The Role of the Double Bromodomain-Containing BET Genes During Mammalian Spermatogenesis

Current Topics in Developmental Biology

Volumn 102, Issue , 2013, Pages 293-326

  Berkovits, Binyamin D ^a   Wolgemuth, Debra J ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

BET family; Bromodomain; Chromatin remodeling; Chromocenter; Epigenetic marks; Heterochromatin euchromatin; Spermiogenesis; Transcription regulation

Indexed keywords

EID: 84871738453     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-416024-8.00011-8     Document Type: Chapter

References (149)

1. Agricola E., Randall R.A., Gaarenstroom T., Dupont S., Hill C.S. Recruitment of TIF1gamma to chromatin via its PHD finger-bromodomain activates its ubiquitin ligase and transcriptional repressor activities. Molecular Cell 2011, 43:85-96.
2. Ai N., Hu X., Ding F., Yu B., Wang H., Lu X., et al. Signal-induced Brd4 release from chromatin is essential for its role transition from chromatin targeting to transcriptional regulation. Nucleic Acids Research 2011, 39:9592-9604.
3. Allton K., Jain A.K., Herz H.M., Tsai W.W., Jung S.Y., Qin J., et al. Trim24 targets endogenous p53 for degradation. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:11612-11616.
4. Arrowsmith C.H., Bountra C., Fish P.V., Lee K., Schapira M. Epigenetic protein families: A new frontier for drug discovery. Nature Reviews. Drug Discovery 2012, 11:384-400.
5. Barboric M., Lenasi T., Chen H., Johansen E.B., Guo S., Peterlin B.M. 7SK snRNP/P-TEFb couples transcription elongation with alternative splicing and is essential for vertebrate development. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:7798-7803.
6. Barda S., Paz G., Yogev L., Yavetz H., Lehavi O., Hauser R., et al. Expression of BET genes in testis of men with different spermatogenic impairments. Fertility and Sterility 2012, 97(46-52):e5.
7. Barlev N.A., Liu L., Chehab N.H., Mansfield K., Harris K.G., Halazonetis T.D., et al. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Molecular Cell 2001, 8:1243-1254.
8. Beck S., Hanson I., Kelly A., Pappin D.J., Trowsdale J. A homologue of the Drosophila female sterile homeotic (fsh) gene in the class II region of the human MHC. DNA Sequence 1992, 2:203-210.
9. Berkovits B.D., Wang L., Guarnieri P., Wolgemuth D.J. The testis-specific double bromodomain-containing protein BRDT forms a complex with multiple spliceosome components and is required for mRNA splicing and 3'-UTR truncation in round spermatids. Nucleic Acids Research 2012, 40:7162-7175.
10. Berkovits B.D., Wolgemuth D.J. The first bromodomain of the testis-specific double bromodomain protein Brdt is required for chromocenter organization that is modulated by genetic background. Developmental Biology 2011, 360:358-368.
11. Bisgrove D.A., Mahmoudi T., Henklein P., Verdin E. Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:13690-13695.
12. Boekelheide K., Schoenfeld H.A. Spermatogenesis by Sisyphus: Proliferating stem germ cells fail to repopulate the testis after 'irreversible' injury. Advances in Experimental Medicine and Biology 2001, 500:421-428.
13. Bonde J.P. Male reproductive organs are at risk from environmental hazards. Asian Journal of Andrology 2010, 12:152-156.
14. Catena R., Ronfani L., Sassone-Corsi P., Davidson I. Changes in intranuclear chromatin architecture induce bipolar nuclear localization of histone variant H1T2 in male haploid spermatids. Developmental Biology 2006, 296:231-238.
15. Christensen M.E., Dixon G.H. Hyperacetylation of histone H4 correlates with the terminal, transcriptionally inactive stages of spermatogenesis in rainbow trout. Developmental Biology 1982, 93:404-415.
16. Chua P., Roeder G.S. Bdf1, a yeast chromosomal protein required for sporulation. Molecular and Cellular Biology 1995, 15:3685-3696.
