Journal of the American Society of Nephrology, Vol 6, 89-94, Copyright © 1995 by American Society of Nephrology

REGULAR ARTICLES

Nitric oxide inhibits sodium reabsorption in the isolated perfused cortical collecting duct

BA Stoos, NH Garcia and JL Garvin
Department of Medicine, Henry Ford Hospital, Detroit, MI 48202, USA.

Indirect evidence suggests that nitric oxide inhibits sodium reabsorption by the collecting duct; however, direct evidence is lacking. It was hypothesized that endothelium-derived nitric oxide inhibits sodium flux in the cortical collecting duct by blocking amiloride-sensitive sodium channels. Tubules were obtained from Sprague- Dawley rats pretreated with deoxycorticosterone acetate (5 mg/rat i.m.) 5 to 9 days before the experiment. Nitric oxide was added to the system by either the addition of endothelial cells and the induction of the release of nitric oxide via acetylcholine (10(-7) M) or by the addition of nitric oxide donors. Acetylcholine-induced nitric oxide release from endothelial cells decreased lumen-to-bath sodium flux by 24 +/- 7% (N = 3; P < 0.05). The addition of the nitric oxide donor, spermine NONOate (10(-5) M), decreased net sodium flux 68% from 10.1 +/- 2.0 to 3.6 +/- 2 pmol/mm.min (N = 5; P < 0.025). To assure that the inhibition of sodium flux was due to nitric oxide, another donor, nitroglycerin (2 x 10(-5) M), was used, which decreased sodium flux by 43%. Luminal amiloride (10 microM) decreased net sodium flux by 83% (from 14.8 +/- 1.2 to 2.4 +/- 0.7 pmol/mm.min; N = 5; P < 0.025). The addition of nitric oxide via spermine NONOate to tubules decreased intracellular sodium levels by 26% (N = 6; P < 0.005). The Na(+)-K+ATPase activity of spermine NONOate-treated tubules was 14.7 +/- 3.2 pmol/mm.min compared with the control value of 10.2 +/- 2.0 pmol/mm.min. Nitroglycerin did not significantly affect pump activity either.(ABSTRACT TRUNCATED AT 250 WORDS)

This article has been cited by other articles:

				M. P. Schneider, Y. Ge, D. M. Pollock, J. S. Pollock, and D. E. Kohan Collecting Duct-Derived Endothelin Regulates Arterial Pressure and Na Excretion via Nitric Oxide Hypertension, June 1, 2008; 51(6): 1605 - 1610. [Abstract] [Full Text] [PDF]

				S. Tiwari, N. Sharma, P. S. Gill, P. Igarashi, C. R. Kahn, J. B. Wade, and C. M. A. Ecelbarger Impaired sodium excretion and increased blood pressure in mice with targeted deletion of renal epithelial insulin receptor PNAS, April 29, 2008; 105(17): 6469 - 6474. [Abstract] [Full Text] [PDF]

				F. Palm, M. L. Onozato, Z. Luo, and C. S. Wilcox Dimethylarginine dimethylaminohydrolase (DDAH): expression, regulation, and function in the cardiovascular and renal systems Am J Physiol Heart Circ Physiol, December 1, 2007; 293(6): H3227 - H3245. [Abstract] [Full Text] [PDF]

				W. Song and S. Matalon Modulation of alveolar fluid clearance by reactive oxygen-nitrogen intermediates Am J Physiol Lung Cell Mol Physiol, October 1, 2007; 293(4): L855 - L858. [Full Text] [PDF]

				T. Slowinski, P. Kalk, M. Christian, F. Schmager, K. Relle, M. Godes, H. Funke-Kaiser, H.-H. Neumayer, C. Bauer, F. Theuring, et al. Cell-type specific interaction of endothelin and the nitric oxide system: pattern of prepro-ET-1 expression in kidneys of L-NAME treated prepro-ET-1 promoter-lacZ-transgenic mice J. Physiol., June 15, 2007; 581(3): 1173 - 1181. [Abstract] [Full Text] [PDF]

