Control of cell number by Drosophila FOXO: Downstream and feedback regulation of the insulin receptor pathway

Genes and Development

Volumn 17, Issue 16, 2003, Pages 2006-2020

  Puig, Oscar ^a   Marr, Michael T ^a   Ruhf, M Laure ^a,b   Tjian, Robert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Drosophila; Feedback; FOXO; Growth; Insulin signaling; Transcription factor

Indexed keywords

INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ARTICLE; CELL COUNT; CELL GROWTH; CELL NUCLEUS; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; DROSOPHILA; FEEDBACK SYSTEM; GENE ACTIVATION; GENE FUNCTION; GROWTH INHIBITION; HORMONE ACTION; INSECT CELL; METAZOON; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CELL COUNT; CELL DIVISION; CELL NUCLEUS; CHROMONES; DROSOPHILA; DROSOPHILA PROTEINS; ENZYME INHIBITORS; FEEDBACK, BIOCHEMICAL; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; INSECT PROTEINS; INSULIN; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MORPHOLINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

INSECTA; METAZOA;

EID: 0042161896     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1098703     Document Type: Article

References (54)

1. Alvarez, B., Martinez, A.C., Burgering, B.M., and Carrera, A.C. 2001. Forkhead transcription factors contribute to execution of the mitotic programme in mammals. Nature 413: 744-747.
2. Andrulis, E.D., Guzman, E., Doring, P., Wemer, J., and Lis, J.T. 2000. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: Roles in promoter proximal pausing and transcription elongation. Genes & Dev. 14: 2635-2649.
3. 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.
4. Biggin, M.D. and Tjian, R. 1988. Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell 53: 699-711.
5. Bohni, R., Riesgo-Escovar, J., Oldham, S., Brogiolo, W., Stocker, H., Andruss, B.F., Beckingham, K., and Hafen, E. 1999. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97: 865-875.
6. Bozzola, J.J. and Russell, L.D. 1999. Electron microscopy, principles and techniques for biologists, 2nd ed. Jones and Bartlett, Sudbury, MA.
7. Brand, A.H. and Perrimon, N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
8. Britton, J.S., Lockwood, W.K., Li, L., Cohen, S.M., and Edgar, B.A. 2002. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2: 239-249.
9. Brogiolo, W., Stocker, H., Ikeya, T., Rintelen, F., Fernandez, R., and Hafen, E. 2001. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11: 213-221.
10. 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.
11. Burgering, B.M. and Kops, G.J. 2002. Cell cycle and death control: Long live Forkheads. Trends Biochem. Sci. 27: 352-360.
12. Cantley, L.C. 2002. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657.
13. Capdevila, J. and Guerrero, I. 1994. Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13: 4459-4468.
14. Chen, C., Jack, J., and Garofalo, R.S. 1996. The Drosophila insulin receptor is required for normal growth. Endocrinology 137: 846-856.
15. Coleman, R.A. and Pugh, B.F. 1997. Slow dimer dissociation of the TATA binding protein dictates the kinetics of DNA binding. Proc. Natl. Acad. Sci. 94: 7221-7226.
16. Datta, S.R., Brunet, A., and Greenberg, M.E. 1999. Cellular survival: A play in three Akts. Genes & Dev. 13: 2905-2927.
17. 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.
18. Durham, S.K., Suwanichkul, A., Scheimann, A.O., Yee, D., Jackson, J.G., Barr, F.G., and Powell, D.R. 1999. FKHR binds the insulin response element in the insulin-like growth factor binding protein-1 promoter. Endocrinology 140: 3140-3146.
19. Fernandez, R., Tabarini, D., Azpiazu, N., Frasch, M., and Schlessinger, J. 1995. The Drosophila insulin receptor homolog: A gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J. 14: 3373-3384.
20. Finch, C.E. and Ruvkun, G. 2001. The genetics of aging. Annu. Rev. Genomics Hum. Genet. 2: 435-462.
21. Gao, X., Neufeld, T.P., and Pan, D. 2000. Drosophila PTEN regulates cell growth and proliferation through PI3K-dependent and -independent pathways. Dev. Biol. 221: 404-418.
22. Gingras, A.C., Kennedy, S.G., O'Leary, M.A., Sonenberg, N., and Hay, N. 1998. 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes & Dev. 12: 502-513.
23. Gingras, A.C., Gygi, S.P., Raught, B., Polakiewicz, R.D., Abraham, R.T., Hoekstra, M.F., Aebersold, R., and Sonenberg, N. 1999. Regulation of 4E-BP1 phosphorylation: A novel two-step mechanism. Genes & Dev. 13: 1422-1437.
24. Gingras, A.C., Raught, B., and Sonenberg, N. 2001. Regulation of translation initiation by FRAP/mTOR. Genes & Dev. 15: 807-826.