17. Chung C.W., Coste H., White J.H., Mirguet O., Wilde J., Gosmini R.L., et al. Discovery and characterization of small molecule inhibitors of the BET family bromodomains. Journal of Medicinal Chemistry 2011, 54:3827-3838.
18. Chung S.S., Wang X., Roberts S.S., Griffey S.M., Reczek P.R., Wolgemuth D.J. Oral administration of a retinoic acid receptor antagonist reversibly inhibits spermatogenesis in mice. Endocrinology 2011, 152:2492-2502.
19. Clowney E.J., Magklara A., Colquitt B.M., Pathak N., Lane R.P., Lomvardas S. High-throughput mapping of the promoters of the mouse olfactory receptor genes reveals a new type of mammalian promoter and provides insight into olfactory receptor gene regulation. Genome Research 2011, 21:1249-1259.
20. Crowley T., Brunori M., Rhee K., Wang X., Wolgemuth D.J. Change in nuclear-cytoplasmic localization of a double-bromodomain protein during proliferation and differentiation of mouse spinal cord and dorsal root ganglia. Brain Research. Developmental Brain Research 2004, 149:93-101.
21. Das D., Scovell W.M. The binding interaction of HMG-1 with the TATA-binding protein/TATA complex. The Journal of Biological Chemistry 2001, 276:32597-32605.
22. Dawson M.A., Prinjha R.K., Dittman A., Giotopoulos G., Bantscheff M., Chan W.I., et al. Inhibition of BET recruitment to chromatin as an effective treatment for MLL-fusion leukaemia. Nature 2011, 478:529-533.
23. Delmore J.E., Issa G.C., Lemieux M.E., Rahl P.B., Shi J., Jacobs H.M., et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011, 146:904-917.
24. Denis G.V. Bromodomain coactivators in cancer, obesity, type 2 diabetes, and inflammation. Discovery Medicine 2010, 10:489-499.
25. Denis G.V., Vaziri C., Guo N., Faller D.V. RING3 kinase transactivates promoters of cell cycle regulatory genes through E2F. Cell Growth & Differentiation 2000, 11:417-424.
26. Dey A., Ellenberg J., Farina A., Coleman A.E., Maruyama T., Sciortino S., et al. A bromodomain protein, MCAP, associates with mitotic chromosomes and affects G(2)-to-M transition. Molecular and Cellular Biology 2000, 20:6537-6549.
27. Dey A., Nishiyama A., Karpova T., McNally J., Ozato K. Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Molecular Biology of the Cell 2009, 20:4899-4909.
28. Dhar S., Thota A., Rao M.R. Insights into role of bromodomain, testis-specific (Brdt) in acetylated histone H4-dependent chromatin remodeling in mammalian spermiogenesis. The Journal of Biological Chemistry 2012, 287:6387-6405.
29. Durant M., Pugh B.F. NuA4-directed chromatin transactions throughout the Saccharomyces cerevisiae genome. Molecular and Cellular Biology 2007, 27:5327-5335.
30. Elliott D.J., Grellscheid S.N. Alternative RNA splicing regulation in the testis. Reproduction 2006, 132:811-819.
31. Fantz D.A., Hatfield W.R., Horvath G., Kistler M.K., Kistler W.S. Mice with a targeted disruption of the H1t gene are fertile and undergo normal changes in structural chromosomal proteins during spermiogenesis. Biology of Reproduction 2001, 64:425-431.
32. Filippakopoulos P., Qi J., Picaud S., Shen Y., Smith W.B., Fedorov O., et al. Selective inhibition of BET bromodomains. Nature 2010, 468:1067-1073.
33. Florence B., Faller D.V. You bet-cha: A novel family of transcriptional regulators. Frontiers in Bioscience 2001, 6:D1008-D1018.
34. Florence B.L., Faller D.V. Drosophila female sterile (1) homeotic is a multifunctional transcriptional regulator that is modulated by Ras signaling. Developmental Dynamics 2008, 237:554-564.
