Evolution of linear motifs within the papillomavirus E7 oncoprotein

Journal of Molecular Biology

Volumn 422, Issue 3, 2012, Pages 336-346

  Chemes, Lucía B ^a   Glavina, Juliana ^b   Faivovich, Julián ^b,c   De Prat Gay, Gonzalo ^a   Sánchez, Ignacio E ^b  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c MUSEO ARGENTINO DE CIENCIAS NATURALES BERNARDINO RIVADAVIA   (Argentina)

Author keywords

adaptive evolution; convergent evolution; intrinsic disorder; sequence motif; virus

Indexed keywords

HOMODIMER; PROTEIN E7;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONVERGENT EVOLUTION; ENZYME PHOSPHORYLATION; GENE MUTATION; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PDZ DOMAIN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; VIRAL TROPISM; VIRUS CELL INTERACTION; VIRUS VIRULENCE;

PAPILLOMAVIRIDAE;

EID: 84865074702     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.05.036     Document Type: Article

References (52)

1. N.E. Davey, K. Van Roey, R.J. Weatheritt, G. Toedt, B. Uyar, and B. Altenberg Attributes of short linear motifs Mol. Biosyst. 2011
2. V. Neduva, and R.B. Russell Linear motifs: evolutionary interaction switches FEBS Lett. 579 2005 3342 3345
3. C.S. Tan, C. Jorgensen, and R. Linding Roles of "junk phosphorylation" in modulating biomolecular association of phosphorylated proteins? Cell Cycle 9 2010 1276 1280
4. L.J. Holt, B.B. Tuch, J. Villen, A.D. Johnson, S.P. Gygi, and D.O. Morgan Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution Science 325 2009 1682 1686
5. N.E. Davey, G. Trave, and T.J. Gibson How viruses hijack cell regulation Trends Biochem. Sci. 36 2011 159 169
6. M. Fuxreiter, P. Tompa, and I. Simon Local structural disorder imparts plasticity on linear motifs Bioinformatics 23 2007 950 956
7. M.M. Garcia-Alai, M. Gallo, M. Salame, D.E. Wetzler, A.A. McBride, and M. Paci Molecular basis for phosphorylation-dependent, PEST-mediated protein turnover Structure 14 2006 309 319
8. K.J. Penrose, M. Garcia-Alai, G.d. Prat Gay, and A.A. McBride Casein kinase II phosphorylation-induced conformational switch triggers degradation of the papillomavirus E2 protein J. Biol. Chem. 279 2004 22430 22439
9. S. Garcia-Vallve, A. Alonso, and I.G. Bravo Papillomaviruses: different genes have different histories Trends Microbiol. 13 2005 514 521
10. I.E. Sanchez, M. Dellarole, K. Gaston, and G. de Prat Gay Comprehensive comparison of the interaction of the E2 master regulator with its cognate target DNA sites in 73 human papillomavirus types by sequence statistics Nucleic Acids Res. 36 2008 756 769
11. L.B. Chemes, I.E. Sánchez, L.G. Alonso, and G. de Prat-Gay Intrinsic disorder in the human papillomavirus E7 protein V.N. Uversky, S. Longhi, Flexible Viruses: Structural Disorder within Viral Proteins vols. 1 2011 John Wiley and Sons 313 347
12. L.G. Alonso, M.M. Garcia-Alai, A.D. Nadra, A.N. Lapena, F.L. Almeida, P. Gualfetti, and G.D. Prat-Gay 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 2002 10510 10518
13. M.M. Garcia-Alai, L.G. Alonso, and G. de Prat-Gay The N-terminal module of HPV16 E7 is an intrinsically disordered domain that confers conformational and recognition plasticity to the oncoprotein Biochemistry 46 2007 10405 10412
14. O. Ohlenschlager, T. Seiboth, H. Zengerling, L. Briese, A. Marchanka, and R. Ramachandran Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7 Oncogene 25 2006 5953 5959
15. X. Liu, A. Clements, K. Zhao, and R. Marmorstein Structure of the human Papillomavirus E7 oncoprotein and its mechanism for inactivation of the retinoblastoma tumor suppressor J. Biol. Chem. 281 2006 578 586
