Targeting human papillomavirus genome replication for antiviral drug discovery

Antiviral Therapy

Volumn 18, Issue 3, 2013, Pages 271-283

  Archambault, Jacques ^a,b   Melendy, Thomas ^c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; DNA DIRECTED DNA POLYMERASE ALPHA; DNA POLYMERASE; DNA PRIMASE; DNA TOPOISOMERASE; GLYCOPROTEIN E1; IMIQUIMOD; PROTEIN A; PROTEIN E6; PROTEIN E7; WART VIRUS VACCINE;

APPLICATION SITE IRRITATION; CELL CYCLE ARREST; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; DRUG RESEARCH; GENE DOSAGE; GENE OVEREXPRESSION; GENE TARGETING; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOMODULATION; NONHUMAN; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PRIORITY JOURNAL; PROPHYLAXIS; PROTEIN PROTEIN INTERACTION; REVIEW; TREATMENT INDICATION; UTERINE CERVIX CANCER; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; VIRUS INHIBITION;

ANTIVIRAL AGENTS; DNA DAMAGE; DNA REPLICATION; DRUG DISCOVERY; GENOME, VIRAL; HUMANS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PREMEDICATION; VIRUS REPLICATION;

EID: 84878033793     PISSN: 13596535     EISSN: 20402058     Source Type: Journal    
DOI: 10.3851/IMP2612     Document Type: Review

References (115)

1. Yanofsky VR, Patel RV, Goldenberg G. Genital warts: a comprehensive review. J Clin Aesthet Dermatol 2012; 5:25-36.
2. Stanley MA. Genital human papillomavirus infections: current and prospective therapies. J Gen Virol 2012; 93:681-691.
3. Wang XI, Thomas J, Zhang S. Changing trends in human papillomavirus- associated head and neck squamous cell carcinoma. Ann Diagn Pathol 2012; 16:7-12.
4. Crow JM. HPV: The global burden. Nature 2012; 488:S2-S3.
5. Rampias T, Sasaki C, Weinberger P, Psyrri A. E6 and E7 gene silencing and transformed phenotype of human papillomavirus 16-positive oropharyngeal cancer cells. J Natl Cancer Inst 2009; 101:412-423.
6. 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; 79:6732-6740. (Pubitemid 40677304)
7. Wilson R, Ryan GB, Knight GL, Laimins LA, Roberts S. The full-length E1E4 protein of human papillomavirus type 18 modulates differentiation-dependent viral DNA amplification and late gene expression. Virology 2007; 362:453-460. (Pubitemid 46678156)
8. 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; 68:6432-6445. (Pubitemid 24294893)
9. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR, Schiller JT. Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2006; 2:e69.
10. Marais D, Gawarecki D, Allan B, et al. The effectiveness of Carraguard, a vaginal microbicide, in protecting women against high-risk human papillomavirus infection. Antivir Ther 2011; 16:1219-1226.
11. Roberts JN, Buck CB, Thompson CD, et al. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 2007; 13:857-861. (Pubitemid 47038188)
12. Clinical Trials Database. A study of V503 in preadolescents and adolescents. (Updated 2 May 2012. Accessed 4 October 2012.) Available from http://clinicaltrials.gov/ct2/show/NCT00943722?term=NCT00943722&rank=1
13. Alphs HH, Gambhira R, Karanam B, et al. Protection against heterologous human papillomavirus challenge by a synthetic lipopeptide vaccine containing a broadly cross-neutralizing epitope of L2. Proc Natl Acad Sci U S A 2008; 105:5850-5855. (Pubitemid 351758461)
14. Gambhira R, Karanam B, Jagu S, et al. A protective and broadly cross-neutralizing epitope of human papillomavirus L2. J Virol 2007; 81:13927-13931. (Pubitemid 350247886)
15. Jagu S, Karanam B, Gambhira R, et al. Concatenated multitype L2 fusion proteins as candidate prophylactic panhuman papillomavirus vaccines. J Natl Cancer Inst 2009; 101:782-792.