35. French C.A. NUT midline carcinoma. Cancer Genetics and Cytogenetics 2010, 203:16-20.
36. Gamsjaeger R., Webb S.R., Lamonica J.M., Billin A., Blobel G.A., Mackay J.P. Structural basis and specificity of acetylated transcription factor GATA1 recognition by BET family bromodomain protein Brd3. Molecular and Cellular Biology 2011, 31:2632-2640.
37. Gans M., Audit C., Masson M. Isolation and characterization of sex-linked female-sterile mutants in Drosophila melanogaster. Genetics 1975, 81:683-704.
38. Gans M., Forquignon F., Masson M. The role of dosage of the region 7D1-7D5-6 of the X chromosome in the production of homeotic transformations in Drosophila melanogaster. Genetics 1980, 96:887-902.
39. Gatewood J.M., Cook G.R., Balhorn R., Schmid C.W., Bradbury E.M. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. The Journal of Biological Chemistry 1990, 265:20662-20666.
40. Govin J., Caron C., Lestrat C., Rousseaux S., Khochbin S. The role of histones in chromatin remodelling during mammalian spermiogenesis. European Journal of Biochemistry 2004, 271:3459-3469.
41. Govin J., Lestrat C., Caron C., Pivot-Pajot C., Rousseaux S., Khochbin S. Histone acetylation-mediated chromatin compaction during mouse spermatogenesis. Ernst Schering Research Foundation Workshop 2006, 57:155-172.
42. Gregory G.D., Vakoc C.R., Rozovskaia T., Zheng X., Patel S., Nakamura T., et al. Mammalian ASH1L is a histone methyltransferase that occupies the transcribed region of active genes. Molecular and Cellular Biology 2007, 27:8466-8479.
43. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997, 389:349-352.
44. Guo N., Faller D.V., Denis G.V. Activation-induced nuclear translocation of RING3. Journal of Cell Science 2000, 113:3085-3091.
45. Haaf T., Ward D.C. Higher order nuclear structure in mammalian sperm revealed by in situ hybridization and extended chromatin fibers. Experimental Cell Research 1995, 219:604-611.
46. Hammoud S.S., Nix D.A., Zhang H., Purwar J., Carrell D.T., Cairns B.R. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009, 460:473-478.
47. Hargreaves D.C., Horng T., Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009, 138:129-145.
48. Haynes S.R., Dollard C., Winston F., Beck S., Trowsdale J., Dawid I.B. The bromodomain: A conserved sequence found in human, Drosophila and yeast proteins. Nucleic Acids Research 1992, 20:2603.
49. Haynes S.R., Mozer B.A., Bhatia-Dey N., Dawid I.B. The Drosophila fsh locus, a maternal effect homeotic gene, encodes apparent membrane proteins. Developmental Biology 1989, 134:246-257.
50. Hazzouri M., Pivot-Pajot C., Faure A.K., Usson Y., Pelletier R., Sele B., et al. Regulated hyperacetylation of core histones during mouse spermatogenesis: Involvement of histone deacetylases. European Journal of Cell Biology 2000, 79:950-960.
51. He Z., Kokkinaki M., Pant D., Gallicano G.I., Dym M. Small RNA molecules in the regulation of spermatogenesis. Reproduction 2009, 137:901-911.
52. Hess J.L. MLL: A histone methyltransferase disrupted in leukemia. Trends in Molecular Medicine 2004, 10:500-507.
53. Hewings D.S., Wang M., Philpott M., Fedorov O., Uttarkar S., Filippakopoulos P., et al. 3,5-dimethylisoxazoles act as acetyl-lysine-mimetic bromodomain ligands. Journal of Medicinal Chemistry 2011, 54:6761-6770.
54. Houzelstein D., Bullock S.L., Lynch D.E., Grigorieva E.F., Wilson V.A., Beddington R.S. Growth and early postimplantation defects in mice deficient for the bromodomain-containing protein Brd4. Molecular and Cellular Biology 2002, 22:3794-3802.
