FGFR3 Activates RSK2 to Mediate Hematopoietic Transformation through Tyrosine Phosphorylation of RSK2 and Activation of the MEK/ERK Pathway

Cancer Cell

Volumn 12, Issue 3, 2007, Pages 201-214

  Kang, Sumin ^a   Dong, Shaozhong ^a   Gu, Ting Lei ^b   Guo, Ailan ^b   Cohen, Michael S ^c   Lonial, Sagar ^a   Khoury, Hanna Jean ^a   Fabbro, Doriano ^d   Gilliland, D Gary ^e   Bergsagel, P Leif ^f   Taunton, Jack ^c   Polakiewicz, Roberto D ^b   Chen, Jing ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CELL SIGNALING TECHNOLOGY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

^e HARVARD MEDICAL SCHOOL   (United States)

^f MAYO CLINIC   (United States)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; CANCER ANTIBODY; FIBROBLAST GROWTH FACTOR RECEPTOR 3; FLUOROMETHYL KETONE; MIDOSTAURIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MUTANT PROTEIN; PROTEIN INHIBITOR; PROTEIN SERINE THREONINE KINASE; REGULATOR PROTEIN; S6 KINASE 1; S6 KINASE 2; SMALL INTERFERING RNA; TYROSINE; UNCLASSIFIED DRUG; WORTMANNIN; Y529 ANTIBODY;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME INHIBITION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; LEUKEMOGENESIS; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN VARIANT; PROTEOMICS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 34548253333     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2007.08.003     Document Type: Article

References (43)

