Modeling and molecular dynamics of the intrinsically disordered e7 proteins from high- and low-risk types of human papillomavirus

Journal of Molecular Modeling

Volumn 19, Issue 9, 2013, Pages 4025-4037

  Nicolau Junior, Nilson ^a   Giuliatti, Silvana ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Ab initio modeling; E7; Homology modeling; Human papillomavirus; Molecular dynamics

Indexed keywords

PROTEIN E7;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; COMPUTER MODEL; HUMAN PAPILLOMAVIRUS TYPE 1; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HYBRID; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; SIMULATION; TEMPERATURE; VIRUS MORPHOLOGY; VIRUS STRAIN; WART VIRUS;

HUMAN PAPILLOMAVIRUS;

ALGORITHMS; AMINO ACID SEQUENCE; AMINO ACIDS; BINDING SITES; DNA-BINDING PROTEINS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

EID: 84882928380     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-013-1915-8     Document Type: Article

References (62)

1. Parkin DM, Bray F (2006) Chapter 2: the burden of HPV-related cancers. Vaccine 24:11-25
2. De Villiers EM, Fauquet C, Broker TR, Bernard HU, Zur Hausen H (2004) Classification of papillomaviruses. Virology 324:17-27
3. Kanodia S, Fahey LM, Kast WM (2007) Mechanisms used by human papillomaviruses to escape the host immune response. Curr Cancer Drug Targets 7:79-89
4. Zur Hausen H, Meinhof W, Scheiber W, Bornkamm GW (1974) Attempts to detect virus-specific DNA sequences in human tumors: I. Nucleic acid hybridizations with complementary RNA of human wart virus. Int J Cancer 13:650-656
5. Kleter B, Van Doorn LJ, Ter Schegget J, Schrauwen L, Van Krimpen K, Burger M, Ter Harmsel B, Quint W (1998) Novel short-fragment PCR assay for highly sensitive broad-spectrum detection of anogenital human papillomaviruses. Am J Pathol 153:1731-1739
6. Zur Hausen H (2002) Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342-350
7. Scheffner M, Werness BA, Huibregtse JM et al (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136
8. Narisawa-Saito M, Kiyono T (2007) Basic mechanisms of high-risk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci 98:1505-1511
9. Boulet G, Horvath C, Vanden BD, Sahebali S, Bogers J (2007) Human papillomavirus: E6 and E7 oncogenes. Int J Biochem Cell Biol 39:2006-2011
10. Clements A, Johnston K, Mazzarelli JM, Ricciardi RP, Marmorstein R (2000) Oligomerization properties of the adenovirus E1A viral oncoproteins and human papillomavirus E7 and their complexes with the protein retinoblastoma. Biochemistry 39:16033-16045
11. Chemes LB, Sanchez IE, Smal C, Prat-Gay G (2010) Targeting mechanism of the retinoblastoma tumor suppressor by the prototypical viral oncoprotein. FEBS J 277:973-988
12. Phelps WC, Yee CL, Munger K, Howley PM (1988) The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to adenovirus E1A. Cell 53:539-547
13. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533
14. Dunker AK, Lawson JD, Brown CJ et al (2001) Intrinsically disordered protein. J Mol Graph Model 19:26-59
15. 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
16. 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(15):6737-6747
17. Dyson N, Howley PM, Munger K, Harlow E (1989) The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 243:934-937
18. 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
19. Jones RE, Heimbrook DC, Huber HE, Wegrzyn RJ, Rotberg NS, Stauffer KJ, Lumma PK et al (1992) Specific N-methylations of HPV-16 E7 peptides alter binding to the retinoblastoma suppressor protein. J Biol Chem 267:908-912
20. Barbosa MS, Lowy DR, Schiller JT (1989) Papillomavirus polypeptides E6 and E7 are zinc-binding proteins. J Virol 63:1404-1407
21. 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
22. 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
23. Haug CJ (2008) Human papillomavirus vaccination-reasons for caution. N Engl J Med 359:861-862
24. Hammound M (2008) HPV vaccine: not immune to controversy. Int J Gynaecol Obstet 101:123-124
25. Moscicki A (2008) HPV vaccines: today and in the future. J Adolesc Health 43:26-40
26. Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN (2010) PONDR-FIT: a meta-predictor of intrinsically disordered amino acids. Biochim Biophys Acta 1804:996-1010
27. Mizianty MJ, Zhang T, Xue B, Zhou Y, Dunker AK, Uversky VN, Kurgan L (2011) In-silico prediction of disorder content using hybrid sequence representation. BMC Bioinforma 12(1):245
