Novel Vasotocin-Regulated Aquaporins Expressed in the Ventral Skin of Semiaquatic Anuran Amphibians: Evolution of Cutaneous Water-Absorbing Mechanisms

Abstract

Until now, it was believed that only one form of arginine vasotocin (AVT)-regulated aquaporin (AQP) existed to control water absorption from the ventral skin of semiaquatic anuran amphibians, eg, AQP-rj3(a) in Rana japonica. In the present study, we have identified a novel form of ventral skin-type AQP, AQP-rj3b, in R. japonica by cDNA cloning. The oocyte swelling assay confirmed that AQP-rj3b can facilitate water permeability. Both AQP-rj3a and AQP-rj3b were expressed abundantly in the ventral hindlimb skin and weakly in the ventral pelvic skin. For the hindlimb skin, water permeability was increased in response to AVT, although the hydroosmotic response was not statistically significant in the pelvic skin. Isoproterenol augmented water permeability of the hindlimb skin, and the response was inhibited by propranolol. These events were well correlated with the intracellular trafficking of the AQPs. Immunohistochemistry showed that both AQP-rj3 proteins were translocated from the cytoplasmic pool to the apical membrane of principal cells in the first-reacting cell layer of the hindlimb skin after stimulation with AVT and/or isoproterenol. The type-b AQP was also found in R. (Lithobates) catesbeiana and R. (Pelophylax) nigromaculata. Molecular phylogenetic analysis indicated that the type-a is closely related to ventral skin-type AQPs from aquatic Xenopus, whereas the type-b is closer to the AQPs from terrestrial Bufo and Hyla, suggesting that the AQPs from terrestrial species are not the orthologue of the AQPs from aquatic species. Based on these results, we propose a model for the evolution of cutaneous water-absorbing mechanisms in association with AQPs.

Phylogenomic and functional analyses of salmon lice aquaporins uncover the molecular diversity of the superfamily in Arthropoda

“…4 ). This suggested that a cAMP-dependent phosphorylation mechanism may be involved in the trafficking of the Glp_v1 channel to the plasma membrane as reported for some vertebrate [ 10 , 12 , 70 – 74 ] and plant aquaporins [ 75 – 77 ]. An in silico analysis of the putative phosphorylation sites indicates that five residues in the N-terminus of Glp1_v1 (Ser 2 , Thr 3 , Tyr 9 , Thr 14 and Ser 21 ) differ in phosphorylation potential compared to the Glp1_v2 isoform (Fig.…”

Temperature and dehydration effects on metabolism, water uptake, and the partitioning between respiratory and cutaneous evaporative water loss in a terrestrial toad

“…Cloudsley-Thompson, 1967;Claussen, 1969;Tracy, 1976). Although uncertain, we suspect that some of the physiological parameters affecting skin permeability respond differently to combined changes in temperature and hydration state, possibly involving adjustments in local microcirculatory perfusion of the pelvic patch (Slivkoff and Warburton, 2001;Viborg and Rosenkilde, 2004;Viborg et al, 2006) and constitutive changes in this region's water permeability (Willumsen et al, 2007), mediated by changes in the expression of aquaporins (Hasegawa et al, 2003;Suzuki et al, 2007;Saitoh et al, 2014).…”

Central Effects of Beta-Blockers May Be Due to Nitric Oxide and Hydrogen Peroxide Release Independently of Their Ability to Cross the Blood-Brain Barrier

“…Little is known in the literature to explain the mode of action of propranolol to avoid H 2 O 2 release. It has been shown that, in the skin of frog, propranolol is able to decrease water permeability induced by arginine vasotocin (AVT) (Ogushi et al, 2010; Saitoh et al, 2014). In this model, aquaporins are translocated at the membrane in response to AVT.…”