Epstein-Barr Virus DNase (BGLF5) induces genomic instability in human epithelial cells

Nucleic Acids Research

Volumn 38, Issue 6, 2009, Pages 1932-1949

  Wu, Chung Chun ^a   Liu, Ming Tsan ^a,b   Chang, Yu Ting ^a   Fang, Chih Yeu ^a   Chou, Sheng Ping ^a   Liao, Hsin Wei ^a   Kuo, Kuan Lin ^c   Hsu, Shih Lung ^c   Chen, Yi Ren ^c   Wang, Pei Wen ^a   Chen, Yu Lian ^a   Chuang, Hsin Ying ^a   Lee, Chia Huei ^a   Chen, Ming ^d   Wayne Chang, Wun Shaing ^a   Chen, Jen Yang ^a,c  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b CENTER FOR DISEASE CONTROL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; HISTONE H2AX; PROTEIN BGLF5; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE, EPSTEIN BARR VIRUS; DEOXYRIBONUCLEASE, EPSTEIN-BARR VIRUS; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHROMOSOME ABERRATION; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; EPITHELIUM CELL; EPSTEIN BARR VIRUS; GENE MUTATION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; MICRONUCLEUS; MICROSATELLITE INSTABILITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; WESTERN BLOTTING; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROTEIN SYNTHESIS; ULTRAVIOLET RADIATION;

HUMAN HERPESVIRUS 4;

CELL LINE; CHROMOSOME ABERRATIONS; DEOXYRIBONUCLEASES; DNA BREAKS; DNA DAMAGE; DNA REPAIR; EPITHELIAL CELLS; GENOMIC INSTABILITY; HUMANS; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MICROSATELLITE INSTABILITY; MUTATION; PROTEIN BIOSYNTHESIS; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS; VIRAL PROTEINS;

EID: 77951226608     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1169     Document Type: Article

References (100)

1. Kuzminov, A. (1999) Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev., 63, 751-813.
2. Li, L. and Rohrmann, G.F. (2000) Characterization of a baculovirus alkaline nuclease. J. Virol., 74, 6401-6407.
3. Martinez, R., Sarisky, R.T., Weber, P.C. and Weller, S.K. (1996) Herpes simplex virus type 1 alkaline nuclease is required for efficient processing of viral DNA replication intermediates. J. Virol., 70, 2075-2085.
4. Porter, I.M. and Stow, N.D. (2004) Virus particles produced by the herpes simplex virus type 1 alkaline nuclease null mutant ambUL12 contain abnormal genomes. J. Gen. Virol., 85, 583-591.
5. Young, L.S. and Rickinson, A.B. (2004) Epstein-Barr virus: 40 years on. Nat. Rev. Cancer, 4, 757-768.
6. Feederle, R., Bannert, H., Lips, H., Muller-Lantzsch, N. and Delecluse, H.J. (2009) The Epstein-Barr virus alkaline exonuclease BGLF5 serves pleiotropic functions in virus replication. J. Virol., 83, 4952-4962.
7. Zhang, C.X., Decaussin, G., de Turenne Tessier, M., Daillie, J. and Ooka, T. (1987) Identification of an Epstein-Barr virus-specific desoxyribonuclease gene using complementary DNA. Nucleic Acids Res., 15, 2707-2717.
8. Baylis, S.A., Purifoy, D.J. and Littler, E. (1989) The characterization of the EBV alkaline deoxyribonuclease cloned and expressed in E. coli. Nucleic Acids Res., 17, 7609-7622.
9. Stolzenberg, M.C. and Ooka, T. (1990) Purification and properties of Epstein-Barr virus DNase expressed in Escherichia coli. J. Virol., 64, 96-104.
10. Chen, M.R., Hsu, T.Y., Chen, J.Y. and Yang, C.S. (1990) Molecular characterization of a cDNA clone encoding the Epstein-Barr virus (EBV) DNase. J. Virol. Methods, 29, 127-141.
11. Lin, S.F., Lin, S.W., Hsu, T.Y., Liu, M.Y., Chen, J.Y. and Yang, C.S. (1994) Functional analysis of the amino terminus of Epstein-Barr virus deoxyribonuclease. Virology, 199, 223-227.
