Nonreciprocal chromosomal translocations in renal cancer involve multiple DSBs and NHEJ associated with breakpoint inversion but not necessarily with transcription

Genes Chromosomes and Cancer

Volumn 52, Issue 4, 2013, Pages 402-409

  Ali, Hanif ^a,c   Daser, Angelika ^b,d   Dear, Paul ^b   Wood, Henry ^a   Rabbitts, Pamela ^a   Rabbitts, Terence ^a,e  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c Kymab Ltd   (United Kingdom)

^d SH Gen Forschungsgesellschaft   (Germany)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; GENOMIC DNA;

ARTICLE; CHROMOSOME INVERSION; CHROMOSOME TRANSLOCATION; COPY NUMBER VARIATION; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; GEL ELECTROPHORESIS; GENE DELETION; GENETIC TRANSCRIPTION; HUMAN; INVERSE POLYMERASE CHAIN REACTION; KIDNEY CARCINOMA; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

BASE SEQUENCE; CELL LINE, TUMOR; CHROMOSOME BREAKPOINTS; CHROMOSOME INVERSION; CHROMOSOMES, HUMAN, PAIR 3; CHROMOSOMES, HUMAN, PAIR 5; DNA BREAKS, DOUBLE-STRANDED; DNA COPY NUMBER VARIATIONS; DNA END-JOINING REPAIR; HUMANS; KIDNEY NEOPLASMS; MOLECULAR SEQUENCE DATA; TRANSCRIPTION, GENETIC; TRANSLOCATION, GENETIC;

EID: 84873734832     PISSN: 10452257     EISSN: 10982264     Source Type: Journal    
DOI: 10.1002/gcc.22038     Document Type: Article

References (34)

