Interferon kappa inhibits human papillomavirus 31 transcription by inducing Sp 100 proteins

Journal of Virology

Volumn 90, Issue 2, 2016, Pages 694-704

  Habiger, Christina ^a   Jäger, Günter ^a   Walter, Michael ^a   Iftner, Thomas ^a   Stubenrauch, Frank ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CYTOKINE; DOXYCYCLINE; INTERFERON; PROTEIN; RNA; SP100 PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; AUTOANTIGEN; CELL NUCLEUS ANTIGEN; INTERFERON KAPPA; SP100 PROTEIN, HUMAN;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; EXTRACHROMOSOMAL INHERITANCE; GENE CONTROL; GENE EXPRESSION; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 31; KERATINOCYTE; NONHUMAN; PAPILLOMAVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR; RNA INTERFERENCE; RNA SEQUENCE; TRANSCRIPTION INITIATION; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSCRIPTION; EPITHELIUM CELL; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; TUMOR CELL LINE; VIROLOGY;

ANTIGENS, NUCLEAR; AUTOANTIGENS; CELL LINE, TUMOR; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 31; HUMANS; INTERFERON TYPE I; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

EID: 84954184193     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02137-15     Document Type: Article

References (56)

1. Parkin DM, Bray F. 2006. The burden of HPV-related cancers. Vaccine 24(Suppl 3):11-25.
2. Stubenrauch F, Laimins LA. 1999. Human papillomavirus life cycle: active and latent phases. Semin Cancer Biol 9:379-386. http://dx.doi.org/10.1006/scbi.1999.0141.
3. Moody CA, Laimins LA. 2010. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 10:550-560. http://dx.doi.org/10.1038/nrc2886.
4. Chang YE, Laimins LA. 2000. Microarray analysis identifies interferoninducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J Virol 74:4174-4182. http://dx.doi.org/10.1128/JVI.74.9.4174-4182.2000.
5. Karstensen B, Poppelreuther S, Bonin M, Walter M, Iftner T, Stubenrauch F. 2006. Gene expression profiles reveal an upregulation of E2F and downregulation of interferon targets by HPV18 but no changes between keratinocytes with integrated or episomal viral genomes. Virology 353: 200-209. http://dx.doi.org/10.1016/j.virol.2006.05.030.
6. Nees M, Geoghegan JM, Hyman T, Frank S, Miller L, Woodworth CD. 2001. Papillomavirus type 16 oncogenes downregulate expression of interferon-responsive genes and upregulate proliferation-associated and NF-kappaB-responsive genes in cervical keratinocytes. J Virol 75:4283-4296. http://dx.doi.org/10.1128/JVI.75.9.4283-4296.2001.
7. McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. 2015. Type I interferons in infectious disease. Nat Rev Immunol 15:87-103. http://dx.doi.org/10.1038/nri3787.
8. Schneider WM, Chevillotte MD, Rice CM. 2014. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 32:513-545. http://dx.doi.org/10.1146/annurev-immunol-032713-120231.
9. Chang YE, Pena L, Sen GC, Park JK, Laimins LA. 2002. Long-term effect of interferon on keratinocytes that maintain human papillomavirus type 31. J Virol 76:8864-8874. http://dx.doi.org/10.1128/JVI.76.17.8864-8874.2002.
10. Herdman MT, Pett MR, Roberts I, Alazawi WO, Teschendorff AE, Zhang XY, Stanley MA, Coleman N. 2006. Interferon-beta treatment of cervical keratinocytes naturally infected with human papillomavirus 16 episomes promotes rapid reduction in episome numbers and emergence of latent integrants. Carcinogenesis 27:2341-2353. http://dx.doi.org/10.1093/carcin/bgl172.
