Oncogenic gene fusion FGFR3-TACC3 Is regulated by tyrosine phosphorylation

Molecular Cancer Research

Volumn 14, Issue 5, 2016, Pages 458-469

  Nelson, Katelyn N ^a   Meyer, April N ^a   Siari, Asma ^b   Campos, Alexandre R ^c   Motamedchaboki, Khatereh ^c   Donoghue, Daniel J ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIV GRENOBLE ALPES   (France)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3; HYBRID PROTEIN; SYNAPSIN II; TRANSFORMING ACIDIC COILED COIL CONTAINING PROTEIN 3; UNCLASSIFIED DRUG; FGFR3 PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; ONCOPROTEIN; TACC3 PROTEIN, HUMAN; TYROSINE;

ARTICLE; BLADDER CANCER; CARCINOGENICITY; CELL ACTIVATION; CELL GROWTH; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; DNA SEQUENCE; ENZYME ACTIVITY; FRACTIONATION; GALLBLADDER CANCER; GENE CONTROL; GENE FUSION; GENE MUTATION; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIQUID CHROMATOGRAPHY; LUNG CANCER; MEASUREMENT ACCURACY; MOUTH CANCER; ONCOGENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; THANATOPHORIC DWARFISM; UTERINE CERVIX CANCER; ANIMAL; CELL PROLIFERATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; MOUSE; NEOPLASM; NIH 3T3 CELL LINE; PHOSPHORYLATION; PROCEDURES; PROTEOMICS; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASMS; NIH 3T3 CELLS; ONCOGENE PROTEINS, FUSION; PHOSPHORYLATION; PROTEIN DOMAINS; PROTEOMICS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; TANDEM MASS SPECTROMETRY; TYROSINE;

EID: 84969135911     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-15-0497     Document Type: Article

References (47)

