Genomic and epigenomic approaches to the study of X chromosome inactivation

Current Opinion in Genetics and Development

Volumn 16, Issue 3, 2006, Pages 240-245

  Valley, Cory M ^a   Willard, Huntington F ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIVISION; CIS ISOMER; DNA MICROARRAY; EMBRYO DEVELOPMENT; EPIGENETICS; GENE CLUSTER; GENE CONTROL; GENE DOSAGE; GENE EXPRESSION; GENE INACTIVATION; GENE SEQUENCE; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOMICS; HETEROCHROMATIN; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; TRANS ISOMER; X CHROMOSOME INACTIVATION; X CHROMOSOME LINKAGE; ANIMAL; GENETIC EPIGENESIS; GENETICS; X CHROMOSOME;

MAMMALIA;

ANIMALS; EPIGENESIS, GENETIC; GENOMICS; HETEROCHROMATIN; HUMANS; X CHROMOSOME; X CHROMOSOME INACTIVATION;

EID: 33746521889     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2006.04.008     Document Type: Review

References (53)

1. Verona R.I., Mann M.R., and Bartolomei M.S. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu Rev Cell Dev Biol 19 (2003) 237-259
2. Liang H.E., Hsu L.Y., Cado D., and Schlissel M.S. Variegated transcriptional activation of the immunoglobulin kappa locus in pre-B cells contributes to the allelic exclusion of light-chain expression. Cell 118 (2004) 19-29
3. Mostoslavsky R., Singh N., Tenzen T., Goldmit M., Gabay C., Elizur S., Qi P., Reubinoff B.E., Chess A., Cedar H., et al. Asynchronous replication and allelic exclusion in the immune system. Nature 414 (2001) 221-225
4. Chess A., Simon I., Cedar H., and Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell 78 (1994) 823-834
5. Jung D., and Alt F.W. Unraveling V(D)J recombination; insights into gene regulation. Cell 116 (2004) 299-311
6. Shykind B.M., Rohani S.C., O'Donnell S., Nemes A., Mendelsohn M., Sun Y., Axel R., and Barnea G. Gene switching and the stability of odorant receptor gene choice. Cell 117 (2004) 801-815
7. Heard E. Delving into the diversity of facultative heterochromatin: the epigenetics of the inactive X chromosome. Curr Opin Genet Dev 15 (2005) 482-489
8. Morley M., Molony C.M., Weber T.M., Devlin J.L., Ewens K.G., Spielman R.S., and Cheung V.G. Genetic analysis of genome-wide variation in human gene expression. Nature 430 (2004) 743-747
9. Yan H., Yuan W., Velculescu V.E., Vogelstein B., and Kinzler K.W. Allelic variation in human gene expression. Science 297 (2002) 1143
10. Lyon M.F. Gene action in the X-chromosome of the mouse (Mus musculus L.). Naturwissenschaften 190 (1961) 372-373
11. Chow J.C., Yen Z., Ziesche S.M., and Brown C.J. Silencing of the mammalian X chromosome. Annu Rev Genomics Hum Genet 6 (2005) 69-92
12. Heard E. Recent advances in X chromosome inactivation. Curr Opin Genet Dev 14 (2004) 155-164
13. Barr M.L., and Bertram E.G. A morphological distinction between neurones of the male and female and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis. Nature 163 (1949) 676-677
14. Chadwick B.P., and Willard H.F. Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. Semin Cell Dev Biol 14 (2003) 359-367
15. Chadwick B.P., and Willard H.F. Multiple spatially distinct types of facultative heterochromatin on the human inactive X chromosome. Proc Natl Acad Sci USA 101 (2004) 17450-17455. This study used immunohistochemistry to demonstrate the existence of two spatially different types of heterochromatin on the human Xi. The composition of each of these types correlates with the timing of DNA replication. One type is similar to heterochromatin in other organisms, whereas the other has features that appear to be unique to X inactivation. The study adds a previously unsuspected degree of epigenetic complexity to X inactivation.
16. Duthie S.M., Nesterova T.B., Formstone E.J., Keohane A.M., Turner B.M., Zakian S.M., and Brockdorff N. Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum Mol Genet 8 (1999) 195-204
