Correlation between aquaporin and water permeability in response to vasotocin, hydrin and β-adrenergic effectors in the ventral pelvic skin of the tree frog<i>Hyla japonica</i>

Ogushi, Yuji; Kitagawa, Dai; Hasegawa, Takahiro; Suzuki, Masakazu; Tanaka, Shigeyasu

doi:10.1242/jeb.036871

Cited by 25 publications

(19 citation statements)

References 25 publications

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“…The Bayesian analyes show that the wholly aquatic Western-clawed frog has two paralogs of AQP5 , a canonical form ( AQP5 , formerly annotated as AQP-x5 , [28]) and a related paralog ( AQP5L , formerly annotated as AQP2 ) encoded between two AQP6 genes, the urinary bladder-type ( AQP6ub ) and the ventral skin type ( AQP6vs ) formerly identified as (h2-like and h3-like) type-a2 anuran specific aquaporins [23], [24], [32]. Amongst other Anura the Bayesian data provide statistical support for three paralogs of AQP6 (see Table S2), the urinary bladder type ( AQP6ub ) and two paralogs ( AQP6vs1 , -6vs2 ) that mediate cutaneous hydration through the ventral skin of semi-aquatic and semi-terrestrial anurans [33], [35]. Canonical AQP2 (formerly annotated as AQP-h2k or HC-2, [25], [26]) is found in the genomes of Anura, including the arboreal Pacific treefrog ( Pseudacris regilla ) and the aquatic green frog ( Rana clamitans ), but the absence of an assembled linkage map currently precludes comparison of the loci.…”

Section: Resultsmentioning

confidence: 85%

The Lineage-Specific Evolution of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation

Finn

Chauvigné

Hlidberg³

et al. 2014

PLoS ONE

150

183

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A major physiological barrier for aquatic organisms adapting to terrestrial life is dessication in the aerial environment. This barrier was nevertheless overcome by the Devonian ancestors of extant Tetrapoda, but the origin of specific molecular mechanisms that solved this water problem remains largely unknown. Here we show that an ancient aquaporin gene cluster evolved specifically in the sarcopterygian lineage, and subsequently diverged into paralogous forms of AQP2, -5, or -6 to mediate water conservation in extant Tetrapoda. To determine the origin of these apomorphic genomic traits, we combined aquaporin sequencing from jawless and jawed vertebrates with broad taxon assembly of >2,000 transcripts amongst 131 deuterostome genomes and developed a model based upon Bayesian inference that traces their convergent roots to stem subfamilies in basal Metazoa and Prokaryota. This approach uncovered an unexpected diversity of aquaporins in every lineage investigated, and revealed that the vertebrate superfamily consists of 17 classes of aquaporins (Aqp0 - Aqp16). The oldest orthologs associated with water conservation in modern Tetrapoda are traced to a cluster of three aqp2-like genes in Actinistia that likely arose >500 Ma through duplication of an aqp0-like gene present in a jawless ancestor. In sea lamprey, we show that aqp0 first arose in a protocluster comprised of a novel aqp14 paralog and a fused aqp01 gene. To corroborate these findings, we conducted phylogenetic analyses of five syntenic nuclear receptor subfamilies, which, together with observations of extensive genome rearrangements, support the coincident loss of ancestral aqp2-like orthologs in Actinopterygii. We thus conclude that the divergence of sarcopterygian-specific aquaporin gene clusters was permissive for the evolution of water conservation mechanisms that facilitated tetrapod terrestrial adaptation.