12. Cheng, Y.C., Chen, J.Y., Glaser, R. and Henle, W. (1980) Frequency and levels of antibodies to Epstein-Barr virus-specific DNase are elevated in patients with nasopharyngeal carcinoma. Proc. Natl Acad. Sci. USA, 77, 6162-6165.
13. Chen, J.Y., Hwang, L.Y., Beasley, R.P., Chien, C.S. and Yang, C.S. (1985) Antibody response to Epstein-Barr-virus-specific DNase in 13 patients with nasopharyngeal carcinoma in Taiwan: a retrospective study. J. Med. Virol., 16, 99-105.
14. Sbih-Lammali, F., Berger, F., Busson, P. and Ooka, T. (1996) Expression of the DNase encoded by the BGLF5 gene of Epstein-Barr virus in nasopharyngeal carcinoma epithelial cells. Virology, 222, 64-74.
15. Hanahan, D. and Weinberg, R.A. (2000) The hallmarks of cancer. Cell, 100, 57-70.
16. Michor, F., Iwasa, Y., Lengauer, C. and Nowak, M.A. (2005) Dynamics of colorectal cancer. Semin. Cancer Biol., 15, 484-493.
17. Fukasawa, K. (2005) Centrosome amplification, chromosome instability and cancer development. Cancer Lett., 230, 6-19.
18. Huang, D.P., Lo, K.W., Choi, P.H., Ng, A.Y., Tsao, S.Y., Yiu, G.K. and Lee, J.C. (1991) Loss of heterozygosity on the short arm of chromosome 3 in nasopharyngeal carcinoma. Cancer Genet. Cytogenet., 54, 91-99.
19. Lengauer, C., Kinzler, K.W. and Vogelstein, B. (1998) Genetic instabilities in human cancers. Nature, 396, 643-649.
20. Nowak, M.A., Komarova, N.L., Sengupta, A., Jallepalli, P.V., Shih Ie, M., Vogelstein, B. and Lengauer, C. (2002) The role of chromosomal instability in tumor initiation. Proc. Natl Acad. Sci. USA, 99, 16226-16231.
21. Dixon, K. and Kopras, E. (2004) Genetic alterations and DNA repair in human carcinogenesis. Semin. Cancer Biol., 14, 441-448.
22. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kacmaz, K. and Linn, S. (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem., 73, 39-85.
23. Iliakis, G., Wang, H., Perrault, A.R., Boecker, W., Rosidi, B., Windhofer, F., Wu, W., Guan, J., Terzoudi, G. and Pantelias, G. (2004) Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome Res., 104, 14-20.
24. Gollin, S.M. (2005) Mechanisms leading to chromosomal instability. Semin. Cancer Biol., 15, 33-42.
25. Jefford, C.E. and Irminger-Finger, I. (2006) Mechanisms of chromosome instability in cancers. Crit. Rev. Oncol. Hematol., 59, 1-14.
26. Tsukasaki, K. (2002) Genetic instability of adult T-cell leukemia/lymphoma by comparative genomic hybridization analysis. J. Clin. Immunol., 22, 57-63.
27. Machida, K., Cheng, K.T., Sung, V.M., Shimodaira, S., Lindsay, K.L., Levine, A.M., Lai, M.Y. and Lai, M.M. (2004) Hepatitis C virus induces a mutator phenotype: enhanced mutations of immunoglobulin and protooncogenes. Proc. Natl Acad. Sci. USA, 101, 4262-4267.
28. Kadaja, M., Sumerina, A., Verst, T., Ojarand, M., Ustav, E. and Ustav, M. (2007) Genomic instability of the host cell induced by the human papillomavirus replication machinery. EMBO J., 26, 2180-2191.
29. Pan, H., Zhou, F. and Gao, S.J. (2004) Kaposi's sarcoma-associated herpesvirus induction of chromosome instability in primary human endothelial cells. Cancer Res., 64, 4064-4068.
30. Gualandi, G., Giselico, L., Carloni, M., Palitti, F., Mosesso, P. and Alfonsi, A.M. (2001) Enhancement of genetic instability in human B cells by Epstein-Barr virus latent infection. Mutagenesis, 16, 203-208.
31. Kamranvar, S.A., Gruhne, B., Szeles, A. and Masucci, M.G. (2007) Epstein-Barr virus promotes genomic instability in Burkitt's lymphoma. Oncogene., 26, 5115-5123.
