Pendrin as a regulator of ECF and blood pressure

Current Opinion in Nephrology and Hypertension

Volumn 18, Issue 4, 2009, Pages 356-362

  Eladari, Dominique ^a,b,c,f   Chambrey, Régine ^a   Frische, Sebastian ^d   Vallet, Marion ^a,b,c   Edwards, Aurélie ^a,e  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL NECKER ENFANTS MALADES   (France)

^d AARHUS UNIVERSITY   (Denmark)

^e Tufts University   (United States)

^f CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

Chloride; hypertension; intercalated cells; mathematical model; pendrin

Indexed keywords

ALDOSTERONE; CHLORIDE; PENDRIN; SODIUM; SODIUM CHLORIDE;

BLOOD PRESSURE; BLOOD PRESSURE REGULATION; CHLORIDE TRANSPORT; EXTRACELLULAR SPACE; GITELMAN SYNDROME; HUMAN; HYPERTENSION; KIDNEY COLLECTING TUBULE; KIDNEY DISTAL TUBULE; MATHEMATICAL MODEL; NEPHRON; NONHUMAN; PATHOPHYSIOLOGY; PENDRED SYNDROME; PRIORITY JOURNAL; REVIEW; SODIUM BALANCE; SODIUM RESTRICTION; SODIUM TRANSPORT;

ANIMALS; BLOOD PRESSURE; CHLORIDE-BICARBONATE ANTIPORTERS; CHLORIDES; EXTRACELLULAR FLUID; HUMANS; ION TRANSPORT; KIDNEY; KIDNEY TUBULES, DISTAL; MEMBRANE TRANSPORT PROTEINS; NEPHRONS; SODIUM CHLORIDE;

EID: 67849093815     PISSN: 10624821     EISSN: None     Source Type: Journal    
DOI: 10.1097/MNH.0b013e32832c91f4     Document Type: Review

References (68)

