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A pioneer factor locally opens compacted chromatin to enable targeted ATP-dependent nucleosome remodeling

Nature Structural & Molecular Biology volume 30, pages 31–37 (2023)Cite this article

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Abstract

To determine how different pioneer transcription factors form a targeted, accessible nucleosome within compacted chromatin and collaborate with an ATP-dependent chromatin remodeler, we generated nucleosome arrays in vitro with a central nucleosome containing binding sites for the hematopoietic E-Twenty Six (ETS) factor PU.1 and Basic Leucine Zipper (bZIP) factors C/EBPα and C/EBPβ. Our long-read sequencing reveals that each factor can expose a targeted nucleosome on linker histone-compacted arrays, but with different nuclease sensitivity patterns. The DNA binding domain of PU.1 binds mononucleosomes, but requires an additional intrinsically disordered domain to bind and open compacted chromatin. The canonical mammalian SWI/SNF (cBAF) remodeler was unable to act upon two forms of locally open chromatin unless cBAF was enabled by a separate transactivation domain of PU.1. cBAF potentiates the PU.1 DNA binding domain to weakly open chromatin in the absence of the PU.1 disordered domain. Our findings reveal a hierarchy by which chromatin is opened and show that pioneer factors can provide specificity for action by nucleosome remodelers.

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Fig. 1: Different patterns of chromatin opening by PU.1 and C/EBP.
Fig. 2: Domains outside of DBDs are needed to open chromatin.
Fig. 3: PU.1 enables further chromatin opening by cBAF.
Fig. 4: cBAF action requires AQ and IDR domains of PU.1.

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Data availability

All cloned reagents described are available from the authors. Nanopore FASTq and mapped bigwig files have been deposited to the NCBI GEO under accession no. GSE216065. Source data are provided with this paper.

Code availability

All code for data analysis and visualization is available from the corresponding author on request.

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Acknowledgements

M.A.F. was supported by NIH training grant T32 DK07780 and NIH fellowship F31 DK123886. K.E.W. was supported by the National Science Foundation NSF Graduate Research Fellowship Program Award and the Harvard Medical School Landry Cancer Biology Award. We are grateful to N. Mashtalir (Kadoch Lab) for guidance and technical support with respect to purification of cBAF complexes. The research was supported by grant no. NIH GM36477 to K.S.Z.

Author information

Authors and Affiliations

  1. Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Megan A. Frederick, Meilin Fernandez Garcia, Ryan L. McCarthy, Greg Donahue, Edgar Luzete Monteiro, Naomi Takenaka, Janice Reynaga & Kenneth S. Zaret

  2. Penn Epigenetics Institute, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Megan A. Frederick, Meilin Fernandez Garcia, Ryan L. McCarthy, Greg Donahue, Edgar Luzete Monteiro, Naomi Takenaka, Janice Reynaga & Kenneth S. Zaret

  3. Department Cell and Developmental Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Megan A. Frederick, Meilin Fernandez Garcia, Ryan L. McCarthy, Greg Donahue, Edgar Luzete Monteiro, Naomi Takenaka, Janice Reynaga & Kenneth S. Zaret

  4. Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Megan A. Frederick

  5. Department of Pediatric Oncology, Dana–Farber Cancer Institute and Harvard Medical School, Boston, MA, USA

    Kaylyn E. Williamson & Cigall Kadoch

  6. Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Meilin Fernandez Garcia & Max B. Ferretti

  7. Department of Biology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, USA

    Edgar Luzete Monteiro

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Contributions

M.A.F. and K.S.Z. designed the study and wrote the manuscript, with input from C.K. and all other authors. M.A.F. carried out the design and generation of all end-labeled nucleosome array templates, nucleosome array reconstitution, transcription factor binding reactions with nucleosome arrays, nuclease hypersensitivity assays, nucleosome remodeling assays, and nanopore sequencing sample preparation, sequencing, and analysis with M.B.F, R.L.M and G.D. M.A.F. constructed and purified wild-type and mutant transcription factors with M.F.G, and E.L.M., M.A.F, M.F.G and J.R. performed EMSAs with mononucleosomes generated by M.F.G. K.E.W purified the human cBAF complex. N.T. generated the purified histone octamers.

Corresponding author

Correspondence to Kenneth S. Zaret.

