Mouse Y-Linked and Are Expressed during the Male-Specific Interphase between Meiosis I and Meiosis II and Promote the 2 Meiotic Division

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The mouse Y chromosome genes Zfy1 and Zfy2 were first identified in the late 1980s during the search for the gene on the Y that triggers male development; they encode proteins that regulate the expression of other genes to which they bind via a ‘zinc finger’ domain. We have now discovered that these genes play important roles during spermatogenesis. Zfy2 proved to be essential for the efficient operation of a ‘checkpoint’ during the first meiotic division that identifies and kills cells that would otherwise produce sperm with an unbalanced chromosome set. Female meiosis, which does not have an equivalent checkpoint, generates a significant proportion of eggs with an unbalanced chromosome set. In the present study we show that Zfy2 also has a major role in ensuring that the second meiotic division occurs, with Zfy1 and a related gene, Zfx, on the X chromosome providing some support. In order to fulfil this function all three genes are expressed in the ‘interphase’ stage between the two divisions. In female meiosis there is no interphase stage between the two meiotic divisions but in this case essential functions during the divisions are supported by stored RNAs, so an interphase is not needed.

Vyšlo v časopise: Mouse Y-Linked and Are Expressed during the Male-Specific Interphase between Meiosis I and Meiosis II and Promote the 2 Meiotic Division. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004444
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004444

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Zdroje

1. BurgoynePS, LevyER, McLarenA (1986) Spermatogenic failure in male mice lacking H-Y antigen. Nature 320: 170–172.

2. TiepoloL, ZuffardiO (1976) Localization of factors controlling spermatogenesis in the nonfluorescent portion of the human Y chromosome long arm. Human Genetics 34: 119–124.

3. PageDC, MosherR, SimpsonEM, FisherEMC, MardonG, et al. (1987) The sex-determining region of the human Y chromosome encodes a finger protein. Cell 51: 1091–1104.

4. MardonG, MosherR, DistecheCM, NishiokaY, McLarenA, et al. (1989) Duplication, deletion, and polymorphism in the sex-determining region of the mouse Y chromosome. Science 243: 78–80.

5. MardonG, PageDC (1989) The sex-determining region of the mouse Y chromosome encodes a protein with a highly acidic domain and 13 zinc fingers. Cell 56: 765–770.

6. MazeyratS, SautN, SargentCA, GrimmondS, LongepiedG, et al. (1998) The mouse Y chromosome interval necessary for spermatogonial proliferation is gene dense with syntenic homology to the human AZFa region. Hum Mol Genet 7: 1713–1724.

7. DecarpentrieF, VernetN, MahadevaiahSK, LongepiedG, StreichembergerE, et al. (2012) Human and mouse ZFY genes produce a conserved testis-specific transcript encoding a zinc finger protein with a short acidic domain and modified transactivation potential. Hum Mol Genet 21: 2631–2645.

8. MazeyratS, SautN, GrigorievV, MahadevaiahSK, OjarikreOA, et al. (2001) A Y-encoded subunit of the translation initiation factor Eif2 is essential for mouse spermatogenesis. Nat Genet 29: 49–53.

9. KotMC, HandelMA (1990) Spermatogenesis in XO,Sxr mice: role of the Y chromosome. J Exp Zool 256: 92–105.

10. SutcliffeMJ, DarlingSM, BurgoynePS (1991) Spermatogenesis in XY, XYSxra and XOSxra mice: a quantitative analysis of spermatogenesis throughout puberty. Mol Reprod Dev 30: 81–89.

11. VernetN, MahadevaiahSK, OjarikreOA, LongepiedG, ProsserHM, et al. (2011) The Y-encoded gene Zfy2 acts to remove cells with unpaired chromosomes at the first meiotic metaphase in male mice. Curr Biol 21: 787–793.

12. BurgoynePS, MahadevaiahSK, TurnerJM (2009) The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10: 207–216.

13. SimpsonEM, PageDC (1991) An interstitial deletion in mouse Y chromosomal DNA created a transcribed Zfy fusion gene. Genomics 11: 601–608.

