The Broad-Spectrum Antiviral Protein ZAP Restricts Human Retrotransposition

PLoS Genetics

Volumn 11, Issue 5, 2015, Pages

  Goodier, John L ^a   Pereira, Gavin C ^a   Cheung, Ling E ^a   Rose, Rebecca J ^a   Kazazian, Haig H ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONIN; L1 RNA; PROTEIN MOV10; PROTEIN ZAP; RIBONUCLEOPROTEIN; RNA; RNA HELICASE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; DNA VIRUS; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; INTERFERON REGULATORY FACTOR; MOV10 PROTEIN, HUMAN; RETROPOSON; RNA BINDING PROTEIN; ZC3HAV1 PROTEIN, HUMAN;

ARTICLE; CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA VIRUS; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MOLECULAR GENETICS; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RETROPOSON; RETROVIRIDAE; RNA DEGRADATION; TILOVIRIDAE; TOGAVIRIDAE; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; MOLECULAR CLONING; MOLECULAR EVOLUTION; RNA STABILITY;

RETROVIRIDAE; SIMIAN IMMUNODEFICIENCY VIRUS; TOGAVIRIDAE;

CLONING, MOLECULAR; DNA VIRUSES; EVOLUTION, MOLECULAR; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; INTERFERON REGULATORY FACTORS; RETROELEMENTS; RNA HELICASES; RNA STABILITY; RNA-BINDING PROTEINS;

EID: 84930807844     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005252     Document Type: Article

References (137)

1. Haller O, Kochs GJ, (2011) Human MxA protein: an interferon-induced dynamin-like GTPase with broad antiviral activity. Interferon Cytokine Res 31: 79–87. Review. doi: 10.1089/jir.2010.0076 21166595
2. Lu J, Pan Q, Rong L, Liu SL, Liang C, (2011) The IFITM proteins inhibit HIV-1 infection. J Virol 85: 12881–12889. doi: 10.1128/JVI.05633-11 21976647
3. Diamond MS, Farzan M, (2013) The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 13: 46–57. doi: 10.1038/nri3344 23237964
4. Neil SJ, (2013) The antiviral activities of tetherin. Curr Top Microbiol Immunol 371: 67–104 doi: 10.1007/978-3-642-37765-5_3 23686232
5. Helbig KJ, Beard MR, (2014) The role of viperin in the innate antiviral response. J Mol Biol 426: 1210–1219. doi: 10.1016/j.jmb.2013.10.019 24157441
6. Koshiba T, (2013) Mitochondrial-mediated antiviral immunity. Biochim Biophys Acta 1833: 225–232. Review. doi: 10.1016/j.bbamcr.2012.03.005 22440325
7. Degols G, Eldin P, Mechti N, (2007) ISG20, an actor of the innate immune response. Biochimie 89: 831–835. 17445960
8. Allouch A, Di Primio C, Alpi E, Lusic M, Arosio D, Giacca M, et al. (2011) The TRIM family protein KAP1 inhibits HIV-1 integration. Cell Host Microbe 9: 484–495. doi: 10.1016/j.chom.2011.05.004 21669397
9. Katoh I, Kurata SI, (2013) Association of endogenous retroviruses and long terminal repeats with human disorders. Front Oncol 3: 234. doi: 10.3389/fonc.2013.00234 24062987
10. Alfahad T, Nath A, (2013) Retroviruses and amyotrophic lateral sclerosis. Antiviral Res 99: 180–187. doi: 10.1016/j.antiviral.2013.05.006 23707220
11. Cusick MF, Libbey JE, Fujinami RS, (2013) Multiple sclerosis: autoimmunity and viruses. Curr Opin Rheumatol 25: 496–501. doi: 10.1097/BOR.0b013e328362004d 23656710
12. Tugnet N, Rylance P, Roden D, Trela M, Nelson P, (2013) Human endogenous retroviruses (HERVs) and autoimmune rheumatic disease: is there a link? Open Rheumatol J 7: 13–21. doi: 10.2174/1874312901307010013 23750183
13. Cordaux R, Batzer MA, (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10: 691–703. doi: 10.1038/nrg2640 19763152
