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Genetics Research International
Volume 2012, Article ID 430587, 9 pages
http://dx.doi.org/10.1155/2012/430587
Review Article

Homologue Pairing in Flies and Mammals: Gene Regulation When Two Are Involved

Department of Biological Sciences, Wayne State University, Detroit, MI 48202, USA

Received 27 June 2011; Revised 17 September 2011; Accepted 26 September 2011

Academic Editor: Douglas M. Ruden

Copyright © 2012 Manasi S. Apte and Victoria H. Meller. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Stevens, “Study of the germ cells of certain Diptera, with reference to the Heterochromosomes and the Phenomena of Synapsis,” Journal of Experimental Zoology, vol. 5, pp. 359–374, 1908. View at Google Scholar
  2. C. W. Metz, “Chromosome studies on the Diptera. II. The paired association of chromosomes in the Diptera, and its significance,” Journal of Experimental Zoology, vol. 21, pp. 213–279, 1916. View at Google Scholar
  3. A. Lorenz, J. Fuchs, R. Bürger, and J. Loidl, “Chromosome pairing does not contribute to nuclear architecture in vegetative yeast cells,” Eukaryotic Cell, vol. 2, no. 5, pp. 856–866, 2003. View at Publisher · View at Google Scholar
  4. H. Scherthan, J. Bähler, and J. Kohli, “Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast,” Journal of Cell Biology, vol. 127, no. 2, pp. 273–285, 1994. View at Publisher · View at Google Scholar
  5. R. Aramayo and R. L. Metzenberg, “Meiotic transvection in fungi,” Cell, vol. 86, no. 1, pp. 103–113, 1996. View at Publisher · View at Google Scholar
  6. J. B. Hollick, J. E. Dorweiler, and V. L. Chandler, “Paramutation and related allelic interactions,” Trends in Genetics, vol. 13, no. 8, pp. 302–308, 1997. View at Publisher · View at Google Scholar
  7. J. Bender, “Cytosine methylation of repeated sequences in eukaryotes: the role of DNA pairing,” Trends in Biochemical Sciences, vol. 23, no. 7, pp. 252–256, 1998. View at Publisher · View at Google Scholar
  8. A. J. Matzke, K. Watanabe, J. Van Der Winden, U. Naumann, and M. Matzke, “High frequency, cell type-specific visualization of fluorescent-tagged genomic sites in interphase and mitotic cells of living Arabidopsis plants,” Plant Methods, vol. 6, article 2, 2010. View at Publisher · View at Google Scholar · View at PubMed
  9. E. P. Arnoldus, A. C. Peters, G. T. Bots, A. K. Raap, and M. Van Der Ploeg, “Somatic pairing of chromosome 1 centromeres in interphase nuclei of human cerebellum,” Human Genetics, vol. 83, no. 3, pp. 231–234, 1989. View at Google Scholar
  10. E. P. Arnoldus, A. Noordermeer, A. C. Peters, A. K. Raap, and M. Van Der Ploeg, “Interphase cytogenetics reveals somatic pairing of chromosome 17 centromeres in normal human brain tissue, but no trisomy 7 or sex-chromosome loss,” Cytogenetics and Cell Genetics, vol. 56, no. 3-4, pp. 214–216, 1991. View at Google Scholar
  11. S. J. Dalrymple, J. F. Herath, T. J. Borell, C. A. Moertel, and R. B. Jenkins, “Correlation of cytogenetic and fluorescence in situ hybridization (FISH) studies in normal and gliotic brain,” Journal of Neuropathology and Experimental Neurology, vol. 53, no. 5, pp. 448–456, 1994. View at Google Scholar
  12. N. B. Atkin and Z. Jackson, “Evidence for somatic pairing of chromosome 7 and 10 homologs in a follicular lymphoma,” Cancer Genetics and Cytogenetics, vol. 89, no. 2, pp. 129–131, 1996. View at Publisher · View at Google Scholar
  13. J. M. Koeman, R. C. Russell, M. H. Tan et al., “Somatic pairing of chromosome 19 in renal oncocytoma is associated with deregulated EGLN2-mediated [corrected] oxygen-sensing response,” PLoS Genetics, vol. 4, no. 9, Article ID e1000176, 2008. View at Google Scholar
  14. T. Cremer and C. Cremer, “Chromosome territories, nuclear architecture and gene regulation in mammalian cells,” Nature Reviews Genetics, vol. 2, no. 4, pp. 292–301, 2001. View at Publisher · View at Google Scholar · View at PubMed