16. Y.J. Liang, H.S. Chang, C.Y. Wang, and W.C. Yu DYRK1A stabilizes HPV16E7 oncoprotein through phosphorylation of the threonine 5 and threonine 7 residues Int. J. Biochem. Cell Biol. 40 2008 2431 2441
17. S. Himpel, W. Tegge, R. Frank, S. Leder, H.G. Joost, and W. Becker Specificity determinants of substrate recognition by the protein kinase DYRK1A J. Biol. Chem. 275 2000 2431 2438
18. B. Xiao, J. Spencer, A. Clements, N. Ali-Khan, S. Mittnacht, and C. Broceno Crystal structure of the retinoblastoma tumor suppressor protein bound to E2F and the molecular basis of its regulation Proc. Natl Acad. Sci. USA 100 2003 2363 2368
19. X. Liu, and R. Marmorstein Structure of the retinoblastoma protein bound to adenovirus E1A reveals the molecular basis for viral oncoprotein inactivation of a tumor suppressor Genes Dev. 21 2007 2711 2716
20. C. Lee, J.H. Chang, H.S. Lee, and Y. Cho Structural basis for the recognition of the E2F transactivation domain by the retinoblastoma tumor suppressor Genes Dev. 16 2002 3199 3212
21. J. Wang, D. Zhou, A. Prabhu, R. Schlegel, and H. Yuan The canine papillomavirus and gamma HPV E7 proteins use an alternative domain to bind and destabilize the retinoblastoma protein PLoS Pathog. 6 2010 e1001089
22. J.E. Allende, and C.C. Allende Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation FASEB J. 9 1995 313 323
23. T. Guttler, T. Madl, P. Neumann, D. Deichsel, L. Corsini, and T. Monecke NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1 Nat. Struct. Mol. Biol. 17 2010 1367 1376
24. C.M. Gould, F. Diella, A. Via, P. Puntervoll, C. Gemund, and S. Chabanis-Davidson ELM: the status of the 2010 eukaryotic linear motif resource Nucleic Acids Res. 38 2010 D167 D180
25. E. Reinstein, M. Scheffner, M. Oren, A. Ciechanover, and A. Schwartz Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue Oncogene 19 2000 5944 5950
26. L.B. Chemes, I.E. Sanchez, C. Smal, and G. de Prat-Gay Targeting mechanism of the retinoblastoma tumor suppressor by a prototypical viral oncoprotein. Structural modularity, intrinsic disorder and phosphorylation of human papillomavirus E7 FEBS J. 277 2010 973 988
27. J.O. Lee, A.A. Russo, and N.P. Pavletich Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7 Nature 391 1998 859 865
28. J.M. Firzlaff, D.A. Galloway, R.N. Eisenman, and B. Luscher The E7 protein of human papillomavirus type 16 is phosphorylated by casein kinase II New Biol. 1 1989 44 53
29. L.B. Chemes, I.E. Sanchez, and G. de Prat-Gay Kinetic recognition of the retinoblastoma tumor suppressor by a specific protein target J. Mol. Biol. 412 2011 267 284
30. C. Smal, D.E. Wetzler, K.I. Dantur, L.B. Chemes, M.M. Garcia-Alai, and M. Dellarole The human papillomavirus E7-E2 interaction mechanism in vitro reveals a finely tuned system for modulating available E7 and E2 proteins Biochemistry 48 2009 11939 11949
31. A.A. Knapp, P.M. McManus, K. Bockstall, and J. Moroianu Identification of the nuclear localization and export signals of high risk HPV16 E7 oncoprotein Virology 383 2009 60 68
32. V. Tomaic, D. Gardiol, P. Massimi, M. Ozbun, M. Myers, and L. Banks Human and primate tumour viruses use PDZ binding as an evolutionarily conserved mechanism of targeting cell polarity regulators Oncogene 28 2009 1 8
33. S.J. Ghim, A. Rector, H. Delius, J.P. Sundberg, A.B. Jenson, and M. Van Ranst Equine papillomavirus type 1: complete nucleotide sequence and characterization of recombinant virus-like particles composed of the EcPV-1 L1 major capsid protein Biochem. Biophys. Res. Commun. 324 2004 1108 1115