17. Heard E., Rougeulle C., Arnaud D., Avner P., Allis C.D., and Spector D.L. Methylation of histone H3 at Lys-9 is an early mark on the X chromosome during X inactivation. Cell 107 (2001) 727-738
18. Rougeulle C., Chaumeil J., Sarma K., Allis C.D., Reinberg D., Avner P., and Heard E. Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24 (2004) 5475-5484
19. Lachner M., Sengupta R., Schotta G., and Jenuwein T. Trilogies of histone lysine methylation as epigenetic landmarks of the eukaryotic genome. Cold Spring Harb Symp Quant Biol 69 (2004) 209-218
20. Dhillon N., and Kamakaka R.T. Breaking through to the other side: silencers and barriers. Curr Opin Genet Dev 12 (2002) 188-192
21. Carrel L., and Willard H.F. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434 (2005) 400-404. In this report, it is shown that 15% of human X-linked genes escape inactivation at least to some degree, and that an additional 10% show variable patterns of expression among different females. This suggests a previously unsuspected degree of expression heterogeneity among females in the population.
22. Ross M.T., Grafham D.V., Coffey A.J., Scherer S., McLay K., Muzny D., Platzer M., Howell G.R., Burrows C., Bird C.P., et al. The DNA sequence of the human X chromosome. Nature 434 (2005) 325-337. This landmark report describes and analyzes the complete sequence of the human X chromosome. In addition to its significance in contributing to studies of X-linked disease, the availability of the sequence will enable computational analysis of the possible role of X chromosome sequence features in determining X inactivation status.
23. Kohn M., Kehrer-Sawatzki H., Vogel W., Graves J.A., and Hameister H. Wide genome comparisons reveal the origins of the human X chromosome. Trends Genet 20 (2004) 598-603. Using comparative sequence data from the chicken, pufferfish and zebrafish genomes, the authors provide an in-depth view of the evolutionary history of the mammalian X chromosome.
24. Lahn B.T., and Page D.C. Four evolutionary strata on the human X chromosome. Science 286 (1999) 964-967
25. Sandstedt S.A., and Tucker P.K. Evolutionary strata on the mouse X chromosome correspond to strata on the human X chromosome. Genome Res 14 (2004) 267-272
26. Marshall Graves JA, Koina E, Sankovic N: How the gene content of the human sex chromosomes evolved. Curr Opin Genet Dev 2006. 16: in press.
27. Ross MT, Bentley DR, Tyler-Smith C: The sequences of the human sex chromosomes. Curr Opin Genet Dev 2006. 16: in press.
28. Filippova G.N., Cheng M.K., Moore J.M., Truong J.P., Hu Y.J., Nguyen D.K., Tsuchiya K.D., and Disteche C.M. Boundaries between chromosomal domains of X inactivation and escape bind CTCF and lack CpG methylation during early development. Dev Cell 8 (2005) 31-42. This study provides insights into the nature of genomic elements that might serve as boundaries between chromosomal domains containing genes that are subject to or escape from inactivation. The existence of binding sites for the CTCF transcription factor at the 5′ end of three genes that escape inactivation suggests that they might serve as a barrier to the spread of heterochromatin.
29. Sudbrak R., Wieczorek G., Nuber U.A., Mann W., Kirchner R., Erdogan F., Brown C.J., Wohrle D., Sterk P., Kalscheuer V.M., et al. X chromosome-specific cDNA arrays: identification of genes that escape from X-inactivation and other applications. Hum Mol Genet 10 (2001) 77-83
30. Craig I.W., Mill J., Craig G.M., Loat C., and Schalkwyk L.C. Application of microarrays to the analysis of the inactivation status of human X-linked genes expressed in lymphocytes. Eur J Hum Genet 12 (2004) 639-646
31. Skuse D.H. X-linked genes and mental functioning. Hum Mol Genet 14 (2005) R27-R32
32. Xu J., Burgoyne P.S., and Arnold A.P. Sex differences in sex chromosome gene expression in mouse brain. Hum Mol Genet 11 (2002) 1409-1419
33. Carruth L.L., Reisert I., and Arnold A.P. Sex chromosome genes directly affect brain sexual differentiation. Nat Neurosci 5 (2002) 933-934