55. Hoyer-Fender S., Singh P.B., Motzkus D. The murine heterochromatin protein M31 is associated with the chromocenter in round spermatids and Is a component of mature spermatozoa. Experimental Cell Research 2000, 254:72-79.
56. Huang D.H., Dawid I.B. The maternal-effect gene fsh is essential for the specification of the central region of the Drosophila embryo. The New Biologist 1990, 2:163-170.
57. Huang H., Zhang J., Shen W., Wang X., Wu J., Wu J., et al. Solution structure of the second bromodomain of Brd2 and its specific interaction with acetylated histone tails. BMC Structural Biology 2007, 7:57.
58. Idler R.K., Yan W. Control of messenger RNA fate by RNA binding proteins: An emphasis on mammalian spermatogenesis. Journal of Andrology 2012, 33:309-337.
59. Jacobson R.H., Ladurner A.G., King D.S., Tjian R. Structure and function of a human TAFII250 double bromodomain module. Science 2000, 288:1422-1425.
60. Jang M.K., Mochizuki K., Zhou M., Jeong H.S., Brady J.N., Ozato K. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Molecular Cell 2005, 19:523-534.
61. Jeanmougin F., Wurtz J.M., Le Douarin B., Chambon P., Losson R. The bromodomain revisited. Trends in Biochemical Sciences 1997, 22:151-153.
62. Jones M.H., Numata M., Shimane M. Identification and characterization of BRDT: A testis-specific gene related to the bromodomain genes RING3 and Drosophila fsh. Genomics 1997, 45:529-534.
63. Kanno T., Kanno Y., Siegel R.M., Jang M.K., Lenardo M.J., Ozato K. Selective recognition of acetylated histones by bromodomain proteins visualized in living cells. Molecular Cell 2004, 13:33-43.
64. Kennedy B.P., Davies P.L. Acid-soluble nuclear proteins of the testis during spermatogenesis in the winter flounder. Loss of the high mobility group proteins. The Journal of Biological Chemistry 1980, 255:2533-2539.
65. Kierszenbaum A.L., Rivkin E., Tres L.L. Cytoskeletal track selection during cargo transport in spermatids is relevant to male fertility. Spermatogenesis 2011, 1:221-230.
66. Ladurner A.G., Inouye C., Jain R., Tjian R. Bromodomains mediate an acetyl-histone encoded antisilencing function at heterochromatin boundaries. Molecular Cell 2003, 11:365-376.
67. Lamonica J.M., Deng W., Kadauke S., Campbell A.E., Gamsjaeger R., Wang H., et al. Bromodomain protein Brd3 associates with acetylated GATA1 to promote its chromatin occupancy at erythroid target genes. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:E159-E168.
68. Lenasi T., Barboric M. P-TEFb stimulates transcription elongation and pre-mRNA splicing through multilateral mechanisms. RNA Biology 2010, 7:145-150.
69. Lenasi T., Peterlin B.M., Barboric M. Cap-binding protein complex links pre-mRNA capping to transcription elongation and alternative splicing through positive transcription elongation factor b (P-TEFb). The Journal of Biological Chemistry 2011, 286:22758-22768.
70. LeRoy G., Rickards B., Flint S.J. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Molecular Cell 2008, 30:51-60.
71. Lewis J.D., Abbott D.W., Ausio J. A haploid affair: Core histone transitions during spermatogenesis. Biochemistry and Cell Biology 2003, 81:131-140.
72. Liang Q., Deng H., Li X., Wu X., Tang Q., Chang T.H., et al. Tripartite motif-containing protein 28 is a small ubiquitin-related modifier E3 ligase and negative regulator of IFN regulatory factor 7. The Journal of Immunology 2011, 187:4754-4763.
73. Licatalosi D.D., Geiger G., Minet M., Schroeder S., Cilli K., McNeil J.B., et al. Functional interaction of yeast pre-mRNA 3' end processing factors with RNA polymerase II. Molecular Cell 2002, 9:1101-1111.
74. Lin S., Coutinho-Mansfield G., Wang D., Pandit S., Fu X.D. The splicing factor SC35 has an active role in transcriptional elongation. Nature Structural & Molecular Biology 2008, 15:819-826.
