Skip to main content
SpringerLink
Log in

Usp9y (ubiquitin-specific protease 9 gene on the Y) is associated with a functional promoter and encodes an intact open reading frame homologous to Usp9x that is under selective constraint

  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

Sequences complementary to the X-linked ubiquitin-specific protease gene Usp9x (Dffrx) have been shown to map to the Sxrb interval of the mouse Y Chromosome (chr) and to be expressed in a testis-specific manner. In humans, ubiquitously expressed functional homologues (USP9Y and USP9X DFFRY/DFFRX) are present on both sex chromosomes, whereas in mouse it remains to be demonstrated that the Y-linked sequences encode a functional protein. In this paper, it is shown that the Usp9y gene encodes a potentially functional ubiquitin-specific protease possessing a core promoter region that shares several features characteristic of other testis-specific genes. Analysis of synonymous and nonsynonymous nucleotide changes suggests that there is constraint on the amino acid sequence of both the mouse Usp9x and Usp9y genes, a finding that mirrors similar analysis of the human orthologs. Thus, in both mouse and human, selection is acting to maintain the amino acid sequence of the X and Y-linked genes. This indicates that in both species the genes on each sex chromosome continue to encode an important function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. M Ambhaikar E Goldberg (1999) ArticleTitleDNA-protein interactions in the CCAAT box region of the murine lactate dehydrogenase C promoter. Mol Reprod Dev 52 360–365 Occurrence Handle10.1002/(SICI)1098-2795(199904)52:4<360::AID-MRD4>3.0.CO;2-I Occurrence Handle1:CAS:528:DyaK1MXhsl2iu7k%3D Occurrence Handle10092115

    Article  CAS  PubMed  Google Scholar 

  2. FJ Ayala A Rzhetsky (1998) ArticleTitleOrigin of the metazoan phyla: molecular clocks confirm paleontological estimates. Proc Natl Acad Sci USA 95 606–611 Occurrence Handle10.1073/pnas.95.2.606 Occurrence Handle1:CAS:528:DyaK1cXmtFajsg%3D%3D Occurrence Handle9435239

    Article  CAS  PubMed  Google Scholar 

  3. A Barberis G Superti-Furga M Busslinger (1987) ArticleTitleMutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell 50 347–359 Occurrence Handle1:CAS:528:DyaL1cXltVCltw%3D%3D Occurrence Handle3607873

    CAS  PubMed  Google Scholar 

  4. AR Bellvé CF Millette YM Bhatnagar DA O'Brien (1977) ArticleTitleDissociation of the mouse testis and characterization of isolated spermatogenic cells. J Histochem Cytochem 25 480–494 Occurrence Handle893996

    PubMed  Google Scholar 

  5. PH Boer CN Adra YF Lau MW McBurney (1987) ArticleTitleThe testis-specific phosphoglycerate kinase gene pgk-2 is a recruited retroposon. Mol Cell Biol 7 3107–3112 Occurrence Handle1:CAS:528:DyaL1cXltValtQ%3D%3D Occurrence Handle2823118

    CAS  PubMed  Google Scholar 

  6. C Bonny LA Cooker E Goldberg (1998) ArticleTitleDeoxyribonucleic acid-protein interactions and expression of the human testis-specific lactate dehydrogenase promoter: transcription factor Sp1 plays a major role. Biol Reprod 58 754–759 Occurrence Handle1:CAS:528:DyaK1cXhtlansro%3D Occurrence Handle9510963

    CAS  PubMed  Google Scholar 

  7. GM Brown RA Furlong CA Sargent RP Erickson G Longepied et al. (1998) ArticleTitleCharacterisation of the coding sequence and fine mapping of the human DFFRY gene and comparative expression analysis and mapping to the Sxrb interval of the mouse Y chromosome of the Dffry gene. Hum Mol Genet 7 97–107 Occurrence Handle10.1093/hmg/7.1.97 Occurrence Handle1:CAS:528:DyaK1cXotVyksA%3D%3D Occurrence Handle9384609

    Article  CAS  PubMed  Google Scholar 

  8. TA Brown SL McKnight (1992) ArticleTitleSpecificities of protein-protein and protein-DNA interaction of GABP alpha and two newly defined ets-related proteins. Genes Dev 6 2502–2512 Occurrence Handle1:CAS:528:DyaK3sXkvVOrsbc%3D Occurrence Handle1340465

