TurboCas: A method for locus-specific labeling of genomic regions and isolating their associated protein interactome

Mol Cell. 2024 Dec 19;84(24):4929-4944.e8. doi: 10.1016/j.molcel.2024.11.007.

Abstract

Regulation of gene expression during development and stress response requires the concerted action of transcription factors and chromatin-binding proteins. Because this process is cell-type specific and varies with cellular conditions, mapping of chromatin factors at individual regulatory loci is crucial for understanding cis-regulatory control. Previous methods only characterize static protein binding. We present "TurboCas," a method combining a proximity-labeling (PL) enzyme, miniTurbo, with CRISPR-dCas9 that allows for efficient and site-specific labeling of chromatin factors in mammalian cells. Validating TurboCas at the FOS promoter, we identify proteins recruited upon heat shock, cross-validated via RNA polymerase II and P-TEFb immunoprecipitation. These methodologies reveal canonical and uncharacterized factors that function to activate expression of heat-shock-responsive genes. Applying TurboCas to the MYC promoter, we identify two P-TEFb coactivators, the super elongation complex (SEC) and BRD4, as MYC co-regulators. TurboCas provides a genome-specific targeting PL, with the potential to deepen our molecular understanding of transcriptional regulatory pathways in development and stress response.

Keywords: BRD4; FOS; FUBP3; MYC; chromatin-binding proteins; dCas9; gene regulation; heat shock; proximity labeling.

MeSH terms

  • Bromodomain Containing Proteins
  • CRISPR-Cas Systems
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Chromatin* / genetics
  • Chromatin* / metabolism
  • Gene Expression Regulation
  • HEK293 Cells
  • Heat-Shock Response / genetics
  • Humans
  • Positive Transcriptional Elongation Factor B / genetics
  • Positive Transcriptional Elongation Factor B / metabolism
  • Promoter Regions, Genetic*
  • Protein Binding
  • Protein Interaction Maps
  • Proto-Oncogene Proteins c-fos / genetics
  • Proto-Oncogene Proteins c-fos / metabolism
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Transcription Factors
  • BRD4 protein, human
  • Chromatin
  • RNA Polymerase II
  • Cell Cycle Proteins
  • Positive Transcriptional Elongation Factor B
  • Proto-Oncogene Proteins c-myc
  • Proto-Oncogene Proteins c-fos
  • MYC protein, human
  • Bromodomain Containing Proteins