75. Lin Q., Sirotkin A., Skoultchi A.I. Normal spermatogenesis in mice lacking the testis-specific linker histone H1t. Molecular and Cellular Biology 2000, 20:2122-2128.
76. Liu D., Brockman J.M., Dass B., Hutchins L.N., Singh P., McCarrey J.R., et al. Systematic variation in mRNA 3'-processing signals during mouse spermatogenesis. Nucleic Acids Research 2007, 35:234-246.
77. Liu H., Mulholland N., Fu H., Zhao K. Cooperative activity of BRG1 and Z-DNA formation in chromatin remodeling. Molecular and Cellular Biology 2006, 26:2550-2559.
78. Lu L.Y., Wu J., Ye L., Gavrilina G.B., Saunders T.L., Yu X. RNF8-dependent histone modifications regulate nucleosome removal during spermatogenesis. Developmental Cell 2010, 18:371-384.
79. Lygerou Z., Conesa C., Lesage P., Swanson R.N., Ruet A., Carlson M., et al. The yeast BDF1 gene encodes a transcription factor involved in the expression of a broad class of genes including snRNAs. Nucleic Acids Research 1994, 22:5332-5340.
80. Martianov I., Brancorsini S., Catena R., Gansmuller A., Kotaja N., Parvinen M., et al. Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:2808-2813.
81. Martianov I., Brancorsini S., Gansmuller A., Parvinen M., Davidson I., Sassone-Corsi P. Distinct functions of TBP and TLF/TRF2 during spermatogenesis: Requirement of TLF for heterochromatic chromocenter formation in haploid round spermatids. Development (Cambridge, England) 2002, 129:945-955.
82. Martinson H.G. An active role for splicing in 3'-end formation. Wiley Interdisciplinary Reviews: RNA 2011, 2:459-470.
83. Matangkasombut O., Buratowski R.M., Swilling N.W., Buratowski S. Bromodomain factor 1 corresponds to a missing piece of yeast TFIID. Genes & Development 2000, 14:951-962.
84. Meistrich M.L. Critical components of testicular function and sensitivity to disruption. Biology of Reproduction 1986, 34:17-28.
85. Meistrich M.L. Effects of chemotherapy and radiotherapy on spermatogenesis. European Urology 1993, 23:136-141. discussion 142.
86. Meistrich M.L., Mohapatra B., Shirley C.R., Zhao M. Roles of transition nuclear proteins in spermiogenesis. Chromosoma 2003, 111:483-488.
87. Meistrich M.L., Trostle-Weige P.K., Lin R., Bhatnagar Y.M., Allis C.D. Highly acetylated H4 is associated with histone displacement in rat spermatids. Molecular Reproduction and Development 1992, 31:170-181.
88. Mertz J.A., Conery A.R., Bryant B.M., Sandy P., Balasubramanian S., Mele D.A., et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:16669-16674.
89. Meyer-Ficca M., Muller-Navia J., Scherthan H. Clustering of pericentromeres initiates in step 9 of spermiogenesis of the rat (Rattus norvegicus) and contributes to a well defined genome architecture in the sperm nucleus. Journal of Cell Science 1998, 111(Pt 10):1363-1370.
90. Miki K., Qu W., Goulding E.H., Willis W.D., Bunch D.O., Strader L.F., et al. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16501-16506.
91. Mishima Y., Miyagi S., Saraya A., Negishi M., Endoh M., Endo T.A., et al. The Hbo1-Brd1/Brpf2 complex is responsible for global acetylation of H3K14 and required for fetal liver erythropoiesis. Blood 2011, 118:2443-2453.
92. Moriniere J., Rousseaux S., Steuerwald U., Soler-Lopez M., Curtet S., Vitte A.L., et al. Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 2009, 461:664-668.
93. Mujtaba S., Zeng L., Zhou M.M. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 2007, 26:5521-5527.
94. Nicodeme E., Jeffrey K.L., Schaefer U., Beinke S., Dewell S., Chung C.W., et al. Suppression of inflammation by a synthetic histone mimic. Nature 2010, 468:1119-1123.
