An RNA Aptamer Provides a Novel Approach for the Induction of Apoptosis by Targeting the HPV16 E7 Oncoprotein

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Nicol, Clare ^a   Cesur, Özlem ^a   Forrest, Sophie ^a   Belyaeva, Tamara A ^a   Bunka, David H J ^a   Blair, G Eric ^a   Stonehouse, Nicola J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; APTAMER; CELL CYCLE PROTEIN; LIPOCORTIN 5; PEGAPTANIB; PROPIDIUM IODIDE; PROTEIN E7; PROTEIN PRB; SINGLE STRANDED RNA; STAUROSPORINE; UNCLASSIFIED DRUG; VIRUS DNA;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CARCINOMA CELL; CELL PROLIFERATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IN VITRO STUDY; MOLECULAR DYNAMICS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; UTERINE CERVIX CARCINOMA;

APOPTOSIS; APTAMERS, NUCLEOTIDE; BASE SEQUENCE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, VIRAL; HUMANS; PAPILLOMAVIRUS E7 PROTEINS; RETINOBLASTOMA PROTEIN; TRANSFECTION;

HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 84878495086     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064781     Document Type: Article

References (69)

1. de Villiers E-M, Fauquet C, Broker TR, Bernard H-U, zur Hausen H, (2004) Classification of papillomaviruses. Virology 324: 17-27.
2. Bernard H-U, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, et al. (2010) Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401: 70-79.
3. Muñoz N, Bosch FX, Castellsagué X, Díaz M, de Sanjose S, et al. (2004) Against which human papillomavirus types shall we vaccinate and screen? The international perspective. International Journal of Cancer 111: 278-285.
4. Parkin DM, Bray F, (2006) Chapter 2: The burden of HPV-related cancers. Vaccine 24: S11-S25.
5. Jeon S, Lambert PF, (1995) Integration of human papillomavirus type 16 DNA into the human genome leads to increased stability of E6 and E7 mRNAs: implications for cervical carcinogenesis. Proceedings of the National Academy of Sciences (USA) 92: 1654-1658.
6. Pett M, Coleman N, (2007) Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? Journal of Pathology 212: 356-367.
7. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM, (1990) The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63: 1129-1136.
8. Lechner MS, Laimins LA, (1994) Inhibition of p53 DNA binding by human papillomavirus E6 proteins. Journal of Virology 68: 4262-4273.
9. Dyson N, Howley PM, Munger K, Harlow E, (1989) The human papilloma virus-16 E7-oncoprotein is able to bind to the retinoblastoma gene-product. Science 243: 934-937.
10. Boyer SN, Wazer DE, Band V, (1996) E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Research 56: 4620-4624.
11. Chellappan S, Kraus VB, Kroger B, Munger K, Howley PM, et al. (1992) Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proceedings of the National Academy of Sciences (USA) 89: 4549-4553.
12. zur Hausen H, (2000) Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis. Journal of the National Cancer Institute 92: 690-698.
13. Wise-Draper T, Wells S, (2008) Papillomavirus E6 and E7 proteins and their cellular targets. Frontiers in Bioscience 13: 1003-1017.
14. Nicol C, Bunka DHJ, Blair GE, Stonehouse NJ, (2011) Effects of single nucleotide changes on the binding and activity of RNA aptamers to human papillomavirus 16 E7 oncoprotein. Biochemical and Biophysical Research Communications 405: 417-421.
15. Blank M, Blind M, (2005) Aptamers as tools for target validation. Current Opinion in Chemical Biology 9: 336-342.
16. Bunka DH, Stockley PG, (2006) Aptamers come of age- at last. Nature Reviews Microbiology 4: 588-596.
17. Mayer G, (2009) The Chemical Biology of Aptamers. Angewandte Chemie International Edition 48: 2672-2689.
18. Ellington AD, Szostak JW, (1990) In vitro selection of RNA molecules that bind specific ligands. Nature 346: 818-822.
19. Robertson DL, Joyce GF, (1990) Selection in vitro of an RNA enzyme that specifically cleaves single-stranded DNA. Nature 344: 467-468.
20. Tuerk C, Gold L, (1990) Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249: 505-510.
21. James W, (2007) Aptamers in the virologists' toolkit. Journal of General Virology 88: 351-364.
22. Ni X, Castanares M, Mukherjee A, Lupold SE, (2011) Nucleic acid aptamers: clinical applications and promising new horizons. Current Medicinal Chemistry 18: 4206-4214.