32. Fang, C.Y., Lee, C.H., Wu, C.C., Chang, Y.T., Yu, S.L., Chou, S.P., Huang, P.T., Chen, C.L., Hou, J.W. and Chang, Y. (2009) Recurrent chemical reactivations of EBV promotes genome instability and enhances tumor progression of nasopharyngeal carcinoma cells. Int. J. Cancer, 124, 2016-2025.
33. Russo, C.A., Weber, T.K., Volpe, C.M., Stoler, D.L., Petrelli, N.J., Rodriguez-Bigas, M., Burhans, W.C. and Anderson, G.R. (1995) An anoxia inducible endonuclease and enhanced DNA breakage as contributors to genomic instability in cancer. Cancer Res., 55, 1122-1128.
34. Gladdy, R.A., Taylor, M.D., Williams, C.J., Grandal, I., Karaskova, J., Squire, J.A., Rutka, J.T., Guidos, C.J. and Danska, J.S. (2003) The RAG-1/2 endonuclease causes genomic instability and controls CNS complications of lymphoblastic leukemia in p53/Prkdc-deficient mice. Cancer Cell, 3, 37-50.
35. Chang, I.Y., Kim, S.H., Cho, H.J., Lee, D.Y., Kim, M.H., Chung, M.H. and You, H.J. (2005) Human AP endonuclease suppresses DNA mismatch repair activity leading to microsatellite instability. Nucleic Acids Res., 33, 5073-5081.
36. Fautrel, A., Andrieux, L., Musso, O., Boudjema, K., Guillouzo, A. and Langouet, S. (2005) Overexpression of the two nucleotide excision repair genes ERCC1 and XPC in human hepatocellular carcinoma. J. Hepatol., 43, 288-293.
37. Rouet, P., Smih, F. and Jasin, M. (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell Biol., 14, 8096-8106.
38. Bryant, P.E. and Riches, A.C. (1989) Oncogenic transformation of murine C3H 10T1/2 cells resulting from DNA double-strand breaks induced by a restriction endonuclease. Br. J. Cancer, 60, 852-854.
39. Bryant, P.E. and Johnston, P.J. (1993) Restriction-endonuclease-induced DNA double-strand breaks and chromosomal aberrations in mammalian cells. Mutat. Res., 299, 289-296.
40. Singh, B. and Bryant, P.E. (1991) Induction of mutations at the thymidine kinase locus in CHO cells by restriction endonucleases. Mutagenesis, 6, 219-223.
41. Chenet-Monte, C., Mohammad, F., Celluzzi, C.M., Schaffer, P.A. and Farber, F.E. (1986) Herpes simplex virus gene products involved in the induction of chromosomal aberrations. Virus Res., 6, 245-260.
42. Lin, C.T., Wong, C.I., Chan, W.Y., Tzung, K.W., Ho, J.K., Hsu, M.M. and Chuang, S.M. (1990) Establishment and characterization of two nasopharyngeal carcinoma cell lines. Lab Invest., 62, 713-724.
43. Kim, M.S., Li, S.L., Bertolami, C.N., Cherrick, H.M. and Park, N.H. (1993) State of p53, Rb and DCC tumor suppressor genes in human oral cancer cell lines. Anticancer Res., 13, 1405-1413.
44. Toolan, H.W. (1954) Transplantable human neoplasms maintained in cortisone-treated laboratory animals: H.S. No. 1; H.Ep. No. 1; H.Ep. No. 2; H.Ep. No. 3; and H.Emb.Rh. No. 1. Cancer Res., 14, 660-666.
45. Tsai, C.H., Liu, M.T., Chen, M.R., Lu, J., Yang, H.L., Chen, J.Y. and Yang, C.S. (1997) Characterization of monoclonal antibodies to the Zta and DNase proteins of Epstein-Barr virus. J. Biomed. Sci., 4, 69-77.
46. Liu, M.T., Hu, H.P., Hsu, T.Y. and Chen, J.Y. (2003) Site-directed mutagenesis in a conserved motif of Epstein-Barr virus DNase that is homologous to the catalytic centre of type II restriction endonucleases. J. Gen. Virol., 84, 677-686.
