Correlation between water flow and intramembrane particle aggregates in toad epidermis

Brown, Dennis; Grosso, A.; DeSousa, Ryan

doi:10.1152/ajpcell.1983.245.5.c334

Cited by 112 publications

(24 citation statements)

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“…We were able to show here that IP induces the translocation of AQP-h2 and AQP-h3 proteins from the cytoplasmic pool to the apical plasma membrane, thereby increasing water permeability. This observation confirms earlier findings using freeze-fracture techniques that showed IP stimulating the movement of the intramembrane particle aggregates (Brown et al, 1983). However, our experiments provide new insight to this field in terms of elucidating the molecular mechanisms underlying the water flow across the pelvic skin of the tree frog by identifying the AQP molecules such as AQP-h2 and AQP-h3.…”

Section: Y Ogushi and Otherssupporting

confidence: 91%

“…Brown et al measured a correlation between the aggregation of intramembrane particles (termed aggrephore) and water flow in toads skin in response to the mammalian antidiuretic hormone arginine vasopressin (Brown et al, 1983). These particles were subsequently shown to be a class of integral membranes [termed aquaporins (AQPs)] that form selective water channels in the plasma membranes in various cells of various organisms (Preston et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

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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

Ogushi

Kitagawa

Hasegawa

et al. 2010

Journal of Experimental Biology

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SUMMARYThe ventral pelvic skin of the tree frog Hyla japonica expresses two kinds of arginine vasotocin (AVT)-stimulated aquaporins (AQP-h2 and AQP-h3), which affect the capacity of the frog's skin to absorb water. As such, it can be used as a model system for analyzing the molecular mechanisms of water permeability. We investigated AQP dynamics and water permeability in the pelvic skin of H. japonica following challenge with AVT, hydrins (intermediate peptides of pro-AVT) and -adrenergic effectors. In the in vivo experiment, both AQP-h2 and AQP-h3 proteins were translocated to the apical plasma membrane in the principal cells of the first-reacting cell (FRC) layer in the pelvic skin following challenge with AVT, hydrin 1 and hydrin 2, thereby increasing the water permeability of the pelvic skin. The -adrenergic receptor agonist isoproterenol (IP) and its anatagonist propranolol (PP) in combination with AVT or hydrins were used as challenge in the in vitro experiment. IP increased water permeability whereas PP inhibited it, and both events were well correlated with the translocation of the AQPs to the apical membrane. In the PP+AVT-treated skins, labels for AQP-h2 and AQP-h3 were differentially visible among the principal cells; the apical plasma membrane of some cells was labeled while others were not, indicating that the response of PP or AVT is different from cell to cell. These results provide morphological evidence that the principal cells of the FRC layers may have two kinds of receptors: a V2 receptor and -adrenergic receptor.

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Section: Y Ogushi and Otherssupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

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

Ogushi

Kitagawa

Hasegawa

et al. 2010

Journal of Experimental Biology

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“…Experiments were carried out as in Fig. 1 Based on freeze-fracture electron micrographs in vasopressin-responsive epithelia showing a strong correlation between Pf and the appearance of apical membrane particle aggregates (3)(4)(5), it is assumed that the time course of Pf increase is a measure of membrane exocytosis. To support the interpretation that the time course of Pf decrease is a measure of membrane endocytosis, uptake ofrhodamine-dextran, a fluid phase marker of endocytosis, was measured after vasopressin removal in the presence of bath > lumen, lumen > bath, and lumen = bath osmolalities.…”

Section: Resultsmentioning

confidence: 99%

“…Key words: endocytosis * kidney collecting tubule -vasopressinwater permeability sitive epithelia is thought to involve a cycle of exocytosis and endocytosis where intracellular vesicles containing water channels are inserted into and removed from the cellular apical membrane (1,2). There is a good correlation between the presence ofapical membrane particle aggregates and transepithelial osmotic water permeability in toad bladder granular cells and kidney collecting tubule cells involved in the hydroosmotic response to vasopressin (3)(4)(5). Endosomes isolated from toad urinary bladder that were formed in response to vasopressin contained functional water channels that might be recycled between subcellular and plasma membrane compartments (6).…”

mentioning

confidence: 99%

Transcellular water flow modulates water channel exocytosis and endocytosis in kidney collecting tubule.

Kuwahara

Shi²,

Marumo³

et al. 1991

J. Clin. Invest.

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IntroductionThe regulation of osmotic water permeability (Pf) by vasopressin (VP) in kidney collecting tubule involves the exocytic-endocytic trafficking of vesicles containing water channels between an intracellular compartment and apical plasma membrane. The regulation ofwater permeability in vasopressin (VP)'-sensitive epithelia is thought to involve a cycle of exocytosis and endocytosis where intracellular vesicles containing water channels are inserted into and removed from the cellular apical membrane (1, 2). There is a good correlation between the presence ofapical membrane particle aggregates and transepithelial osmotic water permeability in toad bladder granular cells and kidney collecting tubule cells involved in the hydroosmotic response to vasopressin (3-5). Endosomes isolated from toad urinary bladder that were formed in response to vasopressin contained functional water channels that might be recycled between subcellular and plasma membrane compartments (6).Endosomes containing the vasopressin-sensitive water channel had low urea and proton permeabilities (7), and very high water permeability that was not subject to direct biochemical regulation (8). The signaling mechanism responsible for the modulation of membrane cycling is believed to involve a cAMP-dependent protein kinase and the cell cytoskeleton (9); however, the biochemical and physical factors controlling exocytosis and endocytosis have not been established.In kidney collecting tubule, endocytosis of water channels probably occurs by formation of clathrin-coated pits (10-12); however, little is known about the fate of endocytosed membranes or ofthe mechanism by which intracellular membranes fuse with the apical surface in response to vasopressin addition. Endosomes formed in the papillary collecting tubule from Brattleboro rats contained functional water channels only when the rats had received vasopressin or the V2 agonist DDAVP before endosome isolation (13,14), providing strong evidence for a water channel shuttle mechanism in kidney collecting tubule. The vasopressin-induced endosomes did not acidify in response to ATP, and endocytosed fluid phase markers did not colocalize with lysosomes, raising the interesting possibility that intracellular processing of endosomes containing the vasopressin-sensitive water channel does not involve the conventional endocytotic pathway of progressive acidification (15). In kidney proximal tubule, there is rapid constitutive (hormone-independent) endocytosis that also involves clathrin-coated vesicles (12,16,17). However, in contrast to collecting tubule, endosomes from apical membrane of proximal tubule contain functional water channels and do fuse

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“…After incubation, the skins were examined by immunofluorescence microscopy, as described above, to evaluate incorporation of AQP-h3 and AQP-h2 into the apical membrane of the first reacting cell (FRC) layer that is joined by tight junction to form a continuous barrier between the outside and inside of the body (6,7,11,13,35).…”

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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Correlation between water flow and intramembrane particle aggregates in toad epidermis

Cited by 112 publications

References 0 publications

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

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

Transcellular water flow modulates water channel exocytosis and endocytosis in kidney collecting tubule.

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

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