1. Gallo LH, Nelson KN, Meyer AN, Donoghue DJ. Functions of Fibroblast Growth Factor Receptors in cancer defined by novel translocations and mutations. Cytokine Growth Factor Rev 2015; 26:425-49.
2. Carneiro BA, Elvin JA, Kamath SD, Ali SM, Paintal AS, Restrepo A, et al. FGFR3-TACC3: A novel gene fusion in cervical cancer. Gynecol Oncol Rep 2015; 13:53-6.
3. Parker BC, Annala MJ, Cogdell DE, Granberg KJ, Sun Y, Ji P, et al. The tumorigenic FGFR3-TACC3 gene fusion escapes miR-99a regulation in glioblastoma. J Clin Invest 2013; 123:855-65.
4. Gergely F, Karlsson C, Still I, Cowell J, Kilmartin J, Raff JW. The TACC domain identifies a family of centrosomal proteins that can interact with microtubules. Proc Natl Acad Sci U S A 2000; 97: 14352-7.
5. Schuendeln MM, Piekorz RP, Wichmann C, Lee Y, McKinnon PJ, Boyd K, et al. The centrosomal, putative tumor suppressor protein TACC2 is dispensable for normal development, and deficiency does not lead to cancer. Mol Cell Biol 2004; 24:6403-9.
6. Yim EK, Tong SY, Ho EM, Bae JH, Um SJ, Park JS. Anticancer effects on TACC3 by treatment of paclitaxel in HPV-18 positive cervical carcinoma cells. Oncol Rep 2009; 21:549-57.
7. Fu W, Tao W, Zheng P, Fu J, Bian M, Jiang Q, et al. Clathrin recruits phosphorylated TACC3 to spindle poles for bipolar spindle assembly and chromosome alignment. J Cell Sci 2010; 123:3645-51.
8. Singh P, Thomas GE, Gireesh KK, Manna TK. TACC3 protein regulates microtubule nucleation by affecting gamma-Tubulin ring complexes. J Biol Chem 2014; 289:31719-35.
9. Webster MK, Donoghue DJ. Enhanced signaling and morphological transformation by a membrane-localized derivative of the fibroblast growth factor receptor 3 kinase domain. Mol Cell Biol 1997; 17: 5739-47.
10. Bell CA, Tynan JA, Hart KC, Meyer AN, Robertson SC, Donoghue DJ. Rotational coupling of the transmembrane and kinase domains of the Neu receptor tyrosine kinase. Mol Biol Cell 2000; 11:3589-99.
11. Gallo LH, Meyer AN, Motamedchaboki K, Nelson KN, Haas M, Donoghue DJ. Novel Lys63-linked ubiquitination of IKKbeta induces STAT3 signaling. Cell Cycle 2014; 13:3964-76.
12. Meyer AN, McAndrew CW, Donoghue DJ. Nordihydroguaiaretic acid inhibits an activated fibroblast growth factor receptor 3 mutant and blocks downstream signaling in multiple myeloma cells. Cancer Res 2008; 68: 7362-70.
13. Cox J, HeinMY, Luber CA, Paron I, Nagaraj N, MannM. Accurate proteomewide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics 2014; 13: 2513-26.
14. Chen J, Williams IR, Lee BH, Duclos N, Huntly BJ, Donoghue DJ, et al. Constitutively activated FGFR3 mutants signal through PLC{gamma}-dependent and-independent pathways for hematopoietic transformation. Blood 2005; 106:328-37.
15. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65:55-63.
16. Meyer AN, Drafahl KA, McAndrew CW, Gilda JE, Gallo LH, Haas M, et al. Tyrosine phosphorylation allows integration of multiple signaling inputs by IKKbeta. PLoS One 2013; 8:e84497.
17. Williams SV, Hurst CD, Knowles MA. Oncogenic FGFR3 gene fusions in bladder cancer. Hum Mol Genet 2013; 22:795-803.
18. Thakur HC, Singh M, Nagel-Steger L, Kremer J, Prumbaum D, Fansa EK, et al. The centrosomal adaptor TACC3 and the microtubule polymerase chTOG interact via defined C-Terminal subdomains in an Aurora-A kinaseindependent manner. J Biol Chem 2014; 289:74-88.
19. Lin YC, Boone M, Meuris L, Lemmens I, Van Roy N, Soete A, et al. Genome dynamics of the human embryonic kidney 293 lineage in response to cell biology manipulations. Nat Commun 2014; 5:4767.
20. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, et al. PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-Translational modifications in man and mouse. Nucleic Acids Res 2012; 40: D261-70.
21. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, et al. Quantitative phosphoproteomics revealswidespread full phosphorylation site occupancy during mitosis. Sci Signal 2010; 3:ra3.
22. Shih C, Shilo BZ, Goldfarb MP, Dannenberg A, Weinberg RA. Passage of phenotypes of chemically transformed cells via transfection of DNA and chromatin. Proc Natl Acad Sci U S A 1979; 76:5714-8.
23. Padua RA, CarterG, HughesD, GowJ, Farr C, Oscier D, et al. RASmutations in myelodysplasia detected by amplification, oligonucleotide hybridization, and transformation. Leukemia 1988; 2:503-10.
24. Bafna S, Singh AP, Moniaux N, Eudy JD, Meza JL, Batra SK. MUC4, a multifunctional transmembrane glycoprotein, induces oncogenic transformation of NIH3T3 mouse fibroblast cells. Cancer Res 2008; 68:9231-8.
