WNK1-OSR1 kinase-mediated phospho-activation of Na+-K+-2Cl- cotransporter facilitates glioma migration

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Zhu, Wen ^a   Begum, Gulnaz ^a   Pointer, Kelli ^b   Clark, Paul A ^b   Yang, Sung Sen ^d   Lin, Shih Hua ^d   Kahle, Kristopher T ^e   Kuo, John S ^b,c   Sun, Dandan ^a,f  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Bumetanide; Cell volume; Ezrin; Ion cotransporter; Temozolomide

Indexed keywords

EZRIN; MOESIN; OXIDATIVE STRESS RESPONSIVE KINASE 1; PROTEIN KINASE; PROTEIN KINASE WNK1; RADIXIN; SMALL INTERFERING RNA; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ANALYSIS OF VARIANCE; ARTICLE; CANCER CHEMOTHERAPY; CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL VOLUME; CHEMOTAXIS; CHEMOTAXIS ASSAY; CONTROLLED STUDY; DOWN REGULATION; FACILITATION; FLUORESCENCE; GENE SILENCING; GLIOBLASTOMA; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; NEURAL STEM CELL; POST HOC ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; TISSUE MICROARRAY; UPREGULATION; WESTERN BLOTTING;

BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; GENE KNOCKDOWN TECHNIQUES; GLIOMA; HUMANS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN-SERINE-THREONINE KINASES; SOLUTE CARRIER FAMILY 12, MEMBER 2; TISSUE ARRAY ANALYSIS;

EID: 84896718225     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-31     Document Type: Article

