Genomic rearrangements in inherited disease and cancer

Seminars in Cancer Biology

Volumn 20, Issue 4, 2010, Pages 222-233

  Chen, Jian Min ^a,b,c   Cooper, David N ^d   Férec, Claude ^a,b,c,e   Kehrer Sawatzki, Hildegard ^f   Patrinos, George P ^g  

^a ETABLISSEMENT FRANÇAIS DU SANG   (France)

^b INSERM   (France)

^c FACULTÉ DE MÉDECINE ET DES SCIENCES DE LA SANTÉ   (France)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e CHU MORVAN   (France)

^f UNIVERSITY OF ULM   (Germany)

^g UNIVERSITY OF PATRAS   (Greece)

Author keywords

Cancer; Copy number variation; Genomic rearrangements; Homologous recombination; Non homologous end joining

Indexed keywords

CHROMOSOME DELETION; CHROMOSOME DUPLICATION; CHROMOSOME INSERTION; CHROMOSOME INVERSION; CHROMOSOME TRANSLOCATION; DNA SEQUENCE; DNA STRUCTURE; GENE CONVERSION; GENE MUTATION; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC DISORDER; HOMOLOGOUS RECOMBINATION; HUMAN; LONG INTERSPERSED REPEAT; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; MALIGNANT NEOPLASTIC DISEASE; NUCLEOTIDE SEQUENCE; REVIEW; SEQUENCE ANALYSIS; TELOMERE;

CHROMOSOME ABERRATIONS; GENETIC DISEASES, INBORN; GENOME, HUMAN; HUMANS; MODELS, BIOLOGICAL; MUTATION; NEOPLASMS; RECOMBINATION, GENETIC; TRANSLOCATION, GENETIC;

EID: 77956849313     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2010.05.007     Document Type: Review

References (96)