1. Berghoff RS, Geraci AS. The influence of sodium chloride on blood pressure. Ill Med J 1929; 56:395-397.
2. Morgan TO. The effect of potassium and bicarbonate ions on the rise in blood pressure caused by sodium chloride. Clin Sci 1982; 63:407s-409s.
3. Kurtz TW, Al-Bander HA, Morris RC Jr. "Salt-sensitive" essential hypertension in men. Is the sodium ion alone important? N Engl J Med 1987; 317:1043-1048. This article confirmed in humans the requirement for chloride together with sodium to raise blood pressure.
4. Kurtz TW, Morris RC Jr. Dietary chloride as a determinant of "sodium-dependent" hypertension. Science 1983; 222:1139-1141. This article is the first that clearly demonstrates that sodium has to be administered as a chloride salt to raise blood pressure. This observation has a major important impact on our understanding of the pathophysiology of hypertension and paved the way toward a specific role of a chloride transporter, like pendrin, in this disease.
5. Schmidlin O, Tanaka M, Bollen AW, et al. Chloride-dominant salt sensitivity in the stroke-prone spontaneously hypertensive rat. Hypertension 2005; 45:867-873.
6. Tanaka M, Schmidlin O, Yi SL, et al. Genetically determined chloride-sensitive hypertension and stroke. Proc Natl Acad Sci USA 1997; 94:14748-14752.
7. Whitescarver SA, Ott CE, Jackson BA, et al. Salt-sensitive hypertension: contribution of chloride. Science 1984; 223:1430-1432.
8. Luft FC, Zemel MB, Sowers JA, et al. Sodium bicarbonate and sodium chloride: effects on blood pressure and electrolyte homeostasis in normal and hypertensive man. J Hypertens 1990; 8:663-670.
9. Schorr U, Distler A, Sharma AM. Effect of sodium chloride- and sodium bicarbonate-rich mineral water on blood pressure and metabolic parameters in elderly normotensive individuals: a randomized double-blind crossover trial. J Hypertens 1996; 14:131-135.
10. Kahle KT, Macgregor GG, Wilson FH, et al. Paracellular Cl- permeability is regulated by WNK4 kinase: insight into normal physiology and hypertension. Proc Natl Acad Sci USA 2004; 101:14877-14882.
11. Schambelan M, Sebastian A, Rector FC Jr. Mineralocorticoid-resistant renal hyperkalemia without salt wasting (type II pseudohypoaldosteronism): role of increased renal chloride reabsorption. Kidney Int 1981; 19:716-727.
12. Take C, Ikeda K, Kurasawa T, Kurokawa K. Increased chloride reabsorption as an inherited renal tubular defect in familial type II pseudohypoaldosteronism. N Engl J Med 1991; 324:472-476.
13. Yamauchi K, Rai T, Kobayashi K, et al. Disease-causing mutant WNK4 increases paracellular chloride permeability and phosphorylates claudins. Proc Natl Acad Sci USA 2004; 101:4690-4694.
14. Lifton RP, Gharavi AG, Geller DS. Molecular mechanisms of human hypertension. Cell 2001; 104:545-556.
15. Guyton AC. Blood pressure control: special role of the kidneys and body fluids. Science 1991; 252:1813-1816.
16. Loffing J, Kaissling B. Sodium and calcium transport pathways along the mammalian distal nephron: from rabbit to human. Am J Physiol Renal Physiol 2003; 284:F628-F643.
17. Madsen KM, Tisher CC. Structural-functional relationships along the distal nephron. Am J Physiol 1986; 250:F1-F15.
18. Teng-umnuay P, Verlander JW, Yuan W, et al. Identification of distinct subpopulations of intercalated cells in the mouse collecting duct. J Am Soc Nephrol 1996; 7:260-274.
19. Alper SL, Natale J, Gluck S, et al. Subtypes of intercalated cells in rat kidney collecting duct defined by antibodies against erythroid band 3 and renal vacuolar H-ATPase. Proc Natl Acad Sci USA 1989; 86:5429-5433. 20 Gamba G, Saltzberg SN, Lombardi M, et al. Primary structure and functional expression of a cDNA encoding the thiazide-sensitive, electroneutral sodium-chloride cotransporter. Proc Natl Acad Sci USA 1993; 90:2749-2753.
20. Simon DB, Nelson-Williams C, Bia MJ, et al. Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat Genet 1996; 12:24-30.
21. Schultheis PJ, Lorenz JN, Meneton P, et al. Phenotype resembling Gitelman's syndrome in mice lacking the apical Na-Cl cotransporter of the distal convoluted tubule. J Biol Chem 1998; 273:29150-29155.
