The testis-specific double bromodomain-containing protein BRDT forms a complex with multiple spliceosome components and is required for mRNA splicing and 30-UTR truncation in round spermatids

Nucleic Acids Research

Volumn 40, Issue 15, 2012, Pages 7162-7175

  Berkovits, Binyamin D ^a   Wang, Li ^a   Guarnieri, Paolo ^a   Wolgemuth, Debra J ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRDT PROTEIN; DEAD BOX PROTEIN; DEAD BOX PROTEIN 5; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENOUS NUCLEAR RIBONUCLEOPROTEIN K; MESSENGER RNA; SPLICING FACTOR ARGININE SERINE RICH 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DEAD BOX POLYPEPTIDE 5 GENE; GENE; GENE EXPRESSION; HETEROGENOUS NUCLEAR RIBONUCLEOPROTEIN K GENE; MALE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SPLICING; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPLICEOSOME; SPLICING FACTOR ARGININE SERINE RICH 2 GENE; TAR DNA BINDING PROTEIN GENE; TESTIS; TRANSCRIPTION REGULATION; UPREGULATION;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; ANIMALS; CELL LINE; GENE EXPRESSION REGULATION; MALE; MICE; MUTATION; NUCLEAR PROTEINS; PROTEIN ISOFORMS; RNA 3' END PROCESSING; RNA, MESSENGER; SPERMATIDS; SPLICEOSOMES; TESTIS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84867097905     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks342     Document Type: Article

References (79)

1. Florence, B. and Faller, D. V. (2001) You bet-cha: a novel family of transcriptional regulators. Front. Biosci., 6, D1008-D1018.
2. Chiang, C. M. (2009) Brd4 engagement from chromatin targeting to transcriptional regulation: selective contact with acetylated histone H3 and H4. F1000 Biol. Rep., 1, 98.
3. Kanno, T., Kanno, Y., Siegel, R. M., Jang, M. K., Lenardo, M. J. and Ozato, K. (2004) Selective recognition of acetylated histones by bromodomain proteins visualized in living cells. Mol. Cell, 13, 33-43.
4. Huang, H., Zhang, J., Shen, W., Wang, X., Wu, J., Wu, J. and Shi, Y. (2007) Solution structure of the second bromodomain of Brd2 and its specific interaction with acetylated histone tails. BMC Struct. Biol., 7, 57.
5. Moriniere, J., Rousseaux, S., Steuerwald, U., Soler-Lopez, M., Curtet, S., Vitte, A. L., Govin, J., Gaucher, J., Sadoul, K., Hart, D. J. et al. (2009) Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature, 461, 664-668.
6. Taniguchi, Y., Suzuki, H., Ohtsuka, M., Kikuchi, N., Kimura, M. and Inoko, H. (2001) Isolation and characterization of three genes paralogous to mouse Ring3. Nucleic Acids Res. Suppl., 2001, 247-248.
7. Peng, J., Dong, W., Chen, L., Zou, T., Qi, Y. and Liu, Y. (2007) Brd2 is a TBP-associated protein and recruits TBP into E2F-1 transcriptional complex in response to serum stimulation. Mol. Cell Biochem., 294, 45-54.
8. Lamonica, J. M., Deng, W., Kadauke, S., Campbell, A. E., Gamsjaeger, R., Wang, H., Cheng, Y., Billin, A. N., Hardison, R. C., Mackay, J. P. et al. (2011) Bromodomain protein Brd3 associates with acetylated GATA1 to promote its chromatin occupancy at erythroid target genes. Proc. Natl Acad. Sci. USA, 108, E159-E168.
9. Gamsjaeger, R., Webb, S. R., Lamonica, J. M., Billin, A., Blobel, G. A. and Mackay, J. P. (2011) Structural basis and specificity of acetylated transcription factor GATA1 recognition by BET family bromodomain protein Brd3. Mol. Cell Biol., 31, 2632-2640.
10. LeRoy, G., Rickards, B. and Flint, S. J. (2008) The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Mol. Cell, 30, 51-60.
11. Jang, M. K., Mochizuki, K., Zhou, M., Jeong, H. S., Brady, J. N. and Ozato, K. (2005) The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol. Cell, 19, 523-534.
12. Yang, Z., Yik, J. H., Chen, R., He, N., Jang, M. K., Ozato, K. and Zhou, Q. (2005) Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell, 19, 535-545.
