Evolutionary Diversity and Developmental Regulation of X-chromosome Inactivation

Overview

Journal Hum Genet

Specialty Genetics

Date 2011 Jun 21

PMID 21687993

Citations 46

Authors

Martin Escamilla-Del-Arenal

Simao Teixeira da Rocha

Edith Heard

Affiliations

Soon will be listed here.

Abstract

X-chromosome inactivation (XCI) results in the transcriptional silencing of one X-chromosome in females to attain gene dosage parity between XX female and XY male mammals. Mammals appear to have developed rather diverse strategies to initiate XCI in early development. In placental mammals XCI depends on the regulatory noncoding RNA X-inactive specific transcript (Xist), which is absent in marsupials and monotremes. Surprisingly, even placental mammals show differences in the initiation of XCI in terms of Xist regulation and the timing to acquire dosage compensation. Despite this, all placental mammals achieve chromosome-wide gene silencing at some point in development, and this is maintained by epigenetic marks such as chromatin modifications and DNA methylation. In this review, we will summarise recent findings concerning the events that occur downstream of Xist RNA coating of the inactive X-chromosome (Xi) to ensure its heterochromatinization and the maintenance of the inactive state in the mouse and highlight similarities and differences between mammals.

Citing Articles

Oncogenes and tumor suppressor genes: functions and roles in cancers.

Dakal T, Dhabhai B, Pant A, Moar K, Chaudhary K, Yadav V MedComm (2020). 2024; 5(6):e582.

PMID: 38827026 PMC: 11141506. DOI: 10.1002/mco2.582.

Validation of a DNA methylation microarray for 285,000 CpG sites in the mouse genome.

Garcia-Prieto C, Alvarez-Errico D, Musulen E, Bueno-Costa A, Vazquez B, Vaquero A Epigenetics. 2022; 17(12):1677-1685.

PMID: 35297293 PMC: 9621044. DOI: 10.1080/15592294.2022.2053816.

The Molecular and Nuclear Dynamics of X-Chromosome Inactivation.

Dossin F, Heard E Cold Spring Harb Perspect Biol. 2021; 14(4).

PMID: 34312245 PMC: 9121902. DOI: 10.1101/cshperspect.a040196.

New Insights into X-Chromosome Reactivation during Reprogramming to Pluripotency.

Panda A, Zylicz J, Pasque V Cells. 2020; 9(12).

PMID: 33348832 PMC: 7766869. DOI: 10.3390/cells9122706.

The function of a heterozygous p53 mutation in a Li-Fraumeni syndrome patient.

Li Y, Li T, Tang Y, Zhan Z, Ding L, Song L PLoS One. 2020; 15(6):e0234262.

PMID: 32516327 PMC: 7282642. DOI: 10.1371/journal.pone.0234262.

References

Savarese F, Flahndorfer K, Jaenisch R, Busslinger M, Wutz A . Hematopoietic precursor cells transiently reestablish permissiveness for X inactivation. Mol Cell Biol. 2006; 26(19):7167-77. PMC: 1592878. DOI: 10.1128/MCB.00810-06. View

Kouzarides T . Chromatin modifications and their function. Cell. 2007; 128(4):693-705. DOI: 10.1016/j.cell.2007.02.005. View

Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S . Chromosome territories--a functional nuclear landscape. Curr Opin Cell Biol. 2006; 18(3):307-16. DOI: 10.1016/j.ceb.2006.04.007. View

Wang J, MAGER J, Chen Y, Schneider E, CROSS J, Nagy A . Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet. 2001; 28(4):371-5. DOI: 10.1038/ng574. View

Keohane A, ONeill L, Belyaev N, Lavender J, Turner B . X-Inactivation and histone H4 acetylation in embryonic stem cells. Dev Biol. 1996; 180(2):618-30. DOI: 10.1006/dbio.1996.0333. View

Yen Z, Meyer I, Karalic S, Brown C . A cross-species comparison of X-chromosome inactivation in Eutheria. Genomics. 2007; 90(4):453-63. DOI: 10.1016/j.ygeno.2007.07.002. View

Mak W, Nesterova T, de Napoles M, Appanah R, Yamanaka S, Otte A . Reactivation of the paternal X chromosome in early mouse embryos. Science. 2004; 303(5658):666-9. DOI: 10.1126/science.1092674. View

Oda H, Okamoto I, Murphy N, Chu J, Price S, Shen M . Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol Cell Biol. 2009; 29(8):2278-95. PMC: 2663305. DOI: 10.1128/MCB.01768-08. View

Navarro P, Pichard S, Ciaudo C, Avner P, Rougeulle C . Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: implications for X-chromosome inactivation. Genes Dev. 2005; 19(12):1474-84. PMC: 1151664. DOI: 10.1101/gad.341105. View

10.

Maenner S, Blaud M, Fouillen L, Savoye A, Marchand V, Dubois A . 2-D structure of the A region of Xist RNA and its implication for PRC2 association. PLoS Biol. 2010; 8(1):e1000276. PMC: 2796953. DOI: 10.1371/journal.pbio.1000276. View

11.

Csankovszki G, Panning B, Bates B, Pehrson J, Jaenisch R . Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat Genet. 1999; 22(4):323-4. DOI: 10.1038/11887. View

12.

Hasegawa Y, Brockdorff N, Kawano S, Tsutui K, Tsutui K, Nakagawa S . The matrix protein hnRNP U is required for chromosomal localization of Xist RNA. Dev Cell. 2010; 19(3):469-76. DOI: 10.1016/j.devcel.2010.08.006. View

13.

Clemson C, McNeil J, Willard H, Lawrence J . XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol. 1996; 132(3):259-75. PMC: 2120729. DOI: 10.1083/jcb.132.3.259. View

14.

Mahadevaiah S, Royo H, VandeBerg J, McCarrey J, Mackay S, Turner J . Key features of the X inactivation process are conserved between marsupials and eutherians. Curr Biol. 2009; 19(17):1478-84. DOI: 10.1016/j.cub.2009.07.041. View

15.

Fang J, Chen T, Chadwick B, Li E, Zhang Y . Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J Biol Chem. 2004; 279(51):52812-5. DOI: 10.1074/jbc.C400493200. View

16.

Ohno S, HAUSCHKA T . Allocycly of the X-chromosome in tumors and normal tissues. Cancer Res. 1960; 20:541-5. View

17.

Changolkar L, Costanzi C, Leu N, Chen D, McLaughlin K, Pehrson J . Developmental changes in histone macroH2A1-mediated gene regulation. Mol Cell Biol. 2007; 27(7):2758-64. PMC: 1899912. DOI: 10.1128/MCB.02334-06. View

18.

Kalantry S, Mills K, Yee D, Otte A, Panning B, Magnuson T . The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation. Nat Cell Biol. 2006; 8(2):195-202. PMC: 1400591. DOI: 10.1038/ncb1351. View

19.

Li G, Margueron R, Ku M, Chambon P, Bernstein B, Reinberg D . Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 2010; 24(4):368-80. PMC: 2816736. DOI: 10.1101/gad.1886410. View

20.

Norris D, Brockdorff N, Rastan S . Methylation status of CpG-rich islands on active and inactive mouse X chromosomes. Mamm Genome. 1991; 1(2):78-83. DOI: 10.1007/BF02443782. View