Emerging roles for WNK kinases in cancer

Cellular and Molecular Life Sciences

Volumn 67, Issue 8, 2010, Pages 1265-1276

  Moniz, Sónia ^a   Jordan, Peter ^a  

^a NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

Author keywords

Apoptosis; Cell proliferation; Signal transduction; Tumorigenesis; Wnk protein kinases

Indexed keywords

PROTEIN KINASE; PROTEIN KINASE WNK; PROTEIN KINASE WNK1; PROTEIN KINASE WNK2; PROTEIN KINASE WNK3; PROTEIN KINASE WNK4; UNCLASSIFIED DRUG; PROTEIN SERINE THREONINE KINASE; WNK3 PROTEIN, HUMAN;

ADAPTATION; APOPTOSIS; CANCER INVASION; CARCINOGENESIS; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL METABOLISM; CELL PROLIFERATION; GENE MUTATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; NONHUMAN; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; TUMOR CELL; AMINO ACID SEQUENCE; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; NEOPLASM; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 77950604823     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0261-6     Document Type: Review

References (114)

1. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298: 1912-1934 (Pubitemid 35425239)
2. Kostich M, English J, Madison V, Gheyas F, Wang L, Qiu P, Greene J, Laz TM (2002) Human members of the eukaryotic protein kinase family. Genome Biol 3, RESEARCH0043
3. Hanks SK (2003) Genomic analysis of the eukaryotic protein kinase superfamily: a perspective. Genome Biol 4: 111.1-111.7
4. Hanks SK, Hunter T (1995) The eucaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9: 576-596
5. Xu BE, English JM, Wilsbacher JL, Stippec S, Goldsmith EJ, Cobb MH (2000) WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain IL J Biol Chem 275: 16795-16801
6. Veríssimo F, Jordan P (2001) WNK kinases, a novel protein kinase subfamily in multi-cellular organisms. Oncogene 20: 5562-5569 (Pubitemid 32889495)
7. Min X, Lee BH, Cobb MH, Goldsmith EJ (2004) Crystal structure of the kinase domain of WNK1, a kinase that causes a hereditary form of hypertension. Structure 12: 1303-1311 (Pubitemid 38900772)
8. Nakamichi N, Murakami-Kojima M, Sato E, Kishi Y, Yamashino T, Mizuno T (2002) Compilation and characterization of a novel WNK family of protein kinases in Arabiodpsis thaliana with reference to circadian rhythms. Biosci Biotechnol Biochem 66: 2429-2436
9. Xu BE, Min X, Stippec S, Lee BH, Goldsmith EJ, Cobb MH (2002) Regulation of WNK1 by an autoinhibitory domain and autophosphorylation. J Biol Chem 277: 48456-48462 (Pubitemid 35470804)
10. Zagórska A, Pozo-Guisado E, Boudeau J, Vitari AC, Rafiqi FH, Thastrup J, Deak M, Campbell DG, Morrice NA, Prescott AR, Alessi DR (2007) Regulation of activity and localization of the WNK1 protein kinase by hyperosmotic stress. J Cell Biol 176: 89-100 (Pubitemid 46041683)
11. Wang Z, Yang CL, Ellison DH (2004) Comparison of WNK4 and WNK1 kinase and inhibiting activities. Biochem Biophys Res Commun 317: 939-944 (Pubitemid 38481462)
12. Kay BK, Williamson MP, Sudol M (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14: 231-241
13. Xu BE, Lee BH, Min X, Lenertz L, Heise CJ, Stippec S, Goldsmith EJ, Cobb MH (2005) WNK1: analysis of protein kinase structure, downstream targets, and potential roles in hypertension. Cell Res 15: 6-10 (Pubitemid 41653957)
