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Mammalian Genome

, Volume 25, Issue 11–12, pp 618–635 | Cite as

A high resolution map of mammalian X chromosome fragile regions assessed by large-scale comparative genomics

  • Carlos Fernando Prada
  • Paul LaissueEmail author
Article

Abstract

Chromosomal evolution involves multiple changes at structural and numerical levels. These changes, which are related to the variation of the gene number and their location, can be tracked by the identification of syntenic blocks (SB). First reports proposed that ~180–280 SB might be shared by mouse and human species. More recently, further studies including additional genomes have identified up to ~1,400 SB during the evolution of eutherian species. A considerable number of studies regarding the X chromosome’s structure and evolution have been undertaken because of its extraordinary biological impact on reproductive fitness and speciation. Some have identified evolutionary breakpoint regions and fragile sites at specific locations in the human X chromosome. However, mapping these regions to date has involved using low-to-moderate resolution techniques. Such scenario might be related to underestimating their total number and giving an inaccurate location. The present study included using a combination of bioinformatics methods for identifying, at base-pair level, chromosomal rearrangements occurring during X chromosome evolution in 13 mammalian species. A comparative technique using four different algorithms was used for optimizing the detection of hotspot regions in the human X chromosome. We identified a significant interspecific variation in SB size which was related to genetic information gain regarding the human X chromosome. We found that human hotspot regions were enriched by LINE-1 and Alu transposable elements, which may have led to intraspecific chromosome rearrangement events. New fragile regions located in the human X chromosome have also been postulated. We estimate that the high resolution map of X chromosome fragile sites presented here constitutes useful data concerning future studies on mammalian evolution and human disease.

Keywords

Transposable Element Chromosomal Rearrangement Fragile Site Chromosome Evolution Inversion Model 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

PL and CFP are funded by the Universidad del Rosario. This study was supported by The Universidad del Rosario (Grant CS/Genetics 2013).

Supplementary material

335_2014_9537_MOESM1_ESM.tif (1.1 mb)
Figure S1. Cow X chromosome evolution. A minimum of 16 to 17 inversions wererequired to transform ancestral (A1) to cow X chromosome. A) GRIMM software (X1-X17); B) restricted DCJ model (X1-X16); C) HP model (X1-X17); D. inversion model(X1-X17). Inversion breakpoints are represented by arrows. Negative symbols representinverted syntenic blocks. Hypothetical cow ancestral X chromosomes (I to VII) areincluded in the Figure. The hypothetical (VIII) and real X chromosomes as well as the39 syntenic blocks are located at the bottom of the figure. (TIFF 1085 kb)
335_2014_9537_MOESM2_ESM.tif (985 kb)
Figure S1. Continued (TIFF 984 kb)
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Figure S1. Continued (TIFF 1067 kb)
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Figure S1. Continued (TIFF 1048 kb)
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Figure S2. Mouse and rat X chromosome evolution. A minimum of three inversionswere required to transform the mammalian ancestral X chromosome (A1) to the mouseand rat ancestral X chromosome (A2); a minimum of seven inversions were required totransform A2 to mouse and rat X chromosome, respectively. A) GRIMM software; B)restricted DCJ model; C) HP model; D. inversion model. Inversion breakpoints arerepresented by an arrow. Negative symbols represent inverted syntenic blocks.Hypothetical mouse (III to V) and rat (VII to IX) ancestral X chromosomes (I and II) forA2 are included in the Figure. The real mouse and rat X chromosomes are located afterhypothetical chromosomae VI and X. Complete SB deletions in each species arerepresented by rectangles (TIFF 1012 kb)
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Figure S2. Continued (TIFF 888 kb)
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Figure S2. Continued (TIFF 1048 kb)
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Figure S2. Continued (TIFF 1087 kb)
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Figure S3. Anthropoid primates, dog, horse, pig and rabbit X chromosome evolution. Aminimum of one inversion was required to transform the mammalian ancestral Xchromosome (A1) to the ancestral structure of these species (A3 anthropoid primates,dog and horse ancestral chromosome). A minimum of three inversions were required toobtain the rabbit and pig X chromosome. A) GRIMM software; B) restricted DCJmodel; C) HP model; D. inversion model. Inversion breakpoints are represented by anarrow. Negative symbols represent inverted syntenic blocks. The real pig and rabbit Xchromosomes are located after hypothetical chromosomes I and II. Complete syntenicblock deletions are represented by rectangles. Inversions shown in blue were exclusiveto the restricted DCJ model (TIFF 1081 kb)
