Ectopic expression of wild-type FGFR3 cooperates with MYC to accelerate development of B-cell lineage neoplasms

Leukemia

Volumn 24, Issue 6, 2010, Pages 1171-1178

  Zingone, A ^a   Cultraro, C M ^a   Shin, D M ^b   Bean, C M ^a   Morse, H C ^b   Janz, S ^c   Kuehl, W M ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

FGFR3; lymphoma; multiple myeloma; Myc; oncogene

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 3; MYC PROTEIN; FGFR3 PROTEIN, HUMAN; MESSENGER RNA; MYC PROTEIN, MOUSE; TUMOR MARKER;

ARTICLE; B LYMPHOCYTE; CARCINOGENESIS; CELL LINEAGE; CELL MATURATION; CHROMOSOME TRANSLOCATION 14; CHROMOSOME TRANSLOCATION 4; CONTROLLED STUDY; LATENT PERIOD; LYMPHATIC SYSTEM TUMOR; LYMPHOID HYPERPLASIA; MOUSE; MULTIPLE MYELOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC ANIMAL; WILD TYPE; ANIMAL; B CELL LYMPHOMA; DNA MICROARRAY; ENZYME IMMUNOASSAY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; HUMAN; IMMUNOGLOBULIN GENE; IMMUNOPHENOTYPING; IMMUNOPRECIPITATION; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; TRANSGENIC MOUSE; WESTERN BLOTTING;

ANIMALS; BLOTTING, SOUTHERN; BLOTTING, WESTERN; FEMALE; GENE EXPRESSION PROFILING; GENES, IMMUNOGLOBULIN; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPHENOTYPING; IMMUNOPRECIPITATION; LYMPHOMA, B-CELL; MALE; MICE; MICE, TRANSGENIC; MULTIPLE MYELOMA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 77954603996     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2010.50     Document Type: Article

References (44)

1. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin 2007; 57: 43-66.
2. Bergsagel PL, Chesi M, Nardini E, Brents LA, Kirby SL, Kuehl WM. Promiscuous translocations into immunoglobulin heavy chain switch regions in multiple myeloma. Proc Natl Acad Sci USA 1996; 93: 13931-13936. (Pubitemid 26424223)
3. Kuehl WM, Bergsagel PL. Multiple myeloma: evolving genetic events and host interactions. Nat Rev Cancer 2002; 2: 175-187. (Pubitemid 37328787)
4. Bergsagel PL, Kuehl WM. Molecular pathogenesis and a consequent classification of multiple myeloma. J Clin Oncol 2005; 23: 6333-6338. (Pubitemid 46218843)
5. Fonseca R, Blood E, Rue M, Harrington D, Oken MM, Kyle RA et al. Clinical and biologic implications of recurrent genomic aberrations in myeloma. Blood 2003; 101: 4569-4575. (Pubitemid 36857829)
6. Barlogie B, Shaughnessy J, Tricot G, Jacobson J, Zangari M, Anaissie E et al. Treatment of multiple myeloma. Blood 2004; 103: 20-32. (Pubitemid 38029914)
7. Chng WJ, Glebov O, Bergsagel PL, Kuehl WM. Genetic events in the pathogenesis of multiple myeloma. Best Pract Res Clin Haematol 2007; 20: 571-596. (Pubitemid 350215376)
8. Chesi M, Nardini E, Lim RS, Smith KD, Kuehl WM, Bergsagel PL. The t(4;14) translocation in myeloma dysregulates both FGFR3 and a novel gene, MMSET, resulting in IgH/MMSET hybrid transcripts. Blood 1998; 92: 3025-3034. (Pubitemid 28492306)
9. Eswarakumar VP, Lax I, Schlessinger J. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 2005; 16: 139-149. (Pubitemid 40616112)
10. Dailey L, Ambrosetti D, Mansukhani A, Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 2005; 16: 233-247. (Pubitemid 40616120)
11. L'Hote CG, Knowles MA. Cell responses to FGFR3 signalling: growth, differentiation and apoptosis. Exp Cell Res 2005; 304: 417-431. (Pubitemid 40321120)
12. Onwuazor ON, Wen XY, Wang DY, Zhuang L, Masih-Khan E, Claudio J et al. Mutation, SNP, and isoform analysis of fibroblast growth factor receptor 3 (FGFR3) in 150 newly diagnosed multiple myeloma patients. Blood 2003; 102: 772-773. (Pubitemid 36842005)
13. Salazar L, Kashiwada T, Krejci P, Muchowski P, Donoghue D, Wilcox WR et al. A novel interaction between fibroblast growth factor receptor 3 and the p85 subunit of phosphoinositide 3-kinase: activation-dependent regulation of ERK by p85 in multiple myeloma cells. Hum Mol Genet 2009; 18: 1951-1961.
14. Tavormina PL, Shiang R, Thompson LM, Zhu YZ, Wilkin DJ, Lachman RS et al. Thanatophoric dysplasia (types I and II) caused by distinct mutations in fibroblast growth factor receptor 3. Nat Genet 1995; 9: 321-328.
15. Chesi M, Brents LA, Ely SA, Bais C, Robbiani DF, Mesri EA et al. Activated fibroblast growth factor receptor 3 is an oncogene that contributes to tumor progression in multiple myeloma. Blood 2001; 97: 729-736. (Pubitemid 32113407)
16. Chesi M, Nardini E, Brents LA, Schrock E, Ried T, Kuehl WM et al. 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 1997; 16: 260-264. (Pubitemid 27280209)
17. Chen J, Williams IR, Lee BH, Duclos N, Huntly BJ, Donoghue DJ et al. Constitutively activated FGFR3 mutants signal through PLCgamma-dependent and-independent pathways for hematopoietic transformation. Blood 2005; 106: 328-337. (Pubitemid 40967209)
18. Li Z, Zhu YX, Plowright EE, Bergsagel PL, Chesi M, Patterson B et al. The myeloma-associated oncogene fibroblast growth factor receptor 3 is transforming in hematopoietic cells. Blood 2001; 97: 2413-2419. (Pubitemid 32291488)
19. Khnykin D, Troen G, Berner JM, Delabie J. The expression of fibroblast growth factors and their receptors in Hodgkin's lymphoma. J Pathol 2006; 208: 431-438. (Pubitemid 43210531)
20. Gomez-Roman JJ, Saenz P, Molina M, Cuevas Gonzalez J, Escuredo K, Santa Cruz S et al. Fibroblast growth factor receptor is overexpressed in urinary tract carcinomas and modulates the neoplastic cell growth. Clin Cancer Res 2005; 11 (2 Pt 1): 459-465. (Pubitemid 40116867)
21. Tomlinson DC, Baldo O, Harnden P, Knowles MA. FGFR3 protein expression and its relationship to mutation status and prognostic variables in bladder cancer. J Pathol 2007; 213: 91-98. (Pubitemid 47354570)
22. Grose R, Dickson C. Fibroblast growth factor signaling in tumorigenesis. Cytokine Growth Factor Rev 2005; 16: 179-186. (Pubitemid 40616115)
23. Keats JJ, Reiman T, Belch AR, Pilarski LM. Ten years and counting: so what do we know about t(4;14)(p16;q32) multiple myeloma. Leuk Lymphoma 2006; 47: 2289-2300. (Pubitemid 44768421)
