Chromosomal translocations and palindromic AT-rich repeats

Current Opinion in Genetics and Development

Volumn 22, Issue 3, 2012, Pages 221-228

  Kato, Takema ^a   Kurahashi, Hiroki ^b   Emanuel, Beverly S ^a,c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b FUJITA HEALTH UNIVERSITY   (Japan)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CHROMOSOME BREAKAGE; CHROMOSOME DELETION 22Q11; CHROMOSOME TRANSLOCATION; CHROMOSOME TRANSLOCATION 11; CHROMOSOME TRANSLOCATION 22; DNA SEQUENCE; DNA STRUCTURE; GENE REARRANGEMENT; GENE STRUCTURE; GENETIC POLYMORPHISM; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PALINDROMIC AT RICH REPEAT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SPERM; SPERMATOGENESIS;

AT RICH SEQUENCE; CHROMOSOMAL INSTABILITY; CHROMOSOME BREAKPOINTS; CHROMOSOMES, HUMAN, PAIR 22; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; GENOME, HUMAN; HUMANS; INVERTED REPEAT SEQUENCES; MALE; NUCLEIC ACID CONFORMATION; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; SPERMATOZOA; TRANSLOCATION, GENETIC;

EID: 84862504386     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2012.02.004     Document Type: Review

References (65)

