Computational prediction of non-enzymatic RNA degradation patterns

• Authors: Agnieszka Rybarczyk , Paulina Jackowiak , Marek Figlerowicz , Jacek Blazewicz
• Languages of publication: EN

Abstracts

EN

Since the beginning of the 21st century, an increasing interest in the research of ribonucleic acids has been observed in response to a surprising discovery of the role that RNA molecules play in the biological systems. It was demonstrated that they do not only take part in the protein synthesis (mRNA, rRNA, tRNA) but also are involved in the regulation of gene expression. Several classes of small regulatory RNAs have been discovered (e.g. microRNA, small interfering RNA, piwiRNA). Most of them are excised from specific double-stranded RNA precursors by enzymes that belong to the RNaseIII family (Drosha, Dicer or Dicer-like proteins). More recently, it has been shown that small regulatory RNAs are also generated as stable intermediates of RNA degradation (the so called RNA fragments originating from tRNA, snRNA, snoRNA etc.). Unfortunately, the mechanisms underlying biogenesis of the RNA fragments remain unclear. It is thought that several factors may be involved in the formation of the RNA fragments. The most important are the specific RNases, RNA-protein interactions and RNA structure. In this work, we focus on the RNA primary and secondary structures as factors influencing the RNA stability and consequently the pattern of RNA fragmentation. Earlier, we identified the major structural factors affecting non-enzymatic RNA degradation. Now, based on these data, we developed a new branch-and-cut algorithm that is able to predict the products of large RNA molecules' hydrolysis in vitro. We also present the experimental data that verify the results generated using this algorithm.

Keywords

EN

RNA degradation; non-enzymatic RNA hydrolysis; branch-and-cut algorithm

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2016
• Volume: 63
• Issue: 4
• Pages: 745-751

Dates

published

2016

received

2016-05-30

revised

2016-07-21

accepted

2016-07-22

(unknown)

2016-10-19

Contributors

author

Agnieszka Rybarczyk

• Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
• Institute of Computing Science, Poznan University of Technology, Poznań, Poland
• European Centre for Bioinformatics and Genomics, Poznań, Poland

author

Paulina Jackowiak

• Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
• Institute of Chemical Technology and Engineering, Poznan University of Technology, Poznań, Poland

author

Marek Figlerowicz

• Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
• Institute of Computing Science, Poznan University of Technology, Poznań, Poland
• European Centre for Bioinformatics and Genomics, Poznań, Poland

author

Jacek Blazewicz

• Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznań, Poland
• Institute of Computing Science, Poznan University of Technology, Poznań, Poland
• European Centre for Bioinformatics and Genomics, Poznań, Poland

