scholarly journals The gammaherpesviral TATA-box-binding protein directly interacts with the CTD of host RNA Pol II to direct late gene transcription

2020 ◽  
Vol 16 (9) ◽  
pp. e1008843
Author(s):  
Angelica F. Castañeda ◽  
Allison L. Didychuk ◽  
Robert K. Louder ◽  
Chloe O. McCollum ◽  
Zoe H. Davis ◽  
...  
Keyword(s):  
Gene Transcription ◽  
Binding Protein ◽  
Tata Box ◽  
Late Gene ◽  
Rna Pol Ii ◽  
Pol Ii ◽  
Tata Box Binding Protein

scholarly journals The gammaherpesviral TATA-box-binding protein directly interacts with the CTD of host RNA Pol II to direct late gene transcription

2020 ◽  
Author(s):  
Angelica F. Castañeda ◽  
Allison L. Didychuk ◽  
Robert K. Louder ◽  
Chloe O. McCollum ◽  
Zoe H. Davis ◽  
...  
Keyword(s):  
Rna Polymerase Ii ◽  
Gene Transcription ◽  
Binding Protein ◽  
Tata Box ◽  
Late Gene ◽  
Rna Pol Ii ◽  
Eukaryotic Transcription ◽  
Pol Ii ◽  
Terminal Domain ◽  
Tata Box Binding Protein

ABSTRACTβ- and γ-herpesviruses include the oncogenic human viruses Kaposi’s sarcoma-associated virus (KSHV) and Epstein-Barr virus (EBV), and human cytomegalovirus (HCMV), which is a significant cause of congenital disease. Near the end of their replication cycle, these viruses transcribe their late genes in a manner distinct from host transcription. Late gene transcription requires six virally-encoded proteins, one of which is a functional mimic of host TATA-box-binding protein (TBP) that is also involved in recruitment of RNA polymerase II (Pol II) via unknown mechanisms. Here, we applied biochemical protein interaction studies together with electron microscopy-based imaging of a reconstituted human preinitiation complex to define the mechanism underlying Pol II recruitment. These data revealed that the herpesviral TBP, encoded by ORF24 in KSHV, makes a direct protein-protein contact with the C-terminal domain of host RNA polymerase II (Pol II), which is a unique feature that functionally distinguishes viral from cellular TBP. The interaction is mediated by the N-terminal domain (NTD) of ORF24 through a conserved motif that is shared in its β- and γ-herpesvirus homologs. Thus, these herpesviruses employ an unprecedented strategy in eukaryotic transcription, wherein promoter recognition and polymerase recruitment are facilitated by a single transcriptional activator with functionally distinct domains.SIGNIFICANCE STATEMENTThe β- and γ-herpesviruses mediate their late gene transcription through a set of viral transcriptional activators (vTAs). One of these vTAs, ORF24 in Kaposi’s sarcoma-associated herpesvirus (KSHV), is a mimic of host TATA-box-binding protein (TBP). We demonstrate that the N-terminal domain of ORF24 and its homologs from other β- and γ-herpesviruses directly bind the unstructured C-terminal domain (CTD) of RNA Pol II. This functionally distinguishes the viral TBP mimic from cellular TBP, which does not bind Pol II. Thus, herpesviruses encode a transcription factor that has the dual ability to directly interact with promoter DNA and the polymerase, a property which is unique in eukaryotic transcription and is conceptually akin to prokaryotic transcription factors.

scholarly journals Polymerase (Pol) III TATA Box-Binding Protein (TBP)-Associated Factor Brf Binds to a Surface on TBP Also Required for Activated Pol II Transcription

1998 ◽  
Vol 18 (3) ◽  
pp. 1692-1700 ◽  
Author(s):  
Yuhong Shen ◽  
George A. Kassavetis ◽  
Gene O. Bryant ◽  
Arnold J. Berk
Keyword(s):  
Gene Transcription ◽  
Transcription Initiation ◽  
Binding Protein ◽  
Tata Box ◽  
Related Factor ◽  
In Vitro Synthesis ◽  
Pol Ii ◽  
U6 Snrna ◽  
Tata Box Binding Protein ◽  
Pol Iii

