Hydrins, hydroosmotic neurohypophysial peptides: osmoregulatory adaptation in amphibians through vasotocin precursor processing.

Abstract

From neurointermediate pituitary glands of Xenopus laevis and Rana escuknta, previously unreported peptides termed hydrins, active on water permeability of frog urinary bladder and frog skin (Brunn or "water-balance" effect), have been isolated and sequenced. These peptides seem to be derived from the pro-vasotocin-neurophysin precursor. Hydrin 1, found in Xenopus, has been identified as vasotocin C-terminally extended with the Gly-Lys-Arg sequence; hydrin 2, found in Rana, has been identified as vasotocin C-terminally extended with glycine. Hydrin 2 has been detected in several Ranidae (R. esculenta, Rana temporaria, Rana pipiens) and Bufonidae (Bufo bufo, Bufo ictercus) and appears to have a large distribution in terrestrial or semiaquatic anurans. Hydrins, in contrast to vasotocin, are not active on rat uterus or rat blood pressure. They are absent from other vasotocinbearers such as birds and could be involved specifically in water-electrolyte regulation of amphibians.Water-electrolyte regulation in amphibians raised peculiar developmental and evolutionary problems because of the transition from aquatic life to terrestrial conditions. Among order Anura, three families, toads (Bufonidae), frogs (Ranidae), and Xenopus (Pipidae), are mostly terrestrial, semiaquatic, and aquatic, respectively, and could have experienced different molecular adaptations. In nonmammalian tetrapods, the neurohypophysial peptide vasotocin (1-3) is known to play on kidney the antidiuretic role attributed to vasopressin in mammals (4). Furthermore, in frogs and toads, this hormone is also active on urinary bladder, determining water reabsorption across the wall, and on skin, increasing water uptake from hypotonic bathing solutions (Brunn or "water-balance" effect) (5). In these species, aside from vasotocin and mesotocin, which have been chemically characterized in Rana esculenta (1, 6), Rana pipiens (7), and Bufo bufo (2), occurrence of an additional peptide stimulating active sodium transport through the skin ("natriferic effect") has been suggested (8). In Xenopus, however, vasotocin, detected in the posterior pituitary gland (3), is active neither on the bladder nor on the skin ofthis permanently freshwaterdwelling animal in contrast to frogs and toads (5). Therefore, it was of interest to investigate comparatively the maturation of the vasotocin precursor in Rana and Xenopus genera and to look for previously unreported active peptides.In nonmammalian tetrapods, vasotocin is linked to a MSEL-type neurophysin (neurophysin containing methionine-2, serine-3, glutamic acid-6, and leucine-7) in a common precursor (9, 10). This precursor, homologous to the mammalian vasopressin precursor, is processed into two pieces rather than three as is the mammalian one. As a result, along with vasotocin, a "big" neurophysin encompassing two domains homologous to mammalian MSEL-neurophysin and copeptin, respectively, is produced (9, 11). Neurohypophysial peptides of R. esculenta and Xenopus laevis have been examined to specify the vasotocin ...

The water-absorption region of ventral skin of several semiterrestrial and aquatic anuran amphibians identified by aquaporins

“…Like AVT, hydrins stimulate osmotic water movement across the skin and bladder but are devoid of antidiuretic activity in the kidney (19,24). Hydrins are only present in anuran amphibians, and we found that hydrin 1 and hydrin 2, as well as AVT, have stimulatory effects on the water permeability across the pelvic skin in H. japonica (21).…”

“…Of interest, X. laevis secretes hydrin 1, as well as AVT but shows no hydroosmotic response of skin to either. However, AVT and hydrin 1 both stimulate water reabsorption from the urinary bladder and may be involved in the water balance in X. laevis during aestivation (24). …”

Evolutionary specificity of hydrins, new hydroosmotic neuropeptides: occurrence of hydrin 2 (vasotocinyl‐Gly) in the toad Bufo marinus but not in the viper Vipera aspis

“…Hydrins are neurohypophysial peptides discovered in amphibians and endowed with hydroosmotic activity on the skin and the urinary bladder of these animals [ 1,2]. They are physiologically produced by partial processing of the vasotocin-neurophysin precursor and have been found so far in anurans but not in birds such as geese [3].…”

“…They are physiologically produced by partial processing of the vasotocin-neurophysin precursor and have been found so far in anurans but not in birds such as geese [3]. Hydrin 1 (vasotocinyl-Gly-Lys-Arg) has been characterized in the aquatic Xenopus laevis (Pipidae) whereas hydrin 2 (vasotocinyl-Gly) has been identified in semi-aquatic or terrestrial anuran species such as Rana esculenta (Ranidae) [1,2]. Bufo marinus is an exotic toad imported on the American continent and it is of interest to assess whether hydrin 2 is also present in this animal despite its peculiar origin and habitat.…”

“…Bufo marinus is an exotic toad imported on the American continent and it is of interest to assess whether hydrin 2 is also present in this animal despite its peculiar origin and habitat. On the other hand, because hydrins have been assumed to result from an adaptative processing proper to amphibians for facing a particular osmoregulation [1,2], we have examined a reptile, the viper (Vipera aspis) in order to check their absence in this class of vertebrates.…”