Evidence map›Paper›PMID 33820973›Full record

ArticleNature cell biology2021

PANDORA-seq expands the repertoire of regulatory small RNAs by overcoming RNA modifications.

Junchao Shi, Yunfang Zhang, Dongmei Tan, Xudong Zhang, Menghong Yan, Ying Zhang, Reuben Franklin, Marta Shahbazi, Kirsty Mackinlay, Shichao Liu and 22 more

Erratum issuedOpen access · greenAbstract read
PubMed Full text at PMC Publisher
In one paragraph

Article in Nature cell biology, 2021. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 200 papers.

0numbers the graph read from it
0cells of the map it votes in
200citing papers in PubMed
14.3field-weighted citation impact, top 1% 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

200 citing papers in PubMed, 271 citations in OpenAlex.

  1. Article
  2. Review
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  5. Defining cell surface and glycosylated RNAs.Trends in genetics : TIG · 2026
    Review
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  11. Review
  12. Review
  13. Review
  14. Review
  15. Article
  16. Paternal Circadian Disruption Impairs Offspring Cognition via Sperm microRNAs.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026
    Article
  17. Article
  18. Article
  19. Article
  20. Article

140 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

32 authors at 10 institutions in 3 countries.

Junchao Shi *Division of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, CA, USA.ORCID http://orcid.org/0000-0002-1548-5069
Yunfang Zhang *Department of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA.
Dongmei Tan *Department of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA.
Xudong Zhang *Division of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, CA, USA.
Menghong Yan *Department of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA.
Ying Zhang *Division of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, CA, USA.
Reuben Franklin *Department of Biochemistry, Stem Cell Center, University of California, Riverside, Riverside, CA, USA.
Marta ShahbaziDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.ORCID http://orcid.org/0000-0002-1599-5747
Kirsty MackinlayDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.
Shichao LiuDivision of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, CA, USA.
Bernhard KuhleDepartment of Molecular Medicine, The Scripps Research Institute, La Jolla, CA, USA.ORCID http://orcid.org/0000-0002-0501-1150
Emma R JamesDivision of Urology, Department of Surgery, University of Utah School of Medicine, Salt Lake City, UT, USA.
Liwen ZhangState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
Yongcun QuState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
Qiwei ZhaiCAS Key Laboratory of Nutrition, Metabolism and Food Safety, CAS Center for Excellence in Molecular Cell Sciences, Shanghai Institute of Nutrition and Health, Chinese Academy of Sciences, Shanghai, China.ORCID http://orcid.org/0000-0002-9617-7403
Wenxin ZhaoDepartment of Chemistry, University of California, Riverside, Riverside, CA, USA.
Linlin ZhaoDepartment of Chemistry, University of California, Riverside, Riverside, CA, USA.ORCID http://orcid.org/0000-0002-8821-4198
Changcheng ZhouDivision of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, CA, USA.ORCID http://orcid.org/0000-0001-7649-0710
Weifeng GuDepartment of Molecular, Cell and Systems Biology, University of California, Riverside, Riverside, CA, USA.
Jernej MurnDepartment of Biochemistry, Stem Cell Center, University of California, Riverside, Riverside, CA, USA.
Jingtao GuoDivision of Urology, Department of Surgery, University of Utah School of Medicine, Salt Lake City, UT, USA.
Douglas T CarrellDivision of Urology, Department of Surgery, University of Utah School of Medicine, Salt Lake City, UT, USA.
Yinsheng WangDepartment of Chemistry, University of California, Riverside, Riverside, CA, USA.ORCID http://orcid.org/0000-0001-5565-283X
Xuemei ChenDepartment of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, USA.ORCID http://orcid.org/0000-0002-5209-1157
Bradley R CairnsHoward Hughes Medical Institute, Department of Oncological Sciences and Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.ORCID http://orcid.org/0000-0002-9864-8811
Xiang-Lei YangDepartment of Molecular Medicine, The Scripps Research Institute, La Jolla, CA, USA.ORCID http://orcid.org/0000-0003-2554-084X
Paul SchimmelDepartment of Molecular Medicine, The Scripps Research Institute, La Jolla, CA, USA.
Magdalena Zernicka-GoetzDepartment of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK.ORCID http://orcid.org/0000-0002-7004-2471
Sihem CheloufiDepartment of Biochemistry, Stem Cell Center, University of California, Riverside, Riverside, CA, USA. cheloufi@ucr.edu.ORCID http://orcid.org/0000-0002-1726-4796
Ying ZhangState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China. yingzhanglab@gmail.com.
Tong ZhouDepartment of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Reno, NV, USA. tongz@med.unr.edu.ORCID http://orcid.org/0000-0003-2361-1931
Qi ChenDivision of Biomedical Sciences, School of Medicine, University of California, Riverside, Riverside, CA, USA. qi.chen@medsch.ucr.edu.ORCID http://orcid.org/0000-0001-6353-9589
University of California, Riverside · USChinese Academy of Sciences · CNScripps Research Institute · USHoward Hughes Medical Institute · USUniversity of Nevada, Reno · USUniversity of Utah · USCalifornia Institute of Technology · USMRC Laboratory of Molecular Biology · GBShanghai Medical College of Fudan University · CNUniversity of Cambridge · GB