14. VernetN, MahadevaiahSK, EllisPJ, de RooijDG, BurgoynePS (2012) Spermatid development in XO male mice with varying Y chromosome short arm gene content: evidence for a Y gene controlling the initiation of sperm morphogenesis. Reproduction 144: 433–445.

15. EicherEM, HaleDW, HuntPA, LeeBK, TuckerPK, et al. (1991) The mouse Y* chromosome involves a complex rearrangement, including interstitial positioning of the pseudoautosomal region. Cytogenet Cell Genet 57: 221–230.

16. HaleDW, HuntPA, TuckerPK, EicherEM (1991) Synapsis and obligate recombination between the sex chromosomes of male laboratory mice carrying the Y* rearrangement. Cytogenetics and Cell Genetics 57: 231–239.

17. BurgoynePS, EvansEP (2000) A high frequency of XO offspring from X(Paf)Y* male mice: evidence that the Paf mutation involves an inversion spanning the X PAR boundary. Cytogenet Cell Genet 91: 57–61.

18. BurgoynePS, MahadevaiahSK, PerryJ, PalmerSJ, AshworthA (1998) The Y* rearrangement in mice: new insights into a perplexing PAR. Cytogenet Cell Genet 80: 37–40.

19. BurgoynePS, MahadevaiahSK, SutcliffeMJ, PalmerSJ (1992) Fertility in mice requires X-Y pairing and a Y-chromosomal “spermiogenesis” gene mapping to the long arm. Cell 71: 391–398.

20. Alfoldi JE (2008) Sequence of the mouse Y chromosome [Thesis (Ph. D.)]. Massachusetts Institute of Technology

21. FergusonL, EllisPJ, AffaraNA (2009) Two novel mouse genes mapped to chromosome Yp are expressed specifically in spermatids. Mamm Genome 20: 193–206 doi: 10.1007/s00335-009-9175-8

22. LeeJ, HongJ, KimE, KimK, KimSW, et al. (2004) Developmental stage-specific expression of Rbm suggests its involvement in early phases of spermatogenesis. Mol Hum Reprod 10: 259–264.

23. CapelB, SwainA, NicolisS, HackerA, WalterM, et al. (1993) Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73: 1019–1030.

24. DolciS, GrimaldiP, GeremiaR, PesceM, RossiP (1997) Identification of a promoter region generating Sry circular transcripts both in germ cells from male adult mice and in male mouse embryonal gonads. Biol Reprod 57: 1128–1135.

25. TurnerJM (2007) Meiotic sex chromosome inactivation. Development 134: 1823–1831.

26. RoyoH, PolikiewiczG, MahadevaiahSK, ProsserH, MitchellM, et al. (2010) Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr Biol 20: 2117–2123.

27. HansenMA, NielsenJE, TanakaM, AlmstrupK, SkakkebaekNE, et al. (2006) Identification and expression profiling of 10 novel spermatid expressed CYPT genes. Mol Reprod Dev 73: 568–579.

28. NagamineCM, ChanK, HakeLE, LauYF (1990) The two candidate testis-determining Y genes (Zfy-1 and Zfy-2) are differentially expressed in fetal and adult mouse tissues. Genes Dev 4: 63–74.

29. NagamineCM, ChanKM, KozakCA, LauYF (1989) Chromosome mapping and expression of a putative testis-determining gene in mouse. Science 243: 80–83.

30. MardonG, LuohSW, SimpsonEM, GillG, BrownLG, et al. (1990) Mouse Zfx protein is similar to Zfy-2: each contains an acidic activating domain and 13 zinc fingers. Mol Cell Biol 10: 681–688.

31. AshworthA, SkeneB, SwiftS, Lovell-BadgeR (1990) Zfa is an expressed retroposon derived from an alternative transcript of the Zfx gene. Embo J 9: 1529–1534.