1. Burn J., Goodship J. Developmental genetics of the heart. Curr Opin Genet Dev 1996, 6:322-325.
2. Emanuel B.S. Molecular mechanisms and diagnosis of chromosome 22q11.2 rearrangements. Dev Disabil Res Rev 2008, 14:11-18.
3. Edelmann L., Pandita R.K., Spiteri E., Funke B., Goldberg R., Palanisamy N., Chaganti R.S., Magenis E., Shprintzen R.J., Morrow B.E. A common molecular basis for rearrangement disorders on chromosome 22q11. Hum Mol Genet 1999, 8:1157-1167.
4. Shaikh T.H., Kurahashi H., Saitta S.C., O'Hare A.M., Hu P., Roe B.A., Driscoll D.A., McDonald-McGinn D.M., Zackai E.H., Budarf M.L., et al. Chromosome 22-specific low copy repeats and the 22q11.2 deletion syndrome: genomic organization and deletion endpoint analysis. Hum Mol Genet 2000, 9:489-501.
5. Shaikh T.H., O'Connor R.J., Pierpont M.E., McGrath J., Hacker A.M., Nimmakayalu M., Geiger E., Emanuel B.S., Saitta S.C. Low copy repeats mediate distal chromosome 22q11.2 deletions: sequence analysis predicts breakpoint mechanisms. Genome Res 2007, 17:482-491.
6. Stankiewicz P., Lupski J.R. Genome architecture, rearrangements and genomic disorders. Trends Genet 2002, 18:74-82.
7. Edelmann L., Spiteri E., Koren K., Pulijaal V., Bialer M.G., Shanske A., Goldberg R., Morrow B.E. AT-rich palindromes mediate the constitutional t(11;22) translocation. Am J Hum Genet 2001, 68:1-13.
8. Kurahashi H., Emanuel B.S. Long AT-rich palindromes and the constitutional t(11;22) breakpoint. Hum Mol Genet 2001, 10:2605-2617.
9. Kurahashi H., Shaikh T.H., Hu P., Roe B.A., Emanuel B.S., Budarf M.L. Regions of genomic instability on 22q11 and 11q23 as the etiology for the recurrent constitutional t(11;22). Hum Mol Genet 2000, 9:1665-1670.
10. Shaikh T.H., Budarf M.L., Celle L., Zackai E.H., Emanuel B.S. Clustered 11q23 and 22q11 breakpoints and 3:1 meiotic malsegregation in multiple unrelated t(11;22) families. Am J Hum Genet 1999, 65:1595-1607.
11. Tapia-Paez I., Kost-Alimova M., Hu P., Roe B.A., Blennow E., Fedorova L., Imreh S., Dumanski J.P. The position of t(11;22)(q23;q11) constitutional translocation breakpoint is conserved among its carriers. Hum Genet 2001, 109:167-177.
12. Zackai E.H., Emanuel B.S. Site-specific reciprocal translocation, t(11;22) (q23;q11), in several unrelated families with 3:1 meiotic disjunction. Am J Med Genet 1980, 7:507-521.
13. Gotter A.L., Nimmakayalu M.A., Jalali G.R., Hacker A.M., Vorstman J., Conforto Duffy D., Medne L., Emanuel B.S. A palindrome-driven complex rearrangement of 22q11.2 and 8q24.1 elucidated using novel technologies. Genome Res 2007, 17:470-481.
14. Sheridan M.B., Kato T., Haldeman-Englert C., Jalali G.R., Milunsky J.M., Zou Y., Klaes R., Gimelli G., Gimelli S., Gemmill R.M., et al. A palindrome-mediated recurrent translocation with 3:1 meiotic nondisjunction: the t(8;22)(q24.13;q11.21). Am J Hum Genet 2010, 87:209-218.
15. Kehrer-Sawatzki H., Haussler J., Krone W., Bode H., Jenne D.E., Mehnert K.U., Tummers U., Assum G. The second case of a t(17;22) in a family with neurofibromatosis type 1: sequence analysis of the breakpoint regions. Hum Genet 1997, 99:237-247.
16. Kurahashi H., Shaikh T., Takata M., Toda T., Emanuel B.S. The constitutional t(17;22): another translocation mediated by palindromic AT-rich repeats. Am J Hum Genet 2003, 72:733-738.
17. Gotter A.L., Shaikh T.H., Budarf M.L., Rhodes C.H., Emanuel B.S. A palindrome-mediated mechanism distinguishes translocations involving LCR-B of chromosome 22q11.2. Hum Mol Genet 2004, 13:103-115.
18. Nimmakayalu M.A., Gotter A.L., Shaikh T.H., Emanuel B.S. A novel sequence-based approach to localize translocation breakpoints identifies the molecular basis of a t(4;22). Hum Mol Genet 2003, 12:2817-2825.
19. Kurahashi H., Inagaki H., Hosoba E., Kato T., Ohye T., Kogo H., Emanuel B.S. Molecular cloning of a translocation breakpoint hotspot in 22q11. Genome Res 2007, 17:461-469.
