DNA Damage Repair Genes Controlling Human Papillomavirus (HPV) Episome Levels under Conditions of Stability and Extreme Instability

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Edwards, Terri G ^a   Vidmar, Thomas J ^b   Koeller, Kevin ^c   Bashkin, James K ^a,c   Fisher, Chris ^a  

^a NanoVir   (United States)

^b BioSTAT Consultants   (United States)

^c UNIVERSITY OF MISSOURI ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMIDAZOLE; MRE11 PROTEIN; N METHYLPYRROLE IMIDAZOLE HAIRPIN POLYAMIDE; PROTEIN RAD9; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DDR GENE; DNA BINDING; DNA STRAND BREAKAGE; DRUG DNA BINDING; DRUG STRUCTURE; EPISOME; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; GENETIC REGULATION; GENETIC STABILITY; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; NONHUMAN; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REPRESSOR GENE; SOUTHERN BLOTTING; TDP1 GENE; TDP2 GENE; VIRUS CELL INTERACTION; VIRUS GENE; WART VIRUS;

ALPHAPAPILLOMAVIRUS; CELL LINE; DNA DAMAGE; DNA REPAIR; DNA, VIRAL; GENE KNOCKDOWN TECHNIQUES; GENES, VIRAL; HUMANS; IMIDAZOLES; KERATINOCYTES; PLASMIDS; RNA, SMALL INTERFERING;

EID: 84884859066     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075406     Document Type: Article

References (56)