11. Hong S, Mehta KP, Laimins LA. 2011. Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiationdependent genome amplification and plasmid maintenance. J Virol 85: 9486-9494. http://dx.doi.org/10.1128/JVI.05007-11.
12. Terenzi F, Saikia P, Sen GC. 2008. Interferon-inducible protein, P56, inhibits HPV DNA replication by binding to the viral protein E1. EMBO J 27:3311-3321. http://dx.doi.org/10.1038/emboj.2008.241.
13. DeCarlo CA, Severini A, Edler L, Escott NG, Lambert PF, Ulanova M, Zehbe I. 2010. IFN-kappa, a novel type I IFN, is undetectable in HPVpositive human cervical keratinocytes. Lab Invest 90:1482-1491. http://dx.doi.org/10.1038/labinvest.2010.95.
14. LaFleur DW, Nardelli B, Tsareva T, Mather D, Feng P, Semenuk M, Taylor K, Buergin M, Chinchilla D, Roshke V, Chen G, Ruben SM, Pitha PM, Coleman TA, Moore PA. 2001. Interferon-kappa, a novel type I interferon expressed in human keratinocytes. J Biol Chem 276:39765-39771. http://dx.doi.org/10.1074/jbc.M102502200.
15. Reiser J, Hurst J, Voges M, Krauss P, Munch P, Iftner T, Stubenrauch F. 2011. High-risk human papillomaviruses repress constitutive kappa interferon transcription via E6 to prevent pathogen recognition receptor and antiviral-gene expression. J Virol 85:11372-11380. http://dx.doi.org/10.1128/JVI.05279-11.
16. Rincon-Orozco B, Halec G, Rosenberger S, Muschik D, Nindl I, Bachmann A, Ritter TM, Dondog B, Ly R, Bosch FX, Zawatzky R, Rosl F. 2009. Epigenetic silencing of interferon-kappa in human papillomavirus type 16-positive cells. Cancer Res 69:8718-8725. http://dx.doi.org/10.1158/0008-5472.CAN-09-0550.
17. Meerbrey KL, Hu G, Kessler JD, Roarty K, Li MZ, Fang JE, Herschkowitz JI, Burrows AE, Ciccia A, Sun T, Schmitt EM, Bernardi RJ, Fu X, Bland CS, Cooper TA, Schiff R, Rosen JM, Westbrook TF, Elledge SJ. 2011. The pINDUCER lentiviral toolkit for inducible RNA interference in vitro and in vivo. Proc Natl Acad Sci U S A 108:3665-3670. http://dx.doi.org/10.1073/pnas.1019736108.
18. Fertey J, Hurst J, Straub E, Schenker A, Iftner T, Stubenrauch F. 2011. Growth inhibition of HeLa cells is a conserved feature of high-risk human papillomavirus E8ê2C proteins and can also be achieved by an artificial repressor protein. J Virol 85:2918-2926. http://dx.doi.org/10.1128/JVI.01647-10.
19. Berscheminski J, Wimmer P, Brun J, Ip WH, Groitl P, Horlacher T, Jaffray E, Hay RT, Dobner T, Schreiner S. 2014. Sp100 isoform-specific regulation of human adenovirus 5 gene expression. J Virol 88:6076-6092. http://dx.doi.org/10.1128/JVI.00469-14.
20. Everett RD, Parada C, Gripon P, Sirma H, Orr A. 2008. Replication of ICP0-null mutant herpes simplex virus type 1 is restricted by both PML and Sp100. J Virol 82:2661-2672. http://dx.doi.org/10.1128/JVI.02308-07.
21. Guldner HH, Szostecki C, Schroder P, Matschl U, Jensen K, Luders C, Will H, Sternsdorf T. 1999. Splice variants of the nuclear dot-associated Sp100 protein contain homologies to HMG-1 and a human nuclear phosphoprotein-box motif. J Cell Sci 112:733-747.
22. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
23. Rozen SS, Helen J. 2000. Primer3 on theWWWfor general users and for biologist programmers, p 365-386. In Misener S, Krawetz SA (ed), Bioinformatics methods and protocols. Humana Press, Totowa, NJ.
