Identification of the WNK-SPAK/OSR1 signaling pathway in rodent and human lenses

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 1, 2014, Pages 310-321

  Vorontsova, Irene ^a   Lam, Leo ^a   Delpire, Eric ^b   Lim, Julie ^a   Donaldson, Paul ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cataract; Cation chloride cotransporters; Cell volume regulation; Lens; OSR1SPAK knock out; SPAK; WNK

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; FOCAL ADHESION KINASE 2; OXIDATIVE STRESS RESPONSE KINASE 1; PROTEIN KINASE WNK1; PROTEIN KINASE WNK3; PROTEIN KINASE WNK4; UNCLASSIFIED DRUG; OSR1 PROTEIN, HUMAN; OSR1 PROTEIN, MOUSE; PAS DOMAIN KINASES; PERIT1 PROTEIN, RAT; PROTEIN; PROTEIN SERINE THREONINE KINASE; RNA; STK39 PROTEIN, HUMAN; STK39 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ADOLESCENT; ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATARACT; CELLULAR DISTRIBUTION; CHEMOLUMINESCENCE; CONTROLLED STUDY; CORNEA OPACITY; HUMAN; HUMAN TISSUE; LENS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MIDDLE AGED; PATHOLOGY; VERY ELDERLY; WISTAR RAT; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BLOTTING, WESTERN; CATARACT; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; LENS, CRYSTALLINE; MICE; MICE, KNOCKOUT; MIDDLE AGED; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; YOUNG ADULT;

EID: 84921313780     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-15911     Document Type: Article

References (82)

1. Donaldson PJ, Chee K-SN, Lim JC, Webb KF. Regulation of lens volume: implications for lens transparency. Exp Eye Res. 2009; 88:144-150.
2. Jacob TJC. The relationship between cataract, cell swelling and volume regulation. Progr Retin Eye Res. 1999;18:223- 233.
3. Mathias RT, Kistler J, Donaldson P. The lens circulation. J Membr Biol. 2007;216:1-16.
4. Vaghefi E, Pontre BP, Jacobs MD, Donaldson PJ. Visualizing ocular lens fluid dynamics using MRI: manipulation of steady state water content and water fluxes. Am J Physiol. 2011;301: R335-R342.
5. Candia OA, Mathias R, Gerometta R. Fluid circulation determined in the isolated bovine lens. Invest Ophthalmol Vis Sci. 2012;53:7087-7096.
6. Young MA, Tunstall MJ, Kistler J, Donaldson PJ. Blocking chloride channels in the rat lens: localized changes in tissue hydration support the existence of a circulating chloride flux. Invest Ophthalmol Vis Sci. 2000;41:3049-3055.
7. Tunstall MJ, Eckert R, Donaldson P, Kistler J. Localised fibre cell swelling characteristic of diabetic cataract can be induced in normal rat lens using the chloride channel blocker 5-Nitro-2- (3-Phenylpropylamino) benzoic acid. Ophthalmic Res. 1999; 31:317-320.
8. Patterson JW. Lens volume regulation in hypertonic medium. Exp Eye Res. 1981;32:151-162.
9. Chee KN, Kistler J, Donaldson PJ. Roles for KCC transporters in the maintenance of lens transparency. Invest Ophthalmol Vis Sci. 2006;47:673-682.
10. Chee KN, Vorontsova I, Lim JC, Kistler J, Donaldson PJ. Expression of the sodium potassium chloride cotransporter (NKCC1) and sodium chloride cotransporter (NCC) and their effects on rat lens transparency. Mol Vis. 2010;16:800-812.
11. Alvarez LJ, Candia OA, Turner HC, Polikoff LA. Localization of a Na(þ)-K(þ)-2Cl(+) cotransporter in the rabbit lens. Exp Eye Res. 2001;73:669-680.
12. Misri S, Chimote AA, Adragna NC, Warwar R, Brown TL, Lauf PK. KCC isoforms in a human lens epithelial cell line (B3) and lens tissue extracts. Exp Eye Res. 2006;83:1287-1294.
13. Lytle C, McManus T. Coordinate modulation of Na-K-2Cl cotransport and K-Cl cotransport by cell volume and chloride. Am J Physiol Cell Physiol. 2002;283:C1422-C1431.
14. Kahle KT, Rinehart J, Lifton RP. Phosphoregulation of the Na-K- 2Cl and K-Cl cotransporters by the WNK kinases. Biochim Biophys Acta. 2010;1802:1150-1158.
15. Richardson C, Alessi DR. The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J Cell Sci. 2008;121:3293-3304.
16. McCormick JA, Ellison DH. The WNKs: atypical protein kinases with pleiotropic actions. Physiol Rev. 2011;91:177- 219.
