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

Abstract

Takei, Yoshio, and Shigehisa Hirose. The natriuretic peptide system in eels: a key endocrine system for euryhalinity? Am J Physiol Regulatory Integrative Comp Physiol 282: R940-R951, 2002; 10.1152/ajpregu. 00389.2001.-The natriuretic peptide system of a euryhaline teleost, the Japanese eel (Anguilla japonica), consists of three types of hormones [atrial natriuretic peptide (ANP), ventricular natriuretic peptide (VNP), and Ctype natriuretic peptide (CNP)] and four types of receptors [natriuretic peptide receptors (NPR)-A, -B, -C, and -D]. Although ANP is recognized as a volume-regulating hormone that extrudes both Na ϩ and water in mammals, ANP more specifically extrudes Na ϩ in eels. Accumulating evidence shows that ANP is secreted in response to hypernatremia and acts to inhibit the uptake and to stimulate the excretion of Na ϩ but not water, thereby promoting seawater (SW) adaptation. In fact, ANP is secreted immediately after transfer of eels to SW and ameliorates sudden increases in plasma Na ϩ concentration through inhibition of drinking and intestinal absorption of NaCl. ANP also stimulates the secretion of cortisol, a long-acting hormone for SW adaptation, whereas ANP itself disappears quickly from the circulation. Thus ANP is a primary hormone responsible for the initial phase of SW adaptation. By contrast, CNP appears to be a hormone involved in freshwater (FW) adaptation. Recent data show that the gene expression of CNP and its specific receptor, NPR-B, is much enhanced in FW eels. In fact, CNP infusion increases 22 Na uptake from the environment in FW eels. These results show that ANP and CNP, despite high sequence identity, have opposite effects on salinity adaptation in eels. This difference apparently originates from the difference in their specific receptors, ANP for NPR-A and CNP for NPR-B. VNP may compensate the effects of ANP and CNP for adaptation to respective media, because it has high affinity to both receptors. On the basis of these data, the authors suggest that the natriuretic peptide system is a key endocrine system that allows this euryhaline fish to adapt to diverse osmotic environments, particularly in the initial phase of adaptation. atrial natriuretic peptide; ventricular natriuretic peptide; C-type natriuretic peptide; membrane guanylyl cyclase; water and electrolyte balance; molecular evolution; functional evolution; volume regulation; sodium regulation; Anguilla japonica ATRIAL NATRIURETIC PEPTIDE (ANP) was the first member of the natriuretic peptide (NP) family identified in mammals (17,63,69,86). Subsequent to the isolation and sequencing of ANP from the rat atria in 1983, brain natriuretic peptide (BNP) and C-type natriuretic peptide (CNP) were isolated from the porcine brain in 1988 and 1990, respectively, and they were identified as members of the NP family (Fig. 1). Whereas ANP and BNP are circulating hormones secreted from the heart, CNP is principally a paracrine factor in the brain and periphery (71). The basic structure of the NP peptides consists of an intramolecular...

Steroidogenic Acute Regulatory Protein in Eels: cDNA Cloning and Effects of ACTH and Seawater Transfer on Its mRNA Expression

“…This is not surprising, because StAR is mainly involved in the regulation of acute steroid production (Stocco, 2001). Besides, in addition to cortisol, multiple hormones such as growth hormone/insulinlike growth factor I axis, thyroid hormones, ANP, ANG II and urotensins are also implicated in SW adaptation, and some of them have been shown to increase cortisol production in eels and other teleost fishes (Arnold-Reed and Balment, 1994;McCormick, 2001;Tsukada and Takei, 2001;Takei and Hirose 2002). Actually, plasma ANG II and ANP concentrations increased transiently after SW transfer in eels (Tierney et al, 1995;Kaiya and Takei, 1996).…”

Regulation of Ion Transport in Eel Intestine by the Homologous Guanylin Family of Peptides

“…This is also true for the effect on the intestine; ANP is a potent inhibitor for water and ion absorption in teleosts but the effect is negligible in mammals. On the renal effect, however, ANP is weakly natriuretic and antidiuretic in SW eels, suggesting that the common action of ANP in mammals and teleosts is to decrease NaCl from the body but not water (Takei and Hirose, 2002).…”

“…For instance, 100-fold higher doses are required for Ang II to elicit drinking in teleosts and the induced water intake is much smaller than that in mammals (Takei, 2002). In contrast, atrial natriuretic peptide (ANP) injected into the circulation of SW eels almost stopped drinking at low physiological doses that do not change arterial pressure, but ANP is only a weak antidipsogenic hormone in mammals even at much higher hypotensive doses (Takei and Hirose, 2002). Furthermore, many dipsogenic hormones have been identified in mammals, while most hormones that modulate drinking are antidipsogenic in eels (Takei, 2002;Kozaka et al, 2003).…”

Expression of endocrine genes in zebrafish larvae in response to environmental salinity

“…ANP is secreted in response to an increase in blood volume and promotes excretion of water and Na C by the kidney, and functions to inhibit Na C appetite and thirst, thus preventing further accumulation of Na C and water. On the other hand, ANP likely responds to the plasma Na C level, rather than blood volume, in eel, a euryhaline fish, which means it can adapt to both freshwater and seawater (Takei & Hirose 2002. During seawater adaptation, which tends to decrease blood volume but increase plasma Na C concentration, ANP is temporally secreted and prevents excess Na C absorption (Tsukada et al 2005.…”