A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR

Cancer Cell

Volumn 2, Issue 1, 2002, Pages 81-91

  Ramaswamy, Shivapriya ^a   Nakamura, Noriaki ^a   Sansal, Isabelle ^a   Bergeron, Louise ^b   Sellers, William R ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CYCLIN D3; PUROMYCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHR; CYCLINE; DNA BINDING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXO1A PROTEIN, HUMAN; FOXO3A PROTEIN, HUMAN; ONCOPROTEIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; PTEN PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CANCER INHIBITION; CELL CYCLE; CELL TRANSFORMATION; CELL VIABILITY; CHROMATIN; DOWN REGULATION; GENE CONTROL; GENE FUNCTION; GENETIC TRANSCRIPTION; GROWTH DISORDER; HUMAN; IMMUNOPRECIPITATION; KIDNEY CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; TUMOR GROWTH; VIRUS INFECTION; ADENOVIRUS; CARCINOMA; CELL LINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLIOBLASTOMA; KIDNEY TUMOR; KINETICS; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; TUMOR SUPPRESSOR GENE;

MAMMALIA;

ADENOVIRIDAE; CARCINOMA; CELL CYCLE; CELL LINE; CYCLINS; DNA-BINDING PROTEINS; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; GLIOBLASTOMA; HUMANS; KIDNEY NEOPLASMS; KINETICS; PHOSPHORIC MONOESTER HYDROLASES; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 0036651790     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1535-6108(02)00086-7     Document Type: Article

References (44)