14. Dhillon AS, Hagan S, Rath O, Kolch W (2007) MAP kinase signalling pathways in cancer. Oncogene 26: 3279-3290 (Pubitemid 46763021)
15. Xu BE, Stippec S, Lenertz L, Lee B-H, Zhang W, Lee YK, Cobb MH (2004) WNK1 activates ERK5 by an MEKK2/3-dependent mechanism. J Biol Chem 279: 7826-7831 (Pubitemid 38294668)
16. Sun X, Gao L, Yu RK, Zeng G (2006) Down-regulation of WNK1 protein kinase in neural progenitor cells suppresses cell proliferation and migration. J Neurochem 99: 1114-1121 (Pubitemid 44655277)
17. Moniz S, Veríssimo F, Matos P, Brazão R, Silva E, Kotelevets L, Chastre E, Gespach C, Jordan P (2007) Protein kinase WNK2 inhibits cell proliferation by negatively modulating the activation of MEK1/ERK1/2. Oncogene 26: 6071-6081 (Pubitemid 47373812)
18. Hong C, Moorefield KS, Jun P, Aldape KD, Kharbanda S, Phillips HS, Costello JF (2007) Epigenome scans and cancer genome sequencing converge on WNK2, a kinase-independent suppressor of cell growth. Proc Natl Acad Sci USA 104: 10974-10979 (Pubitemid 47175211)
19. Jun P, Hong C, Lal A, Wong JM, McDermott MW, Bollen AW, Plass C, Held WA, Smiraglia DJ, Costello JF (2009) Epigenetic silencing of the kinase tumor suppressor WNK2 is tumor-type and tumor-grade specific. Neuro Oncol 11: 414-422
20. Moniz S, Matos P, Jordan P (2008) WNK2 modulates MEK1 activity through the Rho GTPase pathway. Cell Signal 20: 1762-1768
21. Shaharabany M, Holtzman EJ, Mayan H, Hirschberg K, Seger R, Farfel Z (2008) Distinct pathways for the involvement of WNK4 in the signaling of hypertonicity and EGF. FEBS J 275: 1631-1642 (Pubitemid 351467582)
22. Lenertz LY, Lee BH, Min X, Xu BE, Wedin K, Earnest S, Goldsmith EJ, Cobb MH (2005) Properties of WNK1 and implications for other family members. J Biol Chem 280: 26653-26658 (Pubitemid 41040697)
23. Yang CL, Zhu X, Wang Z, Subramanya AR, Ellison DH (2005) Mechanisms of WNK1 and WNK4 interaction in the regulation of thiazide-sensitive NaCl cotransport. J Clin Invest 115: 1379-1387 (Pubitemid 40629058)
24. Dan I, Watanabe NM, Kusumi A (2001) The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol 11: 220-230 (Pubitemid 32367879)
25. Strange K, Denton J, Nehrke K (2006) Ste20-type kinases: evolutionarily conserved regulators of ion transport and cell volume. Physiology (Bathesda) 21: 61-68 (Pubitemid 43752518)
26. Johnston AM, Naselli G, Gonez LJ, Martin RM, Harrison LC, Deaizpurua HJ (2000) SPAK, a Ste20/SPS1-related kinase that activates the p38 pathway. Oncogene 19: 4290-4297
27. Polek TC, Talpaz M, Spivak-Kroizman T (2006) The TNF receptor, RELT, binds SPAK and uses it to mediate p38 and JNK activation. Biochem Biophys Res Commun 343: 125-134
28. Yan Y, Nguyen H, Dalmasso G, Sitaraman SV, Merlin D (2007) Cloning and characterization of a new intestinal inflammationassociated colonic epithelial Ste20-related protein kinase isoform. Biochim Biophys Acta 1769: 106-116 (Pubitemid 46341448)
29. Solomon A, Bandhakavi S, Jabbar S, Shah R, Beitel GJ, Morimoto RI (2004) Caenorhabditis elegans OSR-1 regulates behavioral and physiological responses to hyperosmotic environments. Genetics 167: 161-170
30. 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 (Pubitemid 41445471)
