Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes

Cell

Volumn 147, Issue 1, 2011, Pages 95-106

  Klein, Isaac A ^a   Resch, Wolfgang ^c   Jankovic, Mila ^a   Oliveira, Thiago ^a,d   Yamane, Arito ^b,c   Nakahashi, Hirotaka ^b,c   Di Virgilio, Michela ^a   Bothmer, Anne ^a   Nussenzweig, Andre ^b   Robbiani, Davide F ^a   Casellas, Rafael ^b,c   Nussenzweig, Michel C ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; DOUBLE STRANDED DNA;

ANIMAL CELL; ARTICLE; B CELL LYMPHOMA; B LYMPHOCYTE; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; ENZYME INDUCTION; GENE REARRANGEMENT; GENE SEQUENCE; GENE TRANSLOCATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION INITIATION; TRANSLOCATION CAPTURE SEQUENCING;

EID: 80053502216     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.07.048     Document Type: Article

References (66)

1. A. Aguilera The connection between transcription and genomic instability EMBO J. 21 2002 195 201 (Pubitemid 34137281)
2. T. Akasaka, I.S. Lossos, and R. Levy BCL6 gene translocation in follicular lymphoma: a harbinger of eventual transformation to diffuse aggressive lymphoma Blood 102 2003 1443 1448 (Pubitemid 36988055)
3. G.M. Argast, K.M. Stephens, M.J. Emond, and R.J. Monnat Jr. I-PpoI and I-CreI homing site sequence degeneracy determined by random mutagenesis and sequential in vitro enrichment J. Mol. Biol. 280 1998 345 353 (Pubitemid 28327275)
4. S. Bea, I. Salaverria, L. Armengol, M. Pinyol, V. Fernandez, E.M. Hartmann, P. Jares, V. Amador, L. Hernandez, and A. Navarro Uniparental disomies, homozygous deletions, amplifications, and target genes in mantle cell lymphoma revealed by integrative high-resolution whole-genome profiling Blood 113 2009 3059 3069
5. A. Bothmer, D.F. Robbiani, M. Di Virgilio, S.F. Bunting, I.A. Klein, N. Feldhahn, J. Barlow, H.T. Chen, D. Bosque, and E. Callen Regulation of DNA End Joining, Resection, and Immunoglobulin Class Switch Recombination by 53BP1 Mol. Cell 42 2011 319 329
6. D. Branzei, and M. Foiani Maintaining genome stability at the replication fork Nat. Rev. Mol. Cell Biol. 11 2010 208 219
7. P.J. Campbell, P.J. Stephens, E.D. Pleasance, S. O'Meara, H. Li, T. Santarius, L.A. Stebbings, C. Leroy, S. Edkins, and C. Hardy Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing Nat. Genet. 40 2008 722 729 (Pubitemid 351748860)
8. J. Chaudhuri, and F.W. Alt Class-switch recombination: interplay of transcription, DNA deamination and DNA repair Nat. Rev. Immunol. 4 2004 541 552 (Pubitemid 38931769)
9. S. Cory, M. Graham, E. Webb, L. Corcoran, and J.M. Adams Variant (6;15) translocations in murine plasmacytomas involve a chromosome 15 locus at least 72 kb from the c-myc oncogene EMBO J. 4 1985 675 681
10. T. Cremer, and C. Cremer Chromosome territories, nuclear architecture and gene regulation in mammalian cells Nat. Rev. Genet. 2 2001 292 301 (Pubitemid 33674777)
11. J.M. Di Noia, and M.S. Neuberger Molecular mechanisms of antibody somatic hypermutation Annu. Rev. Biochem. 76 2007 1 22
12. R.R. Einerson, M.E. Law, H.E. Blair, P.J. Kurtin, R.F. McClure, R.P. Ketterling, H.C. Flynn, A. Dogan, and E.D. Remstein Novel FISH probes designed to detect IGK-MYC and IGL-MYC rearrangements in B-cell lineage malignancy identify a new breakpoint cluster region designated BVR2 Leukemia 20 2006 1790 1799 (Pubitemid 44574990)
13. S. Franco, M. Gostissa, S. Zha, D.B. Lombard, M.M. Murphy, A.A. Zarrin, C. Yan, S. Tepsuporn, J.C. Morales, and M.M. Adams H2AX prevents DNA breaks from progressing to chromosome breaks and translocations Mol. Cell 21 2006 201 214 (Pubitemid 43099936)
