Regulation of the life cycle of HPVs by differentiation and the DNA damage response

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References

• 1  Zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer2(5),342–350 (2002).
  Medline CASGoogle Scholar
• 2  Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger ER. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep.56(RR-2),1–24 (2007).
  MedlineGoogle Scholar
• 3  Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer10(8),550–560 (2010).▪ Describes the critical role of the ATM DNA damage pathway in HPV genome amplification.
  Medline CASGoogle Scholar
• 4  Harper DM, Franco EL, Wheeler CM et al. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet367(9518),1247–1255 (2006).
  Medline CASGoogle Scholar
• 5  Wheeler CM, Castellsague X, Garland SM et al. Cross-protective efficacy of HPV-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by non-vaccine oncogenic HPV types: 4-year end-of-study analysis of the randomised, double-blind PATRICIA trial. Lancet Oncol.13(1),100–110 (2012).
  Medline CASGoogle Scholar
• 6  zur Hausen H. The search for infectious causes of human cancers: where and why (Nobel Lecture). Angew. Chem. Int. Ed.48,5798–5808 (2009).
  Medline CASGoogle Scholar
• 7  Bodily J, Laimins LA. Persistence of human papillomavirus infection: keys to malignant progression. Trends Microbiol.19(1),33–39 (2011).
  Medline CASGoogle Scholar
• 8  Arias-Pulido H, Peyton CL, Joste NE, Vargas H, Wheeler CM. Human papillomavirus type 16 integration in cervical carcinoma in situ and in invasive cervical cancer. J. Clin. Microbiol.44(5),1755–1762 (2006).
  Medline CASGoogle Scholar
• 9  Schneider-Maunoury S, Croissant O, Orth G. Integration of human papillomavirus type 16 DNA sequences: a possible early event in the progression of genital tumors. J. Virol.61(10),3295–3298 (1987).
  Medline CASGoogle Scholar
• 10  Smith PP, Friedman CL, Bryant EM, McDougall JK. Viral integration and fragile sites in human papillomavirus-immortalized human keratinocyte cell lines. Genes Chromosomes Cancer5(2),150–157 (1992).
  Medline CASGoogle Scholar
• 11  Thorland EC, Myers SL, Gostout BS, Smith DI. Common fragile sites are preferential targets for HPV16 integrations in cervical tumors. Oncogene22(8),1225–1237 (2003).
  Medline CASGoogle Scholar
• 12  Romanczuk H, Howley PM. Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl Acad. Sci. USA89(7),3159–3163 (1992).
  Medline CASGoogle Scholar
• 13  Duensing S, Munger K. Mechanisms of genomic instability in human cancer: insights from studies with human papillomavirus oncoproteins. Int. J. Cancer109(2),157–162 (2004).
  Medline CASGoogle Scholar
• 14  Munger K, Baldwin A, Edwards KM et al. Mechanisms of human papillomavirus-induced oncogenesis. J. Virol.78(21),11451–11460 (2004).
  MedlineGoogle Scholar
• 15  Geisen C, Kahn T. Promoter activity of sequences located upstream of the human papillomavirus types of 16 and 18 late regions. J. Gen. Virol.77(Pt 9),2193–2200 (1996).
  Medline CASGoogle Scholar
• 16  Ozbun MA, Meyers C. Temporal usage of multiple promoters during the life cycle of human papillomavirus type 31b. J. Virol.72(4),2715–2722 (1998).
  Medline CASGoogle Scholar
• 17  Braunstein TH, Madsen BS, Gavnholt B, Rosenstierne MW, Johnsen CK, Norrild B. Identification of a new promoter in the early region of the human papillomavirus type 16 genome. J. Gen. Virol.80(Pt 12),3241–3250 (1999).
  Medline CASGoogle Scholar
• 18  Hebner CM, Laimins LA. Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity. Rev. Med. Virol.16(2),83–97 (2006).
  Medline CASGoogle Scholar
• 19  Moody CA, Laimins LA. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog.5(10),e1000605 (2009).
  MedlineGoogle Scholar
• 20  Banerjee NS, Wang HK, Broker TR, Chow LT. Human papillomavirus (HPV) E7 induces prolonged G2 following S phase reentry in differentiated human keratinocytes. J. Biol. Chem.286(17),15473–15482 (2011).
  Medline CASGoogle Scholar
• 21  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.5(4),e1000397 (2009).
  MedlineGoogle Scholar
• 22  Hughes FJ, Romanos MA. E1 protein of human papillomavirus is a DNA helicase/ATPase. Nucleic Acids Res.21(25),5817–5823 (1993).
