Disordered interactome of human papillomavirus

Current Pharmaceutical Design

Volumn 20, Issue 8, 2014, Pages 1274-1292

  Xue, Bin ^a   Ganti, Ketaki ^b   Rabionet, Alejandro ^a   Banks, Lawrence ^b   Uversky, Vladimir N ^a,c,d  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

Author keywords

Human papillomavirus; Intrinsically disordered protein; Protein function; Protein nucleic acid interaction; Protein protein interaction

Indexed keywords

CAPSID PROTEIN; CAPSID PROTEIN L1; CAPSID PROTEIN L2; GLYCOPROTEIN E1; INTRINSICALLY DISORDERED PROTEIN; PROTEIN E6; PROTEIN E7; UNCLASSIFIED DRUG; ONCOPROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; CELL IMMORTALIZATION; CELL TRANSFORMATION; DNA REPLICATION; FUNCTIONAL DISEASE; GENETIC TRANSCRIPTION; HOST CELL; HUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN PROTEIN INTERACTION; REVIEW; TARGET CELL; VIRUS ATTACHMENT; VIRUS CELL TRANSFORMATION; VIRUS ENTRY; WART VIRUS; CELL CYCLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; PROTEIN CONFORMATION; PROTEIN FOLDING; VIROLOGY; VIRUS GENOME;

CELL CYCLE; GENOME, VIRAL; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MODELS, MOLECULAR; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 84903700781     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990072     Document Type: Review

References (301)

1. Wright PE, Dyson HJ. Intrinsically unstructured proteins: reassessing the protein structure-function paradigm. J Mol Biol 1999; 293: 321-31.
2. Uversky VN, Gillespie JR, Fink AL. Why are natively unfolded proteins unstructured under physiologic conditions?, Proteins 2000; 41: 415-27.
3. Dunker AK, Lawson JD, Brown CJ, et al. Intrinsically disordered protein. J Mol Graph Model 2001; 19: 26-59.
4. Tompa P. Intrinsically unstructured proteins, Trends Biochem Sci 2002; 27: 527-33.
5. Uversky, VN. Natively unfolded proteins: a point where biology waits for physics, Protein Sci 2002; 11: 739-56.
6. Uversky VN. What does it mean to be natively unfolded?, Eur J Biochem 2002; 269: 2-12.
7. Tompa P. The functional benefits of disorder. J Mol Structure (Theochem) 2003; 666-67: 361-71.
8. Dunker AK, Obradovic Z. The protein trinity--linking function and disorder, Nat Biotechnol 2001; 19: 805-6.
9. Dunker AK, Brown CJ, Obradovic Z. Identification and functions of usefully disordered proteins, Adv Protein Chem 2002; 62: 25-49.
10. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z. Intrinsic disorder and protein function, Biochemistry 2002; 41: 6573-82.
11. Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions, Nat Rev Mol Cell Biol 2005; 6: 197-208.
12. Tompa P. The interplay between structure and function in intrinsically unstructured proteins, FEBS Lett 2005; 579: 3346-54.
13. Tompa P, Szasz C, Buday L. Structural disorder throws new light on moonlighting, Trends Biochem Sci 2005; 30: 484-9.
14. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK. Intrinsic disorder and functional proteomics, Biophys J 2007; 92: 1439-56.
15. Tompa P, Fuxreiter M, Oldfield CJ, Simon I, Dunker AK, Uversky VN. Close encounters of the third kind: disordered domains and the interactions of proteins, Bioessays 2009; 31: 328-35.
16. Wright PE, Dyson HJ. Linking folding and binding, Curr Opin Struct Biol 2009 19, 31-8.
17. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN. Flexible nets. The roles of intrinsic disorder in protein interaction networks, Febs J 2005; 272: 5129-48.
18. Uversky VN, Oldfield CJ, Dunker AK. Showing your ID: intrinsic disorder as an ID for recognition, regulation and cell signaling. J Mol Recognit 2005; 18: 343-84.
19. Dunker AK, Silman I, Uversky VN, Sussman JL. Function and structure of inherently disordered proteins, Curr Opin Struct Biol 2008; 18: 756-64.
20. Uversky VN, Dunker AK. Understanding protein non-folding, Biochim Biophys Acta 2010; 1804: 1231-64.
21. Turoverov KK, Kuznetsova IM, Uversky VN. The protein kingdom extended: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation, Prog Biophys Mol Biol 2010; 102: 73-84.
22. Uversky VN. Flexible nets of malleable guardians: intrinsically disordered chaperones in neurodegenerative diseases, Chem Rev 2011; 111: 1134-66.
23. Uversky VN. Intrinsically disordered proteins from A to Z, Int J Biochem Cell Biol 2011; 43: 1090-103.
24. Uversky VN. Multitude of binding modes attainable by intrinsically disordered proteins: a portrait gallery of disorder-based complexes, Chem Soc Rev 2011; 40: 1623-34.
25. Tantos A, Han KH, Tompa P. Intrinsic disorder in cell signaling and gene transcription, Mol Cell Endocrinol 2012; 348: 457-65.
26. Dunker AK, Obradovic Z, Romero P, Garner EC, Brown CJ. Intrinsic protein disorder in complete genomes, Genome Inform Ser Workshop Genome Inform 2000; 11: 161-71.
27. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 2004; 337: 635-45.
28. Oldfield CJ, Cheng Y, Cortese MS, Brown CJ, Uversky VN, Dunker AK. Comparing and combining predictors of mostly disordered proteins, Biochemistry 2005; 44: 1989-2000.
29. Uversky VN. The mysterious unfoldome: structureless, underappreciated, yet vital part of any given proteome. J Biomed Biotechnol 2010; 2010: 568068.
30. Schad E, Tompa P, Hegyi H. The relationship between proteome size, structural disorder and organism complexity, Genome Biol 2011; 12: R120.
31. Pancsa R, Tompa P. Structural disorder in eukaryotes, PLoS One 2012; 7, e34687.
32. Xue B, Dunker AK, Uversky VN. Orderly order in protein intrinsic disorder distribution: Disorder in 3500 proteomes from viruses and the three domains of life. J Biomol Structure Dynamics 2012; 30: 131-42.
33. Williams RM, Obradovi Z, Mathura V, et al. The protein nonfolding problem: amino acid determinants of intrinsic order and disorder, Pac Symp Biocomput 2001; 89-100.
34. Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK. Sequence complexity of disordered protein. Proteins 2001; 42: 38-48.
35. Vacic V, Uversky VN, Dunker AK, Lonardi S. Composition Profiler: a tool for discovery and visualization of amino acid composition differences, BMC Bioinformatics 2007; 8: 211.
36. Dunker AK, Garner E, Guilliot S, et al. Protein disorder and the evolution of molecular recognition: theory, predictions and observations, Pac Symp Biocomput 1998; 473-84.
37. Garner E, Cannon P, Romero P, Obradovic Z, Dunker AK. Predicting Disordered Regions from Amino Acid Sequence: Common Themes Despite Differing Structural Characterization, Genome Inform Ser Workshop Genome Inform 1998; 9: 201-13.
38. Li X, Romero P, Rani M, Dunker AK, Obradovic Z. Predicting Protein Disorder for N-, C-, and Internal Regions, Genome Inform Ser Workshop Genome Inform 1999; 10: 30-40.