14. Hancks DC, Kazazian HH, Jr (2012) Active human retrotransposons: variation and disease. Curr Opin Genet Dev 22: 191–203. doi: 10.1016/j.gde.2012.02.006 22406018
15. Brouha B, Schustak J, Badge RM, Lutz-Prigge S, Farley AH, Moran JV, et al. (2003) Hot L1s account for the bulk of retrotransposition in the human population. Proc. Natl Acad. Sci. USA 100: 5280–5285. 12682288
16. Beck CR, Collier P, Macfarlane C, Malig M, Kidd JM, Eichler EE, et al. (2010) LINE-1 retrotransposition activity in human genomes. Cell 141: 1159–1170. doi: 10.1016/j.cell.2010.05.021 20602998
17. Doolittle RF, Feng DF, (1992) Tracing the origin of retroviruses. Curr Top Microbiol Immunol 176: 195–211. 1376225
18. Malik HS, Eickbush TH, (2001) Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res 11: 1187–1197. 11435400
19. Malik HS, Henikoff S, Eickbush TH, (2000) Poised for contagion: evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res 10: 1307–1318. 10984449
20. Schumann GG, (2007) APOBEC3 proteins: major players in intracellular defence against LINE-1-mediated retrotransposition. Biochem Soc Trans 35: 637–642. 17511669
21. Arias JF, Koyama T, Kinomoto M, Tokunaga K, (2012) Retroelements versus APOBEC3 family members: no great escape from the magnificent seven. Front Microbiol 3: 275. doi: 10.3389/fmicb.2012.00275 22912627
22. Richardson SR, Narvaiza I, Planegger RA, Weitzman MD, Moran JV, (2014) APOBEC3A deaminates transiently exposed single-strand DNA during LINE-1 retrotransposition. Elife 3: e02008. doi: 10.7554/eLife.02008 24843014
23. Zhao K, Du J, Han X, Goodier JL, Li P, Zhou X, et al. (2013) Modulation of LINE-1 and Alu/SVA retrotransposition by Aicardi-Goutières syndrome-related SAMHD1. Cell Reports 4: 1108–1115 doi: 10.1016/j.celrep.2013.08.019 24035396
24. Stetson DB, Ko JS, Heidmann T, Medzhitov R, (2008) Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134: 587–598. doi: 10.1016/j.cell.2008.06.032 18724932
25. Zhang A, Dong B, Doucet AJ, Moldovan JB, Moran JV, Silverman RH, (2013) RNase L restricts the mobility of engineered retrotransposons in cultured human cells. Nucleic Acids Res 42: 3803–2820. doi: 10.1093/nar/gkt1308 24371271
26. Arjan-Odedra S, Swanson CM, Sherer NM, Wolinsky SM, Malim MH, (2012) Endogenous MOV10 inhibits the retrotransposition of endogenous retroelements but not the replication of exogenous retroviruses. Retrovirology 9: 53 doi: 10.1186/1742-4690-9-53 22727223
27. Goodier JL, Cheung LE, Kazazian HH, Jr (2012) MOV10 RNA helicase is a potent inhibitor of retrotransposition in cells. PLoS Genet 8: e1002941. doi: 10.1371/journal.pgen.1002941 23093941
28. Li X, Zhang J, Jia R, Cheng V, Xu X, Qiao W, et al. (2013) The MOV10 helicase inhibits LINE-1 mobility. J Biol Chem 288: 21148–21160. doi: 10.1074/jbc.M113.465856 23754279
29. Mao R, Nie H, Cai D, Zhang J, Liu H, Yan R, et al. (2013) Inhibition of hepatitis B virus replication by the host zinc finger antiviral protein. PLoS Pathog 9: e1003494. doi: 10.1371/journal.ppat.1003494 23853601
30. Xuan Y, Gong D, Qi J, Han C, Deng H, Gao G, (2013) ZAP inhibits murine gammaherpesvirus 68 ORF64 expression and is antagonized by RTA. J Virol 87: 2735–2743. doi: 10.1128/JVI.03015-12 23255809
31. Bick MJ, Carroll JW, Gao G, Goff SP, Rice CM, MacDonald MR, (2003) Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J Virol 77: 11555–11562 14557641
32. Kerns JA, Emerman M, Malik HS, (2008) Positive selection and increased antiviral activity associated with the PARP-containing isoform of human zinc-finger antiviral protein. PLoS Genet 4: e21. doi: 10.1371/journal.pgen.0040021 18225958
