Full Text:  <676>

Summary:  <394>

CLC number: R737.33

On-line Access: 2017-03-08

Received: 2016-07-04

Revision Accepted: 2016-11-14

Crosschecked: 2017-02-08

Cited: 0

Clicked: 719

Citations:  Bibtex RefMan EndNote GB/T7714

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2017 Vol.18 No.3 P.215-232

10.1631/jzus.B1600306


DNA damage response is hijacked by human papillomaviruses to complete their life cycle


Author(s):  Shi-yuan Hong

Affiliation(s):  Department of Microbiology-Immunology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA

Corresponding email(s):   Shiyuan-hong@northwestern.edu

Key Words:  Papillomavirus, DNA damage, Amplification, Differentiation, ATM/CHK2, ATR/CHK1, STAT-5


Shi-yuan Hong. DNA damage response is hijacked by human papillomaviruses to complete their life cycle[J]. Journal of Zhejiang University Science B, 2017, 18(4): 215-232.

@article{title="DNA damage response is hijacked by human papillomaviruses to complete their life cycle",
author="Shi-yuan Hong",
journal="Journal of Zhejiang University Science B",
volume="18",
number="3",
pages="215-232",
year="2017",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1600306"
}

%0 Journal Article
%T DNA damage response is hijacked by human papillomaviruses to complete their life cycle
%A Shi-yuan Hong
%J Journal of Zhejiang University SCIENCE B
%V 18
%N 3
%P 215-232
%@ 1673-1581
%D 2017
%I Zhejiang University Press & Springer

TY - JOUR
T1 - DNA damage response is hijacked by human papillomaviruses to complete their life cycle
A1 - Shi-yuan Hong
J0 - Journal of Zhejiang University Science B
VL - 18
IS - 3
SP - 215
EP - 232
%@ 1673-1581
Y1 - 2017
PB - Zhejiang University Press & Springer
ER -


Abstract: 
The DNA damage response (DDR) is activated when DNA is altered by intrinsic or extrinsic agents. This pathway is a complex signaling network and plays important roles in genome stability, tumor transformation, and cell cycle regulation. Human papillomaviruses (HPVs) are the main etiological agents of cervical cancer. Cervical cancer ranks as the fourth most common cancer among women and the second most frequent cause of cancer-related death worldwide. Over 200 types of HPVs have been identified and about one third of these infect the genital tract. The HPV life cycle is associated with epithelial differentiation. Recent studies have shown that HPVs deregulate the DDR to achieve a productive life cycle. In this review, I summarize current findings about how HPVs mediate the ataxia-telangiectasia mutated kinase (ATM) and the ATM-and RAD3-related kinase (ATR) DDRs, and focus on the roles that ATM and ATR signalings play in HPV viral replication. In addition, I demonstrate that the signal transducer and activator of transcription-5 (STAT)-5, an important immune regulator, can promote ATM and ATR activations through different mechanisms. These findings may provide novel opportunities for development of new therapeutic targets for HPV-related cancers.

人类乳突病毒利用DNA损伤修复机制完成其生命周期

概要:本文总结目前学术界对人类乳突病毒如何利用DNA损伤修复来完成其复制的认识。DNA损伤修复对人类乳突病毒复制有不可或缺的作用。乳突病毒通过对许多DNA损伤因子的调控来控制病毒本身的复制。值得注意的是,病毒通过磷酸化STAT-5转录因子激活ATM和ATR DNA损伤修复通路,这意味着在乳突病毒复制的过程中,病毒利用对免疫反应的调节来激活DNA损伤修复机制,从而达到其复制的目的。
关键词:人类乳突病毒;DNA损伤修复;扩展;分化;ATM/CHK2通路;ATR/CHK1通路;STAT-5转录因子

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]Abbas, A.K., Lichtman, A.H., Pillai, S., 2014. Cellular and Molecular Immunology. Elsevier Saunders, Philadelphia, PA.

[2]Aguilar-Quesada, R., Munoz-Gamez, J.A., Martin-Oliva, D., et al., 2007. Interaction between ATM and PARP-1 in response to DNA damage and sensitization of ATM deficient cells through PARP inhibition. BMC Mol. Biol., 8:29.

[3]Ai, W., Narahari, J., Roman, A., 2000. Yin yang 1 negatively regulates the differentiation-specific E1 promoter of human papillomavirus type 6. J. Virol., 74(11):5198-5205.

[4]Ali, A., Zhang, J., Bao, S., et al., 2004. Requirement of protein phosphatase 5 in DNA-damage-induced ATM activation. Genes Dev., 18(3):249-254.

[5]Anacker, D.C., Gautam, D., Gillespie, K.A., et al., 2014. Productive replication of human papillomavirus 31 requires DNA repair factor NBS1. J. Virol., 88(15):8528-8544.

[6]Atamna, H., Cheung, I., Ames, B.N., 2000. A method for detecting abasic sites in living cells: age-dependent changes in base excision repair. PNAS, 97(2):686-691.

[7]Bakr, A., Oing, C., Kocher, S., et al., 2015. Involvement of ATM in homologous recombination after end resection and RAD51 nucleofilament formation. Nucleic Acids Res., 43(6):3154-3166.

