Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Oct 15;88(20):8944–8948. doi: 10.1073/pnas.88.20.8944

X/Y translocations resulting from recombination between homologous sequences on Xp and Yq.

P H Yen 1, S P Tsai 1, S L Wenger 1, M W Steele 1, T K Mohandas 1, L J Shapiro 1
PMCID: PMC52627  PMID: 1924355

Abstract

Several regions of sequence homology between the human X and Y chromosomes have been identified. These segments are thought to represent areas of these chromosomes that have engaged in meiotic recombination in relatively recent evolutionary times. Normally, the X and Y chromosomes pair during meiosis and exchange DNA only within the pseudoautosomal region at the distal short arms of both chromosomes. However, it has been suggested that aberrant recombination involving other segments of high homology could be responsible for the production of X/Y translocations. We have studied four X/Y translocation patients using molecular probes detecting homologous sequences on X and Y chromosomes. In one translocation the breakpoints have been isolated and sequenced. The mapping data are consistent with the hypothesis that X/Y translocations arise by homologous recombination. The sequencing data from one translocation demonstrate this directly.

Full text

PDF
8944

Images in this article

8945Image
on p.8945

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Affara N. A., Florentin L., Morrison N., Kwok K., Mitchell M., Cook A., Jamieson D., Glasgow L., Meredith L., Boyd E. Regional assignment of Y-linked DNA probes by deletion mapping and their homology with X-chromosome and autosomal sequences. Nucleic Acids Res. 1986 Jul 11;14(13):5353–5373. doi: 10.1093/nar/14.13.5353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Agematsu K., Koike K., Morosawa H., Nakahori Y., Nakagome Y., Akabane T. Chondrodysplasia punctata with X;Y translocation. Hum Genet. 1988 Sep;80(1):105–107. doi: 10.1007/BF00451470. [DOI] [PubMed] [Google Scholar]
  3. Arveiler B., Vincent A., Mandel J. L. Toward a physical map of the Xq28 region in man: linking color vision, G6PD, and coagulation factor VIII genes to an X-Y homology region. Genomics. 1989 May;4(4):460–471. doi: 10.1016/0888-7543(89)90269-3. [DOI] [PubMed] [Google Scholar]
  4. Ballabio A., Carrozzo R., Gil A., Gillard B., Affara N., Ferguson-Smith M. A., Fraser N., Craig I., Rocchi M., Romeo G. Molecular characterization of human X/Y translocations suggests their aetiology through aberrant exchange between homologous sequences on Xp and Yq. Ann Hum Genet. 1989 Jan;53(Pt 1):9–14. doi: 10.1111/j.1469-1809.1989.tb01117.x. [DOI] [PubMed] [Google Scholar]
  5. Bardoni B., Guioli S., Raimondi E., Heilig R., Mandel J. L., Ottolenghi S., Camerino G. Isolation and characterization of a family of sequences dispersed on the human X chromosome. Genomics. 1988 Jul;3(1):32–38. doi: 10.1016/0888-7543(88)90155-3. [DOI] [PubMed] [Google Scholar]
  6. Bernstein R., Rosendorff J., Ramsay M., Pinto M. R., Page D. C. A unique dicentric X;Y translocation with Xq and Yp breakpoints: cytogenetic and molecular studies. Am J Hum Genet. 1987 Aug;41(2):145–156. [PMC free article] [PubMed] [Google Scholar]
