The Drosophila ubiquitin-specific protease Puffyeye regulates dMyc-mediated growth

Development (Cambridge)

Volumn 140, Issue 23, 2013, Pages 4776-4787

  Li, Ling ^a   Anderson, Sarah ^a   Secombe, Julie ^b   Eisenman, Robert N ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Deubiquitinase; Drosophila; Growth; Myc; Protein degradation

Indexed keywords

ALANINE; ASPARAGINE; COMPLEMENTARY RNA; CYCLIN E; CYSTEINE; HISTIDINE; ISOPROTEIN; LAMIN C; MYC PROTEIN; PROTEIN HYDROLYSATE; PUFFYEYE; REGULATOR PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN SPECIFIC PROTEASE; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL CYCLE; CELL GROWTH; COMPOUND EYE; DROSOPHILA; EYE DEVELOPMENT; GENE INTERACTION; GROWTH REGULATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; IN VIVO STUDY; NEGATIVE FEEDBACK; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; ORGAN GROWTH; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; TRANSPOSON; WESTERN BLOTTING;

DEUBIQUITINASE; DROSOPHILA; GROWTH; MYC; PROTEIN DEGRADATION;

ANIMALS; CELL PROLIFERATION; CYCLIN E; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; F-BOX PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; UBIQUITIN; UBIQUITIN-SPECIFIC PROTEASES; WING;

EID: 84887903330     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.096941     Document Type: Article

References (58)

1. Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans-Holm, M., Hiesinger, P. R., Schulze, K. L., Rubin, G. M. et al. (2004). The BDGP Gene Disruption Project. Genetics 167, 761-781.
2. Bellosta, P. and Gallant, P. (2010). Myc function in drosophila. Genes & Cancer 1, 542-546.
3. Bhat, K. P. and Greer, S. F. (2011). Proteolytic and non-proteolytic roles of ubiquitin and the ubiquitin proteasome system in transcriptional regulation. Biochim. Biophys. Acta 1809, 150-155.
4. Brooks, C. L. and Gu, W. (2011). p53 regulation by ubiquitin. FEBS Lett. 585, 2803-2809.
5. Brooks, C. L., Li, M., Hu, M., Shi, Y. and Gu, W. (2007). The p53-Mdm2-HAUSP complex is involved in p53 stabilization by HAUSP. Oncogene 26, 7262-7266.
6. Clague, M. J., Coulson, J. M. and Urbé, S. (2012). Cellular functions of the DUBs. J. Cell Sci. 125, 277-286.
7. Dang, C. V. (2012). MYC on the path to cancer. Cell 149, 22-35.
8. Datar, S. A., Jacobs, H. W., de la Cruz, A. F. A., Lehner, C. F. and Edgar, B. A. (2000). The Drosophila cyclin D-Cdk4 complex promotes cellular growth. EMBO J. 19, 4543-4554.
9. de Bie, P. and Ciechanover, A. (2011). Ubiquitination of E3 ligases: self-regulation of the ubiquitin system via proteolytic and non-proteolytic mechanisms. Cell Death Differ. 18, 1393-1402.
10. Dickson, B., Dietzl, G., Keleman, K.; VDRC project members (2007). RNAi construct and insertion data submitted by the Vienna Drosophila RNAi Center. FlyBase, FBrf0200327.
11. Flockhart, I., Booker, M., Kiger, A., Boutros, M., Armknecht, S., Ramadan, N., Richardson, K., Xu, A., Perrimon, N. and Mathey-Prevot, B. (2006). FlyRNAi: the drosophila RNAi screening center database. Nucleic Acids Res. 34, D489-D494.
12. Gallant, P. (2006). Myc/Max/Mad in invertebrates-the evolution of the Max network. Curr. Top. Microbiol. Immunol. 302, 235-253.
13. Gallant, P. (2009). Drosophila Myc. In Advances in Cancer Research, Vol. 103 (ed. F. V. W. George and K. George), pp. 111-144. Academic Press.
14. Gallant, P., Shiio, Y., Cheng, P. F., Parkhurst, S. M. and Eisenman, R. N. (1996). Myc and Max homologs in Drosophila. Science 274, 1523-1527.
15. Galletti, M., Riccardo, S., Parisi, F., Lora, C., Saqcena, M. K., Rivas, L., Wong, B., Serra, A., Serras, F., Grifoni, D. et al. (2009). Identification of domains responsible for ubiquitin-dependent degradation of dMyc by glycogen synthase kinase 3β and casein kinase 1 kinases. Mol. Cell. Biol. 29, 3424-3434.
16. Goodliffe, J. M., Wieschaus, E. and Cole, M. D. (2005). Polycomb mediates Myc autorepression and its transcriptional control of many loci in Drosophila. Genes Dev. 19, 2941-2946.
17. Grandori, C., Cowley, S. M., James, L. P. and Eisenman, R. N. (2000). The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16, 653-699.
18. Hann, S. R. (2006). Role of post-translational modifications in regulating c-Myc proteolysis, transcriptional activity and biological function. Semin. Cancer Biol. 16, 288-302.
19. Herranz, H. and Milán, M. (2008). Signalling molecules, growth regulators and cell cycle control in Drosophila. Cell Cycle 7, 3335-3337.
20. Hu, M., Gu, L., Li, M., Jeffrey, P. D., Gu, W. and Shi, Y. (2006). Structural basis of competitive recognition of p53 and MDM2 by HAUSP/USP7: Implications for the regulation of the p53-MDM2 pathway. PLoS Biol. 4, e27.
21. Johnston, L. A., Prober, D. A., Edgar, B. A., Eisenman, R. N. and Gallant, P. (1999). Drosophila myc regulates cellular growth during development. Cell 98, 779-790.
22. Koepp, D. M., Schaefer, L. K., Ye, X., Keyomarsi, K., Chu, C., Harper, J. W. and Elledge, S. J. (2001). Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 294, 173-177.
23. Komander, D., Clague, M. J. and Urbe, S. (2009). Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 10, 550-563.
24. Kozopas, K. M., Samos, C. H. and Nusse, R. (1998). DWnt-2, a drosophila Wnt gene required for the development of the male reproductive tract, specifies a sexually dimorphic cell fate. Genes Dev. 12, 1155-1165.
25. Liu, J. and Levens, D. (2006). Making Myc. Curr. Top Microbiol. Immunol. 302, 1-32.
26. Maines, J. Z., Stevens, L. M., Tong, X. and Stein, D. (2004). Drosophila dMyc is required for ovary cell growth and endoreplication. Development 131, 775-786.
27. Mandal, S., Freije, W. A., Guptan, P. and Banerjee, U. (2010). Metabolic control of G1-S transition: cyclin E degradation by p53-induced activation of the ubiquitin-proteasome system. J. Cell Biol. 188, 473-479.
28. Min, S.-H., Lau, A. W., Lee, T. H., Inuzuka, H., Wei, S., Huang, P., Shaik, S., Lee, D. Y., Finn, G., Balastik, M. et al. (2012). Negative regulation of the stability and tumor suppressor function of Fbw7 by the Pin1 prolyl isomerase. Mol. Cell 46, 771-783.
29. Moberg, K. H., Bell, D. W., Wahrer, D. C. R., Haber, D. A. and Hariharan, I. K. (2001). Archipelago regulates cyclin E levels in drosophila and is mutated in human cancer cell lines. Nature 413, 311-316.
