The nuclear DNA sensor IFI16 acts as a restriction factor for human papillomavirus replication through epigenetic modifications of the viral promoters

Journal of Virology

Volumn 89, Issue 15, 2015, Pages 7506-7520

  Cigno, Irene Lo ^a   de Andrea, Marco ^a,b   Borgogna, Cinzia ^a   Albertini, Silvia ^a   Landini, Manuela M ^a,b   Peretti, Alberto ^a   Johnson, Karen E ^c   Chandran, Bala ^c   Landolfo, Santo ^b   Gariglio, Marisa ^a  

^a Amedeo Avogadro University   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CELL NUCLEUS DNA; CHEMOKINE; INTERFERON INDUCIBLE PROTEIN IFI16; MINICIRCLE DNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS DNA; IFI16 PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHOPROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; BIOLOGICAL MODEL; CELL DIFFERENTIATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DETERMINATION; DNA MODIFICATION; DNA REPLICATION; DNA RESTRICTION; DNA TRANSCRIPTION; ELECTROPORATION; EPIGENETIC REPRESSION; EPISOME; EUCHROMATIN; EXPRESSION VECTOR; GENE EXPRESSION PROFILING; GENE INTERACTION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HETEROCHROMATIN; HETEROZYGOSITY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 18; IFI16 GENE; IMMORTALIZED CELL LINE; IMMUNOSENSOR; INNATE IMMUNITY; KERATINOCYTE; NONHUMAN; PAPILLOMAVIRUS INFECTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN RNA BINDING; RESTRICTION SITE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIRUS DNA CELL DNA INTERACTION; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION; WART VIRUS; CELL NUCLEUS; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; VIROLOGY;

ADENOVIRIDAE; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 5; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 18;

CELL NUCLEUS; DOWN-REGULATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 18; HUMANS; NUCLEAR PROTEINS; PAPILLOMAVIRUS INFECTIONS; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; VIRUS REPLICATION;

EID: 84937723908     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00013-15     Document Type: Article

References (64)

1. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848-853. http://dx.doi.org/10.1038/nature02343.
2. Bieniasz PD. 2004. Intrinsic immunity: a front-line defense against viral attack. Nat Immunol 5:1109-1115. http://dx.doi.org/10.1038/ni1125.
3. Duggal NK, Emerman M. 2012. Evolutionary conflicts between viruses and restriction factors shape immunity. Nat Rev Immunol 12:687-695. http://dx.doi.org/10.1038/nri3295.
4. Yan N, Chen ZJ. 2012. Intrinsic antiviral immunity. Nat Immunol 13: 214-222. http://dx.doi.org/10.1038/ni.2229.
5. Takeuchi H, Matano T. 2008. Host factors involved in resistance to retroviral infection. Microbiol Immunol 52:318-325. http://dx.doi.org/10.1111/j.1348-0421.2008.00040.x.
6. Tavalai N, Stamminger T. 2011. Intrinsic cellular defense mechanisms targeting human cytomegalovirus. Virus Res 157:128-133. http://dx.doi.org/10.1016/j.virusres.2010.10.002.
7. 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.
8. Adler M, Tavalai N, Müller R, Stamminger T. 2011. Human cytomegalovirus immediate-early gene expression is restricted by the nuclear domain 10 component Sp100. J Gen Virol 92:1532-1538. http://dx.doi.org/10.1099/vir.0.030981-0.
9. Unterholzner L, Bowie AG. 2011. Innate DNA sensing moves to the nucleus. Cell Host Microbe 9:351-353. http://dx.doi.org/10.1016/j.chom.2011.05.001.
10. Neil SJD, Zang T, Bieniasz PD. 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425-430. http://dx.doi.org/10.1038/nature06553.
11. Tokarev A, Skasko M, Fitzpatrick K, Guatelli J. 2009. Antiviral activity of the interferon-induced cellular protein BST-2/tetherin. AIDS Res Hum Retroviruses 25:1197-1210. http://dx.doi.org/10.1089/aid.2009.0253.
12. Sadler AJ, Williams BRG. 2008. Interferon-inducible antiviral effectors. Nat Rev Immunol 8:559-568. http://dx.doi.org/10.1038/nri2314.
13. Fensterl V, Sen GC. 2009. Interferons and viral infections. BioFactors 35:14-20. http://dx.doi.org/10.1002/biof.6.
14. Brennan K, Bowie AG. 2010. Activation of host pattern recognition receptors by viruses. Curr Opin Microbiol 13:503-507. http://dx.doi.org/10.1016/j.mib.2010.05.007.
15. Gariglio M, Mondini M, De Andrea M, Landolfo S. 2011. The multifaceted interferon-inducible p200 family proteins: from cell biology to human pathology. J Interferon Cytokine Res 31:159-172. http://dx.doi.org/10.1089/jir.2010.0106.
16. Ludlow LEA, Johnstone RW, Clarke CJP. 2005. The HIN-200 family: more than interferon-inducible genes?. Exp Cell Res 308:1-17. http://dx.doi.org/10.1016/j.yexcr.2005.03.032.
17. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, Sirois CM, Jin T, Latz E, Xiao TS, Fitzgerald KA, Paludan SR, Bowie AG. 2010. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol 11:997-1004. http://dx.doi.org/10.1038/ni.1932.
18. Kerur N, Veettil MV, Sharma-Walia N, Bottero V, Sadagopan S, Otageri P, Chandran B. 2011. IFI16 acts as a nuclear pathogen sensor to induce the inflammasome in response to Kaposi sarcoma-associated herpesvirus infection. Cell Host Microbe 9:363-375. http://dx.doi.org/10.1016/j.chom.2011.04.008.
19. Veeranki S, Choubey D. 2012. Interferon-inducible p200-family protein IFI16, an innate immune sensor for cytosolic and nuclear double-stranded DNA: regulation of subcellular localization. Mol Immunol 49:567-571. http://dx.doi.org/10.1016/j.molimm.2011.11.004.
20. Li T, Chen J, Cristea IM. 2013. Human cytomegalovirus tegument protein pUL83 inhibits IFI16-mediated DNA sensing for immune evasion. Cell Host Microbe 14:591-599. http://dx.doi.org/10.1016/j.chom.2013.10.007.