1. Sebat J., Lakshmi B., Troge J., Alexander J., Young J., Lundin P., et al. Large-scale copy number polymorphism in the human genome. Science 2004, 305:525-528.
2. Iafrate A.J., Feuk L., Rivera M.N., Listewnik M.L., Donahoe P.K., Qi Y., et al. Detection of large-scale variation in the human genome. Nat Genet 2004, 36:949-951.
3. Scherer S.W., Lee C., Birney E., Altshuler D.M., Eichler E.E., Carter N.P., et al. Challenges and standards in integrating surveys of structural variation. Nat Genet 2007, 39:S7-S15.
4. Chen J.M., Stenson P.D., Cooper D.N., Férec C. A systematic analysis of LINE-1 endonuclease-dependent retrotranspositional events causing human genetic disease. Hum Genet 2005, 117:411-427.
5. Babushok D.V., Kazazian H.H. Progress in understanding the biology of the human mutagen LINE-1. Hum Mutat 2007, 28:527-539.
6. Belancio V.P., Deininger P.L., Roy-Engel A.M. LINE dancing in the human genome: transposable elements and disease. Genome Med 2009, 1:97.
7. Pennaneach V., Putnam C.D., Kolodner R.D. Chromosome healing by de novo telomere addition in Saccharomyces cerevisiae. Mol Microbiol 2006, 59:1357-1368.
8. Jain S., Sugawara N., Lydeard J., Vaze M., Tanguy Le Gac N., Haber J.E. A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev 2009, 23:291-303.
9. Ip S.C., Rass U., Blanco M.G., Flynn H.R., Skehel J.M., West S.C. Identification of Holliday junction resolvases from humans and yeast. Nature 2008, 456:357-361.
10. Gu W., Zhang F., Lupski J.R. Mechanisms for human genomic rearrangements. Pathogenetics 2008, 1:4.
11. Carvalho C.M., Lupski J.R. Copy number variation at the breakpoint region of isochromosome 17q. Genome Res 2008, 18:1724-1732.
12. Forbes S.H., Dorschner M.O., Le R., Stephens K. Genomic context of paralogous recombination hotspots mediating recurrent NF1 region microdeletion. Genes Chrom Cancer 2004, 41:12-25.
13. Raedt T.D., Stephens M., Heyns I., Brems H., Thijs D., Messiaen L., et al. Conservation of hotspots for recombination in low-copy repeats associated with the NF1 microdeletion. Nat Genet 2006, 38:1419-1423.
14. Upadhyaya M., Ruggieri M., Maynard J., Osborn M., Hartog C., Mudd S., et al. Gross deletions of the neurofibromatosis type 1 (NF1) gene are predominantly of maternal origin and commonly associated with a learning disability, dysmorphic features and developmental delay. Hum Genet 1998, 102:591-597.
15. Lopez Correa C., Brems H., Lazaro C., Marynen P., Legius E. Unequal meiotic crossover: a frequent cause of NF1 microdeletions. Am J Hum Genet 2000, 66:1969-1974.
16. Palau F., Lofgren A., De Jonghe P., Bort S., Nelis E., Sevilla T., et al. Origin of the de novo duplication in Charcot-Marie-Tooth disease type 1A: unequal nonsister chromatid exchange during spermatogenesis. Hum Mol Genet 1993, 2:2031-2035.
17. Lopes J., Vandenberghe A., Tardieu S., Ionasescu V., Levy N., Wood N., et al. Sex-dependent rearrangements resulting in CMT1A and HNPP. Nat Genet 1997, 17:136-137.
18. Bengesser K.C.D., Steinmann K., Kluwe L., Chuzhanova N.A., Wimmer K., Tatagiba M., et al. A novel third type of recurrent NF1 microdeletion mediated by non-allelic homologous recombination between LRRC37B-containing low-copy repeats in 17q11.2. Hum Mutat 2010, 31:742-751.
19. Steinmann K., Cooper D.N., Kluwe L., Chuzhanova N.A., Senger C., Serra E., et al. Type 2 NF1 deletions are highly unusual by virtue of the absence of nonallelic homologous recombination hotspots and an apparent preference for female mitotic recombination. Am J Hum Genet 2007, 81:1201-1220.
20. Roehl A.C., Cooper D.N., Kluwe L., Helbrich A., Wimmer K., Hogel J., et al. Extended runs of homozygosity at 17q11. 2: an association with type-2 NF1 deletions?. Hum Mutat 2010, 31:325-334.
21. McQuillan R., Leutenegger A.L., Abdel-Rahman R., Franklin C.S., Pericic M., Barac-Lauc L., et al. Runs of homozygosity in European populations. Am J Hum Genet 2008, 83:359-372.
22. Bacolod M.D., Schemmann G.S., Giardina S.F., Paty P., Notterman D.A., Barany F. Emerging paradigms in cancer genetics: some important findings from high-density single nucleotide polymorphism array studies. Cancer Res 2009, 69:723-727.