    CAS  PubMed  Google Scholar 

  9. D Bunick PA Johnson TR Johnson NB Hecht (1990) ArticleTitleTranscription of the testis-specific mouse protamine 2 gene in a homologous in vitro transcription system. Proc Natl Acad Sci USA 87 891–895 Occurrence Handle1:CAS:528:DyaK3cXhtFentbc%3D Occurrence Handle2300581

    CAS  PubMed  Google Scholar 

  10. PS Burgoyne ER Levy A McLaren (1986) ArticleTitleA spermatogenic failure in male mice lacking H-Y antigen. Nature 320 170–172 Occurrence Handle1:STN:280:BimC2cnovFE%3D Occurrence Handle3951555

    CAS  PubMed  Google Scholar 

  11. B Capel A Swain S Nicolis A Hacker M Walter et al. (1993) ArticleTitleCircular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73 1019–1030 Occurrence Handle1:CAS:528:DyaK3sXksValtbw%3D Occurrence Handle7684656

    CAS  PubMed  Google Scholar 

  12. P Denny S Swift F Connor A Ashworth (1992) ArticleTitleAn SRY-related gene expressed during spermatogenesis in the mouse encodes a sequence-specific DNA-binding protein. Embo J 11 3705–3712 Occurrence Handle1:CAS:528:DyaK3sXkt1ejs74%3D Occurrence Handle1396566

    CAS  PubMed  Google Scholar 

  13. RF Doolittle DF Feng S Tsang G Cho E Little (1996) ArticleTitleDetermining divergence times of the major kingdoms of living organisms with a protein clock. Science 271 470–472 Occurrence Handle1:CAS:528:DyaK28XmvFyktg%3D%3D Occurrence Handle8560259

    CAS  PubMed  Google Scholar 

  14. R Fisher (1931) ArticleTitleThe evolution of dominance. Biol Rev 6 345–368

    Google Scholar 

  15. M Goto Y Masamune Y Nakanishi (1993) ArticleTitleA factor stimulating transcription of the testis-specific Pgk-2 gene recognizes a sequence similar to the binding site for a transcription inhibitor of the somatic-type Pgk-1 gene. Nucleic Acids Res 21 209–214 Occurrence Handle1:CAS:528:DyaK3sXhsVWis7c%3D Occurrence Handle8441629

    CAS  PubMed  Google Scholar 

  16. Hall N (2001) Ph.D. Functional analysis of the promoters of two Y-linked genes, Ubely and Usp9y. Thesis, University of Cambridge.

  17. MC Hofmann RA Hess E Goldberg JL Millan (1994) ArticleTitleImmortalized germ cells undergo meiosis in vitro. Proc Natl Acad Sci USA 91 5533–5537 Occurrence Handle1:STN:280:ByuB287mt1Q%3D Occurrence Handle8202522

    CAS  PubMed  Google Scholar 

  18. MC Hofmann D Abramian JL Millan (1995) ArticleTitleA haploid and a diploid cell coexist in an in vitro immortalized spermatogenic cell line. Dev Genet 16 119–127 Occurrence Handle1:STN:280:ByqB2MvnsVQ%3D Occurrence Handle7736662

    CAS  PubMed  Google Scholar 

  19. RC Iannello HH Dahl (1992) ArticleTitleTranscriptional expression of a testis-specific variant of the mouse pyruvate dehydrogenase E1 alpha subunit. Biol Reprod 47 48–58 Occurrence Handle1:CAS:528:DyaK38XkvVCmtL0%3D Occurrence Handle1637947

    CAS  PubMed  Google Scholar 

  20. RC Iannello J Young S Sumarsono MJ Tymms HH Dahl et al. (1997) ArticleTitleRegulation of Pdha-2 expression is mediated by proximal promoter sequences and CpG methylation. Mol Cell Biol 17 612–619 Occurrence Handle1:CAS:528:DyaK2sXmvVamtg%3D%3D Occurrence Handle9001214

    CAS  PubMed  Google Scholar 

  21. MH Jones RA Furlong H Burkin IJ Chalmers GM Brown et al. (1996) ArticleTitleThe Drosophila developmental gene fat facets has a human homologue in Xp11.4 which escapes X-inactivation and has related sequences on Yq11.2. Hum Mol Genet 5 1695–1701 Occurrence Handle10.1093/hmg/5.11.1695 Occurrence Handle1:CAS:528:DyaK28XmslKht78%3D Occurrence Handle8922996

