Tax impairs DNA replication forks and increases DNA breaks in specific oncogenic genome regions

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Chaib Mezrag, Hassiba ^a   Lemaçon, Delphine ^b,c,d   Fontaine, Hélène ^b,c,d   Bellon, Marcia ^a   Bai, Xue T ^a   Drac, Marjorie ^e   Coquelle, Arnaud ^b,c,d   Nicot, Christophe ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^c UNIV MONTPELLIER   (France)

^d CENTRE VAL D AURELLE   (France)

^e INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; ONCOPROTEIN; PROTEIN BCL 2; TAX PROTEIN; MYC PROTEIN; MYC PROTEIN, HUMAN; NF-KAPPA B KINASE; NITRIC OXIDE; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CELL DEATH; CHROMATIN; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA MODIFICATION; DNA REPLICATION; DNA STRAND BREAKAGE; DOUBLE STRANDED DNA BREAK; GENETIC DISORDER; HUMAN; HUMAN CELL; HUMAN T CELL LEUKEMIA VIRUS 1; ONCOGENE C MYC; PROMOTER REGION; T CELL LEUKEMIA; TRANSFORMED CELL; GENETICS; GENOMIC INSTABILITY; HEK293 CELL LINE; HUMAN GENOME; HUMAN T-LYMPHOTROPIC VIRUS 1; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY;

CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA REPLICATION; GENE PRODUCTS, TAX; GENOME, HUMAN; GENOMIC INSTABILITY; HEK293 CELLS; HUMAN T-LYMPHOTROPIC VIRUS 1; HUMANS; LEUKEMIA-LYMPHOMA, ADULT T-CELL; NITRIC OXIDE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MYC;

EID: 84907419761     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-205     Document Type: Article

References (50)