16. Pastrana DV, Gambhira R, Buck CB, et al. Cross-neutralization of cutaneous and mucosal Papillomavirus types with anti-sera to the amino terminus of L2. Virology 2005; 337:365-372. (Pubitemid 40803480)
17. Roden RB, Yutzy WHt, Fallon R, Inglis S, Lowy DR, Schiller JT. Minor capsid protein of human genital papillomaviruses contains subdominant, cross-neutralizing epitopes. Virology 2000; 270:254-257. (Pubitemid 30333671)
18. Campo MS, Roden RB. Papillomavirus prophylactic vaccines: established successes, new approaches. J Virol 2010; 84:1214-1220.
19. Frazer IH, Leggatt GR, Mattarollo SR. Prevention and treatment of papillomavirus-related cancers through immunization. Annu Rev Immunol 2011; 29:111-138.
20. Gersch ED, Gissmann L, Garcea RL. New approaches to prophylactic human papillomavirus vaccines for cervical cancer prevention. Antivir Ther 2012; 17:425-434.
21. Schiller JT, Lowy DR. Understanding and learning from the success of prophylactic human papillomavirus vaccines. Nat Rev Microbiol 2012; 10:681-692.
22. Stanley M. Prospects for new human papillomavirus vaccines. Curr Opin Infect Dis 2010; 23:70-75.
23. Nieto K, Gissmann L, Schadlich L. Human papillomavirus-specific immune therapy: failure and hope. Antivir Ther 2010; 15:951-957.
24. van der Burg SH, Melief CJ. Therapeutic vaccination against human papilloma virus induced malignancies. Curr Opin Immunol 2011; 23:252-257.
25. Novak N, Yu CF, Bieber T, Allam JP. Toll-like receptor 7 agonists and skin. Drug News Perspect 2008; 21:158-165. (Pubitemid 351809139)
26. Hoy SM. Polyphenon E 10% ointment: in immunocompetent adults with external genital and perianal warts. Am J Clin Dermatol 2012; 13:275-281.
27. Hashimoto C, Tanaka T, Narumi T, Nomura W, Tamamura H. The successes and failures of HIV drug discovery. Expert Opin Drug Discov 2011; 6:1067-1090.
28. Hsieh HP, Hsu JT. Strategies of development of antiviral agents directed against influenza virus replication. Curr Pharm Des 2007; 13:3531-3542. (Pubitemid 350238942)
29. Butz K, Ristriani T, Hengstermann A, Denk C, Scheffner M, Hoppe-Seyler F. siRNA targeting of the viral E6 oncogene efficiently kills human papillomavirus-positive cancer cells. Oncogene 2003; 22:5938-5945. (Pubitemid 37175872)
30. Hall AH, Alexander KA. RNA interference of human papillomavirus type 18 E6 and E7 induces senescence in HeLa cells. J Virol 2003; 77:6066-6069. (Pubitemid 36538997)
31. Kadaja M, Silla T, Ustav E, Ustav M. Papillomavirus DNA replication - from initiation to genomic instability. Virology 2009; 384:360-368.
32. Kadaja M, Sumerina A, Verst T, Ojarand M, Ustav E, Ustav M. Genomic instability of the host cell induced by the human papillomavirus replication machinery. EMBO J 2007; 26:2180-2191. (Pubitemid 46625800)
33. King LE, Fisk JC, Dornan ES, Donaldson MM, Melendy T, Morgan IM. Human papillomavirus E1 and E2 mediated DNA replication is not arrested by DNA damage signalling. Virology 2010; 406:95-102.
34. Baleja JD, Cherry JJ, Liu Z, et al. Identification of inhibitors to papillomavirus type 16 E6 protein based on three-dimensional structures of interacting proteins. Antiviral Res 2006; 72:49-59. (Pubitemid 44291470)
35. Green KL, Brown C, Roeder GE, Southgate TD, Gaston K. A cancer cell-specific inducer of apoptosis. Hum Gene Ther 2007; 18:547-561. (Pubitemid 47036048)
36. Hwang ES, Naeger LK, DiMaio D. Activation of the endogenous p53 growth inhibitory pathway in HeLa cervical carcinoma cells by expression of the bovine papillomavirus E2 gene. Oncogene 1996; 12:795-803. (Pubitemid 26072266)
37. D'Abramo CM, Archambault J. Small molecule inhibitors of human papillomavirus protein - protein interactions. Open Virol J 2011; 5:80-95.