47. Liu, M.T., Chen, Y.R., Chen, S.C., Hu, C.Y., Lin, C.S., Chang, Y.T., Wang, W.B. and Chen, J.Y. (2004) Epstein-Barr virus latent membrane protein 1 induces micronucleus formation, represses DNA repair and enhances sensitivity to DNA-damaging agents in human epithelial cells. Oncogene, 23, 2531-2539.
48. Collins, A.R. (2004) The comet assay for DNA damage and repair: principles, applications and limitations. Mol. Biotechnol., 26, 249-261.
49. Naganuma, A., Dansako, H., Nakamura, T., Nozaki, A. and Kato, N. (2004) Promotion of microsatellite instability by hepatitis C virus core protein in human non-neoplastic hepatocyte cells. Cancer Res., 64, 1307-1314.
50. McGurk, C.J., Cummings, M., Koberle, B., Hartley, J.A., Oliver, R.T. and Masters, J.R. (2006) Regulation of DNA repair gene expression in human cancer cell lines. J. Cell Biochem., 97, 1121-36.
51. Cheng, L., Guan, Y., Legerski, R.J., Einspahr, J., Bangert, J., Alberts, D.S. and Wei, Q. (1999) Expression in normal human tissues of five nucleotide excision repair genes measured simultaneously by multiplex reverse transcription-polymerase chain reaction. Cancer Epidemiol. Biomarkers Prev., 8, 801-7.
52. Vogel, U., Dybdahl, M., Frentz, G. and Nexo, B.A. (2000) DNA repair capacity: inconsistency between effect of over-expression of five NER genes and the correlation to mRNA levels in primary lymphocytes. Mutat. Res., 461, 197-210.
53. Yuan, R., Fan, S., Wang, J.A., Meng, Q., Ma, Y., Schreiber, D., Goldberg, I.D. and Rosen, E.M. (1999) Coordinate alterations in the expression of BRCA1, BRCA2, p300, and Rad51 in response to genotoxic and other stresses in human prostate cancer cells. Prostate, 40, 37-49.
54. Bale, S.S. (1983) Cytological effects of kepone on Chinese hamster cells. J. Hered., 74, 123-124.
55. Liu, M.T., Hsu, T.Y., Lin, S.F., Seow, S.V., Liu, M.Y., Chen, J.Y. and Yang, C.S. (1998) Distinct regions of EBV DNase are required for nuclease and DNA binding activities. Virology, 242, 6-13.
56. Heddle, J.A. (1973) A rapid in vivo test for chromosomal damage. Mutat Res., 18, 187-190.
57. Parry, J.M. and Parry, E.M. (1987) Comparisons of tests for aneuploidy. Mutat. Res., 181, 267-287.
58. Sternes, K.L. and Vig, B.K. (1989) Micronuclei, kinetochores and hypoploidy: tests with some agents. Mutagenesis, 4, 425-431.
59. Coleman, W.B. and Tsongalis, G.J. (1995) Multiple mechanisms account for genomic instability and molecular mutation in neoplastic transformation. Clin. Chem., 41, 644-657.
60. Kastan, M.B. (1997) Genetic instability and tumorigenesis: introduction. Curr. Top Microbiol. Immunol., 221, 1-4.
61. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. and Bonner, W.M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem., 273, 5858-5868.
62. Olive, P.L. and Banath, J.P. (2006) The comet assay: a method to measure DNA damage in individual cells. Nat. Protoc., 1, 23-29.
63. Johnson, J.M. and Latimer, J.J. (2005) Analysis of DNA repair using transfection-based host cell reactivation. Methods Mol. Biol., 291, 321-335.
64. Cenni, B., Kim, H.K., Bubley, G.J., Aebi, S., Fink, D., Teicher, B.A., Howell, S.B. and Christen, R.D. (1999) Loss of DNA mismatch repair facilitates reactivation of a reporter plasmid damaged by cisplatin. Br. J. Cancer, 80, 699-704.
65. Wang, L., Wei, Q., Shi, Q., Guo, Z., Qiao, Y. and Spitz, M.R. (2007) A modified host-cell reactivation assay to measure repair of alkylating DNA damage for assessing risk of lung adenocarcinoma. Carcinogenesis, 28, 1430-1436.
66. Thacker, J. (1994) The study of responses to 'model' DNA breaks induced by restriction endonucleases in cells and cell-free systems: achievements and difficulties. Int. J. Radiat. Biol., 66, 591-596.
