Levels of the E2 interacting protein TopBP1 modulate papillomavirus maintenance stage replication

Virology

Volumn 478, Issue , 2015, Pages 129-136

  Kanginakudru, Sriramana ^a   DeSmet, Marsha ^a   Thomas, Yanique ^a   Morgan, Iain M ^b   Androphy, Elliot J ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

BPV; Cell cycle; Copy number; E2; HPV; Papillomavirus; Replication; TopBP1

Indexed keywords

DNA TOPOISOMERASE; GENOMIC DNA; PROTEIN TOPBP1; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNA BINDING PROTEIN; E2 PROTEIN, BOVINE PAPILLOMAVIRUS; E2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; E2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 31; ONCOPROTEIN; TOPBP1 PROTEIN, MOUSE; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL SURVIVAL; CONTROLLED STUDY; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 31; MITOSIS; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS GENOME; VIRUS REPLICATION; ANIMAL; CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MOUSE; PAPILLOMAVIRIDAE; PHYSIOLOGY;

ANIMALS; CARRIER PROTEINS; CELL LINE; DNA-BINDING PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84925493564     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.01.011     Document Type: Article

References (62)

1. Abbate E.A., Berger J.M., Botchan M.R. The X-ray structure of the papillomavirus helicase in complex with its molecular matchmaker E2. Genes Dev. 2004, 18:1981-1996.
2. Androphy E.J., Lowy D.R., Schiller J.T. Bovine papillomavirus E2 trans-activating gene product binds to specific sites in papillomavirus DNA. Nature 1987, 325:70-73.
3. Balestrini A., Cosentino C., Errico A., Garner E., Costanzo V. GEMC1 is a TopBP1-interacting protein required for chromosomal DNA replication. Nat. Cell Biol. 2010, 12:484-491.
4. Banerjee N.S., Wang H.K., Broker T.R., Chow L.T. Human papillomavirus (HPV) E7 induces prolonged G2 following S phase reentry in differentiated human keratinocytes. J. Biol. Chem. 2011, 286:15473-15482.
5. Bedell M.A., Hudson J.B., Golub T.R., Turyk M.E., Hosken M., Wilbanks G.D., Laimins L.A. Amplification of human papillomavirus genomes in vitro is dependent on epithelial differentiation. J. Virol. 1991, 65:2254-2260.
6. Blackford A.N., Patel R.N., Forrester N.A., Theil K., Groitl P., Stewart G.S., Taylor A.M., Morgan I.M., Dobner T., Grand R.J., Turnell A.S. Adenovirus 12 E4orf6 inhibits ATR activation by promoting TOPBP1 degradation. Proc. Natl. Acad. Sci. USA 2010, 107:12251-12256.
7. Boner W., Taylor E.R., Tsirimonaki E., Yamane K., Campo M.S., Morgan I.M. A Functional interaction between the human papillomavirus 16 transcription/replication factor E2 and the DNA damage response protein TopBP1. J.Biol. Chem. 2002, 277:22297-22303.
8. Chiang C.M., Ustav M., Stenlund A., Ho T.F., Broker T.R., Chow L.T. Viral E1 and E2 proteins support replication of homologous and heterologous papillomaviral origins. Proc. Natl. Acad. Sci. USA 1992, 89:5799-5803.
9. De Geest K., Turyk M.E., Hosken M.I., Hudson J.B., Laimins L.A., Wilbanks G.D. Growth and differentiation of human papillomavirus type 31b positive human cervical cell lines. Gynecol. Oncol. 1993, 49:303-310.
10. Donaldson M.M., Boner W., Morgan I.M. TopBP1 regulates human papillomavirus type 16 E2 interaction with chromatin. J. Virol. 2007, 81:4338-4342.