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References

  1. Alekseyev MA, Pevzner PA (2010) Comparative genomics reveals birth and death of fragile regions in mammalian evolution. Genome Biol 11:R117PubMedCentralPubMedGoogle Scholar
  2. Archibald AL, Bolund L, Churcher C, Fredholm M, Groenen MA, Harlizius B, Lee KT, Milan D, Rogers J, Rothschild MF, Uenishi H, Wang J, Schook LB (2010) Pig genome sequence: analysis and publication strategy. BMC Genom 11:438Google Scholar
  3. Arlt MF, Casper AM, Glover TW (2003) Common fragile sites. Cytogenetic and genome research 100:92–100PubMedGoogle Scholar
  4. Armengol L, Pujana MA, Cheung J, Scherer SW, Estivill X (2003) Enrichment of segmental duplications in regions of breaks of synteny between the human and mouse genomes suggest their involvement in evolutionary rearrangements. Hum Mol Genet 12:2201–2208PubMedGoogle Scholar
  5. Attie O, Darling AE, Yancopoulos S (2011) The rise and fall of breakpoint reuse depending on genome resolution. BMC Bioinformatics 12(Suppl 9):S1PubMedCentralPubMedGoogle Scholar
  6. Bafna V, Pevzner P (1995) Sorting permutations by tanspositions. In: Proceedings of the sixth annual ACM-SIAM symposium on Discrete algorithms: Society for Industrial and Applied Mathematics, pp 614-623Google Scholar
  7. Bailey JA, Eichler EE (2006) Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 7:552–564PubMedGoogle Scholar
  8. Bailey JA, Baertsch R, Kent WJ, Haussler D, Eichler EE (2004) Hotspots of mammalian chromosomal evolution. Genome Biol 5:R23PubMedCentralPubMedGoogle Scholar
  9. Bergeron A, Mixtacki J, Stoye J (2006) A unifying view of genome rearrangements. Algorithms in bioinformatics. Springer, Heidelberg, pp 163–173Google Scholar
  10. Bourque G, Zdobnov EM, Bork P, Pevzner PA, Tesler G (2005) Comparative architectures of mammalian and chicken genomes reveal highly variable rates of genomic rearrangements across different lineages. Genome Res 15:98–110PubMedCentralPubMedGoogle Scholar
  11. Brouwer JR, Willemsen R, Oostra BA (2009) The FMR1 gene and fragile X-associated tremor/ataxia syndrome. Am J Med Genet B 150b:782–798Google Scholar
  12. Caballero OL, Chen YT (2009) Cancer/testis (CT) antigens: potential targets for immunotherapy. Cancer Sci 100:2014–2021PubMedGoogle Scholar
  13. Caceres M, Sullivan RT, Thomas JW (2007) A recurrent inversion on the eutherian X chromosome. Proc Natl Acad Sci USA 104:18571–18576PubMedCentralPubMedGoogle Scholar
  14. Carrasquillo MM, Zou F, Pankratz VS, Wilcox SL, Ma L, Walker LP, Younkin SG, Younkin CS, Younkin LH, Bisceglio GD, Ertekin-Taner N, Crook JE, Dickson DW, Petersen RC, Graff-Radford NR, Younkin SG (2009) Genetic variation in PCDH11X is associated with susceptibility to late-onset Alzheimer’s disease. Nat Genet 41:192–198PubMedCentralPubMedGoogle Scholar
  15. Cheng MK, Disteche CM (2006) A balancing act between the X chromosome and the autosomes. J Biol 5:2PubMedCentralPubMedGoogle Scholar
  16. Chimpanzee S, Analysis C (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87Google Scholar
  17. Cocquet J, Ellis PJ, Mahadevaiah SK, Affara NA, Vaiman D, Burgoyne PS (2012) A genetic basis for a postmeiotic X versus Y chromosome intragenomic conflict in the mouse. PLoS Genet 8:e1002900PubMedCentralPubMedGoogle Scholar
  18. Copeland NG, Jenkins NA, Gilbert DJ, Eppig JT, Maltais LJ, Miller JC, Dietrich WF, Weaver A, Lincoln SE, Steen RG et al (1993) A genetic linkage map of the mouse: current applications and future prospects. Science 262:57–66PubMedGoogle Scholar
  19. Costa A, Gao L, Carrillo F, Caceres-Redondo MT, Carballo M, Diaz-Martin J, Gomez-Garre P, Sobrino F, Lucas M, Lopez-Barneo J, Mir P, Pintado E (2011) Intermediate alleles at the FRAXA and FRAXE loci in Parkinson’s disease. Parkinsonism Relat Disord 17:281–284PubMedGoogle Scholar
  20. Coulibaly MB, Lobo NF, Fitzpatrick MC, Kern M, Grushko O, Thaner DV, Traore SF, Collins FH, Besansky NJ (2007) Segmental duplication implicated in the genesis of inversion 2Rj of Anopheles gambiae. PLoS ONE 2:e849PubMedCentralPubMedGoogle Scholar
  21. Darai-Ramqvist E, Sandlund A, Muller S, Klein G, Imreh S, Kost-Alimova M (2008) Segmental duplications and evolutionary plasticity at tumor chromosome break-prone regions. Genome Res 18:370–379PubMedCentralPubMedGoogle Scholar
  22. Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403PubMedCentralPubMedGoogle Scholar
  23. Darling AE, Miklos I, Ragan MA (2008) Dynamics of genome rearrangement in bacterial populations. PLoS Genet 4:e1000128PubMedCentralPubMedGoogle Scholar
  24. Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147PubMedCentralPubMedGoogle Scholar
  25. Davies JP, Cotter PD, Ioannou YA (1997) Cloning and mapping of human Rab7 and Rab9 cDNA sequences and identification of a Rab9 pseudogene. Genomics 41:131–134PubMedGoogle Scholar
  26. Debacker K, Kooy RF (2007) Fragile sites and human disease. Hum Mol Genet 16(2):R150–158PubMedGoogle Scholar