21. Thompson MR, Sharma S, Atianand M, Jensen SB, Carpenter S, Knipe DM, Fitzgerald KA, Kurt-Jones EA. 2014. Interferon gamma inducible protein (IFI)16 transcriptionally regulates type I interferons and other interferon stimulated genes and controls the interferon response to both DNA and RNA viruses. J Biol Chem 289:23568-23581. http://dx.doi.org/10.1074/jbc.M114.554147.
22. Goubau D, Rehwinkel J, Reise Sousa C. 2010. PYHIN proteins: center stage in DNA sensing. Nat Immunol 11:984-986. http://dx.doi.org/10.1038/ni1110-984.
23. Costa S, Borgogna C, Mondini M, De Andrea M, Meroni PL, Berti E, Gariglio M, Landolfo S. 2011. Redistribution of the nuclear protein IFI16 into the cytoplasm of ultraviolet B-exposed keratinocytes as a mechanism of autoantigen processing. Br J Dermatol 164:282-290. http://dx.doi.org/10.1111/j.1365-2133.2010.10097.x.
24. Dell'Oste V, Gatti D, Gugliesi F, De Andrea M, Bawadekar M, Lo Cigno I, Biolatti M, Vallino M, Marschall M, Gariglio M, Landolfo S. 2014. Innate nuclear sensor IFI16 translocates into the cytoplasm during the early stage of in vitro human cytomegalovirus infection and is entrapped in the egressing virions during the late stage. J Virol 88:6970-6982. http://dx.doi.org/10.1128/JVI.00384-14.
25. Shaw N, Liu Z-J. 2014. Role of the HIN domain in regulation of innate immune responses. Mol Cell Biol 34:2-15. http://dx.doi.org/10.1128/MCB.00857-13.
26. Singh VV, Kerur N, Bottero V, Dutta S, Chakraborty S, Ansari MA, Paudel N, Chikoti L, Chandran B. 2013. Kaposi's sarcoma-associated herpesvirus latency in endothelial and B cells activates gamma interferoninducible protein 16-mediated inflammasomes. J Virol 87:4417-4431. http://dx.doi.org/10.1128/JVI.03282-12.
27. Ansari MA, Singh VV, Dutta S, Veettil MV, Dutta D, Chikoti L, Lu J, Everly D, Chandran B. 2013. Constitutive interferon-inducible protein 16-inflammasome activation during Epstein-Barr virus latency I, II, and III in B and epithelial cells. J Virol 87:8606-8623. http://dx.doi.org/10.1128/JVI.00805-13.
28. Morrone SR, Wang T, Constantoulakis LM, Hooy RM, Delannoy MJ, Sohn J. 2014. Cooperative assembly of IFI16 filaments on dsDNA provides insights into host defense strategy. Proc Natl Acad Sci USA 111: E62-E71. http://dx.doi.org/10.1073/pnas.1313577111.
29. Orzalli MH, DeLuca NA, Knipe DM. 2012. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci USA 109:E3008-E3017. http://dx.doi.org/10.1073/pnas.1211302109.
30. Jakobsen MR, Bak RO, Andersen A, Berg RK, Jensen SB, Tengchuan J, Laustsen A, Hansen K, Ostergaard L, Fitzgerald KA, Xiao TS, Mikkelsen JG, Mogensen TH, Paludan SR. 2013. IFI16 senses DNA forms of the lentiviral replication cycle and controls HIV-1 replication. Proc Natl Acad Sci USA 110:E4571-E4580. http://dx.doi.org/10.1073/pnas.1311669110.
31. Connolly DJ, Bowie AG. 2014. The emerging role of human PYHIN proteins in innate immunity: implications for health and disease. Biochem Pharmacol 92:405-414. http://dx.doi.org/10.1016/j.bcp.2014.08.031.
32. Gariano GR, Dell'Oste V, Bronzini M, Gatti D, Luganini A, De Andrea M, Gribaudo G, Gariglio M, Landolfo S. 2012. The intracellular DNA sensor IFI16 gene acts as restriction factor for human cytomegalovirus replication. PLoS Pathog 8:e1002498. http://dx.doi.org/10.1371/journal.ppat.1002498.
33. Johnson KE, Bottero V, Flaherty S, Dutta S, Singh VV, Chandran B. 2014. IFI16 restricts HSV-1 replication by accumulating on the HSV-1 genome, repressing HSV-1 gene expression, and directly or indirectly modulating histone modifications. PLoS Pathog 10:e1004503. http://dx.doi.org/10.1371/journal.ppat.1004503.