References (42)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008, 359:492-507. 10.1056/NEJMra0708126, 18669428.
2. Stupp R, Pavlidis N, Jelic S. ESMO Minimum Clinical Recommendations for diagnosis, treatment and follow-up of malignant glioma. Ann Oncol 2005, 16(Suppl 1):i64-i65.
3. Frosina G. DNA repair and resistance of gliomas to chemotherapy and radiotherapy. Mol Cancer Res 2009, 7:989-999. 10.1158/1541-7786.MCR-09-0030, 19609002.
4. Cuddapah VA, Sontheimer H. Ion channels and transporters [corrected] in cancer. 2. Ion channels and the control of cancer cell migration. Am J Physiol Cell Physiol 2011, 301:C541-C549. 10.1152/ajpcell.00102.2011, 3174565, 21543740.
5. Garzon-Muvdi T, Schiapparelli P, ap Rhys C, Guerrero-Cazares H, Smith C, Kim DH, Kone L, Farber H, Lee DY, An SS, et al. Regulation of brain tumor dispersal by NKCC1 through a novel role in focal adhesion regulation. PLoS Biol 2012, 10:e1001320. 10.1371/journal.pbio.1001320, 3341330, 22570591.
6. Haas BR, Cuddapah VA, Watkins S, Rohn KJ, Dy TE, Sontheimer H. With-No-Lysine Kinase 3 (WNK3) stimulates glioma invasion by regulating cell volume. Am J Physiol Cell Physiol 2011, 301:C1150-C1160. 10.1152/ajpcell.00203.2011, 3213919, 21813709.
7. Haas BR, Sontheimer H. Inhibition of the Sodium-Potassium-Chloride Cotransporter Isoform-1 reduces glioma invasion. Cancer Res 2010, 70:5597-5606. 10.1158/0008-5472.CAN-09-4666, 2896443, 20570904.
8. Algharabil J, Kintner DB, Wang Q, Begum G, Clark PA, Yang SS, Lin SH, Kahle KT, Kuo JS, Sun D. Inhibition of Na(+)-K(+)-2Cl(-) cotransporter isoform 1 accelerates temozolomide-mediated apoptosis in glioblastoma cancer cells. Cell Physiol Biochem 2012, 30:33-48. 10.1159/000339047, 3603147, 22759954.
9. McCormick JA, Ellison DH. The WNKs: atypical protein kinases with pleiotropic actions. Physiol Rev 2011, 91:177-219. 10.1152/physrev.00017.2010, 3035565, 21248166.
10. Roos WP, Batista LF, Naumann SC, Wick W, Weller M, Menck CF, Kaina B. Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene 2007, 26:186-197. 10.1038/sj.onc.1209785, 16819506.
11. 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. 10.1016/j.bbadis.2010.07.009, 3529164, 20637866.
12. Arpin M, Chirivino D, Naba A, Zwaenepoel I. Emerging role for ERM proteins in cell adhesion and migration. Cell Adh Migr 2011, 5:199-206. 10.4161/cam.5.2.15081, 3084986, 21343695.
13. Vitari AC, Thastrup J, Rafiqi FH, Deak M, Morrice NA, Karlsson HK, Alessi DR. Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 2006, 397:223-231. 10.1042/BJ20060220, 1479760, 16669787.
14. 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. 10.1073/pnas.1018567108, 3029763, 21220314.
15. Zambrowicz BP, Abuin A, Ramirez-Solis R, Richter LJ, Piggott J, BeltrandelRio H, Buxton EC, Edwards J, Finch RA, Friddle CJ, 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. 10.1073/pnas.2336103100, 283554, 14610273.
16. Zeng G, Gao L, Yu RK. Reduced cell migration, tumor growth and experimental metastasis of rat F-11 cells whose expression of GD3-synthase is suppressed. Int J Cancer 2000, 88:53-57. 10.1002/1097-0215(20001001)88:1<53::AID-IJC8>3.0.CO;2-7, 10962439.
17. Anselmo AN, Earnest S, Chen W, Juang YC, Kim SC, Zhao Y, Cobb MH. WNK1 and OSR1 regulate the Na+, K+, 2Cl- cotransporter in HeLa cells. Proc Natl Acad Sci U S A 2006, 103:10883-10888. 10.1073/pnas.0604607103, 1544143, 16832045.
18. Lenertz LY, Lee BH, Min X, Xu BE, Wedin K, Earnest S, Goldsmith EJ, Cobb MH. Properties of WNK1 and implications for other family members. J Biol Chem 2005, 280:26653-26658. 10.1074/jbc.M502598200, 15883153.
19. 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. 10.1242/jcs.029223, 18843116.
20. Zorniak M, Clark PA, Leeper HE, Tipping MD, Francis DM, Kozak KR, Salamat MS, Kuo JS. Differential expression of 2′,3′-cyclic-nucleotide 3′-phosphodiesterase and neural lineage markers correlate with glioblastoma xenograft infiltration and patient survival. Clin Cancer Res 2012, 18:3628-3636. 10.1158/1078-0432.CCR-12-0339, 3597469, 22589395.
21. Zhang M, Herion TW, Timke C, Han N, Hauser K, Weber KJ, Peschke P, Wirkner U, Lahn M, Huber PE. Trimodal glioblastoma treatment consisting of concurrent radiotherapy, temozolomide, and the novel TGF-beta receptor I kinase inhibitor LY2109761. Neoplasia 2011, 13:537-549. 3114247, 21677877.
22. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D. Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998, 78:247-306.