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Competing interests

C.K. is the Scientific Founder, fiduciary Board of Directors member, Scientific Advisory Board member, shareholder and consultant for Foghorn Therapeutics, Inc. C.K. also serves on the scientific advisory boards of Nereid Therapeutics and Nested Therapeutics and is a consultant for Cell Signaling Technologies. K.E.W. is an employee and shareholder of Flare Therapeutics. The remaining authors declare no competing interests.

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Nature Structural & Molecular Biology thanks Sharon Dent and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editor: Carolina Perdigoto, in collaboration with the Nature Structural & Molecular Biology team.

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Extended data

Extended Data Fig. 1 Generation of H1-compacted Cx3cr1 nucleosome arrays.

a, PU.1 and C/EBP ChIP-seq profiles (red) in macrophages and MNase-seq profile (green) in fibroblasts near the Cx3cr1 gene within the displayed region of the mouse genome with TF motifs indicated. b, Diagram of the dCTP-Cy5 end-labeled Cx3cr1 nucleosome array. c, Schematic of linker histone-mediated chromatin compaction. d, Representative EMSA of linker histone-mediated chromatin compaction by native agarose gel electrophoresis. Free DNA (lanes 1 and 5) and nucleosome arrays with nucleosome:linker histone ratios of 0 (lanes 2 and 6), 0.5 (lanes 3 and 7) and 1.0 (lanes 4 and 8) are shown. Representative gel image of 2 biological replicates.

Source data

Extended Data Fig. 2 Nanopore sequencing to determine translational position of nucleosomes in the Cx3cr1 array.

a, Schematic of Nanopore sequencing and endpoint analysis pipeline. b, MNase digestion analysis of free DNA and extended nucleosome arrays at two MNase concentrations (U/mL) visualized by gel electrophoresis. Two biological replicates are shown on the same gel. Lane 1 is a partial EcoRI digest DNA marker (M) with fragments in basepairs corresponding to (from bottom to top): 208, 416, 624, 834, 1028, 1658, 1866, 2074, 2282, 2490, 2733. c, IGV visualization of Nanopore sequencing endpoint analysis of MNase digested free DNA (0.07 U/mL MNase), extended nucleosome arrays (0.3 U/mL) and free DNA signal subtracted from array signal to account for MNase site bias. n = 2 biological replicates in b. Plots show normalized read density on the y axis. For each plot, the maximum value is set to 0.4% of reads. d, Determination of nucleosome translational positions.

Source data

Extended Data Fig. 3 Nanopore sequencing of TFs incubated with H1-compacted arrays.

a, Schematic of DNase I digestion analysis. b, DNase I digestion analysis of TFs binding to H1-compacted nucleosome arrays visualized by gel electrophoresis (10 ng/uL DNase I). Two biological replicates are shown on the same gel. Lanes 1 and 14 are a partial EcoRI digest DNA marker (M) with fragments in basepairs corresponding to (from bottom to top): 416, 624, 834, 1028, 1658, 1866, 2074, 2282, 2490, 2733. c, IGV visualization of Nanopore endpoint analysis of DNase I digested H1-compacted nucleosome arrays incubated with indicated transcription factor(s) from n = 2 biological replicates in b. Plots show normalized read density on the y axis. For each plot, the maximum value is set to 0.4% of reads. d, DNase I digestion analysis of indicated TFs binding to H1-compacted nucleosome arrays visualized by gel electrophoresis. Gel image is representative of 2 biological replicates. Lanes 1 and 8 are a partial EcoRI digest DNA marker (M) with fragments in basepairs corresponding to (from bottom to top): 624, 834, 1028, 1658, 1866, 2074, 2282, 2490, 2733. All lanes shown are from the same gel.

Source data

Extended Data Fig. 4 PU.1 and C/EBPα open chromatin cooperatively.

a, Schematic of DNase I digestion analysis. b, DNase I digestion analysis of TFs binding to H1-compacted nucleosome arrays visualized by gel electrophoresis. Gel image representative of 2 bioligcal replicates. c, Quantified Cy5 signal in each lane normalized to no TF control from n = 2 biological replicates in b.

