MEK-1 activates C-Raf through a Ras-independent mechanism

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 5, 2013, Pages 976-986

  Leicht, Deborah T ^a   Balan, Vitaly ^a   Zhu, Jun ^b   Kaplun, Alexander ^a   Bronisz, Agnieszka ^b   Rana, Ajay ^b,c   Tzivion, Guri ^a,b,d  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEXAS A AND M UNIVERSITY SYSTEM   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

ERK; MAPK; MEK; Phosphorylation; Raf; Ras

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; RAF PROTEIN;

ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VIVO STUDY; PHOSPHORYLATION; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; CELL DIVISION; CERCOPITHECUS AETHIOPS; COS CELLS; DOWN-REGULATION; HUMANS; MAP KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-RAF; PROTO-ONCOGENE PROTEINS P21(RAS);

EID: 84874361241     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.01.015     Document Type: Article

References (70)

1. Leicht D.T., Balan V., Kaplun A., Singh-Gupta V., Kaplun L., Dobson M., Tzivion G. Raf kinases: function, regulation and role in human cancer. Biochim. Biophys. Acta 2007, 1773:1196-1212.
2. Roskoski R. RAF protein-serine/threonine kinases: structure and regulation. Biochem. Biophys. Res. Commun. 2010, 399:313-317.
3. Udell C.M., Rajakulendran T., Sicheri F., Therrien M. Mechanistic principles of RAF kinase signaling. Cell. Mol. Life Sci. 2011, 68:553-565.
4. Matallanas D., Birtwistle M., Romano D., Zebisch A., Rauch J., von Kriegsheim A., Kolch W. Raf family kinases: old dogs have learned new tricks. Genes Cancer 2011, 2:232-260.
5. Avruch J., Zhang X.F., Kyriakis J.M. Raf meets Ras: completing the framework of a signal transduction pathway. Trends Biochem. Sci. 1994, 19:279-283.
6. Avruch J. MAP kinase pathways: the first twenty years. Biochim. Biophys. Acta 2007, 1773:1150-1160.
7. Shaul Y.D., Seger R. The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim. Biophys. Acta 2007, 1773:1213-1226.
8. Katz M., Amit I., Yarden Y. Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim. Biophys. Acta 2007, 1773:1161-1176.
9. Beeram M., Patnaik A., Rowinsky E.K. Raf: a strategic target for therapeutic development against cancer. J. Clin. Oncol. 2005, 23:6771-6790.
10. Sridhar S.S., Hedley D., Siu L.L. Raf kinase as a target for anticancer therapeutics. Mol. Cancer Ther. 2005, 4:677-685.
11. Roberts P.J., Der C.J. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007, 26:3291-3310.
12. Luo Z., Diaz B., Marshall M.S., Avruch J. An intact Raf zinc finger is required for optimal binding to processed Ras and for Ras-dependent Raf activation in situ. Mol. Cell. Biol. 1997, 17:46-53.
13. Zhang X.F., Settleman J., Kyriakis J.M., Takeuchi-Suzuki E., Elledge S.J., Marshall M.S., Bruder J.T., Rapp U.R., Avruch J. Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1. Nature 1993, 364:308-313.
14. Brtva T.R., Drugan J.K., Ghosh S., Terrell R.S., Campbell-Burk S., Bell R.M., Der C.J. Two distinct Raf domains mediate interaction with Ras. J. Biol. Chem. 1995, 270:9809-9812.
15. Tzivion G., Luo Z., Avruch J. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature 1998, 394:88-92.
16. Tzivion G., Avruch J. 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation. J. Biol. Chem. 2002, 277:3061-3064.
17. Tzivion G., Shen Y.H., Zhu J. 14-3-3 proteins; bringing new definitions to scaffolding. Oncogene 2001, 20:6331-6338.