39. Liu J, Rost B. NORSp: Predictions of long regions without regular secondary structure, Nucleic Acids Res 2003; 31: 3833-5.
40. Linding R, Russell RB, Neduva V, Gibson TJ. GlobPlot: Exploring protein sequences for globularity and disorder, Nucleic Acids Res 2003; 31: 3701-8.
41. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, et al. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded, Bioinformatics 2005; 21: 3435-8.
42. Dosztanyi Z, Csizmok V, Tompa P, Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content, Bioinformatics 2005; 21: 3433-4.
43. Jones DT, Ward JJ. Prediction of disordered regions in proteins from position specific score matrices, Proteins 2003; 53 Suppl 6: 573-8.
44. Ward JJ, McGuffin LJ, Bryson K, Buxton BF, Jones DT. The DISOPRED server for the prediction of protein disorder, Bioinformatics 2004; 20: 2138-9.
45. He B, Wang K, Liu Y, Xue B, Uversky VN, Dunker AK. Predicting intrinsic disorder in proteins: an overview, Cell Res 2009; 19: 929-49.
46. Bracken C, Iakoucheva LM, Romero PR, Dunker AK. Combining prediction, computation and experiment for the characterization of protein disorder, Curr Opin Struct Biol 2004; 14: 570-6.
47. Uversky VN, Radivojac P, Iakoucheva LM, Obradovic Z, Dunker AK. Prediction of intrinsic disorder and its use in functional proteomics, Methods Mol Biol 2007; 408: 69-92.
48. Lee H, Mok KH, Muhandiram R, et al. Local structural elements in the mostly unstructured transcriptional activation domain of human p53. J Biol Chem 2000; 275: 29426-32.
49. Adkins JN, Lumb KJ. Intrinsic structural disorder and sequence features of the cell cycle inhibitor p57Kip2, Proteins 2002; 46: 1-7.
50. Chang BS, Minn AJ, Muchmore SW, Fesik SW, Thompson CB. Identification of a novel regulatory domain in Bcl-X(L) and Bcl-2, Embo J 1997; 16: 968-77.
51. Campbell KM, Terrell AR, Laybourn PJ, Lumb KJ. Intrinsic structural disorder of the C-terminal activation domain from the bZIP transcription factor Fos, Biochemistry 2000; 39: 2708-13.
52. Mark WY, Liao JC, Lu Y, et al. Characterization of segments from the central region of BRCA1: an intrinsically disordered scaffold for multiple protein-protein and protein-DNA interactions?. J Mol Biol 2005; 345: 275-87.
53. Iakoucheva LM, Brown CJ, Lawson JD, Obradovic Z, Dunker AK. Intrinsic disorder in cell-signaling and cancer-associated proteins. J Mol Biol 2002; 323: 573-84.
54. Hegyi H, Buday L, Tompa P. Intrinsic structural disorder confers cellular viability on oncogenic fusion proteins, PLoS Comput Biol 2009; 5: e1000552.
55. Erkizan HV, Uversky VN, Toretsky JA. Oncogenic partnerships: EWS-FLI1 protein interactions initiate key pathways of Ewing's sarcoma, Clin Cancer Res 2010; 16: 4077-83.
56. Ghosh RP, Nikitina T, Horowitz-Scherer RA, et al. Unique physical properties and interactions of the domains of methylated DNA binding protein 2, Biochemistry 2010; 49: 4395-410.
57. Yang C, van der Woerd MJ, Muthurajan UM, Hansen JC, Luger K. Biophysical analysis and small-angle X-ray scattering-derived structures of MeCP2-nucleosome complexes, Nucleic Acids Res 2011.
58. Homchaudhuri L, De Avila M, Nilsson SB, et al. Secondary structure and solvent accessibility of a calmodulin-binding Cterminal segment of membrane-associated myelin basic protein. Biochemistry 2010; 49: 8955-66.
59. Narayanan RL, Durr UH, Bibow S, Biernat J, Mandelkow E, Zweckstetter M. Automatic assignment of the intrinsically disordered protein Tau with 441-residues. J Am Chem Soc 2010; 132: 11906-7.
60. Al-Ali H, Rieger ME, Seldeen KL, Harris TK, Farooq A, Briegel KJ. Biophysical characterization reveals structural disorder in the developmental transcriptional regulator LBH. Biochem Biophys Res Commun 2010; 391: 1104-9.
61. Uversky VN, Oldfield CJ, Dunker AK. Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu Rev Biophys 2008; 37: 215-46.
62. Midic U, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN. Protein disorder in the human diseasome: unfoldomics of human genetic diseases, BMC Genomics 2009; 10 Suppl 1: S12.
63. Uversky VN, Roman A, Oldfield CJ, Dunker AK. Protein intrinsic disorder and human papillomaviruses: increased amount of disorder in E6 and E7 oncoproteins from high risk HPVs. J Proteome Res 2006; 5: 1829-42.
64. Cheng Y, LeGall T, Oldfield CJ, Dunker AK, Uversky VN. Abundance of intrinsic disorder in protein associated with cardiovascular disease. Biochemistry 2006; 45: 10448-60.
65. Uversky VN. Intrinsic disorder in proteins associated with neurodegenerative diseases. Front Biosci 2009; 14: 5188-38.
66. Mohan A, Sullivan WJ. Jr, Radivojac P, Dunker AK, Uversky VN. Intrinsic disorder in pathogenic and non-pathogenic microbes: discovering and analyzing the unfoldomes of early-branching eukaryotes, Mol Biosyst 2008; 4: 328-40.
67. Xue B, Williams RW, Oldfield CJ, Goh GK, Dunker AK, Uversky VN. Viral disorder or disordered viruses: do viral proteins possess unique features?, Protein Pept Lett 2010; 17: 932-51.
68. Goh GK, Dunker AK, Uversky VN. Protein intrinsic disorder and influenza virulence: the 1918 H1N1 and H5N1 viruses. Virol J 2009; 6: 69.
69. Goh GK, Dunker AK, Uversky VN. A comparative analysis of viral matrix proteins using disorder predictors, Virol J 2008; 5: 126.
70. Goh GK, Dunker AK, Uversky VN. Protein intrinsic disorder toolbox for comparative analysis of viral proteins, BMC Genomics 2008; 9 Suppl 2: S4.
71. Xue B, Mizianty MJ, Kurgan L, Uversky VN. Protein intrinsic disorder as a flexible armor and a weapon of HIV-1, Cell Mol Life Sci 2012; 69: 1211-59.
72. Midic U, Oldfield CJ, Dunker AK, Obradovic Z, Uversky VN. Protein disorder in the human diseasome: Unfoldomics of human genetic diseases, PLoS Computational Biology 2008In press.
73. Xie H, Vucetic S, Iakoucheva LM, et al. Functional anthology of intrinsic disorder. 1. Biological processes and functions of proteins with long disordered regions. J Proteome Res 2007; 6: 1882-98.
74. Vucetic S, Xie H, Iakoucheva LM, et al. Functional anthology of intrinsic disorder. 2. Cellular components, domains, technical terms, developmental processes, and coding sequence diversities correlated with long disordered regions. J Proteome Res 2007; 6: 1899-916.
75. Xie H, Vucetic S, Iakoucheva LM, et al. Functional anthology of intrinsic disorder. 3. Ligands, post-translational modifications, and diseases associated with intrinsically disordered proteins. J Proteome Res 2007; 6: 1917-32.
