Integrated stability and activity control of the Drosophila Rbf1 retinoblastoma protein

Journal of Biological Chemistry

Volumn 289, Issue 36, 2014, Pages 24863-24873

  Zhang, Liang ^a   Wei, Yiliang ^b   Pushel, Irina ^b   Heinze, Karolin ^c   Elenbaas, Jared ^b   Henry, R William ^a,b   Arnosti, David N ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; MAMMALS; STABILITY; TRANSCRIPTION;

ENHANCED STABILITY; FUNCTIONAL RELATIONSHIP; INTEGRATED STABILITY; KINASE REGULATION; N-TERMINAL THREONINE RESIDUES; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN TURNOVERS; RETINOBLASTOMA PROTEIN;

PROTEINS;

CYCLIN DEPENDENT KINASE ACTIVATING KINASE; INSECT PROTEIN; MUTANT PROTEIN; RETINOBLASTOMA PROTEIN; TUMOR SUPPRESSOR PROTEIN; CYCLIN DEPENDENT KINASE; CYCLINE; DROSOPHILA PROTEIN; LYSINE; RBF1 PROTEIN, DROSOPHILA; SERINE; THREONINE; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CONTROLLED STUDY; DROSOPHILA; EYE DEVELOPMENT; GENE MUTATION; GENETIC CONSERVATION; GENOMIC INSTABILITY; NONHUMAN; PHENOTYPE; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; SENESCENCE; ANIMAL; BINDING SITE; CELL LINE; ELECTRON MICROSCOPY; EYE; FORELIMB; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MUTATION; PHOSPHORYLATION; TRANSGENIC ANIMAL; ULTRASTRUCTURE; WESTERN BLOTTING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BINDING SITES; BLOTTING, WESTERN; CELL LINE; CYCLIN-DEPENDENT KINASES; CYCLINS; DROSOPHILA PROTEINS; EYE; HUMANS; LYSINE; MICROSCOPY, ELECTRON; MUTATION; PHOSPHORYLATION; PROTEIN STABILITY; SERINE; THREONINE; TRANSCRIPTION FACTORS; WING;

EID: 84906972184     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.586818     Document Type: Article

References (44)