23. Fukuda K, Umehara T, Sekiya S, Kunio K, Hasegawa T, et al. (2004) An RNA ligand inhibits hepatitis C virus NS3 protease and helicase activities. Biochemical and Biophysical Research Communications 325: 670-675.
24. Biroccio A, Hamm J, Incitti I, De Francesco R, Tomei L, (2002) Selection of RNA aptamers that are specific and high-affinity ligands of the hepatitis C virus RNA-dependent RNA polymerase. Journal of Virology 76: 3688-3696.
25. Jang KJ, Lee N-R, Yeo W-S, Jeong Y-J, Kim D-E, (2008) Isolation of inhibitory RNA aptamers against severe acute respiratory syndrome (SARS) coronavirus NTPase/Helicase. Biochemical and Biophysical Research Communications 366: 738-744.
26. Cheng C, Dong J, Yao L, Chen A, Jia R, et al. (2008) Potent inhibition of human influenza H5N1 virus by oligonucleotides derived by SELEX. Biochemical and Biophysical Research Communications 366: 670-674.
27. Ellingham M, Bunka DHJ, Rowlands DJ, Stonehouse NJ, (2006) Selection and characterization of RNA aptamers to the RNA-dependent RNA polymerase from foot-and-mouth disease virus. RNA 12: 1970-1979.
28. Beigelman L, McSwiggen JA, Draper KG, Gonzalez C, Jensen K, et al. (1995) Chemical modification of hammerhead ribozymes. Journal of Biological Chemistry 270: 25702-25708.
29. Pieken WA, Olsen DB, Benseler F, Aurup H, Eckstein F, (1991) Kinetic characterization of ribonuclease-resistant 2'-modified hammerhead ribozymes. Science 253: 314-317.
30. Baker CC, Phelps WC, Lindgren V, Braun MJ, Gonda MA, et al. (1987) Structural and transcriptional analysis of human papillomavirus type 16 sequences in cervical carcinoma cell lines. Journal of Virology 61: 962-971.
31. Boukamp P, Petrussevska RT, Breitkreutz D, Hornung J, Markham A, et al. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. Journal of Cell Biology 106: 761-771.
32. Yee C, Krishnan-Hewlett I, Baker C, Schlegel R, Howley P, (1985) Presence and expression of human papillomavirus sequences in human cervical carcinoma cell lines. American Journal of Pathology 119: 361-366.
33. Mincheva A, Gissmann L, zur Hausen H, (1987) Chromosomal integration sites of human papillomavirus DNA in three cervical cancer cell lines mapped by in situ hybridization. Medical Microbiology and Immunology 176: 245-256.
34. Boyd JM, Huang L, Xie L, Moe B, Gabos S, et al. (2008) A cell-microelectronic sensing technique for profiling cytotoxicity of chemicals. Analytica Chimica Acta 615: 80-87.
35. Kirstein SL, Atienza JM, Xi B, Zhu J, Yu N, et al. (2006) Live cell quality control and utility of real-time cell electronic sensing for assay development. Assay and Drug Development Technologies 4: 545-553.
36. Couldwell WT, Hinton DR, He S, Chen TC, Sebat I, et al. (1994) Protein kinase C inhibitors induce apoptosis in human malignant glioma cell lines. FEBS Letters 345: 43-46.
37. Rüegg U, Burgess G, (1989) Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases. Trends in Pharmacological Sciences 10: 218-220.
38. Abassi YA, Xi B, Zhang W, Ye P, Kirstein SL, et al. (2009) Kinetic cell-based morphological screening: prediction of mechanism of compound action and off-target effects. Chemistry and Biology 16: 712-723.
39. Xing JZ, Zhu L, Gabos S, Xie L, (2006) Microelectronic cell sensor assay for detection of cytotoxicity and prediction of acute toxicity. Toxicology in Vitro 20: 995-1004.
40. He X, Wang J, Steele J, Sun X, Nie W, et al. (2009) An ultrasensitive rapid immunocytotoxicity assay for detecting Clostridium difficile toxins. Journal of Microbiological Methods 78: 97-100.
41. Yu S-L, Chan P, Wong C-K, Szeto C-C, Ho S, et al. (2012) Antagonist-mediated down-regulation of toll-like receptors increases the prevalence of human papillomavirus infection in systemic lupus erythematosus. Arthritis Research & Therapy 14: R80.
42. Barbosa MS, Edmonds C, Fisher C, Schiller JT, Lowy DR, et al. (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 Journal 9: 153-160.
43. Jones RE, Wegrzyn RJ, Patrick DR, Balishin NL, Vuocolo GA, et al. (1990) Identification of HPV-16 E7 peptides that are potent antagonists of E7 binding to the retinoblastoma suppressor protein. Journal of Biological Chemistry 265: 12782-12785.