ABSTRACT The TATA box-binding protein (TBP) plays an essential role in transcription by all three eukaryotic nuclear RNA polymerases, polymerases (Pol) I, II, and III. In each case, TBP interacts with class-specific TBP-associated factors (TAFs) to form class-specific transcription initiation factors. For yeast Pol III transcription, TBP associates with Brf (from TFIIB-related factor) and B", two Pol III TAFs, to form Pol III transcription factor TFIIIB. Here, we identify TBP surface residues that are required for interaction with yeast Pol III TAFs. Ninety-one human TBP surface residue mutants with radical substitutions were analyzed for the ability to form stable gel shift complexes with purified Brf and B" and for their activities for in vitro synthesis of yeast U6 snRNA. Mutations in a large positively charged epitope extending from the top (that is, on the surface opposite the DNA-facing “saddle” of TBP) and onto the side of the first TBP repeat inhibited binding to Brf (residues K181, L185, R186, E206, R231, L232, R235, K236, R239, Q242, K243, K249, and F250). A triple-mutant TBP (R231E + R235E + R239S) had greatly reduced activity for yeast U6 snRNA gene transcription while remaining active for Pol II basal transcription. Similar results were observed when selected mutations were introduced into yeast TBP at equivalent positions. A C-terminal fragment of Brf lacking the region of homology with TFIIB retains the ability to bind TBP-DNA complexes (G. Kassavetis, C. Bardeleben, A. Kumar, E. Ramirez, and E. P. Geiduschek, Mol. Cell. Biol. 17:5299–5306, 1997); the same TBP mutations reduced binding by this fragment. Mutations in TBP residues that interact with TFIIB did not affect Brf binding or U6 gene transcription. These results indicate that Brf and TFIIB interact differently with TBP. An extensively overlapping epitope on the top surface of TBP was found previously to be required for activated Pol II transcription and has been hypothesized to interact with Pol II TAFs. Our results map the surface of TBP that interacts with Brf and suggest that Pol II and Pol III TAFs interact with the same surface of TBP.

scholarly journals Ectopic expression of TATA box-binding protein induces shoot proliferation in Arabidopsis

FEBS Letters ◽  
2001 ◽  
Vol 489 (2-3) ◽  
pp. 187-191 ◽  
Author(s):  
You-Fang Li ◽  
Frédéric Dubois ◽  
Dao-Xiu Zhou
Keyword(s):  
Binding Protein ◽  
Ectopic Expression ◽  
Shoot Proliferation ◽  
Tata Box ◽  
Tata Box Binding Protein

scholarly journals Bidirectional binding of the TATA box binding protein to the TATA box

1997 ◽  
Vol 94 (25) ◽  
pp. 13475-13480 ◽  
Author(s):  
J. M. Cox ◽  
M. M. Hayward ◽  
J. F. Sanchez ◽  
L. D. Gegnas ◽  
S. van der Zee ◽  
...  
Keyword(s):  
Binding Protein ◽  
Tata Box ◽  
Tata Box Binding Protein

c-Fos-induced activation of a TATA-box-containing promoter involves direct contact with TATA-box-binding protein

1994 ◽  
Vol 14 (9) ◽  
pp. 6021-6029
Author(s):  
R Metz ◽  
A J Bannister ◽  
J A Sutherland ◽  
C Hagemeier ◽  
E C O'Rourke ◽  
...  
Keyword(s):  
Protein Interactions ◽  
Transcriptional Activation ◽  
Binding Protein ◽  
Tata Box ◽  
Binding Motif ◽  
Protein Protein Interactions ◽  
High Concentrations ◽  
Tata Box Binding Protein

Transcriptional activation in eukaryotes involves protein-protein interactions between regulatory transcription factors and components of the basal transcription machinery. Here we show that c-Fos, but not a related protein, Fra-1, can bind the TATA-box-binding protein (TBP) both in vitro and in vivo and that c-Fos can also interact with the transcription factor IID complex. High-affinity binding to TBP requires c-Fos activation modules which cooperate to activate transcription. One of these activation modules contains a TBP-binding motif (TBM) which was identified through its homology to TBP-binding viral activators. This motif is required for transcriptional activation, as well as TBP binding. Domain swap experiments indicate that a domain containing the TBM can confer TBP binding on Fra-1 both in vitro and in vivo. In vivo activation experiments indicate that a GAL4-Fos fusion can activate a promoter bearing a GAL4 site linked to a TATA box but that this activity does not occur at high concentrations of GAL4-Fos. This inhibition (squelching) of c-Fos activity is relieved by the presence of excess TBP, indicating that TBP is a direct functional target of c-Fos. Removing the TBM from c-Fos severely abrogates activation of a promoter containing a TATA box but does not affect activation of a promoter driven only by an initiator element. Collectively, these results suggest that c-Fos is able to activate via two distinct mechanisms, only one of which requires contact with TBP. Since TBP binding is not exhibited by Fra-1, TBP-mediated activation may be one characteristic that discriminates the function of Fos-related proteins.

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