22. Ji W, Foo JN, O'Roak BJ, et al. Rare independent mutations in renal salt handling genes contribute to blood pressure variation. Nat Genet 2008; 40:592-599.
23. Beyer KH Jr, Baer JE, Russo HF, Noll R. Electrolyte excretion as influenced by chlorothiazide. Science 1958; 127:146-147.
24. Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 2003; 289:2560-2572.
25. Trial. AOaCftACRGTAaL-LTtPHA: major outcomes in high-risk hypertensive patients randomized to angiotensin-converting enzyme inhibitor or calcium channel blocker vs diuretic: the Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial (ALLHAT). JAMA 2002; 288:2981-2997.
26. Lalioti MD, Zhang J, Volkman HM, et al. Wnk4 controls blood pressure and potassium homeostasis via regulation of mass and activity of the distal convoluted tubule. Nat Genet 2006; 38:1124-1132.
27. Kim GH, Masilamani S, Turner R, et al. The thiazide-sensitive Na-Cl cotransporter is an aldosterone-induced protein. Proc Natl Acad Sci USA 1998; 95:14552-14557.
28. Schuster VL, Stokes JB. Chloride transport by the cortical and outer medullary collecting duct. Am J Physiol 1987; 253:F203-F212.
29. Schuster VL, Bonsib SM, Jennings ML. Two types of collecting duct mitochondria-rich (intercalated) cells: lectin and band 3 cytochemistry. Am J Physiol 1986; 251:C347-C355.
30. Schwartz GJ, Barasch J, Al-Awqati Q. Plasticity of functional epithelial polarity. Nature 1985; 318:368-371.
31. Star RA, Burg MB, Knepper MA. Bicarbonate secretion and chloride absorption by rabbit cortical collecting ducts. Role of chloride/bicarbonate exchange. J Clin Invest 1985; 76:1123-1130.
32. Nissant A, Paulais M, Lachheb S, et al. Similar chloride channels in the connecting tubule and cortical collecting duct of the mouse kidney. Am J Physiol Renal Physiol 2006; 290:F1421-F1429.
33. Everett LA, Glaser B, Beck JC, et al. Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat Genet 1997; 17:411-422.
34. Kraiem Z, Heinrich R, Sadeh O, et al. Sulfate transport is not impaired in pendred syndrome thyrocytes. J Clin Endocrinol Metab 1999; 84:2574-2576.
35. Scott DA, Karniski LP. Human pendrin expressed in Xenopus laevis oocytes mediates chloride/formate exchange. Am J Physiol Cell Physiol 2000; 278:C207-C211.
36. Scott DA, Wang R, Kreman TM, et al. The Pendred syndrome gene encodes a chloride-iodide transport protein. Nat Genet 1999; 21:440-443.
37. Soleimani M, Greeley T, Petrovic S, et al. Pendrin: an apical Cl/OH/HCO3 exchanger in the kidney cortex. Am J Physiol Renal Physiol 2001; 280:F356-364.
38. Royaux IE, Wall SM, Karniski LP, et al. Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc Natl Acad Sci USA 2001; 98:4221-4226. This article demonstrated that pendrin is the apical chloride/bicarbonate exchanger of the B-ICs.
39. Kim YH, Kwon TH, Frische S, et al. Immunocytochemical localization of pendrin in intercalated cell subtypes in rat and mouse kidney. Am J Physiol Renal Physiol 2002; 283:F744-F754.
40. Wall SM, Hassell KA, Royaux IE, et al. Localization of pendrin in mouse kidney. Am J Physiol Renal Physiol 2003; 284:F229-F241.
41. Wall SM, Kim YH, Stanley L, et al. NaCl restriction upregulates renal Slc26a4 through subcellular redistribution: role in Cl-conservation. Hypertension 2004; 44:982-987.
42. Frische S, Kwon TH, Frokiaer J, et al. Regulated expression of pendrin in rat kidney in response to chronic NH4Cl or NaHCO3 loading. Am J Physiol Renal Physiol 2003; 284:F584-F593.
43. Petrovic S, Wang Z, Ma L, Soleimani M. Regulation of the apical Cl-/HCO-3 exchanger pendrin in rat cortical collecting duct in metabolic acidosis. Am J Physiol Renal Physiol 2003; 284:F103-F112.
44. Wagner CA, Finberg KE, Stehberger PA, et al. Regulation of the expression of the Cl/anion exchanger pendrin in mouse kidney by acid-base status. Kidney Int 2002; 62:2109-2117.
45. de Seigneux S, Malte H, Dimke H, et al. Renal compensation to chronic hypoxic hypercapnia: downregulation of pendrin and adaptation of the proximal tubule. Am J Physiol Renal Physiol 2007; 292:F1256-F1266.
