RBMY, a probable human spermatogenesis factor, and other hnRNP G proteins interact with Tra2β and affect splicing

Human Molecular Genetics

Volumn 9, Issue 5, 2000, Pages 685-694

  Vanables, J P ^a,b   Elliott, D J ^b   Makarova, O V ^a,c   Makarov, E M ^a,c   Cooke, H J ^b   Eperon, I C ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b WESTERN GENERAL HOSPITAL   (United Kingdom)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; RIBONUCLEOPROTEIN;

ARTICLE; CELL NUCLEUS; HELA CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA SPLICING; SPERMATOCYTE; SPERMATOGENESIS; TESTIS;

DROSOPHILA PROTEINS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MALE; NUCLEAR PROTEINS; RIBONUCLEOPROTEINS; RNA SPLICING; RNA-BINDING PROTEINS; SPERMATOGENESIS; TESTIS; TWO-HYBRID SYSTEM TECHNIQUES; Y CHROMOSOME;

MAMMALIA;

EID: 0034701246     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Hecht, N.B. (1998) Molecular mechanisms of male germ cell differentiation. Bioesays, 20, 555-561.
2. deKretser, D.M., Loveland, K.L., Meinhardt, A., Simorangkir, D. and Wreford, N. (1998) Spermatogenesis. Hum. Reprod., 13, 1-8.
3. Venables, J. and Eperon, I. (1999) The roles of RNA-binding proteins in spermatogenesis and male infertility. Curr. Opin. Genet. Dev., 9, 346-354.
4. Hargreave, T.B. (1997) Human infertility. In Hargreave, T.B. (ed.), Male Infertility. Springer Verlag, Heidelberg, Germany, pp. 1-16.
5. Pryor, J.L., KentFirst, M., Muallem, A., VanBergen, A.H., Nolten, W.E., Meisner, L. and Roberts, K.P. (1997) Microdeletions in the Y chromosome of infertile men. N. Engl. J. Med. 336, 534-539.
6. Tiepolo, L. and Zuffardi, O. (1976) Localisation of factors controlling spermatogenesis in the non-fluorescent portion of the human Y chromosome long arm. Hum. Genet., 34, 119-124.
7. Elliott, D.J. and Cooke, H.J. (1997) The molecular genetics of male infertility. BioEssays, 19, 801-809.
8. Ma, K., Inglis, J.D., Sharkey, A., Bickmore, W.A., Hill, R.E., Prosser, E.J., Speed, R.M., Thomson, E.J., Jobling, M., Taylor, K. et al. (1993) A Y-chromosome gene family with RNA-binding protein homology: candidates for the azoospermia factor AZF controlling human spermatogenesis. Cell, 75, 1287-1295.
9. Delbridge, M.L., Lingenfelter, P.A., Disteche, C.M. and Graves, J.A. (1999) The candidate spermatogenesis gene RBMY has a homologue on the human X chromosome. Nature Genet., 22, 223-224.
10. Chai, N.N., Zhou, H.Y., Hernandez, J., Najmabadi, H., Bhasin, S. and Yen, P.H. (1998) Structure and organization of the RBMY genes on the human Y chromosome: transposition and amplification of an ancestral autosomal hnRNPG gene. Genomics, 49, 283-289.
11. Vogt, P.H. (1997) Human Y chromosome deletions in Yq11 and male fertility. Adv. Exp. Med. Biol., 424, 17-30.
12. Vogt, P.H., Edelmann, A., Kirsch, S., Henegariu, O., Hirschmann, P., Kiesewetter, F., Kohn, F.M., Schill, W.B., Farah, S., Ramos, C. et al. (1996) Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11. Hum. Mol. Genet., 5, 933-943.
13. Elliott, D.J., Millar, M.R., Oghene, K., Ross, A., Kiesewetter, F., Pryor, J., McIntyre, M., Hargreave, T.B., Saunders, P., Vogt, P.H. et al. (1997) Expression of RBM in the nuclei of human germ cells is dependent on a critical region of the Y chromosome long arm. Proc. Natl Acad. Sci. USA, 94, 3848-3853.
14. Burgoyne, P.S. (1998) The mammalian Y chromosome: a new perspective. Bioessays, 20, 363-366.
