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Acid-base Sensing and Regulation in Marine Animals

Abstract

Regulation of acid-base stress (i.e. carbon dioxide [CO2], pH, and bicarbonate [HCO3-]) is essential for proper functioning of cells, organs, and whole-animals; however, the mechanisms for sensing acid-base stress are largely unknown in marine animals. Therefore, for my dissertation research I investigated the evolutionarily conserved acid-base sensor soluble adenylyl cyclase (sAC, adcy10) in leopard sharks (Triakis semifasciata), round rays (Urolophus halleri), and hagfish (Eptatretus stoutii).

Leopard shark gills have two acid-base regulatory cell types: acid-secreting Na¬+/K+-ATPase (NKA)-rich and base-secreting V-H+-ATPase (VHA)-rich cells. Base-secreting VHA-rich cells also contain the Cl-/HCO3- exchanger pendrin. In starved sharks, VHA and pendrin are present in the cell cytoplasm; but, in fed sharks, each translocates to the basolateral and apical membrane, respectively. This translocation is likely mediated by HCO3--stimulated sAC, which is highly abundant in both acid- and base-secreting leopard shark gill cells. sAC is also present in other tissues, including rectal gland, cornea, intestine, muscle, and heart tissues; and it is present in the cell nucleus, where it is likely mediates regulation of gene expression.

In round rays, sAC is also highly abundant in acid-secreting NKA-rich and base-secreting VHA-rich calls. Additionally, sAC is co-expressed along with hormone-regulated transmembrane adenylyl cyclases (tmACs, adcy1-9). However, sAC, and not tmACs, is essential for VHA translocation to the cell membrane of isolated base-secreting gill cells exposed to extracellular alkalosis, an indication that this process is locally regulated by sAC without the involvement of whole-animal hormone regulation.

In hagfish, sAC is present in both the atrial and ventricle heart chambers; and sAC regulates heart beat rate in isolated hearts recovering from anoxia exposure, a previously unknown role for HCO3--activated sAC-cAMP signal transduction pathway that has potential implications for the mammalian heart.

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