[8]Banerjee, N.S., Wang, H.K., Broker, T.R., et al., 2011. Human papillomavirus (HPV) E7 induces prolonged G2 following S phase reentry in differentiated human keratinocytes. J. Biol. Chem., 286(17):15473-15482.

[9]Banin, S., Moyal, L., Shieh, S., et al., 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science, 281(5383):1674-1677.

[10]Beglin, M., Melar-New, M., Laimins, L., 2009. Human papillomaviruses and the interferon response. J. Interferon Cytokine Res., 29(9):629-635.

[11]Beishline, K., Kelly, C.M., Olofsson, B.A., et al., 2012. Sp1 facilitates DNA double-strand break repair through a nontranscriptional mechanism. Mol. Cell. Biol., 32(18):3790-3799.

[12]Blasina, A., de Weyer, I.V., Laus, M.C., et al., 1999. A human homologue of the checkpoint kinase Cds1 directly inhibits Cdc25 phosphatase. Curr. Biol., 9(1):1-10.

[13]Boner, W., Taylor, E.R., Tsirimonaki, E., et al., 2002. A functional interaction between the human papillomavirus 16 transcription/replication factor E2 and the DNA damage response protein TopBP1. J. Biol. Chem., 277(25):22297-22303.

[14]Bouwman, P., Jonkers, J., 2012. The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance. Nat. Rev. Cancer, 12(9):587-598.

[15]Burma, S., Chen, B.P., Murphy, M., et al., 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem., 276(45):42462-42467.

[16]Byun, T.S., Pacek, M., Yee, M.C., et al., 2005. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev., 19(9):1040-1052.

[17]Canman, C.E., Wolff, A.C., Chen, C.Y., et al., 1994. The p53-dependent G1 cell cycle checkpoint pathway and ataxia-telangiectasia. Cancer Res., 54(19):5054-5058.

[18]Carney, J.P., Maser, R.S., Olivares, H., et al., 1998. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell, 93(3):477-486.

[19]Cary, R.B., Peterson, S.R., Wang, J., et al., 1997. DNA looping by Ku and the DNA-dependent protein kinase. PNAS, 94(9):4267-4272.

[20]Chang, Y.E., Laimins, L.A., 2000. Microarray analysis identifies interferon-inducible genes and STAT-1 as major transcriptional targets of human papillomavirus type 31. J. Virol., 74(9):4174-4182.

[21]Chappell, W.H., Gautam, D., Ok, S.T., et al., 2016. Homologous recombination repair factors RAD51 and BRCA1 are necessary for productive replication of human papillomavirus 31. J. Virol., 90(5):2639-2652.

[22]Chen, B., Simpson, D.A., Zhou, Y., et al., 2009. 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.

[23]Chen, J., 2000. Ataxia telangiectasia-related protein is involved in the phosphorylation of BRCA1 following deoxyribonucleic acid damage. Cancer Res., 60(18):5037-5039.

[24]Chen, J., Dexheimer, T.S., Ai, Y., et al., 2011. Selective and cell-active inhibitors of the USP1/UAF1 deubiquitinase complex reverse cisplatin resistance in non-small cell lung cancer cells. Chem. Biol., 18(11):1390-1400.

[25]Chen, L., Gilkes, D.M., Pan, Y., et al., 2005. ATM and Chk2-dependent phosphorylation of mdmx contribute to p53 activation after DNA damage. EMBO J., 24(19):3411-3422.

[26]Cheng, S., Schmidt-Grimminger, D.C., Murant, T., et al., 1995. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev., 9(19):2335-2349.

[27]Cheon, H., Holvey-Bates, E.G., Schoggins, J.W., et al., 2013. IFNβ-dependent increases in STAT1, STAT2, and IRF9 mediate resistance to viruses and DNA damage. EMBO J., 32(20):2751-2763.

[28]Conger, K.L., Liu, J.S., Kuo, S.R., et al., 1999. Human papillomavirus DNA replication. Interactions between the viral E1 protein and two subunits of human DNA polymerase α/PRIMASE. J. Biol. Chem., 274(5):2696-2705.

[29]Cordano, P., Gillan, V., Bratlie, S., et al., 2008. The E6E7 oncoproteins of cutaneous human papillomavirus type 38 interfere with the interferon pathway. Virology, 377(2):408-418.

[30]Cortez, D., Wang, Y., Qin, J., et al., 1999. Requirement of ATM-dependent phosphorylation of BRCA1 in the DNA damage response to double-strand breaks. Science, 286(5442):1162-1166.

[31]Cortez, D., Glick, G., Elledge, S.J., 2004. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. PNAS, 101(27):10078-10083.

[32]Coverley, D., Kenny, M.K., Lane, D.P., et al., 1992. A role for the human single-stranded DNA binding protein HSSB/RPA in an early stage of nucleotide excision repair. Nucleic Acids Res., 20(15):3873-3880.

[33]Cui, Y., Riedlinger, G., Miyoshi, K., et al., 2004. Inactivation of STAT5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol. Cell. Biol., 24(18):8037-8047.