15. Delhridge, M.L., Harry, J.L., Toder, R., ONeill, R., Ma, K., Chandley, A.C. and Graves, J. (1997) A human candidate spermatogenesis gene, RBMI, is conserved and amplified on the marsupial Y chromosome. Nature Genet., 15, 131-136.
16. Elliott, D.J., Ma, K., Kerr, S.M., Thakrar, R., Speed, R., Chandley, A.C. and Cooke, H. (1996) An RBM homologue maps to the mouse Y chromosome and is expressed in germ cells. Hum. Mol. Genet., 5, 869-874.
17. Mahadevaiah, S.K., Odorisio, T., Elliott, D.J., Rattigan, A., Szot, M., Laval, S.H., Washburn, L.L., McCarrey, J.R., Cattanach, B.M., LovellBadge, R. and Burgoyne, P.S. (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.
18. Mazeyrat, S., Saut, N., Mattei, M.G. and Mitchell, M.J. (1999) RBMY evolved on the Y chromosome from a ubiquitously transcribed X-Y identical gene. Nature Genet., 22, 224-226.
19. Dreyfuss, G., Matunis, M.J., PinolRoma, S. and Burd, C.G. (1993) hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem., 62, 289-321.
20. Bennett, M., Piñol-Roma, S., Staknis, D., Dreyfuss, G. and Reed, R. (1992) Differential binding of heterogeneous nuclear ribonucleoproteins to mRNA precursors prior to spliceosome assembly in vitro. Mol. Cell. Biol., 12, 3165-3175.
21. Birney, E., Kumar, S. and Krainer, A.R. (1993) Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan premRNA splicing factors. Nucleic Acids Res., 21, 5803-5816.
22. Valcárcel, J. and Green, M.R. (1996) The SR protein family: pleiotropic functions in pre-mRNA splicing. Trends Biochem. Sci., 21, 296-301.
23. Manley, J.L. and Tacke, R. (1996) SR proteins and splicing control. Genes Dev., 10, 1569-1579.
24. Fu, X.-D. (1995) The superfamily of arginine/serine-rich splicing factors. RNA, 1, 663-680.
25. Delbridge, M.L., Ma, K., Subbarao, M.N., Cooke, H.J., Bhasin, S. and Graves, J.A.M. (1998) Evolution of mammalian HNRNPG and its relationship with the putative azoospermia factor RBM. Mamm Genome, 9, 168-170.
26. Soulard, M., Dellavalle, V., Siomi, M.C., Pinolroma, S., Codogno, P., Bauvy, C., Bellini, M., Lacroix, J.C., Monod, G., Dreyfuss, G. and Larsen, C.J. (1993) HnRNP G: sequence and characterization of a glycosylated RNA-binding protein. Nucleic Acids Res., 21, 4210-4217.
27. Elliott, D.J., Oghene, K., Makarov, G., Makarova, O., Hargreave, T.B., Chandley, A.C., Eperon, I.C. and Cooke, H.J. (1998) Dynamic changes in the subnuclear organisation of pre-mRNA splicing proteins and RBM during human germ cell development. J. Cell Sci. 111, 1255-1265.
28. Chien, C.T., Bartel, P.L., Sternglanz, R. and Fields, S. (1991) The 2-hybrid system - a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl Acatl. Sci. USA, 88, 9578-9582.
29. Venables, J.P., Vernet, C., Chew, S.L., Elliott, D.J., Cowmeadow, R.B., Wu, J., Cooke, H.J., Artzt, K. and Eperon, I.C. (1999) T-STAR/ETOILE: a novel relative of SAM68 that interacts with an RNA-binding protein implicated in spermatogenesis. Hum. Mol. Genet., 8, 959-969.
30. Taylor, S.J. and Shalloway, D. (1994) An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature, 368, 867-871.
31. Fumagalli, S., Totty, N.F., Hsuan, J.J. and Courtneidge, S.A. (1994) A target for Src in mitosis. Nature, 368, 871-874.
32. Lin, Q., Taylor, S.J. and Shalloway, D. (1997) Specificity and determinants of Sam68 RNA binding - implications for the biological function of K homology domains. J. Biol. Chem., 272, 27274-27280.
33. Resnick, RJ., Taylor, S.J., Lin, Q. and Shalloway, D. (1997) Phosphorylation of the Src substrate Sam68 by Cdc2 during mitosis. Oncogene, 15, 1247-1253.