1. Howley PM, Lowy DR (2007) Papillomaviruses. In: Knipe DM, Howley PM, editors. Fields Virology. 5th ed. Philadelphia: Lippincott Williams & Wilkins. pp. 2299-2354.
2. Bodily J, Laimins LA, (2011) Persistence of human papillomavirus infection: keys to malignant progression. Trends in microbiology 19: 33-39.
3. Woodman CB, Collins SI, Young LS, (2007) The natural history of cervical HPV infection: unresolved issues. Nature reviews Cancer 7: 11-22.
4. Chen HC, Schiffman M, Lin CY, Pan MH, You SL, et al. (2011) Persistence of type-specific human papillomavirus infection and increased long-term risk of cervical cancer. Journal of the National Cancer Institute 103: 1387-1396.
5. Kravchenko J, Akushevich I, Sudenga SL, Wilson CM, Levitan EB, et al. (2012) Transitional probability-based model for HPV clearance in HIV-1-positive adolescent females. PloS one 7: e30736.
6. Molho-Pessach V, Lotem M, (2007) Viral carcinogenesis in skin cancer. Current problems in dermatology 35: 39-51.
7. Stanley MA, (2012) Epithelial cell responses to infection with human papillomavirus. Clinical microbiology reviews 25: 215-222.
8. Edwards TG, Koeller KJ, Slomczynska U, Fok K, Helmus M, et al. (2011) HPV episome levels are potently decreased by pyrrole-imidazole polyamides. Antiviral research 91: 177-186.
9. Edwards TG, Helmus MJ, Koeller K, Bashkin JK, Fisher C, (2013) HPV Episome Stability is Reduced by Aphidicolin and Controlled by DNA Damage Response Pathways. Journal of virology 87: 11.
10. Hong S, Mehta KP, Laimins LA, (2011) Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiation-dependent genome amplification and plasmid maintenance. Journal of virology 85: 9486-9494.
11. McBride AA, Sakakibara N, Stepp WH, Jang MK, (2012) Hitchhiking on host chromatin: how papillomaviruses persist. Biochimica et biophysica acta 1819: 820-825.
12. Weitzman MD, Lilley CE, Chaurushiya MS, (2010) Genomes in conflict: maintaining genome integrity during virus infection. Annual review of microbiology 64: 61-81.
13. Nikitin PA, Luftig MA, (2011) At a crossroads: human DNA tumor viruses and the host DNA damage response. Future virology 6: 813-830.
14. Harper JW, Elledge SJ, (2007) The DNA damage response: ten years after. Molecular cell 28: 739-745.
15. Turnell AS, Grand RJ, (2012) DNA viruses and the cellular DNA-damage response. The Journal of general virology 93: 2076-2097.
16. Moody CA, Laimins LA, (2009) Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS pathogens 5: e1000605.
17. Moody CA, Fradet-Turcotte A, Archambault J, Laimins LA, (2007) Human papillomaviruses activate caspases upon epithelial differentiation to induce viral genome amplification. Proceedings of the National Academy of Sciences of the United States of America 104: 19541-19546.
18. Fradet-Turcotte A, Bergeron-Labrecque F, Moody CA, Lehoux M, Laimins LA, et al. (2011) Nuclear accumulation of the papillomavirus E1 helicase blocks S-phase progression and triggers an ATM-dependent DNA damage response. Journal of virology.
19. Sakakibara N, Mitra R, McBride AA, (2011) The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. Journal of virology 85: 8981-8995.
20. Moldovan GL, D'Andrea AD, (2009) How the fanconi anemia pathway guards the genome. Annual review of genetics 43: 223-249.
21. van Zeeburg HJ, Snijders PJ, Wu T, Gluckman E, Soulier J, et al. (2008) Clinical and molecular characteristics of squamous cell carcinomas from Fanconi anemia patients. Journal of the National Cancer Institute 100: 1649-1653.
22. Kutler DI, Wreesmann VB, Goberdhan A, Ben-Porat L, Satagopan J, et al. (2003) Human papillomavirus DNA and p53 polymorphisms in squamous cell carcinomas from Fanconi anemia patients. Journal of the National Cancer Institute 95: 1718-1721.
23. Hoskins EE, Morris TA, Higginbotham JM, Spardy N, Cha E, et al. (2009) Fanconi anemia deficiency stimulates HPV-associated hyperplastic growth in organotypic epithelial raft culture. Oncogene 28: 674-685.
24. Hoskins EE, Morreale RJ, Werner SP, Higginbotham JM, Laimins LA, et al. (2012) The fanconi anemia pathway limits human papillomavirus replication. Journal of virology 86: 8131-8138.
25. Lamarche BJ, Orazio NI, Weitzman MD, (2010) The MRN complex in double-strand break repair and telomere maintenance. FEBS letters 584: 3682-3695.
26. Czornak K, Chughtai S, Chrzanowska KH, (2008) Mystery of DNA repair: the role of the MRN complex and ATM kinase in DNA damage repair. Journal of applied genetics 49: 383-396.
27. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, et al. (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514.
28. Gillespie KA, Mehta KP, Laimins LA, Moody CA, (2012) Human papillomaviruses recruit cellular DNA repair and homologous recombination factors to viral replication centers. Journal of virology 86: 9520-9526.
29. Chenoweth DM, Dervan PB, (2009) Allosteric modulation of DNA by small molecules. Proceedings of the National Academy of Sciences of the United States of America 106: 13175-13179.