23. Assie G., LaFramboise T., Platzer P., Eng C. Frequency of germline genomic homozygosity associated with cancer cases. JAMA 2008, 299:1437-1445.
24. Bacolod M.D., Schemmann G.S., Wang S., Shattock R., Giardina S.F., Zeng Z., et al. The signatures of autozygosity among patients with colorectal cancer. Cancer Res 2008, 68:2610-2621.
25. Chen J.M., Cooper D.N., Chuzhanova N., Férec C., Patrinos G.P. Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet 2007, 8:762-775.
26. Haber J.E., Ira G., Malkova A., Sugawara N. Repairing a double-strand chromosome break by homologous recombination: revisiting Robin Holliday's model. Philos Trans R Soc Lond B Biol Sci 2004, 359:79-86.
27. Chen J.M., Férec C., Cooper D.N. Closely spaced multiple mutations as potential signatures of transient hypermutability in human genes. Hum Mutat 2009, 30:1435-1448.
28. McEachern M.J., Haber J.E. Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem 2006, 75:111-135.
29. Smith C.E., Llorente B., Symington L.S. Template switching during break-induced replication. Nature 2007, 447:102-105.
30. Hastings P.J., Lupski J.R., Rosenberg S.M., Ira G. Mechanisms of change in gene copy number. Nat Rev Genet 2009, 10:551-564.
31. Lieber M.R. The mechanism of human nonhomologous DNA end joining. J Biol Chem 2008, 283:1-5.
32. McVey M., Lee S.E. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet 2008, 24:529-538.
33. Pardo B., Gomez-Gonzalez B., Aguilera A. DNA repair in mammalian cells: DNA double-strand break repair: how to fix a broken relationship. Cell Mol Life Sci 2009, 66:1039-1056.
34. Buysse K., Antonacci F., Callewaert B., Loeys B., Frankel U., Siu V., et al. Unusual 8p inverted duplication deletion with telomere capture from 8q. Eur J Med Genet 2009, 52:31-36.
35. Yatsenko S.A., Brundage E.K., Roney E.K., Cheung S.W., Chinault A.C., Lupski J.R. Molecular mechanisms for subtelomeric rearrangements associated with the 9q34.3 microdeletion syndrome. Hum Mol Genet 2009, 18:1924-1936.
36. Roth D.B., Chang X.B., Wilson J.H. Comparison of filler DNA at immune, nonimmune, and oncogenic rearrangements suggests multiple mechanisms of formation. Mol Cell Biol 1989, 9:3049-3057.
37. McClintock B. Chromosome organization and genic expression. Cold Spring Harb Symp Quant Biol 1951, 16:13-47.
38. Soutoglou E., Dorn J.F., Sengupta K., Jasin M., Nussenzweig A., Ried T., et al. Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 2007, 9:675-682.
39. Nikiforova M.N., Stringer J.R., Blough R., Medvedovic M., Fagin J.A., Nikiforov Y.E. Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 2000, 290:138-141.
40. Meaburn K.J., Misteli T., Soutoglou E. Spatial genome organization in the formation of chromosomal translocations. Semin Cancer Biol 2007, 17:80-90.
41. Tomlins S.A., Rhodes D.R., Perner S., Dhanasekaran S.M., Mehra R., Sun X.W., et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310:644-648.
42. Lin C., Yang L., Tanasa B., Hutt K., Ju B.G., Ohgi K., et al. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 2009, 139:1069-1083.
43. Mani R.S., Tomlins S.A., Callahan K., Ghosh A., Nyati M.K., Varambally S., et al. Induced chromosomal proximity and gene fusions in prostate cancer. Science 2009, 326:1230.
44. Mathas S., Misteli T. The dangers of transcription. Cell 2009, 139:1047-1049.
45. Misteli T., Soutoglou E. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 2009, 10:243-254.
46. Ma J.L., Kim E.M., Haber J.E., Lee S.E. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol Cell Biol 2003, 23:8820-8828.
47. Yan C.T., Boboila C., Souza E.K., Franco S., Hickernell T.R., Murphy M., et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007, 449:478-482.
48. Chen J.M., Chuzhanova N., Stenson P.D., Férec C., Cooper D.N. Meta-analysis of gross insertions causing human genetic disease: novel mutational mechanisms and the role of replication slippage. Hum Mutat 2005, 25:207-221.
49. Chen J.M., Chuzhanova N., Stenson P.D., Férec C., Cooper D.N. Complex gene rearrangements caused by serial replication slippage. Hum Mutat 2005, 26:125-134.