34. Segade, F., Hurle, B., Claudio, E., Ramos, S. and Lazo, P.S. (1996) Molecular cloning of a mouse homologue for the Drosophila splicing regulator Tra2. FEBS Lett., 387, n2-n3.
35. Dauwalder, B., Amayamanzanares, F. and Mattox, W. (1996) A human homolog of the Drosophila sex determination factor transformer-2 has conserved splicing regulatory functions. Proc. Natl Acad. Sci. USA, 93, 9004-9009.
36. Beil, B., Screaton, G. and Stamm, S. (1997) Molecular cloning of hTra2-beta-1 and hTra2-beta-2, two human homologs of TRA-2 generated by alternative splicing. DNA Cell Biol., 16, 679-690.
37. Baker, B.S. (1989) Sex in flies: the splice of life. Nature, 340, 521-524.
38. Finley, K.D., Taylor, B.J., Milstein, M. and McKeown, M. (1997) dissatisfaction, a gene involved in sex-specific behavior and neural development of Drosophila melanogaster. Proc. Natl Acad. Sci. USA, 94, 913-918.
39. MacDougall, C., Harbison, D. and Bownes, M. (1995) The developmental consequences of alternate splicing in sex determination and differentiation in Drosophila. Dev. Biol., 172, 353-376.
40. Ryner, L.C., Goodwin, S.F., Castrillon, D.H., Anand, A., Villella, A., Baker, B.S., Hall, J.C., Taylor, B.J. and Wasserman, S.A. (1996) Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell, 87, 1079-1089.
41. McGuffin, ME., Chandler, D., Somaiya, D., Dauwalder, B. and Mattox, W. (1998) Autoregulation of transformer-2 alternative splicing is necessary for normal male fertility in Drosophila. Genetics, 149, 1477-1486.
42. Amrein, H., Hedley, M.L. and Maniatis, T. (1994) The role of specific protein-RNA and protein-protein interactions in positive and negative control of pre-mRNA splicing by Transformer 2. Cell, 76, 735-746.
43. Tacke, R., Tohyama, M., Ogawa, S. and Manley, J.L. (1998) Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell, 93, 139-148.
44. Chen, T.P., Damaj, B.B., Herrera, C., Lasko, P. and Richard, S. (1997) Self-association of the single-KH-domain family members Sam68, GRP33, GLD-1, and Qk1: role of the KH domain. Mol. Cell. Biol., 17, 5707-5718.
45. Neugebauer, K.M., Stolk, J.A. and Roth, M.B. (1995) A conserved epitope on a subset of SR proteins defines a larger family of pre-messenger RNA splicing factors. J. Cell Biol., 129, 899-908.
46. Graham, I.R., Hamshere, M. and Eperon, I.C. (1992) Alternative splicing of a human alpha-tropomyosin muscle-specific exon: identification of determining sequences. Mol. Cell. Biol., 12, 3872-3882.
47. Eperon, I.C., Ireland, D.C., Smith, R.A., Mayeda, A. and Krainer, A.R. (1993) Pathways for selection of 5′ splice sites by U1 snRNPs and SF2/ ASF. EMBOJ., 12, 3607-3617.
48. Schaal, T.D. and Maniatis, T. (1999) Multiple distinct splicing enhancers in the protein-coding sequences of a constitutively spliced pre-mRNA. Mol. Cell Biol., 19, 261-273.
49. Du, C., McGuffin, M.E., Dauwalder, B., Rabinow, L. and Mattox, W. (1998) Protein phosphorylation plays an essential role in the regulation of alternative splicing and sex determination in Drosophila. Mol. Cell, 2, 741-750.
50. Papoutsopoulou, S., Nikolakaki, E., Chalepakis, G., Kruft, V., Chevaillier, P. and Giannakouros, T. (1999) SR protein-specific kinase 1 is highly expressed in testis and phosphorylates protamine 1. Nucleic Acids Res., 27, 2972-2980.
51. Xiao, S.H. and Manley, J.L. (1997) Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev., 11, 334-344.
52. Wang, J. and Manley, J.L. (1997) Regulation of pre-mRNA splicing in metazoa. Curr. Opin. Genet. Dev., 7, 205-211.
