Increased sex chromosome expression and epigenetic abnormalities in spermatids from male mice with Y chromosome deletions

Journal of Cell Science

Volumn 122, Issue 22, 2009, Pages 4239-4248

  Reynard, Louise N ^a   Turner, James M A ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Chromatin marks; Post meiotic sex chromatin; Sex chromosome; Spermatid

Indexed keywords

HETEROCHROMATIN PROTEIN 1; HISTONE H3; HISTONE H4; TESTIS DETERMINING FACTOR;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME DELETION Y; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HETEROCHROMATIN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SEX CHROMOSOME; SPERMATID; SPERMATOGENESIS; UPREGULATION;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME DELETION; EPIGENESIS, GENETIC; GENES, X-LINKED; GENES, Y-LINKED; HISTONE CODE; HISTONES; MALE; MEIOSIS; MICE; MICE, MUTANT STRAINS; SPERMATIDS; TRANSCRIPTION, GENETIC; UP-REGULATION; Y CHROMOSOME;

MUS;

EID: 70849132322     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.049916     Document Type: Article

References (48)

1. Aravin, A. A., Naumova, N. M., Tulin, A. V., Vagin, V. V., Rozovsky, Y. M. and Gvozdev, V. A. (2001). Double-stranded RNA-mediated silencing of the genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 11, 1017-1027.
2. Baarends, W. M., Hoogerbrugge, J. W., Roest, H. P., Oooms, M., Vreeburg, J., Hoeijmakers, J. H. J. and Grootegoed, J. A. (1999). Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev. Biol. 207, 322-333.
3. Baarends, W. M., Wassenaar, E., van der Laan, R., Hoogerbrugge, J., Sleddens-Linkels, E., Hoeijmakers, J. H., de Boer, P. and Grootegoed, J. A. (2005). Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol. Cell. Biol. 25, 1041-1053.
4. Baarends, W. M., Wassenaar, E., Hoogerbrugge, J. W., Schoenmakers, S., Sun, Z. W. and Grootegoed, J. A. (2007). Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with de-repression of the X chromosome. J. Cell Sci. 120, 1841-1851.
5. Burgoyne, P. S., Mahadevaiah, S. K., Sutcliffe, M. J. and Palmer, S. J. (1992). Fertility in mice requires X-Y pairing and a Y-chromosomal "spermiogenesis" gene mapping to the long arm. Cell 71, 391-398.
6. Burgoyne, P. S., Mahadevaiah, S. K., Perry, J., Palmer, S. J. and Ashworth, A. (1998). The Y* rearrangement in mice: new insights into a perplexing PAR. Cytogenet. Cell Genet. 80, 37-40.
7. Carvalho, A. B., Vaz, S. C. and Klaczko, L. B. (1997). Polymorphism for Y-linked suppressors of sex-ratio in two natural populations of Drosophila mediopunctata. Genetics 146, 891-902.
8. Cattanach, B. M. (1987). Sex-reversed mice and sex determination. Ann. N. Y. Acad. Sci. 513, 27-29.
9. Cattanach, B. M., Pollard, C. E. and Hawkes, S. G. (1971). Sex reversed mice: XX and XO males. Cytogenetics 10, 318-337.
10. Conway, S. J., Mahadevaiah, S. K., Darling, S. M., Capel, B., Rattigan, Á. M. and Burgoyne, P. S. (1994). Y353/B: a candidate multiple-copy spermiogenesis gene on the mouse Y chromosome. Mamm. Genome 5, 203-210.
11. Dubois, V., Van Ginneke, C., De Cock, H., Lambeir, A. M., Van der Veken, P., Augustyns, K., Chen, X., Scharpe, S. and De Meester, I. (2009). Enzyme activity and immunohistochemical localization of dipeptidyl peptidase 8 and 9 in male reproductive tissues. J. Histochem. Cytochem. 57, 531-541.
12. Eicher, E. M., Hale, D. W., Hunt, P. A., Lee, B. K., Tucker, P. K., King, T. R., Eppig, J. T. and Washburn, L. L. (1991). The mouse Y* chromosome involves a complex rearrangement, including interstitial positioning of the pseudoautosomal region. Cytogenet. Cell Genet 57, 221-230.