  27. DeBaryshe PG, Pardue ML (2011) Differential maintenance of DNA sequences in telomeric and centromeric heterochromatin. Genetics 187:51–60PubMedCentralPubMedGoogle Scholar
  28. DeBry RW, Seldin MF (1996) Human/mouse homology relationships. Genomics 33:337–351PubMedGoogle Scholar
  29. Delprat A, Negre B, Puig M, Ruiz A (2009) The transposon Galileo generates natural chromosomal inversions in Drosophila by ectopic recombination. PLoS One 4:e7883PubMedCentralPubMedGoogle Scholar
  30. Di Pasquale E, Beck-Peccoz P, Persani L (2004) Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet 75:106–111PubMedCentralPubMedGoogle Scholar
  31. Drummond AJea (2010) Geneious v5.5Google Scholar
  32. Eichler EE (2001) Recent duplication, domain accretion and the dynamic mutation of the human genome. Trends Genet 17:661–669PubMedGoogle Scholar
  33. Elder FF, Robinson TJ (1989) Rodent common fragile sites: are they conserved? Evidence from mouse and rat. Chromosoma 97:459–464PubMedGoogle Scholar
  34. Emerson JJ, Kaessmann H, Betran E, Long M (2004) Extensive gene traffic on the mammalian X chromosome. Science 303:537–540PubMedGoogle Scholar
  35. Frischer LE, Hagen FS, Garber RL (1986) An inversion that disrupts the Antennapedia gene causes abnormal structure and localization of RNAs. Cell 47:1017–1023PubMedGoogle Scholar
  36. Fundia A, Gorostiaga M, Mudry M (2000) Expression of common fragile sites in two Ceboidea species: Saimiri boliviensis and Alouatta caraya (Primates: Platyrrhini). Genet Sel Evol 32:87–97PubMedCentralPubMedGoogle Scholar
  37. Furuta Y, Kawai M, Yahara K, Takahashi N, Handa N, Tsuru T, Oshima K, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I (2011) Birth and death of genes linked to chromosomal inversion. Proc Natl Acad Sci USA 108:1501–1506PubMedCentralPubMedGoogle Scholar
  38. Gazave E, Darre F, Morcillo-Suarez C, Petit-Marty N, Carreno A, Marigorta UM, Ryder OA, Blancher A, Rocchi M, Bosch E, Baker C, Marques-Bonet T, Eichler EE, Navarro A (2011) Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. Genome Res 21:1626–1639PubMedCentralPubMedGoogle Scholar
  39. George JA, DeBaryshe PG, Traverse KL, Celniker SE, Pardue ML (2006) Genomic organization of the Drosophila telomere retrotransposable elements. Genome Res 16:1231–1240PubMedCentralPubMedGoogle Scholar
  40. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, Scherer S, Scott G, Steffen D, Worley KC, Burch PE, Okwuonu G, Hines S, Lewis L, DeRamo C, Delgado O, Dugan-Rocha S, Miner G, Morgan M, Hawes A, Gill R, Celera, Holt RA, Adams MD, Amanatides PG, Baden-Tillson H, Barnstead M, Chin S, Evans CA, Ferriera S, Fosler C, Glodek A, Gu Z, Jennings D, Kraft CL, Nguyen T, Pfannkoch CM, Sitter C, Sutton GG, Venter JC, Woodage T, Smith D, Lee HM, Gustafson E, Cahill P, Kana A, Doucette-Stamm L, Weinstock K, Fechtel K, Weiss RB, Dunn DM, Green ED, Blakesley RW, Bouffard GG, De Jong PJ, Osoegawa K, Zhu B, Marra M, Schein J, Bosdet I, Fjell C, Jones S, Krzywinski M, Mathewson C, Siddiqui A, Wye N, McPherson J, Zhao S, Fraser CM, Shetty J, Shatsman S, Geer K, Chen Y, Abramzon S, Nierman WC, Havlak PH, Chen R, Durbin KJ, Egan A, Ren Y, Song XZ, Li B, Liu Y, Qin X, Cawley S, Worley KC, Cooney AJ, D’Souza LM, Martin K, Wu JQ, Gonzalez-Garay ML, Jackson AR, Kalafus KJ, McLeod MP, Milosavljevic A, Virk D, Volkov A, Wheeler DA, Zhang Z, Bailey JA, Eichler EE, Tuzun E, Birney E, Mongin E, Ureta-Vidal A, Woodwark C, Zdobnov E, Bork P, Suyama M, Torrents D, Alexandersson M, Trask BJ, Young JM, Huang H, Wang H, Xing H, Daniels S, Gietzen D, Schmidt J, Stevens K, Vitt U, Wingrove J, Camara F, Mar Alba M, Abril JF, Guigo R, Smit A, Dubchak I, Rubin EM, Couronne O, Poliakov A, Hubner N, Ganten D, Goesele C, Hummel O, Kreitler T, Lee YA, Monti J, Schulz H, Zimdahl H, Himmelbauer H, Lehrach H, Jacob HJ, Bromberg S, Gullings-Handley J, Jensen-Seaman MI, Kwitek AE, Lazar J, Pasko D, Tonellato PJ, Twigger S, Ponting CP, Duarte JM, Rice S, Goodstadt L, Beatson SA, Emes RD, Winter EE, Webber C, Brandt P, Nyakatura G, Adetobi M, Chiaromonte F, Elnitski L, Eswara P, Hardison RC, Hou M, Kolbe D, Makova K, Miller W, Nekrutenko A, Riemer C, Schwartz S, Taylor J, Yang S, Zhang Y, Lindpaintner K, Andrews TD, Caccamo M, Clamp M, Clarke L, Curwen V, Durbin R, Eyras E, Searle SM, Cooper GM, Batzoglou S, Brudno M, Sidow A, Stone EA, Venter JC, Payseur BA, Bourque G, Lopez-Otin C, Puente XS, Chakrabarti K, Chatterji S, Dewey C, Pachter L, Bray N, Yap VB, Caspi A, Tesler G, Pevzner PA, Haussler D, Roskin KM, Baertsch R, Clawson H, Furey TS, Hinrichs AS, Karolchik D, Kent WJ, Rosenbloom KR, Trumbower H, Weirauch M, Cooper DN, Stenson PD, Ma B, Brent M, Arumugam M, Shteynberg D, Copley RR, Taylor MS, Riethman H, Mudunuri U, Peterson J, Guyer M, Felsenfeld A, Old S, Mockrin S, Collins F (2004) Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428:493–521PubMedGoogle Scholar
  41. Glover TW, Hoge AW, Miller DE, Ascara-Wilke JE, Adam AN, Dagenais SL, Wilke CM, Dierick HA, Beer DG (1998) The murine Fhit gene is highly similar to its human orthologue and maps to a common fragile site region. Cancer Res 58:3409–3414PubMedGoogle Scholar