  15. M. Bartkuhn and R. Renkawitz, “Long range chromatin interactions involved in gene regulation,” Biochimica et Biophysica Acta, vol. 1783, no. 11, pp. 2161–2166, 2008. View at Publisher · View at Google Scholar · View at PubMed
  16. D. L. Spector, “The dynamics of chromosome organization and gene regulation,” Annual Review of Biochemistry, vol. 72, pp. 573–608, 2003. View at Publisher · View at Google Scholar · View at PubMed
  17. J. A. Croft, J. M. Bridger, S. Boyle, P. Perry, P. Teague, and W. A. Bickmore, “Differences in the localization and morphology of chromosomes in the human nucleus,” Journal of Cell Biology, vol. 145, no. 6, pp. 1119–1131, 1999. View at Publisher · View at Google Scholar
  18. L. B. Caddle, J. L. Grant, J. Szatkiewicz et al., “Chromosome neighborhood composition determines translocation outcomes after exposure to high-dose radiation in primary cells,” Chromosome Research, vol. 15, no. 8, pp. 1061–1073, 2007. View at Publisher · View at Google Scholar · View at PubMed
  19. C. Heride, M. Ricoul, K. Kiêu et al., “Distance between homologous chromosomes results from chromosome positioning constraints,” Journal of Cell Science, vol. 123, no. 23, pp. 4063–4075, 2010. View at Publisher · View at Google Scholar · View at PubMed
  20. J. E. Phillips and V. G. Corces, “CTCF: master weaver of the genome,” Cell, vol. 137, no. 7, pp. 1194–1211, 2009. View at Publisher · View at Google Scholar · View at PubMed
  21. V. V. Lobanenkov, R. H. Nicolas, V. V. Adler et al., “A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5-flanking sequence of the chicken c-myc gene,” Oncogene, vol. 5, no. 12, pp. 1743–1753, 1990. View at Google Scholar
  22. E. M. Klenova, R. H. Nicolas, H. F. Paterson et al., “CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms,” Molecular and Cellular Biology, vol. 13, no. 12, pp. 7612–7624, 1993. View at Google Scholar
  23. G. N. Filippova, S. Fagerlie, E. M. Klenova et al., “An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes,” Molecular and Cellular Biology, vol. 16, no. 6, pp. 2802–2813, 1996. View at Google Scholar
  24. A. A. Vostrov and W. W. Quitschke, “The zinc finger protein CTCF binds to the APBβ domain of the amyloid β-protein precursor promoter: evidence for a role in transcriptional activation,” Journal of Biological Chemistry, vol. 272, no. 52, pp. 33353–33359, 1997. View at Publisher · View at Google Scholar
  25. A. Murrell, S. Heeson, and W. Reik, “Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops,” Nature Genetics, vol. 36, no. 8, pp. 889–893, 2004. View at Publisher · View at Google Scholar · View at PubMed
  26. S. Kurukuti, V. K. Tiwari, G. Tavoosidana et al., “CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 28, pp. 10684–10689, 2006. View at Publisher · View at Google Scholar · View at PubMed
  27. E. Splinter, H. Heath, J. Kooren et al., “CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus,” Genes and Development, vol. 20, no. 17, pp. 2349–2354, 2006. View at Publisher · View at Google Scholar · View at PubMed
  28. C. Hou, H. Zhao, K. Tanimoto, and A. Dean, “CTCF-dependent enhancer-blocking by alternative chromatin loop formation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 51, pp. 20398–20403, 2008. View at Publisher · View at Google Scholar · View at PubMed
  29. T. Li, J. F. Hu, X. Qiu et al., “CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop,” Molecular and Cellular Biology, vol. 28, no. 20, pp. 6473–6482, 2008. View at Publisher · View at Google Scholar · View at PubMed
  30. P. Majumder, J. A. Gomez, B. P. Chadwick, and J. M. Boss, “The insulator factor CTCF controls MHC class II gene expression and is required for the formation of long-distance chromatin interactions,” Journal of Experimental Medicine, vol. 205, no. 4, pp. 785–798, 2008. View at Publisher · View at Google Scholar · View at PubMed
