BioMed Research International

BioMed Research International / 2006 / Article
Special Issue

LINE-1 Retrotransposition: Impact on Genome Stability and Diversity and Human Disease

View this Special Issue

Review Article | Open Access

Volume 2006 |Article ID 59746 | 6 pages | https://doi.org/10.1155/JBB/2006/59746

Do LINEs Have a Role in X-Chromosome Inactivation?

Received31 May 2005
Revised22 Nov 2005
Accepted04 Dec 2005
Published16 Mar 2006

Abstract

There is longstanding evidence that X-chromosome inactivation (XCI) travels less successfully in autosomal than in X-chromosomal chromatin. The interspersed repeat elements LINE1s (L1s) have been suggested as candidates for “boosters” which promote the spread of XCI in the X-chromosome. The present paper reviews the current evidence concerning the possible role of L1s in XCI. Recent evidence, accruing from the human genome sequencing project and other sources, confirms that mammalian X-chromosomes are indeed rich in L1s, except in regions where there are many genes escaping XCI. The density of L1s is the highest in the evolutionarily oldest regions. Recent work on X; autosome translocations in human and mouse suggested failure of stabilization of XCI in autosomal material, so that genes are reactivated, but resistance of autosomal genes to the original silencing is not excluded. The accumulation of L1s on the X-chromosome may have resulted from reduced recombination or late replication. Whether L1s are part of the mechanism of XCI or a result of it remains enigmatic.