76. Haynes C, Oldfield CJ, Ji F, et al. Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes, PLoS Comput Biol 2006; 2: e100.
77. Dosztanyi Z, Chen J, Dunker AK, Simon I, Tompa P. Disorder and sequence repeats in hub proteins and their implications for network evolution. J Proteome Res 2006; 5: 2985-95.
78. Oldfield CJ, Meng J, Yang JY, Yang MQ, Uversky VN, Dunker AK. Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners, BMC Genomics 2008; 9 Suppl 1: S1.
79. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010; 401: 70-9.
80. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology 2004; 324: 17-27.
81. Munger K, Baldwin A, Edwards KM, et al. Mechanisms of human papillomavirus-induced oncogenesis. J Virol 2004; 78, 11451-60.
82. Lacey CJ, Lowndes CM, Shah KV. Chapter 4: Burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease, Vaccine 2006; 24 Suppl 3: S335-S341.
83. Moscicki AB, Schiffman M, Kjaer S, Villa LL. Chapter 5: Updating the natural history of HPV and anogenital cancer, Vaccine 2006; 24 Suppl 3: S342-S351.
84. Hu D, Goldie S. The economic burden of noncervical human papillomavirus disease in the United States, Am J Obstet Gynecol 2008; 198: 500 e501-7.
85. Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues, Nat Rev Cancer 2007; 7: 11-22.
86. Gillison ML. Human papillomavirus-associated head and neck cancer is a distinct epidemiologic, clinical, and molecular entity, Semin Oncol 2004; 31: 744-54.
87. Gillison ML, Lowy DR. A causal role for human papillomavirus in head and neck cancer, Lancet 2004; 363: 1488-9.
88. Syrjanen S. Human papillomavirus (HPV) in head and neck cancer. J Clin Virol 2005; 32 Suppl 1: S59-66.
89. Frisch M, Fenger C, van den Brule AJ, et al. Variants of squamous cell carcinoma of the anal canal and perianal skin and their relation to human papillomaviruses, Cancer Res 1999; 59: 753-7.
90. Johnson LG, Madeleine MM, Newcomer LM, Schwartz SM, Daling JR. Anal cancer incidence and survival: the surveillance, epidemiology, and end results experience 1973-2000; Cancer 2004; 101: 281-8.
91. Daling JR, Madeleine MM, Johnson LG, et al. Human papillomavirus, smoking, and sexual practices in the etiology of anal cancer, Cancer 2004; 101: 270-80.
92. Walboomers JM, Jacobs MV, Manos MM, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999; 189: 12-9.
93. Clifford GM, Smith JS, Aguado T, Franceschi S. Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis, Br J Cancer 2003; 89: 101-105.
94. Braaten KP, Laufer MR. Human Papillomavirus (HPV), HPVRelated Disease, and the HPV Vaccine, Rev Obstet Gynecol 2008; 1: 2-10.
95. D'Souza G, Kreimer AR, Viscidi R, et al. Case-control study of human papillomavirus and oropharyngeal cancer, N Engl J Med 2007; 356: 1944-56.
96. Parkin DM, Bray F. Chapter 2: The burden of HPV-related cancers, Vaccine 2006; 24 Suppl 3: S311-S325.
97. Stanley MA. Genital human papillomavirus infections: current and prospective therapies. J Gen Virol 2012; 93: 681-91.
98. Munger K. The role of human papillomaviruses in human cancers, Front Biosci 2002; 7: d641-9.
99. Tommasino M, Crawford L. Human papillomavirus E6 and E7: proteins which deregulate the cell cycle, Bioessays 1995; 17: 509-18.
100. Schwartz S. HPV-16 RNA processing, Front Biosci 2008; 13: 5880-91.
101. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application, Nat Rev Cancer 2002; 2: 342-50.
102. Longworth MS, Laimins LA. Pathogenesis of human papillomaviruses in differentiating epithelia, Microbiol Mol Biol Rev 2004; 68: 362-72.
103. Hughes FJ, Romanos MA. E1 protein of human papillomavirus is a DNA helicase/ATPase, Nucleic Acids Res 1993; 21: 5817-23.
104. Ustav M, Stenlund A. Transient replication of BPV-1 requires two viral polypeptides encoded by the E1 and E2 open reading frames, Embo J 1991; 10: 449-57.
105. Frattini MG, Laimins LA. Binding of the human papillomavirus E1 origin-recognition protein is regulated through complex formation with the E2 enhancer-binding protein, Proc Natl Acad Sci USA 1994; 91: 12398-402.
106. Mohr IJ, Clark R, Sun S, Androphy EJ, MacPherson P, Botchan MR. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator, Science 1990; 250: 1694-9.
107. Cripe TP, Haugen TH, Turk JP, et al. Transcriptional regulation of the human papillomavirus-16 E6-E7 promoter by a keratinocytedependent enhancer, and by viral E2 trans-activator and repressor gene products: implications for cervical carcinogenesis, Embo J 1987; 6: 3745-53.
108. Gloss B, Bernard HU, Seedorf K, Klock G. The upstream regulatory region of the human papilloma virus-16 contains an E2 protein-independent enhancer which is specific for cervical carcinoma cells and regulated by glucocorticoid hormones, Embo J 1987; 6: 3735-43.
109. Wilson R, Fehrmann F, Laimins LA. Role of the E1--E4 protein in the differentiation-dependent life cycle of human papillomavirus type 31. J Virol 2005; 79: 6732-40.
110. Brown DR, Kitchin D, Qadadri B, Neptune N, Batteiger T, Ermel A. The human papillomavirus type 11 E1--E4 protein is a transglutaminase 3 substrate and induces abnormalities of the cornified cell envelope. Virology 2006; 345: 290-8.
111. Davy CE, Ayub M, Jackson DJ, Das P, McIntosh P, Doorbar J. HPV16 E1;E4 protein is phosphorylated by Cdk2/cyclin A and relocalizes this complex to the cytoplasm. Virology 2006.
112. Fehrmann F, Klumpp DJ, Laimins LA. Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J Virol 2003; 77: 2819-31.
113. Genther SM, Sterling S, Duensing S, Munger K, Sattler C, Lambert PF. Quantitative role of the human papillomavirus type 16 E5 gene during the productive stage of the viral life cycle. J Virol 2003; 77: 2832-42.
114. Zhang B, Li P, Wang E, et al. The E5 protein of human papillomavirus type 16 perturbs MHC class II antigen maturation in human foreskin keratinocytes treated with interferon-gamma. Virology 2003; 310: 100-8.
115. Leechanachai P, Banks L, Moreau F, Matlashewski G. The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus, Oncogene 1992; 7: 19-25.
116. Straight SW, Hinkle PM, Jewers RJ, McCance DJ. The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. J Virol 1993; 67: 4521-32.
117. Sato H, Furuno A, Yoshiike K. Expression of human papillomavirus type 16 E7 gene induces DNA synthesis of rat 3Y1 cells. Virology 1989; 168: 195-9.
118. Lambert PF, Pan H, Pitot HC, Liem A, Jackson M, Griep AE. Epidermal cancer associated with expression of human papillomavirus type 16 E6 and E7 oncogenes in the skin of transgenic mice, Proc Natl Acad Sci USA 1993; 90: 5583-7.
