Meiotic recombination and spatial proximity in the etiology of the recurrent t(11;22)

American Journal of Human Genetics

Volumn 79, Issue 3, 2006, Pages 524-538

  Ashley, Terry ^a   Gaeth, Ann P ^a   Inagaki, Hidehito ^b   Seftel, Allen ^c,d,e   Cohen, Maimon M ^f   Anderson, Lorinda K ^g   Kurahashi, Hiroki ^b   Emanuel, Beverly S ^h,i  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FUJITA HEALTH UNIVERSITY   (Japan)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^e LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^f GREATER BALTIMORE MEDICAL CENTER   (United States)

^g Department of Environmental and Radiological Health Sciences   (United States)

^h CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; FLUORESCEIN ISOTHIOCYANATE; PALINDROMIC DNA; PROTEIN MLH1; RHODAMINE;

ADULT; ARTICLE; CHROMOSOME 11Q; CHROMOSOME 21P; CHROMOSOME 22Q; CHROMOSOME 6Q; CHROMOSOME TRANSLOCATION 11; CHROMOSOME TRANSLOCATION 22; CONTROLLED STUDY; DNA PROBE; DNA SEQUENCE; DNA STRAND BREAKAGE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MALE; MEIOSIS; MEIOTIC RECOMBINATION; OOCYTE; PACHYTENE; PRIORITY JOURNAL; PROPHASE; SPERMATOCYTE;

ROBERTSONIA;

EID: 33748657156     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/507652     Document Type: Article

References (72)