28. Dosztányi Z, Mészáros B, Simon I (2009) ANCHOR: web server for predicting protein binding regions in disordered proteins. Bioinformatics 25(20):2745-2746
29. Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234:779-815
30. Pons JL, Labesse G (2009) @TOME-2: a new pipeline for comparative modeling of protein-ligand complexes. Nucleic Acids Res 37:485-491
31. Rohl CA, Strauss CE, Misura KMS, Baker D (2004) Protein structure prediction using Rosetta. Methods Enzymol 383:66-93
32. Canutescu A, Dunbrack RL Jr (2003) Cyclic coordinate descent: a robotics algorithm for protein loop closure. Protein Sci 12:963-972
33. Wallner B, Elofsson A (2008) Quality assessment of protein models. In: Bujnicki JM (ed) Prediction of protein structures, functions, and interactions. Wiley, Chichester, pp 143-157
34. Laskowski RA, Macarthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283-291
35. Krivov GG, Shapovalov MV, Dunbrack RL Jr (2009) Improved prediction of protein side-chain conformations with SCWRL4. Proteins 77:778-795
36. McGuffin LJ (2008) The ModFOLD server for the quality assessment of protein structural models. Bioinformatics 24:586-587
37. Yang Y, Zhou Y (2008) Specific interactions for ab initio folding of protein terminal regions with secondary structures. Proteins 72:793-803
38. Benkert P, Tosatto SCE, Schomburg D (2008) QMEAN: a comprehensive scoring function for model quality assessment. Proteins 71(1):261-277
39. Wallner B, Elofsson A (2003) Can correct protein models be identified? Protein Sci 12:1073-1086
40. Cristobal S, Zemla A, Fischer D, Rychlewski L, Elofsson A (2001) A study of quality measures for protein threading models. BMC Bioinforma 2:5-20
41. Siew N, Elofsson A, Rychlewski L, Fischer D (2000) Maxsub: an automated measure to assess the quality of protein structure predictions. Bionformatics 16:776-785
42. Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511-1519
43. Bowie JU, Luethy RE, Eisenberg D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253:164-170
44. Luethy R, Bowie JU, Eisenberg D (1992) Assessment of protein models with three-dimensional profiles. Nature 356:83-85
45. Pontius J, Richelle J, Wodak SJ (1996) Deviations from standard atomic volumes as a quality measure of protein crystal structures. J Mol Biol 264:121-136
46. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WR III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiórkiewicz-Kuczera J, Yin D, Karplus M (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586-3616
47. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802
48. Van Gunsteren WF, Berendsen HJC (1977) Algorithms for macromolecular dynamics and constraint dynamics. Mol Phys 34:1311-1327
49. Humphrey W, Dalke A, Schulten K (1996) VMD-visual molecular dynamics. J Mol Graph 14:33-38
50. Tsoulos IG, Stavrakoudis A (2011) Eucb: a C++ program for molecular dynamics trajectory analysis. Comput Phys Commun 182:834-841
51. Glykos NM (2006) Carma: a molecular dynamics analysis program. J Comput Chem 27:1765-1768
52. Andersen CAF, Palmer AG, Brunak S, Rost B (2002) Continuum secondary structure captures protein flexibility. Structure 10:175-185
53. 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
54. Lee H, Mok KH, Muhandiram R, Park JE, Suk KH et al (2000) Local structural elements in mostly the unstructured transcriptional activation domain of human p53. J Biol Chem 275:29426-29432
55. Mark WY, Liao JC, Lu Y, Ayed A, Laister R et al (2005) Characterization of segments from the central region of BRCA1: an intrinsically disordered multiple scaffold for protein-protein and protein-DNA interactions. J Biol 345:275-287
56. Holm L, Park J (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16:566-567
57. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23(21):2947-2948
58. 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(13):1605-1612
59. Uversky VN, Dunker AK (2010) Understanding protein non-folding. Biochim Biophys Acta 1804(6):1231-1264
60. Uversky VN (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci 11(4):739-756
61. Espinoza-Fonseca LM (2009) Leucine-rich hydrophobic clusters promote folding of the N-terminus of the intrinsically disordered transactivation domain of p53. FEBS Lett 583(3):556-560
62. Salma P, Chhatbar C, Seshadri S (2009) Intrinsically unstructured proteins: potential targets for drug discovery. Am J Infect Dis 5:126-134