31. Moriguchi T, Urushiyama S, Hisamoto N, Iemura S, Uchida S, Natsume T, Matsumoto K, Shibuya H (2005) WNK1 regulates phosphorylation of cation-chloride-coupled cotransporters via the STE20-related kinases, SPAK and OSR1. J Biol Chem 280: 42685-42693 (Pubitemid 43049227)
32. - cotransporter in HeLa cells. Proc Natl Acad Sci USA 103: 10883-10888
33. Gagnon KB, England R, Delpire E (2006) Volume sensitivity of cation-chloride cotransporters is modulated by the interaction of two kinases: SPAK and WNK4. Am J Physiol Cell Physiol 290: C134-C142
34. Vitari AC, Thastrup J, Rafiqi FH, Deak M, Morrice NA, Karlsson HK, Alessi DR (2006) Functional interactions of the SPAK/OSR1 kinases with their upstream activator WNK1 and downstream substrate NKCC1. Biochem J 397: 223-231 (Pubitemid 44032854)
35. - cotransporter by the WNKregulated kinases SPAK and OSR1. J Cell Sci 121: 675-684
36. Ponce-Coria J, San-Cristobal P, Kahle KT, Vazquez N, Pacheco-Alvarez D, de Los Heros P, Juárez P, Muñoz E, Michel G, Bobadilla NA, Gimenez I, Lifton RP, Hebert SC, Gamba G (2008) Regulation of NKCC2 by a chloride-sensing mechanism involving the WNK3 and SPAK kinases. Proc Natl Acad Sci USA 105: 8458-8463 (Pubitemid 351904778)
37. Frost JA, Steen H, Shapiro P, Lewis T, Ahn N, Shaw PE, Cobb MH (1997) Cross-cascade activation of ERKs and ternary complex factors by Rho family proteins. EMBO J 16: 6426-6438 (Pubitemid 27483269)
38. Coles LC, Shaw PE (2002) PAK1 primes MEK1 for phosphorylation by Raf-1 kinase during cross-cascade activation of the ERK pathway. Oncogene 21: 2236-2244
39. Eblen ST, Slack JK, Weber MJ, Catling AD (2002) Rac-PAK signaling stimulates extracellular signal-regulated kinase (ERK) activation by regulating formation of MEK1-ERK complexes. Mol Cell Biol 22: 6023-6033
40. Slack-Davis JK, Eblen ST, Zecevic M, Boerner SA, Tarcsafalvi A, Diaz HB, Marshall MS, Weber MJ, Parsons JT, Catling AD (2003) PAK1 phosphorylation of MEK1 regulates fibronectinstimulated MAPK activation. J Cell Biol 162: 281-291 (Pubitemid 36928841)
41. Park ER, Eblen ST, Cading AD (2007) MEK1 activation by PAK: a novel mechanism. Cell Signal 19: 1488-1496
42. Sorkin A, von Zastrow M (2002) Signal transduction and endocytosis: close encounters of many kinds. Nat Rev Mol Cell Biol 3: 600-614
43. González-Gaitán M (2003) Signal dispersal and transduction through the endocytic pathway. Nat Rev Mol Cell Biol 4: 213-224 (Pubitemid 36288043)
44. Cai H, Cebotaru V, Wang YH, Zhang XM, Cebotaru L, Guggino SE, Guggino WB (2006) WNK4 kinase regulates surface expression of the human sodium chloride cotransporter in mammalian cells. Kidney Int 69: 2162-2170 (Pubitemid 43882102)
45. Subramanya AR, Liu J, Ellison DH, Wade JB, Welling PA (2009) WNK4 diverts the thiazide-sensitive NaCl cotransporter to the lysosome and stimulates AP-3 interaction. J Biol Chem 284: 18471-18480
46. + secretion. Nat Genet 35: 372-376
47. Cope G, Murthy M, Golbang AP, Hamad A, Liu CH, Cuthbert AW, O'Shaughnessy KM (2006) WNK1 affects surface expression of die ROMK potassium channel independent of WNK4. J Am Soc Nephrol 17: 1867-1874 (Pubitemid 44036171)
48. He G, Wang HR, Huang SK, Huang CL (2007) Intersectin links WNK kinases to endocytosis of ROMK1. J Clin Invest 117: 1078-1087 (Pubitemid 46556764)
