Fibroblast growth factor receptor 3 associates with and tyrosine phosphorylates p90 RSK2, leading to RSK2 activation that mediates hematopoietic transformation

Molecular and Cellular Biology

Volumn 29, Issue 8, 2009, Pages 2105-2117

  Kang, Sumin ^a   Elf, Shannon ^a   Dong, Shaozhong ^a   Hitosugi, Taro ^a   Lythgoe, Katherine ^a   Guo, Ailan ^b   Ruan, Hong ^b   Lonial, Sagar ^a   Khoury, Han Na J ^a   Williams, Ifor R ^a   Lee, Benjamin H ^c   Roesel, Johannes L ^d   Karsenty, Gerard ^e   Hanauer, André ^f   Taunton, Jack ^g   Boggon, Titus J ^h   Gu, Ting Lei ^b   Chen, Jing ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CELL SIGNALING TECHNOLOGY   (United States)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d NOVARTIS PHARMA AG   (Switzerland)

^e Och Spine at New York Presbyterian Hospitals   (United States)

^f INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3; PROTEIN P90; PROTEIN RSK2; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HEMATOPOIESIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

ANIMALS; BINDING SITES; BONE MARROW TRANSPLANTATION; HEMATOPOIESIS; MICE; MYELOPROLIFERATIVE DISORDERS; PHOSPHORYLATION; PROTEIN BINDING; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; TYROSINE;

MURINAE;

EID: 64649100268     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00998-08     Document Type: Article

References (34)

