Water Adaptation Strategy in Anuran Amphibians: Molecular Diversity of Aquaporin

Abstract

Most adult anuran amphibians except for the aquatic species absorb water across the ventral pelvic skin and reabsorb it from urine in the urinary bladder. Many terrestrial and arboreal species use a region in the posterior or pelvic region of the ventral skin that is specialized for rapid rehydration from shallow water sources or moist substrates. Periods of terrestrial activity can be prolonged by reabsorption of dilute urine from the urinary bladder. Aquaporin (AQP), a water channel protein, plays a fundamental role in these water absorption/reabsorption processes, which are regulated by antidiuretic hormone. Characterization of AQPs from various anurans revealed that the unique water homeostasis is basically mediated by two types of anuran-specific AQPs, i.e. ventral pelvic skin and urinary bladder type, respectively. The bladder-type AQP is further expressed in the pelvic skin of terrestrial and arboreal species, together with the pelvic skin-type AQP. In contrast, the pelvic skin-type AQP (AQP-x3) of the aquatic Xenopus has lost the ability of efficient protein production. The extra C-terminal tail in AQP-x3 consisting of 33 nucleotides within the coding region appears to participate in the posttranscriptional regulation of AQP-x3 gene expression by attenuating protein expression. The positive transcriptional regulation of bladder-type AQP in the pelvic skin and negative posttranscriptional regulation of pelvic skin-type AQP provide flexibility in the water regulation mechanisms, which might have contributed to the evolutionary adaptation of anurans to a wide variety of water environments.

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

“…More recently, we have found AQP-x3 mRNA, that is homologous to AQP-h3, is expressed in the pelvic skin of the aquatic species, Xenopus laevis, but the mRNA is not translated to AQP-x3 protein (20). Given the different patterns of regional specialization seen in terrestrial, arboreal, and semiaquatic species, the second objective of this study was to examine the expression of AQP-x3 mRNA in the skin of the hindlimb, pelvic, pectoral, and dorsal regions.…”

“…The mechanism for baseline and AVT-stimulated water permeability is controlled by aquaporins (AQPs), a class of integral membrane proteins that form selective water channels (pores) in the plasma membranes of various cells in virtually all organisms (1,17,23,30). AVT stimulation results in the fusion of subapical vesicles containing the AQPs, with the apical membrane of epithelial tissues specialized for water absorption and reabsorption.Recently, our group used RT-PCR to identify two forms of AVT-stimulated AQP in epithelial tissues of the skin of the tree frog, Hyla japonica: AQP-h2 was found in the urinary bladder, as well as the pelvic skin region (13,20,31). AQP-h2-like AQPs are also localized in the urinary bladder of Rana and Bufo species (20, 27) and have been referred to as the "urinary bladder-type" amphibian AQP (20).…”

“…Recently, our group used RT-PCR to identify two forms of AVT-stimulated AQP in epithelial tissues of the skin of the tree frog, Hyla japonica: AQP-h2 was found in the urinary bladder, as well as the pelvic skin region (13,20,31). AQP-h2-like AQPs are also localized in the urinary bladder of Rana and Bufo species (20, 27) and have been referred to as the "urinary bladder-type" amphibian AQP (20).…”

“…AQP-h2-like AQPs are also localized in the urinary bladder of Rana and Bufo species (20,27) and have been referred to as the "urinary bladder-type" amphibian AQP (20). The second isoform, AQPh3, was characterized from the ventral skin but not the urinary bladder of H. japonica (31).…”

“…The second isoform, AQPh3, was characterized from the ventral skin but not the urinary bladder of H. japonica (31). AQP-h3-like AQPs have similarly been characterized in ventral skin but not the bladder of Hyla, Bufo, and Rana species and have been termed the "ventral skin-type" AQP (20). This tissue distribution of AQP-h2 and AQP-h3 isoforms is provided in Table 1. A subfamily of AQPs, termed aquaglyceroporins occurs in the basolateral membranes of water-transporting epithelia (1,17) and is permeated by glycerol and urea in addition to water.…”