49. Pelkmans L, Fava E, Grabner H, Hannus M, Habermann B, Krausz E, Zerial M (2005) Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436: 78-86 (Pubitemid 40966188)
50. Pollak M (2008) Insulin and insulin-like growth factor signalling in neoplasia. Nat Rev Cancer 8: 915-928
51. Vitari AC, Deak M, Collins BJ, Morrice N, Prescott AR, Phelan A, Humphreys S, Alessi DR (2004) WNK1, the kinase mutated in an inherited high-blood-pressure syndrome, is a novel PKB (protein kinase B)/Akt substrate. Biochem J 378: 257-268 (Pubitemid 38299565)
52. Jiang ZY, Zhou QL, Holik J, Patel S, Leszyk J, Coleman K, Chouinard M, Czech MP (2005) Identification of WNK1 as a substrate of Akt/protein kinase B and a negative regulator of insulin-stimulated mitogenesis in 3T3-L1 cells. J Biol Chem 280: 21622-21628 (Pubitemid 40805731)
53. Xu BE, Stippec S, Chu PY, Lazrak A, Li XJ, Lee BH, English JM, Ortega B, Huang CL, Cobb MH (2005) WNK1 activates SGK1 to regulate the epithelial sodium channel. Proc Natl Acad Sci USA 102: 10315-10320 (Pubitemid 41023368)
54. Xu BE, Stippec S, Lazrak A, Huang CL, Cobb MH (2005) WNK1 activates SGK1 by a phosphatidylinositol 3-kinasedependent and non-catalytic mechanism. J Biol Chem 280: 34218-34223 (Pubitemid 41443147)
55. Sale EM, Hodgkinson CP, Jones NP, Sale GJ (2006) A new strategy for studying protein kinase B and its three isoforms. Role of protein kinase B in phosphorylating glycogen synthase kinase-3, tuberin, WNK1, and ATP citrate lyase. Biochemistry 45: 213-223
56. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM (2008) mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell 30: 701-711 (Pubitemid 351815130)
57. Massagué J, Blain SW, Lo RS (2000) TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103: 295-309
58. Lee BH, Chen W, Stippec S, Cobb MH (2007) Biological crosstalk between WNK1 and the transforming growth factor beta-Smad signaling pathway. J Biol Chem 282: 17985-17996 (Pubitemid 47100246)
59. Barrios-Rodiles M, Brown KR, Ozdamar B, Bose R, Liu Z, Donovan RS, Shinjo F, Liu Y, Dembowy J, Taylor IW, Luga V, Przulj N, Robinson M, Suzuki H, Hayashizaki Y, Jurisica I, Wrana JL (2005) High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307: 1621-1625 (Pubitemid 40354744)
60. 2+ transport. Nat Rev Cancer 7: 519-530
61. 2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat Rev Cancer 8: 361-375
62. Prevarskaya N, Zhang L, Barritt G (2007) TRP channels in cancer. Biochem Biophys Acta 1772: 937-946
63. Jiang Y, Ferguson WB, Peng JB (2007) 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 292: F545-F554 (Pubitemid 46220521)
64. Zhang W, Na T, Peng JB (2008) WNK3 positively regulates epithelial calcium channels TRPV5 and TRPV6 via a kinase-dependent pathway. Am J Physiol Renal Physiol 295: F1472-F1484
65. Fu Y, Subramanya A, Rozansky D, Cohen DM (2006) WNK kinases influence TRPV4 channel function and localization. Am J Physiol Renal Physiol 290: F1305-F1314 (Pubitemid 43830754)
66. Gatenby RA, Gillies RJ (2008) A microenvironmental model of carcinogenesis. Nat Rev Cancer 8: 56-61
67. Denko NC (2008) Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 8: 705-713
68. Macheda ML, Rogers S, Best JD (2005) Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 202: 654-662 (Pubitemid 40175840)