[34]Curtin, N.J., 2012. DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer, 12(12):801-817.

[35]D'Amours, D., Jackson, S.P., 2002. The MRE11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol., 3(5):317-327.

[36]Darshan, M.S., Lucchi, J., Harding, E., et al., 2004. The L2 minor capsid protein of human papillomavirus type 16 interacts with a network of nuclear import receptors. J. Virol., 78(22):12179-12188.

[37]de Klein, A., Muijtjens, M., van Os, R., et al., 2000. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol., 10(8):479-482.

[38]Diamond, M.S., Farzan, M., 2013. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol., 13(1):46-57.

[39]Dianov, G.L., Hubscher, U., 2013. Mammalian base excision repair: the forgotten archangel. Nucleic Acids Res., 41(6):3483-3490.

[40]Dimaio, D., Petti, L.M., 2013. The E5 proteins. Virology, 445(1-2):99-114.

[41]Doan, T., Melvold, R., Viselli, S., et al., 2008. Lippincott’s Illustrated Reviews: Immunology. Wolters Kluwer Health/Lippincott Williams & Wilkins.

[42]Donaldson, M.M., Mackintosh, L.J., Bodily, J.M., et al., 2012. An interaction between human papillomavirus 16 E2 and TopBP1 is required for optimum viral DNA replication and episomal genome establishment. J. Virol., 86(23):12806-12815.

[43]Doorbar, J., Quint, W., Banks, L., et al., 2012. The biology and life-cycle of human papillomaviruses. Vaccine, 30(Suppl. 5):F55-F70.

[44]Duensing, S., Munger, K., 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res., 62(23):7075-7082.

[45]Duensing, S., Lee, L.Y., Duensing, A., et al., 2000. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. PNAS, 97(18):10002-10007.

[46]Dyson, N., Howley, P.M., Munger, K., et al., 1989. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science, 243(4893):934-937.

[47]Edwards, T.G., Helmus, M.J., Koeller, K., et al., 2013. Human papillomavirus episome stability is reduced by aphidicolin and controlled by DNA damage response pathways. J. Virol., 87(7):3979-3989.

[48]Eilon, T., Barash, I., 2011. Forced activation of Stat5 subjects mammary epithelial cells to DNA damage and preferential induction of the cellular response mechanism during proliferation. J. Cell. Physiol., 226(3):616-626.

[49]Falck, J., Mailand, N., Syljuasen, R.G., et al., 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature, 410(6830):842-847.

[50]Falck, J., Petrini, J.H., Williams, B.R., et al., 2002. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet., 30(3):290-294.

[51]Fan, X., Liu, Y., Heilman, S.A., et al., 2013. Human papillomavirus E7 induces rereplication in response to DNA damage. J. Virol., 87(2):1200-1210.

[52]Ferbeyre, G., Moriggl, R., 2011. The role of STAT5 transcription factors as tumor suppressors or oncogenes. Biochim. Biophys. Acta, 1815(1):104-114.

[53]Fernandez-Capetillo, O., Lee, A., Nussenzweig, M., et al., 2004. H2AX: the histone guardian of the genome. DNA Repair (Amst.), 3(8-9):959-967.

[54]Floyd, S.R., Pacold, M.E., Huang, Q., et al., 2013. The bromodomain protein Brd4 insulates chromatin from DNA damage signalling. Nature, 498(7453):246-250.

[55]Fradet-Turcotte, A., Moody, C., Laimins, L.A., et al., 2010. Nuclear export of human papillomavirus type 31 E1 is regulated by Cdk2 phosphorylation and required for viral genome maintenance. J. Virol., 84(22):11747-11760.

[56]Frattini, M.G., Laimins, L.A., 1994. Binding of the human papillomavirus E1 origin-recognition protein is regulated through complex formation with the E2 enhancer-binding protein. PNAS, 91(26):12398-12402.

[57]Galloway, D.A., Laimins, L.A., 2015. Human papillomaviruses: shared and distinct pathways for pathogenesis. Curr. Opin. Virol., 14:87-92.

[58]Gatei, M., Zhou, B.B., Hobson, K., et al., 2001. 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.

[59]Gauson, E.J., Donaldson, M.M., Dornan, E.S., et al., 2015. Evidence supporting a role for TopBP1 and Brd4 in the initiation but not continuation of human papillomavirus 16 E1/E2-mediated DNA replication. J. Virol., 89(9):4980-4991.

[60]Ghavidel, A., Schultz, M.C., 2001. TATA binding protein-associated CK2 transduces DNA damage signals to the RNA polymerase III transcriptional machinery. Cell, 106(5):575-584.

[61]Gillespie, K.A., Mehta, K.P., Laimins, L.A., et al., 2012. Human papillomaviruses recruit cellular DNA repair and homologous recombination factors to viral replication centers. J. Virol., 86(17):9520-9526.

[62]Goodarzi, A.A., Jonnalagadda, J.C., Douglas, P., et al., 2004. Autophosphorylation of ataxia-telangiectasia mutated is regulated by protein phosphatase 2A. EMBO J., 23(22):4451-4461.

