Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control

Genes and Development

Volumn 26, Issue 11, 2012, Pages 1156-1166

  Burke, Jason R ^a   Hura, Greg L ^b   Rubin, Seth M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Cell cycle regulation; Cyclin dependent kinase; Multisite phosphorylation; Retinoblastoma protein; Small angle X ray scattering (SAXS); X ray crystal structure

Indexed keywords

CYCLIN DEPENDENT KINASE; RETINOBLASTOMA PROTEIN;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; CANONICAL ANALYSIS; CELL CYCLE REGULATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GROWTH INHIBITION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; TRANSACTIVATION;

CELL CYCLE; CRYSTALLOGRAPHY, X-RAY; CYCLIN-DEPENDENT KINASES; MODELS, MOLECULAR; PHOSPHORYLATION; RETINOBLASTOMA PROTEIN;

EID: 84861790525     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.189837.112     Document Type: Article

References (52)

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. Balog ER, Burke JR, Hura GL, Rubin SM. 2011. Crystal structure of the unliganded retinoblastoma protein pocket domain. Proteins 79: 2010-2014.
3. Binne UK, Classon MK, Dick FA, Wei W, Rape M, Kaelin WG Jr, Naar AM, Dyson NJ. 2007. Retinoblastoma protein and anaphase-promoting complex physically interact and functionally cooperate during cell-cycle exit. Nat Cell Biol 9: 225-232.
4. Brehm A, Miska EA, McCance DJ, Reid JL, Bannister AJ, Kouzarides T. 1998. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature 391: 597-601.
5. Brown VD, Phillips RA, Gallie BL. 1999. Cumulative effect of phosphorylation of pRB on regulation of E2F activity. Mol Cell Biol 19: 3246-3256.
6. Buchkovich K, Duffy LA, Harlow E. 1989. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell 58: 1097-1105.
7. Burke JR, Deshong AJ, Pelton JG, Rubin SM. Phosphorylationinduced conformational changes in the retinoblastoma protein inhibit E2F transactivation domain binding. 2010. J Biol Chem 285: 16286-16293.
8. Burkhart DL, Sage J. 2008. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 8: 671-682.
9. DeCaprio JA, Ludlow JW, Lynch D, Furukawa Y, Griffin J, Piwnica-Worms H, Huang CM, Livingston DM. 1989. The product of the retinoblastoma susceptibility gene has properties of a cell cycle regulatory element. Cell 58: 1085-1095.
10. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
11. Gorges LL, Lents NH, Baldassare JJ. 2008. The extreme COOH terminus of the retinoblastoma tumor suppressor protein pRb is required for phosphorylation on Thr-373 and activation of E2F. Am J Physiol Cell Physiol 295: C1151-C1160. doi: 10.1128/MCB.21.14.4773-4784.2001.
12. Hao B, Zheng N, Schulman BA, Wu G, Miller JJ, Pagano M, Pavletich NP. 2005. Structural basis of the Cks1-dependent recognition of p27(Kip1) by the SCF(Skp2) ubiquitin ligase. Mol Cell 20: 9-19.
13. Harbour JW, Luo RX, Dei Santi A, Postigo AA, Dean DC. 1999. Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 98: 859-869.
14. Hassler M, Singh S, Yue WW, Luczynski M, Lakbir R, Sanchez-Sanchez F, Bader T, Pearl LH, Mittnacht S. 2007. Crystal structure of the retinoblastoma protein N domain provides insight into tumor suppression, ligand interaction, and holoprotein architecture. Mol Cell 28: 371-385.
15. Hayward S, Berendsen HJ. 1998. Systematic analysis of domain motions in proteins from conformational change: New results on citrate synthase and T4 lysozyme. Proteins 30: 144-154.
16. Hinds PW, Mittnacht S, Dulic V, Arnold A, Reed SI, Weinberg RA. 1992. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell 70: 993-1006.
17. Holt LJ, Tuch BB, Villen J, Johnson AD, Gygi SP, Morgan DO. 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325: 1682-1686.
18. Howell PL, Smith GD. 1992. Identification of heavy-atom derivatives by normal probability methods. J Appl Crystallogr 25: 81-86.
19. Hura GL, Menon AL, Hammel M, Rambo RP, Poole FL II, Tsutakawa SE, Jenney FE Jr, Classen S, Frankel KA, Hopkins RC, et al. 2009. Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS). Nat Methods 6: 606-612.
