Detection of a 7SL RNA-derived small non-coding RNA using Molecular Beacons
fluorescence
imaging
live cell
molecular beacon
piRNA
sncRNA
Journal
Biological chemistry
ISSN: 1437-4315
Titre abrégé: Biol Chem
Pays: Germany
ID NLM: 9700112
Informations de publication
Date de publication:
26 10 2023
26 10 2023
Historique:
received:
14
04
2023
accepted:
11
08
2023
medline:
9
11
2023
pubmed:
27
8
2023
entrez:
26
8
2023
Statut:
epublish
Résumé
Small non-coding RNAs (sncRNA) are involved in many steps of the gene expression cascade and regulate processing and expression of mRNAs by the formation of ribonucleoprotein complexes (RNP) such as the RNA-induced silencing complex (RISC). By analyzing small RNA Seq data sets, we identified a sncRNA annotated as piR-hsa-1254, which is likely derived from the 3'-end of 7SL RNA2 (RN7SL2), herein referred to as snc7SL RNA. The 7SL RNA is an abundant long non-coding RNA polymerase III transcript and serves as structural component of the cytoplasmic signal recognition particle (SRP). To evaluate a potential functional role of snc7SL RNA, we aimed to define its cellular localization by live cell imaging. Therefore, a Molecular Beacon (MB)-based method was established to compare the subcellular localization of snc7SL RNA with its precursor 7SL RNA. We designed and characterized several MBs
Identifiants
pubmed: 37632732
pii: hsz-2023-0185
doi: 10.1515/hsz-2023-0185
doi:
Substances chimiques
7SL RNA
0
Signal Recognition Particle
0
RNA
63231-63-0
RNA, Small Cytoplasmic
0
RNA, Messenger
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1123-1136Informations de copyright
© 2023 the author(s), published by De Gruyter, Berlin/Boston.
Références
Alexander, J.C., Pandit, A., Bao, G., Connolly, D., and Rochev, Y. (2011). Monitoring mRNA in living cells in a 3D in vitro model using TAT-peptide linked molecular beacons. Lab Chip 11: 3908–3914, https://doi.org/10.1039/c1lc20447e .
doi: 10.1039/c1lc20447e
Andersen, E.S., Rosenblad, M.A., Larsen, N., Westergaard, J.C., Burks, J., Wower, I.K., Wower, J., Gorodkin, J., Samuelsson, T., and Zwieb, C. (2006). The tmRDB and SRPDB resources. Nucleic Acids Res. 34: D163–D168, https://doi.org/10.1093/nar/gkj142 .
doi: 10.1093/nar/gkj142
Basilio Barbosa, V., De Oliveira Martins, E., and Weber, G. (2019). Nearest-neighbour parameters optimized for melting temperature prediction of DNA/RNA hybrids at high and low salt concentrations. Biophys. Chem. 251: 106189, https://doi.org/10.1016/j.bpc.2019.106189 .
doi: 10.1016/j.bpc.2019.106189
Bohlander, P.R., Abba, M.L., Bestvater, F., Allgayer, H., and Wagenknecht, H.A. (2016). Two wavelength-shifting molecular beacons for simultaneous and selective imaging of vesicular miRNA-21 and miRNA-31 in living cancer cells. Org. Biomol. Chem. 14: 5001–5006, https://doi.org/10.1039/c6ob00691d .
doi: 10.1039/c6ob00691d
Bonnet, G., Tyagi, S., Libchaber, A., and Kramer, F.R. (1999). Thermodynamic basis of the enhanced specificity of structured DNA probes. Proc. Natl. Acad. Sci. U. S. A. 96: 6171–6176, https://doi.org/10.1073/pnas.96.11.6171 .
doi: 10.1073/pnas.96.11.6171
Bovia, F. and Strub, K. (1996). The signal recognition particle and related small cytoplasmic ribonucleoprotein particles. J. Cell Sci. 109: 2601–2608, https://doi.org/10.1242/jcs.109.11.2601 .
doi: 10.1242/jcs.109.11.2601
Bratu, D.P., Cha, B.J., Mhlanga, M.M., Kramer, F.R., and Tyagi, S. (2003). Visualizing the distribution and transport of mRNAs in living cells. Proc. Natl. Acad. Sci. U. S. A. 100: 13308–13313, https://doi.org/10.1073/pnas.2233244100 .
doi: 10.1073/pnas.2233244100
Chen, A.K., Rhee, W.J., Bao, G., and Tsourkas, A. (2011). Delivery of molecular beacons for live-cell imaging and analysis of RNA. Methods Mol. Biol. 714: 159–174, https://doi.org/10.1007/978-1-61779-005-8_10 .
