Pseudoautosomal Region 1 Length Polymorphism in the Human Population

English version České info

The human sex chromosomes differ in sequence, except for homologous sequences at both ends, termed the pseudoautosomal regions (PAR1 and PAR2). PAR enables the pairing of chromosomes Y and X during meiosis. The PARs are located at the termini of respectively the short and long arms of chromosomes X and Y. The observation of gradual shortening of the Y chromosome over evolutionary time has led to speculations that the Y chromosome is “doomed to extinction.” However, the Y chromosome has been shaped over evolution not only by the loss of genes, but also by addition of genes as a result of interchromosomal exchanges. In this work, we identified males with a duplication on chromosome Xp22.33 of about 136 kb as an incidental finding during a copy number variation screen. We demonstrate that the duplicon is an insertional translocation due to non-allelic homologous recombination from the X to the Y chromosome that is flanked by a long terminal repeat (LTR6B). We show this translocation event has occurred independently multiple times and that the duplicated region recombines with the X chromosome. Therefore, the duplicated region represents an extension of the pseudoautosomal region, representing a novel mechanism shaping sex chromosomal evolution in humans.

Vyšlo v časopise: Pseudoautosomal Region 1 Length Polymorphism in the Human Population. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004578
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004578

Souhrn

Zdroje

1. BachtrogD (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14: 113–124.

2. OttoSP, PannellJR, PeichelCL, AshmanTL, CharlesworthD, et al. (2011) About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet 27: 358–367.

3. LahnBT, PageDC (1999) Four evolutionary strata on the human X chromosome. Science 286: 964–967.

4. PandeyRS, Wilson SayresMA, AzadRK (2013) Detecting evolutionary strata on the human X chromosome in the absence of gametologous Y-linked sequences. Genome Biol Evol 5: 1863–1871.

5. MaraisG, GaltierN (2003) Sex chromosomes: how X-Y recombination stops. Curr Biol 13: R641–643.

6. KatsuraY, IwaseM, SattaY (2012) Evolution of genomic structures on Mammalian sex chromosomes. Curr Genomics 13: 115–123.

7. AitkenRJ, Marshall GravesJA (2002) The future of sex. Nature 415: 963.

8. Marshall GravesJA (2006) Sex chromosome specialization and degeneration in mammals. Cell 124: 901–914.

9. HughesJF, SkaletskyH, BrownLG, PyntikovaT, GravesT, et al. (2012) Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483: 82–86.

10. WatersPD, DuffyB, FrostCJ, DelbridgeML, GravesJAM (2001) The human Y chromosome derives largely from a single autosomal region added to the sex chromosomes 80-130 million years ago. Cytogenet Cell Genet 92: 74–79.

11. VermeeschJR, PetitP, KermouniA, RenauldJC, Van Den BergheH, et al. (1997) The IL-9 receptor gene, located in the Xq/Yq pseudoautosomal region, has an autosomal origin, escapes X inactivation and is expressed from the Y. Hum Mol Genet 6: 1–8.

12. CharcharFJ, SvartmanM, El-MogharbelN, VenturaM, KirbyP, et al. (2003) Complex events in the evolution of the human pseudoautosomal region 2 (PAR2). Genome Res 13: 281–286.

13. FlaquerA, RappoldGA, WienkerTF, FischerC (2008) The human pseudoautosomal regions: a review for genetic epidemiologists. Eur J Hum Genet 16: 771–779.

14. FilatovDA, GerrardDT (2003) High mutation rates in human and ape pseudoautosomal genes. Gene 317: 67–77.

15. BussellJJ, PearsonNM, KandaR, FilatovDA, LahnBT (2006) Human polymorphism and human-chimpanzee divergence in pseudoautosomal region correlate with local recombination rate. Gene 368: 94–100.

16. SchiebelK, MederJ, RumpA, RosenthalA, WinkelmannM, et al. (2000) Elevated DNA sequence diversity in the genomic region of the phosphatase PPP2R3L gene in the human pseudoautosomal region. Cytogenet Cell Genet 91: 224–230.

17. JorgezCJ, WeedinJW, SahinA, Tannour-LouetM, HanS, et al. (2011) Aberrations in pseudoautosomal regions (PARs) found in infertile men with Y-chromosome microdeletions. J Clin Endocrinol Metab 96: E674–679.

