SLERT Regulates DDX21 Rings Associated with Pol I Transcription

Dysregulated rRNA synthesis by RNA polymerase I (Pol I) is associated with uncontrolled cell proliferation. Here, we report a box H/ACA small nucleolar RNA (snoRNA)-ended long noncoding RNA (lncRNA) that enhances pre-rRNA transcription (SLERT). SLERT requires box H/ACA snoRNAs at both ends for its b...

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Bibliographic Details
Published in:Cell 2017-05, Vol.169 (4), p.664-678.e16
Main Authors: Xing, Yu-Hang, Yao, Run-Wen, Zhang, Yang, Guo, Chun-Jie, Jiang, Shan, Xu, Guang, Dong, Rui, Yang, Li, Chen, Ling-Ling
Format: Article
Language:English
Subjects:
Allosteric Site
Animals
Carcinogenesis
Cell Line
Cell Line, Tumor
DDX21
DEAD-box RNA Helicases - chemistry
DEAD-box RNA Helicases - metabolism
Female
Gene Knockout Techniques
Humans
Mice
Mice, Nude
nucleolus
RNA polymerase I
RNA Polymerase I - metabolism
RNA Precursors - genetics
RNA Precursors - metabolism
RNA, Long Noncoding - metabolism
SIM
SLERT
sno-lncRNA
Transcription, Genetic
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Summary:Dysregulated rRNA synthesis by RNA polymerase I (Pol I) is associated with uncontrolled cell proliferation. Here, we report a box H/ACA small nucleolar RNA (snoRNA)-ended long noncoding RNA (lncRNA) that enhances pre-rRNA transcription (SLERT). SLERT requires box H/ACA snoRNAs at both ends for its biogenesis and translocation to the nucleolus. Deletion of SLERT impairs pre-rRNA transcription and rRNA production, leading to decreased tumorigenesis. Mechanistically, SLERT interacts with DEAD-box RNA helicase DDX21 via a 143-nt non-snoRNA sequence. Super-resolution images reveal that DDX21 forms ring-shaped structures surrounding multiple Pol I complexes and suppresses pre-rRNA transcription. Binding by SLERT allosterically alters individual DDX21 molecules, loosens the DDX21 ring, and evicts DDX21 suppression on Pol I transcription. Together, our results reveal an important control of ribosome biogenesis by SLERT lncRNA and its regulatory role in DDX21 ring-shaped arrangements acting on Pol I complexes. [Display omitted] •SLERT is a box H/ACA snoRNA-ended lncRNA that enhances pre-rRNA transcription•DDX21 forms ring-shaped structures surrounding Pol I and inhibits Pol I transcription•SLERT binds to DDX21 and modulates DDX21 rings to evict their suppression on Pol I•SLERT-DDX21 interactions regulate differential expression of rDNAs A long non-coding RNA promotes pre-ribosomal RNA transcription by loosening the ring-shaped structure surrounding multiple RNA Pol I complexes formed by RNA helicase DDX21.
ISSN:0092-8674
1097-4172
DOI:10.1016/j.cell.2017.04.011