Targeting mechanism of the retinoblastoma tumor suppressor by a prototypical viral oncoprotein: Structural modularity, intrinsic disorder and phosphorylation of human papillomavirus E7

FEBS Journal

Volumn 277, Issue 4, 2010, Pages 973-988

  Chemes, Lucía B ^a   Sánchez, Ignacio E ^a   Smal, Clara ^a   De Prat Gay, Gonzalo ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

LxCxE motif; Natively unfolded proteins; Phosphorylation; Retinoblastoma protein; Viral oncoprotein

Indexed keywords

CASEIN KINASE II; CELL PROTEIN; MONOMER; PROTEIN E7; RETINOBLASTOMA PROTEIN;

ALPHA HELIX; ARTICLE; BINDING AFFINITY; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; VIRUS CELL TRANSFORMATION;

AMINO ACID SEQUENCE; CASEIN KINASE II; CONSERVED SEQUENCE; HUMAN PAPILLOMAVIRUS 16; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RETINOBLASTOMA PROTEIN;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

EID: 76149146350     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07540.x     Document Type: Article

References (79)

1. Friend SH, Bernards R, Rogelj S, Weinberg RA, Rapaport JM, Albert DM Dryja TP (1986) A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma. Nature 323, 643 646.
2. Lohmann DR (1999) RB1 gene mutations in retinoblastoma. Hum Mutat 14, 283 288.
3. Valverde JR, Alonso J, Palacios I Pestana A (2005) RB1 gene mutation up-date, a meta-analysis based on 932 reported mutations available in a searchable database. BMC Genet 6, 53.
4. Burkhart DL Sage J (2008) Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 8, 671 682.
5. Hiebert SW, Chellappan SP, Horowitz JM Nevins JR (1992) The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev 6, 177 185.
6. Khidr L Chen PL (2006) RB, the conductor that orchestrates life, death and differentiation. Oncogene 25, 5210 5219.
7. Morris EJ Dyson NJ (2001) Retinoblastoma protein partners. Adv Cancer Res 82, 1 54.
8. 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.
9. 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.
10. 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.
11. Chow KN Dean DC (1996) Domains A and B in the Rb pocket interact to form a transcriptional repressor motif. Mol Cell Biol 16, 4862 4868.
12. Sellers WR, Rodgers JW Kaelin WG Jr. (1995) A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc Natl Acad Sci USA 92, 11544 11548.
13. Stokes PH, Thompson LS, Marianayagam NJ Matthews JM (2007) Dimerization of CtIP may stabilize in vivo interactions with the Retinoblastoma-pocket domain. Biochem Biophys Res Commun 354, 197 202.
14. Magnaghi-Jaulin L, Groisman R, Naguibneva I, Robin P, Lorain S, Le Villain JP, Troalen F, Trouche D Harel-Bellan A (1998) Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 391, 601 605.
15. Dyson N, Guida P, McCall C Harlow E (1992) Adenovirus E1A makes two distinct contacts with the retinoblastoma protein. J Virol 66, 4606 4611.
16. 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 USA 100, 2363 2368.
17. Dick FA (2007) Structure-function analysis of the retinoblastoma tumor suppressor protein - is the whole a sum of its parts? Cell Div 2, 26.
18. 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.
19. McLaughlin-Drubin ME Munger K (2009) The human papillomavirus E7 oncoprotein. Virology 384, 335 344.
20. Helt AM, Funk JO Galloway DA (2002) Inactivation of both the retinoblastoma tumor suppressor and p21 by the human papillomavirus type 16 E7 oncoprotein is necessary to inhibit cell cycle arrest in human epithelial cells. J Virol 76, 10559 10568.
21. Pelka P, Ablack JN, Fonseca GJ, Yousef AF Mymryk JS (2008) Intrinsic structural disorder in adenovirus E1A: a viral molecular hub linking multiple diverse processes. J Virol 82, 7252 7263.
22. Sullivan CS Pipas JM (2002) T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66, 179 202.
23. Garcia-Alai MM, Alonso LG de Prat-Gay G (2007) The N-terminal module of HPV16 E7 is an intrinsically disordered domain that confers conformational and recognition plasticity to the oncoprotein. Biochemistry 46, 10405 10412.
24. Ohlenschlager O, Seiboth T, Zengerling H, Briese L, Marchanka A, Ramachandran R, Baum M, Korbas M, Meyer-Klaucke W, Durst M et al. (2006) Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7. Oncogene 25, 5953 5959.
25. Liu X, Clements A, Zhao K Marmorstein R (2006) Structure of the human Papillomavirus E7 oncoprotein and its mechanism for inactivation of the retinoblastoma tumor suppressor. J Biol Chem 281, 578 586.