13. Yang, Z., He, N. and Zhou, Q. (2008) Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression. Mol. Cell. Biol., 28, 967-976.
14. Wu, S. Y. and Chiang, C. M. U (2007) The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation. J. Biol. Chem., 282, 13141-13145.
15. Rahman, S., Sowa, M. E., Ottinger, M., Smith, J. A., Shi, Y., Harper, J. W. and Howley, P. M. (2011) The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3. Mol. Cell. Biol., 31, 2641-2652.
16. Bettegowda, A. and Wilkinson, M. F. (2010) Transcription and post-transcriptional regulation of spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci., 365, 1637-1651.
17. Lui, W. C., CY. (2008). Transcription regulation in spermatogenesis. In: Cheng CY (ed). Molecular Mechanisms in Spermatogenesis. Springer, New York, Vol. 636, pp. 115-132.
18. Hogeveen, K. N. and Sassone-Corsi, P. (2006) Regulation of gene expression in post-meiotic male germ cells: CREM-signalling pathways and male fertility. Hum. Fertil., 9, 73-79.
19. Wolgemuth, D. J. and Chung, S. S. (2007) Retinoid signaling during spermatogenesis as revealed by genetic and metabolic manipulations of retinoic acid receptor alpha. Soc. Reprod. Fertil. Suppl., 63, 11-23.
20. Chalmel, F., Rolland, A. D., Niederhauser-Wiederkehr, C., Chung, S. S., Demougin, P., Gattiker, A., Moore, J., Patard, J. J., Wolgemuth, D. J., Jegou, B. et al. (2007) The conserved transcriptome in human and rodent male gametogenesis. Proc. Natl Acad. Sci. USA, 104, 8346-8351.
21. Jaspers, S., Gellersen, B., Kempf, R., Samalecos, A., Bergmann, M. and Steger, K. (2007) Functional characterization of male germ cell-specific CREM isoforms. J. Androl., 28, 59-66.
22. Don, J. and Stelzer, G. (2002) The expanding family of CREB/CREM transcription factors that are involved with spermatogenesis. Mol. Cell Endocrinol., 187, 115-124.
23. Freiman, R. N. (2009) Specific variants of general transcription factors regulate germ cell development in diverse organisms. Biochim. Biophys. Acta, 1789, 161-166.
24. Gan, Q., Chepelev, I., Wei, G., Tarayrah, L., Cui, K., Zhao, K. and Chen, X. (2010) Dynamic regulation of alternative splicing and chromatin structure in Drosophila gonads revealed by RNA-seq. Cell Res., 20, 763-783.
25. Eddy, E. M. (2002) Male germ cell gene expression. Recent Prog. Horm. Res., 57, 103-128.
26. Elliott, D. J. and Grellscheid, S. N. (2006) Alternative RNA splicing regulation in the testis. Reproduction, 132, 811-819.
27. Yeo, G., Holste, D., Kreiman, G. and Burge, C. B. (2004) Variation in alternative splicing across human tissues. Genome Biol., 5, R74.
28. Venables, J. P. (2002) Alternative splicing in the testes. Curr. Opin. Genet. Dev., 12, 615-619.
29. Hecht, N. (1993) Gene expression during male germ cell development. In: Ewing, L. and Desjardins, C. (eds), Cell and Molecular Biology of the Testis. Oxford University Press, Oxford, pp. 464-503.
30. Eddy, E. M. and O'Brien, D. A. (1998) Gene expression during mammalian meiosis. Curr. Top. Dev. Biol., 37, 141-200.
31. Liu, D., Brockman, J. M., Dass, B., Hutchins, L. N., Singh, P., McCarrey, J. R., MacDonald, C. C. and Graber, J. H. (2007) Systematic variation in mRNA 30-processing signals during mouse spermatogenesis. Nucleic Acids Res., 35, 234-246.
32. Wang, H., Sartini, B. L., Millette, C. F. and Kilpatrick, D. L. (2006) A developmental switch in transcription factor isoforms during spermatogenesis controlled by alternative messenger RNA 30-end formation. Biol. Reprod., 75, 318-323.
33. O'Brien, D. A., Welch, J. E., Fulcher, K. D. and Eddy, E. M. (1994) Expression of mannose 6-phosphate receptor messenger ribonucleic acids in mouse spermatogenic and Sertoli cells. Biol. Reprod., 50, 429-435.