				K. Sobczak, A. Willing, K. Kusche, N. Bangel, and W.-M. Weber Amiloride-sensitive sodium absorption is different in vertebrates and invertebrates Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2007; 292(6): R2318 - R2327. [Abstract] [Full Text] [PDF]

				M. N. Helms, L. Yu, B. Malik, D. J. Kleinhenz, C. M. Hart, and D. C. Eaton Role of SGK1 in nitric oxide inhibition of ENaC in Na+-transporting epithelia Am J Physiol Cell Physiol, September 1, 2005; 289(3): C717 - C726. [Abstract] [Full Text] [PDF]

				I. Rodriguez-Gomez, R. Wangensteen, J. M. Moreno, V. Chamorro, A. Osuna, and F. Vargas Effects of chronic inhibition of inducible nitric oxide synthase in hyperthyroid rats Am J Physiol Endocrinol Metab, June 1, 2005; 288(6): E1252 - E1257. [Abstract] [Full Text] [PDF]

				R. Juncos and J. L. Garvin Superoxide enhances Na-K-2Cl cotransporter activity in the thick ascending limb Am J Physiol Renal Physiol, May 1, 2005; 288(5): F982 - F987. [Abstract] [Full Text] [PDF]

				M. W. McBride, M. J. Brosnan, J. Mathers, L. I. McLellan, W. H. Miller, D. Graham, N. Hanlon, C. A. Hamilton, J. M. Polke, W. K. Lee, et al. Reduction of Gstm1 Expression in the Stroke-Prone Spontaneously Hypertension Rat Contributes to Increased Oxidative Stress Hypertension, April 1, 2005; 45(4): 786 - 792. [Abstract] [Full Text] [PDF]

				M. Herrera and J. L. Garvin A high-salt diet stimulates thick ascending limb eNOS expression by raising medullary osmolality and increasing release of endothelin-1 Am J Physiol Renal Physiol, January 1, 2005; 288(1): F58 - F64. [Abstract] [Full Text] [PDF]

				J. Zimpelmann, N. Li, and K. D. Burns Nitric oxide inhibits superoxide-stimulated urea permeability in the rat inner medullary collecting duct Am J Physiol Renal Physiol, December 1, 2003; 285(6): F1160 - F1167. [Abstract] [Full Text]

				S. Turban, X.-Y. Wang, and M. A. Knepper Regulation of NHE3, NKCC2, and NCC abundance in kidney during aldosterone escape phenomenon: role of NO Am J Physiol Renal Physiol, November 1, 2003; 285(5): F843 - F851. [Abstract] [Full Text] [PDF]

				S. Fujii, L. Zhang, J. Igarashi, and H. Kosaka L-Arginine Reverses p47phox and gp91phox Expression Induced by High Salt in Dahl Rats Hypertension, November 1, 2003; 42(5): 1014 - 1020. [Abstract] [Full Text] [PDF]

				H. He, T. Podymow, J. Zimpelmann, and K. D. Burns NO inhibits Na+-K+-2Cl- cotransport via a cytochrome P-450-dependent pathway in renal epithelial cells (MMDD1) Am J Physiol Renal Physiol, June 1, 2003; 284(6): F1235 - F1244. [Abstract] [Full Text] [PDF]

				P. Ortiz, B. A. Stoos, N. J. Hong, D. M. Boesch, C. F. Plato, and J. L. Garvin High-Salt Diet Increases Sensitivity to NO and eNOS Expression But Not NO Production in THALs Hypertension, March 1, 2003; 41(3): 682 - 687. [Abstract] [Full Text] [PDF]

				T. L. Pallone, Z. Zhang, and K. Rhinehart Physiology of the renal medullary microcirculation Am J Physiol Renal Physiol, February 1, 2003; 284(2): F253 - F266. [Abstract] [Full Text] [PDF]

				N. Tian, A. W. Gannon, R. A. Khalil, and R. D. Manning Jr. Mechanisms of salt-sensitive hypertension: role of renal medullary inducible nitric oxide synthase Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2003; 284(2): R372 - R379. [Abstract] [Full Text] [PDF]