20. Akgun E., Zahn J., Baumes S., Brown G., Liang F., Romanienko P.J., Lewis S., Jasin M. Palindrome resolution and recombination in the mammalian germ line. Mol Cell Biol 1997, 17:5559-5570.
21. Collick A., Drew J., Penberth J., Bois P., Luckett J., Scaerou F., Jeffreys A., Reik W. Instability of long inverted repeats within mouse transgenes. EMBO J 1996, 15:1163-1171.
22. Gordenin D.A., Lobachev K.S., Degtyareva N.P., Malkova A.L., Perkins E., Resnick M.A. Inverted DNA repeats: a source of eukaryotic genomic instability. Mol Cell Biol 1993, 13:5315-5322.
23. Leach D.R. Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. Bioessays 1994, 16:893-900.
24. Inagaki H., Ohye T., Kogo H., Yamada K., Kowa H., Shaikh T.H., Emanuel B.S., Kurahashi H. Palindromic AT-rich repeat in the NF1 gene is hypervariable in humans and evolutionarily conserved in primates. Hum Mutat 2005, 26:332-342.
25. Nag D.K., Kurst A. A 140-bp-long palindromic sequence induces double-strand breaks during meiosis in the yeast Saccharomyces cerevisiae. Genetics 1997, 146:835-847.
26. Smith G.R. Meeting DNA palindromes head-to-head. Genes Dev 2008, 22:2612-2620.
27. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31:3406-3415.
28. Kurahashi H., Inagaki H., Yamada K., Ohye T., Taniguchi M., Emanuel B.S., Toda T. Cruciform DNA structure underlies the etiology for palindrome-mediated human chromosomal translocations. J Biol Chem 2004, 279:35377-35383.
29. Lu L., Jia H., Droge P., Li J. The human genome-wide distribution of DNA palindromes. Funct Integr Genomics 2007, 7:221-227.
30. Kurahashi H., Inagaki H., Ohye T., Kogo H., Kato T., Emanuel B.S. Palindrome-mediated chromosomal translocations in humans. DNA Repair (Amst) 2006, 5:1136-1145.
31. Raghavan S.C., Swanson P.C., Wu X., Hsieh C.L., Lieber M.R. A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Nature 2004, 428:88-93.
32. Kurahashi H., Emanuel B.S. Unexpectedly high rate of de novo constitutional t(11;22) translocations in sperm from normal males. Nat Genet 2001, 29:139-140.
33. Kato T., Inagaki H., Yamada K., Kogo H., Ohye T., Kowa H., Nagaoka K., Taniguchi M., Emanuel B.S., Kurahashi H. Genetic variation affects de novo translocation frequency. Science 2006, 311:971.
34. Kato T., Inagaki H., Tong M., Kogo H., Ohye T., Yamada K., Tsutsumi M., Emanuel B.S., Kurahashi H. DNA secondary structure is influenced by genetic variation and alters susceptibility to de novo translocation. Mol Cytogenet 2011, 4:18.
35. Kogo H., Inagaki H., Ohye T., Kato T., Emanuel B.S., Kurahashi H. Cruciform extrusion propensity of human translocation-mediating palindromic AT-rich repeats. Nucleic Acids Res 2007, 35:1198-1208.
36. Tong M., Kato T., Yamada K., Inagaki H., Kogo H., Ohye T., Tsutsumi M., Wang J., Emanuel B.S., Kurahashi H. Polymorphisms of the 22q11.2 breakpoint region influence the frequency of de novo constitutional t(11;22)s in sperm. Hum Mol Genet 2010, 19:2630-2637.
37. Cohen A.J., Li F.P., Berg S., Marchetto D.J., Tsai S., Jacobs S.C., Brown R.S. Hereditary renal-cell carcinoma associated with a chromosomal translocation. N Engl J Med 1979, 301:592-595.
38. Poland K.S., Azim M., Folsom M., Goldfarb R., Naeem R., Korch C., Drabkin H.A., Gemmill R.M., Plon S.E. A constitutional balanced t(3;8)(p14;q24.1) translocation results in disruption of the TRC8 gene and predisposition to clear cell renal cell carcinoma. Genes Chromosomes Cancer 2007, 46:805-812.
39. Ohye T., Inagaki H., Kogo H., Tsutsumi M., Kato T., Tong M., Macville M.V., Medne L., Zackai E.H., Emanuel B.S., et al. Paternal origin of the de novo constitutional t(11;22)(q23;q11). Eur J Hum Genet 2010, 18:783-787.
40. Trinh T.Q., Sinden R.R. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli. Nature 1991, 352:544-547.
41. Mirkin S.M. Expandable DNA repeats and human disease. Nature 2007, 447:932-940.
42. Mirkin S.M., Smirnova E.V. Positioned to expand. Nat Genet 2002, 31:5-6.