  42. Gordon L, Yang S, Tran-Gyamfi M, Baggott D, Christensen M, Hamilton A, Crooijmans R, Groenen M, Lucas S, Ovcharenko I, Stubbs L (2007) Comparative analysis of chicken chromosome 28 provides new clues to the evolutionary fragility of gene-rich vertebrate regions. Genome Res 17:1603–1613PubMedCentralPubMedGoogle Scholar
  43. Graves JA, Koina E, Sankovic N (2006) How the gene content of human sex chromosomes evolved. Curr Opin Genet Dev 16:219–224PubMedGoogle Scholar
  44. Gregory SG, Sekhon M, Schein J, Zhao S, Osoegawa K, Scott CE, Evans RS, Burridge PW, Cox TV, Fox CA, Hutton RD, Mullenger IR, Phillips KJ, Smith J, Stalker J, Threadgold GJ, Birney E, Wylie K, Chinwalla A, Wallis J, Hillier L, Carter J, Gaige T, Jaeger S, Kremitzki C, Layman D, Maas J, McGrane R, Mead K, Walker R, Jones S, Smith M, Asano J, Bosdet I, Chan S, Chittaranjan S, Chiu R, Fjell C, Fuhrmann D, Girn N, Gray C, Guin R, Hsiao L, Krzywinski M, Kutsche R, Lee SS, Mathewson C, McLeavy C, Messervier S, Ness S, Pandoh P, Prabhu AL, Saeedi P, Smailus D, Spence L, Stott J, Taylor S, Terpstra W, Tsai M, Vardy J, Wye N, Yang G, Shatsman S, Ayodeji B, Geer K, Tsegaye G, Shvartsbeyn A, Gebregeorgis E, Krol M, Russell D, Overton L, Malek JA, Holmes M, Heaney M, Shetty J, Feldblyum T, Nierman WC, Catanese JJ, Hubbard T, Waterston RH, Rogers J, de Jong PJ, Fraser CM, Marra M, McPherson JD, Bentley DR (2002) A physical map of the mouse genome. Nature 418:743–750PubMedGoogle Scholar
  45. Hannenhalli S, Pevzner PA (1995) Transforming men into mice (polynomial algorithm for genomic distance problem). Proceedings of the 36th Annual IEEE Symposium on Foundations of Computer Science, 1995, pp. 581–592Google Scholar
  46. Helmrich A, Stout-Weider K, Hermann K, Schrock E, Heiden T (2006) Common fragile sites are conserved features of human and mouse chromosomes and relate to large active genes. Genome Res 16:1222–1230PubMedCentralPubMedGoogle Scholar
  47. Hilker R, Sickinger C, Pedersen CN, Stoye J (2012) UniMoG: a unifying framework for genomic distance calculation and sorting based on DCJ. Bioinformatics (Oxford, England) 28:2509–2511Google Scholar
  48. Hofmann O, Caballero OL, Stevenson BJ, Chen YT, Cohen T, Chua R, Maher CA, Panji S, Schaefer U, Kruger A, Lehvaslaiho M, Carninci P, Hayashizaki Y, Jongeneel CV, Simpson AJ, Old LJ, Hide W (2008) Genome-wide analysis of cancer/testis gene expression. Proc Natl Acad Sci USA 105:20422–20427PubMedCentralPubMedGoogle Scholar
  49. Horvath JE, Schwartz S, Eichler EE (2000) The mosaic structure of human pericentromeric DNA: a strategy for characterizing complex regions of the human genome. Genome Res 10:839–852PubMedCentralPubMedGoogle Scholar
  50. Hough RB, Lengeling A, Bedian V, Lo C, Bucan M (1998) Rump white inversion in the mouse disrupts dipeptidyl aminopeptidase-like protein 6 and causes dysregulation of Kit expression. Proc Natl Acad Sci USA 95:13800–13805PubMedCentralPubMedGoogle Scholar
  51. Humphray SJ, Scott CE, Clark R, Marron B, Bender C, Camm N, Davis J, Jenks A, Noon A, Patel M, Sehra H, Yang F, Rogatcheva MB, Milan D, Chardon P, Rohrer G, Nonneman D, de Jong P, Meyers SN, Archibald A, Beever JE, Schook LB, Rogers J (2007) A high utility integrated map of the pig genome. Genome Biol 8:R139PubMedCentralPubMedGoogle Scholar
  52. Mitelman F, Johansson B, Mertens F (2013) Mitelman Database of Chromosome Aberrations and Gene Fusions in CancerGoogle Scholar
  53. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467PubMedGoogle Scholar
  54. Kirkpatrick M, Barton N (2006) Chromosome inversions, local adaptation and speciation. Genetics 173:419–434PubMedCentralPubMedGoogle Scholar
  55. Kleinjan DA, Lettice LA (2008) Long-range gene control and genetic disease. Adv Genet 61:339–388PubMedGoogle Scholar
  56. Kleinjan DA, van Heyningen V (2005) Long-range control of gene expression: emerging mechanisms and disruption in disease. Am J Hum Genet 76:8–32PubMedCentralPubMedGoogle Scholar
  57. Knight SJ, Flannery AV, Hirst MC, Campbell L, Christodoulou Z, Phelps SR, Pointon J, Middleton-Price HR, Barnicoat A, Pembrey ME et al (1993) Trinucleotide repeat amplification and hypermethylation of a CpG island in FRAXE mental retardation. Cell 74:127–134PubMedGoogle Scholar
  58. Kolb J, Chuzhanova NA, Hogel J, Vasquez KM, Cooper DN, Bacolla A, Kehrer-Sawatzki H (2009) Cruciform-forming inverted repeats appear to have mediated many of the microinversions that distinguish the human and chimpanzee genomes. Chromosom Res 17:469–483Google Scholar
  59. Kovac J, Warren R, Braga MD, Stoye J (2011) Restricted DCJ model: rearrangement problems with chromosome reincorporation. J Comput Biol 18:1231–1241PubMedGoogle Scholar
  60. Kremer EJ, Pritchard M, Lynch M, Yu S, Holman K, Baker E, Warren ST, Schlessinger D, Sutherland GR, Richards RI (1991) Mapping of DNA instability at the fragile X to a trinucleotide repeat sequence p(CCG)n. Science 252:1711–1714PubMedGoogle Scholar