32. McCarreyJR, DilworthDD, SharpRM (1992) Semiquantitative analysis of X-linked gene expression during spermatogenesis in the mouse: ethidium bromide staining of RT-PCR products. Genetic Analysis - Techniques and Applications 9: 117–123.

33. LuohSW, PageDC (1994) The structure of the Zfx gene on the mouse X chromosome. Genomics 19: 310–319.

34. MitchellM, SimonD, AffaraN, Ferguson-SmithM, AvnerP, et al. (1989) Localization of murine X and autosomal sequences homologous to the human Y located testis-determining region. Genetics 121: 803–809.

35. EricksonRP, ZwingmanT, AoA (1993) Gene expression, X-inactivation, and methylation during spermatogenesis: the case of Zfa, Zfx, and Zfy in mice. Molecular Reproduction and Development 35: 114–120.

36. HuntP, LeMaireR, EmburyP, SheeanL, MrozK (1995) Analysis of chromosome behavior in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum Mol Genet 4: 2007–2012.

37. NagaokaSI, HodgesCA, AlbertiniDF, HuntPA (2011) Oocyte-Specific Differences in Cell-Cycle Control Create an Innate Susceptibility to Meiotic Errors. Curr Biol 21: 651–7 doi: 10.1016/j.cub.2011.03.003

38. GuiL, HomerH (2012) Spindle assembly checkpoint signalling is uncoupled from chromosomal position in mouse oocytes. Development 139: 1941–1946.

39. KolanoA, BrunetS, SilkAD, ClevelandDW, VerlhacMH (2012) Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc Natl Acad Sci U S A 109: E1858–1867.

40. LaneSI, YunY, JonesKT (2012) Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development 139: 1947–1955.

41. SebestovaJ, DanylevskaA, NovakovaL, KubelkaM, AngerM (2012) Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle 11: 3011–3018.

42. BurgoynePS, MahadevaiahSK, TurnerJM (2007) The management of DNA double-strand breaks in mitotic G(2), and in mammalian meiosis viewed from a mitotic G(2) perspective. Bioessays 29: 974–986.

43. CocquetJ, EllisPJ, MahadevaiahSK, AffaraNA, VaimanD, et al. (2012) A genetic basis for a postmeiotic x versus y chromosome intragenomic conflict in the mouse. PLoS Genet 8: e1002900.

44. CocquetJ, EllisPJ, YamauchiY, MahadevaiahSK, AffaraNA, et al. (2009) The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Biol 7: e1000244.

45. LuohSW, BainPA, PolakiewiczRD, GoodheartML, GardnerH, et al. (1997) Zfx mutation results in small animal size and reduced germ cell number in male and female mice. Development 124: 2275–2284.

46. MonesiV (1964) Ribonucleic Acid Synthesis during Mitosis and Meiosis in the Mouse Testis. J Cell Biol 22: 521–532.

47. MonesiV (1965) Synthetic activities during spermatogenesis in the mouse. Experimental Cell Research 39: 197–224.

48. ReynardLN, CocquetJ, BurgoynePS (2009) The Multi-Copy Mouse Gene Sycp3-Like Y-Linked (Sly) Encodes an Abundant Spermatid Protein That Interacts with a Histone Acetyltransferase and an Acrosomal Protein. Biol Reprod 81: 250–7 doi: 10.1095/biolreprod.108.075382

49. MuellerJL, MahadevaiahSK, ParkPJ, WarburtonPE, PageDC, et al. (2008) The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40: 794–799.

50. NamekawaSH, ParkPJ, ZhangLF, ShimaJE, McCarreyJR, et al. (2006) Postmeiotic sex chromatin in the male germline of mice. Curr Biol 16: 660–667.

51. TurnerJM, MahadevaiahSK, EllisPJ, MitchellMJ, BurgoynePS (2006) Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 10: 521–529.

52. van RheedeT, BastiaansT, BooneDN, HedgesSB, de JongWW, et al. (2006) The platypus is in its place: nuclear genes and indels confirm the sister group relation of monotremes and Therians. Mol Biol Evol 23: 587–597.