50. Chen J.M., Chuzhanova N., Stenson P.D., Férec C., Cooper D.N. Intrachromosomal serial replication slippage in trans gives rise to diverse genomic rearrangements involving inversions. Hum Mutat 2005, 26:362-373.
51. Lee J.A., Carvalho C.M., Lupski J.R. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 2007, 131:1235-1247.
52. Chauvin A., Chen J.M., Quemener S., Masson E., Kehrer-Sawatzki H., Ohmle B., et al. Elucidation of the complex structure and origin of the human trypsinogen locus triplication. Hum Mol Genet 2009, 18:3605-3614.
53. Sheen C.R., Jewell U.R., Morris C.M., Brennan S.O., Férec C., George P.M., et al. Double complex mutations involving F8 and FUNDC2 caused by distinct break-induced replication. Hum Mutat 2007, 28:1198-1206.
54. Koszul R., Caburet S., Dujon B., Fischer G. Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J 2004, 23:234-243.
55. Bauters M., Van Esch H., Friez M.J., Boespflug-Tanguy O., Zenker M., Vianna-Morgante A.M., et al. Nonrecurrent MECP2 duplications mediated by genomic architecture-driven DNA breaks and break-induced replication repair. Genome Res 2008, 18:847-858.
56. Collie A., Landsverk M., Ruzzo E., Mefford H., Buysse K., Adkins J., et al. Non-recurrent SEPT9 duplications cause hereditary neuralgic amyotrophy. J Med Genet 2009, doi:10.1136/jmg.2009.072348.
57. Hastings P.J., Ira G., Lupski J.R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet 2009, 5:e1000327.
58. Zhang F., Khajavi M., Connolly A.M., Towne C.F., Batish S.D., Lupski J.R. The DNA replication FoSTeS/MMBIR mechanism can generate genomic, genic and exonic complex rearrangements in humans. Nat Genet 2009, 41:849-853.
59. Abeysinghe S.S., Stenson P.D., Krawczak M., Cooper D.N. Gross Rearrangement Breakpoint Database (GRaBD). Hum Mutat 2004, 23:219-221.
60. Abeysinghe S.S., Chuzhanova N., Krawczak M., Ball E.V., Cooper D.N. Translocation and gross deletion breakpoints in human inherited disease and cancer I: Nucleotide composition and recombination-associated motifs. Hum Mutat 2003, 22:229-244.
61. Chuzhanova N., Abeysinghe S.S., Krawczak M., Cooper D.N. Translocation and gross deletion breakpoints in human inherited disease and cancer II: Potential involvement of repetitive sequence elements in secondary structure formation between DNA ends. Hum Mutat 2003, 22:245-251.
62. Bacolla A., Jaworski A., Larson J.E., Jakupciak J.P., Chuzhanova N., Abeysinghe S.S., et al. Breakpoints of gross deletions coincide with non-B DNA conformations. Proc Natl Acad Sci U S A 2004, 101:14162-14167.
63. Raghavan S.C., Lieber M.R. DNA structures at chromosomal translocation sites. Bioessays 2006, 28:480-494.
64. Bacolla A., Wells R.D. Non-B DNA conformations as determinants of mutagenesis and human disease. Mol Carcinog 2009, 48:273-285.
65. Herbert A., Rich A. Left-handed Z-DNA: structure and function. Genetica 1999, 106:37-47.
66. Hirai H., Ogawa S., Kurokawa M., Yazaki Y., Mitani K. Molecular characterization of the genomic breakpoints in a case of t(3;21)(q26;q22). Genes Chrom Cancer 1999, 26:92-96.
67. Cao X., Eu K.W., Seow-Choen F., Zhao Y., Cheah P.Y. Topoisomerase-I- and Alu-mediated genomic deletions of the APC gene in familial adenomatous polyposis. Hum Genet 2001, 108:436-442.
68. Frank-Kamenetskii M.D., Mirkin S.M. Triplex DNA structures. Annu Rev Biochem 1995, 64:65-95.
69. Chuzhanova N., Chen J.M., Bacolla A., Patrinos G.P., Férec C., Wells R.D., et al. Gene conversion causing human inherited disease: evidence for involvement of non-B-DNA-forming sequences and recombination-promoting motifs in DNA breakage and repair. Hum Mutat 2009, 30:1189-1198.
70. Turner D.J., Miretti M., Rajan D., Fiegler H., Carter N.P., Blayney M.L., et al. Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nat Genet 2008, 40:90-95.
71. Quemener S., Chen J.M., Chuzhanova N., Benech C., Casals T., Macek M., et al. Complete ascertainment of intragenic copy number mutations (CNMs) in the CFTR gene and its implications for CNM formation at other autosomal loci. Hum Mutat 2010, 31:421-428.