  61. Krummel KA, Denison SR, Calhoun E, Phillips LA, Smith DI (2002) The common fragile site FRA16D and its associated gene WWOX are highly conserved in the mouse at Fra8E1. Genes Chromosom Cancer 34:154–167PubMedGoogle Scholar
  62. Kupiec M, Petes TD (1988) Allelic and ectopic recombination between Ty elements in yeast. Genetics 119:549–559PubMedCentralPubMedGoogle Scholar
  63. Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286:964–967PubMedGoogle Scholar
  64. Laissue P, Vinci G, Veitia RA, Fellous M (2008) Recent advances in the study of genes involved in non-syndromic premature ovarian failure. Mol Cell Endocrinol 282:101–111PubMedGoogle Scholar
  65. Lakich D, Kazazian HH Jr, Antonarakis SE, Gitschier J (1993) Inversions disrupting the factor VIII gene are a common cause of severe haemophilia A. Nat Genet 5:236–241PubMedGoogle Scholar
  66. Lambert JC, Heath S, Even G, Campion D, Sleegers K, Hiltunen M, Combarros O, Zelenika D, Bullido MJ, Tavernier B, Letenneur L, Bettens K, Berr C, Pasquier F, Fievet N, Barberger-Gateau P, Engelborghs S, De Deyn P, Mateo I, Franck A, Helisalmi S, Porcellini E, Hanon O, de Pancorbo MM, Lendon C, Dufouil C, Jaillard C, Leveillard T, Alvarez V, Bosco P, Mancuso M, Panza F, Nacmias B, Bossu P, Piccardi P, Annoni G, Seripa D, Galimberti D, Hannequin D, Licastro F, Soininen H, Ritchie K, Blanche H, Dartigues JF, Tzourio C, Gut I, Van Broeckhoven C, Alperovitch A, Lathrop M, Amouyel P (2009) Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer’s disease. Nat Genet 41:1094–1099PubMedGoogle Scholar
  67. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann N, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blocker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowski J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, International Human Genome Sequencing C (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedGoogle Scholar
  68. Larkin DM, Pape G, Donthu R, Auvil L, Welge M, Lewin HA (2009) Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. Genome Res 19:770–777PubMedCentralPubMedGoogle Scholar
  69. Lim JK, Simmons MJ (1994) Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. BioEssays 16:269–275PubMedGoogle Scholar
  70. Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ, Washietl S, Kheradpour P, Ernst J, Jordan G, Mauceli E, Ward LD, Lowe CB, Holloway AK, Clamp M, Gnerre S, Alfoldi J, Beal K, Chang J, Clawson H, Cuff J, Di Palma F, Fitzgerald S, Flicek P, Guttman M, Hubisz MJ, Jaffe DB, Jungreis I, Kent WJ, Kostka D, Lara M, Martins AL, Massingham T, Moltke I, Raney BJ, Rasmussen MD, Robinson J, Stark A, Vilella AJ, Wen J, Xie X, Zody MC, Baldwin J, Bloom T, Chin CW, Heiman D, Nicol R, Nusbaum C, Young S, Wilkinson J, Worley KC, Kovar CL, Muzny DM, Gibbs RA, Cree A, Dihn HH, Fowler G, Jhangiani S, Joshi V, Lee S, Lewis LR, Nazareth LV, Okwuonu G, Santibanez J, Warren WC, Mardis ER, Weinstock GM, Wilson RK, Delehaunty K, Dooling D, Fronik C, Fulton L, Fulton B, Graves T, Minx P, Sodergren E, Birney E, Margulies EH, Herrero J, Green ED, Haussler D, Siepel A, Goldman N, Pollard KS, Pedersen JS, Lander ES, Kellis M (2011) A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:476–482PubMedCentralPubMedGoogle Scholar
  71. Lister C, Jackson D, Martin C (1993) Transposon-induced inversion in Antirrhinum modifies nivea gene expression to give a novel flower color pattern under the control of cycloidearadialis. Plant Cell 5:1541–1553PubMedCentralPubMedGoogle Scholar
  72. Lukusa T, Fryns JP (2008) Human chromosome fragility. Biochim Biophys Acta 1779:3–16PubMedGoogle Scholar
  73. Ma J, Zhang L, Suh BB, Raney BJ, Burhans RC, Kent WJ, Blanchette M, Haussler D, Miller W (2006) Reconstructing contiguous regions of an ancestral genome. Genome Res 16:1557–1565PubMedCentralPubMedGoogle Scholar
  74. Ma K, Qiu L, Mrasek K, Zhang J, Liehr T, Quintana LG, Li Z (2012) Common fragile sites: genomic hotspots of DNA damage and carcinogenesis. Int J Mol Sci 13:11974–11999PubMedCentralPubMedGoogle Scholar
  75. Marques-Bonet T, Girirajan S, Eichler EE (2009) The origins and impact of primate segmental duplications. Trends Genet 25:443–454PubMedCentralPubMedGoogle Scholar
  76. Mouse Genome Sequencing C, Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P, Botcherby M, Bray N, Brent MR, Brown DG, Brown SD, Bult C, Burton J, Butler J, Campbell RD, Carninci P, Cawley S, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Clee C, Collins FS, Cook LL, Copley RR, Coulson A, Couronne O, Cuff J, Curwen V, Cutts T, Daly M, David R, Davies J, Delehaunty KD, Deri J, Dermitzakis ET, Dewey C, Dickens NJ, Diekhans M, Dodge S, Dubchak I, Dunn DM, Eddy SR, Elnitski L, Emes RD, Eswara P, Eyras E, Felsenfeld A, Fewell GA, Flicek P, Foley K, Frankel WN, Fulton LA, Fulton RS, Furey TS, Gage D, Gibbs RA, Glusman G, Gnerre S, Goldman N, Goodstadt L, Grafham D, Graves TA, Green ED, Gregory S, Guigo R, Guyer M, Hardison RC, Haussler D, Hayashizaki Y, Hillier LW, Hinrichs A, Hlavina W, Holzer T, Hsu F, Hua A, Hubbard T, Hunt A, Jackson I, Jaffe DB, Johnson LS, Jones M, Jones TA, Joy A, Kamal M, Karlsson EK, Karolchik D, Kasprzyk A, Kawai J, Keibler E, Kells C, Kent WJ, Kirby