119. Griep AE, Herber R, Jeon S, Lohse JK, Dubielzig RR, Lambert PF. Tumorigenicity by human papillomavirus type 16 E6 and E7 in transgenic mice correlates with alterations in epithelial cell growth and differentiation. J Virol 1993; 67: 1373-84.
120. Barbosa MS, Schlegel R. The E6 and E7 genes of HPV-18 are sufficient for inducing two-stage in vitro transformation of human keratinocytes, Oncogene 1989; 4: 1529-32.
121. Watt FM. Epidermal stem cells: markers, patterning and the control of stem cell fate, Philos Trans R Soc Lond B Biol Sci 1998; 353: 831-7.
122. Hebner CM, Laimins LA. Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity, Rev Med Virol 2006; 16: 83-97.
123. Bergant Marusic M, Ozbun MA, Campos SK, Myers MP, Banks L. Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17, Traffic 2012; 13: 455-67.
124. D'Abramo CM, Archambault J. Small molecule inhibitors of human papillomavirus protein - protein interactions, Open Virol J 2011; 5: 80-95.
125. Flores ER, Allen-Hoffmann BL, Lee D, Lambert PF. The human papillomavirus type 16 E7 oncogene is required for the productive stage of the viral life cycle. J Virol 2000; 74: 6622-31.
126. Garner-Hamrick PA, Fostel JM, Chien WM, et al. Global effects of human papillomavirus type 18 E6/E7 in an organotypic keratinocyte culture system. J Virol 2004; 78: 9041-50.
127. Abramson AL, Nouri M, Mullooly V, Fisch G, Steinberg BM. Latent Human Papillomavirus infection is comparable in the larynx and trachea. J Med Virol 2004; 72: 473-7.
128. Moore RA, Nicholls PK, Santos EB, Gough GW, Stanley MA. Absence of canine oral papillomavirus DNA following prophylactic L1 particle-mediated immunotherapeutic delivery vaccination. J Gen Virol 2002; 83: 2299-301.
129. Pim D, Banks L. Interaction of viral oncoproteins with cellular target molecules: infection with high-risk vs low-risk human papillomaviruses, APMIS 2010; 118: 471-93.
130. Rancurel C, Khosravi M, Dunker AK, Romero PR, Karlin D. Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 2009; 83: 10719-36.
131. Xue B, Oldfield CJ, Dunker AK, Uversky VN. CDF it all: consensus prediction of intrinsically disordered proteins based on various cumulative distribution functions, FEBS Lett 2009; 583: 1469-74.
132. Wetherill LF, Holmes KK, Verow M, et al. High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors. J Virol 2012; 86: 5341-51.
133. Sapp M, Fligge C, Petzak I, Harris JR, Streeck RE. Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines. J Virol 1998; 72: 6186-9.
134. Buck CB, Thompson CD, Pang YY, Lowy DR, Schiller JT. Maturation of papillomavirus capsids. J Virol 2005; 79: 2839-46.
135. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus L1 major capsid protein self-assembles into viruslike particles that are highly immunogenic, Proc Natl Acad Sci USA 1992; 89: 12180-4.
136. Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16, Mol Cell 2000; 5: 557-67.
137. Li M, Cripe TP, Estes PA, Lyon MK, Rose RC, Garcea RL. Expression of the human papillomavirus type 11 L1 capsid protein in Escherichia coli: characterization of protein domains involved in DNA binding and capsid assembly. J Virol 1997; 71: 2988-95.
138. Zhou J, Doorbar J, Sun XY, Crawford LV, McLean CS, Frazer IH. Identification of the nuclear localization signal of human papillomavirus type 16 L1 protein. Virology 1991; 185: 625-32.
139. Christensen ND, Kreider JW, Cladel NM, Patrick SD, Welsh PA. Monoclonal antibody-mediated neutralization of infectious human papillomavirus type 11. J Virol 1990; 64: 5678-81.
140. Christensen ND, Kreider JW. Antibody-mediated neutralization in vivo of infectious papillomaviruses. J Virol 1990; 64: 3151-6.
141. Bishop B, Dasgupta J, Klein M, et al. Crystal structures of four types of human papillomavirus L1 capsid proteins: understanding the specificity of neutralizing monoclonal antibodies. J Biol Chem 2007; 282: 31803-11.
142. Ludmerer SW, Benincasa D, Mark GE. 3rd; Christensen ND. A neutralizing epitope of human papillomavirus type 11 is principally described by a continuous set of residues which overlap a distinct linear, surface-exposed epitope. J Virol 1997; 71: 3834-9.
143. Christensen ND, Cladel NM, Reed CA, et al. Hybrid papillomavirus L1 molecules assemble into virus-like particles that reconstitute conformational epitopes and induce neutralizing antibodies to distinct HPV types. Virology 2001; 291: 324-34.
144. Lowe J, Panda D, Rose S, et al. Evolutionary and structural analyses of alpha-papillomavirus capsid proteins yields novel insights into L2 structure and interaction with L1, Virol J 2008; 5: 150.
145. Finnen RL, Erickson KD, Chen XS, Garcea RL. Interactions between papillomavirus L1 and L2 capsid proteins. J Virol 2003; 77: 4818-26.
146. Buck CB, Cheng N, Thompson CD, et al. Arrangement of L2 within the papillomavirus capsid. J Virol 2008; 82: 5190-7.
147. Sun XY, Frazer I, Muller M, Gissmann L, Zhou J. Sequences required for the nuclear targeting and accumulation of human papillomavirus type 6B L2 protein. Virology 1995; 213: 321-7.
148. Ma T, Zou N, Lin BY, Chow LT, Harper JW. Interaction between cyclin-dependent kinases and human papillomavirus replicationinitiation protein E1 is required for efficient viral replication, Proc Natl Acad Sci USA 1999; 96: 382-7.
149. Ma T, Van Tine BA, Wei Y, et al. Cell cycle-regulated phosphorylation of p220(NPAT) by cyclin E/Cdk2 in Cajal bodies promotes histone gene transcription, Genes Dev 2000; 14: 2298-313.
150. Deng W, Lin BY, Jin G, et al. Cyclin/CDK regulates the nucleocytoplasmic localization of the human papillomavirus E1 DNA helicase. J Virol 2004; 78: 13954-65.
151. Morin G, Fradet-Turcotte A, Di Lello P, Bergeron-Labrecque F, Omichinski JG, Archambault J. A conserved amphipathic helix in the N-terminal regulatory region of the papillomavirus E1 helicase is required for efficient viral DNA replication. J Virol 2011; 85: 5287-300.
152. Giri I, Yaniv M. Structural and mutational analysis of E2 transactivating proteins of papillomaviruses reveals three distinct functional domains, Embo J 1988; 7: 2823-9.
153. Falconi M, Santolamazza A, Eliseo T, de Prat-Gay G, Cicero DO, Desideri A. Molecular dynamics of the DNA-binding domain of the papillomavirus E2 transcriptional regulator uncover differential properties for DNA target accommodation, Febs J 2007; 274: 2385-95.
154. Falconi M, Oteri F, Eliseo T, Cicero DO, Desideri A. MD simulations of papillomavirus DNA-E2 protein complexes hints at a protein structural code for DNA deformation, Biophys J 2008; 95: 1108-17.
