The role of senescence and prosurvival signaling in controlling the oncogenic activity of FGFR2 mutants associated with cancer and birth defects

Human Molecular Genetics

Volumn 18, Issue 14, 2009, Pages 2609-2621

  Ota, Sara ^a   Zhou, Zi Qiang ^a   Link, Jason M ^a   Hurlin, Peter J ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; BETA GALACTOSIDASE; FIBROBLAST GROWTH FACTOR RECEPTOR 2; MYC PROTEIN; PROTEIN P53;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BIRTH DEFECT; CELL AGING; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENZYME ACTIVITY; FIBROBLAST; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN CELL; MALIGNANT NEOPLASTIC DISEASE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION;

AGING; ANIMALS; CELL LINE; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CONGENITAL ABNORMALITIES; FIBROBLASTS; HUMANS; MALE; MICE; MICE, NUDE; MUTATION; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 67649857200     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp195     Document Type: Article

References (52)

1. Dailey, L., Ambrosetti, D., Mansukhani, A. and Basilico, C. (2005) Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev., 16, 233-247.
2. Chen, L. and Deng, C.X. (2005) Roles of FGF signaling in skeletal development and human genetic diseases. Front. Biosci., 10, 1961-1976.
3. Wilkie, A.O. (2005) Bad bones, absent smell, selfish testes: The pleiotropic consequences of human FGF receptor mutations. Cytokine Growth Factor Rev., 16, 187-203.
4. Jang, J.H., Shin, K.H. and Park, J.G. (2001) Mutations in fibroblast growth factor receptor 2 and fibroblast growth factor receptor 3 genes associated with human gastric and colorectal cancers. Cancer Res., 61, 3541-3543.
5. Pollock, P.M., Gartside, M.G., Dejeza, L.C., Powell, M.A., Mallon, M.A., Davies, H., Mohammadi, M., Futreal, P.A., Stratton, M.R., Trent, J.M. and Goodfellow, P.J. (2007) Frequent activating FGFR2 mutations in endometrial carcinomas parallel germline mutations associated with craniosynostosis and skeletal dysplasia syndromes. Oncogene, 26 7158-7162.
6. Byron, S.A., Gartside, M.G., Wellens, C.L., Mallon, M.A., Keenan, J.B., Powell, M.A., Goodfellow, P.J. and Pollock, P.M. (2008) Inhibition of activated fibroblast growth factor receptor 2 in endometrial cancer cells induces cell death despite PTEN abrogation. Cancer Res., 68, 6902-6907.
7. Dutt, A., Salvesen, H.B., Chen, T.H., Ramos, A.H., Onofrio, R.C., Hatton, C., Nicoletti, R., Winckler, W., Grewal, R., Hanna, M. et al. (2008) Drug-sensitive FGFR2 mutations in endometrial carcinoma. Proc. Natl Acad. Sci. USA, 105, 8713-8717.
8. Cappellen, D., De Oliveira, C., Ricol, D., de Medina, S., Bourdin, J., Sastre-Garau, X., Chopin, D., Thiery, J.P. and Radvanyi, F. (1999) Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas. Nat. Genet., 23, 18-20.
9. Chesi, M., Nardini, E., Brents, L.A., Schröck, E., Ried, T., Kuehl, W.M. and Bergsagel, P.L. (1997) 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, 260-264.
10. Richelda, R., Ronchetti, D., Baldini, L., Cro, L., Viggiano, L., Marzella, R., Rocchi, M., Otsuki, T., Lombardi, L., Maiolo, A.T. and Neri, A. (1997) A novel chromosomal translocation t(4; 14)(p16.3; q32) in multiple myeloma involves the fibroblast growth-factor receptor 3 gene. Blood, 90, 4062-4070.
11. Rand, V., Huang, J., Stockwell, T., Ferriera, S., Buzko, O., Levy, S., Busam, D., Li, K., Edwards, J.B., Eberhart, C. et al. (2005) Sequence survey of receptor tyrosine kinases reveals mutations in glioblastomas. Proc. Natl Acad. Sci. USA, 102, 14344-14349.
12. Logié, A., Dunois-Lardé, C., Rosty, C., Levrel, O., Blanche, M., Ribeiro, A., Gasc, J.M., Jorcano, J., Werner, S., Sastre-Garau, X., Thiery, J.P. and Radvanyi, F. (2005) Activating mutations of the tyrosine kinase receptor FGFR3 are associated with benign skin tumors in mice and humans. Hum. Mol. Genet., 14, 1153-1160.
