SPAK and OSR1 play essential roles in potassium homeostasis through actions on the distal convoluted tubule

Journal of Physiology

Volumn 594, Issue 17, 2016, Pages 4945-4966

  Ferdaus, Mohammed Z ^a   Barber, Karl W ^b,c   López Cayuqueo, Karen I ^d   Terker, Andrew S ^a   Argaiz, Eduardo R ^e   Gassaway, Brandon M ^b,c   Chambrey, Régine ^d   Gamba, Gerardo ^e   Rinehart, Jesse ^b,c   McCormick, James A ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

^d PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^e INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; ISOPROTEIN; OXIDATIVE STRESS RESPONSE KINASE 1; PHOSPHOTRANSFERASE; SODIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 2; SPS 1 RELATED PROLINE ALANINE RICH KINASE; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROLYTE EXCRETION; FEMALE; HOMEOSTASIS; HYPOKALEMIA; KIDNEY; KIDNEY DISTAL TUBULE; KIDNEY MEDULLA; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PHENOTYPE; POLYURIA; POTASSIUM BLOOD LEVEL; POTASSIUM HOMEOSTASIS; POTASSIUM RESTRICTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SALT WASTING; SODIUM RESTRICTION; SODIUM TRANSPORT; SYSTOLIC BLOOD PRESSURE; THICK ASCENDING LIMB; WILD TYPE; XENOPUS LAEVIS;

EID: 84986266734     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP272311     Document Type: Article

References (73)