    Article  CAS  PubMed  Google Scholar 

  22. BT Lahn DC Page (1997) ArticleTitleFunctional coherence of the human Y chromosome. Science 278 675–680 Occurrence Handle10.1126/science.278.5338.675 Occurrence Handle1:CAS:528:DyaK2sXmvVygu70%3D Occurrence Handle9381176

    Article  CAS  PubMed  Google Scholar 

  23. BT Lahn DC Page (1999) ArticleTitleFour evolutionary strata on the human X chromosome. Science 286 964–967 Occurrence Handle10.1126/science.286.5441.964 Occurrence Handle1:CAS:528:DyaK1MXntFaqtrk%3D Occurrence Handle10542153

    Article  CAS  PubMed  Google Scholar 

  24. WH Li (1993) ArticleTitleUnbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36 96–99 Occurrence Handle1:CAS:528:DyaK3sXnsVCmsA%3D%3D Occurrence Handle8433381

    CAS  PubMed  Google Scholar 

  25. S Mazeyrat N Saut CA Sargent S Grimmond G Longepied et al. (1998) ArticleTitleThe mouse Y chromosome interval necessary for spermatogonial proliferation is gene dense with syntenic homology to the human AZFa region. J Human Mol Genet 7 1713–1724 Occurrence Handle10.1093/hmg/7.11.1713 Occurrence Handle1:CAS:528:DyaK1cXmsVOgs78%3D

    Article  CAS  Google Scholar 

  26. S Mazeyrat N Saut V Grigoriev SK Mahadevaiah OA Ojarikre et al. (2001) ArticleTitleA Y-encoded subunit of the translation initiation factor Eif2 is essential for mouse spermatogenesis. Nat Genet 29 49–53 Occurrence Handle10.1038/ng717 Occurrence Handle1:CAS:528:DC%2BD3MXmvFGmsbY%3D Occurrence Handle11528390

    Article  CAS  PubMed  Google Scholar 

  27. MJ Mitchell (2000) ArticleTitleSpermatogenesis and the mouse Y chromosome: specialisation out of decay. Results Probl Cell Differ 28 233–270 Occurrence Handle1:CAS:528:DC%2BD3cXjsVSqtg%3D%3D Occurrence Handle10626301

    CAS  PubMed  Google Scholar 

  28. T Odorisio TA Rodriguez EP Evans AR Clarke PS Burgoyne (1998) ArticleTitleThe meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat Genet 18 257–261 Occurrence Handle1:CAS:528:DyaK1cXhtlKktbc%3D Occurrence Handle9500548

    CAS  PubMed  Google Scholar 

  29. SP Persengiev PJ Raval S Rabinovitch CF Millette DL Kilpatrick (1996) ArticleTitleTranscription factor Sp1 is expressed by three different developmentally regulated messenger ribonucleic acids in mouse spermatogenic cells. Endocrinology 137 638–646 Occurrence Handle1:CAS:528:DyaK28XntVCgtA%3D%3D Occurrence Handle8593813

    CAS  PubMed  Google Scholar 

  30. MO Robinson JR McCarrey MI Simon (1989) ArticleTitleTranscriptional regulatory regions of testis-specific PGK2 defined in transgenic mice. Proc Natl Acad Sci USA 86 8437–8441 Occurrence Handle1:CAS:528:DyaK3cXjtFClug%3D%3D Occurrence Handle2813402

    CAS  PubMed  Google Scholar 

  31. JD Saffer SP Jackson MB Annarella (1991) ArticleTitleDevelopmental expression of Sp1 in the mouse. Mol Cell Biol 11 2189–2199 Occurrence Handle1:CAS:528:DyaK3MXhvVaktbg%3D Occurrence Handle2005904

    CAS  PubMed  Google Scholar 

  32. CA Sargent CA Boucher S Kirsch G Brown B Weiss et al. (1999) ArticleTitleThe critical region of overlap defining the AZFa male infertility interval of proximal Yq contains three transcribed sequences. J Med Genet 36 670–677 Occurrence Handle1:CAS:528:DyaK1MXms1Sqsrs%3D Occurrence Handle10507722