1. Anjum R., Roux P.P., Ballif B.A., Gygi S.P., and Blenis J. The tumor suppressor DAP kinase is a target of RSK-mediated survival signaling. Curr. Biol. 15 (2005) 1762-1767
2. Bergsagel P.L., Chesi M., Nardini E., Brents L.A., Kirby S.L., and Kuehl W.M. Promiscuous translocations into immunoglobulin heavy chain switch regions in multiple myeloma. Proc. Natl. Acad. Sci. USA 93 (1996) 13931-13936
3. Bergsagel P.L., and Kuehl W.M. Chromosome translocations in multiple myeloma. Oncogene 20 (2001) 5611-5622
4. Blenis J. Signal transduction via the MAP kinases: Proceed at your own RSK. Proc. Natl. Acad. Sci. USA 90 (1993) 5889-5892
5. Buck M., Poli V., Hunter T., and Chojkier M. C/EBPbeta phosphorylation by RSK creates a functional XEXD caspase inhibitory box critical for cell survival. Mol. Cell 8 (2001) 807-816
6. Cappellen D., De Oliveira C., Ricol D., de Medina S., Bourdin J., Sastre-Garau X., Chopin D., Thiery J.P., and Radvanyi F. Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas. Nat. Genet. 23 (1999) 18-20
7. Chen J., Lee B.H., Williams I.R., Kutok J.L., Mitsiades C.S., Duclos N., Cohen S., Adelsperger J., Okabe R., Coburn A., et al. FGFR3 as a therapeutic target of the small molecule inhibitor PKC412 in hematopoietic malignancies. Oncogene 24 (2005) 8259-8267
8. Chen J., Williams I.R., Lee B.H., Duclos N., Huntly B.J., Donoghue D.J., and Gilliland D.G. Constitutively activated FGFR3 mutants signal through PLCgamma-dependent and -independent pathways for hematopoietic transformation. Blood 106 (2005) 328-337
9. Chesi M., Bergsagel P.L., Brents L.A., Smith C.M., Gerhard D.S., and Kuehl W.M. Dysregulation of cyclin D1 by translocation into an IgH gamma switch region in two multiple myeloma cell lines. Blood 88 (1996) 674-681
10. Chesi M., Bergsagel P.L., Shonukan O.O., Martelli M.L., Brents L.A., Chen T., Schrock E., Ried T., and Kuehl W.M. Frequent dysregulation of the c-maf proto-oncogene at 16q23 by translocation to an Ig locus in multiple myeloma. Blood 91 (1998) 4457-4463
11. Chesi M., Brents L.A., Ely S.A., Bais C., Robbiani D.F., Mesri E.A., Kuehl W.M., and Bergsagel P.L. Activated fibroblast growth factor receptor 3 is an oncogene that contributes to tumor progression in multiple myeloma. Blood 97 (2001) 729-736
12. Chesi M., Nardini E., Brents L.A., Schrock E., Ried T., Kuehl W.M., and Bergsagel P.L. Frequent translocation t(4;14)(p16.3;q32.3) in multiple myeloma is associated with increased expression and activating mutations of fibroblast growth factor receptor 3. Nat. Genet. 16 (1997) 260-264
13. Chesi M., Nardini E., Lim R.S., Smith K.D., Kuehl W.M., and Bergsagel P.L. The t(4;14) translocation in myeloma dysregulates both FGFR3 and a novel gene, MMSET, resulting in IgH/MMSET hybrid transcripts. Blood 92 (1998) 3025-3034
14. Cohen M.S., Hadjivassiliou H., and Taunton J. A clickable inhibitor reveals context-dependent autoactivation of p90 RSK. Nat. Chem. Biol. 3 (2007) 156-160
15. Cohen M.S., Zhang C., Shokat K.M., and Taunton J. Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 308 (2005) 1318-1321
16. Colvin J.S., Bohne B.A., Harding G.W., McEwen D.G., and Ornitz D.M. Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat. Genet. 12 (1996) 390-397
17. David E., Sun S.Y., Waller E.K., Chen J., Khuri F.R., and Lonial S. The combination of the farnesyl transferase inhibitor lonafarnib and the proteasome inhibitor bortezomib induces synergistic apoptosis in human myeloma cells that is associated with down-regulation of p-AKT. Blood 106 (2005) 4322-4329
18. Deng C., Wynshaw-Boris A., Zhou F., Kuo A., and Leder P. Fibroblast growth factor receptor 3 is a negative regulator of bone growth. Cell 84 (1996) 911-921
19. Fisher T.L., and Blenis J. Evidence for two catalytically active kinase domains in pp90rsk. Mol. Cell. Biol. 16 (1996) 1212-1219
20. Frodin M., and Gammeltoft S. Role and regulation of 90 kDa ribosomal S6 kinase (RSK) in signal transduction. Mol. Cell. Endocrinol. 151 (1999) 65-77
21. Frodin M., Jensen C.J., Merienne K., and Gammeltoft S. A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J. 19 (2000) 2924-2934
22. Gavin A.C., and Nebreda A.R. A MAP kinase docking site is required for phosphorylation and activation of p90(rsk)/MAPKAP kinase-1. Curr. Biol. 9 (1999) 281-284
23. Golla A., Lichmer P., von Gernet S., Winterpacht A., Fairley J., Murken J., and Schuffenhauer S. Phenotypic expression of the fibroblast growth factor receptor 3 (FGFR3) mutation P250R in a large craniosynostosis family. J. Med. Genet. 34 (1997) 683-684
