Coupling of Active Ion Transport and Aerobic Respiratory Rate in Isolated Renal Tubules

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1980 Jan 1

PMID 6244559

Citations 25

Authors

R S Balaban

L J Mandel

S P Soltoff

J M Storey

Affiliations

Soon will be listed here.

Abstract

We report the results of studies in which the cytoplasmic coupling between Na+,K+-ATPase activity (presumably a measure of active transport) and the mitochondrial respiratory rate was investigated in a tubule suspension from the rabbit kidney cortex. Simultaneous measurements of the redox state of mitochondrial nicotinamide adenine dinucleotide (NAD) (performed fluorometrically), the cellular ATP and ADP concentrations, and the oxygen consumption rate (QO2) were made under conditions known to alter the Na+,K+-ATPase turnover. Ouabain (25 microM) caused: (i) a 54% inhibition of QO2, (ii) a net reduction of NAD, and (iii) a 30% increase in the ATP/ADP ratio. The addition of K+ (5 ?M) to K+-depleted tubules caused: (i) an initial 127% stimulation of QO2 followed by a new steady-state QO2 50% above control, (ii) an initial large oxidation of NAD followed by a new steady state more oxidized than the control level, and (iii) a 47% decrease in the cellular ATP/ADP ratio. These data indicate that the cellular ATP and ADP concentrations or the ATP/ADP ratio may be part of the coupling mechanism linking Na+,K+-ATPase turnover and the aerobic metabolic rate in kidney.

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References

Blond D, Whittam R . The regulation of kidney respiration by sodium and potassium ions. Biochem J. 1964; 92(1):158-67. PMC: 1215453. DOI: 10.1042/bj0920158. View

ZERAHN K . Oxygen consumption and active sodium transport in the isolated and short-circuited frog skin. Acta Physiol Scand. 1956; 36(4):300-18. DOI: 10.1111/j.1748-1716.1956.tb01327.x. View

Whittembury G . Sodium and water transport in kidney proximal tubular cells. J Gen Physiol. 1968; 51(5):Suppl:303S+. View

JOBSIS F, STAINSBY W . Oxidation of NADH during contractions of circulated mammalian skeletal muscle. Respir Physiol. 1968; 4(3):292-300. DOI: 10.1016/0034-5687(68)90035-2. View

Atkinson D . The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry. 1968; 7(11):4030-4. DOI: 10.1021/bi00851a033. View

Kessler R, Landwehr D, Quintanilla A, Weseley S, Kaufmann W, ARCILA H . Effects of certain inhibitors on renal sodium reabsorption and ATP specific activity. Nephron. 1968; 5(6):474-88. DOI: 10.1159/000179657. View

Handler J, Preston A, ORLOFF J . Effect of ADH, aldosterone, ouabain, and amiloride on toad bladder epithelial cells. Am J Physiol. 1972; 222(5):1071-4. DOI: 10.1152/ajplegacy.1972.222.5.1071. View

Maxild J . Energy requirements for active transport of p-aminohippurate in renal cortical slices. Arch Int Physiol Biochim. 1973; 81(3):501-21. DOI: 10.3109/13813457309073400. View

Rea C, Segal S . ATP content of rat kidney cortex slices: relation to alpha-aminoisobutyric acid uptake. Kidney Int. 1972; 2(2):101-6. DOI: 10.1038/ki.1972.77. View

10.

Nellans H, Finn A . Oxygen consumption and sodium transport in the toad urinary bladder. Am J Physiol. 1974; 227(3):670-5. DOI: 10.1152/ajplegacy.1974.227.3.670. View

11.

Wilson D, Erecinska M, Dutton P . Thermodynamic relationships in mitochondrial oxidative phosphorylation. Annu Rev Biophys Bioeng. 1974; 3(0):203-30. DOI: 10.1146/annurev.bb.03.060174.001223. View

12.

Franke H, BARLOW C, Chance B . Oxygen delivery in perfused rat kidney: NADH fluorescence and renal functional state. Am J Physiol. 1976; 231(4):1082-9. DOI: 10.1152/ajplegacy.1976.231.4.1082. View

13.

KIIL F . Renal energy metabolism and regulation of sodium reabsorption. Kidney Int. 1977; 11(3):153-60. DOI: 10.1038/ki.1977.23. View

14.

Erecinska M, Stubbs M, Miyata Y, Ditre C . Regulation of cellular metabolism by intracellular phosphate. Biochim Biophys Acta. 1977; 462(1):20-35. DOI: 10.1016/0005-2728(77)90186-4. View

15.

Sachs G . Ion pumps in the renal tubule. Am J Physiol. 1977; 233(5):F359-65. DOI: 10.1152/ajprenal.1977.233.5.F359. View

16.

Cala P, Cogswell N, Mandel L . Binding of [3H]ouabain to split frog skin: the role of the Na,K-ATPase in the generation of short circuit current. J Gen Physiol. 1978; 71(4):347-67. PMC: 2215734. DOI: 10.1085/jgp.71.4.347. View

17.

Balaban R, Soltoff S, Storey J, Mandel L . Improved renal cortical tubule suspension: spectrophotometric study of O2 delivery. Am J Physiol. 1980; 238(1):F50-9. DOI: 10.1152/ajprenal.1980.238.1.F50. View

18.

LOWRY O, ROSEBROUGH N, FARR A, RANDALL R . Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. View

19.

Whittam R . Active cation transport as a pace-maker of respiration. Nature. 1961; 191:603-4. DOI: 10.1038/191603a0. View

20.

Chance B, Cohen P, Jobsis F, Schoener B . Intracellular oxidation-reduction states in vivo. Science. 1962; 137(3529):499-508. DOI: 10.1126/science.137.3529.499. View