24. Chesi M, Bergsagel PL, Kuehl WM. The enigma of ectopic expression of FGFR3 in multiple myeloma: a critical initiating event or just a target for mutational activation during tumor progression. Curr Opin Hematol 2002; 9: 288-293. (Pubitemid 34596872)
25. Paterson JL, Li Z, Wen XY, Masih-Khan E, Chang H, Pollett JB et al. Preclinical studies of fibroblast growth factor receptor 3 as a therapeutic target in multiple myeloma. Br J Haematol 2004; 124: 595-603. (Pubitemid 38297091)
26. Trudel S, Ely S, Farooqi Y, Affer M, Robbiani DF, Chesi M et al. Inhibition of fibroblast growth factor receptor 3 induces differentiation and apoptosis in t(4;14) myeloma. Blood 2004; 103: 3521-3528. (Pubitemid 38525687)
27. Trudel S, Stewart AK, Rom E, Wei E, Li ZH, Kotzer S et al. The inhibitory anti-FGFR3 antibody, PRO-001, is cytotoxic to t(4;14) multiple myeloma cells. Blood 2006; 107: 4039-4046. (Pubitemid 43726812)
28. Trudel S, Li ZH, Wei E, Wiesmann M, Chang H, Chen C et al. CHIR-258, a novel, multitargeted tyrosine kinase inhibitor for the potential treatment of t(4;14) multiple myeloma. Blood 2005; 105: 2941-2948. (Pubitemid 40446289)
29. Masih-Khan E, Trudel S, Heise C, Li Z, Paterson J, Nadeem V et al. MIP-1alpha (CCL3) is a downstream target of FGFR3 and RAS-MAPK signaling in multiple myeloma. Blood 2006; 108: 3465-3471.
30. Qian S, Somlo G, Zhou B, Zhu L, Mi S, Mo X et al. Ribozyme cleavage leads to decreased expression of fibroblast growth factor receptor 3 in human multiple myeloma cells, which is associated with apoptosis and downregulation of vascular endothelial growth factor. Oligonucleotides 2005; 15: 1-11. (Pubitemid 40411521)
31. Iritani BM, Forbush KA, Farrar MA, Perlmutter RM. Control of B cell development by Ras-mediated activation of Raf. EMBO J 1997; 16: 7019-7031. (Pubitemid 27520802)
32. Park SS, Kim JS, Tessarollo L, Owens JD, Peng L, Han SS et al. Insertion of c-Myc into Igh induces B-cell and plasma-cell neoplasms in mice. Cancer Res 2005; 65: 1306-1315. (Pubitemid 40270157)
33. Morse III HC, Anver MR, Fredrickson TN, Haines DC, Harris AW, Harris NL et al. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood 2002; 100: 246-258. (Pubitemid 35177454)
34. Janz S, Morse H, Teitell MA. Mouse models of mature B-cell and plasma cell neoplasm. In: Li S (ed). Mouse Models of Human Blood Cancers: Basic Research and Pre-clinical Application. Springer, 2008, pp 180-200.
35. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98: 5116-5121. (Pubitemid 32397092)
36. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002; 18: 207-208. (Pubitemid 34145055)
37. Zhan F, Barlogie B, Arzoumanian V, Huang Y, Williams DR, Hollmig K et al. Gene-expression signature of benign monoclonal gammopathy evident in multiple myeloma is linked to good prognosis. Blood 2007; 109: 1692-1700. (Pubitemid 46239604)
38. Zhan F, Huang Y, Colla S, Stewart JP, Hanamura I, Gupta S et al. The molecular classification of multiple myeloma. Blood 2006; 108: 2020-2028. (Pubitemid 44395016)
39. Cariappa A, Chen L, Haider K, Tang M, Nebelitskiy E, Moran ST et al. A catalytically inactive form of protein kinase C-associated kinase/receptor interacting protein 4, a protein kinase C betaassociated kinase that mediates NF-kappa B activation, interferes with early B cell development. J Immunol 2003; 171: 1875-1880. (Pubitemid 36966470)
40. Iseki M, Kubo-Akashi C, Kwon SM, Yamaguchi A, Takatsu K, Takaki S. APS, an adaptor molecule containing PH and SH2 domains, has a negative regulatory role in B cell proliferation. Biochem Biophys Res Commun 2005; 330: 1005-1013. (Pubitemid 40462185)
41. Kim JS, Han SS, Park SS, McNeil N, Janz S. Plasma cell tumour progression in iMycEmu gene-insertion mice. J Pathol 2006; 209: 44-55.
42. Zhu D, Qi CF, Morse III HC, Janz S, Stevenson FK. Deregulated expression of the Myc cellular oncogene drives development of mouse 'Burkitt-like' lymphomas from naive B cells. Blood 2005; 105: 2135-2137. (Pubitemid 40731803)
43. Qing J, Du X, Chen Y, Chan P, Li H, Wu P et al. Antibody-based targeting of FGFR3 in bladder carcinoma and t(4;14)-positive multiple myeloma in mice. J Clin Invest 2009; 119: 1216-1229.
44. Chesi M, Robbiani DF, Sebag M, Chng WJ, Affer M, Tiedemann R et al. AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies. Cancer Cell 2008; 13: 167-180. (Pubitemid 351163163)