25. Sun M, Wang G, Paciga JE, Feldman RI, Yuan ZQ, Ma XL, et al. AKT1/PKBalpha kinase is frequently elevated in human cancers and its constitutive activation is required for oncogenic transformation in NIH3T3 cells. Am J Pathol 2001; 159:431-7.
26. Petti LM, Irusta PM, DiMaio D. Oncogenic activation of the PDGF beta receptor by the transmembrane domain of p185neu. Oncogene 1998; 16: 843-51.
27. Roll JD, ReutherGW. ALK-Activating homologous mutations in LTK induce cellular transformation. PLoS One 2012; 7:e31733.
28. Kawai H, Matsushita H, Suzuki R, Sheng Y, Lu J, Matsuzawa H, et al. Functional analysis of the SEPT9-ABL1 chimeric fusion gene derived from T-prolymphocytic leukemia. Leuk Res 2014; 38:1451-9.
29. Tao W, Leng X, Chakraborty SN, Ma H, Arlinghaus RB. c-Abl activates janus kinase 2 in normal hematopoietic cells. J Biol Chem 2014; 289:21463-72.
30. Laneuville P, Heisterkamp N, Groffen J. Expression of the chronic myelogenous leukemia-Associated p210bcr/abl oncoprotein in a murine IL-3 dependent myeloid cell line. Oncogene 1991; 6:275-82.
31. Yamamoto Y, Kiyoi H, Nakano Y, Suzuki R, Kodera Y, Miyawaki S, et al. Activating mutation of D835 within the activation loop of FLT3 in human hematologic malignancies. Blood 2001; 97:2434-9.
32. Greenberger JS, Sakakeeny MA, Humphries RK, Eaves CJ, Eckner RJ. Demonstration of permanent factor-dependent multipotential (erythroid/neutrophil/basophil) hematopoietic progenitor cell lines. Proc Natl Acad Sci U S A 1983; 80:2931-5.
33. Migliaccio G, Migliaccio AR, Kreider BL, Rovera G, Adamson JW. Selection of lineage-restricted cell lines immortalized at different stages of hematopoietic differentiation from the murine cell line 32D. J Cell Biol 1989; 109:833-41.
34. AhmedN, Berridge MV. Regulation of glucose transport by interleukin-3 in growth factor-dependent and oncogene-Transformed bone marrowderived cell lines. Leuk Res 1997; 21:609-18.
35. Wei W, Liu W, Cassol C, Zheng W, Asa SL, Ezzat S. The breast cancer susceptibility gene FGFR2 serves as a scaffold for regulation of NF-kappabeta signaling. Mol Cell Biol 2012; 32:4662-73.
36. Johnston CL, Cox HC, Gomm JJ, Coombes RC. Fibroblast growth factor receptors (FGFRs) localize in different cellular compartments. Asplice variant of FGFR-3 localizes to the nucleus. J Biol Chem 1995; 270:30643-50.
37. Ronchetti D, Greco A, Compasso S, Colombo G, Dell'Era P, Otsuki T, et al. Deregulated FGFR3 mutants in multiple myeloma cell lines with t(4; 14): comparative analysis of Y373C, K650E and the novel G384D mutations. Oncogene 2001; 20:3553-62.
38. Tavormina PL, Shiang R, Thompson LM, Zhu YZ, Wilkin DJ, Lachman RS, et al. Thanatophoric dysplasia (types I and II) caused by distinctmutations in fibroblast growth factor receptor 3. Nat Genet 1995; 9:321-8.
39. Naski MC, Wang Q, Xu J, Ornitz DM. Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat Genet 1996; 13:233-7.
40. Hart KC, Robertson SC, Donoghue DJ. 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 2001; 12:931-42.
41. Lievens PM, Liboi E. The thanatophoric dysplasia type II mutation hampers complete maturation of FGF receptor 3, which activates STAT1 from the endoplasmic reticulum. J Biol Chem 2003; 278:17344-9.
42. Krejci P, Murakami S, Prochazkova J, Trantirek L, Chlebova K, Ouyang Z, et al. NF449 is a novel inhibitor of fibroblast growth factor receptor 3 (FGFR3) signaling active in chondrocytes and multiple myeloma cells. J Biol Chem 2010; 285:20644-53.
43. Webster MK, D'Avis PY, Robertson SC, Donoghue DJ. Profound ligandindependent kinase activation of fibroblast growth factor receptor 3 by the activation loop mutation responsible for a lethal skeletal dysplasia, thanatophoric dysplasia type II. Mol Cell Biol 1996; 16:4081-7.
44. Wu YM, Su F, Kalyana-Sundaram S, Khazanov N, Ateeq B, Cao X, et al. Identification of targetable FGFR gene fusions in diverse cancers. Cancer Discov 2013; 3:636-47.
45. Gutierrez-Caballero C, Burgess SG, Bayliss R, Royle SJ. TACC3-ch-TOG track the growing tips of microtubules independently of clathrin and Aurora-A phosphorylation. Biol Open 2015; 4:170-9.
46. Singh D, Chan JM, Zoppoli P, Niola F, Sullivan R, Castano A, et al. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 2012; 337:1231-5.
47. Acquaviva J, He S, Zhang C, Jimenez JP, Nagai M, Sang J, et al. FGFR3 translocations in bladder cancer: differential sensitivity to HSP90 inhibition based on drug metabolism. Mol Cancer Res 2014; 12:1042-54.