18. Zhu J., Balan V., Bronisz A., Balan K., Sun H., Leicht D.T., Luo Z., Qin J., Avruch J., Tzivion G. Identification of Raf-1S471 as a novel phosphorylation site critical for Raf-1 and B-Raf kinase activities and for MEK binding. Mol. Biol. Cell 2005, 16:4733-4744.
19. King A.J., Sun H., Diaz B., Barnard D., Miao W., Bagrodia S., Marshall M.S. The protein kinase Pak3 positively regulates Raf-1 activity through phosphorylation of serine 338. Nature 1998, 396:180-183.
20. Yip-Schneider M.T., Miao W., Lin A., Barnard D.S., Tzivion G., Marshall M.S. Regulation of the Raf-1 kinase domain by phosphorylation and 14-3-3 association. Biochem. J. 2000, 351:151-159.
21. Ishikawa F., Sakai R., Ochiai M., Takaku F., Sugimura T., Nagao M. Identification of a transforming activity suppressing sequence in the c-Raf oncogene. Oncogene 1988, 3:653-658.
22. Stanton V.P., Nichols D.W., Laudano A.P., Cooper G.M. Definition of the human raf amino-terminal regulatory region by deletion mutagenesis. Mol. Cell. Biol. 1989, 9:639-647.
23. Whitehurst C.E., Owaki H., Bruder J.T., Rapp U.R., Geppert T.D. The MEK kinase activity of the catalytic domain of RAF-1 is regulated independently of Ras binding in T cells. J. Biol. Chem. 1995, 270:5594-5599.
24. Chong H., Guan K.L. Regulation of Raf through phosphorylation and N terminus-C terminus interaction. J. Biol. Chem. 2003, 278:36269-36276.
25. Tran N.H., Frost J.A. Phosphorylation of Raf-1 by p21-activated kinase 1 and Src regulates Raf-1 autoinhibition. J. Biol. Chem. 2003, 278:11221-11226.
26. Sozeri O., Vollmer K., Liyanage M., Frith D., Kour G., Mark G.E., Stabel S. Activation of the c-Raf protein kinase by protein kinase C phosphorylation. Oncogene 1992, 7:2259-2262.
27. Kolch W., Heidecker G., Kochs G., Hummel R., Vahidi H., Mischak H., Finkenzeller G., Marme D., Rapp U.R. Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature 1993, 364:249-252.
28. Marais R., Light Y., Mason C., Paterson H., Olson M.F., Marshall C.J. Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 1998, 280:109-112.
29. Barnard D., Diaz B., Clawson D., Marshall M. Oncogenes, growth factors and phorbol esters regulate Raf-1 through common mechanisms. Oncogene 1998, 17:1539-1547.
30. Anderson N.G., Li P., Marsden L.A., Williams N., Roberts T.M., Sturgill T.W. Raf-1 is a potential substrate for mitogen-activated protein kinase in vivo. Biochem. J. 1991, 277(Pt. 2):573-576.
31. Kyriakis J.M., Force T.L., Rapp U.R., Bonventre J.V., Avruch J. Mitogen regulation of c-Raf-1 protein kinase activity toward mitogen-activated protein kinase-kinase. J. Biol. Chem. 1993, 268:16009-16019.
32. Kyriakis J.M., App H., Zhang X.F., Banerjee P., Brautigan D.L., Rapp U.R., Avruch J. Raf-1 activates MAP kinase-kinase. Nature 1992, 358:417-421.
33. Dougherty M.K., Muller J., Ritt D.A., Zhou M., Zhou X.Z., Copeland T.D., Conrads T.P., Veenstra T.D., Lu K.P., Morrison D.K. Regulation of Raf-1 by direct feedback phosphorylation. Mol. Cell 2005, 17:215-224.
34. Balan V., Leicht D.T., Zhu J., Balan K., Kaplun A., Singh-Gupta V., Qin J., Ruan H., Comb M.J., Tzivion G. Identification of novel in vivo Raf-1 phosphorylation sites mediating positive feedback Raf-1 regulation by extracellular signal-regulated kinase. Mol. Biol. Cell 2006, 17:1141-1153.
35. Alessandrini A., Greulich H., Huang W., Erikson R.L. Mek1 phosphorylation site mutants activate Raf-1 in NIH 3T3 cells. J. Biol. Chem. 1996, 271:31612-31618.