95. Nishiyama A., Dey A., Miyazaki J., Ozato K. Brd4 is required for recovery from antimicrotubule drug-induced mitotic arrest: Preservation of acetylated chromatin. Molecular Biology of the Cell 2006, 17:814-823.
96. O'Carroll D., Scherthan H., Peters A.H., Opravil S., Haynes A.R., Laible G., et al. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Molecular and Cellular Biology 2000, 20:9423-9433.
97. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87:953-959.
98. Ohshima T., Suganuma T., Ikeda M. A novel mutation lacking the bromodomain of the transcriptional coactivator p300 in the SiHa cervical carcinoma cell line. Biochemical and Biophysical Research Communications 2001, 281:569-575.
99. Owen D.J., Ornaghi P., Yang J.C., Lowe N., Evans P.R., Ballario P., et al. The structural basis for the recognition of acetylated histone H4 by the bromodomain of histone acetyltransferase gcn5p. The EMBO Journal 2000, 19:6141-6149.
100. Paillisson A., Levasseur A., Gouret P., Callebaut I., Bontoux M., Pontarotti P., et al. Bromodomain testis-specific protein is expressed in mouse oocyte and evolves faster than its ubiquitously expressed paralogs BRD2, -3, and -4. Genomics 2007, 89:215-223.
101. Peng J., Dong W., Chen L., Zou T., Qi Y., Liu Y. Brd2 is a TBP-associated protein and recruits TBP into E2F-1 transcriptional complex in response to serum stimulation. Molecular and Cellular Biochemistry 2007, 294:45-54.
102. Petrelli G., Figa-Talamanca I. Reduction in fertility in male greenhouse workers exposed to pesticides. European Journal of Epidemiology 2001, 17:675-677.
103. Pittoggi C., Magnano A.R., Sciamanna I., Giordano R., Lorenzini R., Spadafora C. Specific localization of transcription factors in the chromatin of mouse mature spermatozoa. Molecular Reproduction and Development 2001, 60:97-106.
104. Pivot-Pajot C., Caron C., Govin J., Vion A., Rousseaux S., Khochbin S. Acetylation-dependent chromatin reorganization by BRDT, a testis-specific bromodomain-containing protein. Molecular and Cellular Biology 2003, 23:5354-5365.
105. Plaseski T., Noveski P., Popeska Z., Efremov G.D., Plaseska-Karanfilska D. Association study of single nucleotide polymorphisms in FASLG, JMJDIA, LOC203413, TEX15, BRDT, OR2W3, INSR and TAS2R38 genes with male infertility. Journal of Andrology 2011, 33:675-683.
106. Platt G.M., Simpson G.R., Mittnacht S., Schulz T.F. Latent nuclear antigen of Kaposi's sarcoma-associated herpesvirus interacts with RING3, a homolog of the Drosophila female sterile homeotic (fsh) gene. Journal of Virology 1999, 73:9789-9795.
107. Potashnik G., Ben-Aderet N., Israeli R., Yanai-Inbar I., Sober I. Suppressive effect of 1,2-dibromo-3-chloropropane on human spermatogenesis. Fertility and Sterility 1978, 30:444-447.
108. Racki L.R., Yang J.G., Naber N., Partensky P.D., Acevedo A., Purcell T.J., et al. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 2009, 462:1016-1021.
109. Rahman S., Sowa M.E., Ottinger M., Smith J.A., Shi Y., Harper J.W., et al. The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3. Molecular and Cellular Biology 2011, 31:2641-2652.
110. Rhee K., Brunori M., Besset V., Trousdale R., Wolgemuth D.J. Expression and potential role of Fsrg1, a murine bromodomain-containing homologue of the Drosophila gene female sterile homeotic. Journal of Cell Science 1998, 111:3541-3550.