69. Thurmond DC, Pessin JE (2001) Molecular machinery involved in the insulin-regulated fusion of GLUT4-containing vesicles with the plasma membrane. Mol Membr Biol 18: 237-245
70. Oh E, Heise CJ, English JM, Cobb MH, Thurmond DC (2007) WNK1 is a novel regulator of Munc18c-syntaxin 4 complex formation in SNARE-mediated vesicle exocytosis. J Biol Chem 282: 32613-32622
71. Song J, Hu X, Riazi S, Tiwari S, Wade JB, Ecelbarger CA (2006) Regulation of blood pressure, the epithelial sodium channel (ENaC), and other key renal sodium transporters by chronic insulin infusion in rats. Am J Physiol Renal Physiol 290: F1055-F1064 (Pubitemid 43724904)
72. Lee BH, Min X, Heise CJ, Xu BE, Chen S, Shu H, Luby-Phelps K, Goldsmith EJ, Cobb MH (2004) WNK1 phosphorylates synaptotagmin 2 and modulates its membrane binding. Mol Cell 15: 741-751 (Pubitemid 39194904)
73. Wilson FH, Disse-Nicodeme S, Choate KA, Ishikawa K, Nelson-Williams C, Desitter I, Gunel M, Milford DV, Lipkin GW, Achard JM, Feely MP, Dussol B, Berland Y, Unwin RJ, Mayan H, Simon DB, Farfel Z, Jeunemaitre X, Lifton RP (2001) Human hypertension caused by mutations in WNK kinases. Science 293: 1107-1112 (Pubitemid 32758085)
74. Kahle KT, Wilson FH, Lalioti M, Toka H, Qin H, Lifton RP (2004) WNK kinases: molecular regulators of integrated epithelial ion transport. Curr Opin Nephrol Hypertens 13: 557-562 (Pubitemid 39150083)
75. Gamba G (2005) Role of WNK kinases in regulating tubular salt and potassium transport and in the development of hypertension. Am J Physiol Renal Physiol 288: F245-F252
76. Kahle KT, Rinehart J, Ring A, Gimenez I, Gamba G, Hebert SC, Lifton RP (2006) WNK protein kinases modulate cellular Clflux by altering the phosphorylation state of the Na-K-Cl and K-Cl cotransporters. Physiology (Bethesda) 21: 326-335 (Pubitemid 44511760)
77. Kahle KT, Ring AM, Lifton RP (2008) Molecular physiology of the WNK kinases. Annu Rev Physiol 70: 329-355
78. + exchanger in metastasis. Nat Rev Cancer 5: 786-795
79. - flux in extrarenal epithelia. Proc Natl Acad Sci USA 101: 2064-2069
80. Dorwart MR, Sahcheynikov N, Wang Y, Stippec S, Muallem S (2007) SLC26A9 is a Cl(-) channel regulated by the WNK kinases. J Physiol 584: 333-345 (Pubitemid 47504877)
81. Kunzelmann K (2005) Ion channels and cancer. J Membr Biol 205: 159-173
82. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659
83. Igney FH, Krammer P (2002) Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2: 277-288
84. Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I (2006) Bistability in apoptosis: roles of bax, bc1-2, and mitochondrial permeability transition pores. Biophys J 90: 1546-1559
85. Dogu Y, Díaz J (2009) Mathematical model of a network of interaction between p53 and Bc1-2 during genotoxic-induced apoptosis. Biophys Chem 143: 44-54
86. Veríssimo F, Silva E, Morris JD, Pepperkok R, Jordan P (2006) Protein kinase WNK3 increases cell survival in a caspase 3-dependent pathway. Oncogene 25: 4172-4182 (Pubitemid 44079451)
87. MacKeigan JP, Murphy LO, Blenis J (2005) Sensitized RNAi screen of human kinases and phosphatases identifies new regulators of apoptosis and chemoresistance. Nat Cell Biol 7: 591-600
88. Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, Koch B, Haas SA, Paro R, Perrimon N (2004) Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303: 832-835
89. Choe K, Strange K (2007) Evolutionarily conserved WNK and Ste20 kinases are essential for acute volume recovery and survival following hypertonic shrinkage in Caenorhabditis elegans. Am J Physiol Cell Physiol 293: C915-C927 (Pubitemid 47437372)
90. Delpire E, Gagnon KB (2008) SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem J 409: 321-331 (Pubitemid 351184951)
91. Richardson C, Alessi DR (2008) The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signalling pathway. J Cell Sci 121: 3293-3304
92. Thiery JP (2003) Epithelial-mesenchymal transitions in development and pathologies. Curr Opin Cell Biol 15: 740-746
93. Padua D, Massagué J (2009) Roles of TGFβ in metastasis. Cell Res 19: 89-102
94. Thuault S, Tan EJ, Peinado H, Cano A, Heldin CH, Moustakas A (2008) HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J Biol Chem 283: 33437-33446
95. Zeng G, Gao L, Yu RK (2000) Reduced cell migration, tumor growth and experimental metastasis of rat F-11 cells whose expression of ganglioside GD3 was suppressed. Int J Cancer 88: 53-57
96. Zeng G, Gao L, Xia T, Gu Y, Yu RK (2005) Expression of the mouse WNK1 gene in correlation with ganglioside GD3 and functional analysis of the mouse WNK1 promoter. Gene 344: 233-239 (Pubitemid 40126809)
97. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302: 1704-1709 (Pubitemid 37505725)
98. Zhang Z, Xu X, Zhang Y, Zhou J, Yu Z, He C (2009) LINGO-1 interacts with WNK1 to regulate Nogo-induced inhibition of neurite extension. J Biol Chem 284: 15717-15728
99. Ekstrand AJ, James CD, Cavenee WK, Seliger B, Pettersson RF, Collins VP (1991) Genes for epidermal growth factor receptor, transforming growth factor a, and epidermal growth f actor and their expression in human gliomas in vivo. Cancer Res 51: 2164-2172
100. Scanlan MJ, Chen YT, Williamson B, Gure AO, Stockert E, Gordan JD, Türeci O, Sahin U, Pfreundschuh M, Old LJ (1998) Characterization of human colon cancer antigens recognized by autologous antibodies. Int J Cancer 76: 652-658 (Pubitemid 28243936)
101. Ito M, Shichijo S, Tsuda N, Ochi M, Harashima N, Saito N, Itoh K (2001) Molecular basis of T cell-mediated recognition of pancreatic cancer cells. Cancer Res 61: 2038-2046 (Pubitemid 32692025)
102. Delaloy C, Lu J, Houot AM, Disse-Nicodeme S, Gase JM, Corvol P, Jeunemaitre X (2003) Multiple promoters in the WNK1 gene: one controls expression of a kidney-specific kinase-defective isoform. Mol Cell Biol 23: 9208-9221 (Pubitemid 37499808)
103. Holden S, Cox J, Raymond FL (2004) Cloning, genomic organization, alternative splicing and expression analysis of the human gene WNK3 (PRKWNK3). Gene 335: 109-119 (Pubitemid 38759757)
104. Schwerk C, Schulze-Osthoff K (2005) Regulation of apoptosis by alternative pre-mRNA splicing. Mol Cell 19: 1-13 (Pubitemid 40884653)
105. Venables JP (2006) Unbalanced alternative splicing and its significance in cancer. BioEssays 28: 378-386
106. Srebrow A, Kornblihtt AR (2006) The connection between splicing and cancer. J Cell Sci 119: 2635-2641
107. Glover M, Zuber AM, O'Shaughnessy KM (2009) Renal and brain isoforms of WNK3 have opposite effects on NCCT expression. J Am Soc Nephrol 20: 1314-1322