155. Eliseo T, Sanchez IE, Nadra AD, et al. Indirect DNA readout on the protein side: coupling between histidine protonation, global structural cooperativity, dynamics, and DNA binding of the human papillomavirus type 16 E2C domain. J Mol Biol 2009; 388: 327-44.
156. Hegde RS, Grossman SR, Laimins LA, Sigler PB. Crystal structure at 1.7 A of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target, Nature 1992; 359: 505-12.
157. Cicero DO, Nadra AD, Eliseo T, Dellarole M, Paci M, de Prat-Gay G. Structural and thermodynamic basis for the enhanced transcriptional control by the human papillomavirus strain-16 E2 protein, Biochemistry 2006; 45: 6551-60.
158. Brown C, Campos-Leon K, Strickland M, et al. Protein flexibility directs DNA recognition by the papillomavirus E2 proteins, Nucleic Acids Res 2011; 39: 2969-80.
159. McBride AA, Byrne JC, Howley PM. E2 polypeptides encoded by bovine papillomavirus type 1 form dimers through the common carboxyl-terminal domain: transactivation is mediated by the conserved amino-terminal domain, Proc Natl Acad Sci USA 1989; 86: 510-4.
160. Hegde RS. The papillomavirus E2 proteins: structure, function, and biology, Annu Rev Biophys Biomol Struct 2002; 31: 343-60.
161. Gunasekaran K, Tsai CJ, Nussinov R. Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers. J Mol Biol 2004; 341: 1327-41.
162. Giesel GM, Lima LM, Faber-Barata J, Guimaraes JA, Verli H. Characterization of the papillomavirus alpha(1)E2 peptide unfolded to folded transition upon DNA binding, FEBS Lett 2008; 582: 3619-24.
163. Veeraraghavan S, Mello CC, Androphy EJ, Baleja JD. Structural correlates for enhanced stability in the E2 DNA-binding domain from bovine papillomavirus, Biochemistry 1999; 38: 16115-24.
164. Roberts S, Ashmole I, Gibson LJ, Rookes SM, Barton GJ, Gallimore PH. Mutational analysis of human papillomavirus E4 proteins: identification of structural features important in the formation of cytoplasmic E4/cytokeratin networks in epithelial cells. J Virol 1994; 68: 6432-45.
165. McIntosh PB, Martin SR, Jackson DJ, et al. Structural analysis reveals an amyloid form of the human papillomavirus type 16 E1-- E4 protein and provides a molecular basis for its accumulation. J Virol 2008; 82: 8196-203.
166. Roberts S, Ashmole I, Johnson GD, Kreider JW, Gallimore PH. Cutaneous and mucosal human papillomavirus E4 proteins form intermediate filament-like structures in epithelial cells. Virology 1993; 197: 176-87.
167. Bubb V, McCance DJ, Schlegel R. DNA sequence of the HPV-16 E5 ORF and the structural conservation of its encoded protein. Virology 1988; 163: 243-6.
168. Yang DH, Wildeman AG, Sharom FJ. Overexpression, purification, and structural analysis of the hydrophobic E5 protein from human papillomavirus type 16, Protein Expr Purif 2003; 30: 1-10.
169. Gieswein CE, Sharom FJ, Wildeman AG. Oligomerization of the E5 protein of human papillomavirus type 16 occurs through multiple hydrophobic regions. Virology 2003; 313: 415-26.
170. Conrad M, Bubb VJ, Schlegel R. The human papillomavirus type 6 and 16 E5 proteins are membrane-associated proteins which associate with the 16-kilodalton pore-forming protein. J Virol 1993; 67: 6170-8.
171. Lowy DR, Dvoretzky I, Shober R, Law MF, Engel L, Howley PM. In vitro tumorigenic transformation by a defined sub-genomic fragment of bovine papilloma virus DNA, Nature 1980; 287: 72-4.
172. Dvoretzky I, Shober R, Chattopadhyay SK, Lowy DR. A quantitative in vitro focus assay for bovine papilloma virus. Virology 1980; 103: 369-75.
173. Schlegel R, Wade-Glass M, Rabson MS, Yang YC. The E5 transforming gene of bovine papillomavirus encodes a small, hydrophobic polypeptide, Science 1986; 233: 464-7.
174. Surti T, Klein O, Aschheim K, DiMaio D, Smith SO. Structural models of the bovine papillomavirus E5 protein, Proteins 1998; 33: 601-12.
175. Alonso A, Reed J. Modelling of the human papillomavirus type 16 E5 protein, Biochim Biophys Acta 2002; 1601: 9-18.
176. Chiti F, Webster P, Taddei N, et al. Designing conditions for in vitro formation of amyloid protofilaments and fibrils, Proc Natl Acad Sci USA 1999; 96: 3590-4.
177. Uversky VN, Li J, Fink AL. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J Biol Chem 2001; 276: 10737-44.
178. Souillac PO, Uversky VN, Millett IS, Khurana R, Doniach S, Fink AL. Elucidation of the molecular mechanism during the early events in immunoglobulin light chain amyloid fibrillation. Evidence for an off-pathway oligomer at acidic pH. J Biol Chem 2002; 277: 12666-79.
179. von Bergen M, Barghorn S, Biernat J, Mandelkow EM, Mandelkow E. Tau aggregation is driven by a transition from random coil to beta sheet structure, Biochim Biophys Acta 2005; 1739: 158-66.
180. Uversky VN. Mysterious oligomerization of the amyloidogenic proteins, Febs J 2010; 277: 2940-53.
181. Dao KK, Pey AL, Gjerde AU, et al. The regulatory subunit of PKA-I remains partially structured and undergoes beta-aggregation upon thermal denaturation, PLoS One 2011; 6: e17602.
182. Vetri V, Canale C, Relini A, et al. Amyloid fibrils formation and amorphous aggregation in concanavalin A, Biophys Chem 2007; 125: 184-90.
183. Chakrabarti O, Krishna S. Molecular interactions of 'high risk' human papillomaviruses E6 and E7 oncoproteins: implications for tumour progression. J Biosci 2003; 28: 337-48.
184. Cole ST, Danos O. Nucleotide sequence and comparative analysis of the human papillomavirus type 18 genome. Phylogeny of papillomaviruses and repeated structure of the E6 and E7 gene products. J Mol Biol 1987; 193: 599-608.
185. Pim D, Storey A, Thomas M, Massimi P, Banks L. Mutational analysis of HPV-18 E6 identifies domains required for p53 degradation in vitro, abolition of p53 transactivation in vivo and immortalisation of primary BMK cells, Oncogene 1994; 9: 1869-76.
186. Thomas M, Pim D, Banks L. The role of the E6-p53 interaction in the molecular pathogenesis of HPV, Oncogene 1999; 18: 7690-700.
187. Nomine Y, Ristriani T, Laurent C, Lefevre JF, Weiss E, Trave G. Formation of soluble inclusion bodies by hpv e6 oncoprotein fused to maltose-binding protein, Protein Expr Purif 2001; 23: 22-32.
188. Nomine Y, Charbonnier S, Ristriani T, et al. Domain substructure of HPV E6 oncoprotein: biophysical characterization of the E6 Cterminal DNA-binding domain, Biochemistry 2003; 42: 4909-17.
189. Garcia-Alai MM, Dantur KI, Smal C, Pietrasanta L, de Prat-Gay G. High-risk HPV E6 oncoproteins assemble into large oligomers that allow localization of endogenous species in prototypic HPVtransformed cell lines, Biochemistry 2007; 46: 341-9.