1. Zackai EH, Emanuel, BS (1980) Site-specific reciprocal translocation, t(11;22))q23;q11), in several unrelated families with 3:1 meiotic disjunction. Am J Med Genet 7:507-521
2. Fraccaro M, Lindsten J, Ford C, Iselius L (1980) The 11q;22q translocation: a European collaborative analysis of 43 cases. Hum Genet 56:21-51
3. Shaikh TH, Budarf M, Celle L, Zackai EH, Emanuel BS (1999) Clustered 11q23 and 22q11 breakpoints and 3:1 meiotic malsegragation in multiple unrelated t(11;22) families. Am J Hum Genet 65:1595-1607
4. Lin TY, Viswanathan S, Wood C, Wilson PG, Wolf N, Fuller MT (1996) Coordinate developmental control of the meiotic cell cycle and spermatid defferentiation in Drosophila males. Development 122:1331-1341
5. Kurahashi H, Shaikh TH, Hu P, Roe BA, Emanuel BS, Budarf M (2000) Regions of genomic instability on 22q11 and 11q23 as the etiology for the recurrent constitutional t(11;22). Hum Mol Genet 9:1665-1670
6. Kurahashi H, Shaikh TH, Zackai EH, Celle L, Driscoll DA, Budarf ML, Emanuel BS (2000) Tightly clustered 11q23 and 22q11 breakpoints permit PCR-based detection of the recurrent constitutional t(11;22). Am J Hum Genet 67:763-768
7. Kurahashi H, Emanuel BS (2001) Unexpectedly high rate of de novo constitutional t(11;22) translocations in sperm from normal males. Nat Genet 29:139-140
8. Kato T, Inagaki H, Yamada K, Kogo H, Ohye T, Kowa H, Nagaoka K, Taniguchi M, Emanuel BS, Kurahashi H (2006) Genetic variation affects de novo translocation frequency. Science 311:971
9. Kurahashi H, Emanuel BS (2001) Long AT-rich palindromes and the constitutional t(11;22) breakpoint. Hum Mol Genet 10:2605-2617
10. Edelmann L, Spiteri E, Koren K, Pulifaal V, Bialer M, Shanske A, Goldberg R, Morrow BE (2001) AT-rich palindromes mediate the consitutional t(11;22) translocation. Am J Hum Genet 68:1-13
11. Connelly JC, Leach DR (1996) The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes Cells 1:285-291
12. Kurahashi H, Inagaki H, Yamada K, Ohye T, Taniguchi M, Emanuel BS, Toda T (2004) Cruciform DNA structure underlies the etiology for palindrome-mediated human chromosomal translocations. J Biol Chem 279:35377-35383
13. Roth DB, Menetski JP, Nakajima PB, Bosma MJ, Gellert M (1992) V(D)J recombination: broken DNA molecules with covalently sealed (hairpin) coding ends in scid mouse thymocytes. Cell 70:983-991
14. Cunningham LA, Cote AG, Cam-Ozdemir C, Lewis SM (2003) Rapid, stabilizing palindrome rearrangements in somatic cells by the center-break mechanism. Mol Cell Biol 23:8740-8750
15. Connelly JC, Kirkham L, Leach D (1998) The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc Nat Acad Sci USA 95:7969-7974
16. Majewski J, Ott J (2000) GT repeats are associated with recombination on human chromosome 22. Genome Res 10:1108-1114
17. Lynn A, Koehler KE, Judis L, Chan ER, Cherry JP, Schwartz S, Seftel A, Hunt PA, Hassold TJ (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296:2222-2225
18. Saitta SC, Harris SE, Gaeth AP, Driscoll DA, McDonald-McGinn DM, Maisenbacher MK, Yersak JM, Chakraborty PK, Hacker AM, Zackai EH, Ashley T, Emanuel BS (2004) Aberrant interchromosomal exchanges are the predominant cause of the 22q11.2 deletion. Hum Mol Genet 13:417-428
19. Sun F, Trpkov K, Rademaker A, Ko E, Martin R (2005) Variation in meiotic recombination frequencies among human males. Hum Genet 116:172-178
20. Tease C, Hartshorne GM, Hultén MA (2002) Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 70:1469-1479
21. Nielsen J, Sillesen I (1975) Incidence of chromosome aberrations among 11148 newborn children. Humangenetik 30:1-12
22. Nagele RG, Freeman T, Fazekas J, Lee KM, Thomson Z, Lee HY (1998) Chromosome spatial order in human cells: evidence of early origin and faithful propagation. Chromosoma 107:330-338
23. Vourc'h C, Taruscio D, Boyle AL, Ward DC (1993) Cell cycle-dependent distribution of telomeres, centromeres and chromosome-specific subsatellite domains in the interphase nucleus of mouse lymphocytes. Exp Cell Res 205:142-151
24. Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore W (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119-1131
25. Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum Mol Genet 10:211-219
26. Kozubek S, Lukasova E, Mareckova A, Skalnikova M, Kozubek M, Bartova E, Kroha V, Krahulcova E, Slotova J (1999) The topological organization of chromosomes 9 and 22 in cell nuclei has a determinative role in the induction of t(9,22) translocations and in the pathogenesis of t(9,22) leukemias. Chromosoma 108:426-435
27. Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE (2000) Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 290:138-141
28. Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, Christie DM, Monell C, Arnheim N, Bradley A, Ashley T, Liskay RM (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336-342
29. Edelmann W, Cohen PE, Kane M, Lau K, Morrow B, Bennett S, Umar A, Kunkel T, Cattoretti G, Chaganti R, Pollard JW, Kolodner RD, Kucherlapati R (1996) Meiotic pachytene arrest in Mlh1-deficient mice. Cell 85:1125-1134
30. Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossovers on mouse chromosomes using immunofluorescent localization of MLH1 protein. Genetics 151:1569-1579
31. Froenicke L, Anderson LK, Wienberg J, Ashley T (2002) Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71:1353-1368
32. Evans EP, Breckon G, Ford CE (1964) An air-drying method for meiotic preparations from mammalian testis. Cytogenetics 3:288-295
33. Dodson G, Shi L, Tibbetts RS (2004) DNA replication defects, spontaneous DNA damage, and ATM-dependent checkpoint activation in replication protein A-deficient cells. J Biol Chem 279:34010-34014
34. Walpita D, Plug AW, Neff N, German J, Ashley T (1999) Bloom's syndrome protein (BLM) co-localizes with RPA in meiotic pro-phase nuclei of mammalian spermatocytes. Proc Natl Acad Sci USA 96:5622-5627
35. Ashley T, Plug AW, Xu J, Solari AJ, Reddy G, Golub EI, Ward DC (1995) Dynamic changes in Rad51 distribution on chromatin during meiosis in male and female vertebrates. Chromosoma 104:19-28
36. Lichter P, Tang CC, Call K, Hermanson G, Evans GA, Housman D, Ward DC (1990) High-resolution mapping of human chromosome 11 by in situ hybridization with cosmid clones. Science 247:64-69
37. Reeves A (2001) Micromeasure: a new computer program for the collection and analysis of cytogenetic data. Genome 44:439-443
38. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406-3415
39. Gotter AL, Shaikh TH, Budarf ML, Rhodes CH, Emanuel BS (2004) A palindrome-mediated mechanism distinguishes translocations involving LCR-B of chromosome 22q11.2. Hum Mol Genet 13:103-115
40. Lynn A, Ashley T, Hassold T (2004) Variation in human meiotic recombination. In: Lander E, Page D, Chakravarti A (eds) Annual review of genomics and human genetics. Annual Reviews, Palo Alto, pp 317-349
41. Misteli T (2004) Spatial positioning: a new dimension in genome function. Cell 119:153-156
42. Parada L, Sotiria S, Misteli T (2004) Spatial genome organization. Exp Cell Res 296:64-70
43. Parada L, McQueen P, Munson P, Misteli T (2002) Conservation of relative chromosome positioning in normal and cancer cells. Curr Biol 12:1692-1697
44. Scherthan H, Weich S, Schweger H, Heyting C, Karle M, Cremer T (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134:1109-1125
45. Cheng EY, Naluai-Cecchini T (2004) FISHing for acrocentric associations between chromosomes 14 and 21 in human oogenesis. Am J Obstet Gynecol 190:1781-1795
46. Cheng EY, Chen YJ, Disteche CM, Gartler SM (1999) Analysis of a paracentric inversion in human oocytes: nonhomologous pairing in pachytene. Hum Genet 105:191-196
47. Stahl A, Luciani JM, Hartung M, Devictor M, Berge-Lefranc JL, Guichaoua M (1983) Structural basis for Robertsonian translocations in man: association of ribosomal genes in the nucleolar fibrillar center in meiotic spermatocytes and oocytes. Proc Natl Acad Sci USA 80:5946-5950
48. Bandyopadhyay R, Heller A, Knox-DuBois C, McCaskill C, Berend SA, Page SL, Shaffer LG (2002) Parental origin and timing of de novo Robertsonian translocation formation. Am J Hum Genet 71:1456-1462
49. Assenmacher N, Hopfner KP (2004) MRE11/RAD50/NBS1: complex activities. Chromosoma 113:157-166
50. Paull TT, Gellert M (1999) Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev 13:1276-1288
