Human Papillomaviruses Activate and Recruit SMC1 Cohesin Proteins for the Differentiation-Dependent Life Cycle through Association with CTCF Insulators

PLoS Pathogens

Volumn 11, Issue 4, 2015, Pages

  Mehta, Kavi ^a   Gunasekharan, Vignesh ^a   Satsuka, Ayano ^a   Laimins, Laimonis A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; COHESIN; PROTEIN P53; SMC1 COHESIN PROTEIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; CCCTC-BINDING FACTOR; CELL CYCLE PROTEIN; NONHISTONE PROTEIN; REPRESSOR PROTEIN; STRUCTURAL MAINTENANCE OF CHROMOSOME PROTEIN 1;

ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA DAMAGE; GENE AMPLIFICATION; GENETIC REGULATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; KERATINOCYTE; LIFE CYCLE; NONHUMAN; NORTHERN BLOTTING; PLASMID; PROTEIN ANALYSIS; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS; SOUTHERN BLOTTING; VIRAL GENE DELIVERY SYSTEM; VIRUS REPLICATION; WART VIRUS; WESTERN BLOTTING; CELL CULTURE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; IMMUNOBLOTTING; METABOLISM; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTION; PHYSIOLOGY; VIROLOGY; VIRUS ACTIVATION;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRIDAE;

CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; KERATINOCYTES; MUTAGENESIS, SITE-DIRECTED; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; REPRESSOR PROTEINS; TRANSFECTION; VIRUS ACTIVATION; VIRUS REPLICATION;

EID: 84929497859     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004763     Document Type: Article

References (52)