13. Ellis, P. J. I., Clemente, E. J., Ball, P., Toure, A., Ferguson, L., Turner, J. M. A., Loveland, K. L., Affara, N. A. and Burgoyne, P. S. (2005). Deletions on mouse Yq lead to up-regulation of multiple X- and Y-linked transcripts in spermatids. Hum. Mol. Genet. 14, 2705-2715.
14. Ellis, P. J., Ferguson, L., Clemente, E. J. and Affara, N. A. (2007). Bidirectional transcription of a novel chimeric gene mapping to mouse chromosome Yq. BMC Evol. Biol. 7, 171.
15. Fernandez-Capetillo, O., Mahadevaiah, S. K., Celeste, A., Romanienko, P. J., Camerini-Otero, R. D., Bonner, W. M., Manova, K., Burgoyne, P. and Nussenzweig, A. (2003). H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell 4, 497-508.
16. Fisher, R. A. (1930). The Genetical Theory of Natural Selection (ed. H. Bennett). Oxford: Clarendon Press.
17. Greaves, I. K., Rangasamy, D., Devoy, M., Marshall Graves, J. A. and Tremethick, D. J. (2006). The X and Y chromosomes assemble into H2A.Z, containing facultative heterochromatin, following meiosis. Mol. Cell. Biol. 26, 5394-5405.
18. Hadjantonakis, A. K., Gertsenstein, M., Ikawa, M., Okabe, M. and Nagy, A. (1998). Non-invasive sexing of preimplantation stage mammalian embryos. Nature Genetics 19, 220-222.
19. Hadjantonakis, A.-K., Cox, L. L., Tam, P. P. L. and Nagy, A. (2001). An X-linked GFP transgene reveals unexpected paternal X-chromosome activity in trophoblast giant cells of the mouse placenta. Genesis 29, 133-140.
20. Hamilton, W. D. (1967). Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science 156, 477-488.
21. Hoyer-Fender, S., Costanzi, C. and Pehrson, J. R. (2000). Histone macroH2A1.2 is concentrated in the XY-body by the early pachytene stage of spermatogenesis. Exp. Cell Res. 258, 254-260.
22. Hurst, L. D. (1992). Is Stellate a relict meiotic driver? Genetics 130, 229-230.
23. Khalil, A. M., Boyar, F. Z. and Driscoll, D. J. (2004). Dynamic histone modifications mark sex chromosome inactivation and reactivation during mammalian spermatogenesis. Proc. Natl. Acad. Sci. USA 101, 16583-16587.
24. Khalil, A. M. and Driscoll, D. J. (2006). Histone H3 lysine 4 dimethylation is enriched on the inactive sex chromosomes in male meiosis but absent on the inactive X in female somatic cells. Cytogenet. Genome Res. 112, 11-15.
25. Khil, P. P., Smirnova, N. A., Romanienko, P. J. and Camerini-Otero, R. D. (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.
26. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K. and Jenuwein, T. (2001). Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410, 116-120.
27. Lercher, M. J., Urrutia, A. O. and Hurst, L. D. (2003). Evidence that the human X chromosome is enriched for male-specific but not female-specific genes. Mol. Biol. Evol. 20, 1113-1116.
28. Mahadevaiah, S. K., Turner, J. M. A., Baudat, F., Rogakou, E. P., de Boer, P., Blanco-Rodriguez, J., Jasin, M., Keeney, S., Bonner, W. M. and Burgoyne, P. S. (2001). Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27, 271-276.
29. McKee, B. D. and Handel, M. A. (1993). Sex chromosomes, recombination, and chromatin conformation. Chromosoma (Berlin) 102, 71-80.
30. Montchamp-Moreau, C. (2006). Sex-ratio meiotic drive in Drosophila simulans: cellular mechanism, candidate genes and evolution. Biochem. Soc. Trans. 34, 562-565.
31. Mueller, J. L., Mahadevaiah, S. K., Park, P. J., Warburton, P. E., Page, D. C. and Turner, J. M. (2008). The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat. Genet. 40, 794-799.
