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Evolutionary isolation of ryanodine receptor isoform 1 for muscle-based thermogenesis in mammals. | LitMetric

AI Article Synopsis

  • Resting skeletal muscle in mammals produces heat for body warmth, which is not the case for amphibians, highlighting differences in thermogenesis despite similarities in muscle contraction systems.
  • This heat generation in mammals is driven by a specific calcium release mechanism involving ryanodine receptors and the sarcoplasmic reticulum that allows for controlled calcium levels without disrupting muscle relaxation.
  • Research shows that in mammals, the sympathetic nervous system regulates this process, enhancing heat production via a mechanism that includes phosphorylation of ryanodine receptors, suggesting evolutionary adaptations for maintaining warm body temperatures.

Article Abstract

Resting skeletal muscle generates heat for endothermy in mammals but not amphibians, while both use the same Ca-handling proteins and membrane structures to conduct excitation-contraction coupling apart from having different ryanodine receptor (RyR) isoforms for Ca release. The sarcoplasmic reticulum (SR) generates heat following Adenosine triphosphate (ATP) hydrolysis at the Ca pump, which is amplified by increasing RyR1 Ca leak in mammals, subsequently increasing cytoplasmic [Ca] ([Ca]). For thermogenesis to be functional, rising [Ca] must not interfere with cytoplasmic effectors of the sympathetic nervous system (SNS) that likely increase RyR1 Ca leak; nor should it compromise the muscle remaining relaxed. To achieve this, Ca activated, regenerative Ca release that is robust in lower vertebrates needs to be suppressed in mammals. However, it has not been clear whether: i) the RyR1 can be opened by local increases in [Ca]; and ii) downstream effectors of the SNS increase RyR Ca leak and subsequently, heat generation. By positioning amphibian and malignant hyperthermia-susceptible human-skinned muscle fibers perpendicularly, we induced abrupt rises in [Ca] under identical conditions optimized for activating regenerative Ca release as Ca waves passed through the junction of fibers. Only mammalian fibers showed resistance to rising [Ca], resulting in increased SR Ca load and leak. Fiber heat output was increased by cyclic adenosine monophosphate (cAMP)-induced RyR1 phosphorylation at Ser2844 and Ca leak, indicating likely SNS regulation of thermogenesis. Thermogenesis occurred despite the absence of SR Ca pump regulator sarcolipin. Thus, evolutionary isolation of RyR1 provided increased dynamic range for thermogenesis with sensitivity to cAMP, supporting endothermy.

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Source
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9942912PMC
http://dx.doi.org/10.1073/pnas.2117503120DOI Listing

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