1. Hausen zur H, Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer. Nature Publishing Group; 2002 May 1;2(5):342–50. 12044010
2. Moody CA, Laimins LA, Human papillomavirus oncoproteins:pathways to transformation. Nature Publishing Group. Nature Publishing Group; 2010 Jul 1;10(8):550–60.
3. Howley PM, Lowy DR, Knipe DM, Howley PM, Papillomaviruses. 5 ed. Philadelphia: Lippincott Williams & Wilkins; 2007. 56 p.
4. McBride AA, Sakakibara N, Stepp WH, Jang MK, Hitchhiking on host chromatin: how papillomaviruses persist. Biochimica et Biophysica Acta (BBA)—Gene Regulatory Mechanisms. 2012 Jul;1819(7):820–5. doi: 10.1016/j.bbagrm.2012.01.011 22306660
5. Sakakibara N, Chen D, McBride AA, Papillomaviruses use recombination-dependent replication to vegetatively amplify their genomes in differentiated cells. PLoS Pathog. 2013 Jul;9(7):e1003321. doi: 10.1371/journal.ppat.1003321 23853576
6. Banerjee NS, Wang H-K, Broker TR, Chow LT, Human papillomavirus (HPV) E7 induces prolonged G2 following S phase reentry in differentiated human keratinocytes. J Biol Chem. 2011 Apr 29;286(17):15473–82. doi: 10.1074/jbc.M110.197574 21321122
7. Grassmann K, Rapp B, Maschek H, Petry KU, Iftner T, Identification of a differentiation-inducible promoter in the E7 open reading frame of human papillomavirus type 16 (HPV-16) in raft cultures of a new cell line containing high copy numbers of episomal HPV-16 DNA. J Virol. 1996 Apr;70(4):2339–49. 8642661
8. Hummel M, Hudson JB, Laimins LA. Differentiation-Induced and Constitutive Transcription of Human Papillomavirus Type 31b in Cell Lines Containing Viral Episomes. J Virol. 1992 Oct 1;(Oct. 1992):6070–80.
9. Kastan MB, Lim DS, The many substrates and functions of ATM. Nat Rev Mol Cell Biol. 2000 Dec;1(3):179–86. 11252893
10. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, Hurov KE, Luo J, et al. ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage. Science. 2007 May 25;316(5828):1160–6. 17525332
11. Kitagawa R, Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes & Development. 2004 Jun 15;18(12):1423–38.
12. Yazdi PT, SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes & Development. 2002 Mar 1;16(5):571–82.
13. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science. 1998 Sep 11;281(5383):1677–9. 9733515
14. Kim ST, Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes & Development. 2002 Mar 1;16(5):560–70.
15. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A, H2AX: the histone guardian of the genome. DNA Repair (Amst). 2004 Aug;3(8–9):959–67.
16. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM, A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Current Biology. 2000 Aug;10(15):886–95. 10959836
17. Hirano T, SMC proteins and chromosome mechanics: from bacteria to humans. Philosophical Transactions of the Royal Society B: Biological Sciences. 2005 Mar 29;360(1455):507–14. 15897176
18. Jessberger R, Riwar B, Baechtold H, Akhmedov AT, SMC proteins constitute two subunits of the mammalian recombination complex RC-1. EMBO J. 1996 Aug 1;15(15):4061–8. 8670910
19. Moody CA, Laimins LA, Galloway D, Human Papillomaviruses Activate the ATM DNA Damage Pathway for Viral Genome Amplification upon Differentiation. PLoS Pathog. 2009 Oct 2;5(10):e1000605. doi: 10.1371/journal.ppat.1000605 19798429
20. Gillespie KA, Mehta KP, Laimins LA, Moody CA, Human papillomaviruses recruit cellular DNA repair and homologous recombination factors to viral replication centers. J Virol. 2012 Sep;86(17):9520–6. doi: 10.1128/JVI.00247-12 22740399
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. 2009 Apr;5(4):e1000397. doi: 10.1371/journal.ppat.1000397 19390600
22. Ström L, Lindroos HB, Shirahige K, Sjogren C, Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell. 2004 Dec 22;16(6):1003–15. 15610742
23. Schär P, Fäsi M, Jessberger R. SMC1 coordinates DNA double-strand break repair pathways. Nucleic Acids Research. 2004.
24. Bauerschmidt C, Woodcock M, Stevens DL, Hill MA, Rothkamm K, Helleday T, Cohesin phosphorylation and mobility of SMC1 at ionizing radiation-induced DNA double-strand breaks in human cells. Exp Cell Res. 2011 Feb 1;317(3):330–7. doi: 10.1016/j.yexcr.2010.10.021 21056556
25. Sjogren C, Nasmyth K, Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Current Biology. London, UK: Current Biology Ltd., c1991; 2001;11(12):991–5. 11448778
26. Golding SE, Rosenberg E, Valerie N, Hussaini I, Frigerio M, Cockcroft XF, et al. Improved ATM kinase inhibitor KU-60019 radiosensitizes glioma cells, compromises insulin, AKT and ERK prosurvival signaling, and inhibits migration and invasion. Molecular Cancer Therapeutics. 2009 Oct 12;8(10):2894–902. doi: 10.1158/1535-7163.MCT-09-0519 19808981
27. Stokes MP, Rush J, Macneill J, Ren JM, Sprott K, Nardone J, et al. Profiling of UV-induced ATM/ATR signaling pathways. Proc Natl Acad Sci USA. 2007 Dec 11;104(50):19855–60. 18077418
28. Söderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius K-J, Jarvius J, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006 Dec;3(12):995–1000. 17072308
29. Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature. 2008 Jan 30;451(7180):796–801. doi: 10.1038/nature06634 18235444
30. Gomes NP, Espinosa JM, Gene-specific repression of the p53 target gene PUMA via intragenic CTCF-Cohesin binding. Genes & Development. 2010 May 15;24(10):1022–34.
31. Ren L, Shi M, Wang Y, Yang Z, Wang X, Zhao Z, CTCF and cohesin cooperatively mediate the cell-type specific interchromatin interaction between Bcl11b and Arhgap6 loci. Mol Cell Biochem. 2011 Sep 23;360(1–2):243–51.
32. Sun M, Nishino T, Marko JF, The SMC1-SMC3 cohesin heterodimer structures DNA through supercoiling-dependent loop formation. Nucleic Acids Research. 2013 Jul 1;41(12):6149–60. doi: 10.1093/nar/gkt303 23620281
33. Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, et al. Cohesins Functionally Associate with CTCF on Mammalian Chromosome Arms. Cell. 2008 Feb;132(3):422–33. doi: 10.1016/j.cell.2008.01.011 18237772
34. Merkenschlager M, Odom DT, CTCF and cohesin: linking gene regulatory elements with their targets. Cell. 2013 Mar 14;152(6):1285–97. doi: 10.1016/j.cell.2013.02.029 23498937
35. Feeney KM, Wasson CW, Parish JL, Cohesin: a regulator of genome integrity and gene expression. Biochem J. 2010 May 13;428(2):147–61. doi: 10.1042/BJ20100151 20462401
36. Anacker DC, Gautam D, Gillespie KA, Chappell WH, Moody CA, Productive replication of human papillomavirus 31 requires DNA repair factor Nbs1. J Virol. 2014 Aug;88(15):8528–44. doi: 10.1128/JVI.00517-14 24850735
37. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll JS, et al. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Research. 2010 May;20(5):578–88. doi: 10.1101/gr.100479.109 20219941
38. Zlatanova J, Caiafa P, CTCF and its protein partners: divide and rule? Journal of Cell Science. 2009 May 1;122(Pt 9):1275–84. doi: 10.1242/jcs.039990 19386894
39. Lobanenkov VV, Nicolas RH, Adler VV, Paterson H, Klenova EM, Polotskaja AV, et al. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5'-flanking sequence of the chicken c-myc gene. Oncogene. 1990 Dec;5(12):1743–53. 2284094
40. Kang H, Wiedmer A, Yuan Y, Robertson E, Lieberman PM, Coordination of KSHV latent and lytic gene control by CTCF-cohesin mediated chromosome conformation. PLoS Pathog. 2011 Aug;7(8):e1002140. doi: 10.1371/journal.ppat.1002140 21876668
41. Tempera I, Klichinsky M, Lieberman PM, EBV latency types adopt alternative chromatin conformations. PLoS Pathog. 2011 Jul;7(7):e1002180. doi: 10.1371/journal.ppat.1002180 21829357
42. Tempera I, Wiedmer A, Dheekollu J, Lieberman PM, CTCF prevents the epigenetic drift of EBV latency promoter Qp. PLoS Pathog. 2010;6(8):e1001048. doi: 10.1371/journal.ppat.1001048 20730088
43. Parish JL, Bean AM, Park RB, Androphy EJ, ChlR1 is required for loading papillomavirus E2 onto mitotic chromosomes and viral genome maintenance. Mol Cell. 2006 Dec 28;24(6):867–76. 17189189
44. 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. 1997 Oct;71(10):7167–79. 9311789
45. Sowd GA, Li NY, Fanning E, ATM and ATR activities maintain replication fork integrity during SV40 chromatin replication. PLoS Pathog. 2013;9(4):e1003283. doi: 10.1371/journal.ppat.1003283 23592994
46. Halbert CL, Demers GW, Galloway DA. The E6 and E7 genes of human papillomavirus type 6 have weak immortalizing activity in human epithelial cells. J Virol. 1992.
47. Longworth MS, Laimins LA, The binding of histone deacetylases and the integrity of zinc finger-like motifs of the E7 protein are essential for the life cycle of human papillomavirus type 31. J Virol. 2004 Apr;78(7):3533–41. 15016876
48. 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 USA. 2007 Dec 4;104(49):19541–6. 18048335
49. Thomas JT, Hubert WG, Ruesch MN, Laimins LA, Human papillomavirus type 31 oncoproteins E6 and E7 are required for the maintenance of episomes during the viral life cycle in normal human keratinocytes. Proceedings of the National Academy of Sciences. 1999 Jul 20;96(15):8449–54. 10411895
50. Wong P-P, Pickard A, McCance DJ, p300 alters keratinocyte cell growth and differentiation through regulation of p21(Waf1/CIP1). PLoS ONE. 2010;5(1):e8369. doi: 10.1371/journal.pone.0008369 20084294
51. McCance DJ, Kopan R, Fuchs E, Laimins LA, Human papillomavirus type 16 alters human epithelial cell differentiation in vitro. Proceedings of the National Academy of Sciences. 1988 Oct;85(19):7169–73. 2459699
52. Fehrmann F, Klumpp DJ, Laimins LA, Human papillomavirus type 31 E5 protein supports cell cycle progression and activates late viral functions upon epithelial differentiation. J Virol. 2003 Mar;77(5):2819–31. 12584305