1. Burkhart, D. L., and Sage, J. (2008) Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer 8, 671-682
2. Chau, B. N., and Wang, J. Y. (2003) Coordinated regulation of life and death by RB. Nat. Rev. Cancer 3, 130-138
3. Munro, S., Carr, S. M., and La Thangue, N. B. (2012) Diversity within the pRb pathway: is there a code of conduct? Oncogene 31, 4343-4352
4. Classon, M., and Dyson, N. (2001) p107 and p130: versatile proteins with interesting pockets. Exp. Cell Res. 264, 135-147
5. Mittnacht, S. (1998) Control of pRB phosphorylation. Curr. Opin. Genet. Dev. 8, 21-27
6. Delston, R. B., Matatall, K. A., Sun, Y., Onken, M. D., and Harbour, J. W. (2011) p38 phosphorylates Rb on Ser567 by a novel, cell cycle-independent mechanism that triggers Rb-Hdm2 interaction and apoptosis. Oncogene 30, 588-599
7. Inoue, Y., Kitagawa, M., and Taya, Y. (2007) Phosphorylation of pRB at Ser612 by Chk1/2 leads to a complex between pRB and E2F-1 after DNA damage. EMBO J. 26, 2083-2093
8. Buchkovich, K., Duffy, L. A., and Harlow, E. (1989) The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58, 1097-1105
9. Tedesco, D., Lukas, J., and Reed, S. I. (2002) The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCF(Skp2). Genes Dev. 16, 2946-2957
10. Rubin, S. M. (2013) Deciphering the retinoblastoma protein phosphorylation code. Trends Biochem. Sci 38, 12-19
11. Adams, P. D. (2001) Regulation of the retinoblastoma tumor suppressor protein by cyclin/cdks. Biochim. Biophys. Acta 1471, M123-M133
12. 1/S cyclin-dependent kinases. J. Biol. Chem. 272, 12738-12746
13. Knudsen, E. S., and Wang, J. Y. (1996) Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J. Biol. Chem. 271, 8313-8320
14. Uchida, C., Miwa, S., Kitagawa, K., Hattori, T., Isobe, T., Otani, S., Oda, T., Sugimura, H., Kamijo, T., Ookawa, K., Yasuda, H., and Kitagawa, M. (2005) Enhanced Mdm2 activity inhibits pRB function via ubiquitin-dependent degradation. EMBO J. 24, 160-169
15. Sdek, P., Ying, H., Chang, D. L., Qiu, W., Zheng, H., Touitou, R., Allday, M. J., and Xiao, Z. X. (2005) MDM2 promotes proteasome-dependent ubiquitin-independent degradation of retinoblastoma protein. Mol. Cell 20, 699-708
16. Sdek, P., Ying, H., Zheng, H., Margulis, A., Tang, X., Tian, K., and Xiao, Z. X. (2004) The central acidic domain of MDM2 is critical in inhibition of retinoblastoma-mediated suppression of E2F and cell growth. J. Biol. Chem. 279, 53317-53322
17. Rubin, S. M., Gall, A. L., Zheng, N., and Pavletich, N. P. (2005) Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release. Cell 123, 1093-1106
18. van den Heuvel, S., and Dyson, N. J. (2008) Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9, 713-724
19. Xin, S., Weng, L., Xu, J., and Du, W. (2002) The role of RBF in developmentally regulated cell proliferation in the eye disc and in Cyclin D/Cdk4 induced cellular growth. Development 129, 1345-1356
20. Ullah, Z., Buckley, M. S., Arnosti, D. N., and Henry, R. W. (2007) Retinoblastoma protein regulation by the COP9 signalosome. Mol. Biol. Cell 18, 1179-1186
21. Acharya, P., Raj, N., Buckley, M. S., Zhang, L., Duperon, S., Williams, G., Henry, R. W., and Arnosti, D. N. (2010) Paradoxical instability-activity relationship defines a novel regulatory pathway for retinoblastoma proteins. Mol. Biol. Cell 21, 3890-3901
22. Raj, N., Zhang, L., Wei, Y., Arnosti, D. N., and Henry, R. W. (2012) Ubiquitination of retinoblastoma family protein 1 potentiates gene-specific repression function. J. Biol. Chem. 287, 41835-41843
23. Ryu, J. R., and Arnosti, D. N. (2003) Functional similarity of Knirps CtBP-dependent and CtBP-independent transcriptional repressor activities. Nucleic Acids Res. 31, 4654-4662
24. Bischof, J., Maeda, R. K., Hediger, M., Karch, F., and Basler, K. (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. U.S.A. 104, 3312-3317
25. Kinoshita, E., and Kinoshita-Kikuta, E. (2011) Improved Phos-tag SDS-PAGE under neutral pH conditions for advanced protein phosphorylation profiling. Proteomics 11, 319-323
26. Frolov, M. V., Stevaux, O., Moon, N. S., Dimova, D., Kwon, E. J., Morris, E. J., and Dyson, N. J. (2003) G1 cyclin-dependent kinases are insufficient to reverse dE2F2-mediated repression. Genes Dev. 17, 723-728