33. Goossens KE, Karpala AJ, Ward A, Bean AG, (2014) Characterisation of chicken ZAP. Dev Comp Immunol 46: 373–381. doi: 10.1016/j.dci.2014.05.011 24877657
34. Esnault C, Maestre J, Heidmann T, (2000) Human LINE retrotransposons generate processed pseudogenes. Nat Genet 24: 363–367. 10742098
35. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, Kazazian HH, et al. (2001) Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 21: 1429–1439. 11158327
36. Kimberland ML, Divoky V, Prchal J, Schwahn U, Berger W, Kazazian HH, Jr (1999) Full-length human L1 insertions retain the capacity for high frequency retrotransposition in cultured cells. Hum Mol Genet 8: 1557–1560. 10401005
37. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, Kazazian HH, Jr (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87: 917–927. 8945518
38. Ostertag EM, Prak ET, DeBerardinis RJ, Moran JV, Kazazian HH, Jr (2000) Determination of L1 retrotransposition kinetics in cultured cells. Nucleic Acids Res 28: 1418–1423. 10684937
39. Wei W, Morrish TA, Alisch RS, Moran JV, (2000) A transient assay reveals that cultured human cells can accommodate multiple LINE-1 retrotransposition events. Anal Biochem 284: 435–438. 10964437
40. Nguyen K-L, Llano M, Akari H, Miyagi E, Poeschla EM, Strebel K, et al. (2004) Codon optimization of the HIV-1 vpu and vif genes stabilizes their messenger RNA and allows for highly efficient Rev-independent expression. Virology 319: 163. 15015498
41. King MC, Raposo G, Lemmon MA, (2004) Inhibition of nuclear import and cell-cycle progression by mutated forms of the dynamin-like GTPase MxB. Proc Natl Acad Sci USA 101: 8957–62. 15184662
42. Kane M, Yadav SS, Bitzegeio J, Kutluay SB, Zang T, Wilson SJ, et al. (2013) MX2 is an interferon-induced inhibitor of HIV-1 infection. Nature 502: 563–6. doi: 10.1038/nature12653 24121441
43. Liu Z, Pan Q, Ding S, Qian J, Xu F, Zhou J, et al. (2013) The interferon-inducible MxB protein inhibits HIV-1 infection. Cell Host Microbe 14: 398–410. doi: 10.1016/j.chom.2013.08.015 24055605
44. Goujon C, Moncorgé O, Bauby H, Doyle T, Barclay WS, Malim MH, (2014) Transfer of the amino-terminal nuclear envelope targeting domain of human MX2 converts MX1 into an HIV-1 resistance factor. J Virol 88: 9017–9026. doi: 10.1128/JVI.01269-14 24899177
45. Goujon C, Moncorgé O, Bauby H, Doyle T, Ward CC, Schaller T, et al. (2013) Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature 502: 559–562. doi: 10.1038/nature12542 24048477
46. Goodier JL, Cheung LE, Kazazian HH, Jr (2013) Mapping the LINE1 ORF1 protein interactome reveals associated inhibitors of human retrotransposition. Nucleic Acids Res 41: 7401–7419. doi: 10.1093/nar/gkt512 23749060
47. Marsischky GT, Wilson BA, Collier RJ, (1995) Role of glutamic acid 988 of human poly-ADP-ribose polymerase in polymer formation. Evidence for active site similarities to the ADP-ribosylating toxins. J Biol Chem 270: 3247–3254. 7852410
48. Kleine H, Poreba E, Lesniewicz K, Hassa PO, Hottiger MO, Litchfield DW, et al. (2008) Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol Cell 32: 57–69. doi: 10.1016/j.molcel.2008.08.009 18851833
49. Gao G, Guo X, Goff SP, (2002) Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 297: 1703–1706. 12215647
50. Guo X, Carroll JW, Macdonald MR, Goff SP, Gao G, (2004) The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J Virol 78: 12781–12787. 15542630