44. 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. Journal of Biological Chemistry 281: 578-586.
45. Bernat A, Avvakumov N, Mymryk JS, Banks L, (2003) Interaction between the HPV E7 oncoprotein and the transcriptional coactivator p300. Oncogene 22: 7871-7881.
46. Massimi P, Pim D, Banks L, (1997) 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. Journal of General Virology 78: 2607-2613.
47. Robinson MA, Wood JPA, Capaldi SA, Baron AJ, Gell C, et al. (2006) Affinity of molecular interactions in the bacteriophage phi29 DNA packaging motor. Nucleic Acids Research 34: 2698-2709.
48. Gopinath SCB, (2007) Antiviral aptamers. Archives of Virology 152: 2137-2157.
49. Bunka DHJ, Platonova O, Stockley PG, (2010) Development of aptamer therapeutics. Current Opinion in Pharmacology 10: 557-562.
50. Oh K-J, Kalinina A, Wang J, Nakayama K, Nakayama KI, et al. (2004) The papillomavirus E7 oncoprotein is ubiquitinated by UbcH7 and Cullin 1- and Skp2-containing E3 ligase. Journal of Virology 78: 5338-5346.
51. Reinstein E, Scheffner M, Oren M, Ciechanover A, Schwartz A, (2000) Degradation of the E7 human papillomavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue. Oncogene 19: 5944-5950.
52. 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.
53. Ohlenschlager O, Seiboth T, Zengerling H, Briese L, Marchanka A, et al. (2006) Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7. Oncogene 25: 5953-5959.
54. 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. Journal of Proteome Research 5: 1829-1842.
55. Ryan JB, Wesley AB, Susanne IW, Erik SK, (2009) Activation of the retinoblastoma tumor suppressor mediates cell cycle inhibition and cell death in specific cervical cancer cell lines. Molecular Carcinogenesis 48: 45-55.
56. Jiang M, Milner J, (2002) Selective silencing of viral gene expression in HPV-positive human cervical carcinoma cells treated with siRNA, a primer of RNA interference. Oncogene 21: 6041-6048.
57. Bottley G, Watherston OG, Hiew YL, Norrild B, Cook GP, et al. (2007) High-risk human papillomavirus E7 expression reduces cell-surface MHC class I molecules and increases susceptibility to natural killer cells. Oncogene 27: 1794-1799.
58. Yamato K, Yamada T, Kizaki M, Ui-Tei K, Natori Y, et al. (2007) New highly potent and specific E6 and E7 siRNAs for treatment of HPV16 positive cervical cancer. Cancer Gene Therapy 15: 140-153.
59. Guo C, Liu K, Luo H, Chen H, Zheng Y, et al. (2011) Potent anti-tumor effect generated by a novel human papillomavirus (HPV) antagonist peptide reactivating the pRb/E2F pathway. PLoS ONE 6: e17734.
60. Guo C, Liu K, Zheng Y, Luo H, Chen H, et al. (2011) Apoptosis induced by an antagonist peptide against HPV16 E7 in vitro and in vivo via restoration of p53. Apoptosis 16: 606-618.
61. Nauenburg S, Zwerschke W, Jansen-Dürr P, (2001) Induction of apoptosis in cervical carcinoma cells by peptide aptamers that bind to the HPV-16 E7 oncoprotein. FASEB Journal 15: 592-594.
62. Toscano-Garibay JD, Benítez-Hess ML, Alvarez-Salas LM, (2011) Isolation and characterization of an RNA aptamer for the HPV-16 E7 oncoprotein. Archives of Medical Research 42: 88-96.
63. Edmonds C, Vousden KH, (1989) A point mutational analysis of human papillomavirus type 16 E7 protein. Journal of Virology 63: 2650-2656.
64. Friedl F, Kimura I, Osato T, Ito Y, (1970) Studies on a new human cell line (SiHa) derived from carcinoma of uterus. I. Its establishment and morphology. Proceedings of the Society for Experimental Biology and Medicine 135: 543-545.
65. Pattillo R, Hussa R, Story M, Ruckert A, Shalaby M, et al. (1977) Tumor antigen and human chorionic gonadotropin in CaSki cells: a new epidermoid cervical cancer cell line. Science 196: 1456-1458.
66. Gey GO, Coffman WD, Kubicek MT, (1952) Tissue culture studies of the proliferative capacity of cervical carcinoma and normal epithelium. Cancer Research 12: 264-265.
67. Auersperg N, (1964) Long-term cultivation of hypodiploid human tumor cells. Journal of the National Cancer Institute 32: 135-163.
68. Padilla R, Sousa R, (2002) A Y639F/H784A T7 RNA polymerase double mutant displays superior properties for synthesizing RNAs with non-canonical NTPs. Nucleic Acids Research 30: e138.
69. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406-3415.