doi: 10.1007/978-1-61779-005-8_10
Cole, C., Sobala, A., Lu, C., Thatcher, S.R., Bowman, A., Brown, J.W., Green, P.J., Barton, G.J., and Hutvagner, G. (2009). Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 15: 2147–2160, https://doi.org/10.1261/rna.1738409 .
doi: 10.1261/rna.1738409
Consortium, R.N., Petrov, A.I., Ribas, C.E., Finn, R.D., Bateman, A., Szymanski, M., Karlowski, W.M., Seemann, S.E., Gorodkin, J., Cannone, J.J., et al.. (2021). RNAcentral 2021: secondary structure integration, improved sequence search and new member databases. Nucleic Acids Res. 49: D212–D220, https://doi.org/10.1093/nar/gkaa921 .
doi: 10.1093/nar/gkaa921
Czech, B. and Hannon, G.J. (2016). One loop to rule them all: the ping-pong cycle and piRNA-guided silencing. Trends Biochem. Sci. 41: 324–337, https://doi.org/10.1016/j.tibs.2015.12.008 .
doi: 10.1016/j.tibs.2015.12.008
De Marco Zompit, M. and Stucki, M. (2021). Mechanisms of genome stability maintenance during cell division. DNA Repair (Amst) 108: 103215, https://doi.org/10.1016/j.dnarep.2021.103215 .
doi: 10.1016/j.dnarep.2021.103215
Dieci, G., Fiorino, G., Castelnuovo, M., Teichmann, M., and Pagano, A. (2007). The expanding RNA polymerase III transcriptome. Trends Genet. 23: 614–622, https://doi.org/10.1016/j.tig.2007.09.001 .
doi: 10.1016/j.tig.2007.09.001
Ferreira, I., Jolley, E.A., Znosko, B.M., and Weber, G. (2019). Replacing salt correction factors with optimized RNA nearest-neighbour enthalpy and entropy parameters. Chem. Phys. 521: 69–76, https://doi.org/10.1016/j.chemphys.2019.01.016 .
doi: 10.1016/j.chemphys.2019.01.016
Fish, L., Zhang, S., Yu, J.X., Culbertson, B., Zhou, A.Y., Goga, A., and Goodarzi, H. (2018). Cancer cells exploit an orphan RNA to drive metastatic progression. Nat. Med. 24: 1743–1751, https://doi.org/10.1038/s41591-018-0230-4 .
doi: 10.1038/s41591-018-0230-4
Gruber, A.R., Lorenz, R., Bernhart, S.H., Neubock, R., and Hofacker, I.L. (2008). The Vienna RNA websuite. Nucleic Acids Res. 36: W70–W74, https://doi.org/10.1093/nar/gkn188 .
doi: 10.1093/nar/gkn188
Ha, M. and Kim, V.N. (2014). Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15: 509–524, https://doi.org/10.1038/nrm3838 .
doi: 10.1038/nrm3838
Hashim, A., Rizzo, F., Marchese, G., Ravo, M., Tarallo, R., Nassa, G., Giurato, G., Santamaria, G., Cordella, A., Cantarella, C., et al.. (2014). RNA sequencing identifies specific PIWI-interacting small non-coding RNA expression patterns in breast cancer. Oncotarget 5: 9901–9910, https://doi.org/10.18632/oncotarget.2476 .
doi: 10.18632/oncotarget.2476
Hasler, D. and Meister, G. (2016). From tRNA to miRNA: RNA-folding contributes to correct entry into noncoding RNA pathways. FEBS Lett. 590: 2354–2363, https://doi.org/10.1002/1873-3468.12294 .
doi: 10.1002/1873-3468.12294
Hasler, D., Lehmann, G., Murakawa, Y., Klironomos, F., Jakob, L., Grasser, F.A., Rajewsky, N., Landthaler, M., and Meister, G. (2016). The Lupus autoantigen La prevents mis-channeling of tRNA fragments into the human MicroRNA pathway. Mol. Cell 63: 110–124, https://doi.org/10.1016/j.molcel.2016.05.026 .
doi: 10.1016/j.molcel.2016.05.026
Hock, J. and Meister, G. (2008). The Argonaute protein family. Genome Biol. 9: 210, https://doi.org/10.1186/gb-2008-9-2-210 .