30. Moberg, K. H., Mukherjee, A., Veraksa, A., Artavanis-Tsakonas, S. and Hariharan, I. K. (2004). The drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr. Biol. 14, 965-974.
31. 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.
32. Montero, L., Müller, N. and Gallant, P. (2008). Induction of apoptosis by drosophila Myc. Genesis 46, 104-111.
33. Mortimer, N. T. and Moberg, K. H. (2007). The drosophila F-box protein archipelago controls levels of the trachealess transcription factor in the embryonic tracheal system. Dev. Biol. 312, 560-571.
34. Müller, J. and Eilers, M. (2009). Ubiquitination of Myc: proteasomal degradation and beyond. In The Ubiquitin System in Health and Disease, Vol. 2008/1 (ed. S. Jentsch and B. Haendler), pp. 99-113. Berlin, Heidelberg: Springer.
35. Nakayama, K. I. and Nakayama, K. (2006). Ubiquitin ligases: cell-cycle control and cancer. Nat. Rev. Cancer 6, 369-381.
36. Nicholson, S. C., Nicolay, B. N., Frolov, M. V. and Moberg, K. H. (2011). Notchdependent expression of the archipelago ubiquitin ligase subunit in the Drosophila eye. Development 138, 251-260.
37. Orme, M. and Meier, P. (2009). Inhibitor of apoptosis proteins in drosophila: gatekeepers of death. Apoptosis 14, 950-960.
38. Parisi, F., Riccardo, S., Daniel, M., Saqcena, M., Kundu, N., Pession, A., Grifoni, D., Stocker, H., Tabak, E. and Bellosta, P. (2011). Drosophila insulin and target of rapamycin (TOR) pathways regulate GSK3 beta activity to control Myc stability and determine Myc expression in vivo. BMC Biol. 9, 65.
39. Pierce, S. B. (2004). dMyc is required for larval growth and endoreplication in drosophila. Development 131, 2317-2327.
40. Popov, N., Herold, S., Llamazares, M., Schülein, C. and Eilers, M. (2007a). Fbw7 and Usp28 regulate Myc protein stability in response to DNA damage. Cell Cycle 6, 2327-2331.
41. Popov, N., Wanzel, M., Madiredjo, M., Zhang, D., Beijersbergen, R., Bernards, R., Moll, R., Elledge, S. J. and Eilers, M. (2007b). The ubiquitin-specific protease USP28 is required for MYC stability. Nat. Cell Biol. 9, 765-774.
42. Prober, D. A. and Edgar, B. A. (2001). Growth regulation by oncogenes-new insights from model organisms. Curr. Opin. Genet. Dev. 11, 19-26.
43. Quesada, V. C., Díaz-Perales, A., Gutiérrez-Fernández, A., Garabaya, C., Cal, S. and López-Otín, C. (2004). Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases. Biochem. Biophys. Res. Commun. 314, 54-62.
44. Reyes-Turcu, F. E., Ventii, K. H. and Wilkinson, K. D. (2009). Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 78, 363-397.
45. Riemer, D., Stuurman, N., Berrios, M., Hunter, C., Fisher, P. A. and Weber, K. (1995). Expression of drosophila lamin C is developmentally regulated: analogies with vertebrate A-type lamins. J. Cell Sci. 108, 3189-3198.
46. Rorth, P., Szabo, K., Bailey, A., Laverty, T., Rehm, J., Rubin, G. M., Weigmann, K., Milan, M., Benes, V., Ansorge, W. et al. (1998). Systematic gain-of-function genetics in drosophila. Development 125, 1049-1057.
47. Secombe, J., Pispa, J., Saint, R. and Richardson, H. (1998). Analysis of a drosophila cyclin E hypomorphic mutation suggests a novel role for cyclin E in cell proliferation control during eye imaginal disc development. Genetics 149, 1867-1882.
48. Secombe, J., Li, L., Carlos, L. and Eisenman, R. N. (2007). The trithorax group protein lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 21, 537-551.
49. Sheng, Y., Saridakis, V., Sarkari, F., Duan, S., Wu, T., Arrowsmith, C. H. and Frappier, L. (2006). Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat. Struct. Mol. Biol. 13, 285-291.
50. Sowa, M. E., Bennett, E. J., Gygi, S. P. and Harper, J. W. (2009). Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403.
51. Steller, H. (2008). Regulation of apoptosis in drosophila. Cell Death Differ. 15, 1132-1138.
52. Thomas, L. R. and Tansey, W. P. (2011). Proteolytic control of the oncoprotein transcription factor Myc. In Advances in Cancer Research, Vol. 110 (ed. K. George), pp. 77-106. Academic Press.
53. Tsou, W.-L., Sheedlo, M. J., Morrow, M. E., Blount, J. R., McGregor, K. M., Das, C. and Todi, S. V. (2012). Systematic analysis of the physiological importance of deubiquitinating enzymes. PLoS ONE 7, e43112.
54. Tweedie, S., Ashburner, M., Falls, K., Leyland, P., McQuilton, P., Marygold, S., Millburn, G., Osumi-Sutherland, D., Schroeder, A., Seal, R. et al. (2009). FlyBase: enhancing drosophila gene ontology annotations. Nucleic Acids Res. 37, D555-D559.
55. Varshavsky, A. (2012). The ubiquitin system, an immense realm. Annu. Rev. Biochem. 81, 167-176.
56. Ventii, K. H. and Wilkinson, K. D. (2008). Protein partners of deubiquitinating enzymes. Biochem. J. 414, 161-175.
57. Vervoorts, J., Lüscher-Firzlaff, J. and Lüscher, B. (2006). The ins and outs of MYC regulation by posttranslational mechanisms. J. Biol. Chem. 281, 34725-34729.
58. Wu, D. C. and Johnston, L. A. (2010). Control of wing size and proportions by drosophila Myc. Genetics 184, 199-211.