11. Donaldson M.M., Mackintosh L.J., Bodily J.M., Dornan E.S., Laimins L.A., Morgan I.M. An interaction between human papillomavirus 16 E2 and TopBP1 is required for optimum viral DNA replication and episomal genome establishment. J. Virol. 2012, 86:12806-12815.
12. Duursma A.M., Driscoll R., Elias J.E., Cimprich K.A. A role for the MRN complex in ATR activation via TOPBP1 recruitment. Mol. Cell 2013, 50:116-122.
13. Edwards T.G., Vidmar T.J., Koeller K., Bashkin J.K., Fisher C. DNA damage repair genes controlling human papillomavirus (HPV) episome levels under conditions of stability and extreme instability. PloS ONE 2013, 8:e75406.
14. Feijoo C., Hall-Jackson C., Wu R., Jenkins D., Leitch J., Gilbert D.M., Smythe C. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J. Cell Biol. 2001, 154:913-923.
15. Fradet-Turcotte A., Bergeron-Labrecque F., Moody C.A., Lehoux M., Laimins L.A., Archambault J. Nuclear accumulation of the papillomavirus E1 helicase blocks S-phase progression and triggers an ATM-dependent DNA damage response. J. Virol. 2011, 85:8996-9012.
16. Fradet-Turcotte A., Moody C., Laimins L.A., Archambault J. Nuclear export of human papillomavirus type 31 E1 is regulated by Cdk2 phosphorylation and required for viral genome maintenance. J. Virol. 2010, 84:11747-11760.
17. Fradet-Turcotte A., Morin G., Lehoux M., Bullock P.A., Archambault J. Development of quantitative and high-throughput assays of polyomavirus and papillomavirus DNA replication. Virology 2010, 399:65-76.
18. Garcia V., Furuya K., Carr A.M. Identification and functional analysis of TopBP1 and its homologs. DNA Repair 2005, 4:1227-1239.
19. Grossel M.J., Sverdrup F., Breiding D.E., Androphy E.J. Transcriptional activation function is not required for stimulation of DNA replication by bovine papillomavirus type 1 E2. J. Virol. 1996, 70:7264-7269.
20. Heilman S.A., Nordberg J.J., Liu Y., Sluder G., Chen J.J. Abrogation of the postmitotic checkpoint contributes to polyploidization in human papillomavirus E7-expressing cells. J. Virol. 2009, 83:2756-2764.
21. Hoskins E.E., Morreale R.J., Werner S.P., Higginbotham J.M., Laimins L.A., Lambert P.F., Brown D.R., Gillison M.L., Nuovo G.J., Witte D.P., Kim M.O., Davies S.M., Mehta P.A., Butsch Kovacic M., Wikenheiser-Brokamp K.A., Wells S.I. The fanconi anemia pathway limits human papillomavirus replication. J. Virol. 2012, 86:8131-8138.
22. Howley P.M. Papillomaviridae: The Viruses And Their Replication 1996.
23. Hughes F.J., Romanos M.A. E1 protein of human papillomavirus is a DNA helicase/ATPase. Nucleic Acids Res. 1993, 21:5817-5823.
24. Jeon Y., Ko E., Lee K.Y., Ko M.J., Park S.Y., Kang J., Jeon C.H., Lee H., Hwang D.S. TopBP1 deficiency causes an early embryonic lethality and induces cellular senescence in primary cells. J. Biol. Chem. 2011, 286:5414-5422.
25. Jeon Y., Lee K.Y., Ko M.J., Lee Y.S., Kang S., Hwang D.S. Human TopBP1 participates in cyclin E/CDK2 activation and preinitiation complex assembly during G1/S transition. J. Biol. Chem. 2007, 282:14882-14890.
26. Kim J.E., McAvoy S.A., Smith D.I., Chen J. Human TopBP1 ensures genome integrity during normal S phase. Mol. Cell. Biol. 2005, 25:10907-10915.
27. King L.E., Fisk J.C., Dornan E.S., Donaldson M.M., Melendy T., Morgan I.M. Human papillomavirus E1 and E2 mediated DNA replication is not arrested by DNA damage signalling. Virology 2010, 406:95-102.
