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Context-specific effects of sequence elements on subcellular localization of linear and circular RNAs

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  • Maya Ron

    (Weizmann Institute of Science)

  • Igor Ulitsky

    (Weizmann Institute of Science)

Abstract

Long RNAs vary extensively in their post-transcriptional fates, and this variation is attributed in part to short sequence elements. We used massively parallel RNA assays to study how sequences derived from noncoding RNAs influence the subcellular localization and stability of circular and linear RNAs, including spliced and unspliced forms. We find that the effects of sequence elements strongly depend on the host RNA context, with limited overlap between sequences that drive nuclear enrichment of linear and circular RNAs. Binding of specific RNA binding proteins underpins some of these differences—SRSF1 binding leads to nuclear enrichment of circular RNAs; SAFB binding is associated with nuclear enrichment of predominantly unspliced linear RNAs; and IGF2BP1 promotes export of linear spliced RNA molecules. The post-transcriptional fate of long RNAs is thus dictated by combinatorial contributions of specific sequence elements, of splicing, and of the presence of the terminal features unique to linear RNAs.

Suggested Citation

  • Maya Ron & Igor Ulitsky, 2022. "Context-specific effects of sequence elements on subcellular localization of linear and circular RNAs," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30183-0
    DOI: 10.1038/s41467-022-30183-0
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    1. Sebastian Memczak & Marvin Jens & Antigoni Elefsinioti & Francesca Torti & Janna Krueger & Agnieszka Rybak & Luisa Maier & Sebastian D. Mackowiak & Lea H. Gregersen & Mathias Munschauer & Alexander Lo, 2013. "Circular RNAs are a large class of animal RNAs with regulatory potency," Nature, Nature, vol. 495(7441), pages 333-338, March.
    2. Eric L. Nostrand & Peter Freese & Gabriel A. Pratt & Xiaofeng Wang & Xintao Wei & Rui Xiao & Steven M. Blue & Jia-Yu Chen & Neal A. L. Cody & Daniel Dominguez & Sara Olson & Balaji Sundararaman & Liju, 2020. "A large-scale binding and functional map of human RNA-binding proteins," Nature, Nature, vol. 583(7818), pages 711-719, July.
    3. Nian Liu & Cameron H. Lee & Tomek Swigut & Edward Grow & Bo Gu & Michael C. Bassik & Joanna Wysocka, 2018. "Selective silencing of euchromatic L1s revealed by genome-wide screens for L1 regulators," Nature, Nature, vol. 553(7687), pages 228-232, January.
    4. Lesca M. Holdt & Anika Stahringer & Kristina Sass & Garwin Pichler & Nils A. Kulak & Wolfgang Wilfert & Alexander Kohlmaier & Andreas Herbst & Bernd H. Northoff & Alexandros Nicolaou & Gabor Gäbel & F, 2016. "Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    5. Yoav Lubelsky & Igor Ulitsky, 2018. "Sequences enriched in Alu repeats drive nuclear localization of long RNAs in human cells," Nature, Nature, vol. 555(7694), pages 107-111, March.
    6. Debashish Ray & Hilal Kazan & Kate B. Cook & Matthew T. Weirauch & Hamed S. Najafabadi & Xiao Li & Serge Gueroussov & Mihai Albu & Hong Zheng & Ally Yang & Hong Na & Manuel Irimia & Leah H. Matzat & R, 2013. "A compendium of RNA-binding motifs for decoding gene regulation," Nature, Nature, vol. 499(7457), pages 172-177, July.
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