  Medline CASGoogle Scholar
• 23  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.274(5),2696–2705 (1999).
  Medline CASGoogle Scholar
• 24  Oliveira JG, Colf LA, McBride AA. Variations in the association of papillomavirus E2 proteins with mitotic chromosomes. Proc. Natl Acad. Sci. USA103(4),1047–1052 (2006).
  Medline CASGoogle Scholar
• 25  Poddar A, Reed SC, McPhillips MG, Spindler JE, McBride AA. The human papillomavirus type 8 E2 tethering protein targets the ribosomal DNA loci of host mitotic chromosomes. J. Virol.83(2),640–650 (2009).
  Medline CASGoogle Scholar
• 26  Kukimoto I, Takeuchi T, Kanda T. CCAAT/enhancer binding protein beta binds to and activates the P670 promoter of human papillomavirus type 16. Virology346(1),98–107 (2006).
  Medline CASGoogle Scholar
• 27  Patel D, Huang SM, Baglia LA, McCance DJ. The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J.18(18),5061–5072 (1999).
  Medline CASGoogle Scholar
• 28  Hebner C, Beglin M, Laimins LA. Human papillomavirus E6 proteins mediate resistance to interferon-induced growth arrest through inhibition of p53 acetylation. J. Virol.81(23),12740–12747 (2007).
  Medline CASGoogle Scholar
• 29  Liu X, Dakic A, Zhang Y, Dai Y, Chen R, Schlegel R. HPV E6 protein interacts physically and functionally with the cellular telomerase complex. Proc. Natl Acad. Sci. USA106(44),18780–18785 (2009).
  Medline CASGoogle Scholar
• 30  Wise-Draper TM, Wells SI. Papillomavirus E6 and E7 proteins and their cellular targets. Front. Biosci.13,1003–1017 (2008).
  Medline CASGoogle Scholar
• 31  Howie HL, Katzenellenbogen RA, Galloway DA. Papillomavirus E6 proteins. Virology384(2),324–334 (2009).
  Medline CASGoogle Scholar
• 32  Dyson N, Howley PM, Munger K, Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science243(4893),934–937 (1989).
  Medline CASGoogle Scholar
• 33  Munger K, Werness BA, Dyson N, Phelps WC, Harlow E, Howley PM. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J.8(13),4099–4105 (1989).
  Medline CASGoogle Scholar
• 34  Longworth MS, Wilson R, Laimins LA. HPV31 E7 facilitates replication by activating E2F2 transcription through its interaction with HDACs. EMBO J.24(10),1821–1830 (2005).
  Medline CASGoogle Scholar
• 35  Regan JA, Laimins LA. Bap31 is a novel target of the human papillomavirus E5 protein. J. Virol.82(20),10042–10051 (2008).
  Medline CASGoogle Scholar
• 36  Nelson LM, Rose RC, Moroianu J. Nuclear import strategies of high risk HPV16 L1 major capsid protein. J. Biol. Chem.277(26),23958–23964 (2002).
  Medline CASGoogle Scholar
• 37  Darshan MS, Lucchi J, Harding E, Moroianu J. The l2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors. J. Virol.78(22),12179–12188 (2004).
  Medline CASGoogle Scholar
• 38  Ai W, Narahari J, Roman A. Yin yang 1 negatively regulates the differentiation-specific E1 promoter of human papillomavirus type 6. J. Virol.74(11),5198–5205 (2000).
  Medline CASGoogle Scholar
• 39  Hartley KA, Alexander KA. Human TATA binding protein inhibits human papillomavirus type 11 DNA replication by antagonizing E1–E2 protein complex formation on the viral origin of replication. J. Virol.76(10),5014–5023 (2002).
  Medline CASGoogle Scholar
• 40  Offord EA, Beard P. A member of the activator protein 1 family found in keratinocytes but not in fibroblasts required for transcription from a human papillomavirus type 18 promoter. J. Virol.64(10),4792–4798 (1990).
  Medline CASGoogle Scholar
• 41  O’Connor M, Bernard HU. Oct-1 activates the epithelial-specific enhancer of human papillomavirus type 16 via a synergistic interaction with NFI at a conserved composite regulatory element. Virology207(1),77–88 (1995).
  MedlineGoogle Scholar
• 42  Stunkel W, Bernard HU. The chromatin structure of the long control region of human papillomavirus type 16 represses viral oncoprotein expression. J. Virol.73(3),1918–1930 (1999).