1. Ares GR, Caceres PS & Ortiz PA (2011). Molecular regulation of NKCC2 in the thick ascending limb. Am J Physiol Renal Physiol 301, F1143–1159.
2. – cotransporter is modulated by intracellular chloride. J Am Soc Nephrol 26, 1781–1786.
3. Bhalla V & Hallows KR (2008). Mechanisms of ENaC regulation and clinical implications. J Am Soc Nephrol 19, 1845–1854.
4. Boersema PJ, Raijmakers R, Lemeer S, Mohammed S & Heck AJ (2009). Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4, 484–494.
5. Bostanjoglo M, Reeves WB, Reilly RF, Velazquez H, Robertson N, Litwack G, Morsing P, Dorup J, Bachmann S & Ellison DH (1998). 11β-hydroxysteroid dehydrogenase, mineralocorticoid receptor, and thiazide-sensitive Na–Cl cotransporter expression by distal tubules. J Am Soc Nephrol 9, 1347–1358.
6. Carmosino M, Rizzo F, Procino G, Basco D, Valenti G, Forbush B, Schaeren-Wiemers N, Caplan MJ & Svelto M (2010). MAL/VIP17, a new player in the regulation of NKCC2 in the kidney. Mol Biol Cell 21, 3985–3997.
7. + intake: insights into the signaling pathways involved. Am J Physiol Renal Physiol 306, F1507–1519.
8. Cox J & Mann M (2008). MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26, 1367–1372.
9. Dimke H, San-Cristobal P, de Graaf M, Lenders JW, Deinum J, Hoenderop JG & Bindels RJ (2011). γ-Adducin stimulates the thiazide-sensitive NaCl cotransporter. J Am Soc Nephrol 22, 508–517.
10. Eladari D, Chambrey R, Picard N & Hadchouel J (2014). Electroneutral absorption of NaCl by the aldosterone-sensitive distal nephron: implication for normal electrolytes homeostasis and blood pressure regulation. Cell Mol Life Sci 71, 2879–2895.
11. Faresse N, Lagnaz D, Debonneville A, Ismailji A, Maillard M, Fejes-Toth G, Naray-Fejes-Toth A & Staub O (2012). Inducible kidney-specific Sgk1 knockout mice show a salt-losing phenotype. Am J Physiol Renal Physiol 302, F977–985.
12. Feric M, Zhao B, Hoffert JD, Pisitkun T & Knepper MA (2011). Large-scale phosphoproteomic analysis of membrane proteins in renal proximal and distal tubule. Am J Physiol Cell Physiol 300, C755–770.
13. Filippi BM, de los Heros P, Mehellou Y, Navratilova I, Gourlay R, Deak M, Plater L, Toth R, Zeqiraj E & Alessi DR (2011). MO25 is a master regulator of SPAK/OSR1 and MST3/MST4/YSK1 protein kinases. EMBO J 30, 1730–1741.
14. – co-transporter NKCC2 by AMP-activated protein kinase (AMPK). Biochem J 405, 85–93.
15. Giebisch G, Hebert SC & Wang WH (2003). New aspects of renal potassium transport. Pflugers Arch 446, 289–297.
16. 2 terminus of the renal Na-K-Cl cotransporter (NKCC2). Am J Physiol Renal Physiol 289, F1341–1345.
17. Grimm PR, Lazo-Fernandez Y, Delpire E, Wall SM, Dorsey SG, Weinman EJ, Coleman R, Wade JB & Welling PA (2015). Integrated compensatory network is activated in the absence of NCC phosphorylation. J Clin Invest 125, 2136–2150.
18. Grimm PR, Taneja TK, Liu J, Coleman R, Chen YY, Delpire E, Wade JB & Welling PA (2012). SPAK isoforms and OSR1 regulate sodium-chloride co-transporters in a nephron-specific manner. J Biol Chem 287, 37673–37690.
19. Gunaratne R, Braucht DW, Rinschen MM, Chou CL, Hoffert JD, Pisitkun T & Knepper MA (2010). Quantitative phosphoproteomic analysis reveals cAMP/vasopressin-dependent signaling pathways in native renal thick ascending limb cells. Proc Natl Acad Sci USA 107, 15653–15658.
20. Hannemann A & Flatman PW (2011). Phosphorylation and transport in the Na-K-2Cl cotransporters, NKCC1 and NKCC2A, compared in HEK-293 cells. PloS ONE 6, e17992.
21. Hao P, Ren Y, Dutta B & Sze SK (2013). Comparative evaluation of electrostatic repulsion-hydrophilic interaction chromatography (ERLIC) and high-pH reversed phase (Hp-RP) chromatography in profiling of rat kidney proteome. J Proteomics 82, 254–262.
22. Huttlin EL, Jedrychowski MP, Elias JE, Goswami T, Rad R, Beausoleil SA, Villen J, Haas W, Sowa ME & Gygi SP (2010). A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 143, 1174–1189.
23. Kaplan MR, Plotkin MD, Brown D, Hebert SC & Delpire E (1996). Expression of the mouse Na-K-2Cl cotransporter, mBSC2, in the terminal inner medullary collecting duct, the glomerular and extraglomerular mesangium, and the glomerular afferent arteriole. J Clin Invest 98, 723–730.
24. Kettenbach AN & Gerber SA (2011). Rapid and reproducible single-stage phosphopeptide enrichment of complex peptide mixtures: application to general and phosphotyrosine-specific phosphoproteomics experiments. Anal Chem 83, 7635–7644.
25. Lalioti MD, Zhang J, Volkman HM, Kahle KT, Hoffmann KE, Toka HR, Nelson-Williams C, Ellison DH, Flavell R, Booth CJ, Lu Y, Geller DS & Lifton RP (2006). Wnk4 controls blood pressure and potassium homeostasis via regulation of mass and activity of the distal convoluted tubule. Nat Genet 38, 1124–1132.
