The high heart performance in mako shark is related to increased caveolin expression in buoyant fraction

Abstract

Mammalian hearts have a developed sympathetic system coupled to complex intracellular signaling pathways to markedly increase heart rate and contractility. Caveolae are sub-cellular structures enriched in caveolin proteins and are essential for t-tubules formation, signaling, and calcium homeostatsis. In general, species from this clade, such as mako shark, can attain mammalian-like cardiac function. This study examined the plausible traits in the design of a high performance heart of the regional endothermic mako sharks to the ectothermic blue sharks and rats by comparing caveolin distribution and myocyte ultrastructure. Caveolin 1/3 distribution was determined by sucrose density fractionation of heart homogenates. Electron microscopy (EM) was performed to assess the presence of caveolae and t-tubule. Following fractionation, caveolin was predominantly detected in buoyant fraction (BF) with relatively little heavy fraction (HF) in both sharks, findings akin to rat vascular smooth muscle cells (VSMC, Figure), which lack t-tubules. In rats, caveolin was present in both BF and HF, the latter indicative of t-tubule in mammals. EM analyses showed no t-tubules in both shark hearts, but were found in rats. Compared to blue sharks, the preponderance in BF of Cav1/3 (i.e., more caveolae) in the mako is one of the traits in achieving higher heart performance.