5-Hydroxymethylcytosine in E-box motifs ACAT|GTG and ACAC|GTG increases DNA-binding of the B-HLH transcription factor TCF4

Integr Biol (Camb). 2016 Sep 12;8(9):936-45. doi: 10.1039/c6ib00079g. Epub 2016 Aug 3.

Abstract

We evaluated DNA binding of the B-HLH family members TCF4 and USF1 using protein binding microarrays (PBMs) containing double-stranded DNA probes with cytosine on both strands or 5-methylcytosine (5mC) or 5-hydroxymethylcytosine (5hmC) on one DNA strand and cytosine on the second strand. TCF4 preferentially bound the E-box motif (CAN|NTG) with strongest binding to the 8-mer CAG|GTGGT. 5mC uniformly decreases DNA binding of both TCF4 and USF1. The bulkier 5hmC also inhibited USF1 binding to DNA. In contrast, 5hmC dramatically enhanced TCF4 binding to E-box motifs ACAT|GTG and ACAC|GTG, being better bound than any 8-mer containing cytosine. Examination of X-ray structures of the closely related TCF3 and USF1 bound to DNA suggests TCF3 can undergo a conformational shift to preferentially bind to 5hmC while the USF1 basic region is bulkier and rigid precluding a conformation shift to bind 5hmC. These results greatly expand the regulatory DNA sequence landscape bound by TCF4.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • 5-Methylcytosine / analogs & derivatives*
  • 5-Methylcytosine / chemistry
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / chemistry*
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / ultrastructure
  • Binding Sites
  • DNA / chemistry*
  • DNA / ultrastructure
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / ultrastructure
  • E-Box Elements*
  • Protein Array Analysis / methods*
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Protein Interaction Mapping
  • Transcription Factor 4 / chemistry*
  • Transcription Factor 4 / ultrastructure

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • DNA-Binding Proteins
  • TCF4 protein, human
  • Transcription Factor 4
  • 5-hydroxymethylcytosine
  • 5-Methylcytosine
  • DNA