67. Martin, L.P., Hamilton, T.C. and Schilder, R.J. (2008) Platinum resistance: the role of DNA repair pathways. Clin. Cancer Res., 14, 1291-1295.
68. Drablos, F., Feyzi, E., Aas, P.A., Vaagbo, C.B., Kavli, B., Bratlie, M.S., Pena-Diaz, J., Otterlei, M., Slupphaug, G. and Krokan, H.E. (2004) Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair, 3, 1389-1407.
69. 6-methylguanine adducts. Mol. Cell, 22, 501-510.
70. Sedgwick, B., Bates, P.A., Paik, J., Jacobs, S.C. and Lindahl, T. (2007) Repair of alkylated DNA: recent advances. DNA Repair (Amst), 6, 429-442.
71. Glaunsinger, B. and Ganem, D. (2004) Lytic KSHV infection inhibits host gene expression by accelerating global mRNA turnover. Mol. Cell., 13, 713-723.
72. Rowe, M., Glaunsinger, B., van Leeuwen, D., Zuo, J., Sweetman, D., Ganem, D., Middeldorp, J., Wiertz, E.J. and Ressing, M.E. (2007) Host shutoff during productive Epstein-Barr virus infection is mediated by BGLF5 and may contribute to immune evasion. Proc. Natl Acad. Sci. USA, 104, 3366-3371.
73. Glaunsinger, B., Chavez, L. and Ganem, D. (2005) The exonuclease and host shutoff functions of the SOX protein of Kaposi's sarcoma-associated herpesvirus are genetically separable. J. Virol., 79, 7396-7401.
74. Zuo, J., Thomas, W., van Leeuwen, D., Middeldorp, J.M., Wiertz, E.J., Ressing, M.E. and Rowe, M. (2008) The DNase of gammaherpesviruses impairs recognition by virus-specific CD8+ T cells through an additional host shutoff function. J. Virol., 82, 2385-2393.
75. Kinner, A., Wu, W., Staudt, C. and Iliakis, G. (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res., 36, 5678-5694.
76. Kim, P.M., Allen, C., Wagener, B.M., Shen, Z. and Nickoloff, J.A. (2001) Overexpression of human RAD51 and RAD52 reduces double-strand break-induced homologous recombination in mammalian cells. Nucleic Acids Res., 29, 4352-4360.
77. Ferry, K.V., Hamilton, T.C. and Johnson, S.W. (2000) Increased nucleotide excision repair in cisplatin-resistant ovarian cancer cells: role of ERCC1-XPF. Biochem. Pharmacol., 60, 1305-1313.
78. Muotri, A.R., Marchetto, M.C., Suzuki, M.F., Okazaki, K., Lotfi, C.F., Brumatti, G., Amarante-Mendes, G.P. and Menck, C.F. (2002) Low amounts of the DNA repair XPA protein are sufficient to recover UV-resistance. Carcinogenesis, 23, 1039-1046.
79. Gibson, S.L., Narayanan, L., Hegan, D.C., Buermeyer, A.B., Liskay, R.M. and Glazer, P.M. (2006) Overexpression of the DNA mismatch repair factor, PMS2, confers hypermutability and DNA damage tolerance. Cancer Lett., 244, 195-202.
80. Rouet, P., Smih, F. and Jasin, M. (1994) Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc. Natl Acad. Sci. USA, 91, 6064-6068.
81. Chandriani, S. and Ganem, D. (2007) Host transcript accumulation during lytic KSHV infection reveals several classes of host responses. PLoS ONE, 2, 1-10.
82. Lee, Y.J. and Glaunsinger, B.A. (2009) Aberrant herpesvirus-induced polyadenylation correlates with cellular messenger RNA destruction. PLoS Biol., 7, e1000107.
83. Shokolenko, I.N., Alexeyev, M.F., Robertson, F.M., LeDoux, S.P. and Wilson, G.L. (2003) The expression of exonuclease III from E. coli in mitochondria of breast cancer cells diminishes mitochondrial DNA repair capacity and cell survival after oxidative stress. DNA Repair, 2, 471-482.
