Transcriptional activation inDrosophilaspermatogenesis involves the mutually dependent function ofalyand a novel meiotic arrest genecookie monster

Jiang, Jiahua; White-Cooper, Helen

doi:10.1242/dev.00246

Cited by 58 publications

(64 citation statements)

References 33 publications

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“…Drosophila strains are described previously (Ayyar et al, 2003;Gonczy et al, 1997;Hiller et al, 2004;Hiller et al, 2001;Jiang et al, 2007;Jiang and White-Cooper, 2003;Lin et al, 1996;McKearin and Ohlstein, 1995;McKearin and Spradling, 1990;Perezgasga et al, 2004;White-Cooper et al, 2000;White-Cooper et al, 1998 -/-clones were induced by FLP recombinase that was exclusively expressed in germ cells using the germline-specific nos-GAL4 driver with a UAS-FLP transgene in males of genotype nos-GAL4/Y; UAS-FLP; E(z) 731 FRT2A/GFP3-13-7 FRT2A.…”

Section: Fly Strains and Husbandrymentioning

confidence: 99%

“…In spermatocytes, a dramatic, cell type-specific transcription program is initiated in preparation for subsequent spermatid differentiation. This transcription program requires the cooperative activity of spermatocyte-specific homologs of components of the core transcription factor TF II D complex (the tTAFs) Hiller et al, 2001;Lin et al, 1996), as well as the testisspecific meiotic arrest (tMAC) complex, which resembles the mammalian MIP/dREAM (Drosophila RB, E2F and Myb) and the C. elegans SynMuv complexes (Ayyar et al, 2003;Beall et al, 2007;Jiang et al, 2007;Jiang and White-Cooper, 2003;Perezgasga et al, 2004;White-Cooper et al, 2000;White-Cooper et al, 1998). Expression of the tTAFs and testis-specific components of the tMAC complex, such as always early (aly), is turned on for the first time in spermatocytes, early in the G2 phase of meiosis I (WhiteCooper et al, 2000;Hiller et al, 2001;Hiller et al, 2004;Chen et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Sequential changes at differentiation gene promoters as they become active in a stem cell lineage

Chen

Prado

et al. 2011

Development

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SUMMARYTranscriptional silencing of terminal differentiation genes by the Polycomb group (PcG) machinery is emerging as a key feature of precursor cells in stem cell lineages. How, then, is this epigenetic silencing reversed for proper cellular differentiation? Here, we investigate how the developmental program reverses local PcG action to allow expression of terminal differentiation genes in the Drosophila male germline stem cell (GSC) lineage. We find that the silenced state, set up in precursor cells, is relieved through developmentally regulated sequential events at promoters once cells commit to spermatocyte differentiation. The programmed events include global downregulation of Polycomb repressive complex 2 (PRC2) components, recruitment of hypophosphorylated RNA polymerase II (Pol II) to promoters, as well as the expression and action of testis-specific homologs of TATA-binding proteinassociated factors (tTAFs). In addition, action of the testis-specific meiotic arrest complex (tMAC), a tissue-specific version of the MIP/dREAM complex, is required both for recruitment of tTAFs to target differentiation genes and for proper cell type-specific localization of PRC1 components and tTAFs within the spermatocyte nucleolus. Together, the action of the tMAC and tTAF cell type-specific chromatin and transcription machinery leads to loss of Polycomb and release of stalled Pol II from the terminal differentiation gene promoters, allowing robust transcription.