  31. R. I. Verona, M. R. Mann, and M. S. Bartolomei, “Genomic imprinting: intricacies of epigenetic regulation in clusters,” Annual Review of Cell and Developmental Biology, vol. 19, pp. 237–259, 2003. View at Publisher · View at Google Scholar · View at PubMed
  32. K. D. Tremblay, J. R. Saam, R. S. Ingram, S. M. Tilghman, and M. S. Bartolomei, “A paternal-specific methylation imprint marks the alleles of the mouse H19 gene,” Nature Genetics, vol. 9, no. 4, pp. 407–413, 1995. View at Google Scholar
  33. A. T. Hark, C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman, “CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus,” Nature, vol. 405, no. 6785, pp. 486–489, 2000. View at Publisher · View at Google Scholar · View at PubMed
  34. A. M. Fedoriw, P. Stein, P. Svoboda, R. M. Schultz, and M. S. Bartolomei, “Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting,” Science, vol. 303, no. 5655, pp. 238–240, 2004. View at Publisher · View at Google Scholar · View at PubMed
  35. A. C. Bell and G. Felsenfeld, “Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene,” Nature, vol. 405, no. 6785, pp. 482–485, 2000. View at Publisher · View at Google Scholar · View at PubMed
  36. C. Kanduri, V. Pant, D. Loukinov et al., “Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive,” Current Biology, vol. 10, no. 14, pp. 853–856, 2000. View at Publisher · View at Google Scholar
  37. P. Szabó, S. H. Tang, A. Rentsendorj, G. P. Pfeifer, and J. R. Mann, “Maternal-specific footprints at putative CTCF sites in the H19 imprinting control region give evidence for insulator function,” Current Biology, vol. 10, no. 10, pp. 607–610, 2000. View at Publisher · View at Google Scholar
  38. C. J. Schoenherr, J. M. Levorse, and S. M. Tilghman, “CTCF maintains differential methylation at the Igf2/H19 locus,” Nature Genetics, vol. 33, no. 1, pp. 66–69, 2003. View at Publisher · View at Google Scholar · View at PubMed
  39. J. Q. Ling, T. Li, J. F. Hu et al., “CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1,” Science, vol. 312, no. 5771, pp. 269–272, 2006. View at Publisher · View at Google Scholar · View at PubMed
  40. K. S. Sandhu, C. Shi, M. Sjölinder et al., “Nonallelic transvection of multiple imprinted loci is organized by the H19 imprinting control region during germline development,” Genes and Development, vol. 23, no. 22, pp. 2598–2603, 2009. View at Publisher · View at Google Scholar · View at PubMed
  41. J. M. LaSalle and M. Lalande, “Homologous association of oppositely imprinted chromosomal domains,” Science, vol. 272, no. 5262, pp. 725–728, 1996. View at Google Scholar
  42. M. Lalande, “Parental imprinting and human disease,” Annual Review of Genetics, vol. 30, pp. 173–195, 1996. View at Publisher · View at Google Scholar · View at PubMed
  43. K. N. Thatcher, S. Peddada, D. H. Yasui, and J. M. LaSalle, “Homologous pairing of 15q11-13 imprinted domains in brain is developmentally regulated but deficient in Rett and autism samples,” Human Molecular Genetics, vol. 14, no. 6, pp. 785–797, 2005. View at Publisher · View at Google Scholar · View at PubMed
  44. V. Gupta, M. Parisi, D. Sturgill et al., “Global analysis of X-chromosome dosage compensation,” Journal of Biology, vol. 5, article 3, 2006. View at Publisher · View at Google Scholar · View at PubMed
  45. D. K. Nguyen and C. M. Disteche, “Dosage compensation of the active X chromosome in mammals,” Nature Genetics, vol. 38, no. 1, pp. 47–53, 2006. View at Publisher · View at Google Scholar · View at PubMed
  46. M. Royce-Tolland and B. Panning, “X-inactivation: it takes two to count,” Current Biology, vol. 18, no. 6, pp. R255–R256, 2008. View at Publisher · View at Google Scholar · View at PubMed
  47. J. T. Lee, “Homozygous Tsix mutant mice reveal a sex-ratio distortion and revert to random X-inactivation,” Nature Genetics, vol. 32, no. 1, pp. 195–200, 2002. View at Publisher · View at Google Scholar · View at PubMed
