Role of membrane fusion in CO2 stimulation of proton secretion by turtle bladder

Stetson, David L.; Steinmetz, Philip R.

doi:10.1152/ajpcell.1983.245.1.c113

Cited by 264 publications

(47 citation statements)

References 18 publications

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“…Addition of CO2 caused fusion of some of these vesicles with the apical plasma membrane leading to an increase in the number of these functional H+ pumps exposed to the luminal fluid. This insertion of H+ pumps was correlated with enhanced H+ secretion across the bladder (5), and ultrastructurally, with increased luminal membrane area and decreased number of cytoplasmic vesicles in carbonic anhydrase-containing cells (6). Recently, similar ultrastructural changes were seen in the intercalated cells of the rat collecting tubule (9).…”

Section: Introductionmentioning

confidence: 79%

Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules.

Schwartz¹,

Al‐Awqati²

1985

J. Clin. Invest.

233

105

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In the turtle bladder it has recently been shown that CO2 stimulates H' secretion, at least in part, by causing fusion of vesicles enriched in H' pumps with the luminal plasma membrane. To test for the presence of this mechanism in the kidney we perfused collecting ducts and proximal straight tubules on the stage of an inverted epifluorescence microscope with fluorescein isothiocyanate dextran (70,000 mol wt) in CO2-free medium. After washout we noted punctate fluorescence in endocytic vesicles in some collecting ducts and in all proximal straight tubule cells. More cells took up fluorescent dextran in outer medullary than in cortical collecting ducts. Using the pH dependence of the excitation spectrum of fluorescein we found the pH of the vesicles to be acid (-pH 6). Addition of proton ionophores increased vesicular pH by 0.6±0.1 U, suggesting that the acidity of the vesicles was caused by H' pumps. CO2 added to the medium (25 mmHg, pH 7.6 at 370C) reduced fluorescence intensity by 24±5% in cortical collecting ducts, 27±5% in medullary collecting ducts, and 25±5% in proximal straight tubules. Since this effect was prevented by the prior addition of colchicine to the bath, we believe that CO2 caused a decrease in cytoplasmic fluorescence by stimulating exocytotic fusion of the vesicles and thereby secretion of fluorescent dextran. This exocytotic fusion also occurred when tubules that were loaded with fluorescent dextran at a pCO2 of 37 mmHg were exposed isohydrically to a pCO2 of 114 mmHg; the mean decrease was 53±4%.We conclude that some cells in the collecting ducts and all cells in the proximal straight tubule incorporate fluorescent dextran into the apical cytoplasmic vesicles and acidify them with H+ pumps. CO2 causes fusion of these vesicles with the luminal membrane, but whether CO2 stimulates H+ secretion by increasing the number of functioning H+ pumps remains to be determined.

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Section: Introductionmentioning

confidence: 79%

Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules.

Schwartz¹,

Al‐Awqati²

1985

J. Clin. Invest.

233

105

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“…Moreover, the apical surface of the intercalated MR cell is enlarged by slender, branching microfolds that, from scanning electron microscopy, can be seen to produce a honeycomb appearance (Figs·2A,·3C). As primarily shown in the epithelium of the turtle urinary bladder, the extent of such enlargements, which varies markedly amongst intercalated MR cells, is inversely related to the number of membranous tubules and vesicles in the apical cytoplasm, which are incorporated into and removed from the apical membrane by exo-and endocytosis, respectively (Stetson and Steinmetz, 1983;Brown, 1989;Brown and Breton, 2000). A coat of studs projects about 12·nm outwards from the cytoplasmic side of the apical membrane (Fig.·2B).…”

Section: The Freshwater Phases In the Life Cycle The Intercalated Mr mentioning

confidence: 91%

Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys

Bartels

Potter

2004

Journal of Experimental Biology

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SUMMARY Lampreys, one of the only two surviving groups of agnathan (jawless)vertebrates, contain several anadromous species that, during their life cycle,thus migrate from fresh to seawater and back to freshwater. Lampreys have independently evolved the same overall osmoregulatory mechanisms as the gnathostomatous (jawed) and distantly related teleost fishes. Lamprey gills thus likewise play a central role in taking up and secreting monovalent ions. However, the ultrastructural characteristics and distribution of their epithelial cell types [ammocoete mitochondria-rich (MR) cell, intercalated MR cell, chloride cell and pavement cell] differ in several respects from those of teleosts. The ultrastructural characteristics of these cells are distinctive and closely resemble those of certain ion-transporting epithelia in other vertebrates, for which the function has been determined. The data on each cell type, together with the stage in the life cycle at which it is found, i.e. whether in fresh or seawater, enable the following proposals to be made regarding the ways in which lampreys use their gill epithelial cells for osmoregulating in hypo- and hypertonic environments. In freshwater, the intercalated MR cell takes up Cl– and secretes H+,thereby facilitating the uptake of Na+ through pavement cells. In seawater, the chloride cell uses a secondarily active transcellular transport of Cl– to provide the driving force for the passive movement of Na+ through leaky paracellular pathways between these cells.

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“…cells (Dixon et al, 1986;Gluck et al, 1982;Stetson and Steinmetz, 1983). In this tissue, cells that are homologous to A-IC and B-IC, i.e.…”

Section: Recycling Of the V-atpase In Icmentioning

confidence: 99%

Regulation of the V-ATPase in kidney epithelial cells: dual role in acid–base homeostasis and vesicle trafficking

Brown

Păunescu

Breton

et al. 2009

Journal of Experimental Biology

135

100

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SummaryThe proton-pumping V-ATPase is a complex, multi-subunit enzyme that is highly expressed in the plasma membranes of some epithelial cells in the kidney, including collecting duct intercalated cells. It is also located on the limiting membranes of intracellular organelles in the degradative and secretory pathways of all cells. Different isoforms of some V-ATPase subunits are involved in the targeting of the proton pump to its various intracellular locations, where it functions in transporting protons out of the cell across the plasma membrane or acidifying intracellular compartments. The former process plays a critical role in proton secretion by the kidney and regulates systemic acid-base status whereas the latter process is central to intracellular vesicle trafficking, membrane recycling and the degradative pathway in cells. We will focus our discussion on two cell types in the kidney: (1) intercalated cells, in which proton secretion is controlled by shuttling V-ATPase complexes back and forth between the plasma membrane and highly-specialized intracellular vesicles, and (2) proximal tubule cells, in which the endocytotic pathway that retrieves proteins from the glomerular ultrafiltrate requires V-ATPase-dependent acidification of post-endocytotic vesicles. The regulation of both of these activities depends upon the ability of cells to monitor the pH and/or bicarbonate content of their extracellular environment and intracellular compartments. Recent information about these pH-sensing mechanisms, which include the role of the V-ATPase itself as a pH sensor and the soluble adenylyl cyclase as a bicarbonate sensor, will be addressed in this review.

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Role of membrane fusion in CO2 stimulation of proton secretion by turtle bladder

Cited by 264 publications

References 18 publications

Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules.

Carbon dioxide causes exocytosis of vesicles containing H+ pumps in isolated perfused proximal and collecting tubules.

Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys

Regulation of the V-ATPase in kidney epithelial cells: dual role in acid–base homeostasis and vesicle trafficking

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