  7. Bickmore W. A., Cooke H. J. Evolution of homologous sequences on the human X and Y chromosomes, outside of the meiotic pairing segment. Nucleic Acids Res. 1987 Aug 11;15(15):6261–6271. doi: 10.1093/nar/15.15.6261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bodrug S. E., Ray P. N., Gonzalez I. L., Schmickel R. D., Sylvester J. E., Worton R. G. Molecular analysis of a constitutional X-autosome translocation in a female with muscular dystrophy. Science. 1987 Sep 25;237(4822):1620–1624. doi: 10.1126/science.3629260. [DOI] [PubMed] [Google Scholar]
  9. Cameron I. T., Buckton K. E., Baird D. T. X-Y translocation. A case report. Hum Genet. 1984;67(4):457–459. doi: 10.1007/BF00291411. [DOI] [PubMed] [Google Scholar]
  10. Chandley A. C., Goetz P., Hargreave T. B., Joseph A. M., Speed R. M. On the nature and extent of XY pairing at meiotic prophase in man. Cytogenet Cell Genet. 1984;38(4):241–247. doi: 10.1159/000132070. [DOI] [PubMed] [Google Scholar]
  11. Chen S. J., Chen Z., Font M. P., d'Auriol L., Larsen C. J., Berger R. Structural alterations of the BCR and ABL genes in Ph1 positive acute leukemias with rearrangements in the BCR gene first intron: further evidence implicating Alu sequences in the chromosome translocation. Nucleic Acids Res. 1989 Oct 11;17(19):7631–7642. doi: 10.1093/nar/17.19.7631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Croce C. M. Role of chromosome translocations in human neoplasia. Cell. 1987 Apr 24;49(2):155–156. doi: 10.1016/0092-8674(87)90552-6. [DOI] [PubMed] [Google Scholar]
  13. Ellis N., Goodfellow P. N. The mammalian pseudoautosomal region. Trends Genet. 1989 Dec;5(12):406–410. doi: 10.1016/0168-9525(89)90199-6. [DOI] [PubMed] [Google Scholar]
  14. Fraser N., Ballabio A., Zollo M., Persico G., Craig I. Identification of incomplete coding sequences for steroid sulphatase on the human Y chromosome: evidence for an ancestral pseudoautosomal gene? Development. 1987;101 (Suppl):127–132. doi: 10.1242/dev.101.Supplement.127. [DOI] [PubMed] [Google Scholar]
  15. Geldwerth D., Bishop C., Guellaën G., Koenig M., Vergnaud G., Mandel J. L., Weissenbach J. Extensive DNA sequence homologies between the human Y and the long arm of the X chromosome. EMBO J. 1985 Jul;4(7):1739–1743. doi: 10.1002/j.1460-2075.1985.tb03844.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Geller R. L., Shapiro L. J., Mohandas T. K. Fine mapping of the distal short arm of the human X chromosome using X/Y translocations. Am J Hum Genet. 1986 Jun;38(6):884–890. [PMC free article] [PubMed] [Google Scholar]
  17. Gessler M., Simola K. O., Bruns G. A. Cloning of breakpoints of a chromosome translocation identifies the AN2 locus. Science. 1989 Jun 30;244(4912):1575–1578. doi: 10.1126/science.2544995. [DOI] [PubMed] [Google Scholar]
  18. Johnston K., Schonberg S., Littman V., Gregory T., Gelbart S., O'Donnell J., Cox D. R. De novo X;Y translocation associated with imperforate anus and retinal pigmentary abnormalities. Am J Med Genet. 1987 Jul;27(3):603–611. doi: 10.1002/ajmg.1320270313. [DOI] [PubMed] [Google Scholar]
  19. Knowlton R. G., Nelson C. A., Brown V. A., Page D. C., Donis-Keller H. An extremely polymorphic locus on the short arm of the human X chromosome with homology to the long arm of the Y chromosome. Nucleic Acids Res. 1989 Jan 11;17(1):423–437. doi: 10.1093/nar/17.1.