13. Hafner, C., van Oers, J.M., Hartmann, A., Landthaler, M., Stoehr, R., Blaszyk, H., Hofstaedter, F., Zwarthoff, E.C. and Vogt, T. (2006) High frequency of FGFR3 mutations in adenoid seborrheic keratoses. J. Invest. Dermatol., 126, 2404-2407.
14. Hernández, S., Toll, A., Baselga, E., Ribé, A., Azua-Romeo, J., Pujol, R.M. and Real, F.X. (2007) Fibroblast growth factor receptor 3 mutation in epidermal nevi and associated low grade bladder tumors. J. Invest. Dermatol., 127, 1664-1666.
15. Easton, D.F., Pooley, K.A., Dunning, A.M., Pharoah, P.D., Thompson, D., Ballinger, D.G., Struewing, J.P., Morrison, J., Field, H., Luben, R. et al. (2007) Genome-wide association study identifies novel breast cancer susceptibility loci. Nature, 447, 1087-1093.
16. Hunter, D.J., Kraft, P., Jacobs, K.B., Cox, D.G., Yeager, M., Hankinson, S.E., Wacholder, S., Wang, Z., Welch, R., Hutchinson, A. et al. (2007) A genome-wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer. Nat. Genet., 39, 870-874.
17. Meyer, K.B., Maia, A.T., O'Reilly, M., Teschendorff, A.E., Chin, S.F., Caldas, C. and Ponder, B.A. (2008) Allele-specific up-regulation of FGFR2 increases susceptibility to breast cancer. PLoS Biol., 6 e108.
18. Katoh, M. (2008) Cancer genomics and genetics of FGFR2. Int. J. Oncol., 33, 233-237.
19. Li, Y., Mangasarian, K., Mansukhani, A. and Basilico, C. (1997) Activation of FGF receptors by mutations in the transmembrane domain. Oncogene, 14, 1397-1406.
20. Chesi, M., Brents, L.A., Ely, S.A., Bais, C., Robbiani, D.F., Mesri, E.A., Kuehl, W.M. and Bergsagel, P.L. (2001) Activated fibroblast growth factor receptor 3 is an oncogene that contributes to tumor progression in multiple myeloma. Blood, 97, 729-736.
21. 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. (2001) The myeloma-associated oncogene fibroblast growth factor receptor 3 is transforming in hematopoietic cells. Blood, 97, 2413-2419.
22. Bernard-Pierrot, I., Brams, A., Dunois-Lardé, C., Caillault, A., Diez de Medina, S.G., Cappellen, D., Graff, G., Thiery, J.P., Chopin, D., Ricol, D. and Radvanyi, F. (2006) Oncogenic properties of the mutated forms of fibroblast growth factor receptor 3b. Carcinogenesis, 27, 740-747.
23. L'Hôte, C.G. and Knowles, M.A. (2005) Cell responses to FGFR3 signalling: Growth, differentiation and apoptosis. Exp. Cell Res., 304, 417-431.
24. Shukla, V., Coumoul, X., Wang, R.H., Kim, H.S. and Deng, C.X. (2007) RNA interference and inhibition of MEK-ERK signaling prevent abnormal skeletal phenotypes in a mouse model of craniosynostosis. Nat. Genet. 39, 1145-1150.
25. Anderson, J., Burns, H.D., Enriquez-Harris, P., Wilkie, A.O. and Heath, J.K. (1998) Apert syndrome mutations in fibroblast growth factor receptor 2 exhibit increased affinity for FGF ligand. Hum. Mol. Genet., 7, 1475-1483.
26. Yu, K., Herr, A.B., Waksman, G. and Ornitz, D.M. (2000) Loss of fibroblast growth factor receptor 2 ligand-binding specificity in Apert syndrome. Proc. Natl Acad. Sci. USA, 97, 14536-14541.
27. Ibrahimi, O.A., Zhang, F., Eliseenkova, A.V., Itoh, N., Linhardt, R.J. and Mohammadi, M. (2004) Biochemical analysis of pathogenic ligand-dependent FGFR2 mutations suggests distinct pathophysiological mechanisms for craniofacial and limb abnormalities. Hum. Mol. Genet. 13, 2313-2324.
28. Serrano, M., Lin, A.W., McCurrach, M.E., Beach, D. and Lowe, S.W. (1997) Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell, 88, 593-602.
29. Lin, A.W., Barradas, M., Stone, J.C., van Aelst, L., Serrano, M. and Lowe, S.W. (1998) Premature senescence involving p53 and p16 is activated in response to constitutive MEK/MAPK mitogenic signaling. Genes Dev., 12, 3008-3019.
30. Zhu, J., Woods, D., McMahon, M. and Bishop, J.M. (1998) Senescence of human fibroblasts induced by oncogenic Raf. Genes Dev., 12, 2997-3007.
31. Chen, Z., Trotman, L.C., Shaffer, D., Lin, H.K., Dotan, Z.A., Niki, M., Koutcher, J.A., Scher, H.I., Ludwig, T., Gerald, W. et al. (2005) Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature, 43, 725-730.