34. Raefski A.S., and O'Neill M.J. Identification of a cluster of X-linked imprinted genes in mice. Nat Genet 37 (2005) 620-624
35. Davies W., Isles A., Smith R., Karunadasa D., Burrmann D., Humby T., Ojarikre O., Biggin C., Skuse D., Burgoyne P., and Wilkinson L. Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nat Genet 37 (2005) 625-629
36. Nguyen D.K., and Disteche C.M. Dosage compensation of the active X chromosome in mammals. Nat Genet 38 (2006) 47-53. Using gene expression microarrays, the authors test the hypothesis that a distinct dosage compensation mechanism exists to upregulate gene expression on the Xa to equalize effective gene dosage with autosomes. These findings extend and unify the concept of balanced gene-dosage for all genes in the genome as a requirement for normal embryogenesis.
37. Lucchesi J.C., Kelly W.G., and Panning B. Chromatin remodeling in dosage compensation. Annu Rev Genet 39 (2005) 615-651
38. Lyon M.F. X-chromosome inactivation: a repeat hypothesis. Cytogenet Cell Genet 80 (1998) 133-137
39. Gartler S.M., and Riggs A.D. Mammalian X-chromosome inactivation. Annu Rev Genet 17 (1983) 155-190
40. Bailey J.A., Carrel L., Chakravarti A., and Eichler E.E. Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci USA 97 (2000) 6634-6639
41. Allen E., Horvath S., Tong F., Kraft P., Spiteri E., Riggs A.D., and Marahrens Y. High concentrations of long interspersed nuclear element sequence distinguish monoallelically expressed genes. Proc Natl Acad Sci USA 100 (2003) 9940-9945
42. Tsuchiya K.D., Greally J.M., Yi Y., Noel K.P., Truong J.P., and Disteche C.M. Comparative sequence and X-inactivation analyses of a domain of escape in human Xp11.2 and the conserved segment in mouse. Genome Res 14 (2004) 1275-1284
43. Harsha H.C., Suresh S., Amanchy R., Deshpande N., Shanker K., Yatish A.J., Muthusamy B., Vrushabendra B.M., Rashmi B.P., Chandrika K.N., et al. A manually curated functional annotation of the human X chromosome. Nat Genet 37 (2005) 331-332
44. Luedi P.P., Hartemink A.J., and Jirtle R.L. Genome-wide prediction of imprinted murine genes. Genome Res 15 (2005) 875-884. This study uses computational and statistical methods to search for sequence features that can identify imprinted genes. The authors find that the number, type and orientation of various repeated elements flanking a gene are important for predicting whether the gene is imprinted. This provides a model for similar studies of genes that are subject to or escape from X inactivation.
45. Schubeler D., MacAlpine D.M., Scalzo D., Wirbelauer C., Kooperberg C., van Leeuwen F., Gottschling D.E., O'Neill L.P., Turner B.M., Delrow J., et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18 (2004) 1263-1271
46. Bernstein B.E., Humphrey E.L., Erlich R.L., Schneider R., Bouman P., Liu J.S., Kouzarides T., and Schreiber S.L. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci USA 99 (2002) 8695-8700
47. Jia S., Kobayashi R., and Grewal S.I. Ubiquitin ligase component Cul4 associates with Clr4 histone methyltransferase to assemble heterochromatin. Nat Cell Biol 7 (2005) 1007-1013
48. Cam H.P., Sugiyama T., Chen E.S., Chen X., FitzGerald P.C., and Grewal S.I. Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37 (2005) 809-819
49. Mito Y., Henikoff J.G., and Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37 (2005) 1090-1097
50. Speicher M.R., and Carter N. The new cytogenetics, blurring the boundaries with molecular biology. Nat Rev Genet 6 (2005) 782-792
51. Rougeulle C., Navarro P., and Avner P. Promoter-restricted H3 Lys 4 di-methylation is an epigenetic mark for monoallelic expression. Hum Mol Genet 12 (2003) 3343-3348
52. Gilbert S.L., and Sharp P.A. Promoter-specific hypoacetylation of X-inactivated genes. Proc Natl Acad Sci USA 96 (1999) 13825-13830
53. Choo J.H., Kim J.D., Chung J.H., Stubbs L., and Kim J. Allele-specific deposition of macroH2A1 in imprinting control regions. Hum Mol Genet 15 (2006) 717-724