  48. C. P. Bacher, M. Guggiari, B. Brors et al., “Transient colocalization of X-inactivation centres accompanies the initiation of X inactivation,” Nature Cell Biology, vol. 8, no. 3, pp. 293–299, 2006. View at Publisher · View at Google Scholar · View at PubMed
  49. S. Augui, G. J. Filion, S. Huart et al., “Sensing X chromosome pairs before X inactivation via a novel X-pairing region of the Xic,” Science, vol. 318, no. 5856, pp. 1632–1636, 2007. View at Publisher · View at Google Scholar · View at PubMed
  50. J. Chow and E. Heard, “X inactivation and the complexities of silencing a sex chromosome,” Current Opinion in Cell Biology, vol. 21, no. 3, pp. 359–366, 2009. View at Publisher · View at Google Scholar · View at PubMed
  51. J. T. Lee, “Lessons from X-chromosome inactivation: long ncRNA as guides and tethers to the epigenome,” Genes and Development, vol. 23, no. 16, pp. 1831–1842, 2009. View at Publisher · View at Google Scholar · View at PubMed
  52. N. Xu, M. E. Donohoe, S. S. Silva, and J. T. Lee, “Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein,” Nature Genetics, vol. 39, no. 11, pp. 1390–1396, 2007. View at Publisher · View at Google Scholar · View at PubMed
  53. W. Chao, K. D. Huynh, R. J. Spencer, L. S. Davidow, and J. T. Lee, “CTCF, a candidate trans-acting factor for X-inactivation choice,” Science, vol. 295, no. 5553, pp. 345–347, 2002. View at Publisher · View at Google Scholar · View at PubMed
  54. N. Xu, C. L. Tsai, and J. T. Lee, “Transient homologous chromosome pairing marks the onset of X inactivation,” Science, vol. 311, no. 5764, pp. 1149–1152, 2006. View at Publisher · View at Google Scholar · View at PubMed
  55. M. Xu and P. R. Cook, “The role of specialized transcription factories in chromosome pairing,” Biochimica et Biophysica Acta, vol. 1783, no. 11, pp. 2155–2160, 2008. View at Publisher · View at Google Scholar · View at PubMed
  56. M. E. Donohoe, S. S. Silva, S. F. Pinter, N. Xu, and J. T. Lee, “The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting,” Nature, vol. 460, no. 7251, pp. 128–132, 2009. View at Publisher · View at Google Scholar · View at PubMed
  57. A. Wutz and R. Jaenisch, “A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation,” Molecular Cell, vol. 5, no. 4, pp. 695–705, 2000. View at Google Scholar
  58. J. A. Wallace and G. Felsenfeld, “We gather together: insulators and genome organization,” Current Opinion in Genetics and Development, vol. 17, no. 5, pp. 400–407, 2007. View at Publisher · View at Google Scholar · View at PubMed
  59. T. M. Yusufzai, H. Tagami, Y. Nakatani, and G. Felsenfeld, “CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species,” Molecular Cell, vol. 13, no. 2, pp. 291–298, 2004. View at Publisher · View at Google Scholar
  60. O. Masui, I. Bonnet, P. Le Baccon et al., “Live-cell chromosome dynamics and outcome of X chromosome pairing events during ES cell differentiation,” Cell, vol. 145, no. 3, pp. 447–458, 2011. View at Publisher · View at Google Scholar · View at PubMed
  61. D. Ivanov and K. Nasmyth, “A physical assay for sister chromatid cohesion in vitro,” Molecular Cell, vol. 27, no. 2, pp. 300–310, 2007. View at Publisher · View at Google Scholar · View at PubMed
  62. K. Nasmyth and C. H. Haering, “Cohesin: its roles and mechanisms,” Annual Review of Genetics, vol. 43, pp. 525–558, 2009. View at Publisher · View at Google Scholar · View at PubMed
  63. V. Parelho, S. Hadjur, M. Spivakov et al., “Cohesins functionally associate with CTCF on mammalian chromosome arms,” Cell, vol. 132, no. 3, pp. 422–433, 2008. View at Publisher · View at Google Scholar · View at PubMed
  64. K. S. Wendt, K. Yoshida, T. Itoh et al., “Cohesin mediates transcriptional insulation by CCCTC-binding factor,” Nature, vol. 451, no. 7180, pp. 796–801, 2008. View at Publisher · View at Google Scholar · View at PubMed