20. Ji P, Jiang H, Rekhtman K, Bloom J, Ichetovkin M, Pagano M, Zhu L. 2004. An Rb-Skp2-p27 pathway mediates acute cell cycle inhibition by Rb and is retained in a partial-penetrance Rb mutant. Mol Cell 16: 47-58.
21. Kim SY, Ferrell JE Jr. 2007. Substrate competition as a source of ultrasensitivity in the inactivation of Wee1. Cell 128: 1133-1145.
22. Knudsen ES, Wang JY. 1996. Differential regulation of retinoblastoma protein function by specific Cdk phosphorylation sites. J Biol Chem 271: 8313-8320.
23. Knudsen ES, Wang JY. 1997. Dual mechanisms for the inhibition of E2F binding to RB by cyclin-dependent kinase-mediated RB phosphorylation. Mol Cell Biol 17: 5771-5783.
24. Koivomagi M, Valk E, Venta R, Iofik A, Lepiku M, Balog ER, Rubin SM, Morgan DO, Loog M. 2011. Cascades of multisite phosphorylation control Sic1 destruction at the onset of S phase. Nature 480: 128-131.
25. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: AWindows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 36: 1277-1282.
26. Konarev PV, Petoukhov MV, Volkov VV, Svergun DI. 2006. ATSAS 2.1, a program package for small-angle scattering data analysis. J Appl Crystallogr 39: 277-286.
27. 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.
28. 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.
29. Lees JA, Buchkovich KJ, Marshak DR, Anderson CW, Harlow E. 1991. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J 10: 4279-4290.
30. Lents NH, Gorges LL, Baldassare JJ. 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.
31. Leslie AG. 2006. The integration of macromolecular diffraction data. Acta Crystallogr D Biol Crystallogr 62: 48-57.
32. Liu X, Marmorstein R. 2007. Structure of the retinoblastoma protein bound to adenovirus E1A reveals the molecular basis for viral oncoprotein inactivation of a tumor suppressor. Genes Dev 21: 2711-2716.
33. Manning AL, Dyson NJ. 2011. pRB, a tumor suppressor with a stabilizing presence. Trends Cell Biol 21: 433-441.
34. Mccoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40: 658-674.
35. Mimura S, Seki T, Tanaka S, Diffley JF. 2004. Phosphorylationdependent binding of mitotic cyclins to Cdc6 contributes to DNA replication control. Nature 431: 1118-1123.
36. Nash P, Tang X, Orlicky S, Chen Q, Gertler FB, Mendenhall MD, Sicheri F, Pawson T, Tyers M. 2001. Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414: 514-521.
37. Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, O'Carroll D, Firestein R, Cleary M, Jenuwein T, Herrera RE, et al. 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412: 561-565.
38. Orlicky S, Tang X, Willems A, Tyers M, Sicheri F. 2003. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 112: 243-256.
39. Pelikan M, Hura GL, Hammel M. 2009. Structure and flexibility within proteins as identified through small angle X-ray scattering. Gen Physiol Biophys 28: 174-189.
40. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
41. Putnam CD, Hammel M, Hura GL, Tainer JA. 2007. X-ray solution scattering (SAXS) combined with crystallography and computation: Defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 40: 191-285.
42. Rambo RP, Tainer JA. 2011. Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law. Biopolymers 95: 559-571.
43. 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.
44. Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
45. Schneidman-Duhovny D, Hammel M, Sali A. 2010. FoXS: A Web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res 38: W540-W544. doi: 10.1093/nar/gkq461.
46. Singh M, Krajewski M, Mikolajka A, Holak TA. 2005. Molecular determinants for the complex formation between the reti-noblastoma protein and LXCXE sequences. J Biol Chem 280: 37868-37876.
47. Svergun DI. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 25: 495-503.
48. Svergun DI, Petoukhov MV, Koch MH. 2001. Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80: 2946-2953.
49. van den Heuvel S, Dyson NJ. 2008. Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Biol 9: 713-724.
50. Weinberg RA. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323-330.
51. 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.
52. Zarkowska T, Mittnacht S. 1997. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J Biol Chem 272: 12738-12746.