32. Di Micco, R., Fumagalli, M., Cicalese, A., Piccinin, S., Gasparini, P., Luise, C., Schurra, C., Garre', M., Nuciforo, P.G., Bensimon, A. et al. (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature, 444, 638-642.
33. Mallette, F.A., Gaumont-Leclerc, M.F. and Ferbeyre, G. (2007) The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes Dev., 21, 43-48.
34. Lowe, S.W., Cepero, E. and Evan, G. (2004) Intrinsic tumour suppression. Nature, 432, 307-315.
35. Bartek, J., Bartkova, J. and Lukas, J. (2007) DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 26, 7773-7779.
36. Courtois-Cox, S., Jones, S.L. and Cichowski, K. (2008) Many roads lead to oncogene-induced senescence. Oncogene, 27, 2801-2809.
37. Harris, S.L. and Levine, A.J. (2005) The p53 pathway: Positive and negative feedback loops. Oncogene, 24, 2899-28908.
38. Trumpp, A., Refaeli, Y., Oskarsson, T., Gasser, S., Murphy, M., Martin, G.R. and Bishop, J.M. (2001) c-MYC regulates mammalian body size by controlling cell number but not cell size. Nature, 414, 768-773.
39. Bazarov, A.V., Adachi, S., Li, S.F., Mateyak, M.K., Wei, S. and Sedivy, J.M. (2001) A modest reduction in c-myc expression has minimal effects on cell growth and apoptosis but dramatically reduces susceptibility to Ras and Raf transformation. Cancer Res., 61, 1178-1186.
40. Hurlin, P.J., Zhou, Z.Q., Toyo-oka, K., Ota, S., Walker, W.L., Hirotsune, S. and Wynshaw-Boris, A. (2003) Deletion of Mnt leads to disrupted cell cycle control and tumorigenesis. EMBO J., 22, 4584-4596.
41. Zindy, F., Eischen, C.M., Randle, D.H., Kamijo, T., Cleveland, J.L., Sherr, C.J. and Roussel, M.F. (1998) Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev., 12, 2424-2433.
42. Pelengaris, S., Khan, M. and Evan, G. (2002) c-MYC: More than just a matter of life and death. Nat. Rev. Cancer, 2, 764-776.
43. Nilsson, J.A. and Cleveland, J.L. (2003) Myc pathways provoking cell suicide and cancer. Oncogene, 22, 9007-9021.
44. Mohammadi, M., Froum, S., Hamby, J.M., Schroeder, M.C., Panek, R.L., Lu, G.H., Eliseenkova, A.V., Green, D., Schlessinger, J. and Hubbard, S.R. (1998) Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J., 17, 5896-5904.
45. Halazonetis, T.D., Gorgoulis, V.G. and Bartek, J. (2008) An oncogene-induced DNA damage model for cancer development. Science, 319, 1352-1355.
46. Denoyelle, C., Abou-Rjaily, G., Bezrookove, V., Verhaegen, M., Johnson, T.M., Fullen, D.R., Pointer, J.N., Gruber, S.B., Su, L.D., Nikiforov, M.A. et al. (2006) Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nat. Cell Biol., 8, 1053-1063.
47. Courtois-Cox, S., Genther Williams, S.M., Reczek, E.E., Johnson, B.W., McGillicuddy, L.T., Johannessen, C.M., Hollstein, P.E., MacCollin, M. and Cichowski, K. (2006) A negative feedback signaling network underlies oncogene-induced senescence. Cancer Cell, 10, 459-472.
48. Walker, W., Zhou, Z.Q., Ota, S., Wynshaw-Boris, A. and Hurlin, P.J. (2005) Mnt- Max to Myc-Max complex switching regulates cell cycle entry. J. Cell Biol., 169, 405-413.
49. Wu, C.H., van Riggelen, J., Yetil, A., Fan, A.C., Bachireddy, P. and Felsher, D.W. (2007) Cellular senescence is an important mechanism of tumor regression upon c-Myc inactivation. Proc. Natl Acad. Sci. USA 104, 13028-13033.
50. Zhuang, D., Mannava, S., Grachtchouk, V., Tang, W.H., Patil, S., Wawrzyniak, J.A., Berman, A.E., Giordano, T.J., Prochownik, E.V., Soengas, M.S. et al. (2008) C-MYC overexpression is required for continuous suppression of oncogene-induced senescence in melanoma cells. Oncogene, 27, 6623-6634.
51. Kunii, K., Davis, L., Gorenstein, J., Hatch, H., Yashiro, M., Di Bacco, A., Elbi, C. and Lutterbach, B. (2008) FGFR2-amplified gastric cancer cell lines require FGFR2 and Erbb3 signaling for growth and survival. Cancer Res., 68, 2340-2348.
52. Carlson, H., Ota, S., Campbell, C.E. and Hurlin, P.J. (2001) A dominant repression domain in Tbx3 mediates transcriptional repression and cell immortalization: Relevance to mutations in Tbx3 that cause ulnar-mammary syndrome. Hum. Mol. Genet., 10, 2403-2413.