190. Zanier K, ould M'hamed ould Sidi A, Boulade-Ladame C, et al. Solution structure analysis of the HPV16 E6 oncoprotein reveals a self-association mechanism required for E6-mediated degradation of p53, Structure 2012; 20: 604-17.
191. Gage JR, Meyers C, Wettstein FO. The E7 proteins of the nononcogenic human papillomavirus type 6b (HPV-6b) and of the oncogenic HPV-16 differ in retinoblastoma protein binding and other properties. J Virol 1990; 64: 723-30.
192. Phelps WC, Munger K, Yee CL, Barnes JA, Howley PM. Structure-function analysis of the human papillomavirus type 16 E7 oncoprotein. J Virol 1992; 66: 2418-27.
193. McIntyre MC, Frattini MG, Grossman SR, Laimins LA. Human papillomavirus type 18 E7 protein requires intact Cys-X-X-Cys motifs for zinc binding, dimerization, and transformation but not for Rb binding. J Virol 1993; 67: 3142-50.
194. Reinstein E, Scheffner M, Oren M, Ciechanover A, Schwartz A. Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the Nterminal residue, Oncogene 2000; 19: 5944-50.
195. Oh KJ, Kalinina A, Wang J, Nakayama K, Nakayama KI, Bagchi S. The papillomavirus E7 oncoprotein is ubiquitinated by UbcH7 and Cullin 1- and Skp2-containing E3 ligase. J Virol 2004; 78: 5338-46.
196. Armstrong DJ, Roman A. Mutagenesis of human papillomavirus types 6 and 16 E7 open reading frames alters the electrophoretic mobility of the expressed proteins. J Gen Virol 1992; 73 (Pt 5): 1275-9.
197. Armstrong DJ, Roman A. The anomalous electrophoretic behavior of the human papillomavirus type 16 E7 protein is due to the high content of acidic amino acid residues, Biochem Biophys Res Commun 1993; 192: 1380-7.
198. Pahel G, Aulabaugh A, Short SA, et al. Structural and functional characterization of the HPV16 E7 protein expressed in bacteria. J Biol Chem 1993; 268: 26018-25.
199. Ohlenschlager O, Seiboth T, Zengerling H, et al. Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7, Oncogene 2006.
200. Alonso LG, Garcia-Alai MM, Nadra AD, et al. High-risk (HPV16) human papillomavirus E7 oncoprotein is highly stable and extended, with conformational transitions that could explain its multiple cellular binding partners, Biochemistry 2002; 41: 10510-8.
201. Vousden KH, Doniger J, DiPaolo JA, Lowy DR. The E7 open reading frame of human papillomavirus type 16 encodes a transforming gene, Oncogene Res 1988; 3: 167-75.
202. Halbert CL, Demers GW, Galloway DA. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J Virol 1991; 65: 473-8.
203. Phelps WC, Yee CL, Munger K, Howley PM. The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A, Cell 1988; 53: 539-47.
204. Storey A, Pim D, Murray A, Osborn K, Banks L, Crawford L. Comparison of the in vitro transforming activities of human papillomavirus types, Embo J 1988; 7: 1815-20.
205. Demers GW, Espling E, Harry JB, Etscheid BG, Galloway DA. Abrogation of growth arrest signals by human papillomavirus type 16 E7 is mediated by sequences required for transformation. J Virol 1996; 70: 6862-9.
206. Demers GW, Foster SA, Halbert CL, Galloway DA. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7, Proc Natl Acad Sci USA 1994; 91: 4382-6.
207. Ciccolini F, Di Pasquale G, Carlotti F, Crawford L, Tommasino M. Functional studies of E7 proteins from different HPV types, Oncogene 1994; 9: 2633-8.
208. Baker TS, Newcomb WW, Olson NH, Cowsert LM, Olson C, Brown JC. Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction, Biophys J 1991; 60: 1445-56.
209. Kirnbauer R, Taub J, Greenstone H, et al. Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles. J Virol 1993; 67: 6929-36.
210. Richards RM, Lowy DR, Schiller JT, Day PM. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection, Proc Natl Acad Sci USA 2006; 103: 1522-7.
211. Roden RB, Kirnbauer R, Jenson AB, Lowy DR, Schiller JT. Interaction of papillomaviruses with the cell surface. J Virol 1994; 68: 7260-6.
212. Meyers C, Frattini MG, Hudson JB, Laimins LA. Biosynthesis of human papillomavirus from a continuous cell line upon epithelial differentiation, Science 1992; 257: 971-3.
213. Buck CB, Pastrana DV, Lowy DR, Schiller JT. Efficient intracellular assembly of papillomaviral vectors. J Virol 2004; 78: 751-7.
214. Schiller JT, Day PM, Kines RC. Current understanding of the mechanism of HPV infection, Gynecol Oncol 2010; 118: S12-7.
215. Selinka HC, Florin L, Patel HD, et al. Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus. J Virol 2007; 81: 10970-80.
216. Day PM, Lowy DR, Schiller JT. Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J Virol 2008; 82: 12565-8.
217. Horvath CA, Boulet GA, Renoux VM, Delvenne PO, Bogers JP. Mechanisms of cell entry by human papillomaviruses: an overview, Virol J 2010; 7: 11.
218. Sapp M, Day PM. Structure, attachment and entry of polyoma- and papillomaviruses. Virology 2009; 384: 400-9.
219. Yang R, Day PM, Yutzy WH., Lin KY, Hung CF, Roden RB. Cell surface-binding motifs of L2 that facilitate papillomavirus infection. J Virol 2003; 77: 3531-41.
220. Pelkmans L, Helenius A. Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 2003; 15: 414-22.
221. Smith AE, Helenius A. How viruses enter animal cells, Science 2004; 304: 237-42.
222. Spoden G, Freitag K, Husmann M, et al. Clathrin- and caveolinindependent entry of human papillomavirus type 16--involvement of tetraspanin-enriched microdomains (TEMs), PLoS One 2008; 3: e3313.
223. Berg M, Stenlund A. Functional interactions between papillomavirus E1 and E2 proteins. J Virol 1997; 71: 3853-63.
224. Rocque WJ, Porter DJ, Barnes JA, et al. Replication-associated activities of purified human papillomavirus type 11 E1 helicase, Protein Expr Purif 2000; 18: 148-59.
225. Conger KL, Liu JS, Kuo SR, Chow LT, Wang TS. Human papillomavirus DNA replication. Interactions between the viral E1 protein and two subunits of human dna polymerase alpha/primase. J Biol Chem 1999; 274: 2696-705.
226. Hu Y, Clower RV, Melendy T. Cellular topoisomerase I modulates origin binding by bovine papillomavirus type 1 E1. J Virol 2006; 80: 4363-71.
227. Clower RV, Fisk JC, Melendy T. Papillomavirus E1 protein binds to and stimulates human topoisomerase I. J Virol 2006; 80: 1584-7.
228. Han Y, Loo YM, Militello KT, Melendy T. Interactions of the papovavirus DNA replication initiator proteins, bovine papillomavirus type 1 E1 and simian virus 40 large T antigen, with human replication protein A. J Virol 1999; 73: 4899-907.
229. Loo YM, Melendy T. Recruitment of replication protein A by the papillomavirus E1 protein and modulation by single-stranded DNA. J Virol 2004; 78: 1605-15.