26. Phelps WC, Munger K, Yee CL, Barnes JA Howley PM (1992) Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J Virol 66, 2418 2427.
27. Helt AM Galloway DA (2001) Destabilization of the retinoblastoma tumor suppressor by human papillomavirus type 16 E7 is not sufficient to overcome cell cycle arrest in human keratinocytes. J Virol 75, 6737 6747.
28. Alonso LG, Garcia-Alai MM, Smal C, Centeno JM, Iacono R, Castano E, Gualfetti P de Prat-Gay G (2004) The HPV16 E7 viral oncoprotein self-assembles into defined spherical oligomers. Biochemistry 43, 3310 3317.
29. Clements A, Johnston K, Mazzarelli JM, Ricciardi RP Marmorstein R (2000) Oligomerization properties of the viral oncoproteins adenovirus E1A and human papillomavirus E7 and their complexes with the retinoblastoma protein. Biochemistry 39, 16033 16045.
30. Dantur K, Alonso L, Castano E, Morelli L, Centeno-Crowley JM, Vighi S de Prat-Gay G (2009) Cytosolic accumulation of HPV16 E7 oligomers supports different transformation routes for the prototypic viral oncoprotein: the amyloid-cancer connection. Int J Cancer 125, 1902 1911.
31. Uversky VN, Roman A, Oldfield CJ Dunker AK (2006) Protein intrinsic disorder and human papillomaviruses: increased amount of disorder in E6 and E7 oncoproteins from high risk HPVs. J Proteome Res 5, 1829 1842.
32. Alonso LG, Garcia-Alai MM, Nadra AD, Lapena AN, Almeida FL, Gualfetti P Prat-Gay GD (2002) High-risk (HPV16) human papillomavirus E7 oncoprotein is highly stable and extended, with conformational transitions that could explain its multiple cellular binding partners. Biochemistry 41, 10510 10518.
33. Huang PS, Patrick DR, Edwards G, Goodhart PJ, Huber HE, Miles L, Garsky VM, Oliff A Heimbrook DC (1993) Protein domains governing interactions between E2F, the retinoblastoma gene product, and human papillomavirus type 16 E7 protein. Mol Cell Biol 13, 953 960.
34. 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.
35. Patrick DR, Oliff A Heimbrook DC (1994) Identification of a novel retinoblastoma gene product binding site on human papillomavirus type 16 E7 protein. J Biol Chem 269, 6842 6850.
36. Smotkin D Wettstein FO (1987) The major human papillomavirus protein in cervical cancers is a cytoplasmic phosphoprotein. J Virol 61, 1686 1689.
37. Barbosa MS, Edmonds C, Fisher C, Schiller JT, Lowy DR Vousden KH (1990) The region of the HPV E7 oncoprotein homologous to adenovirus E1a and Sv40 large T antigen contains separate domains for Rb binding and casein kinase II phosphorylation. EMBO J 9, 153 160.
38. Storey A, Almond N, Osborn K Crawford L (1990) Mutations of the human papillomavirus type 16 E7 gene that affect transformation, transactivation and phosphorylation by the E7 protein. J Gen Virol 71, 965 970.
39. Chien WM, Parker JN, Schmidt-Grimminger DC, Broker TR Chow LT (2000) Casein kinase II phosphorylation of the human papillomavirus-18 E7 protein is critical for promoting S-phase entry. Cell Growth Differ 11, 425 435.
40. Genovese NJ, Banerjee NS, Broker TR Chow LT (2008) Casein kinase II motif-dependent phosphorylation of human papillomavirus E7 protein promotes p130 degradation and S-phase induction in differentiated human keratinocytes. J Virol 82, 4862 4873.
41. Dick FA Dyson NJ (2002) Three regions of the pRB pocket domain affect its inactivation by human papillomavirus E7 proteins. J Virol 76, 6224 6234.
42. Davies RC Vousden KH (1992) Functional analysis of human papillomavirus type 16 E7 by complementation with adenovirus E1A mutants. J Gen Virol 73, 2135 2139.
43. 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.
44. Joerger AC Fersht AR (2008) Structural biology of the tumor suppressor p53. Annu Rev Biochem 77, 557 582.
45. Buday L Downward J (2008) Many faces of Ras activation. Biochim Biophys Acta 1786, 178 187.
46. Seeliger MA, Breward SE, Friedler A, Schon O Itzhaki LS (2003) Cooperative organization in a macromolecular complex. Nat Struct Biol 10, 718 724.
47. 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.
48. Munger K, Werness BA, Dyson N, Phelps WC, Harlow E Howley PM (1989) Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J 8, 4099 4105.
49. Rechsteiner M Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21, 267 271.
50. Liu Z, Chen K, Ng A, Shi Z, Woody RW Kallenbach NR (2004) Solvent dependence of PII conformation in model alanine peptides. J Am Chem Soc 126, 15141 15150.
51. Garcia-Alai MM, Gallo M, Salame M, Wetzler DE, McBride AA, Paci M, Cicero DO de Prat-Gay G (2006) Molecular basis for phosphorylation-dependent, PEST-mediated protein turnover. Structure 14, 309 319.