25. Guo, S., Rena, G., Cichy, S., He, X., Cohen, P., and Unterman, T. 1999. Phosphorylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274: 17184-17192.
26. 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.
27. Hansen, S.K., Takada, S., Jacobson, R.H., Lis, J.T., and Tjian, R. 1997. Transcription properties of a cell type-specific TATA-binding protein, TRF. Cell 91: 71-83.
28. Hartwell, L.H., Culotti, J., Pringle, J.R., and Reid, B.J. 1974. Genetic control of the cell division cycle in yeast. Science 183: 46-51.
29. Hay, B.A., Wolff, T., and Rubin, G.M. 1994. Expression of baculovirus P35 prevents cell death in Drosophila. Development 120: 2121-2129.
30. Hazelett, D.J., Bourouis, M., Walldorf, U., and Treisman, J.E. 1998. decapentaplegic and wingless are regulated by eyes absent and eyegone and interact to direct the pattern of retinal differentiation in the eye disc. Development 125: 3741-3751.
31. Hekimi, S., Lakowski, B., Barnes, T.M., and Ewbank, J.J. 1998. Molecular genetics of life span in C. elegans: How much does it teach us? Trends Genet. 14: 14-20.
32. Ikeya, T., Galic, M., Belawat, P., Nairz, K., and Hafen, E. 2002. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12: 1293.
33. Johnston, L.A. and Gallant, P. 2002. Control of growth and organ size in Drosophila. Bioessays 24: 54-64.
34. Johnston, G.C., Pringle, J.R., and Hartwell, L.H. 1977. Coordination of growth with cell division in the yeast Saccharomyces cerevisiae. Exp. Cell Res. 105: 79-98.
35. Jünger, M.A., Rintelen, F., Stocker, H., Radimerski, T., Wasserman, J.D., Greenberg, M.E., and Hafen, E. 2003. Drosophila FOXO is not essential for size control but mediates growth inhibition associated with reduced insulin signaling. J. Biol. (in press).
36. 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.
37. Kozma, S.C. and Thomas, G. 2002. Regulation of cell size in growth, development and human disease: PI3K, PKB and S6K. Bioessays 24: 65-71.
38. Lee Jr., J.T. and McCubrey, J.A. 2002. The Raf/MEK/ERK signal transduction cascade as a target for chemotherapeutic intervention in leukemia. Leukemia 16: 486-507.
39. Leevers, S.J., Weinkove, D., MacDougall, L.K., Hafen, E., and Waterfield, M.D. 1996. The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J. 15: 6584-6594.
40. 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.
41. 3K/Akt signalling and cell growth in Drosophila. Nat. Cell Biol. 3: 596-601.
42. Nadal, A., Marrero, P.F., and Haro, D. 2002. Down-regulation of the mitochondrial 3-hydroxy-3-methylglutaryl-CoA synthase gene by insulin: The role of the forkhead transcription factor FKHRL1. Biochem. J. 366: 289-297.
43. Nakae, J., Kitamura, T., Silver, D.L., and Accili, D. 2001. The forkhead transcription factor Foxol (Fkhr) confers insulin sensitivity onto glucose-6-phosphatase expression. J. Clin. Invest. 108: 1359-1367.
44. Nasrin, N., Ogg, S., Cahill, C.M., Biggs, W., Nui, S., Dore, J., Calvo, D., Shi, Y., Ruvkun, G., and Alexander-Bridges, M.C. 2000. DAF-16 recruits the CREB-binding protein coactivator complex to the insulin-like growth factor binding protein 1 promoter in HepG2 cells. Proc. Natl. Acad. Sci. 97: 10412-10417.
45. 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.
46. Rousseau, D., Gingras, A.C., Pause, A., and Sonenberg, N. 1996. The eIF4E-binding proteins 1 and 2 are negative regulators of cell growth. Oncogene 13: 2415-2420.
47. Rulifson, E.J., Kim, S.K., and Nusse, R. 2002. Ablation of insulin-producing neurons in flies: Growth and diabetic phenotypes. Science 296: 1118-1120.
48. 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 Bα 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.
49. Staehling-Hampton, K. and Hoffmann, F.M. 1994. Ectopic decapentapiegic in the Drosophila midgut alters the expression of five homeotic genes, dpp, and wingless, causing specific morphological defects. Dev. Biol. 164: 502-512.
50. Stocker, H. and Hafen, E. 2000. Genetic control of cell size. Curr. Opin. Genet. Dev. 10: 529-535.
51. 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.
52. Verdu, J., Buratovich, M.A., Wilder, E.L., and Birnbaum, M.J. 1999. Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat. Cell Biol. 1: 500-506.
53. Weigmann, K., Cohen, S.M., and Lehner, C.F. 1997. Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase. Development 124: 3555-3563.
54. Yang, Z., Whelan, J., Babb, R., and Bowen, B.R. 2002. An mRNA splice variant of the AFX gene with altered transcriptional activity. J. Biol. Chem. 277: 8068-8075.