51. Zhu Y, Chen G, Lv F, Wang X, Ji X, Xu Y, et al. (2011) Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation. Proc Natl Acad Sci USA 108: 15834–15839. doi: 10.1073/pnas.1101676108 21876179
52. Chen S, Xu Y, Zhang K, Wang X, Sun J, Gao G, Liu Y, (2012) Structure of N-terminal domain of ZAP indicates how a zinc-finger protein recognizes complex RNA. Nat Struct Mol Biol 19: 430–435. doi: 10.1038/nsmb.2243 22407013
53. Hayakawa S, Shiratori S, Yamato H, Kameyama T, Kitatsuji C, Kashigi F, et al. (2011) ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses. Nat Immunol 12: 37–44. doi: 10.1038/ni.1963 21102435
54. Todorova T, Bock FJ, Chang P, . (2014) PARP13 regulates cellular mRNA post-transcriptionally and functions as a pro-apoptotic factor by destabilizing TRAILR4 transcript. Nat Commun 5: 5362 doi: 10.1038/ncomms6362 25382312
55. Gläsker S, Töller M, Kümmerer BM, (2014) The alternate triad motif of the poly(ADP-ribose) polymerase-like domain of the human zinc finger antiviral protein is essential for its antiviral activity. J Gen Virol 95(Pt 4): 816–822 doi: 10.1099/vir.0.060988-0 24457973
56. Charron G, Li MM, MacDonald MR, Hang HC, (2013) Prenylome profiling reveals S-farnesylation is crucial for membrane targeting and antiviral activity of ZAP long-isoform. Proc Natl Acad Sci USA 110: 11085–11090. doi: 10.1073/pnas.1302564110 23776219
57. An W, Dai L, Niewiadomska AM, Yetil A, O’Donnell KA, Han JS, Boeke JD, (2011) Characterization of a synthetic human LINE-1 retrotransposon ORFeus-Hs. Mobile DNA 2: 2. doi: 10.1186/1759-8753-2-2 21320307
58. Han JS, Boeke JD, (2004) A highly active synthetic mammalian retrotransposon. Nature 429: 314–318. 15152256
59. Naas TP, DeBerardinis RJ, Moran JV, Ostertag EM, Kingsmore SF, Seldin MF, et al. (1998) An actively retrotransposing, novel subfamily of mouse L1 elements. EMBO J 17: 590–597 9430649
60. Bebek F (2012) Towards the identification of novel interferon-alpha induced anti-hepatitis C virus effectors. Ph.D. thesis, School of Biotechnology and Biomolecular Sciences, University of New South Wales, Australia.
61. Dewannieux M, Esnault C, Heidmann T, (2003) LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 35: 41–48 12897783
62. Dewannieux M, Dupressoir A, Harper F, Pierron G, Heidmann T, (2004) Identification of autonomous IAP LTR retrotransposons mobile in mammalian cells. Nat Genet 36: 534–539. 15107856
63. Goodier JL, Zhang L, Vetter MR, Kazazian HH, Jr (2007) LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex. Mol Cell Biol 27: 6469–6483. 17562864
64. Goodier JL, Mandal PK, Zhang L, Kazazian HH, Jr (2010) Discrete subcellular partitioning of human retrotransposon RNAs despite a common mechanism of genome insertion. Hum Mol Genet 19: 1712–1725. doi: 10.1093/hmg/ddq048 20147320
65. Doucet AJ, Hulme AE, Sahinovic E, Kulpa DA, Moldovan JB, Kopera HC, et al. (2010) Characterization of LINE-1 ribonucleoprotein particles. PLoS Genet 6. pii: e1001150. doi: 10.1371/journal.pgen.1001150 20949108
66. Adjibade P, Mazroui R, (2014) Control of mRNA turnover: Implication of cytoplasmic RNA granules. Semin Cell Dev Biol 34:15–23. doi: 10.1016/j.semcdb.2014.05.013 24946962
67. Taylor MS, Lacava J, Mita P, Molloy KR, Huang CR, Li D, et al. (2013) Affinity proteomics reveals human host factors implicated in discrete stages of LINE-1 retrotransposition. Cell 155: 1034–1048. doi: 10.1016/j.cell.2013.10.021 24267889
68. Leung A, Todorova T, Ando Y, Chang P, (2011) Poly(ADP-ribose) regulates post-transcriptional gene regulation in the cytoplasm. RNA Biol 9: 542–548.