    CAS  PubMed  Google Scholar 

  33. HJ Schulten W Engel K Nayernia P Burfeind (1999) ArticleTitleYeast one-hybrid assay identifies YY1 as a binding factor for a proacrosin promoter element. Biochem Biophys Res Commun 257 871–873 Occurrence Handle10.1006/bbrc.1999.0556 Occurrence Handle1:CAS:528:DyaK1MXisVahsrs%3D Occurrence Handle10208876

    Article  CAS  PubMed  Google Scholar 

  34. Y Shi JS Lee KM Galvin (1997) ArticleTitleEverything you have ever wanted to know about Yin Yang 1. Biochim Biophys Acta 1332 F49–F66 Occurrence Handle10.1016/S0304-419X(96)00044-3 Occurrence Handle1:CAS:528:DyaK2sXhvFWiu7w%3D Occurrence Handle9141463

    Article  CAS  PubMed  Google Scholar 

  35. C Sun H Skaletsky B Birren K Devon Z Tang et al. (1999) ArticleTitleAn azoospermic man with a de novo point mutation in the Y-chromosomal gene USP9Y. Nat Genet 23 429–432 Occurrence Handle10.1038/70539 Occurrence Handle1:CAS:528:DyaK1MXnvFOktbs%3D Occurrence Handle10581029

    Article  CAS  PubMed  Google Scholar 

  36. MJ Sutcliffe PS Burgoyne (1989) ArticleTitleAnalysis of the testis of H-Y negative Xosxrb mice suggests that the spermatogenesis gene (Spy) acts during differentiation of A spermatogonia. Development 107 373–380 Occurrence Handle1:STN:280:By%2BB3Mvlt1Y%3D Occurrence Handle2632229

    CAS  PubMed  Google Scholar 

  37. MJ Sutcliffe SM Darling PS Burgoyne (1991) ArticleTitleSpermatogenesis in XY, XYSxra and XOSxra mice: a quantitative analysis of spermatogenesis throughout puberty. Mol Reprod Dev 30 81–89 Occurrence Handle1:STN:280:By2D283ktFM%3D Occurrence Handle1954032

    CAS  PubMed  Google Scholar 

  38. MJ Wolkowicz SA Coonrod PP Reddi JL Millan MC Hofmann et al. (1996) ArticleTitleRefinement of the differentiated phenotype of the spermatogenic cell line GC-2spd(ts). Biol Reprod 55 923–932 Occurrence Handle1:CAS:528:DyaK28Xls1Grsro%3D Occurrence Handle8879510

    CAS  PubMed  Google Scholar 

  39. SA Wood WS Pascoe K Ru T Yamada J Hirchenhain et al. (1997) ArticleTitleCloning and expression analysis of a novel mouse gene with sequence similarity to the Drosophila fat facets gene. Mech Dev 63 29–38 Occurrence Handle10.1016/S0925-4773(97)00672-2 Occurrence Handle1:CAS:528:DyaK2sXjvVKjtLk%3D Occurrence Handle9178254

    Article  CAS  PubMed  Google Scholar 

  40. LP Zhang J Stroud CA Eddy CA Walter JR McCarrey (1999) ArticleTitleMultiple elements influence transcriptional regulation from the human testis-specific PGK2 promoter in transgenic mice. Biol Reprod 60 1329–1337 Occurrence Handle1:CAS:528:DyaK1MXjsVejsLY%3D Occurrence Handle10330089

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Wellcome Trust and the BBSRC. N. Hall was supported by a BBSRC CASE studentship and by PIC International.

Author information

Authors and Affiliations

  1. Human Molecular Genetics Group, Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, UK

    Nicola M. Hall, Graeme M. Brown, Robert A. Furlong, Carole A. Sargent, Dominique Rocha & Nabeel A. Affara

  2. INSERM U406, Genetique Medicale et Developpement, Faculte de Medecine de la Timone, 27, Bd Jean Moulin, 13385 Marseille Cedex 05, France

    Michael Mitchell

Authors
  1. Nicola M. Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graeme M. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert A. Furlong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carole A. Sargent
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dominique Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nabeel A. Affara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nabeel A. Affara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hall, N.M., Brown, G.M., Furlong, R.A. et al. Usp9y (ubiquitin-specific protease 9 gene on the Y) is associated with a functional promoter and encodes an intact open reading frame homologous to Usp9x that is under selective constraint . Mamm Genome 14, 437–447 (2003). https://doi.org/10.1007/s00335-002-3068-4

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-002-3068-4

Keywords

Search

Navigation