Chromosomes and Gene Expression

Fragile nucleosomes are essential for RNA Polymerase II to transcribe in eukaryotes

Lingbo Li
Samuel Hunter
Sonia Leach
Yonghua Zhuang
Haolin Liu
Junfeng Gao
Qianqian Zhang
Timothy J Stasevich
Hiroshi Kimura
Robin Dowell
Gongyi Zhang author has email address

Department of Immunology and Genomic Medicine, National Jewish Health, Denver, United States;
Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, United States;
Biostatistics Shared Resource, University of Colorado Cancer Center, University of Colorado Anschutz Medical Campus, Aurora, United States;
School of Medicine, Zhejiang University, Hangzhou, China;
Department of Biochemistry & Molecular Biology, Colorado State University, Fort Collins, United States;
Cell Biology Center, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama, Japan;
Department of Immunology and Microbiology, School of Medicine, Anschutz Medical Campus, University of Colorado, Aurora, United States

https://doi.org/10.7554/eLife.109411.1

Open access
Copyright information

Figures and data

Genome-wide distribution of pan-acetylation, pan-phosphorylation, active Pol II, RNAs in human HEK293T cells.
A. Acetylated H3K9. B. Acetylated H4K12. C. Active elongating Pol IIs (Ser2ph-CTD of Pol II). D. mRNAs. E. Phosphorylated H3S10. F. Phosphorylated H4S1.

Three types of histone modifications along gene bodies in HEK293T cells and promoter-only acetylation.
A. Pan-acetylation dominated genes. B. Pan-phosphorylation dominated genes. C. Both pan-acetylation and pan-phosphorylation genes. D. Acetylation at promoters.

Classified Protein-coding Genes

Transcription is completely shut down by DRB (for a total of 4,772 no-overlapping genes).
A. DRB completely inhibits the phosphorylation of Ser5-CTD of Rpd1 of Pol II. B. PRO-seq results of genome-wide of HEK293 after inhibition by DRB at 5 minutes, 15 minutes, and 30 minutes. C. Examples of the gradual shutdown of genes with time course after adding DRB.

Active Pol IIs are lost with the addition of DRB while they come back with the removal of DRB (for a total of 4,772 no-overlapping genes).
A. Active Pol IIs gradually disappear with DRB. B. Active Pol IIs come back with the removal of DRB.

Pan-acetylation couples with transcription activation (total of 13,940 genes, with 5,009 acetylation-dominated genes and with 8,931 both acetylation and phosphorylation).
A. DRB inhibition leads to the drop of H3K9ac while H3K9ac comes back with the removal of DRB. B. The change of H4K12ac has a similar pattern to that of H4K12ac.

Pan-phosphorylation couples with transcription activation (Total of 10,411 genes, with 1480 phosphorylation dominated and with 8,931 both acetylation and phosphorylation).
A. DRB inhibition leads to the drop of H3S10ph while H3S10ph comes back with the removal of DRB. B. The change of H4S1ph has a similar pattern to that of H3S10ph.

A model of the general transcription regulation mechanism of Pol II in eukaryotes.
Methylated H3.3K4 usually exists at the promoters (-1) and the enhancers (-N). Four forms of fragile nucleosomes, including “tailless,” “pan-acetylated,” “pan-phosphorylated,” and “both acetylated and phosphorylated” within gene bodies (+1/N), are generated in metazoans for Pol II to transcribe along gene bodies smoothly.

A general model of transcription from bacteria to human beings.
RNAPs could be blocked by nucleosomes or hexasomes with or without arginine methylation. RNAPs could transcribe on naked DNA (in bacteria), tailless nucleosomes (in Archaea), tail-cleaved nucleosomes (+1 nucleosome for some genes in metazoans), pan-acetylated nucleosomes, pan-phosphorylated nucleosomes, both pan-acetylated and pan-phosphorylated nucleosomes.

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