69. Lee H, Komano J, Saitoh Y, Yamaoka S, Kozaki T, Misawa T, et al. (2013) Zinc-finger antiviral protein mediates retinoic acid inducible gene I-like receptor-independent antiviral response to murine leukemia virus. Proc Natl Acad Sci USA 110: 12379–12384. doi: 10.1073/pnas.1310604110 23836649
70. Wang ZF, Wang XL, Gao GX, (2012) PR65A regulates the activity of the zinc-finger antiviral protein. Prog Biochem Biophysics 39: 431–437.
71. Sun L, Lv F, Guo X, Gao G, (2012) Glycogen synthase kinase 3β (GSK3β) modulates antiviral activity of zinc-finger antiviral protein (ZAP). J Biol Chem 287: 22882–22888. doi: 10.1074/jbc.M111.306373 22514281
72. Guo X, Ma J, Sun J, Gao G, (2007) The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc Natl Acad Sci USA 104: 151–156. 17185417
73. Ye P, Liu S, Zhu Y, Chen G, Gao G, (2010) DEXH-Box protein DHX30 is required for optimal function of the zinc-finger antiviral protein. Protein Cell 1: 956–964. doi: 10.1007/s13238-010-0117-8 21204022
74. Sheth U, Parker R, (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300: 805–808. 12730603
75. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, et al. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916–920. 17392790
76. Chen Z, Zhou Y, Song J, Zhang Z, (2013) hCKSAAP UbSite: Improved prediction of human ubiquitination site by exploiting amino acid pattern and properties. Biochim Biophys Acta 1834: 1461–1467. doi: 10.1016/j.bbapap.2013.04.006 23603789
77. Radivojac P, Vacic V, Haynes C, Cocklin RR, Mohan A, Heyen JW, et al. (2010) Identification, analysis and prediction of protein ubiquitination sites. Proteins 78: 365–380. doi: 10.1002/prot.22555 19722269
78. Willison KR, Grantham J, Lund P, (2001) The roles of the cytosolic chaperonin, CCT, in normal eukaryotic cell growth. In Molecular Chaperones in the Cell, (ed), pp 90–118. Oxford: Oxford University Press.
79. Dekker C, Stirling PC, McCormack EA, Filmore H, Paul A, et Brost RL, , al. (2008) The interaction network of the chaperonin CCT. EMBO J 27: 1827–1839. doi: 10.1038/emboj.2008.108 18511909
80. Gregersen LH, Schueler M, Munschauer M, Mastrobuoni G, Chen W, Kempa S, et al. (2014) MOV10 is a 5' to 3' RNA helicase contributing to UPF1 mRNA target degradation by translocation along 3' UTRs. Mol Cell 54: 573–585. doi: 10.1016/j.molcel.2014.03.017 24726324
81. Kulpa DA, Moran JV, (2006) Cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat Struct Mol Biol 13: 655–660. 16783376
82. Zhu Y, Wang X, Goff SP, Gao G, . (2012) Translational repression precedes and is required for ZAP-mediated mRNA decay. EMBO J 31: 4236–4246. doi: 10.1038/emboj.2012.271 23023399
83. Jacobs JL, Coyne CB, (2013) Mechanisms of MAVS regulation at the mitochondrial membrane. J Mol Biol 425: 5009–5019. doi: 10.1016/j.jmb.2013.10.007 24120683
84. Chiang JJ, Davis ME, Gack MU, (2014) Regulation of RIG-I-like receptor signaling by host and viral proteins. Cytokine Growth Factor Rev 25: 491–505. doi: 10.1016/j.cytogfr.2014.06.005 25023063
85. Espert L, Degols G, Lin Y-L, Vincent T, Benkirane M, Mechti N, (2005) Interferon-induced exonuclease ISG20 exhibits an antiviral activity against human immunodeficiency virus type 1. J Gen Virol 86: 2221–2229 16033969
86. Zhou Z, Wang N, Woodson SE, Dong Q, Wang J, Liang Y, et al. (2011) Antiviral activities of ISG20 in positive-strand RNA virus infections. Virology 409: 175–188. doi: 10.1016/j.virol.2010.10.008 21036379
87. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, et al. (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237–240. doi: 10.1038/nature08674 20075919
88. Wolf D, Goff SP, (2007) TRIM28 mediates primer binding site- targeted silencing of murine leukemia virus in embryonic cells. Cell 131: 46–57. 17923087
89. Mandal PK, Ewing AD, Hancks DC, Kazazian HH, Jr (2013) Enrichment of processed pseudogene transcripts in L1-ribonucleoprotein particles. Hum MolGenet 22: 3730–3748. doi: 10.1093/hmg/ddt225 23696454
90. Lu C, Luo Z, Jäger S, Krogan NJ, Peterlin BM, (2012) Moloney leukemia virus type 10 inhibits reverse transcription and retrotransposition of intracisternal a particles. J Virol 86: 10517–10523 doi: 10.1128/JVI.00868-12 22811528
91. Leung AK, Calabrese JM, Sharp PA, (2006) Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc Natl Acad Sci USA 103: 18125–18130. 17116888
92. Leung AK, Vyas S, Rood JE, Bhutkar A, Sharp PA, Chang P, (2011) Poly (ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol Cell 42: 489–499. doi: 10.1016/j.molcel.2011.04.015 21596313
93. Nano N, Houry WA, (2013) Chaperone-like activity of the AAA+ proteins Rvb1 and Rvb2 in the assembly of various complexes. Philos Trans R Soc Lond B Biol Sci 368: 20110399. doi: 10.1098/rstb.2011.0399 23530256
94. Wolf D, Goff SP, (2009) Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 458: 1201–1204. doi: 10.1038/nature07844 19270682
95. Iyengar S, Ivanov AV, Jin VX, Rauscher FJ, 3rdFarnham PJ, Friedli M, et al. (2011) Functional analysis of KAP1 genomic recruitment. Mol Cell Biol 31: 1833–1847. doi: 10.1128/MCB.01331-10 21343339
96. Castro-Diaz N, Ecco G, Coluccio A, Kapopoulou A, Yazdanpanah B, et al. 2014 Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev 28: 1397–1409. doi: 10.1101/gad.241661.114 24939876
97. Van Meter M, Kashyap M, Rezazadeh S, Geneva AJ, Morello TD, Seluanov A, et al. (2014) SIRT6 represses LINE1 retrotransposons by ribosylating KAP1 but this repression fails with stress and age. Nat Commun 5: 5011. doi: 10.1038/ncomms6011 25247314
98. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, et al. (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927–931. doi: 10.1038/nature08858 20164836
99. Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, Tang JX, et al. (2011) DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8: 676–687. doi: 10.1016/j.stem.2011.04.004 21624812
100. Maksakova IA, Thompson PJ, Goyal P, Jones SJ, Singh PB, Karimi MM, et al. (2013) Distinct roles of KAP1, HP1 and G9a/GLP in silencing of the two-cell-specific retrotransposon MERVL in mouse ES cells. Epigenetics Chromatin 6: 15. doi: 10.1186/1756-8935-6-15 23735015
101. Reichmann J, Crichton JH, Madej MJ, Taggart M, Gautier P, Garcia-Perez JL, et al. (2012) Microarray analysis of LTR retrotransposon silencing identifies Hdac1 as a regulator of retrotransposon expression in mouse embryonic stem cells. PLoS Comput Biol 8: e1002486. doi: 10.1371/journal.pcbi.1002486 22570599
102. Liu L, Chen G, Ji X, Gao G, (2004) ZAP is a CRM1-dependent nucleocytoplasmic shuttling protein. Biochem Biophys Res Commun 321: 517–523 15358138
103. MacDonald MR, Machlin ES, Albin OR, Levy DE, (2007) The zinc finger antiviral protein acts synergistically with an interferon-induced factor for maximal activity against alphaviruses. J Virol 81: 13509–13518. 17928353
104. Karki S, Li MM, Schoggins JW, Tian S, Rice CM, MacDonald MR, (2012) Multiple interferon stimulated genes synergize with the zinc finger antiviral protein to mediate anti-alphavirus activity. PLoS One 7:e37398. doi: 10.1371/journal.pone.0037398 22615998
