Fibroblast Growth Factor 2 Causes G2/M Cell Cycle Arrest in Ras-Driven Tumor Cells through a Src-Dependent Pathway

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Salotti, Jacqueline ^a,c   Dias, Matheus H ^a,b   Koga, Marianna M ^a   Armelin, Hugo A ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO BUTANTAN   (Brazil)

^c NATIONAL CANCER INSTITUTE   (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; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; 4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; FIBROBLAST GROWTH FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; RAS PROTEIN; PROTEIN KINASE P60; PROTEIN P21;

ADRENAL CORTEX CARCINOMA; ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSTASIS; EMBRYO; ENZYME INHIBITION; G2 PHASE CELL CYCLE CHECKPOINT; MITOGENESIS; MOUSE; NONHUMAN; TUMOR CELL; ANIMAL; CELL CYCLE G2 PHASE; CELL DIVISION; DNA REPLICATION; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIVISION; DNA REPLICATION; FIBROBLAST GROWTH FACTOR 2; G2 PHASE; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS P21(RAS); PROTO-ONCOGENE PROTEINS PP60(C-SRC);

EID: 84883108840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072582     Document Type: Article

References (58)

1. Itoh N, (2007) The Fgf families in humans, mice, and zebrafish: their evolutional processes and roles in development, metabolism, and disease. Biol Pharm Bull 30: 1819-1825.
2. Armelin HA, (1973) Pituitary extracts and steroid hormones in the control of 3T3 cell growth. Proc Natl Acad Sci U S A 70: 2702-2706.
3. Bottcher RT, Niehrs C, (2005) Fibroblast growth factor signaling during early vertebrate development. Endocr Rev 26: 63-77.
4. Sorensen V, Nilsen T, Wiedlocha A, (2006) Functional diversity of FGF-2 isoforms by intracellular sorting. Bioessays 28: 504-514.
5. Maret A, Galy B, Arnaud E, Bayard F, Prats H, (1995) Inhibition of fibroblast growth factor 2 expression by antisense RNA induced a loss of the transformed phenotype in a human hepatoma cell line. Cancer Res 55: 5075-5079.
6. Polnaszek N, Kwabi-Addo B, Peterson LE, Ozen M, Greenberg NM, et al. (2003) Fibroblast growth factor 2 promotes tumor progression in an autochthonous mouse model of prostate cancer. Cancer Res 63: 5754-5760.
7. Ribatti D, Vacca A, Rusnati M, Presta M, (2007) The discovery of basic fibroblast growth factor/fibroblast growth factor-2 and its role in haematological malignancies. Cytokine Growth Factor Rev 18: 327-334.
8. Korc M, Friesel RE, (2009) The role of fibroblast growth factors in tumor growth. Curr Cancer Drug Targets 9: 639-651.
9. Pardo OE, Wellbrock C, Khanzada UK, Aubert M, Arozarena I, et al. (2006) FGF-2 protects small cell lung cancer cells from apoptosis through a complex involving PKCepsilon, B-Raf and S6K2. EMBO J 25: 3078-3088.
10. Sahni M, Raz R, Coffin JD, Levy D, Basilico C, (2001) STAT1 mediates the increased apoptosis and reduced chondrocyte proliferation in mice overexpressing FGF2. Development 128: 2119-2129.
11. Westwood G, Dibling BC, Cuthbert-Heavens D, Burchill SA, (2002) Basic fibroblast growth factor (bFGF)-induced cell death is mediated through a caspase-dependent and p53-independent cell death receptor pathway. Oncogene 21: 809-824.
12. Williamson AJ, Dibling BC, Boyne JR, Selby P, Burchill SA, (2004) Basic fibroblast growth factor-induced cell death is effected through sustained activation of p38MAPK and up-regulation of the death receptor p75NTR. J Biol Chem 279: 47912-47928.
13. Wang H, Rubin M, Fenig E, DeBlasio A, Mendelsohn J, et al. (1997) Basic fibroblast growth factor causes growth arrest in MCF-7 human breast cancer cells while inducing both mitogenic and inhibitory G1 events. Cancer Res 57: 1750-1757.
