Oncogenic KRAS and BRAF activation of the MEK/ERK signaling pathway promotes expression of dual-specificity phosphatase 4 (DUSP4/MKP2) resulting in nuclear ERK1/2 inhibition

Oncogene

Volumn 32, Issue 5, 2013, Pages 564-576

  Cagnol, S ^a   Rivard, N ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

BRAF; colorectal cancer; DUSP; ERK; intestinal epithelial cells; KRAS

Indexed keywords

B RAF KINASE; DUAL SPECIFICITY PHOSPHATASE; DUAL SPECIFICITY PHOSPHATASE 4; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PERVANADATE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CARCINOGENESIS; CELL NUCLEUS; COLORECTAL CANCER; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME INHIBITION; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

CELL LINE; CELL NUCLEUS; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; CYTOPLASM; DUAL-SPECIFICITY PHOSPHATASES; GENES, RAS; HUMANS; INTESTINAL MUCOSA; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; MUTATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS B-RAF; TRANSCRIPTIONAL ACTIVATION;

EID: 84873409839     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.88     Document Type: Article

References (53)

1. Adachi M, Fukuda M, Nishida E. (1999). Two co-existing mechanisms for nuclear import of MAP kinase: passive diffusion of a monomer and active transport of a dimer. EMBO J 18: 5347-5358. (Pubitemid 29465584)
2. Aliaga JC, Deschenes C, Beaulieu JF, Calvo EL, Rivard N. (1999). Requirement of the MAP kinase cascade for cell cycle progression and differentiation of human intestinal cells. Am J Physiol 277: G631-G641. (Pubitemid 29458237)
3. Andreolas C, Kalogeropoulou M, Voulgari A, Pintzas A. (2008). Fra-1 regulates vimentin during Ha-RAS-induced epithelial mesenchymal transition in human colon carcinoma cells. Int J Cancer 122: 1745-1756. (Pubitemid 351413420)
4. Armstrong SP, Caunt CJ, McArdle CA. (2009). Gonadotropinreleasing hormone and protein kinase C signaling to ERK: spatiotemporal regulation of ERK by docking domains and dualspecificity phosphatases. Mol Endocrinol 23: 510-519.
5. Avruch J. (2007). MAP kinase pathways: the first twenty years. Biochim Biophys Acta 1773: 1150-1160. (Pubitemid 47125973)
6. Bergeron S, Lemieux E, Durand V, Cagnol S, Carrier JC, Lussier JG et al. (2010). The serine protease inhibitor serpinE2 is a novel target of ERK signaling involved in human colorectal tumorigenesis. Mol Cancer 9: 271.
7. Brami-Cherrier K, Valjent E, Herve D, Darragh J, Corvol JC, Pages C et al. (2005). Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice. J Neurosci 25: 11444-11454. (Pubitemid 43083716)
8. Brondello JM, Brunet A, Pouyssegur J, McKenzie FR. (1997). The dual specificity mitogen-activated protein kinase phosphatase-1 and -2 are induced by the p42/p44MAPK cascade. J Biol Chem 272: 1368-1376. (Pubitemid 27034642)
9. Brondello JM, Pouyssegur J, McKenzie FR. (1999). Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation. Science 286: 2514-2517.
10. Cagnol S, Van Obberghen-Schilling E, Chambard JC. (2006). Prolonged activation of ERK1, 2 induces FADD-independent caspase 8 activation and cell death. Apoptosis 11: 337-346.
11. Caunt CJ, Armstrong SP, Rivers CA, Norman MR, McArdle CA. (2008a). Spatiotemporal regulation of ERK2 by dual specificity phosphatases. J Biol Chem 283: 26612-26623.
12. Caunt CJ, Finch AR, Sedgley KR, McArdle CA. (2006). Seventransmembrane receptor signalling and ERK compartmentalization. Trends Endocrinol Metab 17: 276-283. (Pubitemid 44287475)
13. Caunt CJ, Rivers CA, Conway-Campbell BL, NormanMR, McArdle CA. (2008b). Epidermal growth factor receptor and protein kinase C signaling to ERK2: spatiotemporal regulation of ERK2 by dual specificity phosphatases. J Biol Chem 283: 6241-6252.
14. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S et al. (2002). Mutations of the BRAF gene in human cancer. Nature 417: 949-954. (Pubitemid 34716871)
