CircPrimer 2.0: a software for annotating circRNAs and predicting translation potential of circRNAs

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Abstract

Background

Some circular RNAs (circRNAs) can be translated into functional peptides by small open reading frames (ORFs) in a cap-independent manner. Internal ribosomal entry site (IRES) and N ⁶-methyladenosine (m ⁶A) were reported to drive translation of circRNAs. Experimental methods confirming the presence of IRES and m ⁶A site are time consuming and labor intensive. Lacking computational tools to predict ORFs, IRESs and m ⁶A sites for circRNAs makes it harder.

Results

In this report, we present circPrimer 2.0, a Java based software for annotating circRNAs and predicting ORFs, IRESs, and m6A sites of circRNAs. circPrimer 2.0 has a graphical and a command-line interface that enables the tool to be embed into an analysis pipeline.

Conclusions

circprimer 2.0 is an easy-to-use software for annotating circRNAs and predicting translation potential of circRNAs, and freely available at www.bio-inf.cn.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12859-022-04705-y.

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Most cited references 28

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Circ-ZNF609 Is a Circular RNA that Can Be Translated and Functions in Myogenesis

Ivano Legnini, Gaia Di Timoteo, Francesca Rossi … (2017)

Summary Circular RNAs (circRNAs) constitute a family of transcripts with unique structures and still largely unknown functions. Their biogenesis, which proceeds via a back-splicing reaction, is fairly well characterized, whereas their role in the modulation of physiologically relevant processes is still unclear. Here we performed expression profiling of circRNAs during in vitro differentiation of murine and human myoblasts, and we identified conserved species regulated in myogenesis and altered in Duchenne muscular dystrophy. A high-content functional genomic screen allowed the study of their functional role in muscle differentiation. One of them, circ-ZNF609, resulted in specifically controlling myoblast proliferation. Circ-ZNF609 contains an open reading frame spanning from the start codon, in common with the linear transcript, and terminating at an in-frame STOP codon, created upon circularization. Circ-ZNF609 is associated with heavy polysomes, and it is translated into a protein in a splicing-dependent and cap-independent manner, providing an example of a protein-coding circRNA in eukaryotes.

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Extensive translation of circular RNAs driven by N6-methyladenosine

Yun Yang, Xiaojuan Fan, Miaowei Mao … (2017)

Extensive pre-mRNA back-splicing generates numerous circular RNAs (circRNAs) in human transcriptome. However, the biological functions of these circRNAs remain largely unclear. Here we report that N 6-methyladenosine (m6A), the most abundant base modification of RNA, promotes efficient initiation of protein translation from circRNAs in human cells. We discover that consensus m6A motifs are enriched in circRNAs and a single m6A site is sufficient to drive translation initiation. This m6A-driven translation requires initiation factor eIF4G2 and m6A reader YTHDF3, and is enhanced by methyltransferase METTL3/14, inhibited by demethylase FTO, and upregulated upon heat shock. Further analyses through polysome profiling, computational prediction and mass spectrometry reveal that m6A-driven translation of circRNAs is widespread, with hundreds of endogenous circRNAs having translation potential. Our study expands the coding landscape of human transcriptome, and suggests a role of circRNA-derived proteins in cellular responses to environmental stress.

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Translation of CircRNAs

Nagarjuna Reddy Pamudurti, Osnat Bartok, Marvin Jens … (2017)

Summary Circular RNAs (circRNAs) are abundant and evolutionarily conserved RNAs of largely unknown function. Here, we show that a subset of circRNAs is translated in vivo. By performing ribosome footprinting from fly heads, we demonstrate that a group of circRNAs is associated with translating ribosomes. Many of these ribo-circRNAs use the start codon of the hosting mRNA, are bound by membrane-associated ribosomes, and have evolutionarily conserved termination codons. In addition, we found that a circRNA generated from the muscleblind locus encodes a protein, which we detected in fly head extracts by mass spectrometry. Next, by performing in vivo and in vitro translation assays, we show that UTRs of ribo-circRNAs (cUTRs) allow cap-independent translation. Moreover, we found that starvation and FOXO likely regulate the translation of a circMbl isoform. Altogether, our study provides strong evidence for translation of circRNAs, revealing the existence of an unexplored layer of gene activity.

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Author and article information

Contributors

Jifeng Feng:

ORCID: http://orcid.org/0000-0002-3541-2342

feng_jifeng@sina.com

Journal

Journal ID (nlm-ta): BMC Bioinformatics

Journal ID (iso-abbrev): BMC Bioinformatics

Title: BMC Bioinformatics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2105

Publication date (Electronic): 6 June 2022

Publication date PMC-release: 6 June 2022

Publication date Collection: 2022

Volume: 23

Electronic Location Identifier: 215

Affiliations

[1 ]GRID grid.452509.f, ISNI 0000 0004 1764 4566, Center of Clinical Laboratory Science, , The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, ; Nanjing, 210009 China

[2 ]GRID grid.452509.f, ISNI 0000 0004 1764 4566, Department of Medical Oncology, , The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer Research, ; Baiziting 42, Nanjing, 210009 China

Author information

Jifeng Feng http://orcid.org/0000-0002-3541-2342

Article

Publisher ID: 4705

DOI: 10.1186/s12859-022-04705-y

PMC ID: 9169404

PubMed ID: 35668371

SO-VID: c7b64ac2-9b6d-487a-b2d0-6e957ff0c2eb

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 7 July 2021

Date accepted : 29 April 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, national natural science foundation of china;

Award ID: 81602551

Award Recipient : Shanliang Zhong

Funded by: young talents program of jiangsu cancer hospital

Award ID: QL201810

Award Recipient : Shanliang Zhong

Funded by: Special Foundation for National Science and Technology Basic Research Program of China

Award ID: 2019FY101200

Award Recipient : Shanliang Zhong

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ScienceOpen disciplines: Bioinformatics & Computational biology

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CircPrimer 2.0: a software for annotating circRNAs and predicting translation potential of circRNAs

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Abstract

Background

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Supplementary Information

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Genetoberfest

Most cited references 28

Circ-ZNF609 Is a Circular RNA that Can Be Translated and Functions in Myogenesis

Extensive translation of circular RNAs driven by N6-methyladenosine

Translation of CircRNAs

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Cited by 11

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