HPV16-E2 induces prophase arrest and activates the cellular DNA damage response in vitro and in precursor lesions of cervical carcinoma

Oncotarget

Volumn 6, Issue 33, 2015, Pages 34979-34991

  Xue, Yuezhen ^a,e   Toh, Shen Yon ^a   He, Pingping ^a   Lim, Thimothy ^b   Lim, Diana ^c   Pang, Chai Ling ^d   Abastado, Jean Pierre ^d   Thierry, Françoise ^a  

^a INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^b KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^c NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^d AGENCY FOR SCIENCE   (Singapore)

^e AGENCY FOR SCIENCE   (Singapore)

Author keywords

Cell cycle; Cervical intraepithelial neoplasia; DNA damage response; HPV16 E2; Prophase

Indexed keywords

DNA; UNCLASSIFIED DRUG; VIRUS E2 PROTEIN; VIRUS PROTEIN; DNA BINDING PROTEIN; E2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; FEMALE; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALIGNANT TRANSFORMATION; NONHUMAN; PROPHASE; PROTEIN EXPRESSION; UTERINE CERVIX CARCINOMA IN SITU; VIRUS CARCINOGENESIS; VIRUS CELL INTERACTION; CELL CYCLE CHECKPOINT; CELL TRANSFORMATION; COMPLICATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; METABOLISM; PAPILLOMAVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; PRECANCER; UTERINE CERVIX TUMOR; VIROLOGY; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL CYCLE CHECKPOINTS; CELL TRANSFORMATION, NEOPLASTIC; CERVICAL INTRAEPITHELIAL NEOPLASIA; DNA DAMAGE; DNA-BINDING PROTEINS; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PRECANCEROUS CONDITIONS; PROPHASE; UTERINE CERVICAL NEOPLASMS;

EID: 84946605705     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5512     Document Type: Article

References (30)

