Silencing of X-Linked MicroRNAs by Meiotic Sex Chromosome Inactivation

English version České info

During male germ cell formation, the X and the Y chromosomes are inactivated. This process is conserved and it is essential for germ cell generation. It is believed that X/Y silencing affects all protein-coding genes, but the status of miRNAs and other non-coding genes needs further investigation. MicroRNAs from the X-chromosome (X-miRNAs) have been reported as potential silencing escapers, and they have been proposed to play a role in the inactivation mechanism itself. By looking at the individual cell level, we show unambiguously that X-miRNAs are subject to X/Y silencing, a finding that contradicts the current literature. Moreover, we generated mouse mutants in which we forced expression of X-miRNAs during X/Y silencing, and this lead to germ cell death. We propose that X/Y silencing can influence transcription of essential germ cell genes by regulating X-repressors.

Vyšlo v časopise: Silencing of X-Linked MicroRNAs by Meiotic Sex Chromosome Inactivation. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005461
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005461

Souhrn

Zdroje

1. McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102: 71–80. 8432196

2. Inagaki A, Schoenmakers S, Baarends WM (2010) DNA double strand break repair, chromosome synapsis and transcriptional silencing in meiosis. Epigenetics 5: 255–266. 20364103

3. Turner JM (2007) Meiotic sex chromosome inactivation. Development 134: 1823–1831. 17329371

4. Yan W, McCarrey JR (2009) Sex chromosome inactivation in the male. Epigenetics 4: 452–456. 19838052

5. Ichijima Y, Sin HS, Namekawa SH (2012) Sex chromosome inactivation in germ cells: emerging roles of DNA damage response pathways. Cell Mol Life Sci.

6. Solari AJ (1964) The Morphology and Ultrastructure of the Sex Vesicle in the Mouse. Exp Cell Res 36: 160–168. 14222737

7. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, et al. (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37: 41–47. 15580272

8. Baarends WM, Wassenaar E, van der Laan R, Hoogerbrugge J, Sleddens-Linkels E, et al. (2005) Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol 25: 1041–1053. 15657431

9. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, et al. (2006) Postmeiotic sex chromatin in the male germline of mice. Curr Biol 16: 660–667. 16581510

10. Sin HS, Ichijima Y, Koh E, Namiki M, Namekawa SH (2012) Human postmeiotic sex chromatin and its impact on sex chromosome evolution. Genome Res 22: 827–836. doi: 10.1101/gr.135046.111 22375025

11. Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS (2006) Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 10: 521–529. 16580996

12. Greaves IK, Rangasamy D, Devoy M, Marshall Graves JA, Tremethick DJ (2006) The X and Y chromosomes assemble into H2A.Z-containing [corrected] facultative heterochromatin [corrected] following meiosis. Mol Cell Biol 26: 5394–5405. 16809775

13. Lu LY, Yu X (2015) Double-strand break repair on sex chromosomes: challenges during male meiotic prophase. Cell Cycle 14: 516–525. doi: 10.1080/15384101.2014.998070 25565522

14. Royo H, Polikiewicz G, Mahadevaiah SK, Prosser H, Mitchell M, et al. (2010) Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr Biol 20: 2117–2123. doi: 10.1016/j.cub.2010.11.010 21093264

15. Barchi M, Mahadevaiah S, Di Giacomo M, Baudat F, de Rooij DG, et al. (2005) Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol Cell Biol 25: 7203–7215. 16055729

16. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, et al. (2008) The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40: 794–799. doi: 10.1038/ng.126 18454149

17. Turner JM, Aprelikova O, Xu X, Wang R, Kim S, et al. (2004) BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14: 2135–2142. 15589157

18. Xu X, Aprelikova O, Moens P, Deng CX, Furth PA (2003) Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice. Development 130: 2001–2012. 12642502

19. Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD (2004) The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36: 642–646. 15156144

20. Margolin G, Khil PP, Kim J, Bellani MA, Camerini-Otero RD (2014) Integrated transcriptome analysis of mouse spermatogenesis. BMC Genomics 15: 39. doi: 10.1186/1471-2164-15-39 24438502

21. Sin HS, Barski A, Zhang F, Kartashov AV, Nussenzweig A, et al. (2012) RNF8 regulates active epigenetic modifications and escape gene activation from inactive sex chromosomes in post-meiotic spermatids. Genes Dev 26: 2737–2748. doi: 10.1101/gad.202713.112 23249736