34. Maglennon GA, Doorbar J. 2012. The biology of papillomavirus latency. Open Virol J 6:190-197. http://dx.doi.org/10.2174/1874357901206010190.
35. Quint KD, Genders RE, de Koning MNC, Borgogna C, Gariglio M, Bouwes Bavinck JN, Doorbar J, Feltkamp MC. 2015. Human betapapillomavirus infection and keratinocyte carcinomas. J Pathol 235:342-354. http://dx.doi.org/10.1002/path.4425.
36. Gariglio M, Azzimonti B, Pagano M, Palestro G, De Andrea M, Valente G, Voglino G, Navino L, Landolfo S. 2002. Immunohistochemical expression analysis of the human interferon-inducible gene IFI16, a member of the HIN200 family, not restricted to hematopoietic cells. J Interferon Cytokine Res 22:815-821. http://dx.doi.org/10.1089/107999002320271413.
37. Geimanen J, Isok-Paas H, Pipitch R, Salk K, Laos T, Orav M, Reinson T, Ustav M, Ustav E. 2011. Development of a cellular assay system to study the genome replication of high-and low-risk mucosal and cutaneous human papillomaviruses. J Virol 85:3315-3329. http://dx.doi.org/10.1128/JVI.01985-10.
38. Isaacson Wechsler E, Wang Q, Roberts I, Pagliarulo E, Jackson D, Untersperger C, Coleman N, Griffin H, Doorbar J. 2012. Reconstruction of human papillomavirus type 16-mediated early-stage neoplasia implicates E6/E7 deregulation and the loss of contact inhibition in neoplastic progression. J Virol 86:6358-6364. http://dx.doi.org/10.1128/JVI.07069-11.
39. Wilson R, Laimins LA. 2005. Differentiation of HPV-containing cells using organotypic "raft" culture or methylcellulose. Methods Mol Med 119:157-169. http://dx.doi.org/10.1385/1-59259-982-6157.
40. Reinson T, Toots M, Kadaja M, Pipitch R, Allik M, Ustav E, Ustav M. 2013. Engagement of the ATR-dependent DNA damage response at the human papillomavirus 18 replication centers during the initial amplification. J Virol 87:951-964. http://dx.doi.org/10.1128/JVI.01943-12.
41. Baggetta R, De Andrea M, Gariano GR, Mondini M, Rittà M, Caposio P, Giovarelli M, Gariglio M, Landolfo S. 2010. The interferon-inducible gene IFI16 secretome of endothelial cells drives the early steps of the inflammatory response. Eur J Immunol 40:2182-2189. http://dx.doi.org/10.1002/eji.200939995.
42. Schweiger M-R, Ottinger M, You J, Howley PM. 2007. Brd4-independent transcriptional repression function of the papillomavirus e2 proteins. J Virol 81:9612-9622. http://dx.doi.org/10.1128/JVI.00447-07.
43. Hoppe-Seyler F, Butz K. 1992. Activation of human papillomavirus type 18 E6-E7 oncogene expression by transcription factor Sp1. Nucleic Acids Res 20:6701-6706. http://dx.doi.org/10.1093/nar/20.24.6701.
44. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. 2013. RNA-guided human genome engineering via Cas9. Science 339:823-826. http://dx.doi.org/10.1126/science.1232033.
45. Gugliesi F, Mondini M, Ravera R, Robotti A, De Andrea M, Gribaudo G, Gariglio M, Landolfo S. 2005. Up-regulation of the interferoninducible IFI16 gene by oxidative stress triggers p53 transcriptional activity in endothelial cells. J Leukoc Biol 77:820-829. http://dx.doi.org/10.1189/jlb.0904507.
46. Caposio P, Gugliesi F, Zannetti C, Sponza S, Mondini M, Medico E, Hiscott J, Young HA, Gribaudo G, Gariglio M, Landolfo S. 2007. A novel role of the interferon-inducible protein IFI16 as inducer of proinflammatory molecules in endothelial cells. J Biol Chem 282:33515-33529. http://dx.doi.org/10.1074/jbc.M701846200.
47. Stewart WE, II, Lin LS, Wiranowska-Stewart M, Cantell K. 1977. Elimination of size and charge heterogeneities of human leukocyte interferons by chemical cleavage. Proc Natl Acad Sci USA 74:4200-4204. http://dx.doi.org/10.1073/pnas.74.10.4200.