1. Ward JD, Barber LJ, Petalcorin MI, Yanowitz J, Boulton SJ. Replication blocking lesions present a unique substrate for homologous recombination. EMBO J 2007, 26:3384-3396. 10.1038/sj.emboj.7601766, 1933397, 17611606.
2. Michel B, Ehrlich SD, Uzest M. DNA double-strand breaks caused by replication arrest. EMBO J 1997, 16:430-438. 10.1093/emboj/16.2.430, 1169647, 9029161.
3. Lundin C, Erixon K, Arnaudeau C, Schultz N, Jenssen D, Meuth M, Helleday T. Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol Cell Biol 2002, 22:5869-5878. 10.1128/MCB.22.16.5869-5878.2002, 133974, 12138197.
4. Tuduri S, Crabbe L, Conti C, Tourriere H, Holtgreve-Grez H, Jauch A, Pantesco V, De VJ, Thomas A, Theillet C, Pommier Y, Tazi J, Coquelle A, Pasero P. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat Cell Biol 2009, 11:1315-1324. 10.1038/ncb1984, 2912930, 19838172.
5. Ohnishi T, Mori E, Takahashi A. DNA double-strand breaks: their production, recognition, and repair in eukaryotes. Mutat Res 2009, 669:8-12. 10.1016/j.mrfmmm.2009.06.010, 19576233.
6. Riches LC, Lynch AM, Gooderham NJ. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 2008, 23:331-339. 10.1093/mutage/gen039, 18644834.
7. Phillips ER, McKinnon PJ. DNA double-strand break repair and development. Oncogene 2007, 26:7799-7808. 10.1038/sj.onc.1210877, 18066093.
8. Marcais A, Suarez F, Sibon D, Frenzel L, Hermine O, Bazarbachi A. Therapeutic options for adult T-cell leukemia/lymphoma. Curr Oncol Rep 2013, 15:457-464. 10.1007/s11912-013-0332-6, 23943384.
9. Tsukasaki K, Hermine O, Bazarbachi A, Ratner L, Ramos JC, Harrington W, O'Mahony D, Janik JE, Bittencourt AL, Taylor GP, Yamaguchi K, Utsunomiya A, Tobinai K, Watanabe T. Definition, prognostic factors, treatment, and response criteria of adult T-cell leukemia-lymphoma: a proposal from an international consensus meeting. J Clin Oncol 2009, 27:453-459. 2737379, 19064971.
10. Bai XT, Nicot C. Overview on HTLV-1 p12, p8, p30, p13: accomplices in persistent infection and viral pathogenesis. Front Microbiol 2012, 3:400. 3518833, 23248621.
11. Wattel E, Vartanian JP, Pannetier C, Wain-Hobson S. Clonal expansion of human T-cell leukemia virus type I-infected cells in asymptomatic and symptomatic carriers without malignancy. J Virol 1995, 69:2863-2868. 188982, 7707509.
12. Nicot C, Dundr M, Johnson JM, Fullen JR, Alonzo N, Fukumoto R, Princler GL, Derse D, Misteli T, Franchini G. HTLV-I-encoded p30II is a post-transcriptional negative regulator of viral replication. Nat Med 2004, 10:197-201. 10.1038/nm984, 14730358.
13. Ko NL, Taylor JM, Bellon M, Bai XT, Shevtsov SP, Dundr M, Nicot C. PA28gamma is a novel corepressor of HTLV-1 replication and controls viral latency. Blood 2013, 121:791-800. 10.1182/blood-2012-03-420414, 3563364, 23104922.
14. Bellon M, Baydoun HH, Yao Y, Nicot C. HTLV-I Tax-dependent and -independent events associated with immortalization of human primary T lymphocytes. Blood 2010, 115:2441-2448. 10.1182/blood-2009-08-241117, 2845900, 20093405.
15. Tanaka A, Takahashi C, Yamaoka S, Nosaka T, Maki M, Hatanaka M. Oncogenic transformation by the tax gene of human T-cell leukemia virus type I in vitro. Proc Natl Acad Sci U S A 1990, 87:1071-1075. 10.1073/pnas.87.3.1071, 53412, 2300570.
16. Coscoy L, Gonzalez-Dunia D, Tangy F, Syan S, Brahic M, Ozden S. Molecular mechanism of tumorigenesis in mice transgenic for the human T cell leukemia virus Tax gene. Virology 1998, 248:332-341. 10.1006/viro.1998.9298, 9721242.
17. Grossman WJ, Kimata JT, Wong FH, Zutter M, Ley TJ, Ratner L. Development of leukemia in mice transgenic for the tax gene of human T-cell leukemia virus type I. Proc Natl Acad Sci U S A 1995, 92:1057-1061. 10.1073/pnas.92.4.1057, 42636, 7862633.
18. Nerenberg MI. An HTLV-I transgenic mouse model: role of the tax gene in pathogenesis in multiple organ systems. Curr Top Microbiol Immunol 1990, 160:121-128.
19. Green JE, Hinrichs SH, Vogel J, Jay G. Exocrinopathy resembling Sjogren's syndrome in HTLV-1 tax transgenic mice. Nature 1989, 341:72-74. 10.1038/341072a0, 2788824.
20. Giam CZ, Jeang KT. HTLV-1 Tax and adult T-cell leukemia. Front Biosci 2007, 12:1496-1507. 10.2741/2163, 17127397.
21. Marriott SJ, Semmes OJ. Impact of HTLV-I Tax on cell cycle progression and the cellular DNA damage repair response. Oncogene 2005, 24:5986-5995. 10.1038/sj.onc.1208976, 16155605.
22. Pise-Masison CA, Jeong SJ, Brady JN. Human T cell leukemia virus type 1: the role of Tax in leukemogenesis. Arch Immunol Ther Exp (Warsz) 2005, 53:283-296.
23. Taylor G. Molecular aspects of HTLV-I infection and adult T-cell leukaemia/lymphoma. J Clin Pathol 2007, 60:1392-1396. 2095577, 18042695.
24. Matsuoka M, Jeang KT. Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation. Nat Rev Cancer 2007, 7:270-280. 10.1038/nrc2111, 17384582.
25. Hall WW, Fujii M. Deregulation of cell-signaling pathways in HTLV-1 infection. Oncogene 2005, 24:5965-5975. 10.1038/sj.onc.1208975, 16155603.
26. Bellon M, Datta A, Brown M, Pouliquen JF, Couppie P, Kazanji M, Nicot C. Increased expression of telomere length regulating factors TRF1, TRF2 and TIN2 in patients with adult T-cell leukemia. Int J Cancer 2006, 119:2090-2097. 10.1002/ijc.22026, 16786598.