  65. T. Xiao, J. Wallace, and G. Felsenfeld, “Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity,” Molecular and Cellular Biology, vol. 31, no. 11, pp. 2174–2183, 2011. View at Publisher · View at Google Scholar · View at PubMed
  66. S. Hadjur, L. M. Williams, N. K. Ryan et al., “Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus,” Nature, vol. 460, no. 7253, pp. 410–413, 2009. View at Publisher · View at Google Scholar · View at PubMed
  67. R. Nativio, K. S. Wendt, Y. Ito et al., “Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus,” PLoS Genetics, vol. 5, no. 11, Article ID e1000739, 2009. View at Publisher · View at Google Scholar · View at PubMed
  68. E. E. Holohan, C. Kwong, B. Adryan et al., “CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex,” PLoS genetics, vol. 3, no. 7, p. e112, 2007. View at Publisher · View at Google Scholar · View at PubMed
  69. O. Kyrchanova, T. Ivlieva, S. Toshchakov, A. Parshikov, O. Maksimenko, and P. Georgiev, “Selective interactions of boundaries with upstream region of Abd-B promoter in Drosophila bithorax complex and role of dCTCF in this process,” Nucleic Acids Research, vol. 39, pp. 3042–3052, 2011. View at Google Scholar
  70. W. A. MacDonald, D. Menon, N. J. Bartlett et al., “The Drosophila homolog of the mammalian imprint regulator, CTCF, maintains the maternal genomic imprint in Drosophila melanogaster,” BMC Biology, vol. 8, article 105, 2010. View at Publisher · View at Google Scholar · View at PubMed
  71. J. C. Fung, W. F. Marshall, A. Dernburg, D. A. Agard, and J. W. Sedat, “Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations,” Journal of Cell Biology, vol. 141, no. 1, pp. 5–20, 1998. View at Publisher · View at Google Scholar
  72. Y. Hiraoka, A. F. Dernburg, S. J. Parmelee, M. C. Rykowski, D. A. Agard, and J. W. Sedat, “The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis,” Journal of Cell Biology, vol. 120, no. 3, pp. 591–600, 1993. View at Publisher · View at Google Scholar
  73. V. E. Foe and B. M. Alberts, “Studies of nuclear and cytoplasmic behavior during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis,” Journal of Cell Science, vol. 61, pp. 31–70, 1983. View at Google Scholar
  74. B. Y. Lu, J. Ma, and J. C. Eissenberg, “Developmental regulation of heterochromatin-mediated gene silencing in Drosophila,” Development, vol. 125, no. 12, pp. 2223–2234, 1998. View at Google Scholar
  75. A. K. Csink and S. Henikoff, “Large-scale chromosomal movements during interphase progression in Drosophila,” Journal of Cell Biology, vol. 143, no. 1, pp. 13–22, 1998. View at Publisher · View at Google Scholar
  76. B. R. Williams, J. R. Bateman, N. D. Novikov, and C. T. Wu, “Disruption of topoisomerase II perturbs pairing in Drosophila cell culture,” Genetics, vol. 177, no. 1, pp. 31–46, 2007. View at Publisher · View at Google Scholar · View at PubMed
  77. P. R. Cook, “The transcriptional basis of chromosome pairing,” Journal of Cell Science, vol. 110, no. 9, pp. 1033–1040, 1997. View at Google Scholar
  78. A. P. Santos and P. Shaw, “Interphase chromosomes and the Rabl configuration: does genome size matter?” Journal of Microscopy, vol. 214, no. 2, pp. 201–206, 2004. View at Publisher · View at Google Scholar · View at PubMed
  79. Q. W. Jin, J. Fuchs, and J. Loidl, “Centromere clustering is a major determinant of yeast interphase nuclear organization,” Journal of Cell Science, vol. 113, no. 11, pp. 1903–1912, 2000. View at Google Scholar
  80. E. B. Lewis, “The theory and application of a new method of detecting chromosomal rearrangements in Drosphila melanogaster,” American Naturalist, vol. 88, pp. 225–239, 1954. View at Google Scholar
  81. P. K. Geyer, M. M. Green, and V. G. Corces, “Tissue specific transcriptional enhancers may act in trans on the gene located in the homologous chromosome: the molecular basis of transvection in Drosophila,” EMBO Journal, vol. 9, no. 7, pp. 2247–2256, 1990. View at Google Scholar