Funding

VIRAL MALIGNANCYP30CA023100 · NCI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI Jesse Nodora · 1985 to 2026
$124.9M
Transgenic & Knock-out MouseP30DK063491 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI Andrea L Hevener · 2003 to 2026
$40.4M
San Diego Digestive Diseases Research CenterP30DK120515 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI Bernd G. Schnabl · 2019 to 2026
$10.8M
Mechanism Underlying the Transduction of Epimutations from the Soma to the Male GermlineP50HD098593 · NICHD · UNIVERSITY OF NEVADA RENO · PI YAN, WEI · 2019 to 2024
$7.2M
Sperm tsRNAs/rsRNAs and their RNA modifications in diet-induced epigenetic inheritanceR01HD092431 · NICHD · UTAH STATE HIGHER EDUCATION SYSTEM--UNIVERSITY OF UTAH · PI Qi Chen, David S Milstone · 2017 to 2026
$3.5M
Chemical and Molecular Mechanisms of Mitochondrial DNA DegradationR35GM128854 · NIGMS · UNIVERSITY OF CALIFORNIA RIVERSIDE · PI Linlin Zhao · 2018 to 2026
$3.1M
Exploring the Functions of tRNA Synthetases in the Nucleus and their Relationship to CMTR01NS113583 · NINDS · SCRIPPS RESEARCH INSTITUTE, THE · PI BURGESS, ROBERT W., YANG, XIANG-LEI · 2020 to 2024
$2.9M
Decoding the signature of sperm RNA & RNA modification of environmental stressors on the intergenerational transmission of metabolic phenotypesR01ES032024 · NIEHS · UNIVERSITY OF UTAH · PI CHEN, QI, ZHOU, TONG · 2020 to 2024
$2.1M
A Novel RNA Polyphosphatase PIR-1 Plays Important Roles in Silencing Viruses and Regulating Genes in C. elegansR01GM124349 · NIGMS · UNIVERSITY OF CALIFORNIA RIVERSIDE · PI GU, WEIFENG · 2018 to 2022
$1.8M
Biotechnology and Biological Sciences Research CouncilHoward Hughes Medical InstituteNCI NIH HHS P30 CA023100NICHD NIH HHS P50 HD098593NICHD NIH HHS R01 HD092431NIDDK NIH HHS P30 DK063491NIDDK NIH HHS P30 DK120515NIEHS NIH HHS R01 ES032024NIGMS NIH HHS R01 GM124349NIGMS NIH HHS R35 GM128854NINDS NIH HHS R01 NS113583Wellcome TrustWellcome Trust 207415/Z/17/Z
6 · The paper itself

Abstract

Although high-throughput RNA sequencing (RNA-seq) has greatly advanced small non-coding RNA (sncRNA) discovery, the currently widely used complementary DNA library construction protocol generates biased sequencing results. This is partially due to RNA modifications that interfere with adapter ligation and reverse transcription processes, which prevent the detection of sncRNAs bearing these modifications. Here, we present PANDORA-seq (panoramic RNA display by overcoming RNA modification aborted sequencing), employing a combinatorial enzymatic treatment to remove key RNA modifications that block adapter ligation and reverse transcription. PANDORA-seq identified abundant modified sncRNAs-mostly transfer RNA-derived small RNAs (tsRNAs) and ribosomal RNA-derived small RNAs (rsRNAs)-that were previously undetected, exhibiting tissue-specific expression across mouse brain, liver, spleen and sperm, as well as cell-specific expression across embryonic stem cells (ESCs) and HeLa cells. Using PANDORA-seq, we revealed unprecedented landscapes of microRNA, tsRNA and rsRNA dynamics during the generation of induced pluripotent stem cells. Importantly, tsRNAs and rsRNAs that are downregulated during somatic cell reprogramming impact cellular translation in ESCs, suggesting a role in lineage differentiation.

Indexed as

RNA-SeqDNA, ComplementaryHeLa CellsHumansMicroRNAsRNA Processing, Post-TranscriptionalRNA, RibosomalRNA, Small UntranslatedTranscriptomeDNA, ComplementaryMicroRNAsRNA, RibosomalRNA, Small Untranslated

Identifiers

PMID33820973
PMCPMC8236090
OpenAlexW3139572365

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Registered trials

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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 OpenQuestion graph.