1. Ayala, J.E., Streeper, R.S., Desgrosellier, J.S., Durham, S.K., Suwanichkul, A., Svitek, C.A., Goldman, J.K., Barr, F.G., Powell, D.R., and O'Brien, R.M. (1999). Conservation of an insulin response unit between mouse and human glucose-6-phosphatase catalytic subunit gene promoters: transcription factor FKHR binds the insulin response sequence. Diabetes 48, 1885-1889.
2. Bates, S., Rowan, S., and Vousden, K.H. (1996). Characterisation of human cyclin G1 and G2: DNA damage inducible genes. Oncogene 13, 1103-1109.
3. Biggs, W.H., 3rd, Meisenhelder, J., Hunter, T., Cavenee, W.K., and Arden, K.C. (1999). Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc. Natl. Acad. Sci. USA 96, 7421-7426.
4. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J., and Greenberg, M.E. (1999). Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868.
5. Cheney, I.W., Johnson, D.E., Vaillancourt, M.T., Avanzini, J., Morimoto, A., Demers, G.W., Wills, K.N., Shabram, P.W., Bolen, J.B., Tavtigian, S.V., and Bookstein, R. (1998). Suppression of tumorigenicity of glioblastoma cells by adenovirus-mediated MMAC1/PTEN gene transfer. Cancer Res. 58, 2331-2334.
6. Chiang, L.W., Grenier, J.M., Ettwiller, L., Jenkins, L.P., Ficenec, D., Martin, J., Jin, F., DiStefano, P.S., and Wood, A. (2001). An orchestrated gene expression component of neuronal programmed cell death revealed by cDNA array analysis. Proc. Natl. Acad. Sci. USA 98, 2814-2819.
7. Clark, K.L., Halay, E.D., Lai, E., and Burley, S.K. (1993). Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364, 412-420.
8. Cortes, U., Moyret-Lalle, C., Falette, N., Duriez, C., Ghissassi, F.E., Barnas, C., Morel, A.P., Hainaut, P., Magaud, J.P., and Puisieux, A. (2000). BTG gene expression in the p53-dependent and-independent cellular response to DNA damage. Mol. Carcinog. 27, 57-64.
9. del Peso, L., Gonzalez, V.M., Hernandez, R., Barr, F.G., and Nunez, G. (1999). Regulation of the forkhead transcription factor FKHR, but not the PAX3-FKHR fusion protein, by the serine/threonine kinase Akt. Oncogene 18, 7328-7333.
10. Di Cristofano, A., De Acetis, M., Koff, A., Cordon-Cardo, C., and Pandolfi, P.P. (2001). Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat. Genet. 27, 222-224.
11. Dijkers, P.F., Medema, R.H., Lammers, J.W., Koenderman, L., and Coffer, P.J. (2000). Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr. Biol. 10, 1201-1204.
12. Dimri, G.P., Lee, X., Basile, G., Acosta, M., Scott, G., Roskelley, C., Medrano, E.E., Linskens, M., Rubelj, I., Pereira-Smith, O., et al. (1995). A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92, 9363-9367.
13. Dualan, R., Brody, T., Keeney, S., Nichols, A.F., Admon, A., and Linn, S. (1995). Chromosomal localization and cDNA cloning of the genes (DDB1 and DDB2) for the p127 and p48 subunits of a human damage-specific DNA binding protein. Genomics 29, 62-69.
14. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95, 14863-14868.
15. Furnari, F.B., Lin, H., Huang, H.S., and Cavenee, W.K. (1997). Growth suppression of glioma cells by PTEN requires a functional phosphatase catalytic domain. Proc. Natl. Acad. Sci. USA 94, 12479-12484.
16. Furnari, F.B., Huang, H.J., and Cavenee, W.K. (1998). The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res. 58, 5002-5008.
17. Hall, R.K., Yamasaki, T., Kucera, T., Waltner-Law, M., O'Brien, R., and Granner, D.K. (2000). Regulation of phosphoenolpyruvate carboxykinase and insulin-like growth factor-binding protein-1 gene expression by insulin. The role of winged helix/forkhead proteins. J. Biol. Chem. 275, 30169-30175.
18. He, T.C., Zhou, S., da Costa, L.T., Yu, J., Kinzler, K.W., and Vogelstein, B. (1998). A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95, 2509-2514.
19. Herwig, R., Poustka, A.J., Muller, C., Bull, C., Lehrach, H., and O'Brien, J. (1999). Large-scale clustering of cDNA-fingerprinting data. Genome Res. 9, 1093-1105.
20. Honda, Y., and Honda, S. (1999). The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J. 13, 1385-1393.
21. Jakacka, M., Ito, M., Weiss, J., Chien, P.Y., Gehm, B.D., and Jameson, J.L. (2001). Estrogen receptor binding to DNA is not required for its activity through the nonclassical AP1 pathway. J. Biol. Chem. 276, 13615-13621.
22. Jin, C., Marsden, I., Chen, X., and Liao, X. (1999). Dynamic DNA contacts observed in the NMR structure of winged helix protein-DNA complex. J. Mol. Biol. 289, 683-690.
23. Kops, G.J., de Ruiter, N.D., De Vries-Smits, A.M., Powell, D.R., Bos, J.L., and Burgering, B.M. (1999). Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398, 630-634.
