Expression of the core promoter factors TATA box binding protein and TATA box binding protein‐related factor 2 in <i>Drosophila</i> germ cells and their distinct functions in germline development

Nakamura, Shoichi; Hira, Seiji; Kojima, Makoto; Kondo, Akane; Mukai, Masanori

doi:10.1111/dgd.12701

Cited by 3 publications

(3 citation statements)

References 45 publications

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“…Similar to TBP, TRF2 binds to promoters of all active genes. Previous studies in various species have shown that TBP and its paralogs occupy and regulate distinct sets of genes (82)(83)(84)(85)(86). It was therefore surprising that in mESCs, TRF2 binds to all active genes, though the differences may reflect species-specificity.…”

Section: The Tbp Paralog Trf2 Is Expressed In Mescs and Binds To Prommentioning

confidence: 99%

A TBP-independent mechanism for RNA Polymerase II transcription

Budzyński

et al. 2021

Preprint

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Transcription by RNA Polymerase II (Pol II) is initiated by the hierarchical assembly of the Pre-Initiation Complex onto promoter DNA. Decades of in vitro and yeast research have shown that the TATA-box binding protein (TBP) is essential to Pol II initiation by triggering the binding of other general transcription factors, and ensuring proper Pol II loading. Here, we report instead that acute depletion of TBP in mouse embryonic stem cells (mESCs) has no global effect on ongoing Pol II transcription. Surprisingly, Pol II transcriptional induction through the Heat Shock Response or cellular differentiation also occurs normally in the absence of TBP. In contrast, acute TBP depletion severely impairs initiation by RNA Polymerase III. Lastly, we show that a metazoan-specific paralog of TBP is expressed in mESCs and that it binds to promoter regions of active Pol II genes even in the absence of TBP. Taken together, our findings reveal an unexplored TBP-independent process in mESCs that points to a diversity in Pol II transcription initiation mechanisms.

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Section: The Tbp Paralog Trf2 Is Expressed In Mescs and Binds To Prommentioning

confidence: 99%

A TBP-independent mechanism for RNA Polymerase II transcription

Budzyński

et al. 2021

Preprint

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“…Though these results could be explained by a critical requirement for the Ada2b-and Gcn5 containing ADA or Chiffon complexes [26,27] and no dependency on the SAGA complex during oogenesis, they may also reflect that distinct gene sets, defined by promoter types, have a different genetic requirement for each module. During Drosophila spermatogenesis and oogenesis, both TBP and the structurally related protein TBP-related factor 2 (TRF2) play critical, yet different roles, suggesting that different TBP-binding and/ or containing complexes may be required for oogenesis [28][29][30][31][32][33][34][35][36][37][38][39]. Therefore, we hypothesized that the SAGA complex itself and specifically the TBP-binding core module is important for oogenesis.…”

Section: Introductionmentioning

confidence: 99%

The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

Soffers

Alcántara

et al. 2021

Preprint

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The Spt/Ada-Gcn5 Acetyltransferase (SAGA) coactivator complex has multiple modules with different enzymatic and non-enzymatic functions. How each module contributes to gene activation in specific biological contexts is not well understood. Here we analyzed the role of the non-enzymatic core module during Drosophila oogenesis. We show that depletion of several SAGA-specific subunits belonging to the core module blocked egg chamber development during mid-oogenesis stages, resulting in stronger phenotypes than those obtained after depletion of SAGA’s histone acetyltransferase module or deubiquitination module. These results, as well as additional genetic analyses pointing to an interaction with TBP, suggested a differential role of SAGA modules at different promoter types. However, SAGA subunits co-occupied all promoter types of active genes in ChIP-seq and ChIP-nexus experiments. Thus, the SAGA complex appears to occupy promoters in its entirety, consistent with the strong biochemical integrity of the complex. The high-resolution genomic binding profiles are congruent with SAGA recruitment by activators upstream of the start site, and retention on chromatin by interactions with modified histones downstream of the start site. The stronger genetic requirement of the core module during oogenesis may therefore be explained through its interaction with TBP or its role in recruiting the enzymatic modules to the promoter. We propose the handyman principle, which posits that a distinct genetic requirement for specific components may conceal the fact that the entire complex is physically present.

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“…The SAGA core module interacts with TBP. TBP and the structurally related protein TBP-related factor 2 (TRF2) play critical, yet different roles during spermatogenesis and oogenesis [19][20][21][22][23]. Thus, we hypothesized that the core module is important for oogenesis via the activation of a distinct gene set, in a way that depends on TBP.…”

Section: Introductionmentioning

confidence: 99%

The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

Soffers

Alcantara

et al. 2021

PLoS Genet

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The Spt/Ada-Gcn5 Acetyltransferase (SAGA) coactivator complex has multiple modules with different enzymatic and non-enzymatic functions. How each module contributes to gene expression is not well understood. During Drosophila oogenesis, the enzymatic functions are not equally required, which may indicate that different genes require different enzymatic functions. An analogy for this phenomenon is the handyman principle: while a handyman has many tools, which tool he uses depends on what requires maintenance. Here we analyzed the role of the non-enzymatic core module during Drosophila oogenesis, which interacts with TBP. We show that depletion of SAGA-specific core subunits blocked egg chamber development at earlier stages than depletion of enzymatic subunits. These results, as well as additional genetic analyses, point to an interaction with TBP and suggest a differential role of SAGA modules at different promoter types. However, SAGA subunits co-occupied all promoter types of active genes in ChIP-seq and ChIP-nexus experiments, and the complex was not specifically associated with distinct promoter types in the ovary. The high-resolution genomic binding profiles were congruent with SAGA recruitment by activators upstream of the start site, and retention on chromatin by interactions with modified histones downstream of the start site. Our data illustrate that a distinct genetic requirement for specific components may conceal the fact that the entire complex is physically present and suggests that the biological context defines which module functions are critical.

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Expression of the core promoter factors TATA box binding protein and TATA box binding protein‐related factor 2 in Drosophila germ cells and their distinct functions in germline development

Cited by 3 publications

References 45 publications

A TBP-independent mechanism for RNA Polymerase II transcription

A TBP-independent mechanism for RNA Polymerase II transcription

The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

The SAGA core module is critical during Drosophila oogenesis and is broadly recruited to promoters

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