  82. S. A. Ou, E. Chang, S. Lee, K. So, C. T. Wu, and J. R. Morris, “Effects of chromosomal rearrangements on transvection at the yellow gene of Drosophila melanogaster,” Genetics, vol. 183, no. 2, pp. 483–496, 2009. View at Publisher · View at Google Scholar · View at PubMed
  83. J. L. Chen, K. L. Huisinga, M. M. Viering, S. A. Ou, C. T. Wu, and P. K. Geyer, “Enhancer action in trans is permitted throughout the Drosophila genome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 6, pp. 3723–3728, 2002. View at Publisher · View at Google Scholar · View at PubMed
  84. M. Rassoulzadegan, M. Magliano, and F. Cuzin, “Transvection effects involving DNA methylation during meiosis in the mouse,” EMBO Journal, vol. 21, no. 3, pp. 440–450, 2002. View at Publisher · View at Google Scholar
  85. H. Liu, J. Huang, J. Wang et al., “Transvection mediated by the translocated cyclin D1 locus in mantle cell lymphoma,” Journal of Experimental Medicine, vol. 205, no. 8, pp. 1843–1858, 2008. View at Publisher · View at Google Scholar · View at PubMed
  86. M. M. Golic and K. G. Golic, “A quantitative measure of the mitotic pairing of alleles in Drosophila melanogaster and the influence of structural heterozygosity,” Genetics, vol. 143, no. 1, pp. 385–400, 1996. View at Google Scholar
  87. V. Pirrotta, “The genetics and molecular biology of zeste in Drosophila melanogaster,” Advances in Genetics, vol. 29, pp. 301–348, 1991. View at Publisher · View at Google Scholar
  88. I. W. Duncan, “Transvection effects in Drosophila,” Annual Review of Genetics, vol. 36, pp. 521–556, 2002. View at Publisher · View at Google Scholar · View at PubMed
  89. M. J. Gemkow, P. J. Verveer, and D. J. Arndt-Jovin, “Homologous association of the Bithorax-Complex during embryogenesis: consequences for transvection in Drosophila melanogaster,” Development, vol. 125, no. 22, pp. 4541–4552, 1998. View at Google Scholar
  90. A. J. Kal, T. Mahmoudi, N. B. Zak, and C. P. Verrijzer, “The Drosophila Brahma complex is an essential coactivator for the trithorax group protein Zeste,” Genes and Development, vol. 14, no. 9, pp. 1058–1071, 2000. View at Google Scholar
  91. A. J. Saurin, Z. Shao, H. Erdjument-Bromage, P. Tempst, and R. E. Kingston, “A Drosophila Polycomb group complex includes Zeste and dTAFII proteins,” Nature, vol. 412, no. 6847, pp. 655–660, 2001. View at Google Scholar
  92. J. L. Nitiss, “DNA topoisomerase II and its growing repertoire of biological functions,” Nature Reviews Cancer, vol. 9, no. 5, pp. 327–337, 2009. View at Publisher · View at Google Scholar · View at PubMed
  93. S. M. Gasser, T. Laroche, J. Falquet, E. Boy De La Tour, and U. K. Laemmli, “Metaphase chromosome structure. Involvement of topoisomerase II,” Journal of Molecular Biology, vol. 188, no. 4, pp. 613–629, 1986. View at Google Scholar
  94. Y. Adachi, E. Kas, and U. K. Laemmli, “Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions,” EMBO Journal, vol. 8, no. 13, pp. 3997–4006, 1989. View at Google Scholar
  95. T. Ono, A. Losada, M. Hirano, M. P. Myers, A. F. Neuwald, and T. Hirano, “Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells,” Cell, vol. 115, no. 1, pp. 109–121, 2003. View at Publisher · View at Google Scholar
  96. F. M. Yeong, H. Hombauer, K. S. Wendt et al., “Identification of a subunit of a novel kleisin-β/SMC complex as a potential substrate of protein phosphatase 2A,” Current Biology, vol. 13, no. 23, pp. 2058–2064, 2003. View at Publisher · View at Google Scholar
  97. M. A. Bhat, A. V. Philp, D. M. Glover, and H. J. Bellen, “Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II,” Cell, vol. 87, no. 6, pp. 1103–1114, 1996. View at Publisher · View at Google Scholar
  98. N. Bhalla, S. Biggins, and A. W. Murray, “Mutation of YCS4, a budding yeast condensin subunit, affects mitotic and nonmitotic chromosome behavior,” Molecular Biology of the Cell, vol. 13, no. 2, pp. 632–645, 2002. View at Publisher · View at Google Scholar · View at PubMed