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Section: Resultsmentioning

confidence: 85%

The Lineage-Specific Evolution of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation

Finn

Chauvigné

Hlidberg³

et al. 2014

PLoS ONE

150

183

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“…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). The third objective of this study was to extend these observations and compare them with the response of the Ranid and Bufonid species to AVT.…”

mentioning

confidence: 60%

“…Water permeability was measured across isolated skin from the pectoral, pelvic, and hindlimb regions of B. marinus and the Rana species. Animals were immersed in water for 30 min before being killed to ensure a fully hydrated state for control observations (21). The isolated skin was washed with Ringer solution and then mounted between two chambers connected by an opening having a diameter of 1 cm.…”

Section: Methodsmentioning

confidence: 99%

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

Ogushi

Tsuzuki

Sato

et al. 2010

American Journal of Physiology-Regulatory, Integrative and Comp

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Regions of specialization for water absorption across the skin of Bufonid and Ranid anurans were identified by immunohistochemistry and Western blot analysis, using antibodies raised against arginine vasotocin (AVT)-stimulated aquaporins (AQPs) that are specific to absorbing regions of Hyla japonica. In Bufo marinus, labeling for Hyla urinary bladder-type AQP (AQP-h2), which is also localized in the urinary bladder, occurred in the ventral surface of the hindlimb, pelvic, and pectoral regions. AQP-h2 was not detected in any skin regions of Rana catesbeiana, Rana japonica, or Rana nigromaculata. Hyla ventral skin-type AQP (AQP-h3), which is found in the ventral skin but not the bladder of H. japonica, was localized in the hindlimb, pelvic, and pectoral skins of Bufo marinus, in addition to AQP-h2. AQP-h3 was also localized in ventral skin of the hindlimb of all three Rana species and also in the pelvic region of R. catesbiana. Messenger RNA for AQP-x3, a homolog of AQP-h3, could be identified by RT-PCR from the hindlimb, pectoral, and pelvic regions of the ventral skin of Xenopus laevis, although AVT had no effect on water permeability. In contrast, 10 Ϫ8 M AVT-stimulated water permeability and translocation of AQP-h2 and AQP-h3 into the apical membrane of epithelial cells in regions of the skin of species where they had been localized by immunohistochemistry and Western blot analysis. Finally, water permeability of the hindlimb skin of B. marinus and all the Rana species was stimulated by hydrins 1 and 2 to a similar level as seen for AVT. The present data demonstrate species differences in the occurrence, distribution, and regulation of AQPs in regions of skin specialized for rapid water absorption that can be associated with habitat and also phylogeny. hindlimb skin; arginine vasotocin; immunohistochemistry; water permeability; frogs MANY ADULT ANURAN AMPHIBIANS do not drink through their mouth. Rather, they absorb water across their skin and form dilute urine that is stored in their urinary bladder and can be reabsorbed when foraging away from a hydration source (4, 5). Hillman et al. (14) refer to this water balance strategy as semiterrestrial to distinguish it from terrestrial species that are completely independent of water. The semiterrestrial classification applies to tree frogs in the family Hylidae and toads in the family Bufonidae that have been traditionally classified as arboreal and terrestrial, respectively, in that both have large urinary bladder capacity and specializations for rapidly rehydrating when water is available. Specifically, they utilize an area of skin in the posteroventral region of the body that is specialized for rapid water absorption from shallow water sources or moist substrates. This region, termed the pelvic patch or seat patch, extends laterally to the ventral surface of the hindlimbs and shows a pattern of elevations and grooves termed verrucae hydrophilicae (14). The seat patch is also an area where capillaries form intimate contact with the basement membrane that underli...

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“…Each skin was given 2 30-minute washes with Ringer solution, and then its water permeability was measured basically as reported previously (19,25). Using a modified Ussing chamber, water movement was recorded over a 45-minute period after a 30-minute preincubation with Ringer solution alone, as the control, or with 10 Ϫ8 M AVT in the serosal chamber.…”

Section: Experimental Protocol For Water Permeability In Vitromentioning

confidence: 99%

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

et al. 2014

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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.

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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

Cited by 25 publications

References 25 publications

The Lineage-Specific Evolution of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation

The Lineage-Specific Evolution of Aquaporin Gene Clusters Facilitated Tetrapod Terrestrial Adaptation

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

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

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