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koenig M., Camerino G., Heilig R., Mandel J. L. A DNA fragment from the human X chromosome short arm which detects a partially homologous sequence on the Y chromosomes long arm. Nucleic Acids Res. 1984 May 25;12(10):4097–4109. doi: 10.1093/nar/12.10.4097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Koenig M., Moisan J. P., Heilig R., Mandel J. L. Homologies between X and Y chromosomes detected by DNA probes: localisation and evolution. Nucleic Acids Res. 1985 Aug 12;13(15):5485–5501. doi: 10.1093/nar/13.15.5485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lau E. C., Mohandas T. K., Shapiro L. J., Slavkin H. C., Snead M. L. Human and mouse amelogenin gene loci are on the sex chromosomes. Genomics. 1989 Feb;4(2):162–168. doi: 10.1016/0888-7543(89)90295-4. [DOI] [PubMed] [Google Scholar]
  23. Li X. M., Yen P., Mohandas T., Shapiro L. J. A long range restriction map of the distal human X chromosome short arm around the steroid sulfatase locus. Nucleic Acids Res. 1990 May 11;18(9):2783–2788. doi: 10.1093/nar/18.9.2783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mandel J. L., Willard H. F., Nussbaum R. L., Romeo G., Puck J. M., Davies K. E. Report of the committee on the genetic constitution of the X chromosome. Cytogenet Cell Genet. 1989;51(1-4):384–437. doi: 10.1159/000132801. [DOI] [PubMed] [Google Scholar]
  25. Middlesworth W., Bertelson C., Kunkel L. M. An RFLP detecting single copy X-chromosome fragment, dic56, from Xp22-Xpter [HGM8 assignment no. DXS 143]. Nucleic Acids Res. 1985 Aug 12;13(15):5723–5723. doi: 10.1093/nar/13.15.5723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moses M. J., Counce S. J., Paulson D. F. Synaptonemal complex complement of man in spreads of spermatocytes, with details of the sex chromosome pair. Science. 1975 Jan 31;187(4174):363–365. [PubMed] [Google Scholar]
  27. Page D. C., Harper M. E., Love J., Botstein D. Occurrence of a transposition from the X-chromosome long arm to the Y-chromosome short arm during human evolution. Nature. 1984 Sep 13;311(5982):119–123. doi: 10.1038/311119a0. [DOI] [PubMed] [Google Scholar]
  28. Page D. C., de la Chapelle A., Weissenbach J. Chromosome Y-specific DNA in related human XX males. Nature. 1985 May 16;315(6016):224–226. doi: 10.1038/315224a0. [DOI] [PubMed] [Google Scholar]
  29. Petit C., Levilliers J., Rouyer F., Simmler M. C., Herouin E., Weissenbach J. Isolation of sequences from Xp22.3 and deletion mapping using sex chromosome rearrangements from human X-Y interchange sex reversals. Genomics. 1990 Apr;6(4):651–658. doi: 10.1016/0888-7543(90)90500-t. [DOI] [PubMed] [Google Scholar]
  30. Petit C., Levilliers J., Weissenbach J. Long-range restriction map of the terminal part of the short arm of the human X chromosome. Proc Natl Acad Sci U S A. 1990 May;87(10):3680–3684. doi: 10.1073/pnas.87.10.3680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Petit C., de la Chapelle A., Levilliers J., Castillo S., Noël B., Weissenbach J. An abnormal terminal X-Y interchange accounts for most but not all cases of human XX maleness. Cell. 1987 Jun 5;49(5):595–602. doi: 10.1016/0092-8674(87)90535-6. [DOI] [PubMed] [Google Scholar]
  32. Rabbitts T. H., Boehm T., Mengle-Gaw L. Chromosomal abnormalities in lymphoid tumours: mechanism and role in tumour pathogenesis. Trends Genet. 1988 Nov;4(11):300–304. doi: 10.1016/0168-9525(88)90106-0. [DOI] [PubMed] [Google Scholar]
  33. Rogers J. Oncogene chromosome breakpoints and alu sequences. Nature. 1985 Oct 10;317(6037):559–559. doi: 10.1038/317559a0. [DOI] [PubMed] [Google Scholar]