53. Colwill, K.T., Pawson, T., Andrews, B., Prasad, J., Manley, J.L., Bell, J.C. and Duncan, P.I. (1996) The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J., 15, 265-275.
54. Gui, J.F., Tronchere, H., Chandler, S.D. and Fu, X.D. (1994) Purification and characterization of a kinase specific for the serine- and arginine-rich pre-mRNA splicing factors. Proc. Natl Acad. Sci. USA, 91, 10824-10828.
55. Misteli, T. and Spector, D.L. (1997) Protein phosphorylation and the nuclear organization of pre-mRNA splicing. Trends Cell Biol., 7, 135-138.
56. Mermoud, J.E., Cohen, P. and Lamond, A.I. (1994) Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J., 13, 5679-5688.
57. Cao, W.H., Jamison, S.F. and Garcia-Blanco, M.A. (1997) Both phosphorylation and dephosphorylation of ASF/SF2 are required for premRNA splicing in vitro. RNA, 3, 1456-1467.
58. Chew, S.L., Liu, H.X., Mayeda, A. and Krainer, A.R. (1999) Evidence for the function of an exonic splicing enhancer after the first catalytic step of pre-mRNA splicing. Proc: Natl Acad. Sci. USA, 96, 10655-10660.
59. Kohtz, J.D., Jamison, S.F., Will, C.L., Zuo, P., Luhrmann, R., GarciaBlanco, M.A. and Manley, J.L. (1994) Protein-protein interactions and 5′ splice site recognition in mammalian mRNA precursors. Nature, 368, 119-124.
60. Lynch, K.W. and Maniatis, T. (1995) Synergistic interactions between 2 distinct elements of a regulated splicing enhancer. Genes Dev., 9, 284-293.
61. Lynch, K.W. and Maniatis, T. (1996) Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev., 10, 2089-2101.
62. Boggs, R.T., Gregor, P., Idriss, S., Belote, J.M. and Mckeown, M. (1987) Regulation of sexual-differentiation in Drosophila-melanogaster via alternative splicing of RNA from the transformer gene. Cell, 50, 739-747.
63. Dauwalder, B. and Maltox, W. (1998) Analysis of the functional specificity of RS domains in vivo. EMBO J., 17, 6049-6060.
64. Hanamura, A., Caceres, J.F., Mayeda, A., Franza, B.R. and Krainer, A.R. (1998) Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA, 4, 430-444.
65. Buckanovich, R.J. and Darnell, R.B. (1997) The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol. Cell Biol., 17, 3194-3201.
66. Akamatsu, W., Okano, H.J., Osumi, N., Inoue, T., Nakamura, S., Sakakibara, S.I., Miura, M., Matsuo, N., Darnell, R.B. and Okano, H. (1999) Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc. Natl Acad. Sci. USA, 96, 9885-9890.
67. Zhang, L., Liu, W. and Grabowski, P.J. (1999) Coordinate repression of a trio of neuron-specific splicing events by the splicing regulator PTB. RNA, 5, 117-130.
68. Chan, R.C. and Black, D.L. (1997) The polypyrimidine tract binding protein binds upstream of neural cell-specific c-src exon N1 to repress the splicing of the intron downstream. Mol. Cell. Biol., 17, 4667-4676.
69. Ashiya, M. and Grabowski, P.J. (1997) A neuron-specific splicing switch mediated by an array of pre-mRNA repressor sites: evidence of a regulatory role for the polypyrimidine tract binding protein and a brain-specific PTB counterpart. RNA, 3, 996-1015.
70. Mayeda, A. and Ohshima, Y. (1990) Beta-globin transcripts carrying a single intron with three adjacent nucleotides of 5′ exon are efficiently spliced in vitro irrespective of intron position or surrounding exon sequences. Nucleic Acids Res., 18, 4671-4676.
71. Eperon, I.C. and Krainer, A.R. (1994) Splicing of mRNA precursors in mammalian cells. In Higgins, S.J. and Hames, B.D. (eds), RNA Processing: A Practical Approach. IRL Press, Oxford, UK, pp. 57-101.