230. Chiang CM, Ustav M, Stenlund A, Ho TF, Broker TR, Chow LT. Viral E1 and E2 proteins support replication of homologous and heterologous papillomaviral origins, Proc Natl Acad Sci USA 1992; 89: 5799-803.
231. Ilves I, Kivi S, Ustav M. Long-term episomal maintenance of bovine papillomavirus type 1 plasmids is determined by attachment to host chromosomes, which Is mediated by the viral E2 protein and its binding sites. J Virol 1999; 73: 4404-12.
232. Bernard BA, Bailly C, Lenoir MC, Darmon M, Thierry F, Yaniv M. The human papillomavirus type 18 (HPV18) E2 gene product is a repressor of the HPV18 regulatory region in human keratinocytes. J Virol 1989; 63: 4317-24.
233. Demeret C, Desaintes C, Yaniv M, Thierry F. Different mechanisms contribute to the E2-mediated transcriptional repression of human papillomavirus type 18 viral oncogenes. J Virol 1997; 71: 9343-9.
234. Soeda E, Ferran MC, Baker CC, McBride AA. Repression of HPV16 early region transcription by the E2 protein. Virology 2006; 351: 29-41.
235. Sedman J, Stenlund A. The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities. J Virol 1998; 72: 6893-97.
236. Fouts ET, Yu X, Egelman EH, Botchan MR. Biochemical and electron microscopic image analysis of the hexameric E1 helicase. J Biol Chem 1999; 274: 4447-58.
237. Titolo S, Pelletier A, Pulichino AM, et al. Identification of domains of the human papillomavirus type 11 E1 helicase involved in oligomerization and binding to the viral origin. J Virol 2000; 74: 7349-61.
238. Sanders CM, Stenlund A. Recruitment and loading of the E1 initiator protein: an ATP-dependent process catalysed by a transcription factor, Embo J 1998; 17: 7044-55.
239. McIntyre MC, Ruesch MN, Laimins LA. Human papillomavirus E7 oncoproteins bind a single form of cyclin E in a complex with cdk2 and p107. Virology 1996; 215: 73-82.
240. Massimi P, Pim D, Banks L. Human papillomavirus type 16 E7 binds to the conserved carboxy-terminal region of the TATA box binding protein and this contributes to E7 transforming activity J Gen Virol 1997; 78(Pt 10): 2607-13.
241. Halpern AL, Münger K. HPV-16 E7: Correspondence between primary structure and biological properties, in: HPV Sequence Database, Los Alamos National Laboratory, Los Alamos 1995; pp: III-58-III-73.
242. Jian Y, Schmidt-Grimminger DC, Chien WM, Wu X, Broker TR, Chow LT. Post-transcriptional induction of p21cip1 protein by human papillomavirus E7 inhibits unscheduled DNA synthesis reactivated in differentiated keratinocytes, Oncogene 1998; 17: 2027-38.
243. Tommasino M, Adamczewski JP, Carlotti F, et al. HPV16 E7 protein associates with the protein kinase p33CDK2 and cyclin A, Oncogene 1993; 8: 195-202.
244. Brehm A, Nielsen SJ, Miska EA, et al. The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth, Embo J 1999; 18: 2449-58.
245. Dyson N, Howley PM, Munger K, Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product, Science 1989; 243: 934-7.
246. Zwerschke W, Mazurek S, Massimi P, Banks L, Eigenbrodt E, Jansen-Durr P. Modulation of type M2 pyruvate kinase activity by the human papillomavirus type 16 E7 oncoprotein, Proc Natl Acad Sci USA 1999; 96: 1291-6.
247. Mazurek S, Zwerschke W, Jansen-Durr P, Eigenbrodt E. Effects of the human papilloma virus HPV-16 E7 oncoprotein on glycolysis and glutaminolysis: role of pyruvate kinase type M2 and the glycolytic-enzyme complex, Biochem J 2001; 356: 247-56.
248. Pim D, Massimi P, Dilworth SM, Banks L. Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A, Oncogene 2005; 24: 7830-8.
249. Brazil DP, Hemmings BA. Ten years of protein kinase B signalling: a hard Akt to follow, Trends Biochem Sci 2001; 26: 657-64.
250. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53, Cell 1990; 63: 1129-36.
251. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. The HPV- 16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53, Cell 1993; 75: 495-505.
252. Gross-Mesilaty S, Reinstein E, Bercovich B, et al. Basal and human papillomavirus E6 oncoprotein-induced degradation of Myc proteins by the ubiquitin pathway, Proc Natl Acad Sci USA 1998; 95: 8058-63.
253. Ronco LV, Karpova AY, Vidal M, Howley PM. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity, Genes Dev 1998; 12: 2061-72.
254. Patel D, Huang SM, Baglia LA, McCance DJ. The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300, Embo J 1999; 18: 5061-72.
255. Zimmermann H, Degenkolbe R, Bernard HU, O'Connor MJ. The human papillomavirus type 16 E6 oncoprotein can down-regulate p53 activity by targeting the transcriptional coactivator CBP/p300. J Virol 1999; 73: 6209-19.
256. Kumar A, Zhao Y, Meng G, et al. Human papillomavirus oncoprotein E6 inactivates the transcriptional coactivator human ADA3, Mol Cell Biol 2002; 22: 5801-12.
257. Srivenugopal KS, Ali-Osman F. The DNA repair protein, O(6)- methylguanine-DNA methyltransferase is a proteolytic target for the E6 human papillomavirus oncoprotein, Oncogene 2002; 21: 5940-5.
258. Kukimoto I, Aihara S, Yoshiike K, Kanda T. Human papillomavirus oncoprotein E6 binds to the C-terminal region of human minichromosome maintenance 7 protein, Biochem Biophys Res Commun 1998; 249: 258-62.
259. Gao Q, Srinivasan S, Boyer SN, Wazer DE, Band V. The E6 oncoproteins of high-risk papillomaviruses bind to a novel putative GAP protein, E6TP1, and target it for degradation, Mol Cell Biol 1999; 19: 733-44.
260. Gao Q, Kumar A, Srinivasan S, et al. PKN binds and phosphorylates human papillomavirus E6 oncoprotein. J Biol Chem 2000; 275: 14824-30.
261. Chen JJ, Reid CE, Band V, Androphy EJ. Interaction of papillomavirus E6 oncoproteins with a putative calcium-binding protein, Science 1995; 269: 529-31.
262. Filippova M, Song H, Connolly JL, Dermody TS, Duerksen- Hughes PJ. The human papillomavirus 16 E6 protein binds to tumor necrosis factor (TNF) R1 and protects cells from TNFinduced apoptosis. J Biol Chem 2002; 277: 21730-9.
263. Kiyono T, Hiraiwa A, Fujita M, Hayashi Y, Akiyama T, Ishibashi M. Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein, Proc Natl Acad Sci USA 1997; 94: 11612-6.
264. Nakagawa S, Huibregtse JM. Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase, Mol Cell Biol 2000; 20: 8244-53.
265. Glaunsinger BA, Lee SS, Thomas M, Banks L, Javier R. Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins, Oncogene 2000; 19: 5270-80.
266. Lee SS, Glaunsinger B, Mantovani F, Banks L, Javier RT. Multi- PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J Virol 2000; 74: 9680-93.
