Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans)

Abstract

SUMMARY A thermogenic organ is found beneath the brain of billfishes(Istiophoridae), swordfish (Xiphiidae) and the butterfly mackerel(Scombridae). The heater organ has been shown to warm the brain and eyes up to 14°C above ambient water temperature. Heater cells are derived from extraocular muscle fibers and express a modified muscle phenotype with an extensive transverse-tubule (T-tubule) network and sarcoplasmic reticulum (SR)enriched in Ca2+-ATPase (SERCA) pumps and ryanodine receptors(RyRs). Heater cells have a high mitochondria content but have lost most of the contractile myofilaments. Thermogenesis has been hypothesized to be associated with release and reuptake of Ca2+. In this study,Ca2+ fluxes in heater SR vesicles derived from blue marlin(Makaira nigricans) were measured using fura-2 fluorescence. Upon the addition of MgATP, heater SR vesicles rapidly sequestered Ca2+. Uptake of Ca2+ was thapsigargin sensitive, and maximum loading ranged between 0.8 μmol Ca2+ mg-1 protein and 1.0μmol Ca2+ mg-1 protein. Upon the addition of 10 mmol l-1 caffeine or 350 μmol l-1 ryanodine, heater SR vesicles released only a small fraction of the loaded Ca2+. However, ryanodine could elicit a much larger Ca2+ release event when the activity of the SERCA pumps was reduced. RNase protection assays revealed that heater tissue expresses an RyR isoform that is also expressed in fish slow-twitch skeletal muscle but is distinct from the RyR expressed in fish fast-twitch skeletal muscle. The heater and slow-twitch muscle RyR isoform has unique physiological properties. In the presence of adenine nucleotides, this RyR remains open even though cytoplasmic Ca2+ is elevated, a condition that normally closes RyRs. The fast Ca2+sequestration by the heater SR, coupled with a physiologically unique RyR, is hypothesized to promote Ca2+ cycling, ATP turnover and heat generation. A branch of the oculomotor nerve innervates heater organs, and, in this paper, we demonstrate that heater cells contain large `endplate-like'clusters of acetylcholine receptors that appear to provide a mechanism for nervous control of thermogenesis.

Cold adaptation overrides developmental regulation of sarcolipin expression in mice skeletal muscle: SOS for muscle-based thermogenesis?

“…Therefore, having more than one mechanism of heat production would help in minimizing the energy cost (primarily met by food/lactation) for maintaining constant body temperature and allow energy investment in other productive activities. SERCA-based ATP hydrolysis as a means of heat production has been recruited in many species during evolution including the 'heater organ' of endothermic fishes (Morrissette et al, 2003). Moreover, the ability to recruit SLN/SERCA-mediated muscle-based NST without significantly affecting muscle maturation and function will be favorably selected for, specifically in non-tropical climates where temperature and food availability dramatically fluctuate seasonally.…”

Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis

“…The transport of two Ca 2ϩ ions per cycle into the SR involves strong movements of the transmembrane domains, which may be affected by the fatty acid composition of the bilayer (52). tial amounts of chemical energy released as heat (53), and this avenue of thermogenesis is also used by the "heater organ" of billfishes, which can create large thermal gradients between this organ (and the adjacent eye and brain) and ambient water temperature (54). Clearly, this mechanism would counteract temperature-dependent (Arrhenius) effects on SERCA activity in torpid mammals.…”

Zebrafishrelatively relaxedmutants have a ryanodine receptor defect, show slow swimming and provide a model of multi-minicore disease

“…We found that zebrafish have two genes encoding RyR1; ryr1a expressed by slow muscles and ryr1b by fast muscles. A similar division of labor between duplicated RyR1s in slow and fast muscles appears in other fish, such as blue marlin (Makaira nigricans) and yellowfin tuna (Thunnus albacares) (Franck et al, 1998;Morrissette et al, 2000;Morrissette et al, 2003). Although single-channel analysis indicates that channel activity of RyR1 in fast muscle is higher than that in slow muscle (Morrissette et al, 2000), any functional difference in E-C coupling has not been examined.…”