  34. Ross M. T., Ballabio A., Craig I. W. Long-range physical mapping around the human steroid sulfatase locus. Genomics. 1990 Mar;6(3):528–539. doi: 10.1016/0888-7543(90)90482-a. [DOI] [PubMed] [Google Scholar]
  35. Rouyer F., Simmler M. C., Page D. C., Weissenbach J. A sex chromosome rearrangement in a human XX male caused by Alu-Alu recombination. Cell. 1987 Nov 6;51(3):417–425. doi: 10.1016/0092-8674(87)90637-4. [DOI] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sinclair A. H., Berta P., Palmer M. S., Hawkins J. R., Griffiths B. L., Smith M. J., Foster J. W., Frischauf A. M., Lovell-Badge R., Goodfellow P. N. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature. 1990 Jul 19;346(6281):240–244. doi: 10.1038/346240a0. [DOI] [PubMed] [Google Scholar]
  38. Snead M. L., Zeichner-David M., Chandra T., Robson K. J., Woo S. L., Slavkin H. C. Construction and identification of mouse amelogenin cDNA clones. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7254–7258. doi: 10.1073/pnas.80.23.7254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Speevak M., Clifford B., Cox D. M., Hunter A. G. Detection at amniocentesis of a maternally inherited X;Y translocation. Clin Genet. 1985 Jun;27(6):595–599. doi: 10.1111/j.1399-0004.1985.tb02044.x. [DOI] [PubMed] [Google Scholar]
  40. Viskochil D., Buchberg A. M., Xu G., Cawthon R. M., Stevens J., Wolff R. K., Culver M., Carey J. C., Copeland N. G., Jenkins N. A. Deletions and a translocation interrupt a cloned gene at the neurofibromatosis type 1 locus. Cell. 1990 Jul 13;62(1):187–192. doi: 10.1016/0092-8674(90)90252-a. [DOI] [PubMed] [Google Scholar]
  41. Wallace M. R., Marchuk D. A., Andersen L. B., Letcher R., Odeh H. M., Saulino A. M., Fountain J. W., Brereton A., Nicholson J., Mitchell A. L. Type 1 neurofibromatosis gene: identification of a large transcript disrupted in three NF1 patients. Science. 1990 Jul 13;249(4965):181–186. doi: 10.1126/science.2134734. [DOI] [PubMed] [Google Scholar]
  42. Weissenbach J., Goodfellow P. N., Smith K. D. Report of the committee on the genetic constitution of the Y chromosome. Cytogenet Cell Genet. 1989;51(1-4):438–449. doi: 10.1159/000132802. [DOI] [PubMed] [Google Scholar]
  43. Wolfe J., Erickson R. P., Rigby P. W., Goodfellow P. N. Cosmid clones derived from both euchromatic and heterochromatic regions of the human Y chromosome. EMBO J. 1984 Sep;3(9):1997–2003. doi: 10.1002/j.1460-2075.1984.tb02081.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yen P. H., Allen E., Marsh B., Mohandas T., Wang N., Taggart R. T., Shapiro L. J. Cloning and expression of steroid sulfatase cDNA and the frequent occurrence of deletions in STS deficiency: implications for X-Y interchange. Cell. 1987 May 22;49(4):443–454. doi: 10.1016/0092-8674(87)90447-8. [DOI] [PubMed] [Google Scholar]
  45. Yen P. H., Li X. M., Tsai S. P., Johnson C., Mohandas T., Shapiro L. J. Frequent deletions of the human X chromosome distal short arm result from recombination between low copy repetitive elements. Cell. 1990 May 18;61(4):603–610. doi: 10.1016/0092-8674(90)90472-q. [DOI] [PubMed] [Google Scholar]
  46. Yen P. H., Marsh B., Allen E., Tsai S. P., Ellison J., Connolly L., Neiswanger K., Shapiro L. J. The human X-linked steroid sulfatase gene and a Y-encoded pseudogene: evidence for an inversion of the Y chromosome during primate evolution. Cell. 1988 Dec 23;55(6):1123–1135. doi: 10.1016/0092-8674(88)90257-7. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES