Dynamic nucleosome landscape elicits a noncanonical GATA2 pioneer model

Tianbao Li, Qi Liu, Zhong Chen, Kun Fang, Furong Huang, Xueqi Fu, Qianben Wang () and Victor X. Jin ()
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Tianbao Li: University of Texas Health Science Center at San Antonio
Qi Liu: University of Texas Health Science Center at San Antonio
Zhong Chen: Duke University School of Medicine
Kun Fang: University of Texas Health Science Center at San Antonio
Furong Huang: Duke University School of Medicine
Xueqi Fu: Jilin University
Qianben Wang: Duke University School of Medicine
Victor X. Jin: University of Texas Health Science Center at San Antonio

Nature Communications, 2022, vol. 13, issue 1, 1-10

Abstract: Abstract Knowledge gaps remain on how nucleosome organization and dynamic reorganization are governed by specific pioneer factors in a genome-wide manner. In this study, we generate over three billons of multi-omics sequencing data to exploit dynamic nucleosome landscape governed by pioneer factors (PFs), FOXA1 and GATA2. We quantitatively define nine functional nucleosome states each with specific characteristic nucleosome footprints in LNCaP prostate cancer cells. Interestingly, we observe dynamic switches among nucleosome states upon androgen stimulation, accompanied by distinct differential (gained or lost) binding of FOXA1, GATA2, H1 as well as many other coregulators. Intriguingly, we reveal a noncanonical pioneer model of GATA2 that it initially functions as a PF binding at the edge of a nucleosome in an inaccessible crowding array. Upon androgen stimulation, GATA2 re-configures an inaccessible to accessible nucleosome state and subsequently acts as a master transcription factor either directly or recruits signaling specific transcription factors to enhance WNT signaling in an androgen receptor (AR)-independent manner. Our data elicit a pioneer and master dual role of GATA2 in mediating nucleosome dynamics and enhancing downstream signaling pathways. Our work offers structural and mechanistic insight into the dynamics of pioneer factors governing nucleosome reorganization.

Date: 2022
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DOI: 10.1038/s41467-022-30960-x

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