[63]Goodarzi, A.A., Noon, A.T., Deckbar, D., et al., 2008. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell, 31(2):167-177.

[64]Groner, B., 2002. Transcription factor regulation in mammary epithelial cells. Domest. Anim. Endocrinol., 23(1-2):25-32.

[65]Gunasekharan, V., Laimins, L.A., 2013. Human papillomaviruses modulate microRNA 145 expression to directly control genome amplification. J. Virol., 87(10):6037-6043.

[66]Gunasekharan, V., Hache, G., Laimins, L., 2012. Differentiation-dependent changes in levels of C/EBPβ repressors and activators regulate human papillomavirus type 31 late gene expression. J. Virol., 86(9):5393-5398.

[67]Hartley, K.A., Alexander, K.A., 2002. 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.

[68]Hebner, C., Beglin, M., Laimins, L.A., 2007. Human papillomavirus E6 proteins mediate resistance to interferon-induced growth arrest through inhibition of p53 acetylation. J. Virol., 81(23):12740-12747.

[69]Hebner, C.M., Laimins, L.A., 2006. Human papillomaviruses: basic mechanisms of pathogenesis and oncogenicity. Rev. Med. Virol., 16(2):83-97.

[70]Heltemes-Harris, L.M., Farrar, M.A., 2012. The role of STAT5 in lymphocyte development and transformation. Curr. Opin. Immunol., 24(2):146-152.

[71]Herrero, R., Hildesheim, A., Bratti, C., et al., 2000. Population-based study of human papillomavirus infection and cervical neoplasia in rural Costa Rica. J. Natl. Cancer Inst., 92(6):464-474.

[72]Ho, G.Y., Burk, R.D., Klein, S., et al., 1995. Persistent genital human papillomavirus infection as a risk factor for persistent cervical dysplasia. J. Natl. Cancer Inst., 87(18):1365-1371.

[73]Hollingworth, R., Grand, R.J., 2015. Modulation of DNA damage and repair pathways by human tumour viruses. Viruses, 7(5):2542-2591.

[74]Hong, S., Laimins, L.A., 2013a. 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.

[75]Hong, S., Laimins, L.A., 2013b. Regulation of the life cycle of HPVs by differentiation and the DNA damage response. Future Microbiol., 8(12):1547-1557.

[76]Hong, S., Mehta, K.P., Laimins, L.A., 2011. Suppression of STAT-1 expression by human papillomaviruses is necessary for differentiation-dependent genome amplification and plasmid maintenance. J. Virol., 85(18):9486-9494.

[77]Hong, S., Dutta, A., Laimins, L.A., 2015a. The acetyltransferase Tip60 is a critical regulator of the differentiation-dependent amplification of human papillomaviruses. J. Virol., 89(8):4668-4675.

[78]Hong, S., Cheng, S., Iovane, A., et al., 2015b. STAT-5 regulates transcription of the topoisomerase IIβ-binding protein 1 (TopBP1) gene to activate the ATR pathway and promote human papillomavirus replication. MBio, 6(6):e02006-e02015.

[79]Hoskins, E.E., Morreale, R.J., Werner, S.P., et al., 2012. The fanconi anemia pathway limits human papillomavirus replication. J. Virol., 86(15):8131-8138.

[80]Howie, H.L., Koop, J.I., Weese, J., et al., 2011. Beta-HPV 5 and 8 E6 promote p300 degradation by blocking AKT/p300 association. PLoS Pathog., 7(8):e1002211.

[81]Hughes, F.J., Romanos, M.A., 1993. E1 protein of human papillomavirus is a DNA helicase/ATPase. Nucleic Acids Res., 21(25):5817-5823.

[82]Huibregtse, J.M., Scheffner, M., Howley, P.M., 1991. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J., 10(13):4129-4135.

[83]Iftner, T., Elbel, M., Schopp, B., et al., 2002. Interference of papillomavirus E6 protein with single-strand break repair by interaction with XRCC1. EMBO J., 21(17):4741-4748.

[84]Jackson, S.P., Bartek, J., 2009. The DNA-damage response in human biology and disease. Nature, 461(7267):1071-1078.

[85]Jang, M.K., Shen, K., McBride, A.A., 2014. Papillomavirus genomes associate with Brd4 to replicate at fragile sites in the host genome. PLoS Pathog., 10(5):e1004117.

[86]Janssens, S., Tschopp, J., 2006. Signals from within: the DNA-damage-induced NF-κB response. Cell Death Differ., 13(5):773-784.

[87]Jazayeri, A., Falck, J., Lukas, C., et al., 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol., 8(1):37-45.

[88]Kadaja, M., Isok-Paas, H., Laos, T., et al., 2009. Mechanism of genomic instability in cells infected with the high-risk human papillomaviruses. PLoS Pathog., 5(4):e1000397.

[89]Kajitani, N., Satsuka, A., Kawate, A., et al., 2012. Productive lifecycle of human papillomaviruses that depends upon squamous epithelial differentiation. Front. Microbiol., 3:152.