30. Chenoweth DM, Dervan PB, (2010) Structural basis for cyclic Py-Im polyamide allosteric inhibition of nuclear receptor binding. Journal of the American Chemical Society 132: 14521-14529.
31. Wang Y, Ma N, Chen G, (2012) Allosteric analysis of glucocorticoid receptor-DNA interface induced by cyclic Py-Im polyamide: a molecular dynamics simulation study. PloS one 7: e35159.
32. Hunt RA, Munde M, Kumar A, Ismail MA, Farahat AA, et al. (2011) Induced topological changes in DNA complexes: influence of DNA sequences and small molecule structures. Nucleic acids research 39: 4265-4274.
33. Garner-Hamrick PA, Fisher C, (2002) HPV episomal copy number closely correlates with cell size in keratinocyte monolayer cultures. Virology 301: 334-341.
34. Dupre A, Boyer-Chatenet L, Sattler RM, Modi AP, Lee JH, et al. (2008) A forward chemical genetic screen reveals an inhibitor of the Mre11-Rad50-Nbs1 complex. Nature chemical biology 4: 119-125.
35. Baird EED, Dervan PB, (1996) Solid Phase Synthesis of Polyamides Containing Imidazole and Pyrrole Amino Acids. J Am Chem Soc 118: 6141-6146.
36. Walker WL, Landaw EM, Dickerson RE, Goodsell DS, (1997) Estimation of the DNA sequence discriminatory ability of hairpin-linked lexitropsins. Proc Natl Acad Sci (USA) 94: 5634-5639.
37. Sambrook J, Green MR (2012) Molecular Cloning. A Laboratory Manual: Cold Spring Harbor Laboratory Press.
38. Zhang JH, Chung TD, Oldenburg KR, (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. Journal of biomolecular screening 4: 67-73.
39. Synold TW, Xi B, Wu J, Yen Y, Li BC, et al. (2012) Single-dose pharmacokinetic and toxicity analysis of pyrrole-imidazole polyamides in mice. Cancer chemotherapy and pharmacology 70: 617-625.
40. Nickols NG, Szablowski JO, Hargrove AE, Li BC, Raskatov JA, et al. (2013) Activity of a py-im polyamide targeted to the estrogen response element. Molecular cancer therapeutics 12: 675-684.
41. Dickinson LA, Burnett R, Melander C, Edelson BS, Arora PS, et al. (2004) Arresting cancer proliferation by small-molecule gene regulation. Chemistry & biology 11: 1583-1594.
42. Wang S, Nanjunda R, Aston K, Bashkin JK, Wilson WD, (2012) Correlation of local effects of DNA sequence and position of beta-alanine inserts with polyamide-DNA complex binding affinities and kinetics. Biochemistry 51: 9796-9806.
43. Stracker TH, Petrini JH, (2011) The MRE11 complex: starting from the ends. Nature reviews Molecular cell biology 12: 90-103.
44. Kastan MB, (2008) DNA damage responses: mechanisms and roles in human disease: 2007 G.H.A. Clowes Memorial Award Lecture. Molecular cancer research: MCR 6: 517-524.
45. Xu M, Bai L, Gong Y, Xie W, Hang H, et al. (2009) Structure and functional implications of the human rad9-hus1-rad1 cell cycle checkpoint complex. The Journal of biological chemistry 284: 20457-20461.
46. Querol-Audi J, Yan C, Xu X, Tsutakawa SE, Tsai MS, et al. (2012) Repair complexes of FEN1 endonuclease, DNA, and Rad9-Hus1-Rad1 are distinguished from their PCNA counterparts by functionally important stability. Proceedings of the National Academy of Sciences of the United States of America 109: 8528-8533.
47. Gembka A, Toueille M, Smirnova E, Poltz R, Ferrari E, et al. (2007) The checkpoint clamp, Rad9-Rad1-Hus1 complex, preferentially stimulates the activity of apurinic/apyrimidinic endonuclease 1 and DNA polymerase beta in long patch base excision repair. Nucleic acids research 35: 2596-2608.
48. Guan X, Bai H, Shi G, Theriot CA, Hazra TK, et al. (2007) The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates NEIL1 glycosylase. Nucleic acids research 35: 2463-2472.
49. Balakrishnan L, Brandt PD, Lindsey-Boltz LA, Sancar A, Bambara RA, (2009) Long patch base excision repair proceeds via coordinated stimulation of the multienzyme DNA repair complex. The Journal of biological chemistry 284: 15158-15172.
50. Hoffmann R, Hirt B, Bechtold V, Beard P, Raj K, (2006) Different modes of human papillomavirus DNA replication during maintenance. Journal of virology 80: 4431-4439.
51. Spangle JM, Munger K, (2010) The human papillomavirus type 16 E6 oncoprotein activates mTORC1 signaling and increases protein synthesis. Journal of virology 84: 9398-9407.
52. Lu Z, Hu X, Li Y, Zheng L, Zhou Y, et al. (2004) Human papillomavirus 16 E6 oncoprotein interferences with insulin signaling pathway by binding to tuberin. The Journal of biological chemistry 279: 35664-35670.
53. 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.
54. Cortes Ledesma F, El Khamisy SF, Zuma MC, Osborn K, Caldecott KW, (2009) A human 5'-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature 461: 674-678.
55. Pouliot JJ, Yao KC, Robertson CA, Nash HA, (1999) Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 286: 552-555.
56. Nitiss JL, Nitiss KC, (2013) Tdp2: a means to fixing the ends. PLoS genetics 9: e1003370.