1. Aplan PD, Lombardi DP, Ginsberg AM, Cossman J, Bertness VL, Kirsch IR. 1990. Disruption of the human SCL locus by illegitimate V-(D)-J recombinase activity. Science 250: 1426-1429.
2. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Keira Cheetham R, Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS, Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, Rasolonjatovo IM, Reed MT, Rigatti R, Rodighiero C, Ross MT, Sabot A, Sankar SV, Scally A, Schroth GP, Smith ME, Smith VP, Spiridou A, Torrance PE, Tzonev SS, Vermaas EH, Walter K, Wu X, Zhang L, Alam MD, Anastasi C, Aniebo IC, Bailey DM, Bancarz IR, Banerjee S, Barbour SG, Baybayan PA, Benoit VA, Benson KF, Bevis C, Black PJ, Boodhun A, Brennan JS, Bridgham JA, Brown RC, Brown AA, Buermann DH, Bundu AA, Burrows JC, Carter NP, Castillo N, Chiara E Catenazzi M, Chang S, Neil Cooley R, Crake NR, Dada OO, Diakoumakos KD, Dominguez-Fernandez B, Earnshaw DJ, Egbujor UC, Elmore DW, Etchin SS, Ewan MR, Fedurco M, Fraser LJ, Fuentes Fajardo KV, Scott Furey W, George D, Gietzen KJ, Goddard CP, Golda GS, Granieri PA, Green DE, Gustafson DL, Hansen NF, Harnish K, Haudenschild CD, Heyer NI, Hims MM, Ho JT, Horgan AM, Hoschler K, Hurwitz S, Ivanov DV, Johnson MQ, James T, Huw Jones TA, Kang GD, Kerelska TH, Kersey AD, Khrebtukova I, Kindwall AP, Kingsbury Z, Kokko-Gonzales PI, Kumar A, Laurent MA, Lawley CT, Lee SE, Lee X, Liao AK, Loch JA, Lok M, Luo S, Mammen RM, Martin JW, McCauley PG, McNitt P, Mehta P, Moon KW, Mullens JW, Newington T, Ning Z, Ling Ng B, Novo SM, O'Neill MJ, Osborne MA, Osnowski A, Ostadan O, Paraschos LL, Pickering L, Pike AC, Pike AC, Chris Pinkard D, Pliskin DP, Podhasky J, Quijano VJ, Raczy C, Rae VH, Rawlings SR, Chiva Rodriguez A, Roe PM, Rogers J, Rogert Bacigalupo MC, Romanov N, Romieu A, Roth RK, Rourke NJ, Ruediger ST, Rusman E, Sanches-Kuiper RM, Schenker MR, Seoane JM, Shaw RJ, Shiver MK, Short SW, Sizto NL, Sluis JP, Smith MA, Ernest Sohna Sohna J, Spence EJ, Stevens K, Sutton N, Szajkowski L, Tregidgo CL, Turcatti G, Vandevondele S, Verhovsky Y, Virk SM, Wakelin S, Walcott GC, Wang J, Worsley GJ, Yan J, Yau L, Zuerlein M, Rogers J, Mullikin JC, Hurles ME, McCooke NJ, West JS, Oaks FL, Lundberg PL, Klenerman D, Durbin R, Smith AJ. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
3. Brandt VL, Roth DB. 2009. Recent insights into the formation of RAG-induced chromosomal translocations. Adv Exp Med Biol 650: 32-45.
4. Campbell PJ, Stephens PJ, Pleasance ED, O'Meara S, Li H, Santarius T, Stebbings LA, Leroy C, Edkins S, Hardy C, Teague JW, Menzies A, Goodhead I, Turner DJ, Clee CM, Quail MA, Cox A, Brown C, Durbin R, Hurles ME, Edwards PA, Bignell GR, Stratton MR, Futreal PA. 2008. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 40: 722-729.
5. Chiarle R, Zhang Y, Frock RL, Lewis SM, Molinie B, Ho YJ, Myers DR, Choi VW, Compagno M, Malkin DJ, Neuberg D, Monti S, Giallourakis CC, Gostissa M, Alt FW. 2011. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147: 107-119.
6. Daser A, Rabbitts TH. 2005. The versatile mixed lineage leukaemia gene MLL and its many associations in leukaemogenesis. Semin Cancer Biol 15: 175-188.
7. Daser A, Thangavelu M, Pannell R, Forster A, Sparrow L, Chang G, Dear PH, Rabbitts TH. 2006. Interrogation of genomes by Molecular Copy-number Counting (MCC). Nat Methods 3: 447-453.
8. Ebert T, Bander NH, Finstad CL, Ramsawak RD, Old LJ. 1990. Establishment and characterisation of human renal cancer and normal kidney cell lines. Cancer Res 50: 5531-5536.
9. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, Jia M, Shepherd R, Leung K, Menzies A, Teague JW, Campbell PJ, Stratton MR, Futreal PA. 2011. COSMIC: Mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 39: D945-D950.
10. Klein IA, Resch W, Jankovic M, Oliveira T, Yamane A, Nakahashi H, Di Virgilio M, Bothmer A, Nussenzweig A, Robbiani DF, Casellas R, Nussenzweig MC. 2011. Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147: 95-106.
11. Kovacs G, Szucs S, De Riese W, Baumgartel H. 1987. Specific chromosome aberration in human renal cell carcinoma. Int J Cancer 40: 171-178.
12. Kumar-Sinha C, Tomlins SA, Chinnaiyan AM. 2008. Recurrent gene fusions in prostate cancer. Nat Rev Cancer 8: 497-511.
13. H rearrangements in benign lymphoid tissues with follicular hyperplasia. Oncogene 6: 2271-2276.
14. Lin C, Yang L, Tanasa B, Hutt K, Ju BG, Ohgi K, Zhang J, Rose DW, Fu XD, Glass CK, Rosenfeld MG. 2009. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 139: 1069-1083.
15. Liu H, Cheng EHY, Hsieh JJD. 2009. MLL fusions. Canc Biol Therapy 8: 1204-1211.
16. Meaburn KJ, Misteli T, Soutoglou E. 2007. Spatial genome organisation in the formation of chromosomal translocations. Semin Cancer Biol 17: 80-90.
17. Mitelman F, Johansson B, Mertens F. 2007. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 7: 233-245.
18. Mitelman F, Johansson B, Mertens F, (editors.) 2012. Mitelman Database of Chromosome Aberrations in Cancer. Available at: http://cgap.nci.nih.gov/Chromosomes/Mitelman.
19. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102: 553-563.
20. Muramatsu M, Sankaranand VS, Anant S, Sugai M, Kinoshita K, Davidson NO, Honjo T. 1999. Specific expression of activation-induced cytidine deaminse (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem 25: 18470-18476.
21. Ochman H, Gerber AS, Hartl DL 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120: 621-623.
22. Petersen-Mahrt SK, Harris RS, Neuberger MS. 2002. AID mutates E. coli suggesting a DNA deamination mechanism for the antibody diversification. Nature 418: 99-103.
23. Rabbitts TH. 2009. Commonality but diversity in cancer gene fusions. Cell 137: 391-395.
24. Richardson C, Jasin M. 2000. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405: 697-700.
25. Robbiani DF, Bothmer A, Callen E, Reina-San-Martin B, Dorsett Y, Difilippantonio S, Bolland DJ, Chen HT, Corcoran AE, Nussenzweig A, Nussenzweig MC. 2008. AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations. Cell 135: 1028-1038.
26. Strefford JC, Stasevich I, Lane TM, Lu YJ, Oliver T, Young BD. 2005. A combination of molecular cytogenetic analyses reveals complex genetic alterations in conventional renal cell carcinoma. Cancer Gene Cytogene 159: 1-9.
27. Taylor BS, Barretina J, Maki RG, Antonescu CR, Singer S, Ladanyi M. 2011. Advances in sarcoma genomics and new therapeutic targets. Nat Rev Cancer 11: 541-557.
28. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer, R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. 2005. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 310: 644-648.
29. Venkatraman ES, Olshen AB 2007. A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23: 657-663.
30. Weinstock DM, Richardson CA, Elliott B, Jasin M. 2006. Modeling oncogenic translocations: Distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair (Amst) 5: 1065-1074.
31. Welch JP, Lee CL, Beatty-DeSana JW, Hoggard MJ, Cooledge JW, Hecht F, McCaw BK, Peakman D, Robinson A. 1975. Non-random occurrence of 7-14 translocations in human lymphocyte cultures. Nature 255: 241-245.
32. Williamson LM, Lees-Miller SP. 2011. Estrogen receptor alpha-mediated transcription induces cell cycle-dependent DNA double-strand breaks. Carcinogenesis 32: 279-285.
33. Wood HM, Belvedere O, Conway C, Daly C, Chalkley R, Bickerdike M, McKinley C, Egan P, Ross L, Hayward B, Morgan J, Davidson L, MacLeaanan K, Ong TK, Papagiannopoulos K, Cook I, Adam DJ, Taylor GR, Rabbitts P. 2010. Using next-generation sequencing for high resolution multiplex analysis of copy number variation from nanogram quantities of DNA from formalin-fixed paraffin-embedded specimens. Nucleic Acids Res 38: e151.
34. Zhang Y, McCord RP, Ho YJ, Lajoie BR, Hildebrand DG, Simon AC, Becker MS, Alt FW, Dekker J. 2012. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148: 908-921.