Hormone metabolism by the fish gill

The fish gill, like the mammalian lung, is ideally situated to process circulating biomolecules because: 1) the gill is the only organ perfused by the entire cardiac output, 2) the in-series positioning of branchial and systemic circulations permits "conditioning" of blood immediately before systemic perfusion and 3) gill microcirculation is extensive, providing substantial endothelial/pillar cell surface in contact with plasma. In addition, two or three distinct circulatory pathways within the gill may differentially affect plasma substrates, raising the possibility of vasoactive control of hormone titers. Hormones may be activated or inactivated by the gill, the latter involving extraction (uptake) from the plasma, metabolism by enzymes on the endothelial surface without uptake or uptake plus intracellular metabolism. Over 60% of angiotensin I (ANG I) is activated to angiotensin II (ANG II) in a single transit through the gill lamellae by pillar cell angiotensin-converting enzyme, whereas both ANG I and II are inactivated by the non-lamellar filamental vasculature. Gills may accumulate and store (uptake 1) or degrade (uptake 2) catecholamines via intracellular monoamine oxidase and catechol-O-methyl transferase enzymes, and they show substrate preference for norepinephrine over epinephrine. Similar processes may exist for serotonin. Atrial natriuretic peptides are efficiently (60-90%) extracted from plasma in vivo by C-type clearance receptors. Fifty percent of an endothelin-1 bolus is removed in a single transit through the gill circulation, arginine vasotocin extraction is modest and bradykinin is virtually unaffected. Arachidonic acid is completely extracted by the gill, whereas extraction of prostaglandins I2 and E2 is only 13 and 5%, respectively. Intense cytochrome P450 immunofluorescence in the pillar cells suggests that the gill vasculature may be an important site of detoxification and production of biologically active epoxides. Thus, gills appear to be potent and selective effectors of hormonal signals.