51. Borde V, Lin W, Novikov E, Petrini JH, Lichten M, Nicolas A (2004) Association of Mre11 with double-strand break sites during yeast meiosis. Mol Cell 13:389-401
52. Keeney S, Giroux C, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spoil, a member of a widely conserved protein family. Cell 88:375-384
53. Paull TT, Gellert M (2000) A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proc Natl Acad Sci USA 97:6409-6414
54. Maser RS, Mirzoeva OK, Wells J, Olivares H, Williams BR, Zinkel RA, Farnham PJ, Petrini JH (2001) Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol Cell Biol 21:6006-6016
55. Mirozoeva OK, Petrini JH (2003) DNA replication-dependent nuclear dynamics of the Mre11 complex. Mol Cancer Res 1:207-218
56. Goedecke W, Eijpe M, Offenberg HH, van Aalderen M, Heyting C (1999) MRE11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat Genet 23:194-198
57. Lewis SM, Chen S, Strathern JN, Rattray AJ (2005) New approaches to the analysis of palindromic sequences from the human genome: evolution and polymorphism of an intronic site at the NF1 locus. Nucleic Acids Res 33:e186
58. Gellrt M (2002) V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71:101-132
59. Hamer G, Roepers-Gajadien HL, van Duyn-Goedhart A, Gademan IS, Kal HB, van Buul PP, Ashley T, de Rooif DG (2003) Function of DNA-protein kinase catalytic subunit during the early meiotic prophase without Ku70 and Ku86. Biol Reprod 68:717-721
60. Nishant KT, Kumar C, Rao MR (2006) HUMHOT: a database of human meiotic recombination hot spots. Nucleic Acids Res 34:D25-D28
61. Zhou ZH, Akgun E, Jasin M (2001) Repeat expansion by homologous recombination in the mouse germ line at palindromic sequences. Proc Natl Acad Sci USA 98:8326-8333
62. Tapia-Páez I, O'Brien K, Kost-Alimova M, Sahlen S, Kedra D, Bruder C, Andersson B, Roe BA, Hu P, Imreh S, Blennow E, Dumanski JP (2000) Fine mapping of the constitutional translocation t(11;22)(q23;q11). Hum Genet 106:506-516
63. Funke B, Edelmann L, McCain N, Pandita RK, Ferreira J, Merscher S, Zohouri M, Cannizzaro L, Shanske A, Morrow BE (1999) Der(22) syndrome and velo-cardio-facial syndrome/DiGeorge syndrome share a 1.5-Mb region of overlap on chromosome 22q11. Am J Hum Genet 64:747-758
64. Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, Jiang H, Kodadek T (1997) Dmc1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics 147:533-544
65. Plug AW, Peters AH, Keegan KS, Hoekstra MF, de Boer P, Ashley T (1998) Changes in protein composition of meiotic nodules during mammalian meiosis. J Cell Sci 111:413-423
66. Li M, Budarf ML, Chien P, Barnoski BL, Emanuel BS, Driscoll DA (1995) Clustering of DiGeorge/velocardiofacial-associated translocations suggestive of a translocation "hot spot". Am J Hum Genet Suppl 57:A119
67. Kehrer-Sawatzki H, Haussler J, Krone W, Bode H, Jenne DE, Mehnert KU, Tummers U, Assum G (1997) The second case of a t(17;22) in a family with neurofibromatosis type 1: sequence analysis of the breakpoint regions. Hum Genet 99:237-247
68. Rhodes CH, Call KM, Budarf ML, Barnoski BL, Bell CJ, Emanuel BS, Bigner SH, Park JP, Mohandas TK (1997) Molecular studies of an ependymoma-associated constitutional t(1;22) (p22;q11.2). Cytogenet Cell Genet 78:247-252
69. Debeer P, Mols R, Huysmans C, Devriendt K, Van de Ven WJ, Fryns JP (2002) Involvement of a palindromic chromosome 22-specific low-copy repeat in a constitutional t(X;22) (q27;q11). Clin Genet 62:410-414
70. Spiteri E, Babcock M, Kashork CD, Wakui K, Gogineni S, Lewis DA, Williams KM, Minoshima S, Sasaki T, Shimizu N, Potocki L, Pulijaal V, Shanske A, Shaffer LG, Morrow BE (2003) Frequent translocations occur between low copy repeats on chromosome 22q11.2 (LCR22s) and telomeric bands of partner chromosomes. Hum Mol Genet 12:1823-1837
71. Nimmakayalu MA, Gotter AL, Shaikh TH, Emanuel BS (2003) A novel sequence-based approach to localize translocation breakpoints identifies the molecular basis of a t(4;22). Hum Mol Genet 12:2817-2825
72. Barlow AL, Benson FE, West SC, Hultén MA (1997) Distribution of Rad51 recombinase in human and mouse spermatocytes. EMBO J 16:5207-5215