32. Namekawa, S. H., Park, P. J., Zhang, L. F., Shima, J. E., McCarrey, J. R., Griswold, M. D. and Lee, J. T. (2006). Postmeiotic sex chromatin in the male germline of mice. Curr. Biol. 16, 660-667.
33. Reynard, L. N., Turner, J. M., Cocquet, J., Mahadevaiah, S. K., Toure, A., Hoog, C. and Burgoyne, P. S. (2007). Expression analysis of the mouse multi-copy X-linked gene Xlr-related, meiosis-regulated (Xmr), reveals that Xmr encodes a spermatid-expressed cytoplasmic protein, SLX/XMR. Biol. Reprod. 77, 329-335.
34. Reynard, L. N., Cocquet, J. and Burgoyne, P. S. (2009). The mouse multi-copy gene Sycp3-like Y-linked (Sly) encodes an abundant spermatid protein that interacts with a histone acetyltransferase and an acrosomal protein. Biol. Reprod. 81, 250-257.
35. Saifi, G. M. and Chandra, H. S. (1999). An apparent excess of sex- and reproduction-related genes on the human X chromosome. Proc. Biol. Sci. 266, 203-209.
36. Solari, A. J. (1974). The behaviour of the XY pair in mammals. Int. Rev. Cytol. 38, 273-317.
37. Tao, Y., Araripe, L., Kingan, S. B., Ke, Y., Xiao, H. and Hartl, D. L. (2007). A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS Biol. 5, e293.
38. Touré, A., Grigoriev, V., Mahadevaiah, S. K., Rattigan, A., Ojarikre, O. A. and Burgoyne, P. S. (2004a). A protein encoded by a member of the multicopy Ssty gene family located on the long arm of the mouse Y chromosome is expressed during sperm development. Genomics 83, 140-147.
39. Touré, A., Szot, M., Mahadevaiah, S. K., Rattigan, A., Ojarikre, O. A. and Burgoyne, P. S. (2004b). A new deletion of the mouse Y chromosome long arm associated with loss of Ssty expression, abnormal sperm development and sterility. Genetics 166, 901-912.
40. Touré, A., Clemente, E. J., Ellis, P., Mahadevaiah, S. K., Ojarikre, O. A., Ball, P. A. F., Reynard, L., Loveland, K. L., Burgoyne, P. S. and Affara, N. A. (2005). Identification of novel Y chromosome encoded transcripts by testis transcriptome analysis of mice with deletions of the Y chromosome long arm. Genome Biol. 6, R102.
41. Turner, J. M. (2007). Meiotic sex chromosome inactivation. Development 134, 1823-1831.
42. Turner, J. M., Aprelikova, O., Xu, X., Wang, R., Kim, S., Chandramouli, G. V., Barrett, J. C., Burgoyne, P. S. and Deng, C. X. (2004). BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr. Biol. 14, 2135-2142.
43. Turner, J. M., Mahadevaiah, S. K., Ellis, P. J., Mitchell, M. J. and Burgoyne, P. S. (2006). Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev. Cell 10, 521-529.
44. Turner, J. M., Mahadevaiah, S. K., Fernandez-Capetillo, O., Nussenzweig, A., Xu, X., Deng, C. X. and Burgoyne, P. S. (2005). Silencing of unsynapsed meiotic chromosomes in the mouse. Nat. Genet. 37, 41-47.
45. van der Heijden, G. W., Derijck, A. A., Posfai, E., Giele, M., Pelczar, P., Ramos, L., Wansink, D. G., van der Vlag, J., Peters, A. H. and de Boer, P. (2007). Chromosome-wide nucleosome replacement and H3.3 incorporation during mammalian meiotic sex chromosome inactivation. Nat. Genet. 39, 251-258.
46. Wang, P. J., McCarrey, J. R., Yang, F. and Page, D. C. (2001). An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27, 422-426.
47. Yamauchi, Y., Riel, J. M., Wong, S. J., Ojarikre, O. A., Burgoyne, P. S. and Ward, M. A. (2009). Live offspring from mice lacking the Y chromosome long arm gene complement. Biol. Reprod. 81, 353-361.
48. Zofall, M. and Grewal, S. (2006). Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol. Cell. 22, 681-692.