24. Straub E, Dreer M, Fertey J, Iftner T, Stubenrauch F. 2014. The viral E8ê2C repressor limits productive replication of human papillomavirus 16. J Virol 88:937-947. http://dx.doi.org/10.1128/JVI.02296-13.
25. Straub E, Fertey J, Dreer M, Iftner T, Stubenrauch F. 2015. Characterization of the human papillomavirus type 16 E8 promoter. J Virol. 89: 7304-7313. http://dx.doi.org/10.1128/JVI.00616-15.
26. Bedell MA, Hudson JB, Golub TR, Turyk ME, Hosken M, Wilbanks GD, Laimins LA. 1991. Amplification of human papillomavirus genomes in vitro is dependent on epithelial differentiation. J Virol 65:2254-2260.
27. Frattini MG, Lim HB, Laimins LA. 1996. In vitro synthesis of oncogenic human papillomaviruses requires episomal genomes for differentiationdependent late expression. Proc Natl Acad Sci U S A 93:3062-3067. http://dx.doi.org/10.1073/pnas.93.7.3062.
28. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21. http://dx.doi.org/10.1093/bioinformatics/bts635.
29. Anders S, Pyl PT, Huber W. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166-169. http://dx.doi.org/10.1093/bioinformatics/btu638.
30. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111. http://dx.doi.org/10.1093/bioinformatics/btp120.
31. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. http://dx.doi.org/10.1093/bioinformatics/btp616.
32. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289-300.
33. Young MD, Wakefield MJ, Smyth GK, Oshlack A. 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14. http://dx.doi.org/10.1186/gb-2010-11-2-r14.
34. Dolken L, Ruzsics Z, Radle B, Friedel CC, Zimmer R, Mages J, Hoffmann R, Dickinson P, Forster T, Ghazal P, Koszinowski UH. 2008. High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 14:1959-1972. http://dx.doi.org/10.1261/rna.1136108.
35. Stubenrauch F, Hummel M, Iftner T, Laimins LA. 2000. The E8E2C protein, a negative regulator of viral transcription and replication, is required for extrachromosomal maintenance of human papillomavirus type 31 in keratinocytes. J Virol 74:1178-1186. http://dx.doi.org/10.1128/JVI.74.3.1178-1186.2000.
36. Riccardi C, Nicoletti I. 2006. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc 1:1458-1461. http://dx.doi.org/10.1038/nprot.2006.238.
37. Butz K, Ristriani T, Hengstermann A, Denk C, Scheffner M, Hoppe-Seyler F. 2003. siRNA targeting of the viral E6 oncogene efficiently kills human papillomavirus-positive cancer cells. Oncogene 22:5938-5945. http://dx.doi.org/10.1038/sj.onc.1206894.
38. Dowhanick JJ, McBride AA, Howley PM. 1995. Suppression of cellular proliferation by the papillomavirus E2 protein. J Virol 69:7791-7799.
39. Hall AH, Alexander KA. 2003. RNA interference of human papillomavirus type 18 E6 and E7 induces senescence in HeLa cells. J Virol 77:6066-6069. http://dx.doi.org/10.1128/JVI.77.10.6066-6069.2003.
40. Hwang ES, Riese DJ, II, Settleman J, Nilson LA, Honig J, Flynn S, DiMaio D. 1993. Inhibition of cervical carcinoma cell line proliferation by the introduction of a bovine papillomavirus regulatory gene. J Virol 67: 3720-3729.
41. Rusinova I, Forster S, Yu S, Kannan A, Masse M, Cumming H, Chapman R, Hertzog PJ. 2013. Interferome v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res 41:D1040-1046. http://dx.doi.org/10.1093/nar/gks1215.