27. Sinha-Datta U, Horikawa I, Michishita E, Datta A, Sigler-Nicot JC, Brown M, Kazanji M, Barrett JC, Nicot C. Transcriptional activation of hTERT through the NF-kappaB pathway in HTLV-I-transformed cells. Blood 2004, 104:2523-2531. 10.1182/blood-2003-12-4251, 15226182.
28. Datta A, Nicot C. Telomere attrition induces a DNA double-strand break damage signal that reactivates p53 transcription in HTLV-I leukemic cells. Oncogene 2008, 27:1135-1141. 10.1038/sj.onc.1210718, 17704807.
29. Baydoun HH, Bai XT, Shelton S, Nicot C. HTLV-I tax increases genetic instability by inducing DNA double strand breaks during DNA replication and switching repair to NHEJ. PLoS One 2012, 7:e42226. 10.1371/journal.pone.0042226, 3423393, 22916124.
30. Boxus M, Twizere JC, Legros S, Kettmann R, Willems L. Interaction of HTLV-1 Tax with minichromosome maintenance proteins accelerates the replication timing program. Blood 2012, 119:151-160. 10.1182/blood-2011-05-356790, 22058115.
31. Chen L, Nievera CJ, Lee AY, Wu X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 2008, 283:7713-7720. 10.1074/jbc.M710245200, 18171670.
32. Rouet P, Smih F, Jasin M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc Natl Acad Sci U S A 1994, 91:6064-6068. 10.1073/pnas.91.13.6064, 44138, 8016116.
33. Nakachi S, Nakazato T, Ishikawa C, Kimura R, Mann DA, Senba M, Masuzaki H, Mori N. Human T-cell leukemia virus type 1 tax transactivates the matrix metalloproteinase 7 gene via JunD/AP-1 signaling. Biochim Biophys Acta 2011, 1813:731-741. 10.1016/j.bbamcr.2011.02.002, 21315773.
34. Sutton MD, Walker GC. Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination. Proc Natl Acad Sci U S A 2001, 98:8342-8349. 10.1073/pnas.111036998, 37441, 11459973.
35. Livneh Z. Keeping mammalian mutation load in check: regulation of the activity of error-prone DNA polymerases by p53 and p21. Cell Cycle 2006, 5:1918-1922. 10.4161/cc.5.17.3193, 16969082.
36. Avkin S, Sevilya Z, Toube L, Geacintov N, Chaney SG, Oren M, Livneh Z. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol Cell 2006, 22:407-413. 10.1016/j.molcel.2006.03.022, 16678112.
37. Betous R, Rey L, Wang G, Pillaire MJ, Puget N, Selves J, Biard DS, Shin-ya K, Vasquez KM, Cazaux C, Hoffmann JS. Role of TLS DNA polymerases eta and kappa in processing naturally occurring structured DNA in human cells. Mol Carcinog 2009, 48:369-378. 10.1002/mc.20509, 2696892, 19117014.
38. Klein HL. The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair (Amst) 2008, 7:686-693. 10.1016/j.dnarep.2007.12.008, 2430071, 18243065.
39. Budke B, Logan HL, Kalin JH, Zelivianskaia AS, Cameron MW, Miller LL, Stark JM, Kozikowski AP, Bishop DK, Connell PP. RI-1: a chemical inhibitor of RAD51 that disrupts homologous recombination in human cells. Nucleic Acids Res 2012, 40:7347-7357. 10.1093/nar/gks353, 3424541, 22573178.
40. Liu B, Liang MH, Kuo YL, Liao W, Boros I, Kleinberger T, Blancato J, Giam CZ. Human T-lymphotropic virus type 1 oncoprotein tax promotes unscheduled degradation of Pds1p/securin and Clb2p/cyclin B1 and causes chromosomal instability. Mol Cell Biol 2003, 23:5269-5281. 10.1128/MCB.23.15.5269-5281.2003, 165734, 12861013.
41. Kao SY, Marriott SJ. Disruption of nucleotide excision repair by the human T-cell leukemia virus type 1 Tax protein. J Virol 1999, 73:4299-4304. 104211, 10196328.
42. Suzuki T, Uchida-Toita M, Andoh T, Yoshida M. HTLV-1 tax oncoprotein binds to DNA topoisomerase I and inhibits its catalytic activity. Virology 2000, 270:291-298. 10.1006/viro.2000.0266, 10792988.
43. Jeang KT, Widen SG, Semmes OJ, Wilson SH. HTLV-I trans-activator protein, tax, is a trans-repressor of the human beta-polymerase gene. Science 1990, 247:1082-1084. 10.1126/science.2309119, 2309119.
44. Bavoux C, Hoffmann JS, Cazaux C. Adaptation to DNA damage and stimulation of genetic instability: the double-edged sword mammalian DNA polymerase kappa. Biochimie 2005, 87:637-646. 10.1016/j.biochi.2005.02.007, 15989980.
45. Stancel JN, McDaniel LD, Velasco S, Richardson J, Guo C, Friedberg EC. Polk mutant mice have a spontaneous mutator phenotype. DNA Repair (Amst) 2009, 8:1355-1362. 10.1016/j.dnarep.2009.09.003, 2787749, 19783230.
46. Burr KL, Velasco-Miguel S, Duvvuri VS, McDaniel LD, Friedberg EC, Dubrova YE. Elevated mutation rates in the germline of Polkappa mutant male mice. DNA Repair (Amst) 2006, 5:860-862. 10.1016/j.dnarep.2006.04.003, 16731053.
47. Choi JH, Pfeifer GP. The role of DNA polymerase eta in UV mutational spectra. DNA Repair (Amst) 2005, 4:211-220. 10.1016/j.dnarep.2004.09.006, 15590329.
48. Pise-Masison CA, Brady JN. Setting the stage for transformation: HTLV-1 Tax inhibition of p53 function. Front Biosci 2005, 10:919-930. 10.2741/1586, 15569630.
49. Morimoto H, Tsukada J, Kominato Y, Tanaka Y. Reduced expression of human mismatch repair genes in adult T-cell leukemia. Am J Hematol 2005, 78:100-107. 10.1002/ajh.20259, 15682421.
50. Zlatanou A, Despras E, Braz-Petta T, Boubakour-Azzouz I, Pouvelle C, Stewart GS, Nakajima S, Yasui A, Ishchenko AA, Kannouche PL. The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol eta in response to oxidative DNA damage in human cells. Mol Cell 2011, 43:649-662. 10.1016/j.molcel.2011.06.023, 21855803.