96
Views
0
CrossRef citations to date
0
Altmetric
Review

Design stars: how Small DNA Viruses Remodel the Host Nucleus

&
Pages 445-459 | Published online: 17 May 2012

References

  • Howley PM , LowyDR. Papillomaviruses. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA, 2299–2354 (2007).
  • Imperiale MJ , MajorEO. Polyomaviruses. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA, 2263–2298 (2007).
  • Berns K , ParrishCR. Parvoviridae. In: Fields Virology. Knipe DM, Howley PM (Eds). Lippincott Williams & Wilkins, PA, USA, 2299–2349 (2007).
  • Greber UF , KasamatsuH. Nuclear targeting of SV40 and adenovirus. Trends Cell Biol.6(5) , 189–195 (1996).
  • Greber UF , SuomalainenM, StidwillRP, BouckeK, EbersoldMW, HeleniusA. The role of the nuclear pore complex in adenovirus DNA entry. EMBO J.16(19) , 5998–6007 (1997).
  • Trotman LC , MosbergerN, FornerodM, StidwillRP, GreberUF. Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nat. Cell Biol.3(12) , 1092–1100 (2001).
  • Strunze S , EngelkeMF, WangIH et al. Kinesin-1-mediated capsid disassembly and disruption of the nuclear pore complex promote virus infection. Cell Host Microbe 10(3) , 210–223 (2011).
  • Butin-Israeli V , Ben-Nun-ShaulO, KopatzI et al. Simian virus 40 induces lamin A/C fluctuations and nuclear envelope deformation during cell entry. Nucleus 2(4) , 320–330 (2011).
  • Okada Y , SuzukiT, SundenY et al. Dissociation of heterochromatin protein 1 from lamin B receptor induced by human polyomavirus agnoprotein: role in nuclear egress of viral particles. EMBO Rep. 6(5) , 452–457 (2005).
  • Huerfano S , ZilaV, BouraE, SpanielovaH, StokrovaJ, ForstovaJ. Minor capsid proteins of mouse polyomavirus are inducers of apoptosis when produced individually but are only moderate contributors to cell death during the late phase of viral infection. FEBS J.277(5) , 1270–1283 (2010).
  • Raghava S , GiordaKM, RomanoFB, HeuckAP, HebertDN. The SV40 late protein VP4 is a viroporin that forms pores to disrupt membranes for viral release. PLoS Pathog.7(6) , e1002116 (2011).
  • Giorda KM , RaghavaS, HebertDN. The SV40 late viral protein VP4 disrupts the nuclear envelope for viral release. J. Virol.86(6) , 3180–3192 (2012).
  • Cohen S , BehzadAR, CarrollJB, PanteN. Parvoviral nuclear import: bypassing the host nuclear-transport machinery. J. Gen. Virol.87(Pt 11) , 3209–3213 (2006).
  • Cohen S , MarrAK, GarcinP, PanteN. Nuclear envelope disruption involving host caspases plays a role in the parvovirus replication cycle. J. Virol.85(10) , 4863–4874 (2011).
  • Tattersall P . Replication of the parvovirus MVM. I. Dependence of virus multiplication and plaque formation on cell growth. J. Virol.10(4) , 586–590 (1972).
  • Giacinti C , GiordanoA. RB and cell cycle progression. Oncogene25(38) , 5220–5227 (2006).
  • Chellappan S , KrausVB, KrogerB et al. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl Acad. Sci. USA 89(10) , 4549–4553 (1992).
  • Decaprio JA . How the Rb tumor suppressor structure and function was revealed by the study of adenovirus and SV40. Virology384(2) , 274–284 (2009).
  • Ferrari R , PellegriniM, HorwitzGA, XieW, BerkAJ, KurdistaniSK. Epigenetic reprogramming by adenovirus E1A. Science321(5892) , 1086–1088 (2008).
  • Ben-Israel H , KleinbergerT. Adenovirus and cell cycle control. Front. Biosci.7 , d1369–d1395 (2002).
  • Yew PR , BerkAJ. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature357(6373) , 82–85 (1992).
  • Querido E , BlanchetteP, YanQ et al. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15(23) , 3104–3117 (2001).
  • Soria C , EstermannFE, EspantmanKC, O‘SheaCC. Heterochromatin silencing of p53 target genes by a small viral protein. Nature466(7310) , 1076–1081 (2010).