  Medline CASGoogle Scholar
• 43  Stubenrauch F, Lim HB, Laimins LA. Differential requirements for conserved E2 binding sites in the life cycle of oncogenic human papillomavirus type 31. J. Virol.72(2),1071–1077 (1998).
  Medline CASGoogle Scholar
• 44  Steger G, Corbach S. Dose-dependent regulation of the early promoter of human papillomavirus type 18 by the viral E2 protein. J. Virol.71(1),50–58 (1997).
  Medline CASGoogle Scholar
• 45  Thierry F. Transcriptional regulation of the papillomavirus oncogenes by cellular and viral transcription factors in cervical carcinoma. Virology384(2),375–379 (2009).
  Medline CASGoogle Scholar
• 46  Gunasekharan V, Hache G, Laimins L. Differentiation-dependent changes in levels of C/EBPbeta repressors and activators regulate human papillomavirus type 31 late gene expression. J. Virol.86(9),5393–5398 (2012).
  Medline CASGoogle Scholar
• 47  Zheng ZM, Wang X. Regulation of cellular miRNA expression by human papillomaviruses. Biochem. Biophys. Acta1809(11–12),668–677 (2011).
  Medline CASGoogle Scholar
• 48  Melar-New M, Laimins LA. Human papillomaviruses modulate expression of microRNA 203 upon epithelial differentiation to control levels of p63 proteins. J. Virol.84(10),5212–5221 (2010).
  Medline CASGoogle Scholar
• 49  Mighty KK, Laimins LA. p63 is necessary for the activation of human papillomavirus late viral functions upon epithelial differentiation. J. Virol.85(17),8863–8869 (2011).
  Medline CASGoogle Scholar
• 50  Wang X, Tang S, Le SY et al. Aberrant expression of oncogenic and tumor-suppressive microRNAs in cervical cancer is required for cancer cell growth. PLoS ONE3(7),e2557 (2008).
  MedlineGoogle Scholar
• 51  Hong S, Mehta KP, Laimins LA. Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiation-dependent genome amplification and plasmid maintenance. J. Virol.85(18),9486–9494 (2011).
  Medline CASGoogle Scholar
• 52  Terenzi F, Saikia P, Sen GC. Interferon-inducible protein, P56, inhibits HPV DNA replication by binding to the viral protein E1. EMBO J.27(24),3311–3321 (2008).
  Medline CASGoogle Scholar
• 53  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.84(24),13036–13039 (2010).
  Medline CASGoogle Scholar
• 54  Hong S, Laimins LA. The JAK–STAT transcriptional regulator, STAT-5, activates the ATM DNA damage pathway to induce HPV 31 genome amplification upon epithelial differentiation. PLoS Pathog.9(4),e1003295 (2013).▪ Identifies STAT-5 as an important activator of the ATM DNA damage response and consequently a regulator of HPV differentiation-dependent genome amplification.
  Medline CASGoogle Scholar
• 55  Price BD, D’Andrea AD. Chromatin remodeling at DNA double-strand breaks. Cell152(6),1344–1354 (2013).
  Medline CASGoogle Scholar
• 56  Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol. Cell40(2),179–204 (2010).
  Medline CASGoogle Scholar
• 57  Kastan MB. DNA damage responses: mechanisms and roles in human disease: 2007 GHA. Clowes Memorial Award Lecture. Mol. Cancer Res.6(4),517–524 (2008).
  Medline CASGoogle Scholar
• 58  Bouwman P, Jonkers J. The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance. Nat. Rev. Cancer12(9),587–598 (2012).
  Medline CASGoogle Scholar
• 59  Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature481(7381),287–294 (2012).
  Medline CASGoogle Scholar
• 60  Curtin NJ. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer12(12),801–817 (2012).
  Medline CASGoogle Scholar
• 61  Smith J, Tho LM, Xu N, Gillespie DA. The ATM–Chk2 and ATR–Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res.108,73–112 (2010).
  Medline CASGoogle Scholar
• 62  Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature432(7015),316–323 (2004).
  Medline CASGoogle Scholar
• 63  Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev.19(9),1040–1052 (2005).
  Medline CASGoogle Scholar
• 64  Myers JS, Cortez D. Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J. Biol. Chem.281(14),9346–9350 (2006).
  Medline CASGoogle Scholar
• 65  Jazayeri A, Falck J, Lukas C et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol.8(1),37–45 (2006).
  Medline CASGoogle Scholar
• 66  Walker M, Black EJ, Oehler V, Gillespie DA, Scott MT. Chk1 C-terminal regulatory phosphorylation mediates checkpoint activation by de-repression of Chk1 catalytic activity. Oncogene28(24),2314–2323 (2009).