Source data

Extended Data Fig. 5 DNA-binding domains of PU.1 and C/EBPα are sufficient for nucleosome binding.

a–d, Representative EMSAs from 2 biological repeats showing the affinity of increasing amounts of a, Full-length PU.1 (PU.1 FL), b, PU.1-DBD, c, Full-length C/EBPα (C/EBPα FL), d, C/EBP-DBD to Cy5-labeled Cx3cr1 free DNA (black arrows) or mononucleosomes (white arrows).

Source data

Extended Data Fig. 6 cBAF readily remodels extended nucleosome arrays but requires PU.1 to access H1-compacted arrays.

a, silver-stain of affinity-purified cBAF complexes from mammalian HEK293T cells expressing HA-DPF2. b, Schematic of XbaI accessibility assay with extended arrays and cBAF remodeling complex. c, Agarose gel visualization of XbaI accessibility assay of extended nucleosome arrays (no linker histone) incubated without and with cBAF plus ATP. Gel image representative of 2 biological replicates. Lanes 1 is a partial EcoRI digest DNA marker (M) with fragments in basepairs corresponding to (from bottom to top): 1658, 1866, 2074, 2282, 2490, 2733. d, Schematic of DNase I digestion analysis of transcription factors and cBAF with H1-compacted arrays. e, DNase I digestion analysis H1-compacted nucleosome arrays incubated alone (no TF, lanes 2 and 5), PU.1 alone (lanes 3 and 6), and PU.1 with cBAF and ATP (lanes 4 and 7). The same samples were used to perform nanopore sequencing shown in Fig. 3b. Lanes 1 and 8 are a partial EcoRI digest DNA marker (M) with fragments in basepairs corresponding to (from bottom to top): 208, 416, 624, 834, 1028, 1658, 1866, 2074, 2282, 2490, 2733.

Source data

Extended Data Fig. 7 Hierarchy of chromatin binding by PU.1 WT and mutants.

Representative EMSAs of 2 biological repeats showing the affinity of increasing amounts of a, WT PU.1, b, 𝚫IDR, c, 𝚫AQ to Cy5-labeled Cx3cr1 free DNA (black arrows) or mononucleosomes (white arrows). d, Schematic of EMSA performed with transcription factors and extended nucleosome arrays e, Representative EMSA of 2 biological repeats showing the affinity of increasing amounts of WT PU.1 (lanes 1-6), 𝚫IDR (lanes 7-12), and 𝚫AQ (lanes 13-18) to Cy5-labeled extended WT or TF motif mutant Cx3cr1 nucleosome arrays. f, Schematic of EMSA performed with transcription factors and H1-compacted nucleosome arrays. g, Representative EMSA of 2 biological replicates showing the affinity of increasing amounts of WT PU.1 (lanes 1-6), 𝚫IDR (lanes 7-12), and 𝚫AQ (lanes 13-18) to Cy5-labeled H1-compacted WT or TF motif mutant Cx3cr1 nucleosome arrays.

Source data

Extended Data Fig. 8 The IDR domain of PU.1 is most crucial for chromatin opening.

a, Illustration of the PU.1 deletion mutant series. Shown are the positions of the acidic domain (A), Q-rich domain (Q), intrinsically disordered region (IDR) and DNA-binding domain (DBD). b, DNase I digestion analysis of two transcription factor concentrations binding to H1-compacted nucleosome arrays visualized by gel electrophoresis (10 ng/uL DNase I). Two biological repeats are shown. Lanes 1 is a partial EcoRI digest DNA marker (M) with fragments in basepairs corresponding to (from bottom to top): 1028, 1658, 1866, 2074, 2282, 2490, 2733.c, DNase I digestion analysis of H1-compacted nucleosome arrays incubated with no TFs (contrl., lanes 2-5), WT PU.1 (lanes 6-9), DBD (lanes 10-13), and 𝚫IDR deletion (lanes 14-17) with or without the addition of cBAF and ATP. Gel image representative of two biological replicates.

Source data

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Supplementary Data 1

Full DNA sequence of the 2.7-kb Cx3cr1 array.

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Frederick, M.A., Williamson, K.E., Fernandez Garcia, M. et al. A pioneer factor locally opens compacted chromatin to enable targeted ATP-dependent nucleosome remodeling. Nat Struct Mol Biol 30, 31–37 (2023). https://doi.org/10.1038/s41594-022-00886-5

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