  • Huibregtse JM , ScheffnerM, HowleyPM. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J.10(13) , 4129–4135 (1991).
  • Scheffner M , HuibregtseJM, VierstraRD, HowleyPM. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell75(3) , 495–505 (1993).
  • Mietz JA , UngerT, HuibregtseJM, HowleyPM. The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein. EMBO J.11(13) , 5013–5020 (1992).
  • Jeon S , Allen-HoffmannBL, LambertPF. Integration of human papillomavirus type 16 into the human genome correlates with a selective growth advantage of cells. J. Virol.69(5) , 2989–2997 (1995).
  • Corden SA , Sant-CassiaLJ, EastonAJ, MorrisAG. The integration of HPV-18 DNA in cervical carcinoma. Mol. Pathol.52(5) , 275–282 (1999).
  • Munger K , BaldwinA, EdwardsKM et al. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol. 78(21) , 11451–11460 (2004).
  • Bargonetti J , ReynisdottirI, FriedmanPN, PrivesC. Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev.6(10) , 1886–1898 (1992).
  • Jiang D , SrinivasanA, LozanoG, RobbinsPD. SV40 T antigen abrogates p53-mediated transcriptional activity. Oncogene8(10) , 2805–2812 (1993).
  • Sarnow P , HoYS, WilliamsJ, LevineAJ. Adenovirus E1b-58kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 kD cellular protein in transformed cells. Cell28(2) , 387–394 (1982).
  • Dey D , DahlJ, ChoS, BenjaminTL. Induction and bypass of p53 during productive infection by polyomavirus. J. Virol.76(18) , 9526–9532 (2002).
  • Dilworth SM . Cell alterations induced by the large T-antigens of SV40 and polyoma virus. Semin. Cancer Biol.1(6) , 407–414 (1990).
  • Lomax M , FriedM. Polyoma virus disrupts ARF signaling to p53. Oncogene20(36) , 4951–4960 (2001).
  • Demetriou SK , Ona-VuK, SullivanEM, DongTK, HsuSW, OhDH. Defective DNA repair and cell cycle arrest in cells expressing merkel cell polyomavirus T antigen. Int. J. Cancer doi:10.1002/ijc.27440 (2012) (Epub ahead of print).
  • Zhou BB , ElledgeSJ. The DNA damage response: putting checkpoints in perspective. Nature408(6811) , 433–439 (2000).
  • Sancar A , Lindsey-BoltzLA, Unsal-KacmazK, LinnS. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem.73 , 39–85 (2004).
  • Araujo FD , StrackerTH, CarsonCT, LeeDV, WeitzmanMD. Adenovirus type 5 E4orf3 protein targets the Mre11 complex to cytoplasmic aggresomes. J. Virol.79(17) , 11382–11391 (2005).
  • Stracker TH , CarsonCT, WeitzmanMD. Adenovirus oncoproteins inactivate the Mre11–Rad50–Nbs1 DNA repair complex. Nature418(6895) , 348–352 (2002).
  • Liu Y , ShevchenkoA, BerkAJ. Adenovirus exploits the cellular aggresome response to accelerate inactivation of the MRN complex. J. Virol.79(22) , 14004–14016 (2005).
  • Evans JD , HearingP. Relocalization of the Mre11–Rad50–Nbs1 complex by the adenovirus E4 ORF3 protein is required for viral replication. J. Virol.79(10) , 6207–6215 (2005).
  • Carson CT , OrazioNI, LeeDV et al. Mislocalization of the MRN complex prevents ATR signaling during adenovirus infection. EMBO J. 28(6) , 652–662 (2009).
  • Carson CT , SchwartzRA, StrackerTH, LilleyCE, LeeDV, WeitzmanMD. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J.22(24) , 6610–6620 (2003).
  • Mathew SS , BridgeE. The cellular Mre11 protein interferes with adenovirus E4 mutant DNA replication. Virology365(2) , 346–355 (2007).
  • Mathew SS , BridgeE. Nbs1-dependent binding of Mre11 to adenovirus E4 mutant viral DNA is important for inhibiting DNA replication. Virology374(1) , 11–22 (2008).
