A single point mutation in cyclin T1 eliminates binding to Hexim1, Cdk9 and RNA but not to AFF4 and enforces repression of HIV transcription

Retrovirology. 2014 Jul 1:11:51. doi: 10.1186/1742-4690-11-51.

Abstract

Background: Human immunodeficiency virus (HIV) gene expression is primarily regulated at the step of transcription elongation. The viral Tat protein recruits the Positive Transcription Elongation Factor b (P-TEFb) and the Super Elongation Complex (SEC) to the HIV promoter and enhances transcription by host RNA polymerase II.

Results: To map residues in the cyclin box of cyclin T1 that mediate the binding of P-TEFb to its interacting host partners and support HIV transcription, a pool of N-terminal cyclin T1 mutants was generated. Binding and functional assays in cells identified specific positions in cyclin T1 that are important for (i) association of P-TEFb with Hexim1, Cdk9 and SEC/AFF4 (ii) supporting Tat-transactivation in murine cells and (iii) inhibition of basal and Tat-dependent HIV transcription in human cells. Significantly, a unique cyclin T1 mutant where a Valine residue at position 107 was mutated to Glutamate (CycT1-V107E) was identified. CycT1-V107E did not bind to Hexim1 or Cdk9, and also could not assemble on HIV TAR or 7SK-snRNA. However, it bound strongly to AFF4 and its association with HIV Tat was slightly impaired. CycT1-V107E efficiently inhibited HIV replication in human T cell lines and in CD4(+) primary cells, and enforced HIV transcription repression in T cell lines that harbor a transcriptionally silenced integrated provirus.

Conclusions: This study outlines the mechanism by which CycT1-V107E mutant inhibits HIV transcription and enforces viral latency. It defines the importance of N-terminal residues of cyclin T1 in mediating contacts of P-TEFb with its transcription partners, and signifies the requirement of a functional P-TEFb and SEC in mediating HIV transcription.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Animals
  • Cyclin T / chemistry
  • Cyclin T / metabolism*
  • Cyclin-Dependent Kinase 9 / metabolism*
  • HEK293 Cells
  • HIV / genetics*
  • Humans
  • Mice
  • Point Mutation
  • RNA / metabolism*
  • RNA-Binding Proteins / metabolism*
  • Repressor Proteins / metabolism*
  • Structure-Activity Relationship
  • T-Lymphocytes / virology
  • Transcription Factors
  • Transcription, Genetic*
  • Transcriptional Elongation Factors
  • Virus Replication
  • tat Gene Products, Human Immunodeficiency Virus / genetics
  • tat Gene Products, Human Immunodeficiency Virus / physiology

Substances

  • AFF4 protein, human
  • CCNT1 protein, human
  • Cyclin T
  • HEXIM1 protein, human
  • RNA-Binding Proteins
  • Repressor Proteins
  • Transcription Factors
  • Transcriptional Elongation Factors
  • tat Gene Products, Human Immunodeficiency Virus
  • RNA
  • CDK9 protein, human
  • Cyclin-Dependent Kinase 9