Wake-up-call, a lin-52 paralogue, and Always early, a lin-9 homologue physically interact, but have opposing functions in regulating testis-specific gene expression

Developmental Biology

Volumn 355, Issue 2, 2011, Pages 381-393

  Doggett, Karen ^a,c   Jiang, Jianqiao ^b   Aleti, Gajender ^b   White Cooper, Helen ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Drosophila; Male fertility; Testis gene expression; Transcription

Indexed keywords

ALWAYS EARLY PROTEIN; DROSOPHILA PROTEIN; UNCLASSIFIED DRUG; WAKE UP CALL PROTEIN;

ALY GENE; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOSS; GENE REPRESSION; GENE TARGETING; GENETIC SIMILARITY; MALE; NONHUMAN; PARALOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPRESSOR GENE; SEQUENCE HOMOLOGY; SPERMATOGENESIS; TESTIS; WUC GENE;

EID: 79959207002     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.04.030     Document Type: Article

References (41)

1. Ayyar S., Jiang J., Collu A., White-Cooper H., White R. Drosophila TGIF is essential for developmentally regulated transcription in spermatogenesis. Development 2003, 130:2841-2852.
2. Beall E.L., Bell M., Georlette D., Botchan M.R. Dm-myb mutant lethality in Drosophila is dependent on mip130: positive and negative regulation of DNA replication. Genes Dev. 2004, 18:1667-1680.
3. Beall E.L., Lewis P.W., Bell M., Rocha M., Jones D.L., Botchan M. Discovery of tMAC: a Drosophila testis-specific meiotic arrest complex paralogous to Myb-MuvB. Genes Dev. 2007, 21:904-919.
4. Bhatt A.M., Zhang Q., Harris S.A., White-Cooper H., Dickinson H. Gene structure and molecular analysis of Arabidopsis thaliana ALWAYS EARLY homologs. Gene 2004, 336:219-229.
5. Brawley C., Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 2004, 304:1331-1334.
6. Chen D., McKearin D.M. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 2003, 130:1159-1170.
7. Chen X., Hiller M.A., Sancak Y., Fuller M.T. Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation. Science 2005, 310:869-872.
8. Chintapalli V., Wang J., Dow J. Using FlyAtlas to identify better Drosophila models of human disease. Nat. Genet. 2007, 39:715-720.
9. Cui M., Chen J., Myers T., Hwang B.J., Sternberg P.W., Greenwald I., Han M. SynMuv genes redundantly inhibit lin-3/EGF expression to prevent inappropriate vulval induction in C. elegans. Dev. Cell 2006, 10:667-672.
10. Dietzl G., Chen D., Schnorrer F., Su K., Barinova Y., Fellner M., Gasser B., Kinsey K., Oppel S., Scheiblauer S., Couto A., Marra V., Keleman K., Dickson B.J. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 2007, 448:151-156.
11. Eggert U.S., Kiger A.A., Richter C., Perlman Z.E., Perrimon N., Mitchison T.J., Field C.M. Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets. PLoS Biol. 2004, 2:e379.
12. Georlette D., Ahn A., MacAlpine D., Cheung E., Lewis P.W., Beall E.L., Bell S.P., Speed T., Manak J.R., Botchan M. Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb-MuvB/dREAM complex in proliferating cells. Genes Dev. 2007, 21:2880-2896.
13. Goshima G., Wollman R., Goodwin S.S., Zhang N., Scholey J.M., Vale R.D., Stuurman N. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 2007, 316:417-421.
14. Harrison M., Coel C.J., Lu X., Horvitz H.R. Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16782-16787.
15. Hiller M.A., Lin T.-Y., Wood C., Fuller M.T. Developmental regulation of transcription by a tissue-specific TAF homolog. Genes Dev. 2001, 15:1021-1030.
16. Hiller M.A., Chen X., Pringle M.J., Suchorolski M., Sancak Y., Viswanathan S., Bolival B., Lin T.-Y., Marino S., Fuller M.T. Testis-specific TAF homologs collaborate to control a tissue-specific transcription program. Development 2004, 131:5297-5308.
17. Jiang J., White-Cooper H. Transcriptional activation in Drosophila spermatogenesis involves the mutually dependent function of aly and a novel meiotic arrest gene cookie monster. Development 2003, 130:563-573.
18. Jiang J., Benson E., Bausek N., Doggett K., White-Cooper H. Tombola, a tesmin/TSO1 family protein, regulates transcriptional activation in the Drosophila male germline and physically interacts with Always early. Development 2007, 134:1549-1559.