24. Grand E.K., Chase A.J., Heath C., Rahemtulla A., and Cross N.C. Targeting FGFR3 in multiple myeloma: Inhibition of t(4;14)-positive cells by SU5402 and PD173074. Leukemia 18 (2004) 962-966
25. Hart K.C., Robertson S.C., and Donoghue D.J. Identification of tyrosine residues in constitutively activated fibroblast growth factor receptor 3 involved in mitogenesis, Stat activation, and phosphatidylinositol 3-kinase activation. Mol. Biol. Cell 12 (2001) 931-942
26. Jensen C.J., Buch M.B., Krag T.O., Hemmings B.A., Gammeltoft S., and Frodin M. 90-kDa ribosomal S6 kinase is phosphorylated and activated by 3-phosphoinositide-dependent protein kinase-1. J. Biol. Chem. 274 (1999) 27168-27176
27. Li Z., Zhu Y.X., Plowright E.E., Bergsagel P.L., Chesi M., Patterson B., Hawley T.S., Hawley R.G., and Stewart A.K. The myeloma-associated oncogene fibroblast growth factor receptor 3 is transforming in hematopoietic cells. Blood 97 (2001) 2413-2419
28. Ng M.H., Lau K.M., Wong W.S., To K.W., Cheng S.H., Tsang K.S., Chan N.P., Kho B.C., Lo K.W., Tong J.H., et al. Alterations of RAS signalling in Chinese multiple myeloma patients: Absent BRAF and rare RAS mutations, but frequent inactivation of RASSF1A by transcriptional silencing or expression of a non-functional variant transcript. Br. J. Haematol. 123 (2003) 637-645
29. Palmer A., Gavin A.C., and Nebreda A.R. A link between MAP kinase and p34(cdc2)/cyclin B during oocyte maturation: p90(rsk) phosphorylates and inactivates the p34(cdc2) inhibitory kinase Myt1. EMBO J. 17 (1998) 5037-5047
30. Paterson J.L., Li Z., Wen X.Y., Masih-Khan E., Chang H., Pollett J.B., Trudel S., and Stewart A.K. Preclinical studies of fibroblast growth factor receptor 3 as a therapeutic target in multiple myeloma. Br. J. Haematol. 124 (2004) 595-603
31. Richards S.A., Dreisbach V.C., Murphy L.O., and Blenis J. Characterization of regulatory events associated with membrane targeting of p90 ribosomal S6 kinase 1. Mol. Cell. Biol. 21 (2001) 7470-7480
32. Ronchetti D., Greco A., Compasso S., Colombo G., Dell'Era P., Otsuki T., Lombardi L., and Neri A. Deregulated FGFR3 mutants in multiple myeloma cell lines with t(4;14): Comparative analysis of Y373C, K650E and the novel G384D mutations. Oncogene 20 (2001) 3553-3562
33. Roux P.P., Richards S.A., and Blenis J. Phosphorylation of p90 ribosomal S6 kinase (RSK) regulates extracellular signal-regulated kinase docking and RSK activity. Mol. Cell. Biol. 23 (2003) 4796-4804
34. Rush J., Moritz A., Lee K.A., Guo A., Goss V.L., Spek E.J., Zhang H., Zha X.M., Polakiewicz R.D., and Comb M.J. Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 23 (2005) 94-101
35. Sapkota G.P., Cummings L., Newell F.S., Armstrong C., Bain J., Frodin M., Grauert M., Hoffmann M., Schnapp G., Steegmaier M., et al. BI-D1870 is a specific inhibitor of the p90 RSK (ribosomal S6 kinase) isoforms in vitro and in vivo. Biochem. J. 401 (2007) 29-38
36. Shimamura A., Ballif B.A., Richards S.A., and Blenis J. Rsk1 mediates a MEK-MAP kinase cell survival signal. Curr. Biol. 10 (2000) 127-135
37. Smith J.A., Poteet-Smith C.E., Malarkey K., and Sturgill T.W. Identification of an extracellular signal-regulated kinase (ERK) docking site in ribosomal S6 kinase, a sequence critical for activation by ERK in vivo. J. Biol. Chem. 274 (1999) 2893-2898
38. Tavormina P.L., Shiang R., Thompson L.M., Zhu Y.Z., Wilkin D.J., Lachman R.S., Wilcox W.R., Rimoin D.L., Cohn D.H., and Wasmuth J.J. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat. Genet. 9 (1995) 321-328
39. Trudel S., Ely S., Farooqi Y., Affer M., Robbiani D.F., Chesi M., and Bergsagel P.L. Inhibition of fibroblast growth factor receptor 3 induces differentiation and apoptosis in t(4;14) myeloma. Blood 103 (2004) 3521-3528
40. Vaidyanathan H., and Ramos J.W. RSK2 activity is regulated by its interaction with PEA-15. J. Biol. Chem. 278 (2003) 32367-32372
41. Webster M.K., and Donoghue D.J. Constitutive activation of fibroblast growth factor receptor 3 by the transmembrane domain point mutation found in achondroplasia. EMBO J. 15 (1996) 520-527
42. Yagasaki F., Wakao D., Yokoyama Y., Uchida Y., Murohashi I., Kayano H., Taniwaki M., Matsuda A., and Bessho M. Fusion of ETV6 to fibroblast growth factor receptor 3 in peripheral T-cell lymphoma with a t(4;12)(p16;p13) chromosomal translocation. Cancer Res. 61 (2001) 8371-8374
43. Zhang L., Wang H., Liu D., Liddington R., and Fu H. Raf-1 kinase and exoenzyme S interact with 14-3-3zeta through a common site involving lysine 49. J. Biol. Chem. 272 (1997) 13717-13724