Phosphorylation by JNK switches BRD4 functions

Mol Cell. 2024 Nov 21;84(22):4282-4296.e7. doi: 10.1016/j.molcel.2024.09.030. Epub 2024 Oct 24.

Abstract

Bromodomain 4 (BRD4), a key regulator with pleiotropic functions, plays crucial roles in cancers and cellular stress responses. It exhibits dual functionality: chromatin-bound BRD4 regulates remodeling through its histone acetyltransferase (HAT) activity, while promoter-associated BRD4 regulates transcription through its kinase activity. Notably, chromatin-bound BRD4 lacks kinase activity, and RNA polymerase II (RNA Pol II)-bound BRD4 exhibits no HAT activity. This study unveils one mechanism underlying BRD4's functional switch. In response to diverse stimuli, c-Jun N-terminal kinase (JNK)-mediated phosphorylation of human BRD4 at Thr1186 and Thr1212 triggers its transient release from chromatin, disrupting its HAT activity and potentiating its kinase activity. Released BRD4 directly interacts with and phosphorylates RNA Pol II, PTEFb, and c-Myc, thereby promoting transcription of target genes involved in immune and inflammatory responses. JNK-mediated BRD4 functional switching induces CD8 expression in thymocytes and epithelial-to-mesenchymal transition (EMT) in prostate cancer cells. These findings elucidate the mechanism by which BRD4 transitions from a chromatin regulator to a transcriptional activator.

Keywords: BRD4; EMT; JNK; cellular stress; chromatin decompaction; histone acetyltransferase; kinase; phospho-BRD4; thymocyte stimulation; transcription activation.

MeSH terms

  • Animals
  • Bromodomain Containing Proteins
  • Cell Cycle Proteins* / genetics
  • Cell Cycle Proteins* / metabolism
  • Cell Line, Tumor
  • Chromatin / genetics
  • Chromatin / metabolism
  • Epithelial-Mesenchymal Transition
  • HEK293 Cells
  • Histone Acetyltransferases / genetics
  • Histone Acetyltransferases / metabolism
  • Humans
  • JNK Mitogen-Activated Protein Kinases* / genetics
  • JNK Mitogen-Activated Protein Kinases* / metabolism
  • Male
  • Mice
  • Nuclear Proteins* / genetics
  • Nuclear Proteins* / metabolism
  • Phosphorylation
  • Positive Transcriptional Elongation Factor B / genetics
  • Positive Transcriptional Elongation Factor B / metabolism
  • Prostatic Neoplasms / enzymology
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • 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
  • Transcription, Genetic

Substances

  • BRD4 protein, human
  • Transcription Factors
  • Nuclear Proteins
  • RNA Polymerase II
  • Cell Cycle Proteins
  • JNK Mitogen-Activated Protein Kinases
  • Positive Transcriptional Elongation Factor B
  • Proto-Oncogene Proteins c-myc
  • Chromatin
  • Histone Acetyltransferases
  • Brd4 protein, mouse
  • MYC protein, human
  • Bromodomain Containing Proteins