AJP - Regu Ad Instruments
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Am J Physiol Regul Integr Comp Physiol 276: R616-R621, 1999;
0363-6119/99 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Stoner, L. C.
Right arrow Articles by Viggiano, S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Stoner, L. C.
Right arrow Articles by Viggiano, S. C.
Vol. 276, Issue 2, R616-R621, February 1999

RAPID COMMUNICATION
Elevation of basolateral K+ induces K+ secretion by apical maxi K+ channels in Ambystoma collecting tubule

Larry C. Stoner and Susan C. Viggiano

Department of Neuroscience and Physiology, State University of New York, Health Science Center at Syracuse, Syracuse, New York 13210


    ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References

We previously reported that exposure of aquatic-phase Ambystoma tigrinum to a solution containing 50 mM K+ (K+ adaptation) caused a nearly 10-fold increase in the number of detectable maxi K+ channels on the apical membrane of their initial collecting tubules. In apparent contradiction to the notion that maxi K+ channels contribute to K+ secretion, these channels were not routinely active at the resting membrane potential (0 mV voltage clamp). To test the possibility that hyperkalemia yields maxi K+ channels that are secreting K+ (i.e., active at 0 mV), we patch-clamped the apical membranes of initial collecting tubules under conditions of elevated basolateral K+ (15 mM). Seven patches containing maxi K+ channels were studied. Six of the seven patches showed maxi K+ channel activity when voltage was clamped at 0 mV. Open probability and unitary current averaged 0.059 ± 0.016 and 1.65 ± 0.50 pA, respectively. This activity, together with the high density of channels observed (1.06 channels/µm2), indicates that after K+ adaptation, maxi K+ channels contribute to the ability of the late distal nephron of amphibians to secrete K+.

amphibian collecting tubule; homeostatic K+ secretion; K+ adaptation; hyperkalemic conditions


    INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References

IT HAS BEEN POSTULATED that the mechanism of K+ secretion by collecting tubules of amphibians differs from that of mammals (11, 23), in that it occurs via a passive, paracellular mechanism (11). That the apical membrane of amphibian collecting tubule appears to lack a significant K+ conductance (13) and that K+ secretory channels observed in the apical membrane of the mammalian collecting tubule (7, 33) have not been observed in the amphibian (27, 29) support this hypothesis.

Exposure of neonatal Ambystoma tigrinum to environmental K+ for a week or more causes the upregulation of maxi K+ channels in the apical membrane of their initial collecting tubules (29). The extent of the increase in density of maxi K+ channels is nearly 10-fold (29). Others (24) have shown these animals to dramatically increase their rate of renal K+ excretion in response to K+ adaptation (24). These findings have led us to postulate that the upregulated maxi K+ channels may indeed be involved in homeostatic K+ secretion in our K+-adapted animals (29).

Under conditions in which the saline on the basolateral surface of the tubule contained 4.3 mM K+, these maxi K+ channels were not routinely active (29). This observation is in apparent contradiction to the notion that these channels are involved in net K+ secretion. The present study was undertaken to establish whether or not these maxi K+ channels actively secrete K+ under conditions that mimic the dramatic hyperkalemia present in K+-adapted animals (24).

Using a technique unique to our laboratory, we exposed the apical membranes of collecting tubules by everting and perfusing fragments of the renal tubule in vitro. This everted tubule preparation permits us to independently control the K+ concentration on either side of the epithelium (27-29). Thus we can study the activity of upregulated maxi K+ channels under conditions of hyperkalemia and the effect of changes in the concentration of basolateral K+ on channel activity.


    METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References

Biological preparations. Western neonatal tiger salamanders, A. tigrinum, were obtained from Charles Sullivan (Nashville, TN). Animals were kept in special aquariums (Aquaratron; Westminster Scientific, Westminster, MD) containing 3-5 in. of circulating tap water at 50°F. Salamanders were fed crickets daily. For K+ adaptation, animals were transferred to plastic cages containing 3 in. of 50 mM KCl for 14-30 days before the experiment. The cages were kept in the 50°F aquariums.

