KSR2 Is a Calcineurin Substrate that Promotes ERK Cascade Activation in Response to Calcium Signals

Molecular Cell

Volumn 34, Issue 6, 2009, Pages 652-662

  Dougherty, Michele K ^a   Ritt, Daniel A ^a   Zhou, Ming ^a   Specht, Suzanne I ^a   Monson, Daniel M ^a   Veenstra, Timothy D ^a   Morrison, Deborah K ^a  

^a SAIC FREDERICK INC   (United States)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

CALCINEURIN; CALCIUM ION; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN INHIBITOR; SCAFFOLD PROTEIN; SUPPRESSOR OF RAS 1 PROTEIN; SUPPRESSOR OF RAS 2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CELL STRAIN 3T3; CELL STRAIN COS7; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; OOCYTE; PANCREAS ISLET BETA CELL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; XENOPUS;

ANIMALS; CALCINEURIN; CALCIUM SIGNALING; CERCOPITHECUS AETHIOPS; COS CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; PROTEIN-SERINE-THREONINE KINASES; RATS; RNA INTERFERENCE;

MAMMALIA;

EID: 67449164361     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.06.001     Document Type: Article

References (46)

1. Arnette D., Gibson T.B., Lawrence M.C., January B., Khoo S., McGlynn K., Vanderbilt C.A., and Cobb M.H. Regulation of ERK1 and ERK2 by glucose and peptide hormones in pancreatic beta cells. J. Biol. Chem. 278 (2003) 32517-32525
2. Cacace A.M., Michaud N.R., Therrien M., Mathes K., Copeland T., Rubin G.M., and Morrison D.K. 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
3. Casar B., Arozarena I., Sanz-Moreno V., Pinto A., Agudo-Ibanez L., Marais R., Lewis R.E., Berciano M.T., and Crespo P. Ras subcellular localization defines ERK1/2 substrate specificity through distinct utilization of scaffold proteins. Mol. Cell Biol. 29 (2009) 1338-1353 10.1128/MCB.01359-08 Published online December 29, 2008
4. Channavajhala P.L., Wu L., Cuozzo J.W., Hall J.P., Liu W., Lin L.L., and Zhang Y. Identification of a novel human kinase supporter of Ras (hKSR-2) that functions as a negative regulator of Cot (Tpl2) signaling. J. Biol. Chem. 278 (2003) 47089-47097
5. Channavajhala P.L., Rao V.R., Spaulding V., Lin L.L., and Zhang Y.G. hKSR-2 inhibits MEKK3-activated MAP kinase and NF-kappaB pathways in inflammation. Biochem. Biophys. Res. Commun. 334 (2005) 1214-1218
6. Crabtree G.R. Calcium, calcineurin, and the control of transcription. J. Biol. Chem. 276 (2001) 2313-2316
7. Cullen P.J., and Lockyer P.J. Integration of calcium and Ras signalling. Nat. Rev. Mol. Cell Biol. 3 (2002) 339-348
8. Dard N., and Peter M. Scaffold proteins in MAP kinase signaling: more than simple passive activating platforms. Bioessays 28 (2006) 146-156
9. Denouel-Galy A., Douville E.M., Warne P.H., Papin C., Laugier D., Calothy G., Downward J., and Eychene A. Murine Ksr interacts with MEK and inhibits Ras-induced transformation. Curr. Biol. 8 (1998) 46-55
10. Dodge K.L., and Scott J.D. Calcineurin anchoring and cell signaling. Biochem. Biophys. Res. Commun. 311 (2003) 1111-1115
11. Dolmetsch R.E., Pajvani U., Fife K., Spotts J.M., and Greenberg M.E. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294 (2001) 333-339
12. Elion E.A. The Ste5p scaffold. J. Cell Sci. 114 (2001) 3967-3978
13. Garcia-Cozar F.J., Okamura H., Aramburu J.F., Shaw K.T., Pelletier L., Showalter R., Villafranca E., and Rao A. Two-site interaction of nuclear factor of activated T cells with activated calcineurin. J. Biol. Chem. 273 (1998) 23877-23883
14. Hao N., Nayak S., Behar M., Shanks R.H., Nagiec M.J., Errede B., Hasty J., Elston T.C., and Dohlman H.G. Regulation of cell signaling dynamics by the protein kinase-scaffold Ste5. Mol. Cell 30 (2008) 649-656
15. Hogan P.G., Chen L., Nardone J., and Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17 (2003) 2205-2232
16. Khoo S., and Cobb M.H. Activation of mitogen-activating protein kinase by glucose is not required for insulin secretion. Proc. Natl. Acad. Sci. USA 94 (1997) 5599-5604
17. Kolch W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 6 (2005) 827-837
18. Kornfeld K., Hom D.B., and Horvitz H.R. The ksr-1 gene encodes a novel protein kinase involved in Ras-mediated signaling in C. elegans. Cell 83 (1995) 903-913
19. Kortum R.L., and Lewis R.E. The molecular scaffold KSR1 regulates the proliferative and oncogenic potential of cells. Mol. Cell. Biol. 24 (2004) 4407-4416