14. Aikawa T, Segre GV, Lee K, (2001) Fibroblast growth factor inhibits chondrocytic growth through induction of p21 and subsequent inactivation of cyclin E-Cdk2. J Biol Chem 276: 29347-29352.
15. Krejci P, Bryja V, Pachernik J, Hampl A, Pogue R, et al. (2004) FGF2 inhibits proliferation and alters the cartilage-like phenotype of RCS cells. Exp Cell Res 297: 152-164.
16. Jackson TA, Koterwas DM, Bradford AP, (2006) Differential regulation of cell growth and gene expression by FGF-2 and FGF-4 in pituitary lactotroph GH4 cells. Mol Cell Endocrinol 247: 183-191.
17. Smits VA, van Peer MA, Essers MA, Klompmaker R, Rijksen G, et al. (2000) Negative growth regulation of SK-N-MC cells by bFGF defines a growth factor-sensitive point in G2. J Biol Chem 275: 19375-19381.
18. Costa ET, Forti FL, Matos TG, Dermargos A, Nakano F, et al. (2008) Fibroblast growth factor 2 restrains Ras-driven proliferation of malignant cells by triggering RhoA-mediated senescence. Cancer Res 68: 6215-6223.
19. Mohammadi M, Olsen SK, Ibrahimi OA, (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev 16: 107-137.
20. Eswarakumar VP, Lax I, Schlessinger J, (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16: 139-149.
21. Lee PL, Johnson DE, Cousens LS, Fried VA, Williams LT, (1989) Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. Science 245: 57-60.
22. Mansukhani A, Dell'Era P, Moscatelli D, Kornbluth S, Hanafusa H, et al. (1992) Characterization of the murine BEK fibroblast growth factor (FGF) receptor: activation by three members of the FGF family and requirement for heparin. Proc Natl Acad Sci U S A 89: 3305-3309.
23. Sleeman M, Fraser J, McDonald M, Yuan S, White D, et al. (2001) Identification of a new fibroblast growth factor receptor, FGFR5. Gene 271: 171-182.
24. Kim I, Moon S, Yu K, Kim U, Koh GY, (2001) A novel fibroblast growth factor receptor-5 preferentially expressed in the pancreas(1). Biochim Biophys Acta 1518: 152-156.
25. Johnson DE, Lee PL, Lu J, Williams LT, (1990) Diverse forms of a receptor for acidic and basic fibroblast growth factors. Mol Cell Biol 10: 4728-4736.
26. Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, et al. (1992) Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc Natl Acad Sci U S A 89: 246-250.
27. Chellaiah AT, McEwen DG, Werner S, Xu J, Ornitz DM, (1994) Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1. J Biol Chem 269: 11620-11627.
28. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, et al. (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271: 15292-15297.
29. Chaffer CL, Brennan JP, Slavin JL, Blick T, Thompson EW, et al. (2006) Mesenchymal-to-epithelial transition facilitates bladder cancer metastasis: role of fibroblast growth factor receptor-2. Cancer Res 66: 11271-11278.
30. Acevedo VD, Gangula RD, Freeman KW, Li R, Zhang Y, et al. (2007) Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Cancer Cell 12: 559-571.
31. Chang F, Steelman LS, Lee JT, Shelton JG, Navolanic PM, et al. (2003) Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia 17: 1263-1293.
32. Downward J, (2003) Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3: 11-22.
33. Yamamoto T, Ebisuya M, Ashida F, Okamoto K, Yonehara S, et al. (2006) Continuous ERK activation downregulates antiproliferative genes throughout G1 phase to allow cell-cycle progression. Curr Biol 16: 1171-1182.
34. Sewing A, Wiseman B, Lloyd AC, Land H, (1997) High-intensity Raf signal causes cell cycle arrest mediated by p21Cip1. Mol Cell Biol 17: 5588-5597.
35. Woods D, Parry D, Cherwinski H, Bosch E, Lees E, et al. (1997) Raf-induced proliferation or cell cycle arrest is determined by the level of Raf activity with arrest mediated by p21Cip1. Mol Cell Biol 17: 5598-5611.