24. Lin, K., Dorman, J.B., Rodan, A., and Kenyon, C. (1997). daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319-1322.
25. Maehama, T., and Dixon, J.E. (1999). PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol. 9, 125-128.
26. Medema, R.H., Kops, G.J., Bos, J.L., and Burgering, B.M. (2000). AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404, 782-787.
27. Nakamura, N., Ramaswamy, S., Vazquez, F., Signoretti, S., Loda, M., and Sellers, W.R. (2000). Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol. Cell. Biol. 20, 8969-8982.
28. Neuman, E., Ladha, M.H., Lin, N., Upton, T.M., Miller, S.J., DiRenzo, J., Pestell, R.G., Hinds, P.W., Dowdy, S.F., Brown, M., and Ewen, M.E. (1997). Cyclin D1 stimulation of estrogen receptor transcriptional activity independent of cdk4. Mol. Cell. Biol. 17, 5338-5347.
29. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G.I., Lee, L., Tissenbaum, H.A., and Ruvkun, G. (1997). The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999.
30. Pear, W.S., Nolan, G.P., Scott, M.L., and Baltimore, D. (1993). Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90, 8392-8396.
31. Rena, G., Guo, S., Cichy, S.C., Unterman, T.G., and Cohen, P. (1999). Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J. Biol. Chem. 274, 17179-17183.
32. Schmoll, D., Walker, K.S., Alessi, D.R., Grempler, R., Burchell, A., Guo, S., Walther, R., and Unterman, T.G. (2000). Regulation of glucose-6-phosphatase gene expression by protein kinase Balpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and-independent effects of insulin on promoter activity. J. Biol. Chem. 275, 36324-36333.
33. Schuur, E.R., Loktev, A.V., Sharma, M., Sun, Z., Roth, R.A., and Weigel, R.J. (2001). Ligand-dependent interaction of estrogen receptor-α with FKHR. J. Biol. Chem. 276, 33554-33560.
34. Sellers, W.R., Novitch, B.G., Miyake, S., Heith, A., Otterson, G.A., Kaye, F.J., Lassar, A.B., and Kaelin, W.G., Jr. (1998). Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev. 12, 95-106.
35. Shang, Y., Hu, X., DiRenzo, J., Lazar, M.A., and Brown, M. (2000). Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103, 843-852.
36. Takaishi, H., Konishi, H., Matsuzaki, H., Ono, Y., Shirai, Y., Saito, N., Kitamura, T., Ogawa, W., Kasuga, M., Kikkawa, U., and Nishizuka, Y. (1999). Regulation of nuclear translocation of forkhead transcription factor AFX by protein kinase B. Proc. Natl. Acad. Sci. USA 96, 11836-11841.
37. Tang, E.D., Nunez, G., Barr, F.G., and Guan, K.L. (1999). Negative regulation of the forkhead transcription factor FKHR by Akt. J. Biol. Chem. 274, 16741-16746.
38. Tomizawa, M., Kumar, A., Perrot, V., Nakae, J., Accili, D., Rechler, M.M., and Kumaro, A. (2000). Insulin inhibits the activation of transcription by a C-terminal fragment of the forkhead transcription factor FKHR. A mechanism for insulin inhibition of insulin-like growth factor-binding protein-1 transcription. J. Biol. Chem. 275, 7289-7295.
39. Tran, H., Brunet, A., Grenier, J.M., Datta, S.R., Fornace, A.J., Jr., DiStefano, P.S., Chiang, L.W., and Greenberg, M.E. (2002). DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296, 530-534.
40. Vazquez, F., and Sellers, W.R. (2000). The PTEN tumor suppressor protein: an antagonist of phosphoinositide 3-kinase signaling. Biochim. Biophys. Acta 1470, M21-M35.
41. Webb, P., Nguyen, P., Valentine, C., Lopez, G.N., Kwok, G.R., McInerney, E., Katzenellenbogen, B.S., Enmark, E., Gustafsson, J.A., Nilsson, S., and Kushner, P.J. (1999). The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol. Endocrinol. 13, 1672-1685.
42. Weigelt, J., Climent, I., Dahlman-Wright, K., and Wikstrom, M. (2001). Solution structure of the DNA binding domain of the human forkhead transcription factor AFX (FOXO4). Biochemistry 40, 5861-5869.
43. Yeagley, D., Quo, S., Unterman, T., and Quinn, P.G. (2001). Gene- and activation- specific mechanisms for insulin inhibition of basal and glucocorticoid-induced IGFBP-1 and PEPCK transcription: Roles of forkhead and insulin response sequences. J. Biol. Chem. 276, 33705-33710.
44. Zhao, H.H., Herrera, R.E., Coronado-Heinsohn, E., Yang, M.C., Ludes-Meyers, J.H., Seybold-Tilson, K.J., Nawaz, Z., Yee, D., Barr, F.G., Diab, S.G., et al. (2001). Forkhead homologue in rhabdomyosarcoma functions as a bifunctional nuclear receptor-interacting protein with both coactivator and corepressor functions. J. Biol. Chem. 276, 27907-27912.