XAllosteric activation of functionally asymmetric RAF kinase dimers

Cell

Volumn 154, Issue 5, 2013, Pages

  Hu, Jiancheng ^a   Stites, Edward C ^a   Yu, Haiyang ^a   Germino, Elizabeth A ^a   Meharena, Hiruy S ^b   Stork, Philip J S ^c   Kornev, Alexandr P ^b   Taylor, Susan S ^b   Shaw, Andrey S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASYMMETRIC RAF KINASE; B RAF KINASE; DIMER; PHOSPHOTRANSFERASE; RAF PROTEIN; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; AUTOPHOSPHORYLATION; DIMERIZATION; ENZYME ACTIVITY; ENZYME CONFORMATION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; HYDROPHOBICITY; MUTANT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 84883311219     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.07.046     Document Type: Article

References (61)

1. M. Baccarini Second nature: biological functions of the Raf-1 "kinase" FEBS Lett. 579 2005 3271 3277
2. A. Baljuls, R. Mahr, I. Schwarzenau, T. Müller, L. Polzien, M. Hekman, and U.R. Rapp Single substitution within the RKTR motif impairs kinase activity but promotes dimerization of RAF kinase J. Biol. Chem. 286 2011 16491 16503
3. A. Baljuls, T. Mueller, H.C. Drexler, M. Hekman, and U.R. Rapp Unique N-region determines low basal activity and limited inducibility of A-RAF kinase: the role of N-region in the evolutionary divergence of RAF kinase function in vertebrates J. Biol. Chem. 282 2007 26575 26590
4. N. Blom, T. Sicheritz-Pontén, R. Gupta, S. Gammeltoft, and S. Brunak Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence Proteomics 4 2004 1633 1649
5. D.F. Brennan, A.C. Dar, N.T. Hertz, W.C. Chao, A.L. Burlingame, K.M. Shokat, and D. Barford A Raf-induced allosteric transition of KSR stimulates phosphorylation of MEK Nature 472 2011 366 369
6. M.S. Brose, P. Volpe, M. Feldman, M. Kumar, I. Rishi, R. Gerrero, E. Einhorn, M. Herlyn, J. Minna, and A. Nicholson BRAF and RAS mutations in human lung cancer and melanoma Cancer Res. 62 2002 6997 7000
7. A.M. Cacace, N.R. Michaud, M. Therrien, K. Mathes, T. Copeland, G.M. Rubin, and D.K. Morrison Identification of constitutive and ras-inducible phosphorylation sites of KSR: implications for 14-3-3 binding, mitogen-activated protein kinase binding, and KSR overexpression Mol. Cell. Biol. 19 1999 229 240
8. A. Chiloeches, C.S. Mason, and R. Marais S338 phosphorylation of Raf-1 is independent of phosphatidylinositol 3-kinase and Pak3 Mol. Cell. Biol. 21 2001 2423 2434
9. H. Chong, J. Lee, and K.L. Guan Positive and negative regulation of Raf kinase activity and function by phosphorylation EMBO J. 20 2001 3716 3727
10. S.W. Cowan-Jacob, G. Fendrich, P.W. Manley, W. Jahnke, D. Fabbro, J. Liebetanz, and T. Meyer The crystal structure of a c-Src complex in an active conformation suggests possible steps in c-Src activation Structure 13 2005 861 871
11. H. Davies, G.R. Bignell, C. Cox, P. Stephens, S. Edkins, S. Clegg, J. Teague, H. Woffendin, M.J. Garnett, and W. Bottomley Mutations of the BRAF gene in human cancer Nature 417 2002 949 954
12. B. Diaz, D. Barnard, A. Filson, S. MacDonald, A. King, and M. Marshall Phosphorylation of Raf-1 serine 338-serine 339 is an essential regulatory event for Ras-dependent activation and biological signaling Mol. Cell. Biol. 17 1997 4509 4516
13. J.R. Fabian, I.O. Daar, and D.K. Morrison Critical tyrosine residues regulate the enzymatic and biological activity of Raf-1 kinase Mol. Cell. Biol. 13 1993 7170 7179
14. M.A. Farrar, J. Alberol-Ila, and R.M. Perlmutter Activation of the Raf-1 kinase cascade by coumermycin-induced dimerization Nature 383 1996 178 181
15. A.K. Freeman, D.A. Ritt, and D.K. Morrison Effects of Raf dimerization and its inhibition on normal and disease-associated Raf signaling Mol. Cell 49 2013 751 758
16. G. Galabova-Kovacs, A. Kolbus, D. Matzen, K. Meissl, D. Piazzolla, C. Rubiolo, K. Steinitz, and M. Baccarini ERK and beyond: insights from B-Raf and Raf-1 conditional knockouts Cell Cycle 5 2006 1514 1518