				P. A. Ortiz and J. L. Garvin Role of nitric oxide in the regulation of nephron transport Am J Physiol Renal Physiol, May 1, 2002; 282(5): F777 - F784. [Abstract] [Full Text] [PDF]

				T. Chabrashvili, A. Tojo, M. L. Onozato, C. Kitiyakara, M. T. Quinn, T. Fujita, W. J. Welch, and C. S. Wilcox Expression and Cellular Localization of Classic NADPH Oxidase Subunits in the Spontaneously Hypertensive Rat Kidney Hypertension, February 1, 2002; 39(2): 269 - 274. [Abstract] [Full Text] [PDF]

				I. Pagel, T. Langenickel, K. Hohnel, S. Philipp, A. K. Nussler, W. F. Blum, M. L. Aubert, R. Dietz, and R. Willenbrock Cardiac and Renal Effects of Growth Hormone in Volume Overload-Induced Heart Failure: Role of NO Hypertension, January 1, 2002; 39(1): 57 - 62. [Abstract] [Full Text] [PDF]

				P. A. Ortiz, N. J. Hong, and J. L. Garvin NO decreases thick ascending limb chloride absorption by reducing Na+-K+-2Cl- cotransporter activity Am J Physiol Renal Physiol, November 1, 2001; 281(5): F819 - F825. [Abstract] [Full Text] [PDF]

				M. Liang, T. J. Berndt, and F. G. Knox Mechanism underlying diuretic effect of L-NAME at a subpressor dose Am J Physiol Renal Physiol, September 1, 2001; 281(3): F414 - F419. [Abstract] [Full Text] [PDF]

				Y. Kotelevtsev and D. J Webb Endothelin as a natriuretic hormone: the case for a paracrine action mediated by nitric oxide Cardiovasc Res, August 15, 2001; 51(3): 481 - 488. [Full Text] [PDF]

				M. Porst, A. Hartner, H. Krause, K. F. Hilgers, and R. Veelken Inducible nitric oxide synthase and glomerular hemodynamics in rats with liver cirrhosis Am J Physiol Renal Physiol, August 1, 2001; 281(2): F293 - F299. [Abstract] [Full Text] [PDF]

				C. Li, W. Wang, T.-H. Kwon, L. Isikay, J. G. Wen, D. Marples, J. C. Djurhuus, A. Stockwell, M. A. Knepper, S. Nielsen, et al. Downregulation of AQP1, -2, and -3 after ureteral obstruction is associated with a long-term urine-concentrating defect Am J Physiol Renal Physiol, July 1, 2001; 281(1): F163 - F171. [Abstract] [Full Text] [PDF]

				Y.-k. Lou, C. Wen, M. Li, D. J. Adams, M.-x. Wang, F. Yang, B. J. Morris, and J. A. Whitworth Decreased Renal Expression of Nitric Oxide Synthase Isoforms in Adrenocorticotropin-Induced and Corticosterone-Induced Hypertension Hypertension, April 1, 2001; 37(4): 1164 - 1170. [Abstract] [Full Text] [PDF]

				P. A. Ortiz and J. L. Garvin NO Inhibits NaCl Absorption by Rat Thick Ascending Limb Through Activation of cGMP-Stimulated Phosphodiesterase Hypertension, February 1, 2001; 37(2): 467 - 471. [Abstract] [Full Text] [PDF]

				D. Y. Tan, S. Meng, G. W. Cason, and R. D. Manning Jr. Mechanisms of salt-sensitive hypertension: role of inducible nitric oxide synthase Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2000; 279(6): R2297 - R2303. [Abstract] [Full Text] [PDF]

				N. D. Vaziri, Y. Ding, D. S. Sangha, and R. E. Purdy Upregulation of NOS by simulated microgravity, potential cause of orthostatic intolerance J Appl Physiol, July 1, 2000; 89(1): 338 - 344. [Abstract] [Full Text] [PDF]