A, Kolbe DL, Korf I, Kucherlapati RS, Kulbokas EJ, Kulp D, Landers T, Leger JP, Leonard S, Letunic I, Levine R, Li J, Li M, Lloyd C, Lucas S, Ma B, Maglott DR, Mardis ER, Matthews L, Mauceli E, Mayer JH, McCarthy M, McCombie WR, McLaren S, McLay K, McPherson JD, Meldrim J, Meredith B, Mesirov JP, Miller W, Miner TL, Mongin E, Montgomery KT, Morgan M, Mott R, Mullikin JC, Muzny DM, Nash WE, Nelson JO, Nhan MN, Nicol R, Ning Z, Nusbaum C, O’Connor MJ, Okazaki Y, Oliver K, Overton-Larty E, Pachter L, Parra G, Pepin KH, Peterson J, Pevzner P, Plumb R, Pohl CS, Poliakov A, Ponce TC, Ponting CP, Potter S, Quail M, Reymond A, Roe BA, Roskin KM, Rubin EM, Rust AG, Santos R, Sapojnikov V, Schultz B, Schultz J, Schwartz MS, Schwartz S, Scott C, Seaman S, Searle S, Sharpe T, Sheridan A, Shownkeen R, Sims S, Singer JB, Slater G, Smit A, Smith DR, Spencer B, Stabenau A, Stange-Thomann N, Sugnet C, Suyama M, Tesler G, Thompson J, Torrents D, Trevaskis E, Tromp J, Ucla C, Ureta-Vidal A, Vinson JP, Von Niederhausern AC, Wade CM, Wall M, Weber RJ, Weiss RB, Wendl MC, West AP, Wetterstrand K, Wheeler R, Whelan S, Wierzbowski J, Willey D, Williams S, Wilson RK, Winter E, Worley KC, Wyman D, Yang S, Yang SP, Zdobnov EM, Zody MC, Lander ES (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562Google Scholar
  77. Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G, Auvil L, Beever JE, Chowdhary BP, Galibert F, Gatzke L, Hitte C, Meyers SN, Milan D, Ostrander EA, Pape G, Parker HG, Raudsepp T, Rogatcheva MB, Schook LB, Skow LC, Welge M, Womack JE, O’Brien SJ, Pevzner PA, Lewin HA (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617PubMedGoogle Scholar
  78. Nadeau JH, Taylor BA (1984) Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Natl Acad Sci USA 81:814–818PubMedCentralPubMedGoogle Scholar
  79. Navarro A, Betran E, Barbadilla A, Ruiz A (1997) Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146:695–709PubMedCentralPubMedGoogle Scholar
  80. Parrish JE, Oostra BA, Verkerk AJ, Richards CS, Reynolds J, Spikes AS, Shaffer LG, Nelson DL (1994) Isolation of a GCC repeat showing expansion in FRAXF, a fragile site distal to FRAXA and FRAXE. Nat Genet 8:229–235PubMedGoogle Scholar
  81. Pevzner P, Tesler G (2003a) Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. Genome Res 13:37–45PubMedCentralPubMedGoogle Scholar
  82. Pevzner P, Tesler G (2003b) Human and mouse genomic sequences reveal extensive breakpoint reuse in mammalian evolution. Proc Natl Acad Sci USA 100:7672–7677PubMedCentralPubMedGoogle Scholar
  83. Ranz JM, Maurin D, Chan YS, von Grotthuss M, Hillier LW, Roote J, Ashburner M, Bergman CM (2007) Principles of genome evolution in the Drosophila melanogaster species group. PLoS Biol 5:e152PubMedCentralPubMedGoogle Scholar
  84. Richards S, Liu Y, Bettencourt BR, Hradecky P, Letovsky S, Nielsen R, Thornton K, Hubisz MJ, Chen R, Meisel RP, Couronne O, Hua S, Smith MA, Zhang P, Liu J, Bussemaker HJ, van Batenburg MF, Howells SL, Scherer SE, Sodergren E, Matthews BB, Crosby MA, Schroeder AJ, Ortiz-Barrientos D, Rives CM, Metzker ML, Muzny DM, Scott G, Steffen D, Wheeler DA, Worley KC, Havlak P, Durbin KJ, Egan A, Gill R, Hume J, Morgan MB, Miner G, Hamilton C, Huang Y, Waldron L, Verduzco D, Clerc-Blankenburg KP, Dubchak I, Noor MA, Anderson W, White KP, Clark AG, Schaeffer SW, Gelbart W, Weinstock GM, Gibbs RA (2005) Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Res 15:1–18PubMedCentralPubMedGoogle Scholar
  85. Ritchie RJ, Knight SJ, Hirst MC, Grewal PK, Bobrow M, Cross GS, Davies KE (1994) The cloning of FRAXF: trinucleotide repeat expansion and methylation at a third fragile site in distal Xqter. Hum Mol Genet 3:2115–2121PubMedGoogle Scholar
  86. Rodriguez V, Llambi S, Postiglioni A, Guevara K, Rincon G, Fernandez G, Mernies B, Arruga MV (2002) Localisation of aphidicolin-induced break points in Holstein-Friesian cattle (Bos taurus) using RBG-banding. Genet Sel Evol 34:649–656PubMedCentralPubMedGoogle Scholar
  87. Ronne M (1992) Putative fragile sites in the horse karyotype. Hereditas 117:127–136PubMedGoogle Scholar
  88. Ronne M (1995a) Localization of fragile sites in the karyotype of Felis catus. Hereditas 122:279–283PubMedGoogle Scholar
  89. Ronne M (1995b) Localization of fragile sites in the karyotype of Sus scrofa domestica: present status. Hereditas 122:153–162PubMedGoogle Scholar
