MicroRNAs and their isomiRs function cooperatively to target common biological pathways

Cloonan, Nicole; Wani, Shivangi; Xu, Qinying; Gu, Jian; Lea, Kristi; Heater, Sheila; Barbacioru, Catalin; Steptoe, Anita L; Martin, Hilary C; Nourbakhsh, Ehsan; Krishnan, Keerthana; Gardiner, Brooke; Wang, Xiaohui; Nones, Katia; Steen, Jason A; Matigian, Nicholas A; Wood, David L; Kassahn, Karin S; Waddell, Nic; Shepherd, Jill; Lee, Clarence; Ichikawa, Jeff; McKernan, Kevin; Bramlett, Kelli; Kuersten, Scott; Grimmond, Sean M

doi:10.1186/gb-2011-12-12-r126

Cited by 345MicroRNA in disease regulationPlant Molecular Biology ResearchRNA Research and Splicing

MicroRNAs and their isomiRs function cooperatively to target common biological pathways

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Cloonan, Nicole, Wani, Shivangi, Xu, Qinying, Gu, Jian, Lea, Kristi, Heater, Sheila, Barbacioru, Catalin, Steptoe, Anita L +18 more·2011·Genome Biology

DOI 10.1186/gb-2011-12-12-r126PMC PMC3334621

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Abstract

Background: Variants of microRNAs (miRNAs), called isomiRs, are commonly reported in deep-sequencing studies; however, the functional significance of these variants remains controversial. Observational studies show that isomiR patterns are non-random, hinting that these molecules could be regulated and therefore functional, although no conclusive biological role has been demonstrated for these molecules. Results: To assess the biological relevance of isomiRs, we have performed ultra-deep miRNA-seq on ten adult human tissues, and created an analysis pipeline called miRNA-MATE to align, annotate, and analyze miRNAs and their isomiRs. We find that isomiRs share sequence and expression characteristics with canonical miRNAs, and are generally strongly correlated with canonical miRNA expression. A large proportion of isomiRs potentially derive from AGO2 cleavage independent of Dicer. We isolated polyribosome-associated mRNA, captured the mRNA-bound miRNAs, and found that isomiRs and canonical miRNAs are equally associated with translational machinery. Finally, we transfected cells with biotinylated RNA duplexes encoding isomiRs or their canonical counterparts and directly assayed their mRNA targets. These studies allow us to experimentally determine genome-wide mRNA targets, and these experiments showed substantial overlap in functional mRNA networks suppressed by both canonical miRNAs and their isomiRs. Conclusions: Together, these results find isomiRs to be biologically relevant and functionally cooperative partners of canonical miRNAs that act coordinately to target pathways of functionally related genes. This work exposes the complexity of the miRNA-transcriptome, and helps explain a major miRNA paradox: how specific regulation of biological processes can occur when the specificity of miRNA targeting is mediated by only 6 to 11 nucleotides.

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PCR enrichment using a primer targeted to the miRNA causes final reads to lose the original miRNA sequence present in the miRNA:mRNA chimeric molecule, leading to loss of information about differential targeting of miRNA family members and isomiRs.
“Next, because of the use of a primer targeted to the miRNA, the final reads reflect amplified products and have lost the original miRNA sequence present in the miRNA:mRNA chimeric molecule, leading to loss of information about differential targeting of miRNA family members (which often only contain a single nucleotide difference), and isomiRs or other variations which have been described to play”
From Scalable and deep profiling of mRNA targets for individual microRNAs with chimeric eCLIP (2022) · cites this paper as Cloonan et al., 2011
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Experimental — accuracy not yet measured
NGS analysis would enable detection of presently unknown miRNAs as well as miRNA isoforms that have demonstrated to target biological pathways in a cooperative manner (16).
“However, NGS analysis would enable to detect presently unknown miRNAs as well miRNAs iso-forms that have demonstrated to target biological pathways in a cooperative manner (16).”
From Distribution of miRNA expression across human tissues (2016) · cites this paper as [16]

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Maroney PA Yu Y Fisher J Nilsen TW Evidence that microRNAs are associated with translating messenger RNAs in human cells. Nat Struct Mol Biol 2006 13 1102 1107 10.1038/nsmb1174 17128271 · DOI

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Authors: Cloonan, N., Wani, S., Xu, Q., Gu, J., Lea, K., Heater, S., Barbacioru, C., Steptoe, A. L., Martin, H. C., Nourbakhsh, E., Krishnan, K., Gardiner, B., Wang, X., Nones, K., Steen, J. A., Matigian, N. A., Wood, D. L., Kassahn, K. S., Waddell, N., Shepherd, J., Lee, C., Ichikawa, J., McKernan, K., Bramlett, K., Kuersten, S., & Grimmond, S. M.
Affiliations: The University of Queensland (AU)
Corresponding author: Cloonan, Nicole
Kuersten, Scott
Grimmond, Sean M
ORCID: Cloonan, Nicole
Wani, Shivangi
Gu, Jian
Martin, Hilary C
Nourbakhsh, Ehsan
Krishnan, Keerthana
Gardiner, Brooke
Wang, Xiaohui
Steen, Jason A
Matigian, Nicholas A
Wood, David L
Kassahn, Karin S
Lee, Clarence
McKernan, Kevin
Kuersten, Scott
Grimmond, Sean M
Venue: Genome Biology
Publisher: Springer Science and Business Media LLC
Published: 2011-12-30
Volume: 12
Issue: 12
Pages: R126-R126
ISSN: 1465-6906 (ISSN-L)
1474-760X
DOI: 10.1186/gb-2011-12-12-r126
PMC: PMC3334621
OpenAlex: W2119942258
Cited by: 345
References: 79
Citations by year: 2026: 6 · 2025: 13 · 2024: 12 · 2023: 13 · 2022: 24 · 2021: 21 · 2020: 29 · 2019: 27 · 2018: 21 · 2017: 35 · 2016: 23 · 2015: 29 · 2014: 34 · 2013: 39 · 2012: 19
FWCI: 10.01
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/2.0/ (tdm)
creativecommons.org/licenses/by/2.0/ (vor)
Locations: Genome biology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Kent Academic Repository (University of Kent) (acceptedVersion)
Minerva Access (University of Melbourne) (submittedVersion, cc-by)
Griffith Research Online (submittedVersion, cc-by)
Funders: Medical Research Council
Australian Research Council (DP0988754, DP1093164)
National Health and Medical Research Council
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords: microRNA isomiRs, miRNA target networks
MeSH terms: Base Sequence, HeLa Cells, Humans, Molecular Sequence Data, RNA, Messenger, Transfection, Sequence Alignment, Biotinylation, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, MicroRNAs, Ribonuclease III, Gene Regulatory Networks, DEAD-box RNA Helicases, HEK293 Cells, High-Throughput Nucleotide Sequencing, Transcriptome, Argonaute Proteins

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