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Structure paper

TitleStructural insights into human Pol III transcription initiation in action.
Journal, issue, pagesNature, Year 2025
Publish dateJun 4, 2025
AuthorsQianmin Wang / Yulei Ren / Qianwei Jin / Xizi Chen / Yanhui Xu /
PubMed AbstractRNA polymerase III (Pol III) transcribes highly demanded RNAs grouped into three types of classical promoters, including type 1 (5S rRNA), type 2 (tRNA) and type 3 (short non-coding RNAs, such as U6, ...RNA polymerase III (Pol III) transcribes highly demanded RNAs grouped into three types of classical promoters, including type 1 (5S rRNA), type 2 (tRNA) and type 3 (short non-coding RNAs, such as U6, 7SK and RNase H1) promoters. While structures of the Pol III preinitiation complex (PIC) and elongation complex (EC) have been determined, the mechanism underlying the transition from initiation to elongation remains unclear. Here we reconstituted seven human Pol III transcribing complexes (TC4, TC5, TC6, TC8, TC10, TC12 and TC13) halted on U6 promoters with nascent RNAs of 4-13 nucleotides. Cryo-electron microscopy structures captured initially transcribing complexes (ITCs; TC4 and TC5) and ECs (TC6-13). Together with KMnO footprinting, the data reveal extensive modular rearrangements: the transcription bubble expands from PIC to TC5, followed by general transcription factor (GTF) dissociation and abrupt bubble collapse from TC5 to TC6, marking the ITC-EC transition. In TC5, SNAPc and TFIIIB remain bound to the promoter and Pol III, while the RNA-DNA hybrid adopts a tilted conformation with template DNA blocked by BRF2, a TFIIIB subunit. Hybrid forward translocation during ITC-EC transition triggers BRF2-finger retraction, GTF release and transcription-bubble collapse. Pol III then escapes the promoter while GTFs stay bound upstream, potentially enabling reinitiation. These findings reveal molecular insights into Pol III dynamics and reinitiation mechanisms on type 3 promoters of highly demanded small RNAs, with the earliest documented initiation-elongation transition for an RNA polymerase.
External linksNature / PubMed:40468065
MethodsEM (single particle)
Resolution2.8 - 4.8 Å
Structure data

61994

9k2g

EMDB-61994, PDB-9k2g:
Human RNA Polymerase III de novo transcribing complex 13 (TC13)
Method: EM (single particle) / Resolution: 3.0 Å

62006

9k36

EMDB-62006, PDB-9k36:
Human RNA Polymerase III de novo transcribing complex 12 (TC12)
Method: EM (single particle) / Resolution: 2.9 Å

62008

9k38

EMDB-62008, PDB-9k38:
Human RNA Polymerase III de novo transcribing complex 6 (TC6)
Method: EM (single particle) / Resolution: 3.1 Å

62010

9k39

EMDB-62010, PDB-9k39:
Human RNA Polymerase III de novo transcribing complex 8 (TC8)
Method: EM (single particle) / Resolution: 2.8 Å

62012

9k3b

EMDB-62012, PDB-9k3b:
Human RNA Polymerase III de novo transcribing complex 10 overall (TC10-overall)
Method: EM (single particle) / Resolution: 4.8 Å

62029

9k3u

EMDB-62029, PDB-9k3u:
Human RNA Polymerase III de novo transcribing complex 5 (TC5)
Method: EM (single particle) / Resolution: 3.0 Å

62030

9k3v

EMDB-62030, PDB-9k3v:
Human RNA Polymerase III de novo transcribing complex 4 (TC4)
Method: EM (single particle) / Resolution: 3.5 Å

63186

9lkt

EMDB-63186, PDB-9lkt:
Human RNA Polymerase III de novo transcribing complex 10 (TC10)
Method: EM (single particle) / Resolution: 3.5 Å

63482

9lxn

EMDB-63482, PDB-9lxn:
Human RNA Polymerase III de novo transcribing complex 5 (TC5)(without 3'dATP)
Method: EM (single particle) / Resolution: 3.3 Å

63483

9lxo

EMDB-63483, PDB-9lxo:
Human RNA Polymerase III de novo transcribing complex 6 (TC6)(without 3'dATP)
Method: EM (single particle) / Resolution: 3.6 Å

Chemicals

ChemComp-ZN:
Unknown entry

ChemComp-MG:
Unknown entry

ChemComp-3AT:
3'-DEOXYADENOSINE-5'-TRIPHOSPHATE

ChemComp-SF4:
IRON/SULFUR CLUSTER

ChemComp-GTP:
GUANOSINE-5'-TRIPHOSPHATE / GTP, energy-carrying molecule*YM

Source
  • homo sapiens (human)
KeywordsTRANSCRIPTION/DNA/RNA / Elongation complex / TRANSCRIPTION-DNA-RNA complex / initiation transcribing complex / Transcription initiation / complex

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