17. M.J. Garnett, S. Rana, H. Paterson, D. Barford, and R. Marais Wild-type and mutant B-RAF activate C-RAF through distinct mechanisms involving heterodimerization Mol. Cell 20 2005 963 969
18. J.D. Hansen, J. Grina, B. Newhouse, M. Welch, G. Topalov, N. Littman, M. Callejo, S. Gloor, M. Martinson, and E. Laird Potent and selective pyrazole-based inhibitors of B-Raf kinase Bioorg. Med. Chem. Lett. 18 2008 4692 4695
19. G. Hatzivassiliou, K. Song, I. Yen, B.J. Brandhuber, D.J. Anderson, R. Alvarado, M.J. Ludlam, D. Stokoe, S.L. Gloor, and G. Vigers RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth Nature 464 2010 431 435
20. S.J. Heidorn, C. Milagre, S. Whittaker, A. Nourry, I. Niculescu-Duvas, N. Dhomen, J. Hussain, J.S. Reis-Filho, C.J. Springer, C. Pritchard, and R. Marais Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF Cell 140 2010 209 221
21. J. Hu, P. Strauch, A. Rubtsov, E.E. Donovan, R. Pelanda, and R.M. Torres Lsc activity is controlled by oligomerization and regulates integrin adhesion Mol. Immunol. 45 2008 1825 1836
22. J. Hu, H. Yu, A.P. Kornev, J. Zhao, E.L. Filbert, S.S. Taylor, and A.S. Shaw Mutation that blocks ATP binding creates a pseudokinase stabilizing the scaffolding function of kinase suppressor of Ras, CRAF and BRAF Proc. Natl. Acad. Sci. USA 108 2011 6067 6072
23. M. Hüser, J. Luckett, A. Chiloeches, K. Mercer, M. Iwobi, S. Giblett, X.M. Sun, J. Brown, R. Marais, and C. Pritchard MEK kinase activity is not necessary for Raf-1 function EMBO J. 20 2001 1940 1951
24. R.E. Joseph, L. Min, and A.H. Andreotti The linker between SH2 and kinase domains positively regulates catalysis of the Tec family kinases Biochemistry 46 2007 5455 5462
25. F.A. Karreth, G.M. DeNicola, S.P. Winter, and D.A. Tuveson C-Raf inhibits MAPK activation and transformation by B-Raf(V600E) Mol. Cell 36 2009 477 486
26. A.J. King, H. Sun, B. Diaz, D. Barnard, W. Miao, S. Bagrodia, and M.S. Marshall The protein kinase Pak3 positively regulates Raf-1 activity through phosphorylation of serine 338 Nature 396 1998 180 183
27. A.J. King, D.R. Patrick, R.S. Batorsky, M.L. Ho, H.T. Do, S.Y. Zhang, R. Kumar, D.W. Rusnak, A.K. Takle, and D.M. Wilson Demonstration of a genetic therapeutic index for tumors expressing oncogenic BRAF by the kinase inhibitor SB-590885 Cancer Res. 66 2006 11100 11105
28. W. Kolch, G. Heidecker, G. Kochs, R. Hummel, H. Vahidi, H. Mischak, G. Finkenzeller, D. Marmé, and U.R. Rapp Protein kinase C alpha activates RAF-1 by direct phosphorylation Nature 364 1993 249 252
29. A.P. Kornev, N.M. Haste, S.S. Taylor, and L.F. Eyck Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism Proc. Nat. Acad. Sci. USA 103 2006 17783 17788
30. A.P. Kornev, S.S. Taylor, and L.F. Ten Eyck A helix scaffold for the assembly of active protein kinases Proc. Natl. Acad. Sci. USA 105 2008 14377 14382
31. M. LaFevre-Bernt, F. Sicheri, A. Pico, M. Porter, J. Kuriyan, and W.T. Miller Intramolecular regulatory interactions in the Src family kinase Hck probed by mutagenesis of a conserved tryptophan residue J. Biol. Chem. 273 1998 32129 32134
32. D.T. Leicht, V. Balan, J. Zhu, A. Kaplun, A. Bronisz, A. Rana, and G. Tzivion MEK-1 activates C-Raf through a Ras-independent mechanism Biochim. Biophys. Acta 1833 2013 976 986
33. X. Lin, M.K. Ayrapetov, S. Lee, K. Parang, and G. Sun Probing the communication between the regulatory and catalytic domains of a protein tyrosine kinase, Csk Biochemistry 44 2005 1561 1567
34. P.A. Lochhead Protein kinase activation loop autophosphorylation in cis: overcoming a Catch-22 situation Sci. Signal. 2 2009 4
35. R. Marais, Y. Light, H.F. Paterson, and C.J. Marshall Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation EMBO J. 14 1995 3136 3145
36. R. Marais, Y. Light, H.F. Paterson, C.S. Mason, and C.J. Marshall Differential regulation of Raf-1, A-Raf, and B-Raf by oncogenic ras and tyrosine kinases J. Biol. Chem. 272 1997 4378 4383
37. C.S. Mason, C.J. Springer, R.G. Cooper, G. Superti-Furga, C.J. Marshall, and R. Marais Serine and tyrosine phosphorylations cooperate in Raf-1, but not B-Raf activation EMBO J. 18 1999 2137 2148