38. Stenlund A. Initiation of DNA replication: lessons from viral initiator proteins. Nat Rev Mol Cell Biol 2003; 4:777-785. (Pubitemid 37229374)
39. Clower RV, Fisk JC, Melendy T. Papillomavirus E1 protein binds to and stimulates human topoisomerase I. J Virol 2006; 80:1584-1587. (Pubitemid 43134113)
40. Simmons DT, Trowbridge PW, Roy R. Topoisomerase I stimulates SV40 T antigen-mediated DNA replication and inhibits T antigen's ability to unwind DNA at nonorigin sites. Virology 1998; 242:435-443. (Pubitemid 28414749)
41. Trowbridge PW, Roy R, Simmons DT. Human topoisomerase I promotes initiation of simian virus 40 DNA replication in vitro. Mol Cell Biol 1999; 19:1686-1694. (Pubitemid 29098227)
42. Hu Y, Clower RV, Melendy T. Cellular topoisomerase I modulates origin binding by bovine papillomavirus type 1 E1. J Virol 2006; 80:4363-4371.
43. Khopde S, Simmons DT. Simian virus 40 DNA replication is dependent on an interaction between topoisomerase I and the C-terminal end of T antigen. J Virol 2008; 82:1136-1145.
44. Amin AA, Titolo S, Pelletier A, Fink D, Cordingley MG, Archambault J. Identification of domains of the HPV11 E1 protein required for DNA replication in vitro. Virology 2000; 272:137-150. (Pubitemid 30429437)
45. Bonne-Andrea C, Santucci S, Clertant P, Tillier F. Bovine papillomavirus E1 protein binds specifically DNA polymerase alpha but not replication protein A. J Virol 1995; 69:2341-2350.
46. 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; 274:2696-2705. (Pubitemid 29075349)
47. Masterson PJ, Stanley MA, Lewis AP, Romanos MA. A C-terminal helicase domain of the human papillomavirus E1 protein binds E2 and the DNA polymerase alpha-primase p68 subunit. J Virol 1998; 72:7407-7419. (Pubitemid 28377872)
48. Park P, Copeland W, Yang L, Wang T, Botchan MR, Mohr IJ. The cellular DNA polymerase alpha-primase is required for papillomavirus DNA replication and associates with the viral E1 helicase. Proc Natl Acad Sci U S A 1994; 91:8700-8704. (Pubitemid 24273732)
49. Collins KL, Kelly TJ. Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase. Mol Cell Biol 1991; 11:2108-2115. (Pubitemid 21895582)
50. Zhou B, Arnett DR, Yu X, et al. Structural basis for the interaction of a hexameric replicative helicase with the regulatory subunit of human DNA polymerase alpha-primase. J Biol Chem 2012; 287:26854-26866.
51. 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; 73:4899-4907. (Pubitemid 29246750)
52. Loo YM, Melendy T. Recruitment of replication protein A by the papillomavirus E1 protein and modulation by single-stranded DNA. J Virol 2004; 78:1605-1615. (Pubitemid 38176693)
53. Jiang X, Klimovich V, Arunkumar AI, et al. Structural mechanism of RPA loading on DNA during activation of a simple pre-replication complex. EMBO J 2006; 25: 5516-5526. (Pubitemid 44847192)
54. Melendy T, Stillman B. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J Biol Chem 1993; 268:3389-3395. (Pubitemid 23070973)
55. Schneider C, Weisshart K, Guarino LA, Dornreiter I, Fanning E. Species-specific functional interactions of DNA polymerase alpha-primase with simian virus 40 (SV40) T antigen require SV40 origin DNA. Mol Cell Biol 1994; 14:3176-3185. (Pubitemid 24132731)
56. Tsurimoto T, Melendy T, Stillman B. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin. Nature 1990; 346:534-539.
57. Waga S, Stillman B. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature 1994; 369:207-212. (Pubitemid 24154796)
58. Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PM, Kunkel TA. Division of labor at the eukaryotic replication fork. Mol Cell 2008; 30:137-144. (Pubitemid 351626683)
59. Zlotkin T, Kaufmann G, Jiang Y, et al. DNA polymerase epsilon may be dispensable for SV40- but not cellular-DNA replication. EMBO J 1996; 15:2298-2305.