15. De Roock W, De Vriendt V, Normanno N, Ciardiello F, Tejpar S. (2011). KRAS, BRAF, PIK3CA, and PTEN mutations: implications for targeted therapies in metastatic colorectal cancer. Lancet Oncol 12: 594-603.
16. Ebisuya M, Kondoh K, Nishida E. (2005). The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity. J Cell Sci 118: 2997-3002. (Pubitemid 41149904)
17. Fang JY, Richardson BC. (2005). The MAPK signalling pathways and colorectal cancer. Lancet Oncol 6: 322-327. (Pubitemid 40590269)
18. Formstecher E, Ramos JW, Fauquet M, Calderwood DA, Hsieh JC, Canton B et al. (2001). PEA-15 mediates cytoplasmic sequestration of ERK MAP kinase. Dev Cell 1: 239-250. (Pubitemid 33653059)
19. Gaedcke J, Grade M, Jung K, Camps J, Jo P, Emons G et al. (2010). Mutated KRAS results in overexpression of DUSP4, a MAP-kinase phosphatase, and SMYD3, a histone methyltransferase, in rectal carcinomas. Genes Chromosomes Cancer 49: 1024-1034.
20. Huyer G, Liu S, Kelly J, Moffat J, Payette P, Kennedy B et al. (1997). Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J Biol Chem 272: 843-851. (Pubitemid 27034572)
21. Ikenoue T, Hikiba Y, Kanai F, Aragaki J, Tanaka Y, Imamura J et al. (2004). Different effects of point mutations within the B-Raf glycine-rich loop in colorectal tumors on mitogen-activated protein/ extracellular signal-regulated kinase kinase/extracellular signalregulated kinase and nuclear factor kappaB pathway and cellular transformation. Cancer Res 64: 3428-3435. (Pubitemid 38657914)
22. Jacobs D, Glossip D, Xing H, Muslin AJ, Kornfeld K. (1999). Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev 13: 163-175. (Pubitemid 29061947)
23. Jeffrey KL, Camps M, Rommel C, Mackay CR. (2007). Targeting dual-specificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat Rev Drug Discov 6: 391-403. (Pubitemid 46705202)
24. Katagiri C, Masuda K, Urano T, Yamashita K, Araki Y, Kikuchi K et al. (2005). Phosphorylation of Ser-446 determines stability of MKP-7. J Biol Chem 280: 14716-14722. (Pubitemid 40562819)
25. Komatsu K, Buchanan FG, Katkuri S, Morrow JD, Inoue H, OtakaM et al. (2005). Oncogenic potential ofMEK1 in rat intestinal epithelial cells is mediated via cyclooxygenase-2. Gastroenterology 129: 577-590. (Pubitemid 41096645)
26. Kondoh K, Nishida E. (2007). Regulation of MAP kinases by MAP kinase phosphatases. Biochim Biophys Acta 1773: 1227-1237. (Pubitemid 47125976)
27. Kucharska A, Rushworth LK, Staples C, Morrice NA, Keyse SM. (2009). Regulation of the inducible nuclear dualspecificity phosphatase DUSP5 by ERK MAPK. Cell Signal 21: 1794-1805.
28. Lemieux E, Bergeron S, Durand V, Asselin C, Saucier C, Rivard N. (2009). Constitutively active MEK1 is sufficient to induce epithelialto- mesenchymal transition in intestinal epithelial cells and to promote tumor invasion and metastasis. Int J Cancer 125: 1575-1586.
29. Lenormand P, Brondello JM, Brunet A, Pouyssegur J. (1998). Growth factor-induced p42/p44 MAPK nuclear translocation and retention requires both MAPK activation and neosynthesis of nuclear anchoring proteins. J Cell Biol 142: 625-633. (Pubitemid 28381483)
30. Lin YW, Yang JL. (2006). Cooperation of ERK and SCFSkp2 for MKP-1 destruction provides a positive feedback regulation of proliferating signaling. J Biol Chem 281: 915-926.
31. Liu J, Suresh Kumar KG, Yu D, Molton SA, McMahon M, HerlynM et al. (2007). Oncogenic BRAF regulates beta-Trcp expression and NF-kappaB activity in human melanoma cells. Oncogene 26: 1954-1958. (Pubitemid 46474640)
32. Malumbres M, Barbacid M. (2003). RAS oncogenes: the first 30 years. Nat Rev Cancer 3: 459-465. (Pubitemid 37328850)
33. Marchetti S, Gimond C, Chambard JC, Touboul T, Roux D, Pouyssegur J et al. (2005). Extracellular signal-regulated kinases phosphorylate mitogen-activated protein kinase phosphatase 3/ DUSP6 at serines 159 and 197, two sites critical for its proteasomal degradation. Mol Cell Biol 25: 854-864. (Pubitemid 40096604)