46. Quentin F, Chambrey R, Trinh-Trang-Tan MM, et al. The Cl/HCO3 exchanger pendrin in the rat kidney is regulated in response to chronic alterations in chloride balance. Am J Physiol Renal Physiol 2004; 287: F1179-F1188. This article demonstrates that urinary chloride is a primary regulator of pendrin independent of acid-base regulation.
47. Hafner P, Grimaldi R, Capuano P, et al. Pendrin in the mouse kidney is primarily regulated by Cl-excretion but also by systemic metabolic acidosis. Am J Physiol Cell Physiol 2008; 295:C1658-C1667.
48. Verlander JW, Hassell KA, Royaux IE, et al. Deoxycorticosterone upregulates PDS (Slc26a4) in mouse kidney: role of pendrin in mineralocorticoid-induced hypertension. Hypertension 2003; 42:356-362. This article demonstrated that pendrin knock-out mice are protected against mineralocorticoid-induced hypertension. This is a major observation demonstrating that alteration in chloride transport directly affects blood pressure.
49. Pech V, Kim YH, Weinstein AM, et al. Angiotensin II increases chloride absorption in the cortical collecting duct in mice through a pendrin-dependent mechanism. Am J Physiol Renal Physiol 2007; 292:F914-920.
50. Kim YH, Pech V, Spencer KB, et al. Reduced ENaC protein abundance contributes to the lower blood pressure observed in pendrin-null mice. Am J Physiol Renal Physiol 2007; 293:F1314-F1324.
51. Hughey RP, Kleyman TR. Functional cross talk between ENaC and pendrin. Am J Physiol Renal Physiol 2007; 293:F1439-F1440.
52. Leipziger J. Control of epithelial transport via luminal P2 receptors. Am J Physiol Renal Physiol 2003; 284:F419-F432.
53. Pochynyuk O, Bugaj V, Rieg T, et al. Paracrine regulation of the epithelial Na channel in the mammalian collecting duct by purinergic P2Y2 receptor tone. J Biol Chem 2008; 283:36599-36607.
54. Rieg T, Bundey RA, Chen Y, et al. Mice lacking P2Y2 receptors have salt-resistant hypertension and facilitated renal Na and water reabsorption. FASEB J 2007; 21:3717-3726.
55. McCulloch F, Chambrey R, Eladari D, Peti-Peterdi J. Localization of connexin 30 in the luminal membrane of cells in the distal nephron. Am J Physiol Renal Physiol 2005; 289:F1304-F1312.
56. Sipos A, Vargas SL, Toma I, et al. Impaired renal tubular ATP release and pressure natriuresis in connexin30 knockout mice. J Am Soc Nephrol 2009 [Epub ahead of print]
57. Cotrina ML, Lin JH, Alves-Rodrigues A, et al. Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci USA 1998; 95:15735-15740.
58. Bell PD, Lapointe JY, Sabirov R, et al. Macula densa cell signaling involves ATP release through a maxi anion channel. Proc Natl Acad Sci USA 2003; 100:4322-4327.
59. + reabsorption.
60. Terada Y, Knepper MA. Thiazide-sensitive NaCl absorption in rat cortical collecting duct. Am J Physiol 1990; 259:F519-F528.
61. Tomita K, Pisano JJ, Burg MB, Knepper MA. Effects of vasopressin and bradykinin on anion transport by the rat cortical collecting duct. Evidence for an electroneutral sodium chloride transport pathway. J Clin Invest 1986; 77:136-141.
62. Tomita K, Pisano JJ, Knepper MA. Control of sodium and potassium transport in the cortical collecting duct of the rat. Effects of bradykinin, vasopressin, and deoxycorticosterone. J Clin Invest 1985; 76:132-136.
63. Chang H, Fujita T. A numerical model of the renal distal tubule. Am J Physiol 1999; 276:F931-F951.
64. Chang H, Fujita T. A numerical model of acid-base transport in rat distal tubule. Am J Physiol Renal Physiol 2001; 281:F222-F243.
65. Weinstein AM. A mathematical model of rat cortical collecting duct: determinants of the transtubular potassium gradient. Am J Physiol Renal Physiol 2001; 280:F1072-1092.
66. Weinstein AM. A mathematical model of rat distal convoluted tubule. I. Cotransporter function in early DCT. Am J Physiol Renal Physiol 2005; 289:F699-F720.
67. Weinstein AM. A mathematical model of rat distal convoluted tubule. II. Potassium secretion along the connecting segment. Am J Physiol Renal Physiol 2005; 289:F721-F741.
68. Strieter J, Stephenson JL, Giebisch G, Weinstein AM. A mathematical model of the rabbit cortical collecting tubule. Am J Physiol 1992; 263:F1063-F1075.