Cooperation between bHLH transcription factors and histones for DNA access

Alicia K. Michael, Lisa Stoos, Priya Crosby, Nikolas Eggers, Xinyu Y. Nie, Kristina Makasheva, Martina Minnich, Kelly L. Healy, Joscha Weiss, Georg Kempf, Simone Cavadini, Lukas Kater, Jan Seebacher, Luca Vecchia, Deyasini Chakraborty, Luke Isbel, Ralph S. Grand, Florian Andersch, Jennifer L. Fribourgh, Dirk Schübeler, Johannes Zuber, Andrew C. Liu, Peter B. Becker, Beat Fierz, Carrie L. Partch, Jerome S. Menet and Nicolas H. Thomä ()
Additional contact information
Alicia K. Michael: Friedrich Miescher Institute for Biomedical Research
Lisa Stoos: Friedrich Miescher Institute for Biomedical Research
Priya Crosby: University of California, Santa Cruz
Nikolas Eggers: Ludwig-Maximilians-Universität
Xinyu Y. Nie: Texas A&M University
Kristina Makasheva: Ecole Polytechnique Fédérale de Lausanne
Martina Minnich: Vienna BioCenter
Kelly L. Healy: University of Florida
Joscha Weiss: Friedrich Miescher Institute for Biomedical Research
Georg Kempf: Friedrich Miescher Institute for Biomedical Research
Simone Cavadini: Friedrich Miescher Institute for Biomedical Research
Lukas Kater: Friedrich Miescher Institute for Biomedical Research
Jan Seebacher: Friedrich Miescher Institute for Biomedical Research
Luca Vecchia: Friedrich Miescher Institute for Biomedical Research
Deyasini Chakraborty: Friedrich Miescher Institute for Biomedical Research
Luke Isbel: Friedrich Miescher Institute for Biomedical Research
Ralph S. Grand: Friedrich Miescher Institute for Biomedical Research
Florian Andersch: Vienna BioCenter
Jennifer L. Fribourgh: University of California, Santa Cruz
Dirk Schübeler: Friedrich Miescher Institute for Biomedical Research
Johannes Zuber: Vienna BioCenter
Andrew C. Liu: University of Florida
Peter B. Becker: Ludwig-Maximilians-Universität
Beat Fierz: Ecole Polytechnique Fédérale de Lausanne
Carrie L. Partch: University of California, Santa Cruz
Jerome S. Menet: Texas A&M University
Nicolas H. Thomä: Friedrich Miescher Institute for Biomedical Research

Nature, 2023, vol. 619, issue 7969, 385-393

Abstract: Abstract The basic helix–loop–helix (bHLH) family of transcription factors recognizes DNA motifs known as E-boxes (CANNTG) and includes 108 members1. Here we investigate how chromatinized E-boxes are engaged by two structurally diverse bHLH proteins: the proto-oncogene MYC-MAX and the circadian transcription factor CLOCK-BMAL1 (refs. 2,3). Both transcription factors bind to E-boxes preferentially near the nucleosomal entry–exit sites. Structural studies with engineered or native nucleosome sequences show that MYC-MAX or CLOCK-BMAL1 triggers the release of DNA from histones to gain access. Atop the H2A–H2B acidic patch4, the CLOCK-BMAL1 Per-Arnt-Sim (PAS) dimerization domains engage the histone octamer disc. Binding of tandem E-boxes5–7 at endogenous DNA sequences occurs through direct interactions between two CLOCK-BMAL1 protomers and histones and is important for circadian cycling. At internal E-boxes, the MYC-MAX leucine zipper can also interact with histones H2B and H3, and its binding is indirectly enhanced by OCT4 elsewhere on the nucleosome. The nucleosomal E-box position and the type of bHLH dimerization domain jointly determine the histone contact, the affinity and the degree of competition and cooperativity with other nucleosome-bound factors.

Date: 2023
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DOI: 10.1038/s41586-023-06282-3

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