				W. H. Wang The cGMP-dependent protein kinase stimulates the basolateral 18-pS K channel of the rat CCD Am J Physiol Cell Physiol, June 1, 2000; 278(6): C1212 - C1217. [Abstract] [Full Text] [PDF]

				M. Liang and F. G. Knox Production and functional roles of nitric oxide in the proximal tubule Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2000; 278(5): R1117 - R1124. [Abstract] [Full Text] [PDF]

				A. Lazrak, A. Samanta, and S. Matalon Biophysical properties and molecular characterization of amiloride-sensitive sodium channels in A549 cells Am J Physiol Lung Cell Mol Physiol, April 1, 2000; 278(4): L848 - L857. [Abstract] [Full Text] [PDF]

				R. Komers, T. T. Oyama, J. G. Chapman, K. M. Allison, and S. Anderson Effects of Systemic Inhibition of Neuronal Nitric Oxide Synthase in Diabetic Rats Hypertension, February 1, 2000; 35(2): 655 - 661. [Abstract] [Full Text] [PDF]

				J. M. Stulak, L. A. Juncos, J. A. Haas, and J. C. Romero Systemic hemodynamics and renal function in hemorrhaged dogs resuscitated with cross-linked hemoglobin Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2000; 278(1): R28 - R33. [Abstract] [Full Text] [PDF]

				C. F. Plato, E. G. Shesely, and J. L. Garvin eNOS Mediates L-Arginine-Induced Inhibition of Thick Ascending Limb Chloride Flux Hypertension, January 1, 2000; 35(1): 319 - 323. [Abstract] [Full Text] [PDF]

				G. H. ALLCOCK, M. HUKKANEN, J. M. POLAK, J. S. POLLOCK, and D. M. POLLOCK Increased Nitric Oxide Synthase-3 Expression in Kidneys of Deoxycorticosterone Acetate-Salt Hypertensive Rats J. Am. Soc. Nephrol., November 1, 1999; 10(11): 2283 - 2289. [Abstract] [Full Text]

				J. L. Garvin and N. J. Hong Nitric oxide inhibits sodium/hydrogen exchange activity in the thick ascending limb Am J Physiol Renal Physiol, September 1, 1999; 277(3): F377 - F382. [Abstract] [Full Text] [PDF]

				T.-H. Kwon, J. Frokiaer, P. Fernandez-Llama, M. A. Knepper, and S. Nielsen Reduced abundance of aquaporins in rats with bilateral ischemia-induced acute renal failure: prevention by alpha -MSH Am J Physiol Renal Physiol, September 1, 1999; 277(3): F413 - F427. [Abstract] [Full Text] [PDF]

				N. H. Garcia, C. F. Plato, B. A. Stoos, and J. L. Garvin Nitric Oxide–Induced Inhibition of Transport by Thick Ascending Limbs From Dahl Salt-Sensitive Rats Hypertension, September 1, 1999; 34(3): 508 - 513. [Abstract] [Full Text] [PDF]

				F. Wu, F. Park, A. W. Cowley Jr., and D. L. Mattson Quantification of nitric oxide synthase activity in microdissected segments of the rat kidney Am J Physiol Renal Physiol, June 1, 1999; 276(6): F874 - F881. [Abstract] [Full Text] [PDF]

				O. NAKASHIMA, Y. TERADA, S. INOSHITA, M. KUWAHARA, S. SASAKI, and F. MARUMO Inducible Nitric Oxide Synthase Can Be Induced in the Absence of Active Nuclear Factor-{kappa}B in Rat Mesangial Cells: Involvement of the JanusKinase 2 Signaling Pathway J. Am. Soc. Nephrol., April 1, 1999; 10(4): 721 - 729. [Abstract] [Full Text]

				B. C. Kone and S. Higham Nitric oxide inhibits transcription of the Na+-K+-ATPase alpha 1-subunit gene in an MTAL cell line Am J Physiol Renal Physiol, April 1, 1999; 276(4): F614 - F621. [Abstract] [Full Text] [PDF]

