Drosophila p53-related protein kinase is required for PI3K/TOR pathway-dependent growth

Development (Cambridge)

Volumn 140, Issue 6, 2013, Pages 1282-1291

  Ibar, Consuelo ^a   Cataldo, Vicente F ^a   Vásquez Doorman, Constanza ^a,b   Olguín, Patricio ^a,c   Glavic, Álvaro ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF CHILE   (Chile)

Author keywords

Apoptosis; Cell growth; Drosophila; Prpk; TOR pathway

Indexed keywords

DROSOPHILA PROTEIN; INITIATION FACTOR 4E BINDING PROTEIN 1; P53 RELATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; ENDOCYTOSIS; ENZYME ACTIVATION; FEMALE; INSULIN METABOLISM; LARVA; MOLECULAR DYNAMICS; NONHUMAN; NUTRIENT AVAILABILITY; NUTRITIONAL STATUS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; LARVA; ORGANOGENESIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53; WING;

EID: 84874508690     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.086918     Document Type: Article

References (57)

1. Abe, Y., Matsumoto, S., Wei, S., Nezu, K., Miyoshi, A., Kito, K., Ueda, N., Shigemoto, K., Hitsumoto, Y., Nikawa, J. et al. (2001). Cloning and characterization of a p53-related protein kinase expressed in interleukin-2- activated cytotoxic T-cells, epithelial tumor cell lines, and the testes. J. Biol. Chem. 276, 44003-44011.
2. Barcelo, H. and Stewart, M. J. (2002). Altering Drosophila S6 kinase activity is consistent with a role for S6 kinase in growth. Genesis 34, 83-85.
3. 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.
4. Campos-Ortega, J. A. and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster. Berlin: Springer-Verlag.
5. Cenci, G., Ciapponi, L. and Gatti, M. (2005). The mechanism of telomere protection: a comparison between Drosophila and humans. Chromosoma 114, 135-145.
6. Colombani, J., Raisin, S., Pantalacci, S., Radimerski, T., Montagne, J. and Léopold, P. (2003). A nutrient sensor mechanism controls Drosophila growth. Cell 114, 739-749.
7. Cruz, C., Glavic, A., Casado, M. and de Celis, J. F. (2009). A gain-of-function screen identifying genes required for growth and pattern formation of the Drosophila melanogaster wing. Genetics 183, 1005-1026.
8. Danial, N. N. and Korsmeyer, S. J. (2004). Cell death: critical control points. Cell 116, 205-219.
9. Daugeron, M. C., Lenstra, T. L., Frizzarin, M., El Yacoubi, B., Liu, X., Baudin- Baillieu, A., Lijnzaad, P., Decourty, L., Saveanu, C., Jacquier, A. et al. (2011). Gcn4 misregulation reveals a direct role for the evolutionary conserved EKC/KEOPS in the t6A modification of tRNAs. Nucleic Acids Res. 39, 6148-6160.
10. de Celis, J. F. (1997). Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing. Development 124, 1007-1018.
11. Dennis, P. B., Pullen, N., Kozma, S. C. and Thomas, G. (1996). The principal rapamycin-sensitive p70(s6k) phosphorylation sites, T-229 and T-389, are differentially regulated by rapamycin-insensitive kinase kinases. Mol. Cell. Biol. 16, 6242-6251.
12. Downey, M., Houlsworth, R., Maringele, L., Rollie, A., Brehme, M., Galicia, S., Guillard, S., Partington, M., Zubko, M. K., Krogan, N. J. et al. (2006). A genome-wide screen identifies the evolutionarily conserved KEOPS complex as a telomere regulator. Cell 124, 1155-1168.
13. Dufner, A. and Thomas, G. (1999). Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 253, 100-109.
14. Edgar, B. A. (2006). How flies get their size: genetics meets physiology. Nat. Rev. Genet. 7, 907-916.
15. Efstratiadis, A. (1998). Genetics of mouse growth. Int. J. Dev. Biol. 42, 955-976.