17. Franceschi L, Villa-Moruzzi E, Biondani A, et al. Regulation of K-Cl cotransport by protein phosphatase 1a in mouse erythrocytes. Pflügers Arch. 2006;451:760-768.
18. Delpire E, Gagnon K. SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem J. 2008;409:321-331.
19. Delpire E, Gagnon KB. SPAK and OSR1, key kinases involved in the regulation of chloride transport. Acta Physiol. 2006; 187:103-113.
20. Vitari AC, Deak M, Morrice NA, Alessi DR. The WNK1 and WNK4 protein kinases that are mutated in Gordon's hypertension syndrome phosphorylate and activate SPAK and OSR1 protein kinases. Biochem J. 2005;391:17-24.
21. Moriguchi T, Urushiyama S, Hisamoto N, et al. WNK1 regulates phosphorylation of cation-chloride-coupled cotransporters via the STE20-related Kinases, SPAK and OSR1. J Biol Chem. 2005; 280:42685-42693.
22. Nishida H, Sohara E, Nomura N, et al. Phosphatidylinositol 3- Kinase/Akt signaling pathway activates the WNK-OSR1/SPAKNCC phosphorylation cascade in hyperinsulinemic db/db mice/novelty and significance. Hypertension. 2012;60:981- 990.
23. Zagorska A, Pozo-Guisado E, Boudeau J, et al. Regulation of activity and localization of the WNK1 protein kinase by hyperosmotic stress. J Cell Biol. 2007;176:89-100.
24. Anselmo AN, Earnest S, Chen W, et al. WNK1 and OSR1 regulate the Naþ, Kþ, 2Cl- cotransporter in HeLa cells. Proc Natl Acad Sci U S A. 2006;103:10883-10888.
25. Delpire E, Gagnon KBE. Genome-wide analysis of SPAK/OSR1 binding motifs. Physiol Genomics. 2007;28:223-231.
26. Richardson C, Sakamoto K, de los Heros P, et al. Regulation of the NKCC2 ion cotransporter by SPAK-OSR1-dependent and -independent pathways. J Cell Sci. 2011;124:789-800.
27. Garzon-Muvdi T, Pacheco-Alvarez D, Gagnon KBE, et al. WNK4 kinase is a negative regulator of Kþ-Cl- cotransporters. Am J Physiol Renal Physiol. 2007;292:F1197-F1207.
28. Xu B, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, Cobb MH. WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain II. J Biol Chem. 2000;275:16795-16801.
29. Lenertz LY, Lee B-H, Min X, et al. Properties of WNK1 and implications for other family members. J Biol Chem. 2005;280: 26653-26658.
30. Cruz-Rangel S, Melo Z, Vázquez N, et al. Similar effects of all WNK3 variants on SLC12 cotransporters. Am J Physiol Cell Physiol. 2011;301:C601-C608.
31. de los Heros P, Kahle KT, Rinehart J, et al. WNK3 bypasses the tonicity requirement for K-Cl cotransporter activation via a phosphatase-dependent pathway. Proc Natl Acad Sci U S A. 2006;103:1976-1981.
32. Thastrup JO, Rafiqi FH, Vitari AC, et al. SPAK/OSR1 regulate NKCC1 and WNK activity: analysis of WNK isoform interactions and activation by T-loop trans-autophosphorylation. Biochem J. 2012;441:325-337.
33. Golbang AP, Cope G, Hamad A, et al. Regulation of the expression of the Na/Cl cotransporter by WNK4 and WNK1: evidence that accelerated dynamin-dependent endocytosis is not involved. Am J Physiol Renal Physiol. 2006;291:F1369- F1376.
34. Hannemann A, Flatman PW. Phosphorylation and transport in the Na-K-2Cl cotransporters, NKCC1 and NKCC2A, compared in HEK-293 cells. PLoS One. 2011;6:e17992.
35. Gagnon KB, Delpire E. Multiple pathways for protein phosphatase 1 (PP1) regulation of Na-K-2Cl cotransporter (NKCC1) function. J Biol Chem. 2010;285:14115-14121.
36. Darman RB, Flemmer A, Forbush B. Modulation of ion transport by direct targeting of protein phosphatase type 1 to the Na-K-Cl cotransporter. J Biol Chem. 2001;276:34359- 34362.
37. Darman RB, Forbush BA. Regulatory locus of phosphorylation in the N terminus of the Na-K-Cl cotransporter, NKCC1. J Biol Chem. 2002;277:37542-37550.
38. Bize I, Guvenc B, Robb A, Buchbinder G, Brugnara C. Serine/ threonine protein phosphatases and regulation of K-Cl cotransport in human erythrocytes. Am J Physiol Cell Physiol. 1999;277:C926-936.
39. Zhang J, Lauf PK, Adragna NC. PDGF activates K-Cl cotransport through phosphoinositide 3-kinase and protein phosphatase-1 in primary cultures of vascular smooth muscle cells. Life Sci. 2005;77:953-965.
40. Gusev G, Agalakova N. Regulation of K-Cl cotransport in erythrocytes of frog Rana temporaria by commonly used protein kinase and protein phosphatase inhibitors. J Comp Physiol B. 2010;180:385-391.
41. Liu W-B, Li Y, Zhang L, et al. Differential expression of the catalytic subunits for PP-1 and PP-2A and the regulatory subunits for PP-2A in mouse eye. Mol Vis. 2008;14:762-773.
42. Li DW-C, Xiang H, Fass U, Zhang X-Y. Analysis of expression patterns of protein Phosphatase-1 and Phosphatase-2A in rat and bovine lenses. Invest Ophthalmol Vis Sci. 2001;42:2603- 2609.
43. Li DW-C, Liu J-P, Schmid PC, et al. Protein serine/threonine phosphatase-1 dephosphorylates p53 at Ser-15 and Ser-37 to modulate its transcriptional and apoptotic activities. Oncogene. 2006;25:3006-3022.
44. Umeda IO, Nakata H, Nishigori H. Identification of protein phosphatase 2C and confirmation of other protein phosphatases in the ocular lenses. Exp Eye Res. 2004;79:385-392.
45. Bassnett S, Wilmarth PA, David LL. The membrane proteome of the mouse lens fiber cell. Mol Vis. 2009;15:2448-2463.
46. Wang Z, Han J, David LL, Schey KL. Proteomics and phosphoproteomics analysis of human lens fiber cell membranes. Invest Ophthalmol Vis Sci. 2013;54:1135-1143.
47. Geng Y, Hoke A, Delpire E. The Ste20 kinases Ste20-related proline-alanine-rich kinase and oxidative-stress response 1 regulate NKCC1 function in sensory neurons. J Biol Chem. 2009;284:14020-14028.
48. Lim J, Lam YC, Kistler J, Donaldson PJ. Molecular characterization of the cystine/glutamate exchanger and the excitatory amino acid transporters in the rat lens. Invest Ophthalmol Vis Sci. 2005;46:2869-2877.
49. Lim JC, Lam L, Li B, Donaldson PJ. Molecular identification and cellular localization of a potential transport system involved in cystine/cysteine uptake in human lenses. Exp Eye Res. 2013; 116:219-226.
50. Lim JC, Walker KL, Sherwin T, Schey KL, Donaldson PJ. Confocal microscopy reveals zones of membrane remodeling in the outer cortex of the human lens. Invest Ophthalmol Vis Sci. 2009;50:4304-4310.
51. Augusteyn RC. On the growth and internal structure of the human lens. Exp Eye Res. 2010;90:643-654.
52. Jacobs MD, Donaldson PJ, Cannell MB, Soeller C. Resolving morphology and antibody labeling over large distances in tissue sections. Microsc Res Tech. 2003;62:83-91.
53. Piechotta K, Garbarini N, England R, Delpire E. Characterization of the interaction of the stress kinase SPAK with the Naþ- Kþ-2Cl cotransporter in the nervous system. J Biol Chem. 2003;278:52848-52856.
54. Liu Z, Wang H-R, Huang C-L. Regulation of ROMK channel and Kþhomeostasis by kidney-specific WNK1 kinase. J Biol Chem. 2009;284:12198-12206.
55. Gagnon KBE, England R, Delpire E. Characterization of SPAK and OSR1, regulatory kinases of the Na-K-2Cl cotransporter. Mol Cellular Biol. 2006;26:689-698.
56. Shekarabi M, Girard N, Riviere J-B, et al. Mutations in the nervous system-specific HSN2 exon of WNK1 cause hereditary sensory neuropathy type II. J Clin Invest. 2008;118:2496- 2505.
57. Tu SW, Bugde A, Luby-Phelps K, Cobb MH. WNK1 is required for mitosis and abscission. Proc Natl Acad Sci U S A. 2011;108: 1385-1390.
58. Lee S-J, Cobb MH, Goldsmith EJ. Crystal structure of domainswapped STE20 OSR1 kinase domain. Protein Sci. 2009;18: 304-313.
59. Ponce-Coria J, Gagnon KB, Delpire E. Calcium-binding protein 39 facilitates molecular interaction between Ste20p proline alanine-rich kinase and oxidative stress response 1 monomers. Am J Physiol Cell Physiol. 2012;303:C1198-C1205.
60. Brunkener M, Georgatos SD. Membrane-binding properties of filensin, a cytoskeletal protein of the lens fiber cells. J Cell Sci. 1992;103:709-718.
61. Kistler J, Goldie K, Donaldson P, Engel A. Reconstitution of native-type noncrystalline lens fiber gap junctions from isolated hemichannels. J Cell Biol. 1994;126:1047-1058.