doi: 10.1186/gb-2008-9-2-210
Hu, Q., Tanasa, B., Trabucchi, M., Li, W., Zhang, J., Ohgi, K.A., Rose, D.W., Glass, C.K., and Rosenfeld, M.G. (2012). DICER- and AGO3-dependent generation of retinoic acid-induced DR2 Alu RNAs regulates human stem cell proliferation. Nat. Struct. Mol. Biol. 19: 1168–1175, https://doi.org/10.1038/nsmb.2400 .
doi: 10.1038/nsmb.2400
Intine, R.V., Sakulich, A.L., Koduru, S.B., Huang, Y., Pierstorff, E., Goodier, J.L., Phan, L., and Maraia, R.J. (2000). Control of transfer RNA maturation by phosphorylation of the human La antigen on serine 366. Mol. Cell 6: 339–348, https://doi.org/10.1016/s1097-2765(00)00034-4 .
doi: 10.1016/s1097-2765(00)00034-4
Itano, M.S., Arnion, H., Wolin, S.L., and Simon, S.M. (2018). Recruitment of 7SL RNA to assembling HIV-1 virus-like particles. Traffic 19: 36–43, https://doi.org/10.1111/tra.12536 .
doi: 10.1111/tra.12536
Iwakawa, H.O. and Tomari, Y. (2022). Life of RISC: formation, action, and degradation of RNA-induced silencing complex. Mol. Cell 82: 30–43, https://doi.org/10.1016/j.molcel.2021.11.026 .
doi: 10.1016/j.molcel.2021.11.026
Izumi, N., Shoji, K., Suzuki, Y., Katsuma, S., and Tomari, Y. (2020). Zucchini consensus motifs determine the mechanism of pre-piRNA production. Nature 578: 311–316, https://doi.org/10.1038/s41586-020-1966-9 .
doi: 10.1038/s41586-020-1966-9
Jurka, J. (2004). Evolutionary impact of human Alu repetitive elements. Curr. Opin. Genet. Dev. 14: 603–608, https://doi.org/10.1016/j.gde.2004.08.008 .
doi: 10.1016/j.gde.2004.08.008
Keenan, R.J., Freymann, D.M., Stroud, R.M., and Walter, P. (2001). The signal recognition particle. Annu. Rev. Biochem. 70: 755–775, https://doi.org/10.1146/annurev.biochem.70.1.755 .
doi: 10.1146/annurev.biochem.70.1.755
Kostrikis, L.G., Tyagi, S., Mhlanga, M.M., Ho, D.D., and Kramer, F.R. (1998). Spectral genotyping of human alleles. Science 279: 1228–1229, https://doi.org/10.1126/science.279.5354.1228 .
doi: 10.1126/science.279.5354.1228
Kota, V., Sommer, G., Hazard, E.S., Hardiman, G., Twiss, J.L., and Heise, T. (2018). SUMO modification of the RNA-binding protein La regulates cell proliferation and STAT3 protein stability. Mol. Cell. Biol. 38: 1–16. https://doi.org/10.1128/mcb.00129-17 .
doi: 10.1128/mcb.00129-17
Kuehnert, J., Sommer, G., Zierk, A.W., Fedarovich, A., Brock, A., Fedarovich, D., and Heise, T. (2015). Novel RNA chaperone domain of RNA-binding protein La is regulated by AKT phosphorylation. Nucleic Acids Res. 43: 581–594, https://doi.org/10.1093/nar/gku1309 .
doi: 10.1093/nar/gku1309
Kuksa, P.P., Amlie-Wolf, A., Katanic, Z., Valladares, O., Wang, L.S., and Leung, Y.Y. (2019). DASHR 2.0: integrated database of human small non-coding RNA genes and mature products. Bioinformatics 35: 1033–1039, https://doi.org/10.1093/bioinformatics/bty709 .
doi: 10.1093/bioinformatics/bty709
Kumar, P., Kuscu, C., and Dutta, A. (2016). Biogenesis and function of transfer RNA-related fragments (tRFs). Trends Biochem. Sci. 41: 679–689, https://doi.org/10.1016/j.tibs.2016.05.004 .
doi: 10.1016/j.tibs.2016.05.004
Leung, Y.Y., Kuksa, P.P., Amlie-Wolf, A., Valladares, O., Ungar, L.H., Kannan, S., Gregory, B.D., and Wang, L.S. (2016). DASHR: database of small human noncoding RNAs. Nucleic Acids Res. 44: D216–D222, https://doi.org/10.1093/nar/gkv1188 .