34. McMahon, K. W., Hirsch, B. A. and MacDonald, C. C. (2006) Differences in polyadenylation site choice between somatic and male germ cells. BMC Mol. Biol., 7, 35.
35. Singh, P., Alley, T. L., Wright, S. M., Kamdar, S., Schott, W., Wilpan, R. Y., Mills, K. D. and Graber, J. H. (2009) Global changes in processing of mRNA 30 untranslated regions characterize clinically distinct cancer subtypes. Cancer Res., 69, 9422-9430.
36. Rauschendorf, M. A., Zimmer, J., Hanstein, R., Dickemann, C. and Vogt, P. H. (2011) Complex transcriptional control of the AZFa gene DDX3Y in human testis. Int. J. Androl., 34, 84-96.
37. Jones, M. H., Numata, M. and Shimane, M. (1997) Identification and characterization of BRDT: a testis-specific gene related to the bromodomain genes RING3 and Drosophila fsh. Genomics, 45, 529-534.
38. Shang, E., Salazar, G., Crowley, T., Wang, X., Lopez, R. A., Wang, X. and Wolgemuth, D. J. (2004) Identification of unique, differentiation stage-specific patterns of expression of the bromodomain-containing genes Brd2, Brd3, Brd4, and Brdt in the mouse testis. Gene Expr. Patterns, 4, 513-519.
39. Shang, E., Nickerson, H. D., Wen, D., Wang, X. and Wolgemuth, D. J. (2007) The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development, 134, 3507-3515.
40. Bisgrove, D. A., Mahmoudi, T., Henklein, P. and Verdin, E. (2007) Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc. Natl Acad. Sci. USA, v104, 13690-13695.
41. Lygerou, Z., Conesa, C., Lesage, P., Swanson, R. N., Ruet, A., Carlson, M., Sentenac, A. and Seraphin, B. (1994) The yeast BDF1 gene encodes a transcription factor involved in the expression of a broad class of genes including snRNAs. Nucleic Acids Res., 22, 5332-5340.
42. Mattaj, I. W., Tollervey, D. and Seraphin, B. (1993) Small nuclear RNAs in messenger RNA and ribosomal RNA processing. FASEB J., 7, 47-53.
43. Wolgemuth, D. J., Gizang-Ginsberg, E., Engelmyer, E., Gavin, B. J. and Ponzetto, C. (1985) Separation of mouse testis cells on a Celsep (TM) apparatus and their usefulness as a source of high molecular weight DNA or RNA. Gamete Res., 12, 1-10.
44. Lotan, G., Golan, R., Efrati, Y., Vigodner, M., Lewin, L. M., Shochat, L. and Klin, B. (2005) An experimental study of the effect of two distinct surgical techniques of orchiopexy on spermatogenesis and testicular damage in cryptorchid testes. Fertil. Steril., 84, 749-755.
45. Golan, R., Lewin, L. M., Soffer, Y., Lotan, G., Shochat, L. and Vigodner, M. (2003) Evaluation of spermatogenesis using flow cytometry and confocal microscopy. Isr. Med. Assoc. J., 5, 536.
46. Janca, F. C., Jost, L. K. and Evenson, D. P. (1986) Mouse testicular and sperm cell development characterized from birth to adulthood by dual parameter flow cytometry. Biol. Reprod., 34, 613-623.
47. Team, R. D. C. (2008) R: a language and environment for statistical computing. Vienna Austria R Foundation for Statistical Computing, 1, ISBN 3-900051-900007-900050.
48. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, R80.
49. Smyth, G. K. (2005) Limma: linear models for microarray data. In: Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. and Huber, W. (eds), Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Springer, New York, pp. 397-420.
50. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U. and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
51. Binder, H., Preibisch, S. and Berger, H. (2010) Calibration of microarray gene-expression data. Methods Mol. Biol., 3576, 375-407.
52. Berkovits, B. D. and Wolgemuth, D. J. (2011) The first bromodomain of the testis-specific double bromodomain protein Brdt is required for chromocenter organization that is modulated by genetic background. Dev. Biol., 360, 358-368.
53. Chapman, D. L. and Wolgemuth, D. J. (1992) Identification of a mouse B-type cyclin which exhibits developmentally regulated expression in the germ line. Mol. Reprod. Dev., 33, 259-269.