  Medline CASGoogle Scholar
• 67  Yarden RI, Pardo-Reoyo S, Sgagias M, Cowan KH, Brody LC. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet.30(3),285–289 (2002).
  MedlineGoogle Scholar
• 68  Banin S, Moyal L, Shieh S et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science281(5383),1674–1677 (1998).
  Medline CASGoogle Scholar
• 69  Maya R, Balass M, Kim ST et al. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev.15(9),1067–1077 (2001).
  Medline CASGoogle Scholar
• 70  Canman CE, Wolff AC, Chen CY, Fornace AJ Jr, Kastan MB. The p53-dependent G1 cell cycle checkpoint pathway and ataxia-telangiectasia. Cancer Res.54(19),5054–5058 (1994).
  Medline CASGoogle Scholar
• 71  Chen CY, Oliner JD, Zhan Q, Fornace AJ Jr, Vogelstein B, Kastan MB. Interactions between p53 and MDM2 in a mammalian cell cycle checkpoint pathway. Proc. Natl Acad. Sci. USA91(7),2684–2688 (1994).
  Medline CASGoogle Scholar
• 72  Matsuoka S, Huang M, Elledge SJ. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science282(5395),1893–1897 (1998).
  Medline CASGoogle Scholar
• 73  Zhou BB, Chaturvedi P, Spring K et al. Caffeine abolishes the mammalian G(2)/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem.275(14),10342–10348 (2000).
  Medline CASGoogle Scholar
• 74  Gatei M, Zhou BB, Hobson K, Scott S, Young D, Khanna KK. Ataxia telangiectasia mutated (ATM) kinase and ATM and Rad3 related kinase mediate phosphorylation of BRCA1 at distinct and overlapping sites. In vivo assessment using phospho-specific antibodies. J. Biol. Chem.276(20),17276–17280 (2001).
  Medline CASGoogle Scholar
• 75  D’Amours D, Jackson SP. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol.3(5),317–327 (2002).
  MedlineGoogle Scholar
• 76  Lee JH, Paull TT. ATM activation by DNA double-strand breaks through the Mre11–Rad50–Nbs1 complex. Science308(5721),551–554 (2005).
  Medline CASGoogle Scholar
• 77  Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair3(8–9),959–967 (2004).
  Medline CASGoogle Scholar
• 78  Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB. Phosphorylation of SMC1 is a critical downstream event in the ATM–NBS1–BRCA1 pathway. Genes Dev.18(12),1423–1438 (2004).
  Medline CASGoogle Scholar
• 79  Cortez D, Wang Y, Qin J, Elledge SJ. Requirement of ATM-dependent phosphorylation of BRCA1 in the DNA damage response to double-strand breaks. Science286(5442),1162–1166 (1999).
  Medline CASGoogle Scholar
• 80  Chen L, Gilkes DM, Pan Y, Lane WS, Chen J. ATM and Chk2-dependent phosphorylation of MDMX contribute to p53 activation after DNA damage. EMBO J.24(19),3411–3422 (2005).
  Medline CASGoogle Scholar
• 81  Blasina A, De Weyer IV, Laus MC, Luyten WH, Parker AE, McGowan CH. A human homologue of the checkpoint kinase Cds1 directly inhibits Cdc25 phosphatase. Curr. Biol.9(1),1–10 (1999).
  Medline CASGoogle Scholar
• 82  Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA–ssDNA complexes. Science300(5625),1542–1548 (2003).
  Medline CASGoogle Scholar
• 83  Kumagai A, Dunphy WG. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell Biol.5(2),161–165 (2003).
  Medline CASGoogle Scholar
• 84  Kumagai A, Lee J, Yoo HY, Dunphy WG. TopBP1 activates the ATR–ATRIP complex. Cell124(5),943–955 (2006).
  Medline CASGoogle Scholar
• 85  Falck J, Petrini JH, Williams BR, Lukas J, Bartek J. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet.30(3),290–294 (2002).
  MedlineGoogle Scholar
• 86  Lee J, Kumagai A, Dunphy WG. Positive regulation of Wee1 by Chk1 and 14–13–3 proteins. Mol. Biol. Cell12(3),551–563 (2001).
  Medline CASGoogle Scholar
• 87  Sorensen CS, Hansen LT, Dziegielewski J et al. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol.7(2),195–201 (2005).
  Medline CASGoogle Scholar
• 88  Sakakibara N, Mitra R, McBride AA. The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J. Virol.85(17),8981–8995 (2011).