  90. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, Frankish A, Lovell FL, Howe KL, Ashurst JL, Fulton RS, Sudbrak R, Wen G, Jones MC, Hurles ME, Andrews TD, Scott CE, Searle S, Ramser J, Whittaker A, Deadman R, Carter NP, Hunt SE, Chen R, Cree A, Gunaratne P, Havlak P, Hodgson A, Metzker ML, Richards S, Scott G, Steffen D, Sodergren E, Wheeler DA, Worley KC, Ainscough R, Ambrose KD, Ansari-Lari MA, Aradhya S, Ashwell RI, Babbage AK, Bagguley CL, Ballabio A, Banerjee R, Barker GE, Barlow KF, Barrett IP, Bates KN, Beare DM, Beasley H, Beasley O, Beck A, Bethel G, Blechschmidt K, Brady N, Bray-Allen S, Bridgeman AM, Brown AJ, Brown MJ, Bonnin D, Bruford EA, Buhay C, Burch P, Burford D, Burgess J, Burrill W, Burton J, Bye JM, Carder C, Carrel L, Chako J, Chapman JC, Chavez D, Chen E, Chen G, Chen Y, Chen Z, Chinault C, Ciccodicola A, Clark SY, Clarke G, Clee CM, Clegg S, Clerc-Blankenburg K, Clifford K, Cobley V, Cole CG, Conquer JS, Corby N, Connor RE, David R, Davies J, Davis C, Davis J, Delgado O, Deshazo D, Dhami P, Ding Y, Dinh H, Dodsworth S, Draper H, Dugan-Rocha S, Dunham A, Dunn M, Durbin KJ, Dutta I, Eades T, Ellwood M, Emery-Cohen A, Errington H, Evans KL, Faulkner L, Francis F, Frankland J, Fraser AE, Galgoczy P, Gilbert J, Gill R, Glockner G, Gregory SG, Gribble S, Griffiths C, Grocock R, Gu Y, Gwilliam R, Hamilton C, Hart EA, Hawes A, Heath PD, Heitmann K, Hennig S, Hernandez J, Hinzmann B, Ho S, Hoffs M, Howden PJ, Huckle EJ, Hume J, Hunt PJ, Hunt AR, Isherwood J, Jacob L, Johnson D, Jones S, de Jong PJ, Joseph SS, Keenan S, Kelly S, Kershaw JK, Khan Z, Kioschis P, Klages S, Knights AJ, Kosiura A, Kovar-Smith C, Laird GK, Langford C, Lawlor S, Leversha M, Lewis L, Liu W, Lloyd C, Lloyd DM, Loulseged H, Loveland JE, Lovell JD, Lozado R, Lu J, Lyne R, Ma J, Maheshwari M, Matthews LH, McDowall J, McLaren S, McMurray A, Meidl P, Meitinger T, Milne S, Miner G, Mistry SL, Morgan M, Morris S, Muller I, Mullikin JC, Nguyen N, Nordsiek G, Nyakatura G, O’Dell CN, Okwuonu G, Palmer S, Pandian R, Parker D, Parrish J, Pasternak S, Patel D, Pearce AV, Pearson DM, Pelan SE, Perez L, Porter KM, Ramsey Y, Reichwald K, Rhodes S, Ridler KA, Schlessinger D, Schueler MG, Sehra HK, Shaw-Smith C, Shen H, Sheridan EM, Shownkeen R, Skuce CD, Smith ML, Sotheran EC, Steingruber HE, Steward CA, Storey R, Swann RM, Swarbreck D, Tabor PE, Taudien S, Taylor T, Teague B, Thomas K, Thorpe A, Timms K, Tracey A, Trevanion S, Tromans AC, d’Urso M, Verduzco D, Villasana D, Waldron L, Wall M, Wang Q, Warren J, Warry GL, Wei X, West A, Whitehead SL, Whiteley MN, Wilkinson JE, Willey DL, Williams G, Williams L, Williamson A, Williamson H, Wilming L, Woodmansey RL, Wray PW, Yen J, Zhang J, Zhou J, Zoghbi H, Zorilla S, Buck D, Reinhardt R, Poustka A, Rosenthal A, Lehrach H, Meindl A, Minx PJ, Hillier LW, Willard HF, Wilson RK, Waterston RH, Rice CM, Vaudin M, Coulson A, Nelson DL, Weinstock G, Sulston JE, Durbin R, Hubbard T, Gibbs RA, Beck S, Rogers J, Bentley DR (2005) The DNA sequence of the human X chromosome. Nature 434:325–337PubMedCentralPubMedGoogle Scholar
  91. Ruiz-Herrera A, Robinson TJ (2007) Chromosomal instability in Afrotheria: fragile sites, evolutionary breakpoints and phylogenetic inference from genome sequence assemblies. BMC Evol Biol 7:199PubMedCentralPubMedGoogle Scholar
  92. Ruiz-Herrera A, Ponsa M, Garcia F, Egozcue J, Garcia M (2002) Fragile sites in human and Macaca fascicularis chromosomes are breakpoints in chromosome evolution. Chromosom Res 10:33–44Google Scholar
  93. Ruiz-Herrera A, Garcia F, Fronicke L, Ponsa M, Egozcue J, Caldes MG, Stanyon R (2004) Conservation of aphidicolin-induced fragile sites in Papionini (Primates) species and humans. Chromosom Res 12:683–690Google Scholar
  94. Ruiz-Herrera A, Garcia F, Giulotto E, Attolini C, Egozcue J, Ponsa M, Garcia M (2005) Evolutionary breakpoints are co-localized with fragile sites and intrachromosomal telomeric sequences in primates. Cytogenet genome Res 108:234–247PubMedGoogle Scholar
  95. Ruiz-Herrera A, Castresana J, Robinson TJ (2006) Is mammalian chromosomal evolution driven by regions of genome fragility? Genome Biol 7:R115PubMedCentralPubMedGoogle Scholar
  96. Samonte RV, Eichler EE (2002) Segmental duplications and the evolution of the primate genome. Nat Rev Genet 3:65–72PubMedGoogle Scholar
  97. Scanlan MJ, Gure AO, Jungbluth AA, Old LJ, Chen YT (2002) Cancer/testis antigens: an expanding family of targets for cancer immunotherapy. Immunol Rev 188:22–32PubMedGoogle Scholar
  98. Schibler L, Roig A, Mahe MF, Laurent P, Hayes H, Rodolphe F, Cribiu EP (2006) High-resolution comparative mapping among man, cattle and mouse suggests a role for repeat sequences in mammalian genome evolution. BMC Genom 7:194Google Scholar
  99. Schwartz M, Zlotorynski E, Kerem B (2006) The molecular basis of common and rare fragile sites. Cancer Lett 232:13–26PubMedGoogle Scholar
  100. Seki N, Azuma T, Yoshikawa T, Masuho Y, Muramatsu M, Saito T (2000) cDNA cloning of a new member of the Ras superfamily, RAB9-like, on the human chromosome Xq22.1-q22.3 region. J Hum Genet 45:318–322PubMedGoogle Scholar
  101. Shimasaki S, Moore RK, Otsuka F, Erickson GF (2004) The bone morphogenetic protein system in mammalian reproduction. Endocr Rev 25:72–101PubMedGoogle Scholar
  102. Shiraishi T, Druck T, Mimori K, Flomenberg J, Berk L, Alder H, Miller W, Huebner K, Croce CM (2001) Sequence conservation at human and mouse orthologous common fragile regions, FRA3B/FHIT and Fra14A2/Fhit. Proc Natl Acad Sci USA 98:5722–5727PubMedCentralPubMedGoogle Scholar
  103. Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ (2005) Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 5:615–625PubMedGoogle Scholar
  104. Sonoda E, Hochegger H, Saberi A, Taniguchi Y, Takeda S (2006) Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair 5:1021–1029PubMedGoogle Scholar