28. Kumagai A., Lee J., Yoo H.Y., Dunphy W.G. TopBP1 activates the ATR-ATRIP complex. Cell 2006, 124:943-955.
29. Kumagai A., Shevchenko A., Shevchenko A., Dunphy W.G. Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 2010, 140:349-359.
30. Kutler D.I., Wreesmann V.B., Goberdhan A., Ben-Porat L., Satagopan J., Ngai I., Huvos A.G., Giampietro P., Levran O., Pujara K., Diotti R., Carlson D., Huryn L.A., Auerbach A.D., Singh B. Human papillomavirus DNA and p53 polymorphisms in squamous cell carcinomas from Fanconi anemia patients. J. Natl Cancer Inst. 2003, 95:1718-1721.
31. Law M.F., Lowy D.R., Dvoretzky I., Howley P.M. Mouse cells transformed by bovine papillomavirus contain only extrachromosomal viral DNA sequences. Proc. Natl Acad. Sci. USA 1981, 78:2727-2731.
32. Leuchowius K.J., Weibrecht I., Soderberg O. In situ proximity ligation assay for microscopy and flow cytometry. Curr. Protoco. Cytom. 2011, (Chapter 9, Unit 9.36).
33. Liu K., Bellam N., Lin H.Y., Wang B., Stockard C.R., Grizzle W.E., Lin W.C. Regulation of p53 by TopBP1: a potential mechanism for p53 inactivation in cancer. Mol. Cell. Biol. 2009, 29:2673-2693.
34. Liu K., Ling S., Lin W.C. TopBP1 mediates mutant p53 gain of function through NF-Y and p63/p73. Mol. Cell. Biol. 2011, 31:4464-4481.
35. Liu K., Luo Y., Lin F.T., Lin W.C. TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes Dev. 2004, 18:673-686.
36. Liu S., Bekker-Jensen S., Mailand N., Lukas C., Bartek J., Lukas J. Claspin operates downstream of TopBP1 to direct ATR signaling towards Chk1 activation. Mol. Cell. Biol. 2006, 26:6056-6064.
37. Liu Y., Heilman S.A., Illanes D., Sluder G., Chen J.J. p53-independent abrogation of a postmitotic checkpoint contributes to human papillomavirus E6-induced polyploidy. Cancer Res. 2007, 67:2603-2610.
38. Makiniemi M., Hillukkala T., Tuusa J., Reini K., Vaara M., Huang D., Pospiech H., Majuri I., Westerling T., Makela T.P., Syvaoja J.E. BRCT domain-containing protein TopBP1 functions in DNA replication and damage response. J. Biol. Chem. 2001, 276:30399-30406.
39. McBride A.A., Howley P.M. Bovine papillomavirus with a mutation in the E2 serine 301 phosphorylation site replicates at a high copy number. J. Virol. 1991, 65:6528-6534.
40. Melanson S.M., Androphy E.J. Topography of bovine papillomavirus E2 protein on the viral genome during the cell cycle. Virology 2009, 393:258-264.
41. Mendoza-Maldonado R., Paolinelli R., Galbiati L., Giadrossi S., Giacca M. Interaction of the retinoblastoma protein with Orc1 and its recruitment to human origins of DNA replication. PloS ONE 2010, 5:e13720.
42. Mesplede T., Gagnon D., Bergeron-Labrecque F., Azar I., Senechal H., Coutlee F., Archambault J. p53 degradation activity, expression, and subcellular localization of E6 proteins from 29 human papillomavirus genotypes. J. Virol. 2012, 86:94-107.
43. Mohr I.J., Clark R., Sun S., Androphy E.J., MacPherson P., Botchan M.R. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science 1990, 250:1694-1699.
44. Park J.W., Pitot H.C., Strati K., Spardy N., Duensing S., Grompe M., Lambert P.F. Deficiencies in the Fanconi anemia DNA damage response pathway increase sensitivity to HPV-associated head and neck cancer. Cancer Res. 2010, 70:9959-9968.