105. Rusinova I, Forster S, Yu S, Kannan A, Masse M, Chapman R, et al. (2013) INTERFEROME v2. 0: an updated database of annotated interferon-regulated genes. Nucl Acids Res 41 (database issue): D1040–D1046. doi: 10.1093/nar/gks1215 23203888
106. Zhou Y, Ma J, Bushan Roy B, Wu JY, Pan Q, Rong L, Liang C, (2008) The packaging of human immunodeficiency virus type 1 RNA is restricted by overexpression of an RNA helicase DHX30. Virology 372: 97–106. 18022663
107. Bidet K, Dadlani D, Garcia-Blanco MA, (2014) G3BP1, G3BP2 and CAPRIN1 are required for translation of interferon stimulated mRNAs and are targeted by a dengue virus non-coding RNA. PLoS Pathog 10: e1004242. doi: 10.1371/journal.ppat.1004242 24992036
108. Kumar M, Rawat P, Khan SZ, Dhamija N, Chaudhary P, Ravi DS, et al. (2011) Reciprocal regulation of human immunodeficiency virus-1 gene expression and replication by heat shock proteins 40 and 70. J Mol Biol 410: 944–958. doi: 10.1016/j.jmb.2011.04.005 21763498
109. Urano E, Morikawa Y, Komano J, (2013) Novel role of HSP40/DNAJ in the regulation of HIV-1 replication. J Acquir Immune Defic Syndr 64: 154–162 doi: 10.1097/QAI.0b013e31829a2ef8 24047968
110. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, Carnero E, et al. (2009) Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5: 439–449. doi: 10.1016/j.chom.2009.04.006 19454348
111. Meredith M, Orr A, Everett RD, (1994) Herpes simplex virus type 1 immediate-early protein Vmw110 binds strongly and specifically to a 135-kDa cellular protein. Virology 100: 457–469.
112. Ha HC, Juluri K, Zhou Y, Leung S, Hermankova M, Snyder SH, (2001) Poly(ADP-ribose) polymerase-1 is required for efficient HIV-1 integration. Proc Natl Acad Sci USA 98: 3364–3368. 11248084
113. Kameoka M, Nukuzuma S, Itaya A, Tanaka Y, Ota K, Ikuta K, et al. (2004) RNA interference directed against Poly(ADP-Ribose) polymerase 1 efficiently suppresses human immunodeficiency virus type 1 replication in human cells. J Virol 78: 8931–8934. 15280503
114. Tulin A, Stewart D, Spradling AC, (2002) The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev 16: 2108–2119. 12183365
115. Ohsaki E, Ueda K, Sakakibara S, Do E, Yada K, Yamanishi K, (2004) Poly(ADP-ribose) polymerase 1 binds to Kaposi's sarcoma-associated herpesvirus (KSHV) terminal repeat sequence and modulates KSHV replication in latency. J Virol 78: 9936–9946. 15331727
116. Tempera I, Deng Z, Atanasiu C, Chen CJ, D'Erme M, Lieberman PM, (2010) Regulation of Epstein-Barr virus OriP replication by poly(ADP-ribose) polymerase 1. J Virol 84: 4988–4997. doi: 10.1128/JVI.02333-09 20219917
117. Kakugawa S, Shimojima M, Neumann G, Goto H, Kawaoka Y, (2009) RuvB-like protein 2 is a suppressor of influenza A virus polymerases. J Virol. 83: 6429–6434. doi: 10.1128/JVI.00293-09 19369355
118. Yu Q, Carbone CJ, Katlinskaya YV, Zheng H, Zheng K, Luo M, Wang PJ, Greenberg RA, Fuchs SY, (2015) Type I interferon controls propagation of Long Interspersed Element-1. J Biol Chem: 290: 10191–10199. doi: 10.1074/jbc.M114.612374 25716322
119. Frost RJ, Hamra FK, Richardson JA, Qi X, Bassel-Duby R, Olson EN, (2010) MOV10L1 is necessary for protection of spermatocytes against retrotransposons by Piwi-interacting RNAs. Proc Natl Acad Sci USA 107: 11847–52. doi: 10.1073/pnas.1007158107 20547853
120. Crow YJ, (2011) Type I interferonopathies: a novel set of inborn errors of immunity. Ann NY Acad Sci 1238: 91–98. doi: 10.1111/j.1749-6632.2011.06220.x 22129056