23. Jakab M, Ritter M. Cell volume regulatory ion transport in the regulation of cell migration. Contrib Nephrol 2006, 152:161-180.
24. Curto M, McClatchey AI. Ezrin..a metastatic detERMinant?. Cancer Cell 2004, 5:113-114. 10.1016/S1535-6108(04)00031-5, 14998486.
25. Khanna C, Wan X, Bose S, Cassaday R, Olomu O, Mendoza A, Yeung C, Gorlick R, Hewitt SM, Helman LJ. The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat Med 2004, 10:182-186. 10.1038/nm982, 14704791.
26. McClatchey AI. Merlin and ERM proteins: unappreciated roles in cancer development?. Nat Rev Cancer 2003, 3:877-883. 10.1038/nrc1213, 14668818.
27. Ivetic A, Ridley AJ. Ezrin/radixin/moesin proteins and Rho GTPase signalling in leucocytes. Immunology 2004, 112:165-176. 10.1111/j.1365-2567.2004.01882.x, 1782489, 15147559.
28. Shiue H, Musch MW, Wang Y, Chang EB, Turner JR. Akt2 phosphorylates ezrin to trigger NHE3 translocation and activation. J Biol Chem 2005, 280:1688-1695. 1237052, 15531580.
29. Dai C, Zhang B, Liu X, Ma S, Yang Y, Yao Y, Feng M, Bao X, Li G, Wang J, et al. Inhibition of PI3K/AKT/mTOR pathway enhances temozolomide-induced cytotoxicity in pituitary adenoma cell lines in vitro and xenografted pituitary adenoma in female nude mice. Endocrinology 2013, 154:1247-1259. 10.1210/en.2012-1908, 23384836.
30. Caporali S, Levati L, Starace G, Ragone G, Bonmassar E, Alvino E, D'Atri S. AKT is activated in an ataxia-telangiectasia and Rad3-related-dependent manner in response to temozolomide and confers protection against drug-induced cell growth inhibition. Mol Pharmacol 2008, 74:173-183. 10.1124/mol.107.044743, 18413665.
31. Caporali S, Levati L, Graziani G, Muzi A, Atzori MG, Bonmassar E, Palmieri G, Ascierto PA, D'Atri S. NF-kappaB is activated in response to temozolomide in an AKT-dependent manner and confers protection against the growth suppressive effect of the drug. J Transl Med 2012, 10:252. 10.1186/1479-5876-10-252, 3551789, 23259744.
32. 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. 10.1074/jbc.M808751200, 2708869, 19363035.
33. Bush PG, Pritchard M, Loqman MY, Damron TA, Hall AC. A key role for membrane transporter NKCC1 in mediating chondrocyte volume increase in the mammalian growth Plate. J Bone Miner Res 2010, 25:1594-1603. 10.1002/jbmr.47, 3154001, 20200963.
34. Ji T, Liu S, Zheng LF, Wang Q, Dou ZF, Zhang Y, Zhu JX. Cellular distribution of NKCC2 in the gastric mucosa and its response to short-term osmotic shock. Cell Tissue Res 2012, 348:155-165. 10.1007/s00441-012-1359-y, 22388656.
35. Thastrup JO, Rafiqi FH, Vitari AC, Pozo-Guisado E, Deak M, Mehellou Y, Alessi DR. 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. 10.1042/BJ20111879, 3242505, 22032326.
36. Ohta A, Rai T, Yui N, Chiga M, Yang SS, Lin SH, Sohara E, Sasaki S, Uchida S. Targeted disruption of the Wnk4 gene decreases phosphorylation of Na-Cl cotransporter, increases Na excretion and lowers blood pressure. Hum Mol Genet 2009, 18:3978-3986. 10.1093/hmg/ddp344, 19633012.
37. Moriguchi T, Urushiyama S, Hisamoto N, Iemura S, Uchida S, Natsume T, Matsumoto K, Shibuya H. WNK1 regulates phosphorylation of cation-chloride-coupled cotransporters via the STE20-related kinases, SPAK and OSR1. J Biol Chem 2005, 280:42685-42693. 10.1074/jbc.M510042200, 16263722.
38. Clark PA, Iida M, Treisman DM, Kalluri H, Ezhilan S, Zorniak M, Wheeler DL, Kuo JS. Activation of multiple ERBB family receptors mediates glioblastoma cancer stem-like cell resistance to EGFR-targeted inhibition. Neoplasia 2012, 14:420-428. 3384429, 22745588.
39. Svendsen CN, ter Borg MG, Armstrong RJ, Rosser AE, Chandran S, Ostenfeld T, Caldwell MA. A new method for the rapid and long term growth of human neural precursor cells. J Neurosci Methods 1998, 85:141-152. 10.1016/S0165-0270(98)00126-5, 9874150.
40. Rocha-Gonzalez HI, Mao S, Alvarez-Leefmans FJ. Na+, K+,2Cl- cotransport and intracellular chloride regulation in rat primary sensory neurons: thermodynamic and kinetic aspects. J Neurophysiol 2008, 100:169-184. 10.1152/jn.01007.2007, 2493498, 18385481.
41. Kiedrowski L. N-methyl-D-aspartate excitotoxicity: relationships among plasma membrane potential, Na(+)/Ca(2+) exchange, mitochondrial Ca(2+) overload, and cytoplasmic concentrations of Ca(2+), H(+), and K(+). Mol Pharmacol 1999, 56:619-632.
42. Su G, Kintner DB, Flagella M, Shull GE, Sun D. Astrocytes from Na(+)-K(+)-Cl(-) cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am J Physiol Cell Physiol 2002, 282:C1147-C1160. 10.1152/ajpcell.00538.2001, 11940530.