  • Baker A , RohlederKJ, HanakahiLA, KetnerG. Adenovirus E4 34k and E1b 55k oncoproteins target host DNA ligase IV for proteasomal degradation. J. Virol.81(13) , 7034–7040 (2007).
  • Orazio NI , NaegerCM, KarlsederJ, WeitzmanMD. The adenovirus E1b55K/E4orf6 complex induces degradation of the Bloom helicase during infection. J. Virol.85(4) , 1887–1892 (2011).
  • Forrester NA , SedgwickGG, ThomasA et al. Serotype-specific inactivation of the cellular DNA damage response during adenovirus infection. J. Virol. 85(5) , 2201–2211 (2011).
  • Blackford AN , PatelRN, ForresterNA et al. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc. Natl Acad. Sci. USA 107(27) , 12251–12256 (2010).
  • Jayaram S , GilsonT, EhrlichES, YuXF, KetnerG, HanakahiL. E1B 55k-independent dissociation of the DNA ligase IV/XRCC4 complex by E4 34k during adenovirus infection. Virology382(2) , 163–170 (2008).
  • Boyer J , RohlederK, KetnerG. Adenovirus E4 34k and E4 11k inhibit double strand break repair and are physically associated with the cellular DNA-dependent protein kinase. Virology263(2) , 307–312 (1999).
  • Moody CA , LaiminsLA. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog.5(10) , e1000605 (2009).
  • Fradet-Turcotte A , Bergeron-LabrecqueF, MoodyCA, LehouxM, LaiminsLA, ArchambaultJ. Nuclear accumulation of the papillomavirus E1 helicase blocks S-phase progression and triggers an ATM-dependent DNA damage response. J. Virol.85(17) , 8996–9012 (2011).
  • Sakakibara N , MitraR, McbrideAA. The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J. Virol.85(17) , 8981–8995 (2011).
  • King LE , FiskJC, DornanES, DonaldsonMM, MelendyT, MorganIM. Human papillomavirus E1 and E2 mediated DNA replication is not arrested by DNA damage signalling. Virology406(1) , 95–102 (2010).
  • Iftner T , ElbelM, SchoppB et al. Interference of papillomavirus E6 protein with single-strand break repair by interaction with XRCC1. EMBO J. 21(17) , 4741–4748 (2002).
  • Chen B , SimpsonDA, ZhouY et al. Human papilloma virus type16 E6 deregulates CHK1 and sensitizes human fibroblasts to environmental carcinogens independently of its effect on p53. Cell Cycle 8(11) , 1775–1787 (2009).
  • Day T , VaziriC. HPV E6 oncoprotein prevents recovery of stalled replication forks independently of p53 degradation. Cell Cycle8(14) , 2138 (2009).
  • Shin KH , AhnJH, KangMK et al. HPV-16 E6 oncoprotein impairs the fidelity of DNA end-joining via p53-dependent and -independent pathways. Int. J. Oncol. 28(1) , 209–215 (2006).
  • Spardy N , CovellaK, ChaE et al. Human papillomavirus 16 E7 oncoprotein attenuates DNA damage checkpoint control by increasing the proteolytic turnover of claspin. Cancer Res. 69(17) , 7022–7029 (2009).
  • Santegoets LA , Van Baars R, Terlou A et al. Different DNA damage and cell cycle checkpoint control in low- and high-risk human papillomavirus infections of the vulva. Int. J. Cancer130(12) , 2874–2885 (2012).
  • Hoskins EE , MorrisTA, HigginbothamJM et al. Fanconi anemia deficiency stimulates HPV-associated hyperplastic growth in organotypic epithelial raft culture. Oncogene 28(5) , 674–685 (2009).
  • Park JW , PitotHC, StratiK et al. Deficiencies in the Fanconi anemia DNA damage response pathway increase sensitivity to HPV-associated head and neck cancer. Cancer Res. 70(23) , 9959–9968 (2010).
  • Dahl J , YouJ, BenjaminTL. Induction and utilization of an ATM signaling pathway by polyomavirus. J. Virol.79(20) , 13007–13017 (2005).
  • Shi Y , DodsonGE, ShaikhS, RundellK, TibbettsRS. Ataxia-telangiectasia-mutated (ATM) is a T-antigen kinase that controls SV40 viral replication in vivo.J. Biol. Chem.280(48) , 40195–40200 (2005).