72. Conrad D.F., Pinto D., Redon R., Feuk L., Gokcumen O., Zhang Y., et al. Origins and functional impact of copy number variation in the human genome. Nature 2009.
73. Chen J.M., Masson E., Le Marechal C., Férec C. Copy number variations in chronic pancreatitis. Cytogenet Genome Res 2008, 123:102-107.
74. Haverfield E.V., Whited A.J., Petras K.S., Dobyns W.B., Das S. Intragenic deletions and duplications of the LIS1 and DCX genes: a major disease-causing mechanism in lissencephaly and subcortical band heterotopia. Eur J Hum Genet 2009, 17:911-918.
75. Stratton M.R., Campbell P.J., Futreal P.A. The cancer genome. Nature 2009, 458:719-724.
76. Forbes S.A., Tang G., Bindal N., Bamford S., Dawson E., Cole C., et al. COSMIC (the Catalogue of Somatic Mutations in Cancer): a resource to investigate acquired mutations in human cancer. Nucleic Acids Res 2010, 38:D652-D657.
77. Futreal P.A., Coin L., Marshall M., Down T., Hubbard T., Wooster R., et al. A census of human cancer genes. Nat Rev Cancer 2004, 4:177-183.
78. Aman P. Fusion oncogenes in tumor development. Semin Cancer Biol 2005, 15:236-243.
79. Teixeira M.R. Recurrent fusion oncogenes in carcinomas. Crit Rev Oncog 2006, 12:257-271.
80. Ortiz de Mendibil I., Vizmanos J.L., Novo F.J. Signatures of selection in fusion transcripts resulting from chromosomal translocations in human cancer. PLoS One 2009, 4:e4805.
81. Albertson D.G. Gene amplification in cancer. Trends Genet 2006, 22:447-455.
82. Tanaka H., Cao Y., Bergstrom D.A., Kooperberg C., Tapscott S.J., Yao M.C. Intrastrand annealing leads to the formation of a large DNA palindrome and determines the boundaries of genomic amplification in human cancer. Mol Cell Biol 2007, 27:1993-2002.
83. Santarius T., Shipley J., Brewer D., Stratton M.R., Cooper C.S. A census of amplified and overexpressed human cancer genes. Nat Rev Cancer 2010, 10:59-64.
84. Borg J., Georgitsi M., Aleporou-Marinou V., Kollia P., Patrinos G.P. Genetic recombination as a major cause of mutagenesis in the human globin gene clusters. Clin Biochem 2009, 42:1839-1850.
85. Velculescu V.E. Defining the blueprint of the cancer genome. Carcinogenesis 2008, 29:1087-1091.
86. Stephens P.J., McBride D.J., Lin M.L., Varela I., Pleasance E.D., Simpson J.T., et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 2009, 462:1005-1010.
87. Pleasance E.D., Cheetham R.K., Stephens P.J., McBride D.J., Humphray S.J., Greenman C.D., et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010, 463:191-196.
88. Campbell P.J., Stephens P.J., Pleasance E.D., O'Meara S., Li H., Santarius T., et al. Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat Genet 2008, 40:722-729.
89. Weir B.A., Woo M.S., Getz G., Perner S., Ding L., Beroukhim R., et al. Characterizing the cancer genome in lung adenocarcinoma. Nature 2007, 450:893-898.
90. Martin E.S., Tonon G., Sinha R., Xiao Y., Feng B., Kimmelman A.C., et al. Common and distinct genomic events in sporadic colorectal cancer and diverse cancer types. Cancer Res 2007, 67:10736-10743.
91. Lockwood W.W., Chari R., Coe B.P., Girard L., Macaulay C., Lam S., et al. DNA amplification is a ubiquitous mechanism of oncogene activation in lung and other cancers. Oncogene 2008, 27:4615-4624.
92. Soda M., Choi Y.L., Enomoto M., Takada S., Yamashita Y., Ishikawa S., et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007, 448:561-566.
93. Martelli M.P., Sozzi G., Hernandez L., Pettirossi V., Navarro A., Conte D., et al. EML4-ALK rearrangement in non-small cell lung cancer and non-tumor lung tissues. Am J Pathol 2009, 174:661-670.
94. Wong D.W., Leung E.L., So K.K., Tam I.Y., Sihoe A.D., Cheng L.C., et al. The EML4-ALK fusion gene is involved in various histologic types of lung cancers from nonsmokers with wild-type EGFR and KRAS. Cancer 2009, 115:1723-1733.
95. Shaw A.T., Yeap B.Y., Mino-Kenudson M., Digumarthy S.R., Costa D.B., Heist R.S., et al. Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol 2009, 27:4247-4253.
96. Rodig S.J., Mino-Kenudson M., Dacic S., Yeap B.Y., Shaw A., Barletta J.A., et al. Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the western population. Clin Cancer Res 2009, 15:5216-5223.