60. Balakrishnan L, Bambara RA. Eukaryotic lagging strand DNA replication employs a multi-pathway mechanism that protects genome integrity. J Biol Chem 2011; 286:6865-6870.
61. Balakrishnan L, Gloor JW, Bambara RA. Reconstitution of eukaryotic lagging strand DNA replication. Methods 2010; 51:347-357.
62. Clower RV, Hu Y, Melendy T. Papillomavirus E2 protein interacts with and stimulates human topoisomerase I. Virology 2006; 348:13-18.
63. Li R, Botchan MR. The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell 1993; 73:1207-1221. (Pubitemid 23180494)
64. Narahari J, Fisk JC, Melendy T, Roman A. Interactions of the cellular CCAAT displacement protein and human papillomavirus E2 protein with the viral origin of replication can regulate DNA replication. Virology 2006; 350:302-311. (Pubitemid 43928103)
65. Gopalakrishnan V, Khan SA. E1 protein of human papillomavirus type 1a is sufficient for initiation of viral DNA replication. Proc Natl Acad Sci U S A 1994; 91:9597-9601. (Pubitemid 24297962)
66. Moody CA, Laimins LA. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog 2009; 5:e1000605.
67. Sakakibara N, Mitra R, McBride AA. The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J Virol 2011; 85:8981-8995.
68. Kadaja M, Isok-Paas H, Laos T, Ustav E, Ustav M. Mechanism of genomic instability in cells infected with the high-risk human papillomaviruses. PLoS Pathog 2009; 5:e1000397.
69. Fradet-Turcotte A, Bergeron-Labrecque F, Moody CA, Lehoux M, Laimins LA, Archambault J. Nuclear accumulation of the papillomavirus E1 helicase blocks S-phase progression and triggers an ATM-dependent DNA damage response. J Virol 2011; 85:8996-9012.
70. Faucher AM, White PW, Brochu C, Grand-Maitre C, Rancourt J, Fazal G. Discovery of small-molecule inhibitors of the ATPase activity of human papillomavirus E1 helicase. J Med Chem 2004; 47:18-21. (Pubitemid 38040486)
71. White PW, Faucher AM, Massariol MJ, et al. Biphenylsulfonacetic acid inhibitors of the human papillomavirus type 6 E1 helicase inhibit ATP hydrolysis by an allosteric mechanism involving tyrosine 486. Antimicrob Agents Chemother 2005; 49:4834-4842. (Pubitemid 41778892)
72. Rocque WJ, Porter DJ, Barnes JA, et al. Replication-associated activities of purified human papillomavirus type 11 E1 helicase. Protein Expr Purif 2000; 18:148-159. (Pubitemid 30172220)
73. 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; 74:7349-7361. (Pubitemid 30613080)
74. White PW, Pelletier A, Brault K, et al. Characterization of recombinant HPV6 and 11 E1 helicases: effect of ATP on the interaction of E1 with E2 and mapping of a minimal helicase domain. J Biol Chem 2001; 276:22426-22438.
75. Edwards TG, Koeller KJ, Slomczynska U, et al. HPV episome levels are potently decreased by pyrrole-imidazole polyamides. Antiviral Res 2011; 91:177-186.
76. Crute JJ, Grygon CA, Hargrave KD, et al. Herpes simplex virus helicase-primase inhibitors are active in animal models of human disease. Nat Med 2002; 8:386-391. (Pubitemid 34407034)
77. Kleymann G, Fischer R, Betz UA, et al. New helicase-primase inhibitors as drug candidates for the treatment of herpes simplex disease. Nat Med 2002; 8:392-398. (Pubitemid 34407035)
78. White PW, Titolo S, Brault K, et al. Inhibition of human papillomavirus DNA replication by small molecule antagonists of the E1-E2 protein interaction. J Biol Chem 2003; 278:26765-26772. (Pubitemid 36876824)
79. Yoakim C, Ogilvie WW, Goudreau N, et al. Discovery of the first series of inhibitors of human papillomavirus type 11: inhibition of the assembly of the E1-E2-Origin DNA complex. Bioorg Med Chem Lett 2003; 13:2539-2541. (Pubitemid 36830768)
80. Fry DC. Small-molecule inhibitors of protein-protein interactions: how to mimic a protein partner. Curr Pharm Des 2012; 18:4679-84.