  • Lees-Miller SP , ChenYR, AndersonCW. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell Biol.10(12) , 6472–6481 (1990).
  • Zhao X , Madden-FuentesRJ, LouBX et al. Ataxia telangiectasia-mutated damage-signaling kinase- and proteasome-dependent destruction of Mre11–Rad50–Nbs1 subunits in Simian virus 40-infected primate cells. J. Virol. 82(11) , 5316–5328 (2008).
  • Boichuk S , HuL, HeinJ, GjoerupOV. Multiple DNA damage signaling and repair pathways deregulated by simian virus 40 large T antigen. J. Virol.84(16) , 8007–8020 (2010).
  • Rohaly G , KorfK, DehdeS, DornreiterI. Simian virus 40 activates ATR-Delta p53 signaling to override cell cycle and DNA replication control. J. Virol.84(20) , 10727–10747 (2010).
  • Hein J , BoichukS, WuJ et al. Simian virus 40 large T antigen disrupts genome integrity and activates a DNA damage response via Bub1 binding. J. Virol. 83(1) , 117–127 (2009).
  • Wu X , AvniD, ChibaT et al. SV40 T antigen interacts with Nbs1 to disrupt DNA replication control. Genes Dev. 18(11) , 1305–1316 (2004).
  • Orba Y , SuzukiT, MakinoY et al. Large T antigen promotes JC virus replication in G2-arrested cells by inducing ATM- and ATR-mediated G2 checkpoint signaling. J. Biol. Chem. 285(2) , 1544–1554 (2010).
  • Darbinyan A , SiddiquiKM, SloninaD et al. Role of JC virus agnoprotein in DNA repair. J. Virol. 78(16) , 8593–8600 (2004).
  • Trojanek J , CroulS, HoT et al. T-antigen of the human polyomavirus JC attenuates faithful DNA repair by forcing nuclear interaction between IRS-1 and Rad51. J. Cell Physiol. 206(1) , 35–46 (2006).
  • Darbinyan A , WhiteMK, AkanS et al. Alterations of DNA damage repair pathways resulting from JCV infection. Virology 364(1) , 73–86 (2007).
  • Choi YK , NashK, ByrneBJ, MuzyczkaN, SongS. The effect of DNA-dependent protein kinase on adeno-associated virus replication. PLoS One5(12) , e15073 (2010).
  • Cervelli T , PalaciosJA, ZentilinL et al. Processing of recombinant AAV genomes occurs in specific nuclear structures that overlap with foci of DNA-damage-response proteins. J. Cell Sci. 121(Pt 3) , 349–357 (2008).
  • Schwartz RA , PalaciosJA, CassellGD, AdamS, GiaccaM, WeitzmanMD. The Mre11/Rad50/Nbs1 complex limits adeno-associated virus transduction and replication. J. Virol.81(23) , 12936–12945 (2007).
  • Sanlioglu S , BensonP, EngelhardtJF. Loss of ATM function enhances recombinant adeno-associated virus transduction and integration through pathways similar to UV irradiation. Virology268(1) , 68–78 (2000).
  • Luo Y , ChenAY, QiuJ. Bocavirus infection induces a DNA damage response that facilitates viral DNA replication and mediates cell death. J. Virol.85(1) , 133–145 (2011).
  • Adeyemi RO , LandryS, DavisME, WeitzmanMD, PintelDJ. Parvovirus minute virus of mice induces a DNA damage response that facilitates viral replication. PLoS Pathog.6(10) , e1001141 (2010).
  • Jurvansuu J , RajK, StasiakA, BeardP. Viral transport of DNA damage that mimics a stalled replication fork. J. Virol.79(1) , 569–580 (2005).
  • Berthet C , RajK, SaudanP, BeardP. How adeno-associated virus Rep78 protein arrests cells completely in S phase. Proc. Natl Acad. Sci. USA102(38) , 13634–13639 (2005).
  • Schwartz RA , CarsonCT, SchuberthC, WeitzmanMD. Adeno-associated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase. J. Virol.83(12) , 6269–6278 (2009).
  • Vogel R , SeyffertM, StrasserR et al. Adeno-associated virus type 2 modulates the host DNA damage response induced by herpes simplex virus 1 during coinfection. J. Virol. 86(1) , 143–155 (2012).