14. C.E. Gauwerky, K. Huebner, M. Isobe, P.C. Nowell, and C.M. Croce Activation of MYC in a masked t(8;17) translocation results in an aggressive B-cell leukemia Proc. Natl. Acad. Sci. USA 86 1989 8867 8871 (Pubitemid 20010326)
15. S. Gesk, W. Klapper, J.I. Martin-Subero, I. Nagel, L. Harder, K. Fu, H.W. Bernd, D.D. Weisenburger, R. Parwaresch, and R. Siebert A chromosomal translocation in cyclin D1-negative/cyclin D2-positive mantle cell lymphoma fuses the CCND2 gene to the IGK locus Blood 108 2006 1109 1110 (Pubitemid 44154656)
16. J.M. Goldman, and J.V. Melo Chronic myeloid leukemia-advances in biology and new approaches to treatment N. Engl. J. Med. 349 2003 1451 1464 (Pubitemid 37211061)
17. M.S. Gordon, C.M. Kanegai, J.R. Doerr, and R. Wall Somatic hypermutation of the B cell receptor genes B29 (Igbeta, CD79b) and mb1 (Igalpha, CD79a) Proc. Natl. Acad. Sci. USA 100 2003 4126 4131 (Pubitemid 36418168)
18. M. Gostissa, C.T. Yan, J.M. Bianco, M. Cogne, E. Pinaud, and F.W. Alt Long-range oncogenic activation of Igh-c-myc translocations by the Igh 3′ regulatory region Nature 462 2009 803 807
19. P. Gottipati, and T. Helleday Transcription-associated recombination in eukaryotes: link between transcription, replication and recombination Mutagenesis 24 2009 203 210
20. T. Honjo Does AID need another aid? Nat. Immunol. 3 2002 800 801
21. K. Huppi, D. Siwarski, R. Skurla, D. Klinman, and J.F. Mushinski Pvt-1 transcripts are found in normal tissues and are altered by reciprocal(6;15) translocations in mouse plasmacytomas Proc. Natl. Acad. Sci. USA 87 1990 6964 6968
22. S. Iida, P.H. Rao, R. Ueda, R.S. Chaganti, and R. Dalla-Favera Chromosomal rearrangement of the PAX-5 locus in lymphoplasmacytic lymphoma with t(9;14)(p13;q32) Leuk. Lymphoma 34 1999 25 33 (Pubitemid 29248656)
23. L. Impera, F. Albano, C. Lo Cunsolo, S. Funes, P. Iuzzolino, F. Laveder, I. Panagopoulos, M. Rocchi, and C.T. Storlazzi A novel fusion 5′AFF3/3′BCL2 originated from a t(2;18)(q11.2;q21.33) translocation in follicular lymphoma Oncogene 27 2008 6187 6190
24. M. Jankovic, D.F. Robbiani, Y. Dorsett, T. Eisenreich, Y. Xu, A. Tarakhovsky, A. Nussenzweig, and M.C. Nussenzweig Role of the translocation partner in protection against AID-dependent chromosomal translocations Proc. Natl. Acad. Sci. USA 107 2010 187 192
25. R. Kuppers Mechanisms of B-cell lymphoma pathogenesis Nat. Rev. Cancer 5 2005 251 262 (Pubitemid 40488631)
26. E. Lieberman-Aiden, N.L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B.R. Lajoie, P.J. Sabo, and M.O. Dorschner Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
27. M. Liu, J.L. Duke, D.J. Richter, C.G. Vinuesa, C.C. Goodnow, S.H. Kleinstein, and D.G. Schatz Two levels of protection for the B cell genome during somatic hypermutation Nature 451 2008 841 845 (Pubitemid 351253166)
28. D. Lu, and J.J. Yunis Cloning, expression and localization of an RNA helicase gene from a human lymphoid cell line with chromosomal breakpoint 11q23.3 Nucleic Acids Res. 20 1992 1967 1972
29. G.K. Mahowald, J.M. Baron, M.A. Mahowald, S. Kulkarni, A.L. Bredemeyer, C.H. Bassing, and B.P. Sleckman Aberrantly resolved RAG-mediated DNA breaks in Atm-deficient lymphocytes target chromosomal breakpoints in cis Proc. Natl. Acad. Sci. USA 106 2009 18339 18344
30. X. Mao, D. Lillington, F. Child, R. Russell-Jones, B. Young, and S. Whittaker Comparative genomic hybridization analysis of primary cutaneous B-cell lymphomas: identification of common genomic alterations in disease pathogenesis Genes Chromosomes Cancer 35 2002 144 155 (Pubitemid 34919971)