26. + reabsorption process in the renal cortical collecting ducts of mice. J Clin Invest 120, 1627–1635.
27. – cotransporter by oxidative stress-responsive kinase-1 deficiency manifests hypotension and Bartter-like syndrome. Proc Natl Acad Sci USA 108, 17538–17543.
28. Lourdel S, Paulais M, Marvao P, Nissant A & Teulon J (2003). A chloride channel at the basolateral membrane of the distal-convoluted tubule: a candidate ClC-K channel. J Gen Physiol 121, 287–300.
29. Lundby A, Secher A, Lage K, Nordsborg NB, Dmytriyev A, Lundby C & Olsen JV (2012). Quantitative maps of protein phosphorylation sites across 14 different rat organs and tissues. Nat Commun 3, 876.
30. Markadieu N, Rios K, Spiller BW, McDonald WH, Welling PA & Delpire E (2014). Short forms of Ste20-related proline/alanine-rich kinase (SPAK) in the kidney are created by aspartyl aminopeptidase (Dnpep)-mediated proteolytic cleavage. J Biol Chem 289, 29273–29284.
31. McCormick JA, Mutig K, Nelson JH, Saritas T, Hoorn EJ, Yang CL, Rogers S, Curry J, Delpire E, Bachmann S & Ellison DH (2011). A SPAK isoform switch modulates renal salt transport and blood pressure. Cell Metab 14, 352–364.
32. McCormick JA, Yang CL, Zhang C, Davidge B, Blankenstein KI, Terker AS, Yarbrough B, Meermeier NP, Park HJ, McCully B, West M, Borschewski A, Himmerkus N, Bleich M, Bachmann S, Mutig K, Argaiz ER, Gamba G, Singer JD & Ellison DH (2014). Hyperkalemic hypertension-associated cullin 3 promotes WNK signaling by degrading KLHL3. J Clin Invest 124, 4723–4736.
33. – cotransporter: a new model for ions and diuretics interaction. Am J Physiol Renal Physiol 279, F161–169.
34. Mount DB, Mercado A, Song L, Xu J, George AL, Jr, Delpire E & Gamba G (1999). Cloning and characterization of KCC3 and KCC4, new members of the cation-chloride cotransporter gene family. J Biol Chem 274, 16355–16362.
35. – cotransporter is activated and phosphorylated at the amino-terminal domain upon intracellular chloride depletion. J Biol Chem 281, 28755–28763.
36. Palmer LG & Frindt G (2000). Aldosterone and potassium secretion by the cortical collecting duct. Kidney Int 57, 1324–1328.
37. Park HJ, Curry JN & McCormick JA (2013). Regulation of NKCC2 activity by inhibitory SPAK isoforms: KS-SPAK is a more potent inhibitor than SPAK2. Am J Physiol Renal Physiol 305, F1687–1696.
38. Piala AT, Moon TM, Akella R, He H, Cobb MH & Goldsmith EJ (2014). Chloride sensing by WNK1 involves inhibition of autophosphorylation. Sci Signal 7, ra41.
39. + secretion and localization of molecular components. Am J Physiol Renal Physiol 291, F517–529.
40. Ponce-Coria J, Markadieu N, Austin TM, Flammang L, Rios K, Welling PA & Delpire E (2014). A novel Ste20-related proline/alanine-rich kinase (SPAK)-independent pathway involving calcium-binding protein 39 (Cab39) and serine threonine kinase with no lysine member 4 (WNK4) in the activation of Na-K-Cl cotransporters. J Biol Chem 289, 17680–17688.
41. Rafiqi FH, Zuber AM, Glover M, Richardson C, Fleming S, Jovanovic S, Jovanovic A, O'Shaughnessy KM & Alessi DR (2010). Role of the WNK-activated SPAK kinase in regulating blood pressure. EMBO Mol Med 2, 63–75.
42. – cotransporter 2. Mol Cell Biol 30, 3027–3037.
43. – cotransporter by the WNK-regulated kinases SPAK and OSR1. J Cell Sci 121, 675–684.
44. Richardson C, Sakamoto K, de los Heros P, Deak M, Campbell DG, Prescott AR & Alessi DR (2011). Regulation of the NKCC2 ion cotransporter by SPAK-OSR1-dependent and -independent pathways. J Cell Sci 124, 789–800.
45. Rieg T, Tang T, Uchida S, Hammond HK, Fenton RA & Vallon V (2013). Adenylyl cyclase 6 enhances NKCC2 expression and mediates vasopressin-induced phosphorylation of NKCC2 and NCC. Am J Pathol 182, 96–106.
46. Rosenbaek LL, Assentoft M, Pedersen NB, MacAulay N & Fenton RA (2012). Characterization of a novel phosphorylation site in the sodium-chloride cotransporter, NCC. J Physiol 590, 6121–6139.
47. – cotransporter (NCC) in response to a high-salt diet. Am J Physiol Renal Physiol 291, F503–508.
48. Saritas T, Borschewski A, McCormick JA, Paliege A, Dathe C, Uchida S, Terker A, Himmerkus N, Bleich M, Demaretz S, Laghmani K, Delpire E, Ellison DH, Bachmann S & Mutig K (2013). SPAK differentially mediates vasopressin effects on sodium cotransporters. J Am Soc Nephrol 24, 407–418.
49. Schmitt R, Klussmann E, Kahl T, Ellison DH & Bachmann S (2003). Renal expression of sodium transporters and aquaporin-2 in hypothyroid rats. Am J Physiol Renal Physiol 284, F1097–1104.