16. El Yacoubi, B., Hatin, I., Deutsch, C., Kahveci, T., Rousset, J.-P., Iwata-Reuyl, D., Murzin, A. G. and de Crécy-Lagard, V. (2011). A role for the universal Kae1/Qri7/YgjD (COG0533) family in tRNA modification. EMBO J. 30, 882-893.
17. Facchin, S., Lopreiato, R., Stocchetto, S., Arrigoni, G., Cesaro, L., Marin, O., Carignani, G. and Pinna, L. A. (2002a). Structure-function analysis of yeast piD261/Bud32, an atypical protein kinase essential for normal cell life. Biochem. J. 364, 457-463.
18. Facchin, S., Sarno, S., Marin, O., Lopreiato, R., Sartori, G. and Pinna, L. A. (2002b). Acidophilic character of yeast PID261/BUD32, a putative ncestor of eukaryotic protein kinases. Biochem. Biophys. Res. Commun. 296, 1366-1371.
19. Facchin, S., Lopreiato, R., Ruzzene, M., Marin, O., Sartori, G., Götz, C., Montenarh, M., Carignani, G. and Pinna, L. A. (2003). Functional homology between yeast piD261/Bud32 and human PRPK: both phosphorylate p53 and PRPK partially complements piD261/Bud32 deficiency. FEBS Lett. 549, 63-66.
20. Facchin, S., Ruzzene, M., Peggion, C., Sartori, G., Carignani, G., Marin, O., Brustolon, F., Lopreiato, R. and Pinna, L. A. (2007). Phosphorylation and activation of the atypical kinase p53-related protein kinase (PRPK) by Akt/PKB. Cell. Mol. Life Sci. 64, 2680-2689.
21. Gallant, P. (2009). Drosophila Myc. Adv. Cancer Res. 103, 111-144.
22. Guertin, D. A. and Sabatini, D. M. (2007). Defining the role of mTOR in cancer. Cancer Cell 12, 9-22.
23. Hennig, K. M., Colombani, J. and Neufeld, T. P. (2006). TOR coordinates bulk and targeted endocytosis in the Drosophila melanogaster fat body to regulate cell growth. J. Cell Biol. 173, 963-974.
24. Isotani, S., Hara, K., Tokunaga, C., Inoue, H., Avruch, J. and Yonezawa, K. (1999). Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase α in vitro. J. Biol. Chem. 274, 34493-34498.
25. Kim, E., Goraksha-Hicks, P., Li, L., Neufeld, T. P. and Guan, K. L. (2008). Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 10, 935-945.
26. Kisseleva-Romanova, E., Lopreiato, R., Baudin-Baillieu, A., Rousselle, J. C., Ilan, L., Hofmann, K., Namane, A., Mann, C. and Libri, D. (2006). Yeast homolog of a cancer-testis antigen defines a new transcription complex. EMBO J. 25, 3576-3585.
27. 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.
28. Lee, S. B., Kim, S., Lee, J., Park, J., Lee, G., Kim, Y., Kim, J.-M. and Chung, J. (2007). ATG1, an autophagy regulator, inhibits cell growth by negatively regulating S6 kinase. EMBO Rep. 8, 360-365.
29. 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.
30. Lopreiato, R., Facchin, S., Sartori, G., Arrigoni, G., Casonato, S., Ruzzene, M., Pinna, L. A. and Carignani, G. (2004). Analysis of the interaction between piD261/Bud32, an evolutionarily conserved protein kinase of Saccharomyces cerevisiae, and the Grx4 glutaredoxin. Biochem. J. 377, 395-405.
31. Marshall, L., Rideout, E. J. and Grewal, S. S. (2012). Nutrient/TOR-dependent regulation of RNA polymerase III controls tissue and organismal growth in Drosophila. EMBO J. 31, 1916-1930.
32. Meléndez, A. and Neufeld, T. P. (2008). The cell biology of autophagy in metazoans: a developing story. Development 135, 2347-2360.
33. Miron, M., Verdú, J., Lachance, P. E., Birnbaum, M. J., Lasko, P. F. and Sonenberg, N. (2001). The translational inhibitor 4E-BP is an effector of PI(3)K/Akt signalling and cell growth in Drosophila. Nat. Cell Biol. 3, 596-601.
34. Miyoshi, A., Kito, K., Aramoto, T., Abe, Y., Kobayashi, N. and Ueda, N. (2003). Identification of CGI-121, a novel PRPK (p53-related protein kinase)-binding protein. Biochem. Biophys. Res. Commun. 303, 399-405.