[90]Kanginakudru, S., Desmet, M., Thomas, Y., et al., 2015. Levels of the E2 interacting protein TopBP1 modulate papillomavirus maintenance stage replication. Virology, 478:135-142.

[91]Kitagawa, R., Bakkenist, C.J., McKinnon, P.J., et al., 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev., 18(12):1423-1438.

[92]Kivi, N., Greco, D., Auvinen, P., et al., 2008. Genes involved in cell adhesion, cell motility and mitogenic signaling are altered due to HPV 16 E5 protein expression. Oncogene, 27(18):2532-2541.

[93]Koganti, S., Hui-Yuen, J., McAllister, S., et al., 2014. STAT3 interrupts ATR-Chk1 signaling to allow oncovirus-mediated cell proliferation. PNAS, 111(13):4946-4951.

[94]Kumagai, A., Dunphy, W.G., 2003. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell Biol., 5(2):161-165.

[95]Kumagai, A., Lee, J., Yoo, H.Y., et al., 2006. TopBP1 activates the ATR-ATRIP complex. Cell, 124(5):943-955.

[96]Langsfeld, E.S., Bodily, J.M., Laimins, L.A., 2015. The deacetylase sirtuin 1 regulates human papillomavirus replication by modulating histone acetylation and recruitment of DNA damage factors NBS1 and RAD51 to viral genomes. PLoS Pathog., 11(9):e1005181.

[97]Lee, J., Kumagai, A., Dunphy, W.G., 2001. Positive regulation of Wee1 by Chk1 and 14-3-3 proteins. Mol. Biol. Cell, 12(3):551-563.

[98]Lee, J.H., Paull, T.T., 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science, 304(5667):93-96.

[99]Lehoux, M., Gagnon, D., Archambault, J., 2014. E1-mediated recruitment of a UAF1-USP deubiquitinase complex facilitates human papillomavirus DNA replication. J. Virol., 88(15):8545-8555.

[100]Liao, S., Deng, D., Zhang, W., et al., 2013. Human papillomavirus 16/18 E5 promotes cervical cancer cell proliferation, migration and invasion in vitro and accelerates tumor growth in vivo. Oncol. Rep., 29(1):95-102.

[101]Liu, K., Lin, F.T., Ruppert, J.M., et al., 2003. Regulation of E2F1 by BRCT domain-containing protein TopBP1. Mol. Cell. Biol., 23(9):3287-3304.

[102]Liu, Q., Guntuku, S., Cui, X.S., et al., 2000. Chk1 is an essential kinase that is regulated by Atr and required for the G2/M DNA damage checkpoint. Genes Dev., 14(12):1448-1459.

[103]Longworth, M.S., Laimins, L.A., 2004. Pathogenesis of human papillomaviruses in differentiating epithelia. Microbiol. Mol. Biol. Rev., 68(2):362-372.

[104]Longworth, M.S., Wilson, R., Laimins, L.A., 2005. HPV31 E7 facilitates replication by activating E2F2 transcription through its interaction with HDACs. EMBO J., 24(10):1821-1830.

[105]Lord, C.J., Ashworth, A., 2012. The DNA damage response and cancer therapy. Nature, 481(7381):287-294.

[106]Matsuoka, S., Huang, M., Elledge, S.J., 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science, 282(5395):1893-1897.

[107]Matt, S., Hofmann, T.G., 2016. The DNA damage-induced cell death response: a roadmap to kill cancer cells. Cell. Mol. Life Sci., 73(15):2829-2850.

[108]Maya, R., Balass, M., Kim, S.T., et al., 2001. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev., 15(9):1067-1077.

[109]McBride, A.A., 2013. The papillomavirus E2 proteins. Virology, 445(1-2):57-79.

[110]McFadden, K., Luftig, M.A., 2013. Interplay between DNA tumor viruses and the host DNA damage response. Curr. Top Microbiol. Immunol., 371:229-257.

[111]McKinney, C.C., Hussmann, K.L., McBride, A.A., 2015. The role of the DNA damage response throughout the papillomavirus life cycle. Viruses, 7(5):2450-2469.

[112]McPhillips, M.G., Oliveira, J.G., Spindler, J.E., et al., 2006. Brd4 is required for E2-mediated transcriptional activation but not genome partitioning of all papillomaviruses. J. Virol., 80(19):9530-9543.

[113]Mehta, K., Gunasekharan, V., Satsuka, A., et al., 2015. Human papillomaviruses activate and recruit SMC1 cohesin proteins for the differentiation-dependent life cycle through association with ctcf insulators. PLoS Pathog., 11(4):e1004763.

[114]Melar-New, M., Laimins, L.A., 2010. Human papillomaviruses modulate expression of microRNA 203 upon epithelial differentiation to control levels of p63 proteins. J. Virol., 84(10):5212-5221.

[115]Mighty, K.K., Laimins, L.A., 2011. p63 is necessary for the activation of human papillomavirus late viral functions upon epithelial differentiation. J. Virol., 85(17):8863-8869.

[116]Miller, K.M., Tjeertes, J.V., Coates, J., et al., 2010. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol., 17(99):1144-1151.