1. Agorastos T, Miliaras D, Lambropoulos AF, Chrisafi S, Kotsis A, Manthos A, Bontis J. Detection and typing of human papillomavirus DNA in uterine cervices with coexistent grade I and grade III intraepithelial neoplasia: biologic progression or independent lesions?. Eur J Obstet Gynecol Reprod Biol. 2005; 121:99-103.
2. Kruse AJ, Buhr-Wildhagen S, Janssen EA, Baak JP. The relationship between syntactic structure analysis features, histological grade and high-risk HPV DNA in cervical intraepithelial neoplasia. Cell Oncol. 2004; 26:135-141.
3. Syrjanen K, Shabalova I, Naud P, Kozachenko V, Derchain S, Zakharchenko S, Roteli-Martins C, Nerovjna R, Longatto-Filho A, Kljukina L, Tatti S, Branovskaja M, Hammes LS, Branca M, Grunjberga V, Erzen M, et al. Persistent high-risk human papillomavirus infections and other end-point markers of progressive cervical disease among women prospectively followed up in the New Independent States of the Former Soviet Union and the Latin American Screening study cohorts. Int J Gynecol Cancer. 2009; 19:934-942.
4. McCredie MR, Sharples KJ, Paul C, Baranyai J, Medley G, Jones RW, Skegg DC. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol. 2008; 9:425-434.
5. Schiffman M, Rodriguez AC. Heterogeneity in CIN3 diagnosis. Lancet Oncol. 2008; 9:404-406.
6. Xue Y, Bellanger S, Zhang W, Lim D, Low J, Lunny D, Thierry F. HPV16 E2 is an immediate early marker of viral infection, preceding E7 expression in precursor structures of cervical carcinoma. Cancer research. 2010; 70:5316-5325.
7. Rajkumar T, Sabitha K, Vijayalakshmi N, Shirley S, Bose MV, Gopal G, Selvaluxmy G. Identification and validation of genes involved in cervical tumourigenesis. BMC Cancer. 2011; 11:80.
8. Asato T, Nakajima Y, Nagamine M, Nakashima Y, Takei H, Maehama T, Yamashiro T, Higashi M, Nakayama M, Kanazawa K. Correlation between the progression of cervical dysplasia and the prevalence of human papillomavirus. J Infect Dis. 1994; 169:940-941.
9. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, Venere M, Ditullio RA Jr., Kastrinakis NG, Levy B, Kletsas D, Yoneta A, Herlyn M, Kittas C, Halazonetis TD. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature. 2005; 434:907-913.
10. Ariumi Y, Kuroki M, Dansako H, Abe K, Ikeda M, Wakita T, Kato N. The DNA damage sensors ataxia-telangiectasia mutated kinase and checkpoint kinase 2 are required for hepatitis C virus RNA replication. J Virol. 2008; 82:9639-9646.
11. 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. 2011; 85:8996-9012.
12. Moody CA, Laimins LA. Human papillomaviruses activate the ATM DNA damage pathway for viral genome amplification upon differentiation. PLoS Pathog. 2009; 5:e1000605.
13. Bellanger S, Blachon S, Mechali F, Bonne-Andrea C, Thierry F. High-risk but not low-risk HPV E2 proteins bind to the APC activators Cdh1 and Cdc20 and cause genomic instability. Cell Cycle. 2005; 4:1608-1615.
14. Tan CL, Teissier S, Gunaratne J, Quek LS, Bellanger S. Stranglehold on the spindle assembly checkpoint: the human papillomavirus E2 protein provokes BUBR1-dependent aneuploidy. Cell Cycle. 2015; 14:1459-1470.
15. Stolz A, Ertych N, Kienitz A, Vogel C, Schneider V, Fritz B, Jacob R, Dittmar G, Weichert W, Petersen I, Bastians H. The CHK2-BRCA1 tumour suppressor pathway ensures chromosomal stability in human somatic cells. Nat Cell Biol. 2010; 12:492-499.
16. Yang C, Tang X, Guo X, Niikura Y, Kitagawa K, Cui K, Wong ST, Fu L, Xu B. Aurora-B mediated ATM serine 1403 phosphorylation is required for mitotic ATM activation and the spindle checkpoint. Mol Cell. 2011; 44:597-608.
17. Choi E, Park PG, Lee HO, Lee YK, Kang GH, Lee JW, Han W, Lee HC, Noh DY, Lekomtsev S, Lee H. BRCA2 fine-tunes the spindle assembly checkpoint through reinforcement of BubR1 acetylation. Dev Cell. 2012; 22:295-308.
18. Blachon S, Bellanger S, Demeret C, Thierry F. Nucleocytoplasmic shuttling of high risk human Papillomavirus E2 proteins induces apoptosis. J Biol Chem. 2005; 280:36088-36098.
19. Xue Y, Lim D, Zhi L, He P, Abastado JP, Thierry F. Loss of HPV16 E2 Protein Expression Without Disruption of the E2 ORF Correlates with Carcinogenic Progression. Open Virol J. 2012; 6:163-172.
20. Thierry F. Transcriptional regulation of the papillomavirus oncogenes by cellular and viral transcription factors in cervical carcinoma. Virology. 2009; 384:375-379.
21. Prigent C, Dimitrov S. Phosphorylation of serine 10 in histone H3, what for? J Cell Sci. 2003; 116:3677-3685.
22. Trunnell NB, Poon AC, Kim SY, Ferrell JE Jr. Ultrasensitivity in the Regulation of Cdc25C by Cdk1. Mol Cell. 2011; 41:263-274.
23. Karlsson-Rosenthal C, Millar JB. Cdc25: mechanisms of checkpoint inhibition and recovery. Trends Cell Biol. 2006; 16:285-292.
24. Zhao H, Traganos F, Darzynkiewicz Z. Kinetics of histone H2AX phosphorylation and Chk2 activation in A549 cells treated with topotecan and mitoxantrone in relation to the cell cycle phase. Cytometry A. 2008; 73:480-489.
25. Bartek J, Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol. 2007; 19:238-245.
26. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell. 2007; 28:739-745.
27. Bulavin DV, Higashimoto Y, Demidenko ZN, Meek S, Graves P, Phillips C, Zhao H, Moody SA, Appella E, Piwnica-Worms H, Fornace AJ Jr. Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat Cell Biol. 2003; 5:545-551.
28. Chen J, Xue Y, Poidinger M, Lim T, Chew SH, Pang CL, Abastado JP, Thierry F. Mapping of HPV transcripts in four human cervical lesions using RNAseq suggests quantitative rearrangements during carcinogenic progression. Virology. 2014; 462-463:14-24.
29. Lawrence KS, Chau T, Engebrecht J. DNA Damage Response and Spindle Assembly Checkpoint Function throughout the Cell Cycle to Ensure Genomic Integrity. PLoS Genet. 2015; 11:e1005150.
30. Evans MF, Peng Z, Clark KM, Adamson CS, Ma XJ, Wu X, Wang H, Luo Y, Cooper K. HPV E6/E7 RNA in situ hybridization signal patterns as biomarkers of threetier cervical intraepithelial neoplasia grade. PLoS One. 2014; 9:e91142.