doi: 10.1093/nar/gkv1188
Liang, C., Xiong, K., Szulwach, K.E., Zhang, Y., Wang, Z., Peng, J., Fu, M., Jin, P., Suzuki, H.I., and Liu, Q. (2013). Sjogren syndrome antigen B (SSB)/La promotes global microRNA expression by binding microRNA precursors through stem-loop recognition. J. Biol. Chem. 288: 723–736, https://doi.org/10.1074/jbc.m112.401323 .
doi: 10.1074/jbc.m112.401323
Liu, Y., Tan, H., Tian, H., Liang, C., Chen, S., and Liu, Q. (2011). Autoantigen La promotes efficient RNAi, antiviral response, and transposon silencing by facilitating multiple-turnover RISC catalysis. Mol. Cell 44: 502–508, https://doi.org/10.1016/j.molcel.2011.09.011 .
doi: 10.1016/j.molcel.2011.09.011
Lorenz, P., Misteli, T., Baker, B.F., Bennett, C.F., and Spector, D.L. (2000). Nucleocytoplasmic shuttling: a novel in vivo property of antisense phosphorothioate oligodeoxynucleotides. Nucleic Acids Res. 28: 582–592, https://doi.org/10.1093/nar/28.2.582 .
doi: 10.1093/nar/28.2.582
Mao, S., Ying, Y., Wu, R., and Chen, A.K. (2020a). Recent advances in the molecular beacon technology for live-cell single-molecule imaging. iScience 23: 101801, https://doi.org/10.1016/j.isci.2020.101801 .
doi: 10.1016/j.isci.2020.101801
Mao, S., Ying, Y., Wu, X., and Chen, A.K. (2020b). Delivering molecular beacons via an electroporation-based approach enables live-cell imaging of single RNA transcripts and genomic loci. Methods Mol. Biol. 2106: 241–252, https://doi.org/10.1007/978-1-0716-0231-7_15 .
doi: 10.1007/978-1-0716-0231-7_15
Maraia, R.J., Mattijssen, S., Cruz-Gallardo, I., and Conte, M.R. (2017). The La and related RNA-binding proteins (LARPs): structures, functions, and evolving perspectives. Wiley Interdiscip. Rev. RNA 8: e1430, https://doi.org/10.1002/wrna.1430 .
doi: 10.1002/wrna.1430
Megel, C., Morelle, G., Lalande, S., Duchene, A.M., Small, I., and Marechal-Drouard, L. (2015). Surveillance and cleavage of eukaryotic tRNAs. Int. J. Mol. Sci. 16: 1873–1893, https://doi.org/10.3390/ijms16011873 .
doi: 10.3390/ijms16011873
Naim, V. and Rosselli, F. (2009). The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell Biol. 11: 761–768, https://doi.org/10.1038/ncb1883 .
doi: 10.1038/ncb1883
Nakano, S., Fujimoto, M., Hara, H., and Sugimoto, N. (1999). Nucleic acid duplex stability: influence of base composition on cation effects. Nucleic Acids Res. 27: 2957–2965, https://doi.org/10.1093/nar/27.14.2957 .
doi: 10.1093/nar/27.14.2957
Nitin, N. and Bao, G. (2008). NLS peptide conjugated molecular beacons for visualizing nuclear RNA in living cells. Bioconjug. Chem. 19: 2205–2211, https://doi.org/10.1021/bc800322a .
doi: 10.1021/bc800322a
Nitin, N., Santangelo, P.J., Kim, G., Nie, S., and Bao, G. (2004). Peptide-linked molecular beacons for efficient delivery and rapid mRNA detection in living cells. Nucleic Acids Res. 32: e58, https://doi.org/10.1093/nar/gnh063 .
doi: 10.1093/nar/gnh063
Ozata, D.M., Gainetdinov, I., Zoch, A., O’Carroll, D., and Zamore, P.D. (2019). PIWI-interacting RNAs: small RNAs with big functions. Nat. Rev. Genet. 20: 89–108, https://doi.org/10.1038/s41576-018-0073-3 .
doi: 10.1038/s41576-018-0073-3
Pekarsky, Y., Balatti, V., and Croce, C.M. (2023). tRNA-derived fragments (tRFs) in cancer. J. Cell Commun. Signaling 17: 47–54, https://doi.org/10.1007/s12079-022-00690-2 .
doi: 10.1007/s12079-022-00690-2
Pippadpally, S. and Venkatesh, T. (2020). Deciphering piRNA biogenesis through cytoplasmic granules, mitochondria and exosomes. Arch. Biochem. Biophys. 695: 108597, https://doi.org/10.1016/j.abb.2020.108597 .