34. Marshall CJ. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185.
35. Mattison CP, Ota IM. (2000). Two protein tyrosine phosphatases, Ptp2 and Ptp3, modulate the subcellular localization of the Hog1 MAP kinase in yeast. Genes Dev 14: 1229-1235. (Pubitemid 30327503)
36. Murphy LO, Blenis J. (2006). MAPK signal specificity: the right place at the right time. Trends Biochem Sci 31: 268-275. (Pubitemid 43674354)
37. Murphy LO, MacKeigan JP, Blenis J. (2004). A network of immediate early gene products propagates subtle differences in mitogenactivated protein kinase signal amplitude and duration. Mol Cell Biol 24: 144-153. (Pubitemid 38010042)
38. Nagasaka T, Sasamoto H, Notohara K, Cullings HM, Takeda M, Kimura K et al. (2004). Colorectal cancer with mutation in BRAF, KRAS, and wild-type with respect to both oncogenes showing different patterns of DNA methylation. J Clin Oncol 22: 4584-4594. (Pubitemid 41185126)
39. Nandan MO, McConnell BB, Ghaleb AM, Bialkowska AB, Sheng H, Shao J et al. (2008). Kruppel-like factor 5 mediates cellular transformation during oncogenic KRAS-induced intestinal tumorigenesis. Gastroenterology 134: 120-130. (Pubitemid 350309321)
40. Nishimura T. (2008). Total number of genome alterations in sporadic gastrointestinal cancer inferred from pooled analyses in the literature. Tumour Biol 29: 343-350.
41. Owens DM, Keyse SM. (2007). Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26: 3203-3213. (Pubitemid 46763015)
42. Peng DJ, Zhou JY, Wu GS. (2010). Post-translational regulation of mitogen-activated protein kinase phosphatase-2 (MKP-2) by ERK. Cell Cycle 9: 4650-4655.
43. Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE. (2002). Tumorigenesis: RAF/RAS oncogenes and mismatch-repair status. Nature 418: 934. (Pubitemid 34976022)
44. Ramos JW. (2008). The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int J Biochem Cell Biol 40: 2707-2719.
45. Simoneau M, Coulombe G, Vandal G, Vezina A, Rivard N. (2011). SHP-1 inhibits beta-catenin function by inducing its degradation and interfering with its association with TATA-binding protein. Cell Signal 23: 269-279.
46. Smakman N, Borel Rinkes IH, Voest EE, Kranenburg O. (2005). Control of colorectal metastasis formation by K-Ras. Biochim Biophys Acta 1756: 103-114. (Pubitemid 41773137)
47. Smith ER, Smedberg JL, Rula ME, Xu XX. (2004). Regulation of Ras-MAPK pathway mitogenic activity by restricting nuclear entry of activated MAPK in endoderm differentiation of embryonic carcinoma and stem cells. J Cell Biol 164: 689-699. (Pubitemid 38282953)
48. Vakiani E, Solit DB. (2011). KRAS and BRAF: drug targets and predictive biomarkers. J Pathol 223: 219-229.
49. Vial E, Marshall CJ. (2003). Elevated ERK-MAP kinase activity protects the FOS family member FRA-1 against proteasomal degradation in colon carcinoma cells. J Cell Sci 116: 4957-4963. (Pubitemid 38016702)
50. Voisin L, Julien C, Duhamel S, Gopalbhai K, Claveau I, Saba-El-Leil MK et al. (2008). Activation ofMEK1 orMEK2 isoform is sufficient to fully transform intestinal epithelial cells and induce the formation of metastatic tumors. BMC Cancer 8: 337.
51. Volmat V, Camps M, Arkinstall S, Pouyssegur J, Lenormand P. (2001). The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. J Cell Sci 114: 3433-3443. (Pubitemid 33019760)
52. Yeh JJ, Routh ED, Rubinas T, Peacock J, Martin TD, Shen XJ et al. (2009). KRAS/BRAF mutation status and ERK1/2 activation as biomarkers for MEK1/2 inhibitor therapy in colorectal cancer. Mol Cancer Ther 8: 834-843.
53. Yuen ST, Davies H, Chan TL, Ho JW, Bignell GR, Cox C et al. (2002). Similarity of the phenotypic patterns associated with BRAF and KRAS mutations in colorectal neoplasia. Cancer Res 62: 6451-6455. (Pubitemid 35364105)