References

• Aalto AP, Pasquinelli AE (2012) Small non-coding RNAs mount a silent revolution in gene expression. Curr Opin Cell Biol. 24: 333-340. https://doi.org/10.1016/j.ceb.2012.03.006.
• Antczak M, Zok T, Popenda M, Lukasiak P, Adamiak RW, Blazewicz J, Szachniuk M (2014) RNApdbee - a webserver to derive secondary structures from pdb files of knotted and unknotted RNAs. Nucleic Acids Res 42: W368-W372. https://doi.org/10.1093/nar/gku330.
• Bibillo A, Figlerowicz M, Ziomek K, Kierzek R (2000) The nonenzymatic hydrolysis of oligoribonucleotides. VII. Structural elements affecting hydrolysis. Nucleosides Nucleotides Nucleic Acids 19: 977-994. https://doi.org/10.1080/15257770008033037.
• Bibillo A, Figlerowicz M, Kierzek R (1999) The non-enzymatic hydrolysis of oligoribonucleotides VI. The role of biogenic polyamines. Nucleic Acids Res 27: 3931-3937. https://doi.org/10.1093/nar/27.19.3931.
• Blazewicz J, Figlerowicz M, Kasprzak M, Nowacka M, Rybarczyk A (2011) RNA partial degradation problem: motivation, complexity, algorithm. J Comput Biol 18: 821-834. https://doi.org/10.1089/cmb.2010.0153.
• Blazewicz J, Formanowicz P, Guinand F, Kasprzak M (2002) A heuristic managing errors for DNA sequencing. Bioinformatics 18: 652-660.
• Blazewicz J, Szachniuk M, Wojtowicz A (2005) RNA tertiary structure determination: NOE pathway construction by tabu search. Bioinformatics 21: 2356-2361. https://doi.org/10.1093/bioinformatics/bti351.
• Ciesiołka J, Michałowski D, Wrzesinski J, Krajewski J, Krzyzosiak WJ (1998) Patterns of cleavages induced by lead ions in defined RNA secondary structure motifs. J Mol Biol 275: 211-220.
• Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JW, Green PJ, Barton GJ, Hutvagner G (2009) Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 15: 2147-2160.
• Czech B, Hannon GJ (2011) Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12: 19-31. https://doi.org/10.1038/nrg2916.
• Dutkiewicz M, Ciesiolka J (2005) Structural characterization of the highly conserved 98-base sequence at the 3' end of HCV RNA genome and the complementary sequence located at the 5' end of the replicative viral strand. Nucleic Acids Res 33: 693-703. https://doi.org/10.1093/nar/gki218.
• Figlerowicz M (2000) Role of RNA structure in non-homologous recombination between genomic molecules of brome mosaic virus. Nucleic Acids Res 28: 1714-1723.
• Gendron P, Lemieux S, Major F (2001) Quantitative analysis of nucleic acid three-dimensional structures. J Mol Biol 308: 919-936. https://doi.org/10.1006/jmbi.2001.4626.
• Grunberg-Manago M (1999) Messenger RNA Stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet 33: 193-227. https://doi.org/10.1146/annurev.genet.33.1.193.
• Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P (1994) Fast folding and comparison of RNA secondary structures. Monatshefte Für Chem Chem Mon 125: 167-188. https://doi.org/10. 1007/BF00818163
• Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136: 763-776. https://doi.org/10.1016/j.cell.2009.01.019.
• Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151: 2120-2132. https://doi.org/10.1104/pp.109.147280.
• Hsieh LC, Lin SI, Kuo HF, Chiou TJ (2010) Abundance of tRNA-derived small RNAs in phosphate-starved Arabidopsis roots. Plant Signal Behav 5: 537-539. https://doi.org/10.4161/psb.11029.
• Hui MP, Foley PL, Belasco JG (2014) Messenger RNA degradation in bacterial cells. Annu Rev Genet 48: 537-559. https://doi.org/10.1146/annurev-genet-120213-092340.
• Hurto RL (2011) Unexpected functions of tRNA and tRNA processing enzymes. Adv Exp Med Biol 722: 137-155. https://doi.org/10.1007/978-1-4614-0332-6_9.
• Jackowiak P, Nowacka M, Strozycki PM, Figlerowicz M (2011) RNA degradome-its biogenesis and functions. Nucleic Acids Res 39: 7361-7370. https://doi.org/10.1093/nar/gkr450.
• Kaukinen U, Lyytikainen S, Mikkola S, Lonnberg H (2002) The reactivity of phosphodiester bonds within linear single-stranded oligoribonucleotides is strongly dependent on the base sequence. Nucleic Acids Res 30: 468-474. https://doi.org/10.1093/nar/30.2.468.
• Kazakov S, Altman S (1992) A trinucleotide can promote metal ion-dependent specific cleavage of RNA. Proc Natl Acad Sci USA 89: 7939-7943.
• Keck MV, Hecht SM (1995) Sequence-specific hydrolysis of yeast tRNA(Phe) mediated by metal-free bleomycin. Biochemistry 34: 12029-12037. https://doi.org/10.1021/bi00037a046.
• Kierzek R (1992) Nonenzymatic hydrolysis of oligoribonucleotides. Nucleic Acids Res 20: 5079-5084.