  Medline CASGoogle Scholar
• 89  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.85(17),8996–9012 (2011).
  Medline CASGoogle Scholar
• 90  Rogoff HA, Pickering MT, Frame FM et al. Apoptosis associated with deregulated E2F activity is dependent on E2F1 and Atm/Nbs1/Chk2. Mol. Cell Biol.24(7),2968–2977 (2004).
  Medline CASGoogle Scholar
• 91  Flores ER, Lambert PF. Evidence for a switch in the mode of human papillomavirus type 16 DNA replication during the viral life cycle. J. Virol.71(10),7167–7179 (1997).
  Medline CASGoogle Scholar
• 92  Dasgupta S, Zabielski J, Simonsson M, Burnett S. Rolling-circle replication of a high-copy BPV-1 plasmid. J. Mol. Biol.228(1),1–6 (1992).
  Medline CASGoogle Scholar
• 93  Gillespie KA, Mehta KP, Laimins LA, Moody CA. Human papillomaviruses recruit cellular DNA repair and homologous recombination factors to viral replication centers. J. Virol.86(17),9520–9526 (2012).▪ Demonstrates that the members of the homologous DNA recombination pathway along with ATM DNA damage factors are recruited to HPV replication foci to facilitate genome amplification.
  Medline CASGoogle Scholar
• 94  Moody CA, Fradet-Turcotte A, Archambault J, Laimins LA. Human papillomaviruses activate caspases upon epithelial differentiation to induce viral genome amplification. Proc. Natl Acad. Sci. USA104(49),19541–19546 (2007).
  Medline CASGoogle Scholar
• 95  Reinson T, Toots M, Kadaja M et al. Engagement of the ATR-dependent DNA damage response at the human papillomavirus 18 replication centers during the initial amplification. J. Virol.87(2),951–964 (2013).
  Medline CASGoogle Scholar
• 96  Edwards TG, Helmus MJ, Koeller K, Bashkin JK, Fisher C. Human papillomavirus episome stability is reduced by aphidicolin and controlled by DNA damage response pathways. J. Virol.87(7),3979–3989 (2013).
  Medline CASGoogle Scholar
• 97  Ozaki T, Wu D, Sugimoto H, Nagase H, Nakagawara A. Runt-related transcription factor 2 (RUNX2) inhibits p53-dependent apoptosis through the collaboration with HDAC6 in response to DNA damage. Cell Death Dis.4,e610 (2013).
  Medline CASGoogle Scholar
• 98  Croxford JL, Tang ML, Pan MF et al. ATM-dependent spontaneous regression of early Emu-myc-induced murine B-cell leukemia depends on natural killer and T cells. Blood121(13),2512–2521 (2013).
  Medline CASGoogle Scholar
• 99  Yoo J, Lee HN, Choi I et al. Opposing regulation of PROX1 by interleukin-3 receptor and NOTCH directs differential host cell fate reprogramming by Kaposi sarcoma herpes virus. PLoS Pathog.8(6),e1002770 (2012).
  Medline CASGoogle Scholar
• 100  Migone TS, Lin JX, Cereseto A et al. Constitutively activated Jak–STAT pathway in T cells transformed with HTLV-I. Science269(5220),79–81 (1995).
  Medline CASGoogle Scholar
• 101  Zhao X, Madden-Fuentes RJ, Lou BX 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).
  Medline CASGoogle Scholar
• 102  Sowd GA, Li NY, Fanning E. ATM and ATR activities maintain replication fork integrity during SV40 chromatin replication. PLoS Pathog.9(4),e1003283 (2013).
  Medline CASGoogle Scholar
• 103  Li R, Zhu J, Xie Z et al. Conserved herpes virus kinases target the DNA damage response pathway and TIP60 histone acetyltransferase to promote virus replication. Cell Host Microbe10(4),390–400 (2011).
  Medline CASGoogle Scholar
• 104  McFadden K, Luftig MA. Interplay between DNA tumor viruses and the host DNA damage response. Curr. Top. Microbiol. Immunol.371,229–257 (2013).
  Medline CASGoogle Scholar
• 105  Luo Y, Lou S, Deng X et al. Parvovirus B19 infection of human primary erythroid progenitor cells triggers ATR–Chk1 signaling, which promotes B19 virus replication. J. Virol.85(16),8046–8055 (2011).
  Medline CASGoogle Scholar
• 106  Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability – an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol.11(3),220–228 (2010).
  Medline CASGoogle Scholar