  105. Sperlich D, Pfriem P (1986) Chromosomal polymorphism in natural and experimental populations. Genet Biol Drosoph 3:257–309Google Scholar
  106. Sutherland GR (1977) Fragile sites on human chromosomes: demonstration of their dependence on the type of tissue culture medium. Science 197:265–266PubMedGoogle Scholar
  107. Tesler G (2002) GRIMM: genome rearrangements web server. Bioinformatics (Oxford, England) 18:492–493Google Scholar
  108. Tsantoulis PK, Kotsinas A, Sfikakis PP, Evangelou K, Sideridou M, Levy B, Mo L, Kittas C, Wu XR, Papavassiliou AG, Gorgoulis VG (2008) Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene 27:3256–3264Google Scholar
  109. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, Gocayne JD, Amanatides P, Ballew RM, Huson DH, Wortman JR, Zhang Q, Kodira CD, Zheng XH, Chen L, Skupski M, Subramanian G, Thomas PD, Zhang J, Gabor Miklos GL, Nelson C, Broder S, Clark AG, Nadeau J, McKusick VA, Zinder N, Levine AJ, Roberts RJ, Simon M, Slayman C, Hunkapiller M, Bolanos R, Delcher A, Dew I, Fasulo D, Flanigan M, Florea L, Halpern A, Hannenhalli S, Kravitz S, Levy S, Mobarry C, Reinert K, Remington K, Abu-Threideh J, Beasley E, Biddick K, Bonazzi V, Brandon R, Cargill M, Chandramouliswaran I, Charlab R, Chaturvedi K, Deng Z, Di Francesco V, Dunn P, Eilbeck K, Evangelista C, Gabrielian AE, Gan W, Ge W, Gong F, Gu Z, Guan P, Heiman TJ, Higgins ME, Ji RR, Ke Z, Ketchum KA, Lai Z, Lei Y, Li Z, Li J, Liang Y, Lin X, Lu F, Merkulov GV, Milshina N, Moore HM, Naik AK, Narayan VA, Neelam B, Nusskern D, Rusch DB, Salzberg S, Shao W, Shue B, Sun J, Wang Z, Wang A, Wang X, Wang J, Wei M, Wides R, Xiao C, Yan C, Yao A, Ye J, Zhan M, Zhang W, Zhang H, Zhao Q, Zheng L, Zhong F, Zhong W, Zhu S, Zhao S, Gilbert D, Baumhueter S, Spier G, Carter C, Cravchik A, Woodage T, Ali F, An H, Awe A, Baldwin D, Baden H, Barnstead M, Barrow I, Beeson K, Busam D, Carver A, Center A, Cheng ML, Curry L, Danaher S, Davenport L, Desilets R, Dietz S, Dodson K, Doup L, Ferriera S, Garg N, Gluecksmann A, Hart B, Haynes J, Haynes C, Heiner C, Hladun S, Hostin D, Houck J, Howland T, Ibegwam C, Johnson J, Kalush F, Kline L, Koduru S, Love A, Mann F, May D, McCawley S, McIntosh T, McMullen I, Moy M, Moy L, Murphy B, Nelson K, Pfannkoch C, Pratts E, Puri V, Qureshi H, Reardon M, Rodriguez R, Rogers YH, Romblad D, Ruhfel B, Scott R, Sitter C, Smallwood M, Stewart E, Strong R, Suh E, Thomas R, Tint NN, Tse S, Vech C, Wang G, Wetter J, Williams S, Williams M, Windsor S, Winn-Deen E, Wolfe K, Zaveri J, Zaveri K, Abril JF, Guigo R, Campbell MJ, Sjolander KV, Karlak B, Kejariwal A, Mi H, Lazareva B, Hatton T, Narechania A, Diemer K, Muruganujan A, Guo N, Sato S, Bafna V, Istrail S, Lippert R, Schwartz R, Walenz B, Yooseph S, Allen D, Basu A, Baxendale J, Blick L, Caminha M, Carnes-Stine J, Caulk P, Chiang YH, Coyne M, Dahlke C, Mays A, Dombroski M, Donnelly M, Ely D, Esparham S, Fosler C, Gire H, Glanowski S, Glasser K, Glodek A, Gorokhov M, Graham K, Gropman B, Harris M, Heil J, Henderson S, Hoover J, Jennings D, Jordan C, Jordan J, Kasha J, Kagan L, Kraft C, Levitsky A, Lewis M, Liu X, Lopez J, Ma D, Majoros W, McDaniel J, Murphy S, Newman M, Nguyen T, Nguyen N, Nodell M, Pan S, Peck J, Peterson M, Rowe W, Sanders R, Scott J, Simpson M, Smith T, Sprague A, Stockwell T, Turner R, Venter E, Wang M, Wen M, Wu D, Wu M, Xia A, Zandieh A, Zhu X (2001) The sequence of the human genome. Science 291:1304–1351PubMedGoogle Scholar
  110. Verkerk AJ, Pieretti M, Sutcliffe JS, Fu YH, Kuhl DP, Pizzuti A, Reiner O, Richards S, Victoria MF, Zhang FP et al (1991) Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65:905–914PubMedGoogle Scholar
  111. Vibranovski MD, Lopes HF, Karr TL, Long M (2009a) Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet 5:e1000731PubMedCentralPubMedGoogle Scholar
  112. Vibranovski MD, Zhang Y, Long M (2009b) General gene movement off the X chromosome in the Drosophila genus. Genome Res 19:897–903PubMedCentralPubMedGoogle Scholar
  113. Wasserman M (1982) Evolution of the repleta group. Genet Biol Drosoph 3:61–139Google Scholar
  114. Wilson MA, Makova KD (2009) Genomic analyses of sex chromosome evolution. Annu Rev Genomics Hum Genet 10:333–354PubMedGoogle Scholar
  115. Yang MY, Long SE (1993) Folate sensitive common fragile sites in chromosomes of the domestic pig (Sus scrofa). Res Vet Sci 55:231–235PubMedGoogle Scholar
  116. Zhang YE, Vibranovski MD, Landback P, Marais GA, Long M (2010) Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X chromosome. PLoS Biol 8:e1000494PubMedCentralPubMedGoogle Scholar
  117. Zhao S, Shetty J, Hou L, Delcher A, Zhu B, Osoegawa K, de Jong P, Nierman WC, Strausberg RL, Fraser CM (2004) Human, mouse, and rat genome large-scale rearrangements: stability versus speciation. Genome Res 14:1851–1860PubMedCentralPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Unidad de Genética, Grupo GENIUROS, Escuela de Medicina y Ciencias de la SaludUniversidad del RosarioBogotáColombia

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