Ambystoma were doubly pithed immediately before removal of the kidneys. Slices of kidney several millimeters thick were cut and immediately placed in room-temperature saline for the dissection of initial collecting tubules. The methods for dissecting and perfusing renal tubule fragments have been published previously (2, 5, 25, 27, 28). The dissection saline contained, in mM, 105 NaCl, 13.7 KCl, 2.0 CaCl2, 1.3 MgSO4, 1.3 KH2PO4, 5.0 HEPES, and 5.5 dextrose and 1 g/100 ml BSA. The pH was titrated to 7.6. This solution, minus the albumin, was used to bathe the basolateral surface of everted tubules. The apical bath and the patch pipette were filled with a similar saline, in which sodium was used to replace some of the K+ so that the final concentration of K+ was 4.3 mM. In some cases, the 15 mM K+ saline that bathed the basolateral surface was exchanged for 4.3 mM K+ saline.

Patch-clamp methods. The general features of everting amphibian renal tubule fragments have been described in previous publications (5, 27-29). A brief description of the technique is presented here. Dissected tubules were transferred to a setup used to perfuse kidney tubule fragments in vitro (2).

Pipettes used to perfuse and evert Ambystoma collecting tubules were modified from those normally used to perfuse renal tubule fragments (5, 27, 29). The inner perfusion pipette was pulled with a very long (3.0-4.0 mm) narrow parallel section. The outer diameter of this pipette averaged 10-15 µm. To prevent the basement membrane from sticking to the inner pipette, we pretreated it with the albumin-containing dissection solution for twenty or more minutes before mounting the tubule on the pipettes. The outer holding pipette was fabricated with an inner diameter of 85-100 µm to allow ample space for eversion of the tubule.

Eversion of initial collecting tubules was initiated by first retracting the inner perfusion pipet to a point where a small patch of the basement membrane could be snagged and tucked into the lumen of the tubule. After recentering the inner pipet, we could evert the fragment by slowly advancing the inner pipet while applying gentle suction to the outer pipette, everting the tubule onto the inner perfusion pipette (5). A suction pipette mounted to the collection-end V track of the perfusion apparatus was used to gently pull the tubule off the inner perfusion pipette. About 200 µm of the inner pipette remained in the lumen of the everted tubule, through which salines could be perfused over the basolateral surface (27, 28).

Methods for fabricating patch-clamp pipettes and making seals were modified from those of Hamill et al. (10). Pipettes were pulled from 100-µl Microcaps (Drummond Scientific, Broomall, PA) on a Brown-Flaming P-80/PC puller (Sutter Instrument, San Rafael, CA) immediately before use. The tips of pipettes were fire polished on a Narishige microforge (Narishige, Tokyo, Japan) (27, 28). After fire polishing, the planar surface area of the patch was estimated to be 1.4 µm2 (30).

The preparation was viewed via a high-resolution video monitor (Javelin Electronics, Torrance, CA). The perfused tubule was lowered to touch the surface of the coverslip, which was pretreated with CellTac (Collaborative Research, Boston, MA). To form a seal, we typically positioned the pipette directly above the center of the everted tubule with a Narishige hydraulic micromanipulator. Patch pipettes were routinely positioned above areas of the everted collecting tubule that appeared to have a smooth, flat surface. Cells that appeared to bulge out from the surface were avoided. Patch resistances in this study were routinely between 20 and 30 GOmega .

The current signal was monitored via an Axopatch 1-B amplifier (Axon Instruments, Burlingame, CA) equipped with a TMA-1 interface. A permanent record of experimental data was digitized (model VR-10; Instrutech, Mineola, NY) and recorded on videotape for offline analysis. The signal was filtered to tape at 10 kHz. For analysis of channel records, data were fed into the computer at a sampling rate of 50-100 µs/point and filtered at 2,000 Hz. P-CLAMP software (Axon Instruments) was used to analyze the data on a Dell Optiplex PC (Dell Computer).