121. Liu Y, Jesus AA, Marrero B, Yang D, Ramsey SE, Montealegre Sanchez GA, et al. (2014) Activated STING in a vascular and pulmonary syndrome. N Engl J Med 371: 507–518. doi: 10.1056/NEJMoa1312625 25029335
122. Crow YJ, Rehwinkel J, (2009) Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum Mol Genet 18(R2): R130–6. doi: 10.1093/hmg/ddp293 19808788
123. Volkman HE, Stetson DB, (2014) The enemy within: endogenous retroelements and autoimmune disease. Nat Immunol 15: 415–422. doi: 10.1038/ni.2872 24747712
124. Rice GI, Forte GM, Szynkiewicz M, Chase DS, Aeby A, Abdel-Hamid MS, et al. (2013) Assessment of interferon-related biomarkers in Aicardi-Goutières syndrome associated with mutations in TREX1, RNASEH2A, RNASEH2B, RNASEH2C, SAMHD1, and ADAR: a case-control study. Lancet Neurol 12: 1159–1169. doi: 10.1016/S1474-4422(13)70258-8 24183309
125. Rice GI, del Toro Duany Y, Jenkinson EM, Forte GM, Anderson BH, Ariaudo G, et al. (2014) Gain-of-function mutations in IFIH1 cause a spectrum of human disease phenotypes associated with upregulated type I interferon signaling. Nat Genet 46: 503–509. doi: 10.1038/ng.2933 24686847
126. Oda H, Nakagawa K, Abe J, Awaya T, Funabiki M, Hijikata A, et al. (2014) Aicardi-Goutières syndrome is caused by IFIH1 mutations. Am J Hum Genet 95: 121–125. doi: 10.1016/j.ajhg.2014.06.007 24995871
127. Nishikura K, (2007) Editor meets silencer: crosstalk between RNA editing and RNA interference. Nat Genet 7: 919–931
128. Stetson DB, Ko JS, Heidmann T, Medzhitov R, (2008) Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 134: 587–598. doi: 10.1016/j.cell.2008.06.032 18724932
129. Wang X, Han Y, Dang Y, Fu W, Zhou T, Ptak RG, et al. (2010) Moloney leukemia virus 10 (MOV10) protein inhibits retrovirus replication. J Biol Chem 285: 14346–55. doi: 10.1074/jbc.M110.109314 20215113
130. An W, Han JS, Wheelan SJ, Davis ES, Coombes CE, Ye P, et al. (2006) Active retrotransposition by a synthetic L1 element in mice. Proc Natl Acad Sci USA 103: 18662–18667 17124176
131. Langelier MF, Planck JL, Roy S, Pascal JM, (2011) Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA: structural and functional insights into DNA-dependent PARP-1 activity. J Biol Chem 286: 10690–10701. doi: 10.1074/jbc.M110.202507 21233213
132. Agrawal P, Chen YT, Schilling B, Gibson BW, Hughes RE, (2012) Ubiquitin-specific peptidase 9, X-linked (USP9X) modulates activity of mammalian target of rapamycin (mTOR). J Biol Chem 287: 21164–21175. doi: 10.1074/jbc.M111.328021 22544753
133. Sarkari F, Wheaton K, La Delfa A, Mohamed M, Shaikh F, Khatun R, et al. (2013) Ubiquitin-specific protease 7 is a regulator of ubiquitin-conjugating enzyme UbE2E1. J Biol Chem 288: 16975–16985. doi: 10.1074/jbc.M113.469262 23603909
134. Alisch RS, Garcia-Perez JL, Muotri AR, Gage FH, Moran JV, (2006) Unconventional translation of mammalian LINE-1 retrotransposons. Genes Dev 20: 210–224. 16418485
135. Hulme AE, Bogerd HP, Cullen BR, Moran JV, (2007) Selective inhibition of Alu retrotransposition by APOBEC3G. Gene 390: 199–205. 17079095
136. Leibold DM, Swergold GD, Singer MF, Thayer RE, Dombroski BA, Fanning TG, (1990) Translation of LINE-1 DNA elements in vitro and in human cells. Proc Natl Acad Sci USA 87: 6990–6994. 1698287
137. Rodić N, Sharma R, Sharma R, Zampella J, Dai L, Taylor MS, et al. (2014) Long interspersed element-1 protein expression is a hallmark of many human cancers. Am J Pathol 184: 1280–1286. doi: 10.1016/j.ajpath.2014.01.007 24607009