				C. F. Plato, B. A. Stoos, D. Wang, and J. L. Garvin Endogenous nitric oxide inhibits chloride transport in the thick ascending limb Am J Physiol Renal Physiol, January 1, 1999; 276(1): F159 - F163. [Abstract] [Full Text] [PDF]

				R. Zatz and C. Baylis Chronic Nitric Oxide Inhibition Model Six Years On Hypertension, December 1, 1998; 32(6): 958 - 964. [Full Text] [PDF]

				X. Wang, M. Lu, Y. Gao, A. Papapetropoulos, W. C. Sessa, and W. Wang Neuronal nitric oxide synthase is expressed in principal cell of collecting duct Am J Physiol Renal Physiol, September 1, 1998; 275(3): F395 - F399. [Abstract] [Full Text] [PDF]

				M. Lu and W.-H. Wang Reaction of nitric oxide with superoxide inhibits basolateral K+ channels in the rat CCD Am J Physiol Cell Physiol, July 1, 1998; 275(1): C309 - C316. [Abstract] [Full Text] [PDF]

				C. S. Wilcox, X. Deng, and W. J. Welch NO generation and action during changes in salt intake: roles of nNOS and macula densa Am J Physiol Regulatory Integrative Comp Physiol, June 1, 1998; 274(6): R1588 - R1593. [Abstract] [Full Text] [PDF]

				M. Lu, X. Wang, and W. Wang Nitric oxide increases the activity of the apical 70-pS K+ channel in TAL of rat kidney Am J Physiol Renal Physiol, May 1, 1998; 274(5): F946 - F950. [Abstract] [Full Text] [PDF]

				L. Jain, X.-J. Chen, L. A. Brown, and D. C. Eaton Nitric oxide inhibits lung sodium transport through a cGMP-mediated inhibition of epithelial cation channels Am J Physiol Lung Cell Mol Physiol, April 1, 1998; 274(4): L475 - L484. [Abstract] [Full Text] [PDF]

				Y. Guo, M. D. Duvall, J. P. Crow, and S. Matalon Nitric oxide inhibits Na+ absorption across cultured alveolar type II monolayers Am J Physiol Lung Cell Mol Physiol, March 1, 1998; 274(3): L369 - L377. [Abstract] [Full Text] [PDF]

				R. F. Husted, J. P. Rapp, and J. B. Stokes Candidate Genes in the Regulation of Na+ Transport by Inner Medullary Collecting Duct Cells From Dahl Rats Hypertension, February 1, 1998; 31(2): 608 - 614. [Abstract] [Full Text] [PDF]

				D. L. Mattson, C. Y. Maeda, T. D. Bachman, and A. W. Cowley Jr Inducible Nitric Oxide Synthase and Blood Pressure Hypertension, January 1, 1998; 31(1): 15 - 20. [Abstract] [Full Text] [PDF]

				M. I. Madrid, M. Garcia-Salom, J. Tornel, M. De Gasparo, and F. J. Fenoy Effect of interactions between nitric oxide and angiotensin II on pressure diuresis and natriuresis Am J Physiol Regulatory Integrative Comp Physiol, November 1, 1997; 273(5): R1676 - R1682. [Abstract] [Full Text] [PDF]

				D. S. A. Majid, M. Godfrey, and L. G. Navar Pressure Natriuresis and Renal Medullary Blood Flow in Dogs Hypertension, April 1, 1997; 29(4): 1051 - 1057. [Abstract] [Full Text]

				D. S.A. Majid, M. Godfrey, and S. A. Omoro Pressure Natriuresis and Autoregulation of Inner Medullary Blood Flow in Canine Kidney Hypertension, January 1, 1997; 29(1): 210 - 215. [Abstract] [Full Text] [PDF]

				N. H. Garcia, B. A. Stoos, O. A. Carretero, and J. L. Garvin Mechanism of the Nitric Oxide-Induced Blockade of Collecting Duct Water Permeability Hypertension, March 1, 1996; 27(3): 679 - 683. [Abstract] [Full Text]

Copyright © 2008 by the American Society of Nephrology. Online ISSN: 1533-3450 Print ISSN: 1046-6673