Structural mechanisms of DREAM complex assembly and regulation

Genes and Development

Volumn 29, Issue 9, 2015, Pages 961-974

  Guiley, Keelan Z ^a   Liban, Tyler J ^a   Felthousen, Jessica G ^b,c   Ramanan, Parameshwaran ^a   Litovchick, Larisa ^b,c   Rubin, Seth M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Division of Hematology/Oncology   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Cell cycle; Cyclin dependent kinases; DREAMcomplex; MuvB; Phosphorylation; Retinoblastoma like proteins p107 and p130

Indexed keywords

CYCLIN DEPENDENT KINASE; DREAM COMPLEX; DYRK1A KINASE; ONCOPROTEIN; PHOSPHATE; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN P107; PROTEIN P130; RUBIDIUM ION; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; MULTIPROTEIN COMPLEX; MYBL2 PROTEIN, HUMAN; PROTEIN BINDING; TRANSACTIVATOR PROTEIN;

ARTICLE; CELL CYCLE; CRYSTAL STRUCTURE; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; CHEMISTRY; CRYSTALLIZATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

CELL CYCLE; CELL CYCLE PROTEINS; CRYSTALLIZATION; GENE EXPRESSION REGULATION; HUMANS; MULTIPROTEIN COMPLEXES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RETINOBLASTOMA-LIKE PROTEIN P107; RETINOBLASTOMA-LIKE PROTEIN P130; SEQUENCE ALIGNMENT; TRANS-ACTIVATORS;

EID: 84929466352     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.257568.114     Document Type: Article