22. Ro S, Park C, Sanders KM, McCarrey JR, Yan W (2007) Cloning and expression profiling of testis-expressed microRNAs. Dev Biol 311: 592–602. 17936267

23. Meunier J, Lemoine F, Soumillon M, Liechti A, Weier M, et al. (2013) Birth and expression evolution of mammalian microRNA genes. Genome Res 23: 34–45. doi: 10.1101/gr.140269.112 23034410

24. Guo X, Su B, Zhou Z, Sha J (2009) Rapid evolution of mammalian X-linked testis microRNAs. BMC Genomics 10: 97. doi: 10.1186/1471-2164-10-97 19257908

25. Song R, Ro S, Michaels JD, Park C, McCarrey JR, et al. (2009) Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nat Genet 41: 488–493. doi: 10.1038/ng.338 19305411

26. Buchold GM, Coarfa C, Kim J, Milosavljevic A, Gunaratne PH, et al. (2010) Analysis of microRNA expression in the prepubertal testis. PLoS One 5: e15317. doi: 10.1371/journal.pone.0015317 21206922

27. Modzelewski AJ, Holmes RJ, Hilz S, Grimson A, Cohen PE (2012) AGO4 regulates entry into meiosis and influences silencing of sex chromosomes in the male mouse germline. Dev Cell 23: 251–264. doi: 10.1016/j.devcel.2012.07.003 22863743

28. Augui S, Nora EP, Heard E (2011) Regulation of X-chromosome inactivation by the X-inactivation centre. Nat Rev Genet 12: 429–442. doi: 10.1038/nrg2987 21587299

29. Sabin LR, Delas MJ, Hannon GJ (2013) Dogma derailed: the many influences of RNA on the genome. Mol Cell 49: 783–794. doi: 10.1016/j.molcel.2013.02.010 23473599

30. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, et al. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27: 271–276. 11242108

31. Ruiz-Lafuente N, Alcaraz-Garcia MJ, Sebastian-Ruiz S, Garcia-Serna AM, Gomez-Espuch J, et al. (2015) IL-4 Up-Regulates MiR-21 and the MiRNAs Hosted in the CLCN5 Gene in Chronic Lymphocytic Leukemia. PLoS One 10: e0124936. doi: 10.1371/journal.pone.0124936 25909590

32. Chureau C, Chantalat S, Romito A, Galvani A, Duret L, et al. (2011) Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region. Hum Mol Genet 20: 705–718. doi: 10.1093/hmg/ddq516 21118898

33. Bellani MA, Romanienko PJ, Cairatti DA, Camerini-Otero RD (2005) SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. J Cell Sci 118: 3233–3245. 15998665

34. Okamoto I, Arnaud D, Le Baccon P, Otte AP, Disteche CM, et al. (2005) Evidence for de novo imprinted X-chromosome inactivation independent of meiotic inactivation in mice. Nature 438: 369–373. 16227973

35. Rissland OS, Hong SJ, Bartel DP (2011) MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell-cycle changes. Mol Cell 43: 993–1004. doi: 10.1016/j.molcel.2011.08.021 21925387

36. Krol J, Busskamp V, Markiewicz I, Stadler MB, Ribi S, et al. (2010) Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141: 618–631. doi: 10.1016/j.cell.2010.03.039 20478254

37. Gantier MP, McCoy CE, Rusinova I, Saulep D, Wang D, et al. (2011) Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res 39: 5692–5703. doi: 10.1093/nar/gkr148 21447562

38. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6: 989–998. 11106739

39. Gaidatzis D, Lerch A, Hahne F, Stadler MB (2015) QuasR: quantification and annotation of short reads in R. Bioinformatics 31: 1130–1132. doi: 10.1093/bioinformatics/btu781 25417205

40. Mahadevaiah SK, Costa Y, Turner JM (2009) Using RNA FISH to study gene expression during mammalian meiosis. Methods Mol Biol 558: 433–444. doi: 10.1007/978-1-60761-103-5_25 19685339

41. Hammoud SS, Low DH, Yi C, Carrell DT, Guccione E, et al. (2014) Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell 15: 239–253. doi: 10.1016/j.stem.2014.04.006 24835570