31. A. Mottok, C. Renne, M. Seifert, E. Oppermann, W. Bechstein, M.L. Hansmann, R. Kuppers, and A. Brauninger Inactivating SOCS1 mutations are caused by aberrant somatic hypermutation and restricted to a subset of B-cell lymphoma entities Blood 114 2009 4503 4506
32. M. Muramatsu, K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme Cell 102 2000 553 563
33. Y. Nakamura, N. Takahashi, E. Kakegawa, K. Yoshida, Y. Ito, H. Kayano, N. Niitsu, I. Jinnai, and M. Bessho The GAS5 (growth arrest-specific transcript 5) gene fuses to BCL6 as a result of t(1;3)(q25;q27) in a patient with B-cell lymphoma Cancer Genet. Cytogenet. 182 2008 144 149 (Pubitemid 351491334)
34. A. Nussenzweig, and M.C. Nussenzweig Origin of chromosomal translocations in lymphoid cancer Cell 141 2010 27 38
35. I.M. Okazaki, H. Hiai, N. Kakazu, S. Yamada, M. Muramatsu, K. Kinoshita, and T. Honjo Constitutive expression of AID leads to tumorigenesis J. Exp. Med. 197 2003 1173 1181 (Pubitemid 36570072)
36. L. Pasqualucci, P. Neumeister, T. Goossens, G. Nanjangud, R.S. Chaganti, R. Kuppers, and R. Dalla-Favera Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas Nature 412 2001 341 346 (Pubitemid 32691848)
37. R. Pavri, A. Gazumyan, M. Jankovic, M. Di Virgilio, I. Klein, C. Ansarah-Sobrinho, W. Resch, A. Yamane, B. Reina San-Martin, and V. Barreto Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5 Cell 143 2010 122 133
38. J.U. Peled, F.L. Kuang, M.D. Iglesias-Ussel, S. Roa, S.L. Kalis, M.F. Goodman, and M.D. Scharff The biochemistry of somatic hypermutation Annu. Rev. Immunol. 26 2008 481 511 (Pubitemid 351600383)
39. E.D. Pleasance, R.K. Cheetham, P.J. Stephens, D.J. McBride, S.J. Humphray, C.D. Greenman, I. Varela, M.L. Lin, G.R. Ordonez, and G.R. Bignell A comprehensive catalogue of somatic mutations from a human cancer genome Nature 463 2010 191 196
40. E.D. Pleasance, P.J. Stephens, S. O'Meara, D.J. McBride, A. Meynert, D. Jones, M.L. Lin, D. Beare, K.W. Lau, and C. Greenman A small-cell lung cancer genome with complex signatures of tobacco exposure Nature 463 2010 184 190
41. M. Potter Neoplastic development in plasma cells Immunol. Rev. 194 2003 177 195 (Pubitemid 36886436)
42. T.H. Rabbitts Commonality but diversity in cancer gene fusions Cell 137 2009 391 395
43. A.R. Ramiro, M. Jankovic, E. Callen, S. Difilippantonio, H.T. Chen, K.M. McBride, T.R. Eisenreich, J. Chen, R.A. Dickins, and S.W. Lowe Role of genomic instability and p53 in AID-induced c-myc-Igh translocations Nature 440 2006 105 109 (Pubitemid 43336276)
44. A. Ramiro, B. Reina San-Martin, K. McBride, M. Jankovic, V. Barreto, A. Nussenzweig, and M.C. Nussenzweig The role of activation-induced deaminase in antibody diversification and chromosome translocations Adv. Immunol. 94 2007 75 107 (Pubitemid 46856608)
45. P. Revy, T. Muto, Y. Levy, F. Geissmann, A. Plebani, O. Sanal, N. Catalan, M. Forveille, R. Dufourcq-Labelouse, and A. Gennery Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2) Cell 102 2000 565 575
46. N. Riggi, and I. Stamenkovic The Biology of Ewing sarcoma Cancer Lett. 254 2007 1 10 (Pubitemid 47058800)
47. D.F. Robbiani, A. Bothmer, E. Callen, B. Reina-San-Martin, Y. Dorsett, S. Difilippantonio, D.J. Bolland, H.T. Chen, A.E. Corcoran, and A. Nussenzweig AID is required for the chromosomal breaks in c-myc that lead to c-myc/IgH translocations Cell 135 2008 1028 1038
48. D.F. Robbiani, S. Bunting, N. Feldhahn, A. Bothmer, J. Camps, S. Deroubaix, K.M. McBride, I.A. Klein, G. Stone, and T.R. Eisenreich AID produces DNA double-strand breaks in non-Ig genes and mature B cell lymphomas with reciprocal chromosome translocations Mol. Cell 36 2009 631 641