81. Abbate EA, Berger JM, Botchan MR. The X-ray structure of the papillomavirus helicase in complex with its molecular matchmaker E2. Genes Dev 2004; 18:1981-1996. (Pubitemid 39071580)
82. Abroi A, Kurg R, Ustav M. Transcriptional and replicational activation functions in the bovine papillomavirus type 1 E2 protein are encoded by different structural determinants. J Virol 1996; 70:6169-6179. (Pubitemid 26266835)
83. Brokaw JL, Blanco M, McBride AA. Amino acids critical for the functions of the bovine papillomavirus type 1 E2 transactivator. J Virol 1996; 70:23-29. (Pubitemid 126508764)
84. Cooper CS, Upmeyer SN, Winokur PL. Identification of single amino acids in the human papillomavirus 11 E2 protein critical for the transactivation or replication functions. Virology 1998; 241:312-322. (Pubitemid 28384204)
85. Ferguson MK, Botchan MR. Genetic analysis of the activation domain of bovine papillomavirus protein E2: its role in transcription and replication. J Virol 1996; 70:4193-4199. (Pubitemid 26187418)
86. Grossel MJ, Sverdrup F, Breiding DE, Androphy EJ. Transcriptional activation function is not required for stimulation of DNA replication by bovine papillomavirus type 1 E2. J Virol 1996; 70:7264-7269. (Pubitemid 26307450)
87. Sakai H, Yasugi T, Benson JD, Dowhanick JJ, Howley PM. Targeted mutagenesis of the human papillomavirus type 16 E2 transactivation domain reveals separable transcriptional activation and DNA replication functions. J Virol 1996; 70:1602-1611. (Pubitemid 26062919)
88. Wang Y, Coulombe R, Cameron DR, et al. Crystal structure of the E2 transactivation domain of human papillomavirus type 11 bound to a protein interaction inhibitor. J Biol Chem 2004; 279:6976-6985. (Pubitemid 38248841)
89. Biswas S, Field HJ. Herpes simplex virus helicase-primase inhibitors: recent findings from the study of drug resistance mutations. Antivir Chem Chemother 2008; 19:1-6.
90. Biswas S, Swift M, Field HJ. High frequency of spontaneous helicase-primase inhibitor (BAY 57-1293) drug-resistant variants in certain laboratory isolates of HSV-1. Antivir Chem Chemother 2007; 18:13-23. (Pubitemid 46426934)
91. Melendy T, Sedman J, Stenlund A. Cellular factors required for papillomavirus DNA replication. J Virol 1995; 69:7857-7867.
92. Müller F, Seo YS, Hurwitz J. Replication of bovine papillomavirus type 1 origin-containing DNA in crude extracts and with purified proteins. J Biol Chem 1994; 269:17086-17094. (Pubitemid 24204027)
93. Stracker TH, Cassell GD, Ward P, et al. The Rep protein of adeno-associated virus type 2 interacts with single-stranded DNA-binding proteins that enhance viral replication. J Virol 2004; 78:441-453. (Pubitemid 37549754)
94. Brill SJ, DiNardo S, Voelkel-Meiman K, Sternglanz R. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 1987; 326:414-416. (Pubitemid 17053775)
95. Wun-Kim K, Upson R, Young W, Melendy T, Stillman B, Simmons DT. The DNA-binding domain of simian virus 40 tumor antigen has multiple functions. J Virol 1993; 67:7608-7611. (Pubitemid 23343891)
96. Lin BY, Makhov AM, Griffith JD, Broker TR, Chow LT. Chaperone proteins abrogate inhibition of the human papillomavirus (HPV) E1 replicative helicase by the HPV E2 protein. Mol Cell Biol 2002; 22:6592-6604.