The slope conductance of channels was determined from the slope of the I-V relationship. We routinely applied voltage ramps between a pipette-positive 120 mV and pipette-negative 120 mV. The signal of an active patch was monitored for 10-60 s at each voltage. When more than one channel was evident in the patch, the open probability was computed as the fraction of time the individual channels were in the open state divided by the maximal number of levels observed. Mean open times were computed from the time a single channel spends in the level 1 state.

All data presented are from cell-attached patches. Unless stated otherwise, results are presented as means ± SE (number of data points). The t-test for the significance between two independent means was used to evaluate the difference between means. P values <0.05 were considered significant.


    RESULTS
Top
Abstract
Introduction
Methods
Results
Discussion
References

Figure 1 illustrates the difference between the secretory and nonsecretory states of maxi K+ channels. The secreting maxi K+ channel illustrated in Fig. 1A shows maxi K+ activity at a variety of pipette voltages from +20 to -100 mV. At a voltage clamp of 0 mV, the cell is at its resting membrane potential. The basolateral saline of the collecting tubule on which this channel was studied contained 15 mM K+. The presence of activity at 0 mV indicates K+ secretion into the pipette (urinary compartment). The pipette reversal potential of the maxi K+ channel in this patch was +28.5 mV. Figure 1B shows a series of traces from a patch containing a maxi K+ channel in the nonsecretory state. Its basolateral surface is exposed to saline containing 4.3 mM K+. Figure 1C presents the current-voltage relationships of the channels shown in Fig. 1, A and B. The secreting channel expresses activity at the resting membrane potential (0 mV voltage clamp), and the other does not.


View larger version (22K):
[in this window]
[in a new window]
  		Fig. 1.   Characteristics of secretory and nonsecretory apical maxi K+ channels. A: a series of traces illustrating activity of a secretory channel at a number of different pipette voltages. Basolateral surface of cell was exposed to 15 mM K+. B: a series of traces from a nonsecretory channel illustrating lack of 0 mV activity. Basolateral surface was exposed to 4.3 mM K+. Bar indicates a current amplitude of 20 pA, and length of each trace is 1 s. C: current-voltage relationships for patches in A (bullet ) and B ().

Fifteen millimolar K+ saline was used to mimic a hyperkalemic condition on the basolateral surface of the collecting tubule. We measured the plasma K+ contents of 14 animals exposed to 50 mM K+ from 1 to 14 days. The concentration of K+ averaged 8.4 ± 0.6 mM, with values ranging from 5.1 to 12.4 mM. Stiffler et al. (24) obtained similar values of 8.9 ± 0.6 mM of the plasma K+ of K+-adapted Ambystoma. Thus 15 mM K+ seemed a reasonable upper limit of the hyperkalemia experienced by our amphibians during K+ adaptation.

A series of seven patches containing maxi K+ channels on tubules whose basolateral surface was exposed to saline containing 15 mM K+ was studied. Six of the seven maxi K+ channels were in a secretory state. The characteristics of these six channels are presented in Table 1. Their conductance, pipette reversal potential, unitary current, and mean open time are similar to those usually reported for epithelial maxi K+ channels in mammalian collecting tubule (6, 9, 12, 14, 18, 19, 28).

                              
View this table:
[in this window]
[in a new window]
  		Table 1.   Summary of properties of maxi K+ channels secreting potassium

In five of the patches containing secreting maxi K+ channels, we subjected the basolateral surface to a change in K+ concentration from 15 to 4.3 mM while monitoring the activity of the maxi K+ channels for a period of 15 min. The channels were clamped at a pipette voltage of -100 mV to facilitate monitoring of any changes in channel activity. Figure 2, A and B, illustrates the time course of the decrease in relative open probability and unitary current, respectively. The half-time of the decrease in open probability is 4 min, with the maximal effect being attained at nearly 10 min (Fig. 2A). The time course for the decrease in unitary current was similar.