111. Ronfani L., Ferraguti M., Croci L., Ovitt C.E., Scholer H.R., Consalez G.G., et al. Reduced fertility and spermatogenesis defects in mice lacking chromosomal protein Hmgb2. Development (Cambridge, England) 2001, 128:1265-1273.
112. Sanchez R., Zhou M.M. The role of human bromodomains in chromatin biology and gene transcription. Current Opinion in Drug Discovery & Development 2009, 12:659-665.
113. Sankar N., Baluchamy S., Kadeppagari R.K., Singhal G., Weitzman S., Thimmapaya B. p300 provides a corepressor function by cooperating with YY1 and HDAC3 to repress c-Myc. Oncogene 2008, 27:5717-5728.
114. Schotta G., Ebert A., Reuter G. SU(VAR)3-9 is a conserved key function in heterochromatic gene silencing. Genetica 2003, 117:149-158.
115. Schroder S., Cho S., Zeng L., Zhang Q., Kaehlcke K., Mak L., et al. Two-pronged binding with bromodomain-containing protein 4 liberates positive transcription elongation factor b from inactive ribonucleoprotein complexes. The Journal of Biological Chemistry 2012, 287:1090-1099.
116. Shang E., Cui Q., Wang X., Beseler C., Greenberg D.A., Wolgemuth D.J. The bromodomain-containing gene BRD2 is regulated at transcription, splicing, and translation levels. Journal of Cellular Biochemistry 2011, 112:2784-2793.
117. Shang E., Nickerson H.D., Wen D., Wang X., Wolgemuth D.J. 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 (Cambridge, England) 2007, 134:3507-3515.
118. Shang E., Salazar G., Crowley T., Wang X., Lopez R.A., Wang X., et al. Identification of unique, differentiation stage-specific patterns of expression of the bromodomain-containing genes Brd2, Brd3, Brd4, and Brdt in the mouse testis. Gene Expression Patterns 2004, 4:513-519.
119. Shang E., Wang X., Wen D., Greenberg D.A., Wolgemuth D.J. Double bromodomain-containing gene Brd2 is essential for embryonic development in mouse. Developmental Dynamics 2009, 238:908-917.
120. Shankaranarayana G.D., Motamedi M.R., Moazed D., Grewal S.I. Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast. Current Biology 2003, 13:1240-1246.
121. Shogren-Knaak M., Ishii H., Sun J.M., Pazin M.J., Davie J.R., Peterson C.L. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
122. Singh S.R., Burnicka-Turek O., Chauhan C., Hou S.X. Spermatogonial stem cells, infertility and testicular cancer. Journal of Cellular and Molecular Medicine 2011, 15:468-483.
123. Sinha A., Faller D.V., Denis G.V. Bromodomain analysis of Brd2-dependent transcriptional activation of cyclin A. The Biochemical Journal 2005, 387:257-269.
124. Steger K. Haploid spermatids exhibit translationally repressed mRNAs. Anatomy and Embryology 2001, 203:323-334.
125. Suka N., Suka Y., Carmen A.A., Wu J., Grunstein M. Highly specific antibodies determine histone acetylation site usage in yeast heterochromatin and euchromatin. Molecular Cell 2001, 8:473-479.
126. Tae S., Karkhanis V., Velasco K., Yaneva M., Erdjument-Bromage H., Tempst P., et al. Bromodomain protein 7 interacts with PRMT5 and PRC2, and is involved in transcriptional repression of their target genes. Nucleic Acids Research 2011, 39:5424-5438.
127. Tamkun J.W. The role of brahma and related proteins in transcription and development. Current Opinion in Genetics & Development 1995, 5:473-477.
128. Tamkun J.W., Deuring R., Scott M.P., Kissinger M., Pattatucci A.M., Kaufman T.C., et al. brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 1992, 68:561-572.
129. Taniguchi Y., Matsuzaka Y., Fujimoto H., Miyado K., Kohda A., Okumura K., et al. Nucleotide sequence of the ring3 gene in the class II region of the mouse MHC and its abundant expression in testicular germ cells. Genomics 1998, 51:114-123.
