Distribution of ions in a fluid-transporting epithelium determined by electron-probe X-ray microanalysis

Gupta, Brij L.; Hall, T. A.; Maddrell, S. H. P.; Moreton, R. B.

doi:10.1038/264284a0

Cited by 102 publications

(31 citation statements)

References 14 publications

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“…(kg dry wt) -1] is higher and the nuclear chloride content is lower than the corresponding values in the cytoplasm (Rick et al, 1978). In addition, the nuclear potassium content seems somewhat higher than the cytoplasmic content, consistent with microprobe observations in this and other tissues (Gupta et al, 1976(Gupta et al, , 1977, Gupta, Hall & Naftalin, 1978b;Rick et al, 1978;Somlyo, Somlyo & Shuman, 1979;Jones et al, 1979). However, taking into account differences in water content between the nucleus and cytoplasm of the granular cells of toad bladder, the calculated potassium concentrations have been reported to be similar in this tissue (Rick et al, 1978).…”

Section: Baseline Measurementssupporting

confidence: 87%

Microprobe study of toad urinary bladder in absence of serosal K+

1980

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The bulk of the intracellular potassium in mucosal epithelial cells from toad urinary bladder has been previously reported to exchange very slowly with the serosal medium, with a half-time of some 9 hr. This observation, based on chemical analyses of mucosal cell scrapings, has been reexamined with stimultaneous diffractive and energy dispersive electron probe X-ray microanalysis. Fifty-three intracellular sites in hydrated sections and 286 sites in dehydrated sections were studied in bladders from eight toads under baseline conditions and after removal of serosal K+ for 83-133 min, with or without 10(-2) M ouabain. The baseline data confirm and extend previous examinations of the intracellular ionic composition, and provide the most direct measure of intracellular water thus far available for this tissue. Removal of serosal K+ reduced the intracellular K+ content by 20%, increased intracellular Na+ content threefold, and slightly reduced the intracellular Cl- and water contents, qualitatively consistent with published chemical analyses. The intracellular Na+ content of mucosal origin, measured by radioactive tracers and chemical analyses of cell scrapings, has been reported to be unchanged under these conditions. Simultaneous addition of ouabain and removal of external K+ produced a dramatic fall in intracellular K+ of more than 80% in a third of the cells and reduced the mean intracellular K+ content by 60%; 20% of the cells appeared to retain K+ more effectively than the bulk of the epithelial cell population. We conclude that: (i) the low rate of net exchange of intracellular K+ with the serosal bulk solution primarily reflects recycling of K+ across the basolateral membranes, (ii) radioactive tracer and chemical measurements of the intracellular Na+ pool of mucosal origin substantially understimate the total intracellular Na+ content under certain experimental conditions, and (iii) the epithelial cells display a functional heterogeneity of response to the effects of adding ouabain and withdrawing external K+.

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Section: Baseline Measurementssupporting

confidence: 87%

Microprobe study of toad urinary bladder in absence of serosal K+

1980

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“…(equivalent to 245 m-mole/l. H20 assuming 80 % H20) obtained for nuclear K in epithelial cells of Rhodnius Malpighian tubules by Gupta, Hall, Maddrell & Moreton (1976). It may also be noted that a K-sensitive glass micro-electrode in most cells detects essentially all the cell K and thus behaves similarly to the electron microprobe (Lev & Armstrong, 1976), although insome frog musclesthere is evidence of a sequestered fraction of K (Lee & Armstrong, 1974).…”

Section: Discussionmentioning

confidence: 97%

The distribution of sodium, potassium and chloride in the nucleus and cytoplasm of Bufo bufo oocytes measured by electron microprobe analysis.

Dick¹

1978

The Journal of Physiology

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“…The steps identified below correspond to the numbered arrows in the Figure. Step 1 -K + diffuses from the stirred blood side solution to the unstirred basal ECS; fixed negative charges in the basement membrane may elevate the K + concentration there, as in Malpighian tubules and salivary glands (Gupta, Hall, Maddrell & Moreton, 1976;.…”

Section: Midgut K Transport Routementioning

confidence: 99%

X-ray microanalysis of elements in frozen-hydrated sections of an electrogenic K+ transport system: The posterior midgut of tobacco hornworm (Manduca sexta) in vivo andin vitro

et al. 1984

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The lepidopteran midgut is a model for the oxygen-dependent, electrogenic K+ transport found in both alimentary and sensory tissues of many economically important insects. Structural and biochemical evidence places the K+ pump on the portasome-studded apical plasma membrane which borders the extracellular goblet cavity. However, electrochemical evidence implies that the goblet cell K+ concentration is less than 50 mM. We used electron probe X-ray microanalysis of frozen-hydrated cryosections to measure the concentration of Na, Mg, P, S, Cl, K, Ca and H2O in several subcellular sites in the larval midgut of Manduca sexta under several experimental regimes. Na is undetectable at any site. K is at least 100 mM in the cytoplasm of all cells. Typical in vivo values (mM) for K were: blood, 25; goblet and columnar cytoplasm, 120; goblet cavity, 190; and gut lumen, 180. The high K concentration in the apically located goblet cavity declined by 100 mM under anoxia. Both cavity and gut fluid are Cl deficient, but fixed negative charges may be present in the cavity. We conclude that the K+ pump is sited on the goblet cell apical membrane and that K+ follows a nonmixing pathway via only part of the goblet cell cytoplasm. The cavity appears to be electrically isolated in alimentary tissues, as it is in sensory sensilla, thereby allowing a PD exceeding 180 mV (lumen positive) to develop across the apical plasma membrane. This PD appears to couple K+ pump energy to nutrient absorption and pH regulation.

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Distribution of ions in a fluid-transporting epithelium determined by electron-probe X-ray microanalysis

Cited by 102 publications

References 14 publications

Microprobe study of toad urinary bladder in absence of serosal K+

Microprobe study of toad urinary bladder in absence of serosal K+

The distribution of sodium, potassium and chloride in the nucleus and cytoplasm of Bufo bufo oocytes measured by electron microprobe analysis.

X-ray microanalysis of elements in frozen-hydrated sections of an electrogenic K+ transport system: The posterior midgut of tobacco hornworm (Manduca sexta) in vivo andin vitro

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