[117]Moiseeva, O., Mallette, F.A., Mukhopadhyay, U.K., et al., 2006. DNA damage signaling and p53-dependent senescence after prolonged β-interferon stimulation. Mol. Biol. Cell, 17(4):1583-1592.

[118]Moody, C.A., Laimins, L.A., 2009. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog., 5(10):e1000605.

[119]Moody, C.A., Laimins, L.A., 2010. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer, 10(8):550-560.

[120]Moody, C.A., Fradet-Turcotte, A., Archambault, J., et al., 2007. Human papillomaviruses activate caspases upon epithelial differentiation to induce viral genome amplification. PNAS, 104(49):19541-19546.

[121]Munger, K., Howley, P.M., 2002. Human papillomavirus immortalization and transformation functions. Virus Res., 89(2):213-228.

[122]Munger, K., Werness, B.A., Dyson, N., et al., 1989. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J., 8(13):4099-4105.

[123]Myers, J.S., Cortez, D., 2006. Rapid activation of ATR by ionizing radiation requires ATM and MRE11. J. Biol. Chem., 281(14):9346-9350.

[124]Myers, K., Gagou, M.E., Zuazua-Villar, P., et al., 2009. ATR and Chk1 suppress a caspase-3-dependent apoptotic response following DNA replication stress. PLoS Genet., 5(1):e1000324.

[125]Nakahara, T., Tanaka, K., Ohno, S., et al., 2015. Activation of NF-κB by human papillomavirus 16 E1 limits E1-dependent viral replication through degradation of E1. J. Virol., 89(9):5040-5059.

[126]Nelson, L.M., Rose, R.C., Moroianu, J., 2002. Nuclear import strategies of high risk HPV16 L1 major capsid protein. J. Biol. Chem., 277(26):23958-23964.

[127]Nguyen, C.L., McLaughlin-Drubin, M.E., Munger, K., 2008. Delocalization of the microtubule motor dynein from mitotic spindles by the human papillomavirus E7 oncoprotein is not sufficient for induction of multipolar mitoses. Cancer Res., 68(21):8715-8722.

[128]Nuovo, G.J., Wu, X., Volinia, S., et al., 2010. Strong inverse correlation between microRNA-125b and human papillomavirus DNA in productive infection. Diagn. Mol. Pathol., 19(3):135-143.

[129]O'Connor, M., Bernard, H.U., 1995. Oct-1 activates the epithelial-specific enhancer of human papillomavirus type 16 via a synergistic interaction with NFI at a conserved composite regulatory element. Virology, 207(1):77-88.

[130]O'Connor, M.J., 2015. Targeting the DNA damage response in cancer. Mol. Cell, 60(4):547-560.

[131]O'Driscoll, M., Ruiz-Perez, V.L., Woods, C.G., et al., 2003. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in seckel syndrome. Nat. Genet., 33(4):497-501.

[132]Offord, E.A., Beard, P., 1990. 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.

[133]Oliveira, J.G., Colf, L.A., McBride, A.A., 2006. Variations in the association of papillomavirus E2 proteins with mitotic chromosomes. PNAS, 103(4):1047-1052.

[134]Park, J.S., Kim, E.J., Kwon, H.J., et al., 2000. Inactivation of interferon regulatory factor-1 tumor suppressor protein by HPV E7 oncoprotein. Implication for the E7-mediated immune evasion mechanism in cervical carcinogenesis. J. Biol. Chem., 275(10):6764-6769.

[135]Patel, D., Huang, S.M., Baglia, L.A., et al., 1999. The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J., 18(18):5061-5072.

[136]Pearl, L.H., Schierz, A.C., Ward, S.E., et al., 2015. Therapeutic opportunities within the DNA damage response. Nat. Rev. Cancer, 15(3):166-180.

[137]Pedroza-Torres, A., Lopez-Urrutia, E., Garcia-Castillo, V., et al., 2014. MicroRNAs in cervical cancer: evidences for a miRNA profile deregulated by hpv and its impact on radio-resistance. Molecules, 19(5):6263-6281.

[138]Poddar, A., Reed, S.C., McPhillips, M.G., et al., 2009. The human papillomavirus type 8 E2 tethering protein targets the ribosomal DNA loci of host mitotic chromosomes. J. Virol., 83(2):640-650.

[139]Reinson, T., Toots, M., Kadaja, M., et al., 2013. 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.

[140]Rincon-Orozco, B., Halec, G., Rosenberger, S., et al., 2009. Epigenetic silencing of interferon-κ in human papillomavirus type 16-positive cells. Cancer Res., 69(22):8718-8725.

[141]Ronco, L.V., Karpova, A.Y., Vidal, M., et al., 1998. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev., 12(13):2061-2072.

[142]Sakakibara, N., Mitra, R., McBride, A.A., 2011. The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J. Virol., 85(17):8981-8995.

[143]Satsuka, A., Mehta, K., Laimins, L., 2015. p38MAPK and MK2 pathways are important for the differentiation-dependent human papillomavirus life cycle. J. Virol., 89(3):1919-1924.

[144]Scheffner, M., Werness, B.A., Huibregtse, J.M., et al., 1990. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell, 63(6):1129-1136.