  • Fernandez-Capetillo O , LeeA, NussenzweigM, NussenzweigA. H2AX: the histone guardian of the genome. DNA Repair (Amst.)3(8–9) , 959–967 (2004).
  • Chowdhury D , KeoghMC, IshiiH, PetersonCL, BuratowskiS, LiebermanJ. Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell20(5) , 801–809 (2005).
  • Lilley CE , ChaurushiyaMS, WeitzmanMD. Chromatin at the intersection of viral infection and DNA damage. Biochim. Biophys. Acta1799(3–4) , 319–327 (2010).
  • Nichols GJ , SchaackJ, OrnellesDA. Widespread phosphorylation of histone H2AX by species C adenovirus infection requires viral DNA replication. J. Virol.83(12) , 5987–5998 (2009).
  • Fragkos M , BreuleuxM, ClementN, BeardP. Recombinant adeno-associated viral vectors are deficient in provoking a DNA damage response. J. Virol.82(15) , 7379–7387 (2008).
  • Lang SE , HearingP. The adenovirus E1A oncoprotein recruits the cellular TRRAP/GCN5 histone acetyltransferase complex. Oncogene22(18) , 2836–2841 (2003).
  • Horwitz GA , ZhangK, McBrianMA, GrunsteinM, KurdistaniSK, BerkAJ. Adenovirus small E1A alters global patterns of histone modification. Science321(5892) , 1084–1085 (2008).
  • Thomas MC , ChiangCM. E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Mol. Cell17(2) , 251–264 (2005).
  • Duensing S , MungerK. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res.62(23) , 7075–7082 (2002).
  • Zhang B , LaribeeRN, KlemszMJ, RomanA. Human papillomavirus type 16 E7 protein increases acetylation of histone H3 in human foreskin keratinocytes. Virology329(1) , 189–198 (2004).
  • Lee D , LimC, SeoT, KwonH, MinH, ChoeJ. The viral oncogene human papillomavirus E7 deregulates transcriptional silencing by Brm-related gene 1 via molecular interactions. J. Biol. Chem.277(50) , 48842–48848 (2002).
  • Guillaud M , Adler-StorthzK, MalpicaA et al. Subvisual chromatin changes in cervical epithelium measured by texture image analysis and correlated with HPV. Gynecol. Oncol. 99(3 Suppl. 1) , S16–S23 (2005).
  • Bernardi R , PandolfiPP. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol.8(12) , 1006–1016 (2007).
  • Everett RD , Chelbi-AlixMK. PML and PML nuclear bodies: implications in antiviral defence. Biochimie89(6–7) , 819–830 (2007).
  • Tavalai N , StammingerT. New insights into the role of the subnuclear structure ND10 for viral infection. Biochim. Biophys. Acta1783(11) , 2207–2221 (2008).
  • Geoffroy MC , Chelbi-AlixMK. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res.31(1) , 145–158 (2011).
  • Ishov AM , SotnikovAG, NegorevD et al. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 147(2) , 221–234 (1999).
  • Carvalho T , SeelerJS, OhmanK et al. Targeting of adenovirus E1A and E4-ORF3 proteins to nuclear matrix-associated PML bodies. J. Cell Biol. 131(1) , 45–56 (1995).
  • Doucas V , IshovAM, RomoA et al. Adenovirus replication is coupled with the dynamic properties of the PML nuclear structure. Genes Dev. 10(2) , 196–207 (1996).
  • Ullman AJ , HearingP. Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. J. Virol.82(15) , 7325–7335 (2008).
  • Ullman AJ , ReichNC, HearingP. Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. J. Virol.81(9) , 4744–4752 (2007).
  • Stracker TH , LeeDV, CarsonCT, AraujoFD, OrnellesDA, WeitzmanMD. Serotype-specific reorganization of the Mre11 complex by adenoviral E4orf3 proteins. J. Virol.79(11) , 6664–6673 (2005).
  • Hoppe A , BeechSJ, DimmockJ, LeppardKN. Interaction of the adenovirus type 5 E4 Orf3 protein with promyelocytic leukemia protein isoform II is required for ND10 disruption. J. Virol.80(6) , 3042–3049 (2006).
  • Rosa-Calatrava M , GraveL, Puvion-DutilleulF, ChattonB, KedingerC. Functional analysis of adenovirus protein IX identifies domains involved in capsid stability, transcriptional activity, and nuclear reorganization. J. Virol.75(15) , 7131–7141 (2001).