View larger version (12K):
[in this window]
[in a new window]
  		Fig. 2.   Time course of inactivation of channel activity after basolateral K+ is reduced to 4.3 mM. A: relative decrease in open probability. B: reduction in unitary current. Both parameters were measured with pipette voltage clamped to -100 mV.

The effect of 15 min of exposure to 4.3 mM K+ on the channel characteristics is shown in Table 2. Channel activity, as indicated by the decrease in open probability, diminished dramatically over the 15-min period. The pipette reversal potential shifted in the negative direction by 16 mV to a value near zero. This difference in reversal potentials is also illustrated in the representative channel data in Fig. 1C. In addition, the unitary current decreased by nearly 30%, a change consistent with hyperpolarization of the cell caused by reduction of the basolateral K+ contents. That this decrease requires 12 min to be maximal suggests that we cannot exclude the possibility that the decrease in unitary current could, at least in part, be due to changes in cytosolic K+.

                              
View this table:
[in this window]
[in a new window]
  		Table 2.   Effect of changing basolateral K+ concentration from 15 to 4.3 mM

To assure ourselves that the inactivation seen in Fig. 2 was not the result of channel rundown over time, in two patches we studied the reversibility of the effect of changing the basolateral K+ concentration. One patch was first studied in 4.3 mM K+ then switched to 15 mM K+, and the other was first studied in 15 mM K+. The open probability and unitary current were determined in each instance after the tubule was exposed to a given K+ concentration for at least 15 min. In each case, a decrease in both the current amplitude and the open probability were evident when the solution was changed from 15 to 4.3 mM K+. To illustrate the effect of hyperkalemia on the secretion of K+, we calculated the net K+ flux as the product of the amplitude of the unitary current and the open probability divided by the Faraday constant. The reversibility of the effect of changes in the concentration is illustrated in Fig. 3, in which the relative transport current is assigned a value of 1.0 in the first period during which the basolateral K+ is 4.3 mM K+. The rates of K+ flux observed during the first period in which the basolateral K+ was 4.3 mM were calculated to be 0.033 and 0.011 × 10-5 pmol/s. In each case, the effect of change in flux due to the basolateral K+ concentration was reversed when we returned to the original solution.


View larger version (16K):
[in this window]
[in a new window]
  		Fig. 3.   Reversibility of changing concentration of K+ on basolateral surface on K+ flux through apical maxi K+ channel. Relative K+ flux represents product of amplitude of unitary current and open probability divided by Faraday constant and normalized to value during first period of 4.3 mM K+. One patch was first studied in 4.3 mM K+ (bullet ) then switched to 15 mM K+, and the other was first studied in 15 mM K+ ().


    DISCUSSION
Top
Abstract
Introduction
Methods
Results
Discussion
References

In mammals (6, 12, 14, 20, 28) and in amphibians maintained in tap water (29), the density of apical maxi K+ channels of the collecting tubule is low, at 0.08 channel/µm2 of apical membrane (29). They are found in only 3-5% of the successful patches (28, 29). In contrast, the density of maxi K+ channels in the apical membrane of amphibian collecting tubules dissected from K+-adapted animals is high, at nearly 1.0 channel/µm2 (29). This elevated channel density is also reflected in the fact that 65% of our successful patches in this study expressed maxi K+ channels (Table 1). We postulate that this upregulation of maxi K+ channels explains, at least in part, the dramatic increase in K+ secretion observed after K+ adaptation (24).

We are not the first to observe upregulation of K+ channels in the amphibian distal nephron. Wang et al. (32) have reported that in frogs, aldosterone causes the insertion of intermediate conductance K+ channels into the apical membrane of the early distal nephron. Thus both the early distal tubule and the collecting tubule of the amphibian nephron may contribute to homeostatic K+ secretion. Because K+-adapted Ambystoma express elevated levels of plasma aldosterone (24), it is possible that aldosterone may mediate the upregulation of different classes of K+ channels in both the early and late distal nephron of amphibians.