[145]Scheffner, M., Huibregtse, J.M., Vierstra, R.D., et al., 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell, 75(3):495-505.

[146]Sedman, J., Stenlund, A., 1995. Co-operative interaction between the initiator E1 and the transcriptional activator E2 is required for replicator specific DNA replication of bovine papillomavirus in vivo and in vitro. EMBO J., 14(24):6218-6228.

[147]Seebode, C., Lehmann, J., Emmert, S., 2016. Photocarcinogenesis and skin cancer prevention strategies. Anticancer Res., 36(3):1371-1378.

[148]Shreeram, S., Demidov, O.N., Hee, W.K., et al., 2006. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol. Cell, 23(5):757-764.

[149]Smith, J., Tho, L.M., Xu, N., et al., 2010. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res., 108:73-112.

[150]Smith, J.A., White, E.A., Sowa, M.E., et al., 2010. Genome-wide siRNA screen identifies SMCX, EP400, and Brd4 as E2-dependent regulators of human papillomavirus oncogene expression. PNAS, 107(8):3752-3757.

[151]Song, S., Gulliver, G.A., Lambert, P.F., 1998. Human papillomavirus type 16 E6 and E7 oncogenes abrogate radiation-induced DNA damage responses in vivo through p53-dependent and p53-independent pathways. PNAS, 95(5):2290-2295.

[152]Sorensen, C.S., Hansen, L.T., Dziegielewski, J., et al., 2005. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol., 7(2):195-201.

[153]Spardy, N., Duensing, A., Charles, D., et al., 2007. The human papillomavirus type 16 E7 oncoprotein activates the Fanconi anemia (FA) pathway and causes accelerated chromosomal instability in FA cells. J. Virol., 81(23):13265-13270.

[154]Spardy, N., Duensing, A., Hoskins, E.E., et al., 2008. HPV-16 E7 reveals a link between DNA replication stress, fanconi anemia D2 protein, and alternative lengthening of telomere-associated promyelocytic leukemia bodies. Cancer Res., 68(23):9954-9963.

[155]Spardy, N., Covella, K., Cha, E., et al., 2009. Human papillomavirus 16 E7 oncoprotein attenuates DNA damage checkpoint control by increasing the proteolytic turnover of claspin. Cancer Res., 69(17):7022-7029.

[156]Sperka, T., Wang, J., Rudolph, K.L., 2012. DNA damage checkpoints in stem cells, ageing and cancer. Nat. Rev. Mol. Cell Biol., 13(9):579-590.

[157]Srivenugopal, K.S., Ali-Osman, F., 2002. The DNA repair protein, O6-methylguanine-DNA methyltransferase is a proteolytic target for the E6 human papillomavirus oncoprotein. Oncogene, 21(38):5940-5945.

[158]Stanley, M.A., 2012. Epithelial cell responses to infection with human papillomavirus. Clin. Microbiol. Rev., 25(2):215-222.

[159]Steger, G., Corbach, S., 1997. Dose-dependent regulation of the early promoter of human papillomavirus type 18 by the viral E2 protein. J. Virol., 71(1):50-58.

[160]Stubenrauch, F., Hummel, M., Iftner, T., et al., 2000. The E8^E2C protein, a negative regulator of viral transcription and replication, is required for extrachromosomal maintenance of human papillomavirus type 31 in keratinocytes. J. Virol., 74(3):1178-1186.

[161]Stunkel, W., Bernard, H.U., 1999. The chromatin structure of the long control region of human papillomavirus type 16 represses viral oncoprotein expression. J. Virol., 73(3):1918-1930.

[162]Sun, Y., Jiang, X., Chen, S., et al., 2005. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. PNAS, 102(37):13182-13187.

[163]Taniguchi, T., Garcia-Higuera, I., Xu, B., et al., 2002. Convergence of the fanconi anemia and ataxia telangiectasia signaling pathways. Cell, 109(4):459-472.

[164]Thomas, J.T., Hubert, W.G., Ruesch, M.N., et al., 1999. Human papillomavirus type 31 oncoproteins E6 and E7 are required for the maintenance of episomes during the viral life cycle in normal human keratinocytes. PNAS, 96(15):8449-8454.

[165]Thomas, M., Narayan, N., Pim, D., et al., 2008. Human papillomaviruses, cervical cancer and cell polarity. Oncogene, 27(55):7018-7030.

[166]Thomas, M.C., Chiang, C.M., 2005. E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Mol. Cell, 17(2):251-264.

[167]Thurn, K.T., Thomas, S., Raha, P., et al., 2013. Histone deacetylase regulation of ATM-mediated DNA damage signaling. Mol. Cancer Ther., 12(10):2078-2087.

[168]Walker, M., Black, E.J., Oehler, V., et al., 2009. Chk1 C-terminal regulatory phosphorylation mediates checkpoint activation by de-repression of Chk1 catalytic activity. Oncogene, 28(24):2314-2323.

[169]Wallace, N.A., Galloway, D.A., 2014. Manipulation of cellular DNA damage repair machinery facilitates propagation of human papillomaviruses. Semin. Cancer Biol., 26:30-42.