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Section: Fly Strains and Husbandrymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Sequential changes at differentiation gene promoters as they become active in a stem cell lineage

Chen

Prado

et al. 2011

Development

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“…Loss of function of mia or sa had previously been shown to have similar effects on the expression of the same genes as can (White-Cooper et al, 2000). With respect both to levels of target transcripts and effects on expression of twine and cyclin B transcripts in primary spermatocytes, nht was clearly like can, mia and sa rather than like the aly class meiotic arrest genes aly, comr, topi and achi/vis (Ayyar et al, 2003;Jiang and White-Cooper, 2003;Perezgasga et al, 2004;Wang and Mann, 2003;White-Cooper et al, 2000).…”

Section: The Testis Taf Homologs Mediate a Common Gene Expression Promentioning

confidence: 99%

Testis-specific TAF homologs collaborate to control a tissue-specific transcription program

et al. 2004

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Alternate forms of the PolII transcription initiation machinery have been proposed to play a role in selective activation of cell-type-specific gene expression programs during cellular differentiation. The cannonball(can) gene of Drosophila encodes a homolog of a TBP-associated factor (dTAF5) protein expressed only in spermatocytes, where it is required for normal transcription of genes required for spermatid differentiation. We show that Drosophila primary spermatocytes also express four additional tissue-specific TAFs: nht (homolog of dTAF4), mia (homolog of dTAF6), sa (homolog of dTAF8) and rye (homolog of dTAF12). Mutations in nht, mia and sa have similar effects in primary spermatocytes on transcription of several target genes involved in spermatid differentiation, and cause the same phenotypes as mutations in can, blocking both meiotic cell cycle progression and spermatid differentiation. The nht, mia, sa and rye proteins contain histone fold domain dimerization motifs. The nht and rye proteins interact structurally when co-expressed in bacteria, similarly to their generally expressed homologs TAF4 and TAF12,which heterodimerize. Strikingly, the structural interaction is tissue specific: nht did not interact with dTAF12 and dTAF4 did not interact with rye in a bacterial co-expression assay. We propose that the products of the five Drosophila genes encoding testis TAF homologs collaborate in an alternative TAF-containing protein complex to regulate a testis-specific gene expression program in primary spermatocytes required for terminal differentiation of male germ cells.

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“…The aly-class gene products are mainly localized to euchromatin in primary spermatocytes, and this localization is essential for their function, suggesting that the major role of the tMAC complex is transcriptional activation of testis-specific genes (Jiang et al, 2007;Jiang and White-Cooper, 2003;Wang and Mann, 2003;White-Cooper et al, 2000). Thus, it now seems evident that the coordinated transcription of testis-specific genes is regulated by two specific complexes: tTAFs and tMAC.…”

Section: Introductionmentioning

confidence: 99%

The THO complex is required for nucleolar integrity in Drosophila spermatocytes

et al. 2011

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SUMMARYThe THO complex is a conserved multisubunit protein complex that functions in the formation of export-competent messenger ribonucleoprotein (mRNP). Although the complex has been studied extensively at the single-cell level, its exact role at the multicellular organism level has been poorly understood. Here, we isolated a novel Drosophila male sterile mutant, garmcho (garm). Positional cloning indicated that garm encodes a subunit of the Drosophila THO complex, THOC5. Flies lacking THOC5 showed a meiotic arrest phenotype with severe nucleolar disruption in primary spermatocytes. A functional GFP-tagged fusion protein, THOC5-GFP, revealed a unique pattern of THOC5 localization near the nucleolus. The nucleolar distribution of a testisspecific TATA binding protein (TBP)-associated factor (tTAF), SA, which is required for the expression of genes responsible for sperm differentiation, was severely disrupted in mutant testes lacking THOC5. But THOC5 appeared to be largely dispensable for the expression and nuclear export of either tTAF target mRNAs or tTAF-independent mRNAs. Taken together, our study suggests that the Drosophila THO complex is necessary for proper spermatogenesis by contribution to the establishment or maintenance of nucleolar integrity rather than by nuclear mRNA export in spermatocytes.

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Transcriptional activation inDrosophilaspermatogenesis involves the mutually dependent function ofalyand a novel meiotic arrest genecookie monster

Cited by 58 publications

References 33 publications

Sequential changes at differentiation gene promoters as they become active in a stem cell lineage

Sequential changes at differentiation gene promoters as they become active in a stem cell lineage

Testis-specific TAF homologs collaborate to control a tissue-specific transcription program

The THO complex is required for nucleolar integrity in Drosophila spermatocytes

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