53. GravesJA (1995) The origin and function of the mammalian Y chromosome and Y-borne genes–an evolving understanding. Bioessays 17: 311–320.

54. Schneider-GädickeA, Beer-RomeroP, BrownLG, NussbaumR, PageDC (1989) The ZFX gene on the human X chromosome escapes X-inactivation and is closely related to ZFY, the putative sex determinant on the Y chromosome. Cell 57: 1247–1258.

55. JegalianK, PageDC (1998) A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature 394: 776–780.

56. PamiloP, BianchiNO (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Molecular Biology and Evolution 10: 271–281.

57. TuckerPK, AdkinsRM, RestJS (2003) Differential rates of evolution for the ZFY-related zinc finger genes, Zfy, Zfx, and Zfa in the mouse genus Mus. Mol Biol Evol 20: 999–1005.

58. AshworthA, RastanS, Lovell-BadgeR, KayG (1991) X-chromosome inactivation may explain the difference in viability of XO humans and mice. Nature 351: 406–408.

59. ShimminLC, ChangBH, LiWH (1994) Contrasting rates of nucleotide substitution in the X-linked and Y-linked zinc finger genes. J Mol Evol 39: 569–578.

60. LiL, ZhengP, DeanJ (2010) Maternal control of early mouse development. Development 137: 859–870.

61. WangH, HuYC, MarkoulakiS, WelsteadGG, ChengAW, et al. (2013) TALEN-mediated editing of the mouse Y chromosome. Nat Biotechnol 31: 530–532.

62. YamauchiY, RielJM, StoytchevaZ, WardMA (2014) Two Y genes can replace the entire Y chromosome for assisted reproduction in the mouse. Science 343: 69–72.

63. DerijckA, van der HeijdenG, GieleM, PhilippensM, de BoerP (2008) DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum Mol Genet 17: 1922–1937.

64. LieberMR (2008) The mechanism of human nonhomologous DNA end joining. J Biol Chem 283: 1–5.

65. CattanachBM, PollardCE, HawkesSG (1971) Sex reversed mice : XX and XO males. Cytogenetics 10: 318–337.

66. CattanachBM, EvansEP, BurtenshawMD, BarlowJ (1982) Male, female and intersex development in mice of identical chromosome constitution. Nature 300: 445–446.

67. McLarenA, MonkM (1982) Fertile females produced by inactivation of X chromosome of ‘sex-reversed’ mice. Nature 300: 446–448.

68. HadjantonakisAK, GertsensteinM, IkawaM, OkabeM, NagyA (1998) Non-invasive sexing of preimplantation stage mammalian embryos. Nat Genet 19: 220–222.

69. GubbayJ, CollignonJ, KoopmanP, CapelB, EconomouA, et al. (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346: 245–250.

70. GubbayJ, VivianN, EconomouA, JacksonD, GoodfellowP, et al. (1992) Inverted repeat structure of the Sry locus in mice. Proc Natl Acad Sci U S A 89: 7953–7957.

71. MahadevaiahSK, OdorisioT, ElliottDJ, RattiganA, SzotM, et al. (1998) Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids, and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities. Hum Mol Genet 7: 715–727.

72. WrightWE, SassoonDA, LinVK (1989) Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56: 607–617.

73. MahadevaiahSK, TurnerJMA, BaudatF, RogakouEP, de BoerP, et al. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nature Genetics 27: 271–276.

74. MahadevaiahSK, CostaY, TurnerJM (2009) Using RNA FISH to study gene expression during mammalian meiosis. Methods Mol Biol 558: 433–444.

75. GillG, PtashneM (1988) Negative effect of the transcriptional activator GAL4. Nature 334: 721–724.

76. LeeEC, YuD, Martinez de VelascoJ, TessarolloL, SwingDA, et al. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56–65.

77. GuarenteL (1983) Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol 101: 181–191.