Arginine methylation regulates c-Myc-dependent transcription by altering promoter recruitment of the acetyltransferase p300

J Biol Chem. 2017 Aug 11;292(32):13333-13344. doi: 10.1074/jbc.M117.797928. Epub 2017 Jun 26.

Abstract

Protein arginine methyltransferase 1 (PRMT1) is an essential enzyme controlling about 85% of the total cellular arginine methylation in proteins. We have shown previously that PRMT1 is an important regulator of innate immune responses and that it is required for M2 macrophage differentiation. c-Myc is a transcription factor that is critical in regulating cell proliferation and also regulates the M2 transcriptional program in macrophages. Here, we sought to determine whether c-Myc in myeloid cells is regulated by PRMT1-dependent arginine methylation. We found that PRMT1 activity was necessary for c-Myc binding to the acetyltransferase p300. PRMT1 inhibition decreased p300 recruitment to c-Myc target promoters and increased histone deacetylase 1 (HDAC1) recruitment, thereby decreasing transcription at these sites. Moreover, PRMT1 inhibition blocked c-Myc-mediated induction of several of its target genes, including peroxisome proliferator-activated receptor γ (PPARG) and mannose receptor C-type 1 (MRC1), suggesting that PRMT1 is necessary for c-Myc function in M2 macrophage differentiation. Of note, in primary human blood monocytes, p300-c-Myc binding was strongly correlated with PRMT1 expression, and in liver sections, PRMT1, c-Myc, and M2 macrophage levels were strongly correlated with each other. Both PRMT1 levels and M2 macrophage numbers were significantly lower in livers from individuals with a history of spontaneous bacterial peritonitis, known to have defective cellular immunity. In conclusion, our findings demonstrate that PRMT1 is an important regulator of c-Myc function in myeloid cells. PRMT1 loss in individuals with cirrhosis may contribute to their immune defects.

Keywords: M2 macrophage; histone deacetylase 1 (HDAC1); macrophage; monocyte; posttranslational modification (PTM); transcription factor.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus / drug effects
  • Animals
  • Arginine / metabolism
  • Cell Line, Tumor
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • Enzyme Inhibitors / pharmacology
  • Histone Deacetylase 1 / metabolism
  • Humans
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis / immunology
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology
  • Methylation / drug effects
  • Mice, Knockout
  • Myeloid Cells / drug effects
  • Myeloid Cells / immunology
  • Myeloid Cells / metabolism*
  • Myeloid Cells / pathology
  • Promoter Regions, Genetic* / drug effects
  • Protein Processing, Post-Translational* / drug effects
  • Protein-Arginine N-Methyltransferases / antagonists & inhibitors
  • Protein-Arginine N-Methyltransferases / genetics
  • Protein-Arginine N-Methyltransferases / metabolism*
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Transcription, Genetic* / drug effects
  • p300-CBP Transcription Factors / metabolism*

Substances

  • Enzyme Inhibitors
  • Myc protein, mouse
  • Proto-Oncogene Proteins c-myc
  • Arginine
  • Prmt1 protein, mouse
  • Protein-Arginine N-Methyltransferases
  • p300-CBP Transcription Factors
  • p300-CBP-associated factor
  • Hdac1 protein, mouse
  • Histone Deacetylase 1