Evidence map›Paper›PMID 37792516›Full record

ArticleProceedings of the National Academy of Sciences of the United States of America2023

A snoRNA-tRNA modification network governs codon-biased cellular states.

Minjie Zhang, Kongpan Li, Jianhui Bai, Ryan Van Damme, Wei Zhang, Mario Alba, Bangyan L Stiles, Jian-Fu Chen, Zhipeng Lu

Open access · greenAbstract read
In one paragraph

Article in Proceedings of the National Academy of Sciences of the United States of America, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 31 papers.

0numbers the graph read from it
0cells of the map it votes in
31citing papers in PubMed
5.4field-weighted citation impact, top 4% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

31 citing papers in PubMed, 35 citations in OpenAlex.

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  9. Genome-wide profiling of RNA 2'-bioRxiv : the preprint server for biology · 2025
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4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

9 authors at 1 institution in 1 country.

Minjie Zhang *Department of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.ORCID 0000-0001-8561-0729
Kongpan Li *Department of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.
Jianhui Bai *Department of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.
Ryan Van DammeDepartment of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.
Wei ZhangCenter for Craniofacial Molecular Biology, University of Southern California, Los Angeles, CA 90089.
Mario AlbaDepartment of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.
Bangyan L StilesDepartment of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.ORCID 0000-0001-5480-2074
Jian-Fu ChenCenter for Craniofacial Molecular Biology, University of Southern California, Los Angeles, CA 90089.
Zhipeng LuDepartment of Pharmacology and Pharmaceutical Sciences, University of Southern California, Los Angeles, CA 90089.ORCID 0000-0001-5124-7546
University of Southern California · US

Funding

USC/NORRIS COMPREHENSIVE CANCER CENTER (CORE) SUPPORTP30CA014089 · NCI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI MYLES G COCKBURN · 1985 to 2026
$181.4M
The Southernearch Center for ALPD and CirrhosisP50AA011999 · NIAAA · UNIVERSITY OF SOUTHERN CALIFORNIA · PI ANNA S. GUKOVSKAYA · 1999 to 2026
$45.8M
USC RESEARCH CENTER FOR LIVER DISEASES: PILOT PROGRAMSP30DK048522 · NIDDK · UNIVERSITY OF SOUTHERN CALIFORNIA · PI OOKHTENS, MURAD · 1995 to 2020
$21.8M
Decoding global RNP topologies in splicing regulationR01HG012928 · NHGRI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI Zhipeng Lu · 2023 to 2026
$2.2M
High Throughput Determination of RNA 3D Structures and Dynamics in VivoR35GM143068 · NIGMS · UNIVERSITY OF SOUTHERN CALIFORNIA · PI LU, ZHIPENG · 2021 to 2025
$2.1M
Decoding the RNA Structurome: Method Development and Function Analysis.R00HG009662 · NHGRI · UNIVERSITY OF SOUTHERN CALIFORNIA · PI LU, ZHIPENG · 2019 to 2021
$821k
NCI NIH HHS P30 CA014089NHGRI NIH HHS R00 HG009662NHGRI NIH HHS R01 HG012928NIAAA NIH HHS P50 AA011999NIDDK NIH HHS P30 DK048522NIGMS NIH HHS R35 GM143068
6 · The paper itself

Abstract

The dynamic balance between tRNA supply and codon usage demand is a fundamental principle in the cellular translation economy. However, the regulation and functional consequences of this balance remain unclear. Here, we use PARIS2 interactome capture, structure modeling, conservation analysis, RNA-protein interaction analysis, and modification mapping to reveal the targets of hundreds of snoRNAs, many of which were previously considered orphans. We identify a snoRNA-tRNA interaction network that is required for global tRNA modifications, including 2'-O-methylation and others. Loss of Fibrillarin, the snoRNA-guided 2'-O-methyltransferase, induces global upregulation of tRNA fragments, a large group of regulatory RNAs. In particular, the snoRNAs D97/D133 guide the 2'-O-methylation of multiple tRNAs, especially for the amino acid methionine (Met), a protein-intrinsic antioxidant. Loss of D97/D133 snoRNAs in human HEK293 cells reduced target tRNA levels and induced codon adaptation of the transcriptome and translatome. Both single and double knockouts of D97 and D133 in HEK293 cells suppress Met-enriched proliferation-related gene expression programs, including, translation, splicing, and mitochondrial energy metabolism, and promote Met-depleted programs related to development, differentiation, and morphogenesis. In a mouse embryonic stem cell model of development, knockdown and knockout of D97/D133 promote differentiation to mesoderm and endoderm fates, such as cardiomyocytes, without compromising pluripotency, consistent with the enhanced development-related gene expression programs in human cells. This work solves a decades-old mystery about orphan snoRNAs and reveals a function of snoRNAs in controlling the codon-biased dichotomous cellular states of proliferation and development.

Indexed as

Codon UsageRNA, Small NucleolarAnimalsCodonHEK293 CellsHumansMiceRNA, TransferCodonRNA, Small NucleolarRNA, Transfercodon usageRNA modificationssnoRNAstem celltRNA

Identifiers

PMID37792516
PMCPMC10576143
OpenAlexW4387332208

What Socratic holds

Textmetadata
LicenceCC BY-NC-ND
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the Socratic graph.