18. EllisNA, YeTZ, PattonS, GermanJ, GoodfellowPN, et al. (1994) Cloning of PBDX, an MIC2-related gene that spans the pseudoautosomal boundary on chromosome Xp. Nat Genet 6: 394–400.

19. EllisNA, TippettP, PettyA, ReidM, WellerPA, et al. (1994) PBDX is the XG blood group gene. Nat Genet 8: 285–290.

20. GlaserB, MyrtekD, RumplerY, SchiebelK, HauwyM, et al. (1999) Transposition of SRY into the ancestral pseudoautosomal region creates a new pseudoautosomal boundary in a progenitor of simian primates. Hum Mol Genet 8: 2071–2078.

21. Van LaereAS, CoppietersW, GeorgesM (2008) Characterization of the bovine pseudoautosomal boundary: Documenting the evolutionary history of mammalian sex chromosomes. Genome Res 18: 1884–1895.

22. EllisN, YenP, NeiswangerK, ShapiroLJ, GoodfellowPN (1990) Evolution of the pseudoautosomal boundary in Old World monkeys and great apes. Cell 63: 977–986.

23. BallantyneKN, GoedbloedM, FangR, SchaapO, LaoO, et al. (2010) Mutability of Y-chromosomal microsatellites: rates, characteristics, molecular bases, and forensic implications. Am J Hum Genet 87: 341–353.

24. WalshB (2001) Estimating the time to the most recent common ancestor for the Y chromosome or mitochondrial DNA for a pair of individuals. Genetics 158: 897–912.

25. MangsAH, MorrisBJ (2007) The Human Pseudoautosomal Region (PAR): Origin, Function and Future. Curr Genomics 8: 129–136.

26. DurkinK, CoppietersW, DrogemullerC, AharizN, CambisanoN, et al. (2012) Serial translocation by means of circular intermediates underlies colour sidedness in cattle. Nature 482: 81–84.

27. OuZ, StankiewiczP, XiaZ, BremanAM, DawsonB, et al. (2011) Observation and prediction of recurrent human translocations mediated by NAHR between nonhomologous chromosomes. Genome Res 21: 33–46.

28. LiuP, LacariaM, ZhangF, WithersM, HastingsPJ, et al. (2011) Frequency of nonallelic homologous recombination is correlated with length of homology: evidence that ectopic synapsis precedes ectopic crossing-over. Am J Hum Genet 89: 580–588.

29. LiuP, CarvalhoCM, HastingsPJ, LupskiJR (2012) Mechanisms for recurrent and complex human genomic rearrangements. Curr Opin Genet Dev 22: 211–220.

30. ShawCJ, LupskiJR (2005) Non-recurrent 17p11.2 deletions are generated by homologous and non-homologous mechanisms. Hum Genet 116: 1–7.

31. LuoY, HermetzKE, JacksonJM, MulleJG, DoddA, et al. (2011) Diverse mutational mechanisms cause pathogenic subtelomeric rearrangements. Hum Mol Genet 20: 3769–3778.

32. WhiteMA, IkedaA, PayseurBA (2012) A pronounced evolutionary shift of the pseudoautosomal region boundary in house mice. Mamm Genome 23: 454–466.

33. KoumbarisG, Hatzisevastou-LoukidouH, AlexandrouA, IoannidesM, ChristodoulouC, et al. (2011) FoSTeS, MMBIR and NAHR at the human proximal Xp region and the mechanisms of human Xq isochromosome formation. Hum Mol Genet 20: 1925–1936.

34. HigashimotoK, MaedaT, OkadaJ, OhtsukaY, SasakiK, et al. (2013) Homozygous deletion of DIS3L2 exon 9 due to non-allelic homologous recombination between LINE-1s in a Japanese patient with Perlman syndrome. Eur J Hum Genet 21: 1316–1319.

35. JohnsonNC (2011) XG: the forgotten blood group system. Immunohematology 27: 68–71.

36. MuJ, SkuratAV, RoachPJ (1997) Glycogenin-2, a novel self-glucosylating protein involved in liver glycogen biosynthesis. J Biol Chem 272: 27589–27597.