267. Tong X, Howley PM. The bovine papillomavirus E6 oncoprotein interacts with paxillin and disrupts the actin cytoskeleton, Proc Natl Acad Sci USA 1997; 94: 4412-7.
268. Thomas M, Banks L. Inhibition of Bak-induced apoptosis by HPV- 18 E6, Oncogene 1998; 17: 2943-54.
269. Tong X, Boll W, Kirchhausen T, Howley PM. Interaction of the bovine papillomavirus E6 protein with the clathrin adaptor complex AP-1. J Virol 1998; 72: 476-82.
270. Sedman SA, Barbosa MS, Vass WC, et al. The full-length E6 protein of human papillomavirus type 16 has transforming and trans-activating activities and cooperates with E7 to immortalize keratinocytes in culture. J Virol 1991; 65: 4860-6.
271. Morosov A, Phelps WC, Raychaudhuri P. Activation of the c-fos gene by the HPV16 oncoproteins depends upon the cAMPresponse element at -60. J Biol Chem 1994; 269: 18434-40.
272. Dey A, Atcha IA, Bagchi S. HPV16 E6 oncoprotein stimulates the transforming growth factor-beta 1 promoter in fibroblasts through a specific GC-rich sequence. Virology 1997; 228: 190-9.
273. Gewin L, Galloway DA. E box-dependent activation of telomerase by human papillomavirus type 16 E6 does not require induction of c-myc. J Virol 2001; 75: 7198-201.
274. Oh ST, Kyo S, Laimins LA. Telomerase activation by human papillomavirus type 16 E6 protein: induction of human telomerase reverse transcriptase expression through Myc and GC-rich Sp1 binding sites. J Virol 2001; 75: 5559-66.
275. Liu X, Dakic A, Zhang Y, Dai Y, Chen R, Schlegel R. HPV E6 protein interacts physically and functionally with the cellular telomerase complex, Proc Natl Acad Sci USA 2009; 106: 18780-5.
276. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer, Science 1994; 266: 2011-5.
277. Harley CB, Kim NW, Prowse KR, et al. Telomerase, cell immortality, and cancer, Cold Spring Harb Symp Quant Biol 1994; 59: 307-15.
278. Ristriani T, Masson M, Nomine Y, et al. HPV oncoprotein E6 is a structure-dependent DNA-binding protein that recognizes four-way junctions. J Mol Biol 2000; 296: 1189-203.
279. Ristriani T, Nomine Y, Masson M, Weiss E, Trave G. Specific recognition of four-way DNA junctions by the C-terminal zincbinding domain of HPV oncoprotein E6. J Mol Biol 2001; 305: 729-39.
280. Fehrmann F, Laimins LA. Human papillomaviruses: targeting differentiating epithelial cells for malignant transformation, Oncogene 2003; 22: 5201-7.
281. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation, Nat Rev Cancer 2010; 10: 550-60.
282. Disbrow GL, Sunitha I, Baker CC, Hanover J, Schlegel R. Codon optimization of the HPV-16 E5 gene enhances protein expression. Virology 2003; 311: 105-14.
283. Suprynowicz FA, Disbrow GL, Krawczyk E, Simic V, Lantzky K, Schlegel R. HPV-16 E5 oncoprotein upregulates lipid raft components caveolin-1 and ganglioside GM1 at the plasma membrane of cervical cells, Oncogene 2008; 27: 1071-8.
284. Krawczyk E, Suprynowicz FA, Sudarshan SR, Schlegel R. Membrane orientation of the human papillomavirus type 16 E5 oncoprotein. J Virol 2010; 84: 1696-703.
285. Krawczyk E, Suprynowicz FA, Hebert JD, Kamonjoh CM, Schlegel R. The human papillomavirus type 16 E5 oncoprotein translocates calpactin I to the perinuclear region. J Virol 2011; 85: 10968-75.
286. Disbrow GL, Hanover JA, Schlegel R. Endoplasmic reticulumlocalized human papillomavirus type 16 E5 protein alters endosomal pH but not trans-Golgi pH. J Virol 2005; 79: 5839-46.
287. Suprynowicz FA, Krawczyk E, Hebert JD, et al. The human papillomavirus type 16 E5 oncoprotein inhibits epidermal growth factor trafficking independently of endosome acidification. J Virol 2010; 84: 10619-29.
288. Krawczyk E, Suprynowicz FA, Liu X, et al. Koilocytosis: a cooperative interaction between the human papillomavirus E5 and E6 oncoproteins, Am J Pathol 2008; 173: 682-8.
289. Genther Williams SM, Disbrow GL, Schlegel R, Lee D, Threadgill DW, Lambert PF. Requirement of epidermal growth factor receptor for hyperplasia induced by E5, a high-risk human papillomavirus oncogene, Cancer Res 2005; 65: 6534-42.
290. Suprynowicz FA, Disbrow GL, Simic V, Schlegel R. Are transforming properties of the bovine papillomavirus E5 protein shared by E5 from high-risk human papillomavirus type 16?. Virology 2005; 332: 102-13.
291. Nasseri M, Hirochika R, Broker TR, Chow LT. A human papilloma virus type 11 transcript encoding an E1--E4 protein. Virology 1987; 159: 433-9.
292. Davy CE, Jackson DJ, Raj K, et al. Human papillomavirus type 16 E1 E4-induced G2 arrest is associated with cytoplasmic retention of active Cdk1/cyclin B1 complexes. J Virol 2005; 79: 3998-4011.
293. Doorbar J, Ely S, Sterling J, McLean C, Crawford L. Specific interaction between HPV-16 E1-E4 and cytokeratins results in collapse of the epithelial cell intermediate filament network, Nature 1991; 352: 824-7.
294. Davy CE, Jackson DJ, Wang Q, et al. Identification of a G(2) arrest domain in the E1 wedge E4 protein of human papillomavirus type 16. J Virol 2002; 76: 9806-18.
295. Nakahara T, Nishimura A, Tanaka M, Ueno T, Ishimoto A, Sakai H. Modulation of the cell division cycle by human papillomavirus type 18 E4. J Virol 2002; 76: 10914-20.
296. Knight GL, Grainger JR, Gallimore PH, Roberts S. Cooperation between different forms of the human papillomavirus type 1 E4 protein to block cell cycle progression and cellular DNA synthesis. J Virol 2004; 78: 13920-33.
297. Raj K, Berguerand S, Southern S, Doorbar J, Beard P. E1 empty set E4 protein of human papillomavirus type 16 associates with mitochondria. J Virol 2004; 78: 7199-207.
298. Doorbar J, Elston RC, Napthine S, et al. The E1E4 protein of human papillomavirus type 16 associates with a putative RNA helicase through sequences in its C terminus. J Virol 2000; 74: 10081-95.
299. Roberts S, Kingsbury SR, Stoeber K, Knight GL, Gallimore PH, Williams GH. Identification of an arginine-rich motif in human papillomavirus type 1 E1;E4 protein necessary for E4-mediated inhibition of cellular DNA synthesis in vitro and in cells. J Virol 2008; 82: 9056-64.
300. Xue B, Dunbrack RL, Williams RW, Dunker AK, Uversky VN. PONDR-FIT: a meta-predictor of intrinsically disordered amino acids, Biochim Biophys Acta 2010; 1804: 996-1010.
301. Doorbar J. The papillomavirus life cycle. J Clin Virol 2005; 32 Suppl 1: S7-15.