42. Su ZZ, Lee SG, Emdad L, Lebdeva IV, Gupta P, Valerie K, Sarkar D, Fisher PB. 2008. Cloning and characterization of SARI (suppressor of AP-1, regulated by IFN). Proc Natl Acad Sci U S A 105:20906-20911. http://dx.doi.org/10.1073/pnas.0807975106.
43. Bernard HU. 2013. Regulatory elements in the viral genome. Virology 445:197-204. http://dx.doi.org/10.1016/j.virol.2013.04.035.
44. Glass M, Everett RD. 2013. Components of promyelocytic leukemia nuclear bodies (ND10) act cooperatively to repress herpesvirus infection. J Virol 87:2174-2185. http://dx.doi.org/10.1128/JVI.02950-12.
45. Kim YE, Lee JH, Kim ET, Shin HJ, Gu SY, Seol HS, Ling PD, Lee CH, Ahn JH. 2011. Human cytomegalovirus infection causes degradation of Sp100 proteins that suppress viral gene expression. J Virol 85:11928-11937. http://dx.doi.org/10.1128/JVI.00758-11.
46. Negorev DG, Vladimirova OV, Ivanov A, Rauscher F 3rd, Maul GG. 2006. Differential role of Sp100 isoforms in interferon-mediated repression of herpes simplex virus type 1 immediate-early protein expression. J Virol 80:8019-8029. http://dx.doi.org/10.1128/JVI.02164-05.
47. Stepp WH, Meyers JM, McBride AA. 2013. Sp100 provides intrinsic immunity against human papillomavirus infection. mBio 4:e00845-13. http://dx.doi.org/10.1128/mBio.00845-13.
48. Fung KY, Mangan NE, Cumming H, Horvat JC, Mayall JR, Stifter SA, De Weerd N, Roisman LC, Rossjohn J, Robertson SA, Schjenken JE, Parker B, Gargett CE, Nguyen HP, Carr DJ, Hansbro PM, Hertzog PJ. 2013. Interferon-epsilon protects the female reproductive tract from viral and bacterial infection. Science 339:1088-1092. http://dx.doi.org/10.1126/science.1233321.
49. Tavalai N, Stamminger T. 2008. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim Biophys Acta 1783: 2207-2221. http://dx.doi.org/10.1016/j.bbamcr.2008.08.004.
50. Becker KA, Florin L, Sapp C, Maul GG, Sapp M. 2004. Nuclear localization but not PML protein is required for incorporation of the papillomavirus minor capsid protein L2 into virus-like particles. J Virol 78:1121-1128. http://dx.doi.org/10.1128/JVI.78.3.1121-1128.2004.
51. Becker KA, Florin L, Sapp C, Sapp M. 2003. Dissection of human papillomavirus type 33 L2 domains involved in nuclear domains (ND) 10 homing and reorganization. Virology 314:161-167. http://dx.doi.org/10.1016/S0042-6822(03)00447-1.
52. Day PM, Roden RB, Lowy DR, Schiller JT. 1998. The papillomavirus minor capsid protein, L2, induces localization of the major capsid protein, L1, and the viral transcription/replication protein, E2, to PML oncogenic domains. J Virol 72:142-150.
53. Florin L, Sapp C, Streeck RE, Sapp M. 2002. Assembly and translocation of papillomavirus capsid proteins. J Virol 76:10009-10014. http://dx.doi.org/10.1128/JVI.76.19.10009-10014.2002.
54. Florin L, Schafer F, Sotlar K, Streeck RE, Sapp M. 2002. Reorganization of nuclear domain 10 induced by papillomavirus capsid protein l2. Virology 295:97-107. http://dx.doi.org/10.1006/viro.2002.1360.
55. Karanam B, Peng S, Li T, Buck C, Day PM, Roden RB. 2010. Papillomavirus infection requires gamma secretase. J Virol 84:10661-10670. http://dx.doi.org/10.1128/JVI.01081-10.
56. Day PM, Baker CC, Lowy DR, Schiller JT. 2004. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc Natl Acad Sci U S A 101:14252-14257. http://dx.doi.org/10.1073/pnas.0404229101.