38. M.M. McKay, D.A. Ritt, and D.K. Morrison RAF inhibitor-induced KSR1/B-RAF binding and its effects on ERK cascade signaling Curr. Biol. 21 2011 563 568
39. M. Mikula, M. Schreiber, Z. Husak, L. Kucerova, J. Rüth, R. Wieser, K. Zatloukal, H. Beug, E.F. Wagner, and M. Baccarini Embryonic lethality and fetal liver apoptosis in mice lacking the c-raf-1 gene EMBO J. 20 2001 1952 1962
40. D.K. Morrison, and R.E. Cutler The complexity of Raf-1 regulation Curr. Opin. Cell Biol. 9 1997 174 179
41. A. Nguyen, W.R. Burack, J.L. Stock, R. Kortum, O.V. Chaika, M. Afkarian, W.J. Muller, K.M. Murphy, D.K. Morrison, and R.E. Lewis Kinase suppressor of Ras (KSR) is a scaffold which facilitates mitogen-activated protein kinase activation in vivo Mol. Cell. Biol. 22 2002 3035 3045
42. P.I. Poulikakos, C. Zhang, G. Bollag, K.M. Shokat, and N. Rosen RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF Nature 464 2010 427 430
43. J. Qin, P. Xie, C. Ventocilla, G. Zhou, A. Vultur, Q. Chen, Q. Liu, M. Herlyn, J. Winkler, and R. Marmorstein Identification of a novel family of BRAF(V600E) inhibitors J. Med. Chem. 55 2012 5220 5230
44. T. Rajakulendran, M. Sahmi, M. Lefrançois, F. Sicheri, and M. Therrien A dimerization-dependent mechanism drives RAF catalytic activation Nature 461 2009 542 545
45. A.P. Rebocho, and R. Marais ARAF acts as a scaffold to stabilize BRAF:CRAF heterodimers Oncogene 32 2013 3207 3212
46. S.S. Taylor, and A.P. Kornev Protein kinases: evolution of dynamic regulatory proteins Trends Biochem. Sci. 36 2011 65 77
47. J. Tsai, J.T. Lee, W. Wang, J. Zhang, H. Cho, S. Mamo, R. Bremer, S. Gillette, J. Kong, and N.K. Haass Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity Proc. Natl. Acad. Sci. USA 105 2008 3041 3046
48. P.T. Wan, M.J. Garnett, S.M. Roe, S. Lee, D. Niculescu-Duvaz, V.M. Good, C.M. Jones, C.J. Marshall, C.J. Springer, D. Barford, R. Marais Cancer Genome Project Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF Cell 116 2004 855 867
49. C.K. Weber, J.R. Slupsky, H.A. Kalmes, and U.R. Rapp Active Ras induces heterodimerization of cRaf and BRaf Cancer Res. 61 2001 3595 3598
50. C. Wellbrock, M. Karasarides, and R. Marais The RAF proteins take centre stage Nat. Rev. Mol. Cell Biol. 5 2004 875 885
51. R. Wimmer, and M. Baccarini Partner exchange: protein-protein interactions in the Raf pathway Trends Biochem. Sci. 35 2010 660 668
52. W. Xu, A. Doshi, M. Lei, M.J. Eck, and S.C. Harrison Crystal structures of c-Src reveal features of its autoinhibitory mechanism Mol. Cell 3 1999 629 638
53. B.H. Zhang, and K.L. Guan Activation of B-Raf kinase requires phosphorylation of the conserved residues Thr598 and Ser601 EMBO J. 19 2000 5429 5439
54. B.H. Zhang, and K.L. Guan Regulation of the Raf kinase by phosphorylation Exp. Lung Res. 27 2001 269 295
55. X. Zhang, J. Gureasko, K. Shen, P.A. Cole, and J. Kuriyan An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor Cell 125 2006 1137 1149
56. A.K. Freeman, D.A. Ritt, and D.K. Morrison Effects of Raf dimerization and its inhibition on normal and disease-associated Raf signaling Mol. Cell 49 2013 751 758
57. G. Hatzivassiliou, K. Song, I. Yen, B.J. Brandhuber, D.J. Anderson, R. Alvarado, M.J. Ludlam, D. Stokoe, S.L. Gloor, and G. Vigers RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth Nature 464 2010 431 435
58. J. Hu, H. Yu, A.P. Kornev, J. Zhao, E.L. Filbert, S.S. Taylor, and A.S. Shaw Mutation that blocks ATP binding creates a pseudokinase stabilizing the scaffolding function of kinase suppressor of Ras, CRAF and BRAF Proc. Natl. Acad. Sci. USA 108 2011 6067 6072
59. P.I. Poulikakos, C. Zhang, G. Bollag, K.M. Shokat, and N. Rosen RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF Nature 464 2010 427 430
60. B.H. Zhang, and K.L. Guan Activation of B-Raf kinase requires phosphorylation of the conserved residues Thr598 and Ser601 EMBO J. 19 2000 5429 5439
61. B.H. Zhang, and K.L. Guan Regulation of the Raf kinase by phosphorylation Exp. Lung Res. 27 2001 269 295