34. L. Hirt, A. Hirsch-Behnam, and E.M. de Villiers Nucleotide sequence of human papillomavirus (HPV) type 41: an unusual HPV type without a typical E2 binding site consensus sequence Virus Res. 18 1991 179 189
35. J. Ekstrom, O. Forslund, and J. Dillner Three novel papillomaviruses (HPV109, HPV112 and HPV114) and their presence in cutaneous and mucosal samples Virology 397 2010 331 336
36. A. Kohler, M. Gottschling, J. Forster, J. Rowert-Huber, E. Stockfleth, and I. Nindl Genomic characterization of a novel human papillomavirus (HPV-117) with a high viral load in a persisting wart Virology 399 2010 129 133
37. D. Chouhy, M. Gorosito, A. Sanchez, E.C. Serra, A. Bergero, R. Fernandez Bussy, and A.A. Giri New generic primer system targeting mucosal/genital and cutaneous human papillomaviruses leads to the characterization of HPV 115, a novel Beta-papillomavirus species 3 Virology 397 2010 205 216
38. N.D. Christensen, N.M. Cladel, C.A. Reed, and R. Han Rabbit oral papillomavirus complete genome sequence and immunity following genital infection Virology 269 2000 451 461
39. O. Danos, M. Katinka, and M. Yaniv Human papillomavirus 1a complete DNA sequence: a novel type of genome organization among papovaviridae EMBO J. 1 1982 231 236
40. S. Hatama, K. Nobumoto, and T. Kanno Genomic and phylogenetic analysis of two novel bovine papillomaviruses, BPV-9 and BPV-10 J. Gen. Virol. 89 2008 158 163
41. A. Rector, P. Lemey, R. Tachezy, S. Mostmans, S.J. Ghim, and K. Van Doorslaer Ancient papillomavirus-host co-speciation in Felidae Genome Biol. 8 2007 R57
42. C.H. Tan, R. Tachezy, M. Van Ranst, S.Y. Chan, H.U. Bernard, and R.D. Burk The Mastomys natalensis papillomavirus: nucleotide sequence, genome organization, and phylogenetic relationship of a rodent papillomavirus involved in tumorigenesis of cutaneous epithelia Virology 198 1994 534 541
43. H.U. Bernard, R.D. Burk, Z. Chen, K. van Doorslaer, H. Hausen, and E.M. de Villiers Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments Virology 401 2010 70 79
44. I.G. Bravo, S. de Sanjose, and M. Gottschling The clinical importance of understanding the evolution of papillomaviruses Trends Microbiol. 18 2010 432 438
45. A. Narechania, M. Terai, Z. Chen, R. DeSalle, and R.D. Burk 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 2004 1243 1250
46. K. Van Doorslaer, A.O. Sidi, K. Zanier, V. Rybin, F. Deryckere, and A. Rector Identification of unusual E6 and E7 proteins within avian papillomaviruses: cellular localization, biophysical characterization, and phylogenetic analysis J. Virol. 83 2009 8759 8770
47. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797
48. I. Rivals, L. Personnaz, L. Taing, and M.C. Potier Enrichment or depletion of a GO category within a class of genes: which test? Bioinformatics 23 2007 401 407
49. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R. Stat. Soc., B 57 1995 289 300
50. W.M. Fitch Toward defining the course of evolution: minimum change for a specific tree topology Syst. Zool. 20 1971 406 416
51. K. Dantur, L. Alonso, E. Castano, L. Morelli, J.M. Centeno-Crowley, S. Vighi, and G. de Prat-Gay Cytosolic accumulation of HPV16 E7 oligomers supports different transformation routes for the prototypic viral oncoprotein: the amyloid-cancer connection Int. J. Cancer 125 2009 1902 1911
52. K. Kadaveru, J. Vyas, and M.R. Schiller Viral infection and human disease-insights from minimotifs Front Biosci. 13 2008 6455 6471