In the mammal, the apical maxi K+ channels of the collecting tubule do not appear to upregulate in response to K+ loading. It is of interest that upregulation of maxi K+ channels has been reported for the rat distal colon in response to dietary K+ adaptation (3). Only one group (G. Frindt and L. G. Palmer, personal communication) has looked for an effect of dietary K+ adaptation on the density of maxi K+ channels in the apical membrane of the rat collecting tubule. They could find no such correlation. In addition, Hirsch et al. (12) report that treatment of rats with the mineralocorticoid DOCA does not alter the density of maxi K+ channels in rat cortical collecting tubule. One might expect that if the upregulation of maxi K+ channels is mediated by the increase in plasma aldosterone associated with K+ adaptation (24), then DOCA would also increase the frequency of observed maxi K+ channels.

This is the first study to report significant open probability of maxi K+ channels in K+-secreting collecting tubule cells (Table 1). This occurred only when the basolateral surface of the cells was exposed to a solution high in K+ (Table 2). The activity of these channels under conditions that mimic hyperkalemia together with the high density of maxi K+ channels observed argues that maxi K+ channels make a significant contribution to the dramatically increased capacity of Ambystoma kidneys to secrete K+ after K+ adaptation (24).

Numerous investigators have attempted to argue that the renal apical maxi K+ channel of mammals may play a role in homeostatic K+ secretion (1, 9, 14, 15, 19, 22). In most studies, this channel appears to be quiescent at the resting membrane potential and activated when clamped at depolarizing voltages or when elevation of cytoplasmic calcium occurs (6, 20). The failure to observe activity at the resting membrane voltage together with activation of the channels under conditions of hyposmotic stress or membrane stretch (20, 28, 30, 31) has suggested to some that the maxi K+ channel may be involved in cell volume regulation and not net K+ secretion. This physiological role has been proposed for the apical maxi K+ channels of rat thick ascending limb (29), rat cortical collecting tubule (12, 28), and cultured collecting tubule cells (17, 18).

Decreasing the K+ contents of the saline bathing the basolateral surface of the initial collecting tubule results in the inactivation of the apical maxi K+ channels (Fig. 2). Table 1 shows a decrease in open probability of >90%. This observation implies that the plasma K+ concentration in some way influences the gating of the channels. This process of inactivation appears to reverse when the tubule is returned to a solution containing high K+ (Fig. 3).

Curiously, neither the conductance nor the mean open time were changed when the 15 mM K+ basolateral saline was exchanged for one in which the K+ was 4.3 mM (Table 2). The lack of change in conductance was taken to indicate that the level of cellular K+ was similar in both cases. This may indicate that the regulatory mechanisms for maintaining cell K+ levels are different from those that set the level of homeostatic K+ secretion. The lack of change in mean open time was taken to indicate that whatever the mechanism of inactivation was, it did not change the closing rate constant of the channel (21), inferring that the increase in open probability is due solely to a change in the opening rate constant.

A change in one or more of several parameters known to alter gating by the maxi K+ channel could explain the observed inactivation. Parameters known to influence gating in these channels include an increase in the cytosolic calcium concentration (1, 6, 12, 14), phosphorylation of the channel molecule (19, 22), and membrane hyperpolarization (6, 14, 20). Future studies will undoubtedly be required to resolve the question as to what parameter is involved in the observed inactivation.

Perspectives

The amphibian distal nephron shares many histological and functional characteristics with mammals (11, 23, 26, 27, 29). In contrast to mammals (7, 33), amphibians appear to lack low-conductance K+ channels in the apical membrane of the collecting tubule (11, 27, 29). It is believed that K+ secretion in the collecting tubules of the amphibian occurs via a passive, paracellular mechanism (13), a postulate consistent with the relatively low rates of K+ secretion seen in the amphibian collecting tubule (13, 25).