97. Liu JS, Kuo SR, Makhov AM, et al. Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J Biol Chem 1998; 273:30704-30712. (Pubitemid 28545552)
98. Swindle CS, Engler JA. Association of the human papillomavirus type 11 E1 protein with histone H1. J Virol 1998; 72:1994-2001. (Pubitemid 28100753)
99. Lee D, Sohn H, Kalpana GV, Choe J. Interaction of E1 and hSNF5 proteins stimulates replication of human papillomavirus DNA. Nature 1999; 399:487-491. (Pubitemid 29258856)
100. Yasugi T, Vidal M, Sakai H, Howley PM, Benson JD. Two classes of human papillomavirus type 16 E1 mutants suggest pleiotropic conformational constraints affecting E1 multimerization, E2 interaction, and interaction with cellular proteins. J Virol 1997; 71:5942-5951. (Pubitemid 27304931)
101. Fradet-Turcotte A, Brault K, Titolo S, Howley PM, Archambault J. Characterization of papillomavirus E1 helicase mutants defective for interaction with the SUMO-conjugating enzyme Ubc9. Virology 2009; 395:190-201.
102. Rangasamy D, Wilson VG. Bovine papillomavirus E1 protein is sumoylated by the host cell Ubc9 protein. J Biol Chem 2000; 275:30487-30495.
103. Rangasamy D, Woytek K, Khan SA, Wilson VG. SUMO-1 modification of bovine papillomavirus E1 protein is required for intranuclear accumulation. J Biol Chem 2000; 275:37999-38004. (Pubitemid 32004922)
104. Yasugi T, Howley PM. Identification of the structural and functional human homolog of the yeast ubiquitin conjugating enzyme UBC9. Nucleic Acids Res 1996; 24:2005-2010. (Pubitemid 26174540)
105. Côté-Martin A, Moody C, Fradet-Turcotte A, et al. Human papillomavirus E1 helicase interacts with the WD repeat protein p80 to promote maintenance of the viral genome in keratinocytes. J Virol 2008; 82:1271-1283.
106. Lehoux M, Fradet-Turcotte A, Lussier-Price M, Omichinski JG, Archambault J. Inhibition of human papillomavirus DNA replication by an E1-derived p80/UAF1-binding peptide. J Virol 2012; 86:3486-3500.
107. Cueille N, Nougarede R, Mechali F, Philippe M, Bonne-Andrea C. Functional interaction between the bovine papillomavirus virus type 1 replicative helicase E1 and cyclin E-Cdk2. J Virol 1998; 72:7255-7262. (Pubitemid 28377855)
108. Deng W, Lin BY, Jin G, et al. Cyclin/CDK regulates the nucleocytoplasmic localization of the human papillomavirus E1 DNA helicase. J Virol 2004; 78:13954-13965. (Pubitemid 39612792)
109. Fradet-Turcotte A, Moody C, Laimins LA, Archambault J. Nuclear export of human papillomavirus type 31 E1 is regulated by Cdk2 phosphorylation and required for viral genome maintenance. J Virol 2010; 84:11747-11760.
110. Ma T, Zou N, Lin BY, Chow LT, Harper JW. Interaction between cyclin-dependent kinases and human papillomavirus replication-initiation protein E1 is required for efficient viral replication. Proc Natl Acad Sci U S A 1999; 96:382-387. (Pubitemid 29061217)
111. Saikia P, Fensterl V, Sen GC. The inhibitory action of P56 on select functions of E1 mediates interferon's effect on human papillomavirus DNA replication. J Virol 2010; 84:13036-13039.
112. Terenzi F, Saikia P, Sen GC. Interferon-inducible protein, P56, inhibits HPV DNA replication by binding to the viral protein E1. EMBO J 2008; 27:3311-3321.
113. Cohn MA, Kee Y, Haas W, Gygi SP, D'Andrea AD. UAF1 is a subunit of multiple deubiquitinating enzyme complexes. J Biol Chem 2009; 284:5343-5351.
114. Cohn MA, Kowal P, Yang K, et al. UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 2007; 28:786-797. (Pubitemid 350217060)
115. Jolly CE, Gray LJ, Parish JL, Lain S, Herrington CS. Leptomycin B induces apoptosis in cells containing the whole HPV 16 genome. Int J Oncol 2009; 35:649-656.