43. Zhang H., Freudenreich C.H. An AT-rich sequence in human common fragile site FRA16D causes fork stalling and chromosome breakage in S. cerevisiae. Mol Cell 2007, 27:367-379.
44. Braun R.E. Packaging paternal chromosomes with protamine. Nat Genet 2001, 28:10-12.
45. Ward W.S. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod 2010, 16:30-36.
46. Ward W.S. Regulating DNA supercoiling: sperm points the way. Biol Reprod 2011, 84:841-843.
47. Hassold T., Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2001, 2:280-291.
48. Buwe A., Guttenbach M., Schmid M. Effect of paternal age on the frequency of cytogenetic abnormalities in human spermatozoa. Cytogenet Genome Res 2005, 111:213-228.
49. Crow J.F. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet 2000, 1:40-47.
50. Kato T., Yamada K., Inagaki H., Kogo H., Ohye T., Emanuel B.S., Kurahashi H. Age has no effect on de novo constitutional t(11;22) translocation frequency in sperm. Fertil Steril 2007, 88:1446-1448.
51. Kato T., Inagaki H., Kogo H., Ohye T., Yamada K., Emanuel B.S., Kurahashi H. Two different forms of palindrome resolution in the human genome: deletion or translocation. Hum Mol Genet 2008, 17:1184-1191.
52. Kurahashi H., Inagaki H., Kato T., Hosoba E., Kogo H., Ohye T., Tsutsumi M., Bolor H., Tong M., Emanuel B.S. Impaired DNA replication prompts deletions within palindromic sequences, but does not induce translocations in human cells. Hum Mol Genet 2009, 18:3397-3406.
53. Bandyopadhyay R., Heller A., Knox-DuBois C., McCaskill C., Berend S.A., Page S.L., Shaffer L.G. Parental origin and timing of de novo Robertsonian translocation formation. Am J Hum Genet 2002, 71:1456-1462.
54. Giglio S., Calvari V., Gregato G., Gimelli G., Camanini S., Giorda R., Ragusa A., Guerneri S., Selicorni A., Stumm M., et al. Heterozygous submicroscopic inversions involving olfactory receptor-gene clusters mediate the recurrent t(4;8)(p16;p23) translocation. Am J Hum Genet 2002, 71:276-285.
55. Maas N.M., Van Vooren S., Hannes F., Van Buggenhout G., Mysliwiec M., Moreau Y., Fagan K., Midro A., Engiz O., Balci S., et al. The t(4;8) is mediated by homologous recombination between olfactory receptor gene clusters, but other 4p16 translocations occur at random. Genet Couns 2007, 18:357-365.
56. Ou Z., Stankiewicz P., Xia Z., Breman A.M., Dawson B., Wiszniewska J., Szafranski P., Cooper M.L., Rao M., Shao L., et al. Observation and prediction of recurrent human translocations mediated by NAHR between nonhomologous chromosomes. Genome Res 2011, 21:33-46.
57. Lobachev K.S., Gordenin D.A., Resnick M.A. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 2002, 108:183-193.
58. Ashley T., Gaeth A.P., Inagaki H., Seftel A., Cohen M.M., Anderson L.K., Kurahashi H., Emanuel B.S. Meiotic recombination and spatial proximity in the etiology of the recurrent t(11;22). Am J Hum Genet 2006, 79:524-538.
59. Berg I.L., Neumann R., Lam K.W., Sarbajna S., Odenthal-Hesse L., May C.A., Jeffreys A.J. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet 2010, 42:859-863.
60. Kovtun I.V., McMurray C.T. Trinucleotide expansion in haploid germ cells by gap repair. Nat Genet 2001, 27:407-411.
61. Dawson A.J., Mears A.J., Chudley A.E., Bech-Hansen T., McDermid H. Der(22)t(11;22) resulting from a paternal de novo translocation, adjacent 1 segregation, and maternal heterodisomy of chromosome 22. J Med Genet 1996, 33:952-956.
62. Kurahashi H., Shaikh T.H., Zackai E.H., Celle L., Driscoll D.A., Budarf M.L., Emanuel B.S. Tightly clustered 11q23 and 22q11 breakpoints permit PCR-based detection of the recurrent constitutional t(11;22). Am J Hum Genet 2000, 67:763-768.
63. Misteli T. Spatial positioning: a new dimension in genome function. Cell 2004, 119:153-156.
64. Parada L.A., Sotiriou S., Misteli T. Spatial genome organization. Exp Cell Res 2004, 296:64-70.
65. Roix J.J., McQueen P.G., Munson P.J., Parada L.A., Misteli T. Spatial proximity of translocation-prone gene loci in human lymphomas. Nat Genet 2003, 34:287-291.