Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · PLoS Pathogens
 [1];  [2];  [3];  [4];  [5];  [6];  [2]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology; OSTI
  2. Univ. of California, Berkeley, CA (United States). Dept. of Plant and Microbial Biology
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrative Bio-Imaging Division; Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group
  4. Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology
  5. Univ. of California, Berkeley, CA (United States). School of Public Health. Division of Infectious Diseases and Immunity
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrative Bio-Imaging Division; Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology. California Institute for Quantitative Biosciences (QB3). Howard Hughes Medical Inst.
β- 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.
Research Organization:
Univ. of California, Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1815988
Journal Information:
PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 9 Vol. 16; ISSN 1553-7374
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (52)

A New Generation of the IMAGIC Image Processing System journal January 1996
Accurate determination of local defocus and specimen tilt in electron microscopy journal June 2003
Binding of TFIIB to RNA Polymerase II journal August 2003
Identification of Herpes TATT-binding protein journal August 2007
Structure of a Complete Mediator-RNA Polymerase II Pre-Initiation Complex journal September 2016
Influenza Virus Mounts a Two-Pronged Attack on Host RNA Polymerase II Transcription journal May 2018
XMIPP: a new generation of an open-source image processing package for electron microscopy journal November 2004
Appion: An integrated, database-driven pipeline to facilitate EM image processing journal April 2009
DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy journal May 2009
RELION: Implementation of a Bayesian approach to cryo-EM structure determination journal December 2012
Progression through the RNA Polymerase II CTD Cycle journal November 2009
Global Mapping of Herpesvirus-Host Protein Complexes Reveals a Transcription Strategy for Late Genes journal January 2015
ACE: Automated CTF Estimation journal August 2005
The RNA Polymerase II Carboxy-Terminal Domain (CTD) Code journal August 2013
The Writers, Readers, and Functions of the RNA Polymerase II C-Terminal Domain Code journal July 2013
Interference with the assembly of a virus-host transcription complex by peptide competition journal March 1990
Structural visualization of key steps in human transcription initiation journal February 2013
Architecture of the RNA polymerase II–Mediator core initiation complex journal February 2015
Near-atomic resolution visualization of human transcription promoter opening journal May 2016
Structural basis of an essential interaction between influenza polymerase and Pol II CTD journal December 2016
Rational design of a super core promoter that enhances gene expression journal October 2006
The code and beyond: transcription regulation by the RNA polymerase II carboxy-terminal domain journal March 2017
Transcription regulation by the Mediator complex journal December 2017
The Mediator complex: a central integrator of transcription journal February 2015
Phase-separation mechanism for C-terminal hyperphosphorylation of RNA polymerase II journal May 2018
RNA polymerase II clustering through carboxy-terminal domain phase separation journal August 2018
Schizosacharomyces pombe RNA polymerase II at 3.6-A resolution journal May 2009
Structure of the Mediator Head module bound to the carboxy-terminal domain of RNA polymerase II journal October 2012
The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. journal November 1991
The complex structure and function of Mediator journal September 2018
The General Transcription Machinery and General Cofactors journal January 2006
Structural basis of preinitiation complex assembly on human Pol II promoters journal January 2000
Assembly of the isomerized TFIIA--TFIID--TATA ternary complex is necessary and sufficient for gene activation. journal October 1996
The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function journal February 2009
Transcription initiation by human RNA polymerase II visualized at single-molecule resolution journal July 2012
Structure of an RNA Polymerase II–TFIIB Complex and the Transcription Initiation Mechanism journal November 2009
Structure of human TFIID and mechanism of TBP loading onto promoter DNA journal November 2018
The Epstein-Barr Virus BcRF1 Gene Product Is a TBP-Like Protein with an Essential Role in Late Gene Expression journal March 2012
Unconventional Sequence Requirement for Viral Late Gene Core Promoters of Murine Gammaherpesvirus 68 journal March 2014
Epstein-Barr Virus Late Gene Transcription Depends on the Assembly of a Virus-Specific Preinitiation Complex journal August 2014
Interaction between ORF24 and ORF34 in the Kaposi's Sarcoma-Associated Herpesvirus Late Gene Transcription Factor Complex Is Essential for Viral Late Gene Expression journal January 2016
A Functionally Distinct TATA Box Required for Late Progression through the Epstein-Barr Virus Life Cycle journal October 1998
Association of Herpes Simplex Virus Type 1 ICP8 and ICP27 Proteins with Cellular RNA Polymerase II Holoenzyme journal June 2002
Requirement of a 12-Base-Pair TATT-Containing Sequence and Viral Lytic DNA Replication in Activation of the Kaposi's Sarcoma-Associated Herpesvirus K8.1 Late Promoter journal March 2004
ICP27 Interacts with the C-Terminal Domain of RNA Polymerase II and Facilitates Its Recruitment to Herpes Simplex Virus 1 Transcription Sites, Where It Undergoes Proteasomal Degradation during Infection journal April 2006
Structural Insights into the Eukaryotic Transcription Initiation Machinery journal May 2017
Bacterial Sigma Factors: A Historical, Structural, and Genomic Perspective journal September 2014
Transcription Regulation at the Core: Similarities Among Bacterial, Archaeal, and Eukaryotic RNA Polymerases journal September 2013
IPC – Isoelectric Point Calculator journal October 2016
An integrative approach identifies direct targets of the late viral transcription complex and an expanded promoter recognition motif in Kaposi’s sarcoma-associated herpesvirus journal May 2019
RNA decay during gammaherpesvirus infection reduces RNA polymerase II occupancy of host promoters but spares viral promoters journal February 2020
Human cytomegalovirus interactome analysis identifies degradation hubs, domain associations and viral protein functions journal December 2019

Similar Records

Sequence and transcription analysis of the human cytomegalovirus DNA polymerase gene
Journal Article · Wed Dec 31 23:00:00 EST 1986 · J. Virol.; (United States) · OSTI ID:6244419

Structure and Function of the N-Terminal Domain of the Vesicular Stomatitis Virus RNA Polymerase
Journal Article · Tue Dec 29 19:00:00 EST 2015 · Journal of Virology · OSTI ID:1242301

The eIF4AIII RNA helicase is a critical determinant of human cytomegalovirus replication
Journal Article · Sun Feb 14 23:00:00 EST 2016 · Virology · OSTI ID:22581672

Related Subjects