  99. P. A. Coelho, J. Queiroz-Machado, and C. E. Sunkel, “Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis,” Journal of Cell Science, vol. 116, no. 23, pp. 4763–4776, 2003. View at Publisher · View at Google Scholar · View at PubMed
  100. K. Maeshima and U. K. Laemmli, “A Two-step scaffolding model for mitotic chromosome assembly,” Developmental Cell, vol. 4, no. 4, pp. 467–480, 2003. View at Publisher · View at Google Scholar
  101. T. A. Hartl, H. F. Smith, and G. Bosco, “Chromosome alignment and transvection are antagonized by condensin II,” Science, vol. 322, no. 5906, pp. 1384–1387, 2008. View at Publisher · View at Google Scholar · View at PubMed
  102. A. S. Goldsborough and T. B. Kornberg, “Reduction of transcription by homologue asynapsis in Drosophila imaginal discs,” Nature, vol. 381, no. 6585, pp. 807–810, 1996. View at Publisher · View at Google Scholar · View at PubMed
  103. J. C. Lucchesi, “Dosage compensation in Drosophila and the 'complex' world of transcriptional regulation,” BioEssays, vol. 18, no. 7, pp. 541–547, 1996. View at Google Scholar
  104. S. E. Lott, J. E. Villalta, G. P. Schroth, S. Luo, L. A. Tonkin, and M. B. Eisen, “Noncanonical compensation of zygotic X transcription in early Drosophila melanogaster development revealed through single-embryo RNA-seq,” PLoS Biology, vol. 9, Article ID e1000590, 2011. View at Google Scholar
  105. L. Rastelli and M. I. Kuroda, “An analysis of maleless and histone H4 acetylation in Drosophila melanogaster spermatogenesis,” Mechanisms of Development, vol. 71, no. 1-2, pp. 107–117, 1998. View at Publisher · View at Google Scholar
  106. P. Stenberg and J. Larsson, “Buffering and the evolution of chromosome-wide gene regulation,” Chromosoma, vol. 120, no. 3, pp. 213–225, 2011. View at Publisher · View at Google Scholar · View at PubMed
  107. F. N. Hamada, P. J. Park, P. R. Gordadze, and M. I. Kuroda, “Global regulation of X chromosomal genes by the MSL complex in Drosophila melanogaster,” Genes and Development, vol. 19, no. 19, pp. 2289–2294, 2005. View at Publisher · View at Google Scholar · View at PubMed
  108. X. Deng and V. H. Meller, “roX RNAs are required for increased expression of X-linked genes in Drosophila melanogaster males,” Genetics, vol. 174, no. 4, pp. 1859–1866, 2006. View at Publisher · View at Google Scholar · View at PubMed
  109. B. Vicoso and B. Charlesworth, “Evolution on the X chromosome: unusual patterns and processes,” Nature Reviews Genetics, vol. 7, no. 8, pp. 645–653, 2006. View at Publisher · View at Google Scholar · View at PubMed
  110. T. A. Gurbich and D. Bachtrog, “Gene content evolution on the X chromosome,” Current Opinion in Genetics and Development, vol. 18, no. 6, pp. 493–498, 2008. View at Publisher · View at Google Scholar · View at PubMed
  111. M. J. Lercher, A. O. Urrutia, and L. D. Hurst, “Evidence that the human X chromosome is enriched for male-specific but not female-specific genes,” Molecular Biology and Evolution, vol. 20, no. 7, pp. 1113–1116, 2003. View at Publisher · View at Google Scholar · View at PubMed
  112. D. Sturgill, Y. Zhang, M. Parisi, and B. Oliver, “Demasculinization of X chromosomes in the Drosophila genus,” Nature, vol. 450, no. 7167, pp. 238–241, 2007. View at Publisher · View at Google Scholar · View at PubMed
  113. L. M. Mikhaylova and D. I. Nurminsky, “Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome,” BMC Biology, vol. 9, article 29, 2011. View at Publisher · View at Google Scholar · View at PubMed
  114. P. Stenberg, L. E. Lundberg, A. M. Johansson, P. Rydén, M. J. Svensson, and J. Larsson, “Buffering of segmental and chromosomal aneuploidies in Drosophila melanogaster,” PLoS Genetics, vol. 5, no. 5, Article ID e1000465, 2009. View at Publisher · View at Google Scholar · View at PubMed