Adaptive evolution of water homeostasis regulation in amphibians: Vasotocin and hydrins

Abstract

Volemia and osmolality homeostasis is ensured in vertebrates through neuroendocrine reflexes, involving an afferent neural branch from baro- and osmo-receptors to hypothalamus and an efferent endocrine branch from secretory neurons to target hydroosmotic cells equipped with receptors and effectors. Whereas the osmoregulatory system in the tadpole comprises three organs, namely gut, kidney and gills, as in freshwater fishes, the adult displays a quaternary strategy with gut, kidney, urinary bladder and skin. In particular, the cutaneous permeability entails a great evaporative water loss when the animal is in the open air, loss that must be compensated by water reabsorption through the nephron and the urinary bladder and mainly by water uptake through the skin. Adaptation occurred at the level of these organs by regulation of their permeability through neurohypophysial hormones. Aside from vasotocin, active on the three organs, all anuran Amphibia possess hydrin 2 (vasotocinyl-Gly), a peptide resulting from a down-regulation of provasotocin processing. Exceptionally Xenopus laevis, a permanent aquatic toad, has hydrin 1 (vasotocinyl-Gly-Lys-Arg) instead of hydrin 2. Hydrins are somewhat more active than vasotocin on water permeation of skin and bladder but are devoid of antidiuretic activity. Adaptive evolution has created, along with the vasotocin-nephron system, preserved in all terrestrial non-mammalian tetrapods, additional functions such as the hydrin-skin and hydrin-bladder rehydration mechanisms. Specific hydrin receptors might exist in the skin and the bladder, different from those of vasotocin in the kidney. It is assumed that the water channel recruitment mechanism, found for vasopressin acting on the collecting duct principal cells in mammals, is also involved when vasotocin and hydrins stimulate their hydroosmotic target cells and that hormone-regulated aquaporin 2-like proteins could be identified in the three osmoregulatory organs of amphibians.

Correlation between aquaporin and water permeability in response to vasotocin, hydrin and β-adrenergic effectors in the ventral pelvic skin of the tree frogHyla japonica

“…Concerning hydrin, Acher et al (Acher et al, 1997) propose that the primary effect of AVT at its physiological concentration is antidiuresis whereas hydrins have a higher affinity for V2 receptors in the skin and bladder in order to stimulate rehydration and the utilization of bladder water. Our results provide experimental evidence supporting part of this hypothesis by showing that hydrins have a stimulatory effect on water permeability across the pelvic…”

Micropuncture study of ion and water reabsorption regulation range in the distal tubule of triton nephron

“…Chemical evolution of nonapeptides in vertebrates (vasotocin, hydrin 2, and vasopressin) was not accompanied by changes in their functional role [3]. These hormones are involved in the regulation of water-salt metabolism in amphibians, reptilians, birds, and vertebrates [5,11].…”

Localization of prolactin receptor in the dorsal and ventral skin of the frog (Rana ridibunda)

“…In amphibians, osmoregulation is controlled primarily by four hormonal systems: hypothalamo-neurohypophysial system, reninangiotensin-aldosterone system (RAS), hypothalamopituitary-adrenal cortex system and natriuretic peptides system (NPs). Other hormones with osmoregulatory functions such as hydrins, PRL, insulin and guanylins as well as the autonomic nervous system also have a role in osmoregulation (Acher et al 1997;Uchiyama & Konno 2006).…”