doi: 10.1016/j.abb.2020.108597
Quentin, Y. (1994). A master sequence related to a free left Alu monomer (FLAM) at the origin of the B1 family in rodent genomes. Nucleic Acids Res. 22: 2222–2227, https://doi.org/10.1093/nar/22.12.2222 .
doi: 10.1093/nar/22.12.2222
Roy, J. and Mallick, B. (2018). Investigating piwi-interacting RNA regulome in human neuroblastoma. Genes Chromosomes Cancer 57: 339–349, https://doi.org/10.1002/gcc.22535 .
doi: 10.1002/gcc.22535
Santangelo, P.J., Nix, B., Tsourkas, A., and Bao, G. (2004). Dual FRET molecular beacons for mRNA detection in living cells. Nucleic Acids Res. 32: e57, https://doi.org/10.1093/nar/gnh062 .
doi: 10.1093/nar/gnh062
Schwartz, E.I., Intine, R.V., and Maraia, R.J. (2004). CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate rpL37 5′-terminal oligopyrimidine mRNA metabolism. Mol. Cell. Biol. 24: 9580–9591, https://doi.org/10.1128/mcb.24.21.9580-9591.2004 .
doi: 10.1128/mcb.24.21.9580-9591.2004
Shibata, Y., Voeltz, G.K., and Rapoport, T.A. (2006). Rough sheets and smooth tubules. Cell 126: 435–439, https://doi.org/10.1016/j.cell.2006.07.019 .
doi: 10.1016/j.cell.2006.07.019
Sommer, G. and Heise, T. (2021). Role of the RNA-binding protein La in cancer pathobiology. RNA Biol. 18: 218–236, https://doi.org/10.1080/15476286.2020.1792677 .
doi: 10.1080/15476286.2020.1792677
Treiber, T., Treiber, N., and Meister, G. (2019). Regulation of microRNA biogenesis and its crosstalk with other cellular pathways. Nat. Rev. Mol. Cell Biol. 20: 5–20, https://doi.org/10.1038/s41580-018-0059-1 .
doi: 10.1038/s41580-018-0059-1
Tyagi, S. and Kramer, F.R. (1996). Molecular beacons: probes that fluoresce upon hybridization. Nat. Biotechnol. 14: 303–308, https://doi.org/10.1038/nbt0396-303 .
doi: 10.1038/nbt0396-303
Tyagi, S., Bratu, D.P., and Kramer, F.R. (1998). Multicolor molecular beacons for allele discrimination. Nat. Biotechnol. 16: 49–53, https://doi.org/10.1038/nbt0198-49 .
doi: 10.1038/nbt0198-49
Van Niekerk, E.A., Willis, D.E., Chang, J.H., Reumann, K., Heise, T., and Twiss, J.L. (2007). Sumoylation in axons triggers retrograde transport of the RNA-binding protein La. Proc. Natl. Acad. Sci. U. S. A. 104: 12913–12918, https://doi.org/10.1073/pnas.0611562104 .
doi: 10.1073/pnas.0611562104
Wang, J., Shi, Y., Zhou, H., Zhang, P., Song, T., Ying, Z., Yu, H., Li, Y., Zhao, Y., Zeng, X., et al.. (2022). piRBase: integrating piRNA annotation in all aspects. Nucleic Acids Res. 50: D265–D272, https://doi.org/10.1093/nar/gkab1012 .
doi: 10.1093/nar/gkab1012
Weber, G. (2015). Optimization method for obtaining nearest-neighbour DNA entropies and enthalpies directly from melting temperatures. Bioinformatics 31: 871–877, https://doi.org/10.1093/bioinformatics/btu751 .
doi: 10.1093/bioinformatics/btu751
Wolin, S.L. and Cedervall, T. (2002). The La protein. Annu. Rev. Biochem. 71: 375–403, https://doi.org/10.1146/annurev.biochem.71.090501.150003 .
doi: 10.1146/annurev.biochem.71.090501.150003
Yamasaki, S., Ivanov, P., Hu, G.F., and Anderson, P. (2009). Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol. 185: 35–42, https://doi.org/10.1083/jcb.200811106 .
doi: 10.1083/jcb.200811106
Zhang, X.O., Pratt, H., and Weng, Z. (2021). Investigating the potential roles of SINEs in the human genome. Annu. Rev. Genomics Hum. Genet. 22: 199–218, https://doi.org/10.1146/annurev-genom-111620-100736 .
doi: 10.1146/annurev-genom-111620-100736
Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406–3415, https://doi.org/10.1093/nar/gkg595 .
doi: 10.1093/nar/gkg595