An Emerging Role for a Cardiac Peptide Hormone in Fish Osmoregulation

Abstract

It is clear from the extant literature that various fish groups face chronic osmoregulatory problems that depend on the surrounding salinity. Their physiologic and hormonal responses are largely those seen in the mammals, but their terrestrial descendants have lost osmoregulatory structures such as gills and rectal glands and depend primarily on renal function. A data base is now emerging that strongly suggests that a putative atriopeptin plays a role in osmoregulation in fishes. This conclusion is supported by the fact that heterologous AP produces relevant physiologic responses (e.g. natriuresis, vasodilation, stimulation, or inhibition of Na+ secretion by intestine, gills, and rectal gland) in both teleosts and elasmobranchs. Moreover, cardiac and brain extracts from fish can produce similar effects in both fishes and mammals, and these tissues from various fish groups contain immunoreactive AP, as does plasma. Both physiologic and immunologic evidence suggests that the ventricle may be a significant source of AP in fishes, contrary to the situation in mammals. Finally, osmotic perturbations result in a change in plasma and tissue APir levels. The finding that plasma APir levels increase in sea water, and that heterologous AP stimulates salt secretion by the teleost gill and shark rectal gland, and inhibits salt uptake by the teleost intestine, suggests that AP may primarily play a role in salt, rather than fluid, secretion in fishes. The fact that in mammals AP inhibits prolactin secretion, but is itself stimulated by cortisol, supports this conclusion, since prolactin is generally considered to be the dominant osmoregulatory hormone in freshwater fishes, and cortisol serves this function in marine fishes. In addition, if AP inhibits brain AVT release in fishes, as it apparently inhibits vasopressin release in mammals, this also would be adaptive in marine fishes since AVT in fishes is diuretic, rather than antidiuretic. Interactions between AP and these hormones (prolactin, cortisol, and ATV) have not been studied in fishes to date, but these theoretical interactions do lend support to the hypothesis that AP may function primarily in salt homeostasis in fishes. At least one potential hormonal interaction counters this argument, however. Atriopeptin is known to inhibit the production and effects of angiotensin II in mammals, and since this hormone is apparently dipsogenic in fishes, it may play a critical role in osmoregulation in sea water. Finally, it is of some historical interest that in Keys' (67) original description of the eel heart-gill perfusion system in 1931 he commented that gill resistance remained constant for hours only if the heart itself was perfused.(ABSTRACT TRUNCATED AT 400 WORDS)

Regulation of interrenal function in freshwater and sea water adapted tilapia (Oreochromis mossambicus)

“…A N P than atria, con firms results from morphometric and biosynthetic studies on other fish species (Baranowski and Westenfelder 1989). Because we used a heterolo gous R IA , we cannot compare our data directly with other studies on fish, in which a variety of homologous and heterologous antisera was used (Baranowski and Westenfelder 1989;Evans et al 1989;Evans 1990;Broadhead et al 1992;Powell and Miller 1992;Takei et al 1992). Most likely, our antiserum recognized both A N P and VNP (Takei et al 1992).…”

“…We previously demonstrated (Balm et al 1987) that the stimulation of the interrenal which occurs under those conditions concurs with 1) an increased sensitivity of the organ to ACTH and, 2) with a significant hyperplasia of the cortico tropes. Tilapia under low pH conditions benefit 45 from increased branchial active sodium and chlo ride uptake (Balm 1986 Takei and Balment (1993), using a hom olo gous R IA , demonstrated that in SW-adapted eels, plasma A N P levels were actually lower than in FWadapted eels, which conflicts with the opinion held until then that SW adaptation in teleosts was as sociated with elevations of plasma A N P levels (Evans 1990). Our present results further highlight the species differences that exist in the mechanisms of action of A N P in the control of ion homeostasis.…”

The natriuretic peptide system in eels: a key endocrine system for euryhalinity?

“…There are several studies on the osmoregulatory actions of ANP in teleost species other than eels, the results of which are not always consistent with those of eels, as summarized in a number of reviews (23,26,51,86). Plasma ANP concentration is generally higher in SW fish than in FW fish or in euryhaline fish that are in SW than in FW (25,31,77,105).…”

A single and novel natriuretic peptide is expressed in the heart and brain of the most primitive vertebrate, the hagfish (Eptatretus burgeri)

“…Natriuretic peptides (NPs) are a hormone family that plays a pivotal role in cardiovascular and body fluid homeostasis in vertebrates (Brenner et al 1990, Evans 1990, Farrell & Olson 2000, Loretz & Pollina 2000, Takei 2000. While the NP family consists of atrial natriuretic peptide (ANP), brain natriuretic peptide (BNP) and C-type natriuretic peptide (CNP) in mammals and amphibians, ANP, VNP (ventricular natriuretic peptide) and CNP occur in teleost fish.…”