References (48)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213–221.
2. Andrejka L, Wen H, Ashton J, Grant M, Iori K, Wang A, Manak JR, Lipsick JS. 2011. Animal-specific C-terminal domain links myeloblastosis oncoprotein (Myb) to an ancient repressor complex. Proc Natl Acad Sci 108: 17438–17443.
3. Bailey S. 1994. The Ccp4 suite—programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760–763.
4. Balog ER, Burke JR, Hura GL, Rubin SM. 2011. Crystal structure of the unliganded retinoblastoma protein pocket domain. Proteins 79: 2010–2014.
5. Boichuk S, Parry JA, Makielski KR, Litovchick L, Baron JL, Zewe JP, Wozniak A, Mehalek KR, Korzeniewski N, Seneviratne DS, et al. 2013. The DREAM complex mediates GIST cell quiescence and is a novel therapeutic target to enhance imatinibinduced apoptosis. Cancer Res 73: 5120–5129.
6. Burke JR, Deshong AJ, Pelton JG, Rubin SM. 2010. Phosphorylation- induced conformational changes in the retinoblastoma protein inhibit E2F transactivation domain binding. J Biol Chem 285: 16286–16293.
7. Burke JR, Hura GL, Rubin SM. 2012. Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control. Genes Dev 26: 1156–1166.
8. Canhoto AJ, Chestukhin A, Litovchick L, DeCaprio JA. 2000. Phosphorylation of the retinoblastoma-related protein p130 in growth-arrested cells. Oncogene 19: 5116–5122.
9. Cobrinik D. 2005. Pocket proteins and cell cycle control. Oncogene 24: 2796–2809.
10. Dannenberg JH, Schuijff L, Dekker M, van der Valk M, te Riele H. 2004. Tissue-specific tumor suppressor activity of etinoblastomagenehomologsp107andp130. GenesDev18: 2952–2962.
11. Dick FA, Rubin SM. 2013. Molecular mechanisms underlying RB protein function. Nat Rev Mol Cell Biol 14: 297–306.
12. Dowdy SF, Hinds PW, Louie K, Reed SI, Arnold A, Weinberg RA. 1993. Physical interaction of the retinoblastoma protein with human D cyclins. Cell 73: 499–511.
13. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126–2132.
14. Farkas T, Hansen K, Holm K, Lukas J, Bartek J. 2002. Distinct phosphorylation events regulate p130- and p107-mediated repression of E2F-4. J Biol Chem 277: 26741–26752.
15. Fera D, Schultz DC, Hodawadekar S, Reichman M, Donover PS, Melvin J, Troutman S, Kissil JL, Huryn DM, Marmorstein R. 2012. Identification and characterization of small molecule antagonists of pRb inactivation by viral oncoproteins. Chem Biol 19: 518–528.
16. Forristal C, Henley SA, MacDonald JI, Bush JR, Ort C, Passos DT, Talluri S, Ishak CA, Thwaites MJ, Norley CJ, et al. 2014. Loss of the mammalian DREAM complex deregulates chondrocyte proliferation. Mol Cell Biol 34: 2221–2234.
17. Gagrica S, Hauser S, Kolfschoten I, Osterloh L, Agami R, Gaubatz S. 2004. Inhibition of oncogenic transformation by mammalian Lin-9, a pRB-associated protein. EMBO J 23: 4627–4638.
18. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, et al. 2013. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6: p11.
19. Georlette D, Ahn S, MacAlpine DM, Cheung E, Lewis PW, Beall EL, Bell SP, Speed T, Manak JR, Botchan MR. 2007. Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev 21: 2880–2896.
20. Harrison MM, Ceol CJ, Lu X, Horvitz HR. 2006. Some C. Elegans class B synthetic multivulva proteins encode a conserved LIN- 35 Rb-containing complex distinct from a NuRD-like complex. Proc Natl Acad Sci 103: 16782–16787.
21. Henley SA, Dick FA. 2012. The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle. Cell Div 7: 10.
22. Jones RE, Wegrzyn RJ, Patrick DR, Balishin NL, Vuocolo GA, Riemen MW, Defeo-Jones D, Garsky VM, Heimbrook DC, Oliff A. 1990. Identification of HPV-16 E7 peptides that are potent antagonists of E7 binding to the retinoblastoma suppressor protein. J Biol Chem 265: 12782–12785.
23. Korenjak M, Taylor-Harding B, Binne UK, Satterlee JS, Stevaux O, Aasland R, White-Cooper H, Dyson N, Brehm A. 2004. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119: 181–193.
24. Lee JO, Russo AA, Pavletich NP. 1998. Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7. Nature 391: 859–865.
25. Lee C, Chang JH, Lee HS, Cho Y. 2002. Structural basis for the recognition of the E2F transactivation domain by the retinoblastoma tumor suppressor. Genes Dev 16: 3199–3212.
26. Leslie AG. 2006. The integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr 62: 48–57.
27. Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, Botchan MR. 2004. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev 18: 2929–2940.
28. Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, Chen R, Washburn MP, Liu XS, DeCaprio JA. 2007. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell 26: 539–551.
29. Litovchick L, Florens LA, Swanson SK, Washburn MP, DeCaprio JA. 2011. DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev 25: 801–813.
30. Mccoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658–674.
31. Morris EJ, Dyson NJ. 2001. Retinoblastoma protein partners. Adv Cancer Res 82: 1–54.
32. Muller GA, Quaas M, Schumann M, Krause E, Padi M, Fischer M, Litovchick L, DeCaprio JA, Engeland K. 2012. The CHR promoter element controls cell cycle-dependent gene transcription and binds the DREAM and MMB complexes. Nucleic Acids Res 40: 1561–1578.
33. Nor Rashid N, Yusof R, Watson RJ. 2011. Disruption of repressive p130–DREAM complexes by human papillomavirus 16 E6/E7 oncoproteins is required for cell-cycle progression in cervical cancer cells. J Gen Virol 92: 2620–2627.
34. Obenauer JC, Cantley LC, Yaffe MB. 2003. Scansite 2.0: proteome- wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31: 3635–3641.
35. Pilkinton M, Sandoval R, Colamonici OR. 2007. Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex. Oncogene 26: 7535–7543.
36. Reichert N, Wurster S, Ulrich T, Schmitt K, Hauser S, Probst L, Gotz R, Ceteci F, Moll R, Rapp U, et al. 2010. Lin9, a subunit of the mammalian DREAM complex, is essential for embryonic development, for survival of adult mice, and for tumor suppression. Mol Cell Biol 30: 2896–2908.
37. Rubin SM. 2013. Deciphering the retinoblastoma protein phosphorylation code. Trends Biochem Sci 38: 12–19.
38. Rubin SM, Gall AL, Zheng N, Pavletich NP. 2005. Structure of the Rb C-terminal domain bound to E2F1-DP1: a mechanism for phosphorylation-induced E2F release. Cell 123: 1093–1106.
39. Sadasivam S, DeCaprio JA. 2013. The DREAM complex: master coordinator of cell cycle-dependent gene expression. Nat Rev Cancer 13: 585–595.
40. Sadasivam S, Duan S, DeCaprio JA. 2012. The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev 26: 474–489.
41. Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, von Eyss B, Gagrica S, Hanel F, Brehm A, Gaubatz S. 2007. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6: 1903–1913.
42. Singh M, Krajewski M, Mikolajka A, Holak TA. 2005. Molecular determinants for the complex formation between the retinoblastoma protein and LXCXE sequences. J Biol Chem 280: 37868–37876.
43. Smith EJ, Leone G, DeGregori J, Jakoi L, Nevins JR. 1996. The accumulation of an E2F–p130 transcriptional repressor distinguishes a G0 cell state from a G1 cell state. Mol Cell Biol 16: 6965–6976.
44. Ubersax JA, Ferrell JE Jr. 2007. Mechanisms of specificity in protein phosphorylation. Nat Rev Mol Cell Biol 8: 530–541.
45. van den Heuvel S, Dyson NJ. 2008. Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Biol 9: 713–724.
46. Wen H, Andrejka L, Ashton J, Karess R, Lipsick JS. 2008. Epigenetic regulation of gene expression by Drosophila Myb and E2F2–RBF via the Myb–MuvB/dREAM complex. Genes Dev 22: 601–614.
47. Wirt SE, Sage J. 2010. p107 in the public eye: an Rb understudy and more. Cell Div 5: 9.
48. Xiao B, Spencer J, Clements A, Ali-Khan N, Mittnacht S, Broceno C, Burghammer M, Perrakis A, Marmorstein R, Gamblin SJ. 2003. Crystal structure of the retinoblastoma tumor suppressor protein bound to E2F and the molecular basis of its regulation. Proc Natl Acad Sci 100: 2363–2368.