130. Taniguchi Y., Suzuki H., Ohtsuka M., Kikuchi N., Kimura M., Inoko H. Isolation and characterization of three genes paralogous to mouse Ring3. Nucleic Acids Research. Supplement 2001, 1:247-248.
131. Thompson M. Polybromo-1: The chromatin targeting subunit of the PBAF complex. Biochimie 2009, 91:309-319.
132. Thorpe K.L., Gorman P., Thomas C., Sheer D., Trowsdale J., Beck S. Chromosomal localization, gene structure and transcription pattern of the ORFX gene, a homologue of the MHC-linked RING3 gene. Gene 1997, 200:177-183.
133. Trousdale R.K., Wolgemuth D.J. Bromodomain containing 2 (Brd2) is expressed in distinct patterns during ovarian folliculogenesis independent of FSH or GDF9 action. Molecular Reproduction and Development 2004, 68:261-268.
134. Wang R., Li Q., Helfer C.M., Jiao J., You J. The bromodomain protein Brd4 associated with acetylated chromatin is important for maintenance of higher-order chromatin structure. The Journal of Biological Chemistry 2012, 287:10738-10752.
135. Wang L., Mizzen C., Ying C., Candau R., Barlev N., Brownell J., et al. Histone acetyltransferase activity is conserved between yeast and human GCN5 and is required for complementation of growth and transcriptional activation. Molecular and Cellular Biology 1997, 17:519-527.
136. Wilson B.G., Roberts C.W. SWI/SNF nucleosome remodellers and cancer. Nature Reviews. Cancer 2011, 11:481-492.
137. Wolf K.W., Jeppesen P., Mitchell A. Spermatid nucleus of Megaselia scalaris Loew (Insecta, Diptera, Phoridae): A study using anti-histone antibodies, scanning electron microscopy, and a centromere-specific oligonucleotide. Molecular Reproduction and Development 1993, 35:272-276.
138. Wu S.Y., Chiang C.M. The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation. The Journal of Biological Chemistry 2007, 282:13141-13145.
139. Xiao A., Li H., Shechter D., Ahn S.H., Fabrizio L.A., Erdjument-Bromage H., et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 2009, 457:57-62.
140. Yang X.J. Lysine acetylation and the bromodomain: A new partnership for signaling. Bioessays 2004, 26:1076-1087.
141. Yang Z., He N., Zhou Q. Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression. Molecular and Cellular Biology 2008, 28:967-976.
142. Yang Z., Yik J.H., Chen R., He N., Jang M.K., Ozato K., et al. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Molecular Cell 2005, 19:535-545.
143. Yeo G., Holste D., Kreiman G., Burge C.B. Variation in alternative splicing across human tissues. Genome Biology 2004, 5:R74.
144. Yu Z., Raabe T., Hecht N.B. MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biology of Reproduction 2005, 73:427-433.
145. Zalensky A.O., Allen M.J., Kobayashi A., Zalenskaya I.A., Balhorn R., Bradbury E.M. Well-defined genome architecture in the human sperm nucleus. Chromosoma 1995, 103:577-590.
146. Zeng L., Yap K.L., Ivanov A.V., Wang X., Mujtaba S., Plotnikova O., et al. Structural insights into human KAP1 PHD finger-bromodomain and its role in gene silencing. Nature Structural & Molecular Biology 2008, 15:626-633.
147. Zhang G., Liu R., Zhong Y., Plotnikov A.N., Zhang W., Zeng L., et al. Down-regulation of NF-kappaB transcriptional activity in HIV-associated kidney disease by BRD4 inhibition. The Journal of Biological Chemistry 2012, 287:28840-28851.
148. Zheng Y., Yuan W., Zhou Z., Xu M., Sha J.H. Molecular cloning and expression of a novel alternative splice variant of BRDT gene. International Journal of Molecular Medicine 2005, 15:315-321.
149. Zhou Y., Grummt I. The PHD finger/bromodomain of NoRC interacts with acetylated histone H4K16 and is sufficient for rDNA silencing. Current Biology 2005, 15:1434-1438.