in regulating ATP sensitivity in developing muscles.
Main Methods:
- Testing ATP-induced contractions in five different chick skeletal muscles at various embryonic stages.
- Utilizing intracellular recordings to assess muscle fiber responsiveness.
- Performing surgical denervation on specific muscles in newly hatched chicks to observe ATP sensitivity changes.
Main Results:
- All tested muscles showed vigorous contractions upon ATP application at early embryonic stages (Day 6).
- ATP responsiveness significantly declined by Embryonic Day 17 in all five muscles.
- Denervation of muscles in newly hatched chicks led to the reappearance of ATP-induced contractions.
Conclusions:
- The loss of ATP responsiveness in developing chick skeletal muscles correlates with innervation.
- Reappearance of ATP sensitivity after denervation strongly suggests that motor neurons regulate the expression of ATP responsiveness.
- This study highlights a novel mechanism of neuromuscular regulation during muscle development.
Abstract:
Skeletal muscles in developing chick embryos were tested for responsiveness to adenosine 5'-triphosphate (ATP), a substance known to depolarize chick skeletal muscle in culture. The sensitivity to extracellular ATP was tested at various stages of development in five different muscles; pectoralis superficia, anterior latissimus dorsi, posterior latissimus dorsi, sartorious, and gastrocnemius. At the earliest time that muscles were tested (Embryonic Day 6, stage 30 of Hamburger and Hamilton, 1951) application of ATP(50-100 microM) elicited vigorous contractions in all five muscles, but within a few days (Embryonic Day 17, stage 43) none of the muscles contracted in response to ATP. Sensitivity declined at approximately the same time in all five of these muscles. Intracellular recordings made from muscle fibers near the time of hatching (Embryonic Days 18-21 or Postnatal Days 1-2) indicated that the loss of the ability to contract in response to ATP was due to the total loss of responsiveness to ATP. Surgical denervation of the anterior latissimus dorsi and posterior latissimus dorsi was performed in a series of chicks 1-2 days after hatching, and the ability of these muscles to contract in response to ATP was tested 3-10 days after the surgery. Contractions in response to ATP were present in many of the muscles. Thus denervation of muscles in newly hatched chicks led to the reappearance of sensitivity to ATP. The disappearance of ATP responsiveness shortly after muscles become innervated and the reappearance of ATP responsiveness following denervation suggest that the expression of ATP responsiveness is regulated by motor neurons.