50. Seyberth HW & Schlingmann KP (2011). Bartter- and Gitelman-like syndromes: salt-losing tubulopathies with loop or DCT defects. Pediatr Nephrol 26, 1789–1802.
51. Simon DB, Nelson-Williams C, Bia MJ, Ellison D, Karet FE, Molina AM, Vaara I, Iwata F, Cushner HM, Koolen M, Gainza FJ, Gitleman HJ & Lifton RP (1996). Gitelman's variant of Bartter's syndrome, inherited hypokalaemic alkalosis, is caused by mutations in the thiazide-sensitive Na-Cl cotransporter. Nat Genet 12, 24–30.
52. Soleimani M, Barone S, Xu J, Shull GE, Siddiqui F, Zahedi K & Amlal H (2012). Double knockout of pendrin and Na-Cl cotransporter (NCC) causes severe salt wasting, volume depletion, and renal failure. Proc Natl Acad Sci USA 109, 13368–13373.
53. Sorensen MV, Grossmann S, Roesinger M, Gresko N, Todkar AP, Barmettler G, Ziegler U, Odermatt A, Loffing-Cueni D & Loffing J (2013). Rapid dephosphorylation of the renal sodium chloride cotransporter in response to oral potassium intake in mice. Kidney Int 83, 811–824.
54. Takahashi D, Mori T, Nomura N, Khan MZ, Araki Y, Zeniya M, Sohara E, Rai T, Sasaki S & Uchida S (2014). WNK4 is the major WNK positively regulating NCC in the mouse kidney. Biosci Rep 34, e00107.
55. Takahashi N, Chernavvsky DR, Gomez RA, Igarashi P, Gitelman HJ & Smithies O (2000). Uncompensated polyuria in a mouse model of Bartter's syndrome. Proc Natl Acad Sci USA 97, 5434–5439.
56. Take C, Ikeda K, Kurasawa T & Kurokawa K (1991). Increased chloride reabsorption as an inherited renal tubular defect in familial type II pseudohypoaldosteronism. N Engl J Med 324, 472–476.
57. Terker AS, Zhang C, McCormick JA, Lazelle RA, Zhang C, Meermeier NP, Siler DA, Park HJ, Fu Y, Cohen DM, Weinstein AM, Wang WH, Yang CL & Ellison DH (2015). Potassium modulates electrolyte balance and blood pressure through effects on distal cell voltage and chloride. Cell Metab 21, 39–50.
58. Terker AS, Zhang C, Erspamer KJ, Gamba G, Yang CL & Ellison DH (2016). Unique chloride-sensing properties of WNK4 permit the distal nephron to modulate potassium homeostasis. Kidney Int 89, 127–134.
59. Tiwari S, Sharma N, Gill PS, Igarashi P, Kahn CR, Wade JB & Ecelbarger CM (2008). Impaired sodium excretion and increased blood pressure in mice with targeted deletion of renal epithelial insulin receptor. Proc Natl Acad Sci USA 105, 6469–6474.
60. Traykova-Brauch M, Schonig K, Greiner O, Miloud T, Jauch A, Bode M, Felsher DW, Glick AB, Kwiatkowski DJ, Bujard H, Horst J, von Knebel Doeberitz M, Niggli FK, Kriz W, Grone HJ & Koesters R (2008). An efficient and versatile system for acute and chronic modulation of renal tubular function in transgenic mice. Nat Med 14, 979–984.
61. – cotransporter NCC in vivo is regulated by dietary salt, potassium, and SGK1. Am J Physiol Renal Physiol 297, F704–712.
62. +-Cl- cotransporter. Am J Physiol Renal Physiol 305, F1177–1188.
63. Velazquez H & Silva T (2003). Cloning and localization of KCC4 in rabbit kidney: expression in distal convoluted tubule. Am J Physiol Renal Physiol 285, F49–58.
64. Vitari AC, Deak M, Morrice NA & Alessi DR (2005). The WNK1 and WNK4 protein kinases that are mutated in Gordon's hypertension syndrome phosphorylate and activate SPAK and OSR1 protein kinases. Biochem J 391, 17–24.
65. Vitzthum H, Castrop H, Meier-Meitinger M, Riegger GA, Kurtz A, Kramer BK & Wolf K (2002). Nephron specific regulation of chloride channel CLC-K2 mRNA in the rat. Kidney Int 61, 547–554.
66. + diet. Am J Physiol Renal Physiol 308, F923–931.
67. –/anion exchanger pendrin in mouse kidney by acid-base status. Kidney Int 62, 2109–2117.
68. + secretion through the apical K channel of cortical collecting duct. Kidney Int 48, 1024–1030.
69. Weisz OA & Johnson JP (2003). Noncoordinate regulation of ENaC: paradigm lost? Am J Physiol Renal Physiol 285, F833–842.
70. Wessel D & Flugge UI (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138, 141–143.
71. Yang SS, Lo YF, Wu CC, Lin SW, Yeh CJ, Chu P, Sytwu HK, Uchida S, Sasaki S & Lin SH (2010). SPAK-knockout mice manifest Gitelman syndrome and impaired vasoconstriction. J Am Soc Nephrol 21, 1868–1877.
72. Yang SS, Morimoto T, Rai T, Chiga M, Sohara E, Ohno M, Uchida K, Lin SH, Moriguchi T, Shibuya H, Kondo Y, Sasaki S & Uchida S (2007). Molecular pathogenesis of pseudohypoaldosteronism type II: generation and analysis of a Wnk4(D561A/+) knockin mouse model. Cell Metab 5, 331–344.
73. Zhang J, Siew K, Macartney T, O'Shaughnessy KM & Alessi DR (2015). Critical role of the SPAK protein kinase CCT domain in controlling blood pressure. Hum Mol Genet 24, 4545–4558.