54. Chung, S. S. and Wolgemuth, D. J. (2004) Role of retinoid signaling in the regulation of spermatogenesis. Cytogenet. Genome Res., 105, 189-202.
55. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 344-57.
56. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res., 37, 1-13.
57. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B, 57, 289-300.
58. D'Mello, V., Lee, J. Y., MacDonald, C. C. and Tian, B. (2006) Alternative mRNA polyadenylation can potentially affect detection of gene expression by affymetrix genechip arrays. Appl. Bioinformatics, 5, 249-253.
59. Cui, X. and Loraine, A. E. (2009) Consistency analysis of redundant probe sets on affymetrix three-prime expression arrays and applications to differential mRNA processing. PLoS One, 4, e4229.
60. Wang, H. Y., Wang, I. F., Bose, J. and Shen, C. K. (2004) Structural diversity and functional implications of the eukaryotic TDP gene family. Genomics, 83, 130-139.
61. Sureau, A., Gattoni, R., Dooghe, Y., Stevenin, J. and Soret, J. (2001) SC35 autoregulates its expression by promoting splicing events that destabilize its mRNAs. EMBO J., 20, 1785-1796.
62. Kuersten, S. and Goodwin, E. B. (2003) The power of the 30 UTR: translational control and development. Nat. Rev. Genet., 4, 626-637.
63. Idler, R. K. and Yan, W. (2011) Control of messenger RNA fate by RNA binding proteins: an emphasis on mammalian spermatogenesis. J. Androl.
64. Gregory, R. I., Yan, K. P., Amuthan, G., Chendrimada, T., Doratotaj, B., Cooch, N. and Shiekhattar, R. (2004) The Microprocessor complex mediates the genesis of microRNAs. Nature, 432, 235-240.
65. Yu, Z., Raabe, T. and Hecht, N. B. (2005) MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol. Reprod., 73, 427-433.
66. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
67. Ou, S. H., Wu, F., Harrich, D., Garcia-Martinez, L. F. and Gaynor, R. B. (1995) Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol., 69, 3584-3596.
68. Bose, J. K., Wang, I. F., Hung, L., Tarn, W. Y. and Shen, C. K. (2008) TDP-43 overexpression enhances exon 7 inclusion during the survival of motor neuron pre-mRNA splicing. J. Biol. Chem., 283, 28852-28859.
69. Edmonds, M. (2002) A history of poly A sequences: from formation to factors to function. Prog. Nucleic Acid Res. Mol. Biol., 71, 285-389.
70. Martinson, H. G. (2011) An active role for splicing in 30-end formation. Wiley Interdiscip. Rev. RNA, 2, 459-470.
71. Kleene, K. C. (2001) A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech. Dev., 106, 3-23.
72. Steger, K. (2001) Haploid spermatids exhibit translationally repressed mRNAs. Anat. Embryol., 203, 323-334.
73. Moen, P. T. Jr, Smith, K. P. and Lawrence, J. B. (1995) Compartmentalization of specific pre-mRNA metabolism: an emerging view. Hum. Mol. Genet., 4(Spec No), 1779-1789.
74. Bourgeois, C. F., Lejeune, F. and Stevenin, J. (2004) Broad specificity of SR (serine/arginine) proteins in the regulation of alternative splicing of pre-messenger RNA. Prog. Nucleic Acid Res. Mol. Biol., 78, 37-88.
75. Blencowe, B. J., Bowman, J. A., McCracken, S. and Rosonina, E. (1999) SR-related proteins and the processing of messenger RNA precursors. Biochem. Cell Biol., 77, 277-291.
76. Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S. and Fu, X. D. (2008) The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol., 15, 819-826.
77. Lenasi, T. and Barboric, M. (2010) P-TEFb stimulates transcription elongation and pre-mRNA splicing through multilateral mechanisms. RNA Biol., 7, 145-150.
78. Brettschneider, J., Collin, F., Bolstad, B. M. and Speed, T. P. (2008) Quality assessment for short oligonucleotide microarray data. Technometrics, 50, 241-264.
79. Kauffmann, A., Gentleman, R. and Huber, W. (2009) arrayQualityMetrics: a bioconductor package for quality assessment of microarray data. Bioinformatics, 25, 415-416.