1. Cappellen, D., C. De Oliveira, D. Ricol, S. de Medina, J. Bourdin, X. Sastre-Garau, D. Chopin, J. P. Thiery, and F. Radvanyi. 1999. Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas. Nat. Genet. 23:18-20.
2. Chen, J., B. H. Lee, I. R. Williams, J. L. Kutok, C. S. Mitsiades, N. Duclos, S. Cohen, J. Adelsperger, R. Okabe, A. Coburn, S. Moore, B. J. Huntly, D. Fabbro, K. C. Anderson, J. D. Griffin, and D. G. Gilliland. 2005. FGFR3 as a therapeutic target of the small molecule inhibitor PKC412 in hematopoi-etic malignancies. Oncogene 24:8259-8267.
3. Chesi, M, E. Nardini, L. A. Brents, E. Schrock, T. Ried, W. M. Kuehl, and P. L. Bergsagel. 1997. Frequent translocation t(4;14)(pl6.3;q32.3) in multiple myeloma is associated with increased expression and activating mutations of fibroblast growth factor receptor 3. Nat. Genet. 16:260-264.
4. Chesi, M, E. Nardini, R. S. Lim, K. D. Smith, W. M. Kuehl, and P. L. Bergsagel. 1998. The t(4;14) translocation in myeloma dysregulates both FGFR3 and a novel gene, MMSET, resulting in IgH/MMSET hybrid transcripts. Blood 92:3025-3034.
5. Desponts, C, A, L. Hazen, K. H. Paraiso, and W. G. Kerr. 2006. SHIP deficiency enhances HSC proliferation and survival but compromises homing and repopulation. Blood 107:4338-4345.
6. Doyonnas, R., J. S. Nielsen, S. Chelliah, E. Drew, T. Hara, A, Miyajima, and K. M. McNagny. 2005. Podocalyxin is a CD34-related marker of murine hematopoietic stem cells and embryonic erythroid cells. Blood 105:4170-4178.
7. Dufresne, S. D., C. Bjørba;aek, K. El-Haschimi, Y. Zhao, W. G. Aschenbach, D. E. Moller, and L. J. Goodyear. 2001. Altered extracellular signal-regulated kinase signaling and glycogen metabolism in skeletal muscle from p90 ribosomal S6 kinase 2 knockout mice. Mol. Cell. Biol. 21:81-87.
8. rsk. Mol. Cell. Biol. 16:1212-1219.
9. Frodin, M, C. J. Jensen, K. Merienne, and S. Gammeltoft. 2000. A phos-phoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J. 19:2924-2934.
10. Gavin, A, C., and A, R. Nebreda. 1999. A MAP kinase docking site is required for phosphorylation and activation of p90(rsk)/MAPKAP kinase-1. Curr. Biol. 9:281-284.
11. Goldberg, J., A C. Nairn, and J. Kuriyan. 1996. Structural basis for the autoinhibition of calcium/calmodulin-dependent protein kinase I. Cell 84: 875-887.
12. Grand, E. K., A, J. Chase, C. Heath, A, Rahemtulla, and N. C. Cross. 2004. Targeting FGFR3 in multiple myeloma: inhibition of t(4;14)-positive cells by SU5402 and PD173074. Leukemia 18:962-966.
13. Hart, K. C, S. C. Robertson, and D. J. Donoghue. 2001. 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 12:931-942.
14. Hinsby, A, M, J. V. Olsen, K. L. Bennett, and M. Mann. 2003. Signaling initiated by overexpression of the fibroblast growth factor receptor-1 investigated by mass spectrometry. Mol. Cell Proteomics 2:29-36.
15. Jaye, M., J. Schlessinger, and C. A. Dionne. 1992. Fibroblast growth factor receptor tyrosine kinases: molecular analysis and signal transduction. Bio-chim. Biophys. Acta 1135:185-199.
16. Jensen, C. J., M. B. Buch, T. O. Krag, B. A, Hemmings, S. Gammeltoft, and M. Frodin. 1999. 90-kDa ribosomal S6 kinase is phosphorylated and activated by 3-phosphoinositide-dependent protein kinase-1. J. Biol. Chem. 274: 27168-27176.
17. Johnson, D. E., and L. T. Williams. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv. Cancer Res. 60:141.
18. Kang, S., S. Dong, T. L. Gu, A. Guo, M. S. Cohen, S. Lonial, H. J. Khoury, D. Fabbro, D. G. Gilliland, P. L. Bergsagel, J. Taunton, R. D. Polakiewicz, and J. Chen. 2007. FGFR3 activates RSK2 to mediate hematopoietic transformation through tyrosine phosphorylation of RSK2 and activation of the MEK/ERK pathway. Cancer Cell 12:201-214.
19. Kang, S, S. Dong, A, Guo, H. Ruan, S. Lonial, H. J. Khoury, T. L. Gu, and J. Chen. 2008. Epidermal growth factor stimulates RSK2 activation through activation of the MEK/ERK pathway and Src-dependent tyrosine phosphorylation of RSK2 at Tyr-529. J. Biol. Chem. 283:4652-4657.
20. Lin, J. X., R. Spolski, and W. J. Leonard. 2008. Critical role for Rsk2 in T-lymphocyte activation. Blood 111:525-533.
21. Malakhova, M., V. Tereshko, S. Y. Lee, K. Yao, Y. Y. Cho, A, Bode, and Z. Dong. 2008. Structural basis for activation of the autoinhibitory C-terminal kinase domain of p90 RSK2. Nat. Struct. Mol. Biol. 15:112-113.
22. 2+/calmodulin-dependent protein kinase kinase. J. Biol. Chem. 273:21473-21481.
23. Paterson, J. L., Z. Li, X. Y. Wen, E. Masih-Khan, H. Chang, J. B. Pollett, S. Trudel, and A, K. Stewart. 2004. Preclinical studies of fibroblast growth factor receptor 3 as a therapeutic target in multiple myeloma. Br. J. Haema-tol 124:595-603.
24. Poteet-Smith, C. E., J. A, Smith, D. A, Lannigan, T. A, Freed, and T. W. Sturgill. 1999. Generation of constitutively active p90 ribosomal S6 kinase in vivo. Implications for the mitogen-activated protein kinase-activated protein kinase family. J. Biol. Chem. 274:22135-22138.
25. Roux, P. P., S. A, Richards, and J. Blenis. 2003. Phosphorylation of p90 ribosomal S6 kinase (RSK) regulates extracellular signal-regulated kinase docking and RSK activity. Mol. Cell. Biol. 23:4796-4804.
26. Schwaller, J., J. Frantsve, J. Aster, I. R. Williams, M. H. Tomasson, T. S. Ross, P. Peeters, L. Van Rompaey, R. A, Van Etten, R. Ilaria, Jr., P. Marynen, and D. G. Gilliland. 1998. Transformation of hematopoietic cell lines to growth-factor independence and induction of a fatal myelo- and lymphoproliferative disease in mice by retrovirally transduced TEL/JAK2 fusion genes. EMBO J. 17:5321-5333.
27. Schwaller, J., E. Parganas, D. Wang, D. Cain, J. C. Aster, I. R. Williams, C. K. Lee, R. Gerthner, T. Kitamura, J. Frantsve, E. Anastasiadou, M. L. Loh, D. E. Levy, J. N. Ihle, and D. G. Gilliland. 2000. Stat5 is essential for the myelo- and lymphoproliferative disease induced by TEL/JAK2. Mol. Cell 6:693-704.
28. Smith, J. A., C. E. Poteet-Smith, D. A, Lannigan, T. A, Freed, A, J. Zoltoski, and T. W. Sturgill. 2000. Creation of a stress-activated p90 ribosomal S6 kinase. The carboxyl-terminal tail of the MAPK-activated protein kinases dictates the signal transduction pathway in which they function. J. Biol. Chem. 275:31588-31593.
29. Smith, J. A., C. E. Poteet-Smith, K. Malarkey, and T. W. Sturgill. 1999. 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. 274:2893-2898.
30. Tavormina, P. L., R. Shiang, L. M. Thompson, Y. Z. Zhu, D. J. Wilkin, R. S. Lachman, W. R. Wilcox, D. L. Rimoin, D. H. Cohn, and J. J. Wasmuth. 1995. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat. Genet. 9:321-328.
31. Trudel, S., S. Ely, Y. Farooqi, M. Alter, D. F. Robbiani, M. Chesi, and P. L. Bergsagel. 2004. Inhibition of fibroblast growth factor receptor 3 induces differentiation and apoptosis in t(4;14) myeloma. Blood 103:3521-3528.
32. Webster, M. K., and D. J. Donoghue. 1996. Constitutive activation of fibroblast growth factor receptor 3 by the transmembrane domain point mutation found in achondroplasia. EMBO J. 15:520-527.
33. Yagasaki, F., D. Wakao, Y. Yokoyama, Y. Uchida, I. Murohashi, H. Kayano, M. Taniwaki, A. Matsuda, and M. Bessho. 2001. Fusion of ETV6 to fibroblast growth factor receptor 3 in peripheral T-cell lymphoma with a t(4; 12)(pl6;pl3) chromosomal translocation. Cancer Res. 61:8371-8374.
34. Yang, X., K. Matsuda, P. Bialek, S. Jacquot, H. C. Masuoka, T. Schinke, L. Li, S. Brancorsini, P. Sassone-Corsi, T. M. Townes, A Hanauer, and G. Karsenty. 2004. ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology: implication for Coffin-Lowry syndrome. Cell 117:387-398.