36. Zimmermann S., Rommel C., Ziogas A., Lovric J., Moelling K., Radziwill G. MEK1 mediates a positive feedback on Raf-1 activity independently of Ras and Src. Oncogene 1997, 15:1503-1511.
37. Yeung K., Seitz T., Li S., Janosch P., McFerran B., Kaiser C., Fee F., Katsanakis K.D., Rose D.W., Mischak H., Sedivy J.M., Kolch W. Suppression of Raf-1 kinase activity and MAP kinase signalling by RKIP. Nature 1999, 401:173-177.
38. Luo Z., Tzivion G., Belshaw P.J., Vavvas D., Marshall M., Avruch J. Oligomerization activates c-Raf-1 through a Ras-dependent mechanism. Nature 1996, 383:181-185.
39. Boyle W.J., Van Der Geer P., Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 1991, 201:110-149.
40. Luo K.X., Hurley T.R., Sefton B.M. Cyanogen bromide cleavage and proteolytic peptide mapping of proteins immobilized to membranes. Methods Enzymol. 1991, 201:149-152.
41. Stancato L.F., Silverstein A.M., Owens-Grillo J.K., Chow Y.H., Jove R., Pratt W.B. The hsp90-binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J. Biol. Chem. 1997, 272:4013-4020.
42. Catling A.D., Schaeffer H.J., Reuter C.W., Reddy G.R., Weber M.J. A proline-rich sequence unique to MEK1 and MEK2 is required for raf binding and regulates MEK function. Mol. Cell. Biol. 1995, 15:5214-5225.
43. Takekawa M., Tatebayashi K., Saito H. Conserved docking site is essential for activation of mammalian MAP kinase kinases by specific MAP kinase kinase kinases. Mol. Cell 2005, 18:295-306.
44. Heidecker G., Huleihel M., Cleveland J.L., Kolch W., Beck T.W., Lloyd P., Pawson T., Rapp U.R. Mutational activation of c-Raf-1 and definition of the minimal transforming sequence. Mol. Cell. Biol. 1990, 10:2503-2512.
45. Schmidt C.A., Oettle H., Ludwig W.D., Serke S., Pawlaczyk-Peter B., Wilborn F., Binder L.T., Huhn D., Siegert W. Overexpression of the Raf-1 proto-oncogene in human myeloid leukemia. Leuk. Res. 1994, 18:409-413.
46. Damodar Reddy C., Marwaha S., Patti R., Raghunath M., Duhaime A.C., Sutton L., Phillips P.C. Role of MAP kinase pathways in primitive neuroectodermal tumors. Anticancer. Res. 2001, 21:2733-2738.
47. Hajj C., Akoum R., Bradley E., Paquin F., Ayoub J. DNA alterations at proto-oncogene loci and their clinical significance in operable non-small cell lung cancer. Cancer 1990, 66:733-739.
48. McPhillips F., Mullen P., Monia B.P., Ritchie A.A., Dorr F.A., Smyth J.F., Langdon S.P. Association of c-Raf expression with survival and its targeting with antisense oligonucleotides in ovarian cancer. Br. J. Cancer 2001, 85:1753-1758.
49. Jeuken J., van den Broecke C., Gijsen S., Boots-Sprenger S., Wesseling P. RAS/RAF pathway activation in gliomas: the result of copy number gains rather than activating mutations. Acta Neuropathol. 2007, 114:121-133.
50. Fedorov L.M., Papadopoulos T., Tyrsin O.Y., Twardzik T., Gotz R., Rapp U.R. Loss of p53 in craf-induced transgenic lung adenoma leads to tumor acceleration and phenotypic switch. Cancer Res. 2003, 63:2268-2277.
51. Rapp U.R., Fensterle J., Albert S., Gotz R. Raf kinases in lung tumor development. Adv. Enzyme Regul. 2003, 43:183-195.
52. Cekanova M., Majidy M., Masi T., Al-Wadei H.A., Schuller H.M. Overexpressed Raf-1 and phosphorylated cyclic adenosine 3'-5'-monophosphatate response element-binding protein are early markers for lung adenocarcinoma. Cancer 2007, 109:1164-1173.