36. Franke TF, (2008) PI3K/Akt: getting it right matters. Oncogene 27: 6473-6488.
37. Griner EM, Kazanietz MG, (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat Rev Cancer 7: 281-294.
38. Talamonti MS, Roh MS, Curley SA, Gallick GE, (1993) Increase in activity and level of pp60c-src in progressive stages of human colorectal cancer. J Clin Invest 91: 53-60.
39. Yeatman TJ, (2004) A renaissance for SRC. Nat Rev Cancer 4: 470-480.
40. Sandilands E, Serrels B, McEwan DG, Morton JP, Macagno JP, et al. (2012) Autophagic targeting of Src promotes cancer cell survival following reduced FAK signalling. Nat Cell Biol 14: 51-60.
41. Sandilands E, Akbarzadeh S, Vecchione A, McEwan DG, Frame MC, et al. (2007) Src kinase modulates the activation, transport and signalling dynamics of fibroblast growth factor receptors. EMBO Rep 8: 1162-1169.
42. Schwab M, Alitalo K, Varmus HE, Bishop JM, George D, (1983) A cellular oncogene (c-Ki-ras) is amplified, overexpressed, and located within karyotypic abnormalities in mouse adrenocortical tumour cells. Nature 303: 497-501.
43. Kovary K, Armelin MC, Armelin HA, (1989) Ha-Ras-1 oncogene dosage differentially affects Balb/3T3 cells' growth factor requirement and tumorigenicity. Oncogene Res 4: 55-64.
44. Mohammadi M, Froum S, Hamby JM, Schroeder MC, Panek RL, et al. (1998) Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J 17: 5896-5904.
45. Lotfi CF, Armelin HA, (2001) cfos and cjun antisense oligonucleotides block mitogenesis triggered by fibroblast growth factor-2 and ACTH in mouse Y1 adrenocortical cells. J Endocrinol 168: 381-389.
46. Duncia JV, Santella JB, (1998) MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 8: 2839-2844.
47. Forti FL, Schwindt TT, Moraes MS, Eichler CB, Armelin HA, (2002) ACTH promotion of p27(Kip1) induction in mouse Y1 adrenocortical tumor cells is dependent on both PKA activation and Akt/PKB inactivation. Biochemistry 41: 10133-10140.
48. Gschwendt M, Dieterich S, Rennecke J, Kittstein W, Mueller HJ, et al. (1996) Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett 392: 77-80.
49. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, et al. (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck- and FynT-dependent T cell activation. J Biol Chem 271: 695-701.
50. Frame MC, Fincham VJ, Carragher NO, Wyke JA, (2002) v-Src's hold over actin and cell adhesions. Nat Rev Mol Cell Biol 3: 233-245.
51. Berdeaux RL, Diaz B, Kim L, Martin GS, (2004) Active Rho is localized to podosomes induced by oncogenic Src and is required for their assembly and function. J Cell Biol 166: 317-323.
52. Lee HH, Tien SC, Jou TS, Chang YC, Jhong JG, et al. (2010) Src-dependent phosphorylation of ROCK participates in regulation of focal adhesion dynamics. J Cell Sci 123: 3368-3377.
53. Tanji M, Ishizaki T, Ebrahimi S, Tsuboguchi Y, Sukezane T, et al. (2010) mDia1 targets v-Src to the cell periphery and facilitates cell transformation, tumorigenesis, and invasion. Mol Cell Biol 30: 4604-4615.
54. Yasumura Y, Buonassisi V, Sato G, (1966) Clonal analysis of differentiated function in animal cell cultures. I. Possible correlated maintenance of differentiated function and the diploid karyotype. Cancer Res 26: 529-535.
55. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: R100.
56. Brummelkamp TR, Bernards R, Agami R, (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science 296: 550-553.
57. Blochlinger K, Diggelmann H, (1984) Hygromycin B phosphotransferase as a selectable marker for DNA transfer experiments with higher eucaryotic cells. Mol Cell Biol 4: 2929-2931.
58. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.