20. Levchenko A., Bruck J., and Sternberg P.W. Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc. Natl. Acad. Sci. USA 97 (2000) 5818-5823
21. Malumbres M., and Barbacid M. RAS oncogenes: the first 30 years. Nat. Rev. Cancer 3 (2003) 459-465
22. Marshall C.J. Ras effectors. Curr. Opin. Cell Biol. 8 (1996) 197-204
23. Martinez-Martinez S., Rodriguez A., Lopez-Maderuelo M.D., Ortega-Perez I., Vazquez J., and Redondo J.M. Blockade of NFAT activation by the second calcineurin binding site. J. Biol. Chem. 281 (2006) 6227-6235
24. Matheny S.A., Chen C., Kortum R.L., Razidlo G.L., Lewis R.E., and White M.A. Ras regulates assembly of mitogenic signalling complexes through the effector protein IMP. Nature 427 (2004) 256-260
25. Morrison D.K., and Davis R.J. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu. Rev. Cell Dev. Biol. 19 (2003) 91-118
26. Morrison D.K., Heidecker G., Rapp U.R., and Copeland T.D. Identification of the major phosphorylation sites of the Raf-1 kinase. J. Biol. Chem. 268 (1993) 17309-17316
27. Muller J., Ory S., Copeland T., Piwnica-Worms H., and Morrison D.K. C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Mol. Cell 8 (2001) 983-993
28. Nguyen A., Burack W.R., Stock J.L., Kortum R., Chaika O.V., Afkarian M., Muller W.J., Murphy K.M., Morrison D.K., Lewis R.E., et al. Kinase suppressor of Ras (KSR) is a scaffold which facilitates mitogen-activated protein kinase activation in vivo. Mol. Cell. Biol. 22 (2002) 3035-3045
29. Ohmachi M., Rocheleau C.E., Church D., Lambie E., Schedl T., and Sundaram M.V. C. elegans ksr-1 and ksr-2 have both unique and redundant functions and are required for MPK-1 ERK phosphorylation. Curr. Biol. 12 (2002) 427-433
30. Ory S., Zhou M., Conrads T.P., Veenstra T.D., and Morrison D.K. Protein phosphatase 2A positively regulates Ras signaling by dephosphorylating KSR1 and Raf-1 on critical 14-3-3 binding sites. Curr. Biol. 13 (2003) 1356-1364
31. Park S., Uesugi M., and Verdine G.L. A second calcineurin binding site on the NFAT regulatory domain. Proc. Natl. Acad. Sci. USA 97 (2000) 7130-7135
32. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., and Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22 (2001) 153-183
33. Qi M., and Elion E.A. MAP kinase pathways. J. Cell Sci. 118 (2005) 3569-3572
34. Ritt D.A., Zhou M., Conrads T.P., Veenstra T.D., Copeland T.D., and Morrison D.K. CK2 Is a component of the KSR1 scaffold complex that contributes to Raf kinase activation. Curr. Biol. 17 (2007) 179-184
35. Rosen L.B., Ginty D.D., Weber M.J., and Greenberg M.E. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12 (1994) 1207-1221
36. Roy F., Laberge G., Douziech M., Ferland-McCollough D., and Therrien M. KSR is a scaffold required for activation of the ERK/MAPK module. Genes Dev. 16 (2002) 427-438
37. Schmitt J.M., Wayman G.A., Nozaki N., and Soderling T.R. Calcium activation of ERK mediated by calmodulin kinase I. J. Biol. Chem. 279 (2004) 24064-24072
38. Shalin S.C., Hernandez C.M., Dougherty M.K., Morrison D.K., and Sweatt J.D. Kinase suppressor of Ras1 compartmentalizes hippocampal signal transduction and subserves synaptic plasticity and memory formation. Neuron 50 (2006) 765-779
39. Shaul Y.D., and Seger R. The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim. Biophys. Acta 1773 (2007) 1213-1226
40. Stewart S., Sundaram M., Zhang Y., Lee J., Han M., and Guan K.L. Kinase suppressor of Ras forms a multiprotein signaling complex and modulates MEK localization. Mol. Cell. Biol. 19 (1999) 5523-5534
41. Sundaram M., and Han M. The C. elegans ksr-1 gene encodes a novel Raf-related kinase involved in Ras-mediated signal transduction. Cell 83 (1995) 889-901
42. Sundaram M., Yochem J., and Han M. A Ras-mediated signal transduction pathway is involved in the control of sex myoblast migration in Caenorhabditis elegans. Development 122 (1996) 2823-2833
43. Therrien M., Chang H.C., Solomon N.M., Karim F.D., Wassarman D.A., and Rubin G.M. KSR, a novel protein kinase required for RAS signal transduction. Cell 83 (1995) 879-888
44. Therrien M., Michaud N.R., Rubin G.M., and Morrison D.K. KSR modulates signal propagation within the MAPK cascade. Genes Dev. 10 (1996) 2684-2695
45. Wu G.Y., Deisseroth K., and Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. USA 98 (2001) 2808-2813
46. Xing H., Kornfeld K., and Muslin A.J. The protein kinase KSR interacts with 14-3-3 protein and Raf. Curr. Biol. 7 (1997) 294-300