ATP is a Coupling Modulator of Parallel Na,K-ATPase-K-Channel Activity in the Renal Proximal Tubule
A fundamental and essential property of nearly all salt-transporting epithelia is the tight parallel coupling between the magnitude of the K-conductive pathway at the basolateral membrane and the activity of the Na,K-dependent ATPase (Na,K-ATPase). In the present study, we demonstrate that the coupl...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 89; no. 14; pp. 6418 - 6422 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
Washington, DC
National Academy of Sciences of the United States of America
15.07.1992
National Acad Sciences National Academy of Sciences |
Subjects | |
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Abstract | A fundamental and essential property of nearly all salt-transporting epithelia is the tight parallel coupling between the magnitude of the K-conductive pathway at the basolateral membrane and the activity of the Na,K-dependent ATPase (Na,K-ATPase). In the present study, we demonstrate that the coupling response in the renal proximal tubule is governed, at least in part, through the interaction between ATP-sensitive K channels and Na,K-ATPase-mediated changes in intracellular ATP levels. First, we identified a K-selective channel at the basolateral membrane, which is inhibited by the cytosolic addition of ATP. Second, conventional microelectrode analysis in the isolated perfused proximal straight tubule revealed that these channels are the major determinant of the macroscopic K conductance so that ATP-mediated changes in the open probability of the K channel could alter the extent of K recycling. Indeed, the increase in the macroscopic K conductance upon stimulation of transcellular Na transport and pump activity was found to be paralleled by a decrease in intracellular ATP. Finally, a causal link between parallel Na,K-ATPase-K-channel activity and ATP was established by the finding that intracellular ATP loading uncoupled the response. With our recent observations that similar ATP-sensitive K channels are expressed abundantly in other epithelia, we postulate that ATP may act as a universal coupling modulator of parallel Na,K-ATPase-K-channel activity. |
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AbstractList | A fundamental and essential property of nearly all salt-transporting epithelia is the tight parallel coupling between the magnitude of the K-conductive pathway at the basolateral membrane and the activity of the Na,K-dependent ATPase (Na,K-ATPase). In the present study, we demonstrate that the coupling response in the renal proximal tubule is governed, at least in part, through the interaction between ATP-sensitive K channels and Na,K-ATPase-mediated changes in intracellular ATP levels. First, we identified a K-selective channel at the basolateral membrane, which is inhibited by the cytosolic addition of ATP. Second, conventional microelectrode analysis in the isolated perfused proximal straight tubule revealed that these channels are the major determinant of the macroscopic K conductance so that ATP-mediated changes in the open probability of the K channel could alter the extent of K recycling. Indeed, the increase in the macroscopic K conductance upon stimulation of transcellular Na transport and pump activity was found to be paralleled by a decrease in intracellular ATP. Finally, a causal link between parallel Na,K-ATPase-K-channel activity and ATP was established by the finding that intracellular ATP loading uncoupled the response. With our recent observations that similar ATP-sensitive K channels are expressed abundantly in other epithelia, we postulate that ATP may act as a universal coupling modulator of parallel Na,K-ATPase-K-channel activity. We demonstrate that the coupling response in the renal proximal tubule is governed, at least in part, through the interaction between ATP-sensitive K channels and Na,K-ATPase-mediated changes in intracellular ATP levels. We identified a K-selective channel at the basolateral membrane, which is inhibited by the cytosolic addition of ATP. Conventional microelectrode analysis in the isolated perfused proximal straight tubule revealed that these channels are the major determinant of the macroscopic K conductance so that ATP-mediated changes in the open probability of the K channel could alter the extent of K recycling. Indeed, the increase in the macroscopic K conductance upon stimulation of transcellular Na transport and pump activity was found to be paralleled by a decrease in intracellular ATP. A causal link between parallel Na,K-ATPase-K-channel activity and ATP was established by the finding that intracellular ATP loading uncoupled the response. It is demonstrated that the coupling response in the renal proximal tubule is governed in part through the interaction between ATP-sensitive K channels and Na,K-ATPase-mediated changes in intracellular ATP levels. |
Author | Tsuchiya, K. Wang, W. Giebisch, G. Welling, P. A. |
AuthorAffiliation | Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06510 |
AuthorAffiliation_xml | – name: Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06510 |
Author_xml | – sequence: 1 givenname: K. surname: Tsuchiya fullname: Tsuchiya, K. – sequence: 2 givenname: W. surname: Wang fullname: Wang, W. – sequence: 3 givenname: G. surname: Giebisch fullname: Giebisch, G. – sequence: 4 givenname: P. A. surname: Welling fullname: Welling, P. A. |
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Copyright | Copyright 1992 The National Academy of Sciences of the United States of America 1992 INIST-CNRS Copyright National Academy of Sciences Jul 15, 1992 |
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Keywords | Enzyme Electrophysiology Rabbit Ion transport Ionic channel Lagomorpha Kidney Vertebrata Regulation(control) Mammalia Na,K-ATPase Coupling Intracellular ATP Potassium Proximal tube |
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Snippet | A fundamental and essential property of nearly all salt-transporting epithelia is the tight parallel coupling between the magnitude of the K-conductive pathway... It is demonstrated that the coupling response in the renal proximal tubule is governed in part through the interaction between ATP-sensitive K channels and... We demonstrate that the coupling response in the renal proximal tubule is governed, at least in part, through the interaction between ATP-sensitive K channels... |
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SubjectTerms | Adenosine triphosphatases Adenosine Triphosphate - physiology Animals ATP Biochemistry Biological and medical sciences Cell membranes Cell physiology Fundamental and applied biological sciences. Psychology Glyburide - pharmacology In Vitro Techniques Ion Channel Gating Kidney Tubules, Proximal - physiology Kidneys Membrane and intracellular transports Membrane potential Membrane Potentials - drug effects Modulated signal processing Molecular and cellular biology Na super(+)/K super(T)-transporting ATPase P branes Physiological transport Physiology Potassium - metabolism Potassium Channels - physiology Proximal tubules Pumps Rabbits Recycling role Signal Transduction Sodium - metabolism Sodium-Potassium-Exchanging ATPase - physiology |
Title | ATP is a Coupling Modulator of Parallel Na,K-ATPase-K-Channel Activity in the Renal Proximal Tubule |
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