48. Orav M, Henno L, Isok-Paas H, Geimanen J, Ustav M, Ustav E. 2013. Recombination-dependent oligomerization of human papillomavirus genomes upon transientDNAreplication. J Virol 87:12051-12068. http://dx.doi.org/10.1128/JVI.01798-13.
49. Rösl F, Westphal EM, Zur Hausen H. 1989. Chromatin structure and transcriptional regulation of human papillomavirus type 18DNAin HeLa cells. Mol Carcinog 2:72-80. http://dx.doi.org/10.1002/mc.2940020205.
50. Meissner JD. 1999. Nucleotide sequences and further characterization of human papillomavirus DNA present in the CaSki, SiHa and HeLa cervical carcinoma cell lines. J Gen Virol 80:1725-1733.
51. Kang HJ, Lee MH, Kang HL, Kim SH, Ahn JR, Na H, Na TY, Kim YN, Seong JK, Lee MO. 2014. Differential regulation of estrogen receptor α expression in breast cancer cells by metastasis-associated protein 1. Cancer Res 74:1484-1494. http://dx.doi.org/10.1158/0008-5472.CAN-13-2020.
52. Rose B, Steger G, Dong XP, Thompson C, Cossart Y, Tattersall M, Pfister H. 1998. Point mutations in SP1 motifs in the upstream regulatory region of human papillomavirus type 18 isolates from cervical cancers increase promoter activity. J Gen Virol 79:1659-1663.
53. Cosma MP. 2002. Ordered recruitment: gene-specific mechanism of transcription activation. Mol Cell 10:227-236. http://dx.doi.org/10.1016/S1097-2765(02)00604-4.
54. Narlikar GJ, Fan H-Y, Kingston RE. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475-487. http://dx.doi.org/10.1016/S0092-8674(02)00654-2.
55. Wooldridge TR, Laimins LA. 2008. Regulation of human papillomavirus type 31 gene expression during the differentiation-dependent life cycle through histone modifications and transcription factor binding. Virology 374:371-380. http://dx.doi.org/10.1016/j.virol.2007.12.011.
56. Wang X, Meyers C, Wang H-K, Chow LT, Zheng Z-M. 2011. Construction of a full transcription map of human papillomavirus type 18 during productive viral infection. J Virol 85:8080-8092. http://dx.doi.org/10.1128/JVI.00670-11.
57. Sankovski E, Männik A, Geimanen J, Ustav E, Ustav M. 2014. Mapping of betapapillomavirus human papillomavirus 5 transcription and characterization of viral-genome replication function. J Virol 88:961-973. http://dx.doi.org/10.1128/JVI.01841-13.
58. Jakobsen MR, Paludan SR. 2014. IFI16: at the interphase between innate DNA sensing and genome regulation. Cytokine Growth Factor Rev 25: 649-655. http://dx.doi.org/10.1016/j.cytogfr.2014.06.004.
59. Orzalli MH, Conwell SE, Berrios C, DeCaprio JA, Knipe DM. 2013. Nuclear interferon-inducible protein 16 promotes silencing of herpesviral and transfected DNA. Proc Natl Acad Sci USA 110:E4492-E4501. http://dx.doi.org/10.1073/pnas.1316194110.
60. You J. 2010. Papillomavirus interaction with cellular chromatin. Biochim Biophys Acta 1799:192-199. http://dx.doi.org/10.1016/j.bbagrm.2009.09.009.
61. Johannsen E, Lambert PF. 2013. Epigenetics of human papillomaviruses. Virology 445:205-212. http://dx.doi.org/10.1016/j.virol.2013.07.016.
62. Brázda V, Coufal J, Liao JCC, Arrowsmith CH. 2012. Preferential binding of IFI16 protein to cruciform structure and superhelical DNA. Biochem Biophys Res Commun 422:716-720. http://dx.doi.org/10.1016/j.bbrc.2012.05.065.
63. Liao JC, Lam R, Brazda V, Duan S, Ravichandran M, Ma J, Xiao T, Tempel W, Zuo X, Wang YX, Chirgadze NY, Arrowsmith CH. 2011. Interferon-inducible protein 16: insight into the interaction with tumor suppressor p53. Structure 19:418-429. http://dx.doi.org/10.1016/j.str.2010.12.015.
64. 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.