37. MuJ, RoachPJ (1998) Characterization of human glycogenin-2, a self-glucosylating initiator of liver glycogen metabolism. J Biol Chem 273: 34850–34856.

38. Marshall GravesJA (2002) The rise and fall of SRY. Trends Genet 18: 259–264.

39. VermeeschJR, MertensG, DavidG, MarynenP (1995) Assignment of the human glypican gene (GPC1) to 2q35-q37 by fluorescence in situ hybridization. Genomics 25: 327–329.

40. SrisupunditK, BradyPD, DevriendtK, FrynsJP, Cruz-MartinezR, et al. (2010) Targeted array comparative genomic hybridisation (array CGH) identifies genomic imbalances associated with isolated congenital diaphragmatic hernia (CDH). Prenat Diagn 30: 1198–1206.

41. VermeeschJR, MelotteC, FroyenG, Van VoorenS, DuttaB, et al. (2005) Molecular karyotyping: array CGH quality criteria for constitutional genetic diagnosis. J Histochem Cytochem 53: 413–422.

42. UntergasserA, CutcutacheI, KoressaarT, YeJ, FairclothBC, et al. (2012) Primer3–new capabilities and interfaces. Nucleic Acids Res 40: e115.

43. KoressaarT, RemmM (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23: 1289–1291.

44. JurkaJ (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 16: 418–420.

45. Smit AFA, Hubley R, Green P (1996–2010). RepeatMasker Open-3.0. URL http://www.repeatmasker.org.

46. KentWJ, SugnetCW, FureyTS, RoskinKM, PringleTH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996–1006.

47. KarolchikD, BarberGP, CasperJ, ClawsonH, ClineMS, et al. (2014) The UCSC Genome Browser database: 2014 update. Nucleic Acids Res 42: D764–770.

48. BashiardesS, VeileR, HelmsC, MardisER, BowcockAM, et al. (2005) Direct genomic selection. Nat Methods 2: 63–69.

49. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.

50. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20: 1297–1303.

51. DePristoMA, BanksE, PoplinR, GarimellaKV, MaguireJR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491–498.

52. Van der AuweraGA, CarneiroM, HartlC, PoplinR, del AngelG, et al. (2013) From FastQ Data to High-Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline. Curr Protoc Bioinformatics 43: 11.10.1–11.10.33.

53. LarmuseauMH, VanderheydenN, JacobsM, CoomansM, LarnoL, et al. (2011) Micro-geographic distribution of Y-chromosomal variation in the central-western European region Brabant. Forensic Sci Int Genet 5: 95–99.

54. LarmuseauMH, VanoverbekeJ, GielisG, VanderheydenN, LarmuseauHF, et al. (2012) In the name of the migrant father–analysis of surname origins identifies genetic admixture events undetectable from genealogical records. Heredity (Edinb) 109: 90–95.

55. AtheyWT (2006) Haplogroup prediction from Y-STR values using a Bayesian-allele-frequency approach. Journal of Genetic Genealog 2: 34–39.

56. LarmuseauMH, OttoniC, RaeymaekersJA, VanderheydenN, LarmuseauHF, et al. (2012) Temporal differentiation across a West-European Y-chromosomal cline: genealogy as a tool in human population genetics. Eur J Hum Genet 20: 434–440.

57. Van GeystelenA, DecorteR, LarmuseauMH (2013) AMY-tree: an algorithm to use whole genome SNP calling for Y chromosomal phylogenetic applications. BMC Genomics 14: 101.

58. Van GeystelenA, DecorteR, LarmuseauMH (2013) Updating the Y-chromosomal phylogenetic tree for forensic applications based on whole genome SNPs. Forensic Sci Int Genet 7: 573–580.

59. PeakallR, SmousePE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.

60. PeakallR, SmousePE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28: 2537–2539.

61. BandeltHJ, ForsterP, RohlA (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48.

62. QamarR, AyubQ, MohyuddinA, HelgasonA, MazharK, et al. (2002) Y-chromosomal DNA variation in Pakistan. Am J Hum Genet 70: 1107–1124.

63. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

64. LarkinMA, BlackshieldsG, BrownNP, ChennaR, McGettiganPA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.