52. Munoz V Serrano L (1994) Elucidating the folding problem of helical peptides using empirical parameters. Nat Struct Biol 1, 399 409.
53. Jasanoff A Fersht AR (1994) Quantitative determination of helical propensities from trifluoroethanol titration curves. Biochemistry 33, 2129 2135.
54. Liu Z, Song Y, Bia B Cowell JK (1995) Germline mutations in the RB1 gene in patients with hereditary retinoblastoma. Genes Chromosomes Cancer 14, 277 284.
55. Pflum MK, Tong JK, Lane WS Schreiber SL (2001) Histone deacetylase 1 phosphorylation promotes enzymatic activity and complex formation. J Biol Chem 276, 47733 47741.
56. Rihs HP, Jans DA, Fan H Peters R (1991) The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen. EMBO J 10, 633 639.
57. Whalen SG, Marcellus RC, Barbeau D Branton PE (1996) Importance of the Ser-132 phosphorylation site in cell transformation and apoptosis induced by the adenovirus type 5 E1A protein. J Virol 70, 5373 5383.
58. Kim HY, Ahn BY Cho Y (2001) Structural basis for the inactivation of retinoblastoma tumor suppressor by SV40 large T antigen. EMBO J 20, 295 304.
59. Ferreon JC, Martinez-Yamout MA, Dyson HJ Wright PE (2009) Structural basis for subversion of cellular control mechanisms by the adenoviral E1A oncoprotein. Proc Natl Acad Sci USA 106, 13260 13265.
60. Tokuriki N, Oldfield CJ, Uversky VN, Berezovsky IN Tawfik DS (2009) Do viral proteins possess unique biophysical features? Trends Biochem Sci 34, 53 59.
61. Tompa P, Fuxreiter M, Oldfield CJ, Simon I, Dunker AK Uversky VN (2009) Close encounters of the third kind: disordered domains and the interactions of proteins. Bioessays 31, 328 335.
62. Dong WL, Caldeira S, Sehr P, Pawlita M Tommasino M (2001) Determination of the binding affinity of different human papillomavirus E7 proteins for the tumour suppressor pRb by a plate-binding assay. J Virol Methods 98, 91 98.
63. Narechania A, Terai M, Chen Z, DeSalle R Burk RD (2004) Lack of the canonical pRB-binding domain in the E7 ORF of artiodactyl papillomaviruses is associated with the development of fibropapillomas. J Gen Virol 85, 1243 1250.
64. Fuchs PG, Iftner T, Weninger J Pfister H (1986) Epidermodysplasia verruciformis-associated human papillomavirus 8: genomic sequence and comparative analysis. J Virol 58, 626 634.
65. Beltrao P Serrano L (2007) Specificity and evolvability in eukaryotic protein interaction networks. PLoS Comput Biol 3, e25.
66. Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ Kurdistani SK (2008) Epigenetic reprogramming by adenovirus e1a. Science 321, 1086 1088.
67. Hermanson GT (1996) Bioconjugate Techniques. Academic Press, San Diego, CA.
68. Kuzmic P, Moss ML, Kofron JL Rich DH (1992) Fluorescence displacement method for the determination of receptor-ligand binding constants. Anal Biochem 205, 65 69.
69. Schneider TD Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18, 6097 6100.
70. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947 2948.
71. Hubbard TJ, Aken BL, Ayling S, Ballester B, Beal K, Bragin E, Brent S, Chen Y, Clapham P, Clarke L et al. (2009) Ensembl 2009. Nucleic Acids Res 37, D690 D697.
72. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL et al. (2008) The Pfam protein families database. Nucleic Acids Res 36, D281 D288.
73. (2009) The Universal Protein Resource (UniProt) 2009. Nucleic Acids Res 37, D169 D174.
74. Armon A, Graur D Ben-Tal N (2001) ConSurf: an algorithmic tool for the identification of functional regions in proteins by surface mapping of phylogenetic information. J Mol Biol 307, 447 463.
75. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA.
76. Ferreiro DU, Lima LM, Nadra AD, Alonso LG, Goldbaum FA de Prat-Gay G (2000) Distinctive cognate sequence discrimination, bound DNA conformation, and binding modes in the E2 C-terminal domains from prototype human and bovine papillomaviruses. Biochemistry 39, 14692 14701.
77. Dick FA, Sailhamer E Dyson NJ (2000) Mutagenesis of the pRB pocket reveals that cell cycle arrest functions are separable from binding to viral oncoproteins. Mol Cell Biol 20, 3715 3727.
78. MacLellan WR, Xiao G, Abdellatif M Schneider MD (2000) A novel Rb- and p300-binding protein inhibits transactivation by MyoD. Mol Cell Biol 20, 8903 8915.
79. Miyake S, Sellers WR, Safran M, Li X, Zhao W, Grossman SR, Gan J, DeCaprio JA, Adams PD Kaelin WG Jr. (2000) Cells degrade a novel inhibitor of differentiation with E1A-like properties upon exiting the cell cycle. Mol Cell Biol 20, 8889 8902.