35. Montagne, J., Stewart, M. J., Stocker, H., Hafen, E., Kozma, S. C. and Thomas, G. (1999). Drosophila S6 kinase: a regulator of cell size. Science 285, 2126-2129.
36. Nagel, A. C., Maier, D. and Preiss, A. (2002). Green fluorescent protein as a convenient and versatile marker for studies on functional genomics in Drosophila. Dev. Genes Evol. 212, 93-98.
37. O'Donnell, A. F., Tiong, S., Nash, D. and Clark, D. V. (2000). The Drosophila melanogaster ade5 gene encodes a bifunctional enzyme for two steps in the de novo purine synthesis pathway. Genetics 154, 1239-1253.
38. Oldham, S. and Hafen, E. (2003). Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol. 13, 79-85.
39. Oldham, S., Montagne, J., Radimerski, T., Thomas, G. and Hafen, E. (2000). Genetic and biochemical characterization of dTOR, the Drosophila homolog of the target of rapamycin. Genes Dev. 14, 2689-2694.
40. Ollmann, M., Young, L. M., Di Como, C. J., Karim, F., Belvin, M., Robertson, S., Whittaker, K., Demsky, M., Fisher, W. W., Buchman, A. et al. (2000). Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101, 91-101.
41. Peggion, C., Lopreiato, R., Casanova, E., Ruzzene, M., Facchin, S., Pinna, L. A., Carignani, G. and Sartori, G. (2008). Phosphorylation of the Saccharomyces cerevisiae Grx4p glutaredoxin by the Bud32p kinase unveils a novel signaling pathway involving Sch9p, a yeast member of the Akt/PKB subfamily. FEBS J. 275, 5919-5933.
42. Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E. and Zerial, M. (2005). Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436, 78-86.
43. Pullen, N. and Thomas, G. (1997). The modular phosphorylation and activation of p70s6k. FEBS Lett. 410, 78-82.
44. Purdy, A. and Su, T. T. (2004). Telomeres: not all breaks are equal. Curr. Biol. 14, R613-R614.
45. Rusten, T. E., Lindmo, K., Juhász, G., Sass, M., Seglen, P. O., Brech, A. and Stenmark, H. (2004). Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 7, 179-192.
46. Saltiel, A. R. and Kahn, C. R. (2001). Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414, 799-806.
47. Sancak, Y., Peterson, T. R., Shaul, Y. D., Lindquist, R. A., Thoreen, C. C., Bar- Peled, L. and Sabatini, D. M. (2008). The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320, 1496-1501.
48. Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A. L., Nada, S. and Sabatini, D. M. (2010). Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303.
49. Scott, R. C., Schuldiner, O. and Neufeld, T. P. (2004). Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7, 167-178.
50. Scott, R. C., Juhász, G. and Neufeld, T. P. (2007). Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 17, 1-11.
51. Sherr, C. J. (2004). Principles of tumor suppression. Cell 116, 235-246.
52. Spradling, A. C. and Rubin, G. M. (1982). Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341-347.
53. Srinivasan, M., Mehta, P., Yu, Y., Prugar, E., Koonin, E. V., Karzai, A. W. and Sternglanz, R. (2011). The highly conserved KEOPS/EKC complex is essential for a universal tRNA modification, t6A. EMBO J. 30, 873-881.
54. Stocker, H. and Hafen, E. (2000). Genetic control of cell size. Curr. Opin. Genet. Dev. 10, 529-535.
55. van Sluijters, D. A., Dubbelhuis, P. F., Blommaart, E. F. and Meijer, A. J. (2000). Amino-acid-dependent signal transduction. Biochem. J. 351, 545-550.
56. Weinkove, D. D., Neufeld, T. P. T., Twardzik, T. T., Waterfield, M. D. M. and Leevers, S. J. S. (1999). Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor. Curr. Biol. 9, 1019-1029.
57. Zhang, H., Stallock, J. P., Ng, J. C., Reinhard, C. and Neufeld, T. P. (2000). Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes Dev. 14, 2712-2724.