References

  1. M F Lyon, “Gene action in the X-chromosome of the mouse (Mus musculus L.),” Nature, vol. 190, no. 4773, pp. 372–373, 1961. View at: Google Scholar
  2. L B Russell and J W Bangham, “Variegated-type position effects in the mouse,” Genetics, vol. 46, no. 5, pp. 509–525, 1961. View at: Google Scholar
  3. M F Lyon, “Cytogenetics, discussion,” in Proceedings of the Second International Conference on Congenital Malformations, pp. 67–68, New York, NY, July 1963. View at: Google Scholar
  4. L B Russell, “Mammalian X-chromosome action: inactivation limited in spread and region of origin,” Science, vol. 140, pp. 976–978, 1963. View at: Google Scholar
  5. G D Penny, G F Kay, S A Sheardown, S Rastan, and N Brockdorff, “Requirement for Xist in X chromosome inactivation,” Nature, vol. 379, no. 6561, pp. 131–137, 1996. View at: Google Scholar
  6. 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
  7. C M Clemson, J A McNeil, H F Willard, and J B Lawrence, “XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure,” The Journal of Cell Biology, vol. 132, no. 3, pp. 259–275, 1996. View at: Google Scholar
  8. E Heard, “Recent advances in X-chromosome inactivation,” Current Opinion in Cell Biology, vol. 16, no. 3, pp. 247–255, 2004. View at: Google Scholar
  9. S M Gartler and A D Riggs, “Mammalian X-chromosome inactivation,” Annual Review of Genetics, vol. 17, pp. 155–190, 1983. View at: Google Scholar
  10. A D Riggs, “Marsupials and mechanisms of X-chromosome inactivation,” Australian Journal of Zoology, vol. 37, no. 2, pp. 419–441, 1990. View at: Google Scholar
  11. M F Lyon, “Epigenetic inheritance in mammals,” Trends in Genetics, vol. 9, no. 4, pp. 123–128, 1993. View at: Google Scholar
  12. M F Lyon, “X-chromosome inactivation: a repeat hypothesis,” Cytogenetics and Cell Genetics, vol. 80, no. 1–4, pp. 133–137, 1998. View at: Google Scholar
  13. A L Boyle, S G Ballard, and D C Ward, “Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 19, pp. 7757–7761, 1990. View at: Google Scholar
  14. J R Korenberg and M C Rykowski, “Human genome organization: Alu, lines, and the molecular structure of metaphase chromosome bands,” Cell, vol. 53, no. 3, pp. 391–400, 1988. View at: Google Scholar
  15. R J Baker and H A Wichman, “Retrotransposon Mys is concentrated on the sex chromosomes: implications for copy number containment,” Evolution, vol. 44, no. 8, pp. 2083–2088, 1990. View at: Google Scholar
  16. H A Wichman, R A Van den Bussche, M J Hamilton, and R J Baker, “Transposable elements and the evolution of genome organization in mammals,” Genetica, vol. 86, no. 1–3, pp. 287–293, 1992. View at: Google Scholar
  17. D A Parish, P Vise, H A Wichman, J J Bull, and R J Baker, “Distribution of LINEs and other repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation,” Cytogenetic and Genome Research, vol. 96, no. 1–4, pp. 191–197, 2002. View at: Google Scholar
  18. J A Bailey, L Carrel, A Chakravarti, and E E Eichler, “Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 12, pp. 6634–6639, 2000. View at: Google Scholar
  19. M T Ross, D V Grafham, A J Coffey et al., “The DNA sequence of the human X chromosome,” Nature, vol. 434, no. 7031, pp. 325–337, 2005. View at: Google Scholar
  20. J AM Graves and J M Watson, “Mammalian sex chromosomes: evolution of organization and function,” Chromosoma, vol. 101, no. 2, pp. 63–68, 1991. View at: Google Scholar
  21. B T Lahn and D C Page, “Four evolutionary strata on the human X chromosome,” Science, vol. 286, no. 5441, pp. 964–967, 1999. View at: Google Scholar
  22. X Ke and A Collins, “CpG islands in human X-inactivation,” Annals of Human Genetics, vol. 67, no. 3, pp. 242–249, 2003. View at: Google Scholar
  23. L Carrel and H F Willard, “X-inactivation profile reveals extensive variability in X-linked gene expression in females,” Nature, vol. 434, no. 7031, pp. 400–404, 2005. View at: Google Scholar
  24. A D Riggs, “X chromosome inactivation, differentiation, and DNA methylation revisited, with a tribute to Susumu Ohno,” Cytogenetic and Genome Research, vol. 99, no. 1–4, pp. 17–24, 2002. View at: Google Scholar
  25. M A Goldman, K R Stokes, R L Idzerda et al., “A chicken transferrin gene in transgenic mice escapes X-chromosome inactivation,” Science, vol. 236, no. 4801, pp. 593–595, 1987. View at: Google Scholar
  26. M A Goldman, P S Reeves, C M Wirth et al., “Comparative methylation analysis of murine transgenes that undergo or escape X-chromosome inactivation,” Chromosome Research, vol. 6, no. 5, pp. 397–404, 1998. View at: Google Scholar
  27. R H Waterston, K Lindblad-Toh, E Birney et al., “Initial sequencing and comparative analysis of the mouse genome,” Nature, vol. 420, no. 6915, pp. 520–562, 2002. View at: Google Scholar
  28. K D Tsuchiya, J M Greally, Y Yi, K P Noel, J P Truong, and C M Disteche, “Comparative sequence and X-inactivation analyses of a domain of escape in human Xp11.2 and the conserved segment in mouse,” Genome Research, vol. 14, no. 7, pp. 1275–1284, 2004. View at: Google Scholar
  29. L B Russell and C S Montgomery, “Comparative studies on X-autosome translocations in the mouse. II. Inactivation of autosomal loci, segregation, and mapping of autosomal breakpoints in five T(X;1)'S,” Genetics, vol. 64, no. 2, pp. 281–312, 1970. View at: Google Scholar
  30. B M Cattanach, “Position effect variegation in the mouse,” Genetical Research, vol. 23, no. 3, pp. 291–306, 1974. View at: Google Scholar
  31. S M Duthie, T B Nesterova, E J Formstone et al., “Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis,” Human Molecular Genetics, vol. 8, no. 2, pp. 195–204, 1999. View at: Google Scholar
  32. W M White, H F Willard, D L Van Dyke, and D J Wolff, “The spreading of X inactivation into autosomal material of an X;autosome translocation: evidence for a difference between autosomal and X-chromosomal DNA,” The American journal of Human Genetics, vol. 63, no. 1, pp. 20–28, 1998. View at: Google Scholar
  33. A M Keohane, A L Barlow, J Waters, D Bourn, and B M Turner, “H4 acetylation, XIST RNA and replication timing are coincident and define X;autosome boundaries in two abnormal X chromosomes,” Human Molecular Genetics, vol. 8, no. 2, pp. 377–383, 1999. View at: Google Scholar
  34. A J Sharp, H T Spotswood, D O Robinson, B M Turner, and P A Jacobs, “Molecular and cytogenetic analysis of the spreading of X inactivation in X;autosome translocations,” Human Molecular Genetics, vol. 11, no. 25, pp. 3145–3156, 2002. View at: Google Scholar
  35. L L Hall, C M Clemson, M Byron, K Wydner, and J B Lawrence, “Unbalanced X;autosome translocations provide evidence for sequence specificity in the association of XIST RNA with chromatin,” Human Molecular Genetics, vol. 11, no. 25, pp. 3157–3165, 2002. View at: Google Scholar
  36. L L Hall, M Byron, K Sakai, L Carrel, H F Willard, and J B Lawrence, “An ectopic human XIST gene can induce chromosome inactivation in postdifferentiation human HT-1080 cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 13, pp. 8677–8682, 2002. View at: Google Scholar
  37. J T Lee and R Jaenisch, “Long-range cis effects of ectopic X-inactivation centres on a mouse autosome,” Nature, vol. 386, no. 6622, pp. 275–279, 1997. View at: Google Scholar
  38. 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
  39. K E Latham, “X chromosome imprinting and inactivation in preimplantation mammalian embryos,” Trends in Genetics, vol. 21, no. 2, pp. 120–127, 2005. View at: Google Scholar
  40. K D Huynh and J T Lee, “Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos,” Nature, vol. 426, no. 6968, pp. 857–862, 2003. View at: Google Scholar
  41. R S Hansen, “X inactivation-specific methylation of LINE-1 elements by DNMT3B: implications for the Lyon repeat hypothesis,” Human Molecular Genetics, vol. 12, no. 19, pp. 2559–2567, 2003. View at: Google Scholar
  42. M Steinemann and S Steinemann, “Enigma of Y chromosome degeneration: neo-Y and neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution,” Genetica, vol. 102-103, no. 1, pp. 409–420, 1998. View at: Google Scholar
  43. E Allen, S Horvath, F Tong et al., “High concentrations of long interspersed nuclear element sequence distinguish monoallelically expressed genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 17, pp. 9940–9945, 2003. View at: Google Scholar
  44. J AM Graves, “The origin and function of the mammalian Y chromosome and Y-borne genes—an evolving understanding,” BioEssays, vol. 17, no. 4, pp. 311–320, 1995. View at: Google Scholar
  45. C H Langley, E Montgomery, R Hudson, N Kaplan, and B Charlesworth, “On the role of unequal exchange in the containment of transposable element copy number,” Genetical Research, vol. 52, no. 3, pp. 223–235, 1988. View at: Google Scholar

Copyright © 2006 Mary F. Lyon. 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.

0 Views | 0 Downloads | 0 Citations
 PDF  Download Citation  Citation
 Order printed copiesOrder