We have reported a 10-fold increase in maxi K+ channel density in the amphibian collecting tubule as a regulatory response to long-term exposure of Ambystoma to elevated environmental K+ (29). At least under hyperkalemic conditions, these channels are active, secreting K+ into the urinary compartment. Upregulation of apical maxi K+ channels in response to K+ adaption for use in renal K+ secretion may be unique to amphibians. Thus amphibians appear to depend on the activity of maxi K+ channels to increase the rate of K+ secretion.

In mammalian collecting tubule, the maxi K+ channels appear to be used in cell volume regulation (12, 17, 28, 30). Whether or not amphibians also use maxi K+ channels for this purpose is not currently known. It is possible that more than one variant of the maxi K+ channel may exist in amphibian collecting tubule. One variation of the channel may be involved in homeostatic K+ secretion, and another may play a role in cell volume regulation. If so, the gating characteristics of the two types of channels may differ.


    ACKNOWLEDGEMENTS

The authors express their appreciation to Brian Bush for expert technical support. We are grateful to Dr. Peter Holohan for reading the manuscript and for many helpful suggestions during the course of this study.


    FOOTNOTES

This project was supported by a grant from the National Science Foundation, sponsor ID no. IBN-9506128.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Address for reprint requests: L. C. Stoner, Dept. of Neuroscience and Physiology, State Univ. of New York, Health Science Center, 766 Irving Ave., Syracuse, NY 13210.

Received 3 June 1998; accepted in final form 24 November 1998.


    REFERENCES
Top
Abstract
Introduction
Methods
Results
Discussion
References

1.   Bolivar, J. J., and M. Cereijido. Voltage and Ca2+-activated channels in cultured epithelial cells (MDCK). J. Membr. Biol. 97: 43-51, 1987[Medline].

2.   Burg, M. B. Perfusion of isolated renal tubules. Yale J. Biol. Med. 45: 321-326, 1972[Medline].

3.   Butterfield, I., G. Warhurst, M. N. Jones, and G. I. Sandle. Characterization of apical potassium channels induced in rat distal colon during potassium adaptation. J. Physiol. (Lond.) 501: 537-547, 1997[Abstract/Free Full Text].

4.   Dube, L., L. Parent, and R. Sauve. Hypotonic shock activates a maxi K+ channel in primary cultured proximal tubule cells. Am. J. Physiol. 259 (Renal Fluid Electrolyte Physiol. 28): F348-F356, 1990[Abstract/Free Full Text].

5.   Engbretson, B. G., and L. C. Stoner. The everted renal tubule: a methodology for direct assessment of apical membrane function. Am. J. Physiol. 255 (Renal Fluid Electrolyte Physiol. 24): F1276-F1280, 1988[Abstract/Free Full Text].

6.   Frindt, G., and L. G. Palmer. Ca-activated K channels in apical membrane of mammalian CCT, and their role in K secretion. Am. J. Physiol. 252 (Renal Fluid Electrolyte Physiol. 21): F458-F467, 1987[Abstract/Free Full Text].

7.   Frindt, G., and L. G. Palmer. Low-conductance K channels in the apical membrane of rat cortical collecting tubule. Am. J. Physiol. 256 (Renal Fluid Electrolyte Physiol. 25): F143-F151, 1989[Abstract/Free Full Text].

8.   Frindt, G., H. Sackin, and L. G. Palmer. Whole-cell currents in rat cortical collecting tubule: low-Na diet increases amiloride-sensitive conductance. Am. J. Physiol. 258 (Renal Fluid Electrolyte Physiol. 27): F562-F567, 1990[Abstract/Free Full Text].

9.   Gitter, A. H., K. W. Beyenbach, C. W. Christine, P. Gross, W. W. Minuth, and E. Fromter. High-conductance K+ channel in apical membranes of principal cells cultured from rabbit renal cortical collecting tubule anlagen. Pflügers Arch. 408: 282-290, 1987[Medline].

