Unraveling the Hierarchy of cis and trans Factors That Determine the DNA Binding by Peroxisome Proliferator-Activated Receptor γ

Mol Cell Biol. 2020 Mar 16;40(7):e00547-19. doi: 10.1128/MCB.00547-19. Print 2020 Mar 16.

Abstract

Peroxisome proliferator-activated receptor γ (PPARγ) is a nuclear receptor essential for adipocyte development and the maintenance of the alternatively polarized macrophage phenotype. Biochemical studies have established that as an obligate heterodimer with retinoid X receptor (RXR), PPARγ binds directly repeated nuclear receptor half sites spaced by one nucleotide (direct repeat 1 [DR1]). However, it has not been analyzed systematically and genome-wide how cis factors such as the sequences of DR1s and adjacent sequences and trans factors such as cobinding lineage-determining transcription factors (LDTFs) contribute to the direct binding of PPARγ in different cellular contexts. We developed a novel motif optimization approach using sequence composition and chromatin immunoprecipitation with high-throughput sequencing (ChIP-seq) densities from macrophages and adipocytes to complement de novo motif enrichment analysis and to define and classify high-affinity binding sites. We found that approximately half of the PPARγ cistrome represents direct DNA binding; both half sites can be extended upstream, and these are typically not of equal strength within a DR1. Strategically positioned LDTFs have greater impact on PPARγ binding than the quality of DR1, and the presence of the extension of DR1 provides a remarkable synergy with LDTFs. This approach of considering not only nucleotide frequencies but also their contribution to protein binding in a cellular context is applicable to other transcription factors.

Keywords: PPARγ; RXR; adipocytes; direct repeat 1; lineage-determining factors; macrophages; nuclear receptors.

Publication types

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

MeSH terms

  • Adipocytes / cytology*
  • Animals
  • Cells, Cultured
  • Chromatin Immunoprecipitation
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • High-Throughput Nucleotide Sequencing
  • Macrophages / cytology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • PPAR gamma / genetics
  • PPAR gamma / metabolism*
  • Phosphoproteins / genetics
  • Repetitive Sequences, Nucleic Acid / genetics
  • Retinoid X Receptors / metabolism*
  • Transcription Factors / genetics

Substances

  • DNA-Binding Proteins
  • PPAR gamma
  • Phosphoproteins
  • Pparg protein, mouse
  • Retinoid X Receptors
  • Transcription Factors
  • down-regulator of transcription 1