49. J.J. Roix, P.G. McQueen, P.J. Munson, L.A. Parada, and T. Misteli Spatial proximity of translocation-prone gene loci in human lymphomas Nat. Genet. 34 2003 287 291 (Pubitemid 36792860)
50. S. Rosebeck, L. Madden, X. Jin, S. Gu, I.J. Apel, A. Appert, R.A. Hamoudi, H. Noels, X. Sagaert, and P. Van Loo Cleavage of NIK by the API2-MALT1 fusion oncoprotein leads to noncanonical NF-kappaB activation Science 331 2011 468 472
51. H.M. Shen, A. Peters, B. Baron, X. Zhu, and U. Storb Mutation of BCL-6 gene in normal B cells by the process of somatic hypermutation of Ig genes Science 280 1998 1750 1752 (Pubitemid 28283498)
52. O. Staszewski, R.E. Baker, A.J. Ucher, R. Martier, J. Stavnezer, and J.E. Guikema Activation-induced cytidine deaminase induces reproducible DNA breaks at many non-Ig Loci in activated B cells Mol. Cell 41 2011 232 242
53. J. Stavnezer, J.E. Guikema, and C.E. Schrader Mechanism and regulation of class switch recombination Annu. Rev. Immunol. 26 2008 261 292 (Pubitemid 351600377)
54. P.J. Stephens, D.J. McBride, M.L. Lin, I. Varela, E.D. Pleasance, J.T. Simpson, L.A. Stebbings, C. Leroy, S. Edkins, and L.J. Mudie Complex landscapes of somatic rearrangement in human breast cancer genomes Nature 462 2009 1005 1010
55. U. Storb, H.M. Shen, S. Longerich, S. Ratnam, A. Tanaka, G. Bozek, and S. Pylawka Targeting of AID to immunoglobulin genes Adv. Exp. Med. Biol. 596 2007 83 91
56. Y. Takeuchi, T. Horiuchi, and T. Kobayashi Transcription-dependent recombination and the role of fork collision in yeast rDNA Genes Dev. 17 2003 1497 1506 (Pubitemid 36734707)
57. B.J. Thomas, and R. Rothstein Elevated recombination rates in transcriptionally active DNA Cell 56 1989 619 630
58. A.G. Tsai, and M.R. Lieber Mechanisms of chromosomal rearrangement in the human genome BMC Genomics 11 Suppl 1 2010 S1
59. A.G. Tsai, H. Lu, S.C. Raghavan, M. Muschen, C.L. Hsieh, and M.R. Lieber Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity Cell 135 2008 1130 1142
60. C. Ueda, T. Akasaka, M. Kurata, Y. Maesako, M. Nishikori, R. Ichinohasama, K. Imada, T. Uchiyama, and H. Ohno The gene for interleukin-21 receptor is the partner of BCL6 in t(3;16)(q27;p11), which is recurrently observed in diffuse large B-cell lymphoma Oncogene 21 2002 368 376 (Pubitemid 34123799)
61. J.H. Wang, M. Gostissa, C.T. Yan, P. Goff, T. Hickernell, E. Hansen, S. Difilippantonio, D.R. Wesemann, A.A. Zarrin, and K. Rajewsky Mechanisms promoting translocations in editing and switching peripheral B cells Nature 460 2009 231 236
62. S. Wong, and O.N. Witte The BCR-ABL story: bench to bedside and back Annu. Rev. Immunol. 22 2004 247 306 (Pubitemid 38680424)
63. A. Yamane, W. Resch, N. Kuo, S. Kuchen, Z. Li, H.W. Sun, D.F. Robbiani, K. McBride, M.C. Nussenzweig, and R. Casellas Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes Nat. Immunol. 12 2011 62 69
64. C.T. Yan, C. Boboila, E.K. Souza, S. Franco, T.R. Hickernell, M. Murphy, S. Gumaste, M. Geyer, A.A. Zarrin, and J.P. Manis IgH class switching and translocations use a robust non-classical end-joining pathway Nature 449 2007 478 482 (Pubitemid 47509538)
65. S. Yoshida, Y. Kaneita, Y. Aoki, M. Seto, S. Mori, and M. Moriyama Identification of heterologous translocation partner genes fused to the BCL6 gene in diffuse large B-cell lymphomas: 5′-RACE and LA - PCR analyses of biopsy samples Oncogene 18 1999 7994 7999 (Pubitemid 30050560)
66. Y. Zhang, M. Gostissa, D.G. Hildebrand, M.S. Becker, C. Boboila, R. Chiarle, S. Lewis, and F.W. Alt The role of mechanistic factors in promoting chromosomal translocations found in lymphoid and other cancers Adv. Immunol. 106 2010 93 133