27. Gilbert, M. K., Tan, Y. Y., and Hart, C. M. (2006) The Drosophila boundary element-associated factors BEAF-32A and BEAF-32B affect chromatin structure. Genetics 173, 1365-1375
28. Zhai, B., Villén, J., Beausoleil, S. A., Mintseris, J., and Gygi, S. P. (2008) Phosphoproteome analysis of Drosophila melanogaster embryos. J. Proteome Res. 7, 1675-1682
29. Cantin, G. T., Yi, W., Lu, B., Park, S. K., Xu, T., Lee, J. D., and Yates, J. R., 3rd (2008) Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J. Proteome Res. 7, 1346-1351
30. Mayya, V., Lundgren, D. H., Hwang, S. I., Rezaul, K., Wu, L., Eng, J. K., Rodionov, V., and Han, D. K. (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci. Signal 2, ra46
31. Gauci, S., Helbig, A. O., Slijper, M., Krijgsveld, J., Heck, A. J., and Mohammed, S. (2009) Lys-N and trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal. Chem. 81, 4493-4501
32. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 105, 10762-10767
33. Leng, X., Noble, M., Adams, P. D., Qin, J., and Harper, J. W. (2002) Reversal of growth suppression by p107 via direct phosphorylation by cyclin D1/cyclin-dependent kinase 4. Mol. Cell Biol. 22, 2242-2254
34. Canhoto, A. J., Chestukhin, A., Litovchick, L., and DeCaprio, J. A. (2000) Phosphorylation of the retinoblastoma-related protein p130 in growth-arrested cells. Oncogene 19, 5116-5122
35. Kitagawa, M., Higashi, H., Jung, H. K., Suzuki-Takahashi, I., Ikeda, M., Tamai, K., Kato, J., Segawa, K., Yoshida, E., Nishimura, S., and Taya, Y. (1996) The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15, 7060-7069
36. Burke, J. R., Hura, G. L., and Rubin, S. M. (2012) Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control. Genes Dev. 26, 1156-1166
37. Lents, N. H., Gorges, L. L., and Baldassare, J. J. (2006) Reverse mutational analysis reveals threonine-373 as a potentially sufficient phosphorylation site for inactivation of the retinoblastoma tumor suppressor protein (pRB). Cell Cycle 5, 1699-1707
38. Narasimha, A. M., Kaulich, M., Shapiro, G. S., Choi, Y. J., Sicinski, P., and Dowdy, S. F. (2014) Cyclin D activates the Rb tumor suppressor by monophosphorylation. Elife (Cambridge) e02872
39. Adams, P. D., Li, X., Sellers, W. R., Baker, K. B., Leng, X., Harper, J. W., Taya, Y., and Kaelin, W. G., Jr. (1999) Retinoblastoma protein contains a C-terminal motif that targets it for phosphorylation by cyclin-cdk complexes. Mol. Cell Biol. 19, 1068-1080
40. Carr, S. M., Munro, S., Kessler, B., Oppermann, U., and La Thangue, N. B. (2011) Interplay between lysine methylation and Cdk phosphorylation in growth control by the retinoblastoma protein. EMBO J. 30, 317-327
41. Saeed, M., Schwarze, F., Loidl, A., Meraner, J., Lechner, M., and Loidl, P. (2012) In vitro phosphorylation and acetylation of the murine pocket protein Rb2/p130. PLoS One 7, e46174
42. Claudio, P. P., Howard, C. M., Pacilio, C., Cinti, C., Romano, G., Minimo, C., Maraldi, N. M., Minna, J. D., Gelbert, L., Leoncini, L., Tosi, G. M., Hicheli, P., Caputi, M., Giordano, G. G., and Giordano, A. (2000) Mutations in the retinoblastoma-related gene RB2/p130 in lung tumors and suppression of tumor growth in vivo by retrovirus-mediated gene transfer. Cancer Res. 60, 372-382
43. Modi, S., Kubo, A., Oie, H., Coxon, A. B., Rehmatulla, A., and Kaye, F. J. (2000) Protein expression of the RB-related gene family and SV40 large T antigen in mesothelioma and lung cancer. Oncogene 19, 4632-4639
44. Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A. A., Kim, S., Wilson, C. J., Lehár, J., Kryukov, G. V., Sonkin, D., Reddy, A., Liu, M., Murray, L., Berger, M. F., Monahan, J. E., Morais, P., Meltzer, J., Korejwa, A., Jané-Valbuena, J., Mapa, F. A., Thibault, J., Bric-Furlong, E., Raman, P., Shipway, A., Engels, I. H., Cheng, J., Yu, G. K., Yu, J., Aspesi, P., Jr., de Silva, M., Jagtap, K., Jones, M. D., Wang, L., Hatton, C., Palescandolo, E., Gupta, S., Mahan, S., Sougnez, C., Onofrio, R. C., Liefeld, T., MacConaill, L., Winckler, W., Reich, M., Li, N., Mesirov, J. P., Gabriel, S. B., Getz, G., Ardlie, K., Chan, V., Myer, V. E., Weber, B. L., Porter, J., Warmuth, M., Finan, P., Harris, J. L., Meyerson, M., Golub, T. R., Morrissey, M. P., Sellers, W. R., Schlegel, R., and Garraway, L. A. (2012) The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483, 603-607