[170]Wallace, N.A., Galloway, D.A., 2015. Novel functions of the human papillomavirus E6 oncoproteins. Annu. Rev. Virol., 2(1):403-423.

[171]Wallace, N.A., Robinson, K., Howie, H.L., et al., 2012. HPV 5 and 8 E6 abrogate ATR activity resulting in increased persistence of UVB induced DNA damage. PLoS Pathog., 8(7):e1002807.

[172]Wallace, N.A., Gasior, S.L., Faber, Z.J., et al., 2013. HPV 5 and 8 E6 expression reduces ATM protein levels and attenuates LINE-1 retrotransposition. Virology, 443(1):69-79.

[173]Wallace, N.A., Robinson, K., Galloway, D.A., 2014. Beta human papillomavirus E6 expression inhibits stabilization of p53 and increases tolerance of genomic instability. J. Virol., 88(11):6112-6127.

[174]Wallace, N.A., Robinson, K., Howie, H.L., et al., 2015. β-HPV 5 and 8 E6 disrupt homology dependent double strand break repair by attenuating BRCA1 and BRCA2 expression and foci formation. PLoS Pathog., 11(3):e1004687.

[175]Wan, G., Mathur, R., Hu, X., et al., 2011. miRNA response to DNA damage. Trends Biochem. Sci., 36(9):478-484.

[176]Wang, X., Wang, H.K., Li, Y., et al., 2014. MicroRNAs are biomarkers of oncogenic human papillomavirus infections. PNAS, 111(11):4262-4267.

[177]Wang, Y., Taniguchi, T., 2013. MicroRNAs and DNA damage response: implications for cancer therapy. Cell Cycle, 12(1):32-42.

[178]White, D.E., Negorev, D., Peng, H., et al., 2006. KAP1, a novel substrate for PIKK family members, colocalizes with numerous damage response factors at DNA lesions. Cancer Res., 66(24):11594-11599.

[179]Wise-Draper, T.M., Wells, S.I., 2008. Papillomavirus E6 and E7 proteins and their cellular targets. Front. Biosci., 13:1003-1017.

[180]Wohlbold, L., Merrick, K.A., De, S., et al., 2012. Chemical genetics reveals a specific requirement for Cdk2 activity in the DNA damage response and identifies Nbs1 as a Cdk2 substrate in human cells. PLoS Genet., 8(8):e1002935.

[181]Wu, S., Shi, Y., Mulligan, P., et al., 2007. A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat. Struct. Mol. Biol., 14(12):1165-1172.

[182]Wu, S.Y., Lee, A.Y., Hou, S.Y., et al., 2006. Brd4 links chromatin targeting to HPV transcriptional silencing. Genes Dev., 20(17):2383-2396.

[183]Yao, Z., Cui, Y., Watford, W.T., et al., 2006. STAT5a/b are essential for normal lymphoid development and differentiation. PNAS, 103(4):1000-1005.

[184]Yarden, R.I., Pardo-Reoyo, S., Sgagias, M., et al., 2002. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet., 30(3):285-289.

[185]Zhang, R., Zhu, L., Zhang, L., et al., 2016. PTEN enhances G2/M arrest in etoposide-treated MCF7 cells through activation of the ATM pathway. Oncol. Rep., 35(5):2707-2714.

[186]Zhang, W., Hong, S., Maniar, K.P., et al., 2016. KLF13 regulates the differentiation-dependent human papillomavirus life cycle in keratinocytes through STAT5 and IL-8. Oncogene, 35:5565-5575.

[187]Zhang, Y., Cho, Y.Y., Petersen, B.L., et al., 2003. Ataxia telangiectasia mutated proteins, mapks, and RSK2 are involved in the phosphorylation of STAT3. J. Biol. Chem., 278(15):12650-12659.

[188]Zhang, Y., Fan, S., Meng, Q., et al., 2005. BRCA1 interaction with human papillomavirus oncoproteins. J. Biol. Chem., 280(39):33165-33177.

[189]Zhao, H., Jin, S., Fan, F., et al., 2000. Activation of the transcription factor Oct-1 in response to DNA damage. Cancer Res., 60(22):6276-6280.

[190]Zhou, B.B., Chaturvedi, P., Spring, K., et al., 2000. Caffeine

[191]abolishes the mammalian G2/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem., 275(14):10342-10348.

[192]Ziv, Y., Bielopolski, D., Galanty, Y., et al., 2006. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol., 8(8):870-876.

[193]Zou, L., Elledge, S.J., 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300(5625):1542-1548.

[194]Zur Hausen, H., 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer, 2(5):342-350.

[195]Zur Hausen, H., 2009. Papillomaviruses in the causation of human cancers—a brief historical account. Virology, 384(2):260-265.

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Cosaert@Merck KGaA<jan.cosaert@merckgroup.com>

2017-03-13 15:44:27

Content appears a very usefull summary on this pathway

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952276; Fax: +86-571-87952331; E-mail: jzus@zju.edu.cn
Copyright © 2000 - Journal of Zhejiang University-SCIENCE