10.   Hamill, O. P., M. E. Neher, B. Sakman, and F. J. Sigworth. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391: 85-100, 1981[Medline].

11.   Hinton, D. E., L. C. Stoner, M. B. Burg, and B. F. Trump. Structural heterogeneity in the distal nephron of the salamander (Ambystoma tigrinum): an electron microscopic study of isolated tubule segments. Anat. Rec. 204: 21-32, 1982[Medline].

12.   Hirsch, J., J. Leipziger, U. Frobe, and E. Schlatter. Regulation and possible physiological role of the Ca(2+)-dependent K+ channel of cortical collecting ducts of the rat. Pflügers Arch. 422: 492-498, 1993[Medline].

13.   Horisberger, J., M. Hunter, B. Stanton, and G. Giebisch. The collecting tubule of Amphiuma. II: Effects of potassium adaptation. Am. J. Physiol. 253 (Renal Fluid Electrolyte Physiol. 22): F1273-F1282, 1987[Abstract/Free Full Text].

14.   Hunter, M., A. G. Lopes, E. Boulpaep, and G. Giebisch. Regulation of single potassium ion channels from apical membrane of rabbit collecting tubule. Am. J. Physiol. 251 (Renal Fluid Electrolyte Physiol. 20): F725-F733, 1986[Abstract/Free Full Text].

15.   Kolb, H. A., M. Paulmichl, and F. Lang. Epinephrine activates outward rectifying K channel in Madin-Darby canine kidney cells. Pflügers Arch. 408: 584-591, 1987[Medline].

16.   Latorre, R, and C. Miller. Conduction and selectivity in potassium channels. J. Membr. Biol. 71: 11-30, 1983[Medline].

17.   Ling, B. N., C. F. Hinton, and D. C. Eaton. Potassium permeable channels in primary cultures of rabbit cortical collecting tubule. Kidney Int. 40: 441-452, 1991[Medline].

18.   Ling, B. N., C. L. Webster, and D. C. Eaton. Eicosanoids modulate Ca2+-dependent K+ channels in cultured rabbit principal cells. Am. J. Physiol. 263 (Renal Fluid Electrolyte Physiol. 32): F116-F126, 1992[Abstract/Free Full Text].

19.   Marty, A. The physiological role of calcium-dependent channels. Trends Neurosci. 12: 420-424, 1989[Medline].

20.   Pacha, J., G. Frindt, and L. G. Palmer. Apical maxi K channels in intercalated cells of CCT. Am. J. Physiol. 261 (Renal Fluid Electrolyte Physiol. 30): F696-F705, 1991[Abstract/Free Full Text].

21.   Palmer, L. G., and G. Frindt. Amiloride-sensitive Na channels from the apical membrane of the rat cortical collecting tubule. Proc. Natl. Acad. Sci. USA 83: 2767-2770, 1986[Abstract/Free Full Text].

22.   Petersen, O. H., and Y. Maruyama. Calcium-activated potassium channels and their role in secretion. Nature 307: 693-696, 1984[Medline].

23.   Stanton, B. A., D. Biemisderfer, J. B. Wade, and G. Giebisch. Structural and functional study of the rat distal nephron: effects of potassium adaptation and depletion. Kidney Int. 19: 36-48, 1981[Medline].

24.   Stiffler, D. F., M. L. De Ruyter, P. B. Hanson, and M. Marshal. Interrenal function in larval Ambystoma tigrinum. Gen. Comp. Endocrinol. 62: 290-297, 1986[Medline].

25.   Stoner, L. C. Isolated perfused amphibian renal tubules: the diluting segment. Am. J. Physiol. 233 (Renal Fluid Electrolyte Physiol. 2): F438-F444, 1977[Free Full Text].

26.   Stoner, L. C. The movement of solutes and water across the vertebrate distal nephron. Renal Physiol. 8: 237-248, 1985[Medline].