53. Chatterji B., Borlak J. Serum proteomics of lung adenocarcinomas induced by targeted overexpression of c-raf in alveolar epithelium identifies candidate biomarkers. Proteomics 2007, 7:3980-3991.
54. Rohrbeck A., Muller V.S., Borlak J. Molecular characterization of lung dysplasia induced by c-Raf-1. PLoS One 2009, 4:e5637.
55. Smith F.D., Langeberg L.K., Cellurale C., Pawson T., Morrison D.K., Davis R.J., Scott J.D. AKAP-Lbc enhances cyclic AMP control of the ERK1/2 cascade. Nat. Cell Biol. 2010, 12:1242-1249.
56. Hentschel J., Rubio I., Eberhart M., Hipler C., Schiefner J., Schubert K., Loncarevic I.F., Wittig U., Baniahmad A., von Eggeling F. BCR-ABL- and Ras-independent activation of Raf as a novel mechanism of Imatinib resistance in CML. Int. J. Oncol. 2011, 585-591.
57. Fu Z., Kitagawa Y., Shen R., Shah R., Mehra R., Rhodes D., Keller P.J., Mizokami A., Dunn R., Chinnaiyan A.M., Yao Z., Keller E.T. Metastasis suppressor gene Raf kinase inhibitor protein (RKIP) is a novel prognostic marker in prostate cancer. Prostate 2006, 66:248-256.
58. Granovsky A.E., Rosner M.R. Raf kinase inhibitory protein: a signal transduction modulator and metastasis suppressor. Cell Res. 2008, 18:452-457.
59. Zebisch A., Haller M., Hiden K., Goebel T., Hoefler G., Troppmair J., Sill H. Loss of RAF kinase inhibitor protein is a somatic event in the pathogenesis of therapy-related acute myeloid leukemias with C-RAF germline mutations. Leukemia 2009, 23:1049-1053.
60. Kim H.S., Kim G.Y., Lim S.J., Kim Y.W. Loss of Raf-1 kinase inhibitory protein in pancreatic ductal adenocarcinoma. Pathology 2010, 42:655-660.
61. Kim H.S., Kim G.Y., Lim S.J., Kim Y.W. Raf-1 kinase inhibitory protein expression in thyroid carcinomas. Endocr. Pathol. 2010, 21:253-257.
62. Minoo P., Zlobec I., Baker K., Tornillo L., Terracciano L., Jass J.R., Lugli A. Loss of Raf-1 kinase inhibitor protein expression is associated with tumor progression and metastasis in colorectal cancer. Am. J. Clin. Pathol. 2007, 127:820-827.
63. Kaplan F.M., Shao Y., Mayberry M.M., Aplin A.E. Hyperactivation of MEK-ERK1/2 signaling and resistance to apoptosis induced by the oncogenic B-RAF inhibitor, PLX4720, in mutant N-RAS melanoma cells. Oncogene 2011, 30:366-371.
64. Downward J. Targeting RAF: trials and tribulations. Nat. Med. 2011, 17:286-288.
65. Poulikakos P.I., Zhang C., Bollag G., Shokat K.M., Rosen N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010, 464:427-430.
66. Hatzivassiliou G., Song K., Yen I., Brandhuber B.J., Anderson D.J., Alvarado R., Ludlam M.J., Stokoe D., Gloor S.L., Vigers G., Morales T., Aliagas I., Liu B., Sideris S., Hoeflich K.P., Jaiswal B.S., Seshagiri S., Koeppen H., Belvin M., Friedman L.S., Malek S. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010, 464:431-435.
67. Kolch W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 2005, 6:827-837.
68. Rajakulendran T., Sahmi M., Lefrancois M., Sicheri F., Therrien M. A dimerization-dependent mechanism drives RAF catalytic activation. Nature 2009, 461:542-545.
69. Rushworth L.K., Hindley A.D., O'Neill E., Kolch W. Regulation and role of Raf-1/B-Raf heterodimerization. Mol. Cell. Biol. 2006, 26:2262-2272.
70. Baljuls A., Schmitz W., Mueller T., Zahedi R.P., Sickmann A., Hekman M., Rapp U.R. Positive regulation of A-RAF by phosphorylation of isoform-specific hinge segment and identification of novel phosphorylation sites. J. Biol. Chem. 2008, 283:27239-27254.