45. Park P., Copeland W., Yang L., Wang T., Botchan M.R., Mohr I.J. The cellular DNA polymerase alpha-primase is required for papillomavirus DNA replication and associates with the viral E1 helicase. Proc. Natl. Acad. Sci. USA 1994, 91:8700-8704.
46. Phelps W.C., Howley P.M. Transcriptional trans-activation by the human papillomavirus type 16 E2 gene product. J. Virol. 1987, 61:1630-1638.
47. Reinson T., Toots M., Kadaja M., Pipitch R., Allik M., Ustav E., Ustav M. Engagement of the ATR-dependent DNA damage response at the human papillomavirus 18 replication centers during the initial amplification. J. Virol. 2013, 87:951-964.
48. Sakakibara N., Chen D., Jang M.K., Kang D.W., Luecke H.F., Wu S.Y., Chiang C.M., McBride A.A. Brd4 is displaced from HPV replication factories as they expand and amplify viral DNA. PLoS Pathog. 2013, 9:e1003777.
49. Sakakibara N., Mitra R., McBride A.A. The papillomavirus E1 helicase activates a cellular DNA damage response in viral replication foci. J. Virol. 2011, 85:8981-8995.
50. Sambrook J. and Russell D.W., Purification of nucleic acids by extraction with phenol:chloroform. CSH Protoc. 2006, . http://dx.doi.org/10.1101/pdb.prot4455.
51. Sanders C.M., Stenlund A. Recruitment and loading of the E1 initiator protein: an ATP-dependent process catalysed by a transcription factor. EMBO J. 1998, 17:7044-7055.
52. Schwab R.A., Blackford A.N., Niedzwiedz W. ATR activation and replication fork restart are defective in FANCM-deficient cells. EMBO J. 2010, 29:806-818.
53. Spardy N., Duensing A., Charles D., Haines N., Nakahara T., Lambert P.F., Duensing S. The human papillomavirus type 16 E7 oncoprotein activates the Fanconi anemia (FA) pathway and causes accelerated chromosomal instability in FA cells. J. Virol. 2007, 81:13265-13270.
54. Sprague D.L., Phillips S.L., Mitchell C.J., Berger K.L., Lace M., Turek L.P., Klingelhutz A.J. Telomerase activation in cervical keratinocytes containing stably replicating human papillomavirus type 16 episomes. Virology 2002, 301:247-254.
55. Todorovic B., Hung K., Massimi P., Avvakumov N., Dick F.A., Shaw G.S., Banks L., Mymryk J.S. Conserved region 3 of human papillomavirus 16 E7 contributes to deregulation of the retinoblastoma tumor suppressor. J. Virol. 2012, 86:13313-13323.
56. Ustav M., Stenlund A. Transient replication of BPV-1 requires two viral polypeptides encoded by the E1 and E2 open reading frames. EMBO J. 1991, 10:449-457.
57. Voitenleitner C., Botchan M. E1 protein of bovine papillomavirus type 1 interferes with E2 protein-mediated tethering of the viral DNA to mitotic chromosomes. J. Virol. 2002, 76:3440-3451.
58. Wang X., Helfer C.M., Pancholi N., Bradner J.E., You J. Recruitment of Brd4 to the human papillomavirus type 16 DNA replication complex is essential for replication of viral DNA. J. Virol. 2013, 87:3871-3884.
59. Wang X., Naidu S.R., Sverdrup F., Androphy E.J. Tax1BP1 interacts with papillomavirus E2 and regulates E2-dependent transcription and stability. J. Virol. 2009, 83:2274-2284.
60. Yamane K., Wu X., Chen J. A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol. Cell. Biol. 2002, 22:555-566.
61. Yang L., Mohr I., Fouts E., Lim D.A., Nohaile M., Botchan M. The E1 protein of bovine papilloma virus 1 is an ATP-dependent DNA helicase. Proc. Natl. Acad. Sci. USA 1993, 90:5086-5090.
62. Yu T., Peng Y.C., Androphy E.J. Mitotic kinesin-like protein 2 binds and colocalizes with papillomavirus E2 during mitosis. J. Virol. 2007, 81:1736-1745.