27.   Stoner, L. C., B. G. Engbretson, S. C. Viggiano, D. J. Benos, and P. R. Smith. Amiloride-sensitive apical membrane sodium channels of everted Ambystoma collecting tubule. J. Membr. Biol. 144: 147-156, 1995[Medline].

28.   Stoner, L. C., and G. Morley. Effect of basolateral or apical hyposmolarity on apical maxi K channels of everted rat collecting tubule. Am. J. Physiol. 268 (Renal Fluid Electrolyte Physiol. 37): F569-F580, 1995[Abstract/Free Full Text].

29.   Stoner, L. C., and S. C. Viggiano. Environmental KCl causes an upregulation of apical membrane maxi K and ENaC channels in everted Ambystoma collecting tubule. J. Membr. Biol. 162: 107-116, 1998[Medline].

30.   Taniguchi, J., and W. B. Guggino. Membrane stretch: a physiological stimulator of Ca2+-activated K+ channels in thick ascending limb. Am. J. Physiol. 257 (Renal Fluid Electrolyte Physiol. 26): F347-F352, 1989[Abstract/Free Full Text].

31.   Ubl, J., H. Murer, and H. A. Kolb. Ion channels activated by osmotic and mechanical stress in membranes of opossum kidney cells. J. Membr. Biol. 104: 223-232, 1988[Medline].

32.   Wang, W., R. M. Henderson, J. Geibel, S. White, and G. Giebisch. Mechanism of aldosterone-induced increase of K conductance in early distal renal tubule cells of the frog. J. Membr. Biol. 111: 277-289, 1989[Medline].

33.   Wang, W., A. Schwab, and G. Giebisch. Regulation of small-conductance K+ channel in apical membrane of rat cortical collecting tubule. Am. J. Physiol. 259 (Renal Fluid Electrolyte Physiol. 28): F494-F502, 1990[Abstract/Free Full Text].

34.   Wiederholt, M., W. J. Sullivan, and G. Giebisch. Potassium and sodium transport across single distal tubules of Amphiuma. J. Gen. Physiol. 57: 495-525, 1971[Abstract/Free Full Text].

Am J Physiol Regul Integr Compar Physiol 276(2):R616-R621
0002-9513/99 $5.00 Copyright © 1999 the American Physiological Society


This article has been cited by other articles:


Home page
 Am. J. Physiol. Renal Physiol.Home page
L. M. Satlin, M. D. Carattino, W. Liu, and T. R. Kleyman
Regulation of cation transport in the distal nephron by mechanical forces
Am J Physiol Renal Physiol, November 1, 2006; 291(5): F923 - F931.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Renal Physiol.Home page
J. L. Pluznick and S. C. Sansom
BK channels in the kidney: role in K+ secretion and localization of molecular components
Am J Physiol Renal Physiol, September 1, 2006; 291(3): F517 - F529.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Physiol. Renal Physiol.Home page
F. Najjar, H. Zhou, T. Morimoto, J. B. Bruns, H.-S. Li, W. Liu, T. R. Kleyman, and L. M. Satlin
Dietary K+ regulates apical membrane expression of maxi-K channels in rabbit cortical collecting duct
Am J Physiol Renal Physiol, October 1, 2005; 289(4): F922 - F932.
[Abstract] [Full Text] [PDF]

Home page
 Physiol. Rev.Home page
S. C. Hebert, G. Desir, G. Giebisch, and W. Wang
Molecular Diversity and Regulation of Renal Potassium Channels
Physiol Rev, January 1, 2005; 85(1): 319 - 371.
[Abstract] [Full Text] [PDF]

Home page
 J. Exp. Biol.Home page
N. Mobjerg, E. H. Larsen, and I. Novak
K+ transport in the mesonephric collecting duct system of the toad Bufo bufo: microelectrode recordings from isolated and perfused tubules
J. Exp. Biol., April 1, 2002; 205(7): 897 - 904.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Stoner, L. C.
Right arrow Articles by Viggiano, S. C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Stoner, L. C.
Right arrow Articles by Viggiano, S. C.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online