  • Schreiner S , WimmerP, SirmaH et al. Proteasome-dependent degradation of Daxx by the viral E1B-55K protein in human adenovirus-infected cells. J. Virol. 84(14) , 7029–7038 (2010).
  • Schreiner S , WimmerP, GroitlP et al. Adenovirus type 5 early region 1B 55K oncoprotein-dependent degradation of cellular factor Daxx is required for efficient transformation of primary rodent cells. J. Virol. 85(17) , 8752–8765 (2011).
  • Day PM , RodenRB, LowyDR, SchillerJT. 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(1) , 142–150 (1998).
  • Florin L , SchaferF, SotlarK, StreeckRE, SappM. Reorganization of nuclear domain 10 induced by papillomavirus capsid protein l2. Virology295(1) , 97–107 (2002).
  • Kieback E , MullerM. Factors influencing subcellular localization of the human papillomavirus L2 minor structural protein. Virology345(1) , 199–208 (2006).
  • Roberts S , HillmanML, KnightGL, GallimorePH. The ND10 component promyelocytic leukemia protein relocates to human papillomavirus type 1 E4 intranuclear inclusion bodies in cultured keratinocytes and in warts. J. Virol.77(1) , 673–684 (2003).
  • Day PM , BakerCC, LowyDR, SchillerJT. Establishment of papillomavirus infection is enhanced by promyelocytic leukemia protein (PML) expression. Proc. Natl Acad. Sci. USA101(39) , 14252–14257 (2004).
  • Nakahara T , LambertPF. Induction of promyelocytic leukemia (PML) oncogenic domains (PODs) by papillomavirus. Virology366(2) , 316–329 (2007).
  • Ishov AM , MaulGG. The periphery of nuclear domain 10 (ND10) as site of DNA virus deposition. J. Cell Biol.134(4) , 815–826 (1996).
  • Tang Q , BellP, TegtmeyerP, MaulGG. Replication but not transcription of simian virus 40 DNA is dependent on nuclear domain 10. J. Virol.74(20) , 9694–9700 (2000).
  • Gasparovic ML , MaginnisMS, O‘HaraBA, DuganAS, AtwoodWJ. Modulation of PML protein expression regulates JCV infection. Virology390(2) , 279–288 (2009).
  • Jiang M , EntezamiP, GamezM, StammingerT, ImperialeMJ. Functional reorganization of promyelocytic leukemia nuclear bodies during BK virus infection. mBio2(1) , e00281–e00210 (2011).
  • Young PJ , JensenKT, BurgerLR, PintelDJ, LorsonCL. Minute virus of mice NS1 interacts with the SMN protein, and they colocalize in novel nuclear bodies induced by parvovirus infection. J. Virol.76(8) , 3892–3904 (2002).
  • Cziepluch C , LampelS, GrewenigA, GrundC, LichterP, RommelaereJ. H-1 parvovirus-associated replication bodies: a distinct virus-induced nuclear structure. J. Virol.74(10) , 4807–4815 (2000).
  • Greco A . Involvement of the nucleolus in replication of human viruses. Rev. Med. Virol.19(4) , 201–214 (2009).
  • Lam YW , EvansVC, HeesomKJ, LamondAI, MatthewsDA. Proteomics analysis of the nucleolus in adenovirus-infected cells. Mol. Cell Proteomics9(1) , 117–130 (2010).
  • Castiglia CL , FlintSJ. Effects of adenovirus infection on rRNA synthesis and maturation in HeLa cells. Mol. Cell Biol.3(4) , 662–671 (1983).
  • Grinstein E , WernetP, SnijdersPJ et al. Nucleolin as activator of human papillomavirus type 18 oncogene transcription in cervical cancer. J. Exp. Med. 196(8) , 1067–1078 (2002).
  • Wong JM , KusdraL, CollinsK. Subnuclear shuttling of human telomerase induced by transformation and DNA damage. Nat. Cell Biol.4(9) , 731–736 (2002).
  • Jiang H , AlonsoMM, Gomez-ManzanoC, PiaoY, FueyoJ. Oncolytic viruses and DNA-repair machinery: overcoming chemoresistance of gliomas. Expert Rev. Anticancer Ther.6(11) , 1585–1592 (2006).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.