84. Weinberg, R.A. (2007) The Biology of Cancer, 1 edn. Garland Science, New York.
85. Jeang, K.T., Widen, S.G., Semmes, O.J.t. and Wilson, S.H. (1990) HTLV-I trans-activator protein, tax, is a trans-repressor of the human beta-polymerase gene. Science, 247, 1082-1084.
86. Majone, F., Semmes, O.J. and Jeang, K.T. (1993) Induction of micronuclei by HTLV-I Tax: a cellular assay for function. Virology, 193, 456-459.
87. Lee, T.H., Elledge, S.J. and Butel, J.S. (1995) Hepatitis B virus X protein interacts with a probable cellular DNA repair protein. J. Virol., 69, 1107-1114.
88. Livezey, K.W., Negorev, D. and Simon, D. (2002) Increased chromosomal alterations and micronuclei formation in human hepatoma HepG2 cells transfected with the hepatitis B virus HBX gene. Mutat. Res., 505, 63-74.
89. Hsieh, Y.H., Su, I.J., Wang, H.C., Chang, W.W., Lei, H.Y., Lai, M.D., Chang, W.T. and Huang, W. (2004) Pre-S mutant surface antigens in chronic hepatitis B virus infection induce oxidative stress and DNA damage. Carcinogenesis, 25, 2023-2032.
90. Machida, K., Cheng, K.T., Sung, V.M., Lee, K.J., Levine, A.M. and Lai, M.M. (2004) Hepatitis C virus infection activates the immunologic (type II) isoform of nitric oxide synthase and thereby enhances DNA damage and mutations of cellular genes. J. Virol., 78, 8835-8843.
91. Macoska, J.A., Beheshti, B., Rhim, J.S., Hukku, B., Lehr, J., Pienta, K.J. and Squire, J.A. (2000) Genetic characterization of immortalized human prostate epithelial cell cultures. Evidence for structural rearrangements of chromosome 8 and i(8q) chromosome formation in primary tumor-derived cells. Cancer Genet. Cytogenet., 120, 50-57.
92. Duensing, S. and Munger, K. (2002) The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res., 62, 7075-7082.
93. Iftner, T., Elbel, M., Schopp, B., Hiller, T., Loizou, J.I., Caldecott, K.W. and Stubenrauch, F. (2002) Interference of papillomavirus E6 protein with single-strand break repair by interaction with XRCC1. EMBO J., 21, 4741-4748.
94. Si, H. and Robertson, E.S. (2006) Kaposi's sarcoma-associated herpesvirus-encoded latency-associated nuclear antigen induces chromosomal instability through inhibition of p53 function. J. Virol., 80, 697-709.
95. Chen, Y.R., Liu, M.T., Chang, Y.T., Wu, C.C., Hu, C.Y. and Chen, J.Y. (2008) Epstein-Barr virus latent membrane protein 1 represses DNA repair through the PI3K/Akt/FOXO3a pathway in human epithelial cells. J. Virol., 82, 8124-8137.
96. Gruhne, B., Sompallae, R., Marescotti, D., Kamranvar, S.A., Gastaldello, S. and Masucci, M.G. (2009) The Epstein-Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species. Proc. Natl Acad. Sci. USA, 106, 2313-2318.
97. Pan, S.H., Tai, C.C., Lin, C.S., Hsu, W.B., Chou, S.F., Lai, C.C., Chen, J.Y., Tien, H.F., Lee, F.Y. and Wang, W.B. (2009) Epstein-Barr virus nuclear antigen 2 disrupts mitotic checkpoint and causes chromosomal instability. Carcinogenesis, 30, 366-375.
98. Gruhne, B., Sompallae, R. and Masucci, M.G. (2009) Three Epstein-Barr virus latency proteins independently promote genomic instability by inducing DNA damage, inhibiting DNA repair and inactivating cell cycle checkpoints. Oncogene, 28, 3997-4008.
99. Altmann, M. and Hammerschmidt, W. (2005) Epstein-Barr virus provides a new paradigm: a requirement for the immediate inhibition of apoptosis. PLoS Biol., 3, 2148-2157.
100. Wen, W., Iwakiri, D., Yamamoto, K., Maruo, S., Kanda, T. and Takada, K. (2007) Epstein-Barr virus BZLF1 gene, a switch from latency to lytic infection, is expressed as an immediate-early gene after primary infection of B lymphocytes. J. Virol., 81, 1037-42.