19. Kittler R., Pelletier L., Heninger A.-K., Slabicki M., Theis M., Miroslaw L., Poser I., Lawo S., Grabner H., Kozak K., Wagner J., Surendranath V., Richter C., Bowen W., Jackson A., Habermann B., Hyman A., Buchholz F. Genome-scale RNAi profiling of cell division in human tissue culture cells. Nat. Cell Biol. 2007, 9:1401-1412.
20. Knight A., Notaridou M., Watson R.J. A Lin-9 complex is recruited by B-Myb to activate transcription of G2/M genes in undifferentiated embryonal carcinoma cells. Oncogene 2009, 28:1737-1747.
21. Korenjak M., Taylor-Harding B., Binne U.K., Satterlee J.S., Stevaux O., Aasland R., White-Cooper H., Dyson N., Brehm A. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 2004, 119:181-193.
22. Kwon S., Xiao H., Wu C., Badenhorst P. Alternative splicing of NURF301 generates distinct NURF chromatin remodelling complexes with altered modified histone binding specificities. PLoS Genet. 2009, 5:e1000574.
23. Lewis P.W., Beall E.L., Fleischer T.C., Georlette D., Link A.J., Botchan M. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev. 2004, 18.
24. Lin T.-Y., Viswanathan S., Wood C., Wilson P.G., Wolf N., Fuller M.T. Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophila males. Development 1996, 122:1331-1341.
25. Litovchick L., Sadasivam S., Florens L., Zhu X., Swanson S., Velmurugan S., Chen R., Washburn M., Liu X., DeCaprio J. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 2007, 26:539-551.
26. Metcalf C., Wassarman D.A. Nucleolar colocalisation of TAF1 and testis-specific TAFs during Drosophila spermatogenesis. Dev. Dyn. 2007, 236:2836-2843.
27. Morris C., Benson E., White-Cooper H. Determination of gene expression patterns using in situ hybridization to Drosophila testes. Nat. Protoc. 2009, 4:1807-1819.
28. Orihara-Ono M., Suzuki A., Saito M., Yoda Y., Aigaki T., Hama C. The slender lobes gene, identified by retarded mushroom body development, is required for proper nucleolar organisation in Drosophila. Dev. Biol. 2005, 281:121-133.
29. Parker L., Gross S., Alphey L. Vectors for the expression of tagged proteins in Drosophila. Biotechniques 2001, 31:1280-1286.
30. Perezgazga L., Jiang J., Bolival B., Hiller M.A., Benson E., Fuller M.T., White-Cooper H. Regulation of transcription of meiotic cell cycle and terminal differentiation genes by the testis-specific Zn finger protein matotopetli. Development 2004, 131:1691-1702.
31. Reddien P., Andersen E., Huang M., Horvitz H.R. DPL-1 DP, LIN-35 Rb and EFL-1 E2F acti with the MCD-1 zinc-finger protein to promote programmed cell death in Caenorhabditis elegans. Genetics 2007, 175:1719-1733.
32. Schmit F., Korenjak M., Mannefeld M., Schmitt K., Franke C., von Eyss B., Gagrica S., Hanel F., Brehm A., Gaubatz S. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 2007, 6:1903-1913.
33. Solari F., Ahringer J. NURD-complex genes antagonise Ras-inducted vulval development in Caenorhabditis elegans. Curr. Biol. 2000, 10:223-226.
34. Tweedie S., Ashburner M., Falls K., Leyland P., McQuilton P., Marygold S., Millburn G., Osumi-Sutherland D., Schroeder A., Seal R., Zhang H., Consortium F. FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res. 2009, 37:D555-D559.
35. Wang Z., Mann R.S. Requirement for two nearly identical TGIF-related homeobox genes in Drosophila spermatogensis. Development 2003, 130:2853-2865.
36. Wen H., Andrejka L., Ashton J., Karess R., Lipsick J.S. Epigenetic regulation of gene expression by Drosophila Myb and E2F2-RBF via the Myb-MuvB/dREAM complex. Genes Dev. 2008, 22:601-614.
37. White-Cooper H. Spermatogenesis: analysis of meiosis and morphogenesis. Drosophila Cytogenetics Protocols 2004, 45-75. Humana Press, Totowa, New Jersey. D. Henderson (Ed.).
38. White-Cooper H. Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction 2010, 139:11-21.
39. White-Cooper H., Schafer M.A., Alphey L.S., Fuller M.T. Transcriptional and post-transcriptional control mechanisms coordinate the onset of spermatid differentiation with meiosis I in Drosophila. Development 1998, 125:125-134.
40. White-Cooper H., Leroy D., MacQueen A., Fuller M.T. Transcription of meiotic cell cycle and terminal differentiation genes depends on a conserved chromatin associated protein, whose nuclear localisation is regulated. Development 2000, 127:5463-5473.
41. Zhao J., Klyne G., Benson E., Gudmannsdottir E., White-Cooper H., Shotton D. FlyTED: the Drosophila testis gene expression database. Nucleic Acids Res. 2010, 38:D710-D715.