62. Korlimbinis A, Berry Y, Thibault D, Schey KL, Truscott RJW. Protein aging: truncation of aquaporin 0 in human lens regions is a continuous age-dependent process. Exp Eye Res. 2009;88: 966-973.
63. Wang Z, Schey KL. Phosphorylation and truncation sites of bovine lens connexin 46 and connexin 50. Exp Eye Res. 2009; 89:898-904.
64. Markadieu N, Delpire E. Physiology and pathophysiology of SLC12A1/2 transporters. Pflügers Arch. 2014;466:91-105.
65. Zambrowicz BP, Abuin A, Ramirez-Solis R, et al. Wnk1 kinase deficiency lowers blood pressure in mice: a gene-trap screen to identify potential targets for therapeutic intervention. Proc Natl Acad Sci U S A. 2003;100:14109-14114.
66. Zhang Z, Xu X, Zhang Y, Zhou J, Yu Z, He C. LINGO-1 interacts with WNK1 to regulate nogo-induced inhibition of neurite extension. J Biol Chem. 2009;284:15717-15728.
67. Lee B-H, Min X, Heise CJ, et al. WNK1 phosphorylates synaptotagmin 2 and modulates its membrane binding. Molecular Cell. 2004;15:741-751.
68. Oh E, Heise CJ, English JM, Cobb MH, Thurmond DC. WNK1 is a novel regulator of munc18c-syntaxin 4 complex formation in soluble NSF attachment protein receptor (snare)-mediated vesicle exocytosis. J Biol Chem. 2007;282:32613-32622.
69. San-Cristobal P, Ponce-Coria J, Vazquez N, Bobadilla NA, Gamba G. WNK3 and WNK4 amino-terminal domain defines their effect on the renal Naþ-Cl- cotransporter. Am J Physiol Renal Physiol. 2008;295:F1199-F1206.
70. Wilson FH, Disse-Nicodème S, Choate KA, et al. Human hypertension caused by mutations in WNK kinases. Science. 2001;293:1107-1112.
71. Jiang Y, Ferguson WB, Peng J-B. WNK4 enhances TRPV5- mediated calcium transport: potential role in hypercalciuria of familial hyperkalemic hypertension caused by gene mutation of WNK4. Am J Physiol Renal Physiol. 2007;292:F545-F554.
72. Cha S-K, Huang C-L. WNK4 kinase stimulates caveola-mediated endocytosis of TRPV5 amplifying the dynamic range of regulation of the channel by protein kinase C. J Biol Chem. 2010;285:6604-6611.
73. Strange K, Denton J, Nehrke K. Ste20-type kinases: evolutionarily conserved regulators of ion transport and cell volume. Physiology. 2006;21:61-68.
74. Elvira B, Blecua M, Luo D, et al. SPAK-sensitive regulation of glucose transporter SGLT1. J Membr Biol. 2014;1-7.
75. Smith B, Varadaraj R, Krushinski A, Donaldson P, Mathias R, Kistler J. Glucose transport in the lens. Invest Ophthalmol Vis Sci. 2002;43:4646.
76. Piechotta K, Lu J, Delpire E. Cation chloride cotransporters interact with the stress-related kinases ste20-related proline- alanine-rich kinase (SPAK) and oxidative stress response 1 (OSR1). J Biol Chem. 2002;277:50812-50819.
77. Chen W, Yazicioglu M, Cobb MH. Characterization of OSR1, a member of the mammalian Ste20p/germinal center kinase subfamily. J Biol Chem. 2004;279:11129-11136.
78. Sun X, Gao L, Yu RK, Zeng G. Down-regulation of WNK1 protein kinase in neural progenitor cells suppresses cell proliferation and migration. J Neurochem. 2006;99:1114- 1121.
79. Ohta A, Yang S-S, Rai T, Chiga M, Sasaki S, Uchida S. Overexpression of human WNK1 increases paracellular chloride permeability and phosphorylation of claudin-4 in MDCKII cells. Biochem Biophysic Res Commun. 2006;349: 804-808.
80. Wade JB, Fang L, Liu J, et al. WNK1 kinase isoform switch regulates renal potassium excretion. Proc Natl Acad Sci U S A. 2006;103:8558-8563.
81. Hengl T, Kaneko H, Dauner K, Vocke K, Frings S, Möhrlen F. Molecular components of signal amplification in olfactory sensory cilia. Proc Natl Acad Sci U S A. 2010;107:6052-6057.
82. Ushiro H, Tsutsumi T, Suzuki K, Kayahara T, Nakano K. Molecular cloning and characterization of a novel Ste20-related protein kinase enriched in neurons and transporting epithelia. Arch Biochem Biophys. 1998;355:233-240.