108. Davies H, Hunter C, Smith R, Stephens P, Greenman C, Bignell G, Teague J, Butler A, Edkins S, Stevens C, Parker A, O'Meara S, Avis T, Barthorpe S, Brackenbury L, Buck G, Clements J, Cole J, Dicks E, Edwards K, Forbes S, Gorton M, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jones D, Kosmidou V, Laman R, Lugg R, Menzies A, Perry J, Petty R, Raine K, Shepherd R, Small A, Solomon H, Stephens Y, Tofts C, Varian J, Webb A, West S, Widaa S, Yates A, Brasseur F, Cooper CS, Flanagan AM, Green A, Knowles M, Leung SY, Looijenga LH, Malkowicz B, Pierotti MA, Teh BT, Yuen ST, Lakhani SR, Easton DF, Weber BL, Goldstraw P, Nicholson AG, Wooster R, Stratton MR, Futreal PA (2005) Somatic mutations of the protein kinase gene family in human lung cancer. Cancer Res 65: 7591-7595 (Pubitemid 41297230)
109. Stephens P, Edkins S, Davies H, Greenman C, Cox C, Hunter C, Bignell G, Teague J, Smith R, Stevens C, O'Meara S, Parker A, Tarpey P, Avis T, Barthorpe A, Brackenbury L, Buck G, Butler A, Clements J, Cole J, Dicks E, Edwards K, Forbes S, Gorton M, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jones D, Kosmidou V, Laman R, Lugg R, Menzies A, Perry J, Petty R, Raine K, Shepherd R, Small A, Solomon H, Stephens Y, Tofts C, Varian J, Webb A, West S, Widaa S, Yates A, Brasseur F, Cooper CS, Flanagan AM, Green A, Knowles M, Leung SY, Looijenga LH, Malkowicz B, Pierotti MA, Teh B, Yuen ST, Nicholson AG, Lakhani S, Easton DF, Weber BL, Stratton MR, Futreal PA, Wooster R (2005) A screen of the complete protein kinase gene family identifies diverse patterns of somatic mutations in human breast cancer. Nat Genet 37: 590-592 (Pubitemid 40770413)
110. Sjöblom T, Jones S, Wood LD, Parsons DW, Lin J, Barber TD, Mandelker D, Leary RJ, Ptak J, Silliman N, Szabo S, Buckhaults P, Farrell C, Meeh P, Markowitz SD, Willis J, Dawson D, Willson JK, Gazdar AF, Hartigan J, Wu L, Liu C, Parmigiani G, Park BH, Bachman KE, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE (2006) The consensus coding sequences of human breast and colorectal cancers. Science 314: 268-274 (Pubitemid 44571966)
111. Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C, Bignell G, Davies H, Teague J, Butler A, Stevens C, Edkins S, O'Meara S, Vastrik I, Schmidt EE, Avis T, Barthorpe S, Bhamra G, Buck G, Choudhury B, Clements J, Cole J, Dicks E, Forbes S, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jenkinson A, Jones D, Menzies A, Mironenko T, Perry J, Raine K, Richardson D, Shepherd R, Small A, Tofts C, Varian J, Webb T, West S, Widaa S, Yates A, Cahill DP, Louis DN, Goldstraw P, Nicholson AG, Brasseur F, Looijenga L, Weber BL, Chiew YE, DeFazio A, Greaves MF, Green AR, Campbell P, Birney E, Easton DF, Chenevix-Trench G, Tan MH, Khoo SK, Teh BT, Yuen ST, Leung SY, Wooster R, Futreal PA, Stratton MR (2007) Patterns of somatic mutation in human cancer genomes. Nature 446: 153-158 (Pubitemid 46398669)
112. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA Jr, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321: 1807-1812
113. --transporting epithelia. Proc Natl Acad Sci USA 100: 663-668
114. - cotransporters required for normal blood pressure homeostasis. Proc Natl Acad Sci USA 102: 16777-16782