• Kierzek R (2001) Nonenzymatic Cleavage of Oligoribonucleotides, Methods Enzymol 341: 657-675. https://doi.org/10.1016/S0076-6879(01)41183-9.
• Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139. https://doi.org/10.1038/nrm2632.
• Li Z, Ender C, Meister G, Moore PS, Chang Y, John B (2012) Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res 40: 6787-6799. https://doi.org/10.1093/nar/gks307.
• Lorentzen E, Conti E (2006) The exosome and the proteosome: nanocompartments for degradation. Cell 125: 651-654. https://doi.org/10.1016/j.cell.2006.05.002.
• Lu XJ, Olson WK (2003) 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res 31: 5108-5121. https://doi.org/10.1093/nar/gkg680.
• Maivali U, Paier A, Tenson T (2013) When stable RNA becomes unstable: the degradation of ribosomes in bacteria and beyond. Biol Chem 394: 845-855. https://doi.org/10.1515/hsz-2013-0133.
• Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15: R17-R29.
• Mattick JS (2009) The genetic signatures of noncoding RNAs. PLoS Genet 5: e1000459. https://doi.org/10.1371/journal.pgen.1000459.
• Mickiewicz A, Rybarczyk A, Sarzynska J, Figlerowicz M, Blazewicz J (2016) AmiRNA Designer - new method of artificial miRNA design. Acta Biochim Pol 63: 71-77. https://doi.org/10.18388/abp.2015_989.
• Mikkola S, Kaukinen U, Lonnberg H (2001) The effect of secondary structure on cleavage of the phosphodiester bonds of RNA. Cell Biochem Biophys 34: 95-119. https://doi.org/10.1385/CBB:34:1:95.
• Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nature Reviews Genetics 15: 423-437. https://doi.org/10.1038/nrg3722.
• Nowacka M, Jackowiak P, Rybarczyk A, Magacz T, Strozycki PM, Barciszewski J, Figlerowicz M (2012) 2D-PAGE as an effective method of RNA degradome analysis. Molecular Biology Reports 39: 139-146. https://doi.org/10.1007/s11033-011-0718-1.
• Nowacka M, Strozycki PM, Jackowiak P, Hojka-Osinska A, Szymanski M, Figlerowicz M (2013) Identification of stable, high copy number, medium-sized RNA degradation intermediates that accumulate in plants under non-stress conditions. Plant Mol Biol 83: 191-204. https://doi.org/10.1007/s11103-013-0079-3.
• Pederson T. (2010) Regulatory RNAs derived from transfer RNA? RNA 16: 1865-1869. https://doi.org/10.1261/rna.2266510.
• Podkowinski J, Zmienko A, Florek B, Wojciechowski P, Rybarczyk A, Wrzesinski J, Ciesiolka J, Blazewicz J, Kondorosi A, Crespi M, Legocki A (2009) Translational and structural analysis of the shortest legume ENOD40 gene in Lupinus luteus. Acta Biochim Pol 56: 89-102.
• Popenda M, Szachniuk M, Antczak M, Purzycka KJ, Lukasiak P, Bartol N, Blazewicz J, Adamiak RW (2012) Automated 3D structure composition for large RNAs. Nucleic Acids Res 40: e112. https://doi.org/10.1093/nar/gks339.
• Reuter JS, Mathews DH (2010) RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics 11: 129. https://doi.org/10.1186/1471-2105-11-129.
• Ross J (1995) mRNA stability in mammalian cells. Microbiol Rev 59: 423-450.
• Rybarczyk A, Szostak N, Antczak M, Zok T, Popenda M, Adamiak R, Blazewicz J, Szachniuk M (2015) New in silico approach to assessing RNA secondary structures with non-canonical base pairs. BMC Bioinformatics 16: 276. https://doi.org/10.1186/s12859-015-0718-6.
• Sobala A, Hutvagner G (2011) Transfer RNA-derived fragments: Origins, processing, and functions. Wiley Interdiscip Rev RNA 2: 853-862. https://doi.org/10.1002/wrna.96.
• Szostak N, Royo F, Rybarczyk A, Szachniuk M, Blazewicz J, del Sol A, Falcon-Perez JM (2014) Sorting signal targeting mRNA into hepatic extracellular vesicles. RNA Biol 11: 836-844. https://doi.org/10.4161/rna.29305.
• Schweingruber C, Rufener SC, Zund D, Yamashita A, Muhlemann O (2013) Nonsense-mediated mRNA decay - mechanisms of substrate mRNA recognition and degradation in mammalian cells. Biochim Biophys Acta 1829: 612-623. https://doi.org/10.1016/j.bbagrm.2013.02.005.
• Szweykowska-Kulinska Z, Jarmolowski A, Figlerowicz M (2003) RNA interference and its role in the regulation of eukaryotic gene expression. Acta Biochim Pol 50: 217-229.
• Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS (2009) Small RNAs derived from snoRNAs. RNA 15: 1233-1240. https://doi.org/10.1261/rna.1528909.
• Taguchi G (1987) System of Experimental Design: Engineering Methods to Optimize Quality and Minimize Costs, UNIPUB/Kraus International Publications
• Thompson DM, Lu C, Green PJ, Parker R (2008) tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14: 2095-2103. https://doi.org/10.1261/rna.1232808.
• Winkler WC, Breaker RR (2005) Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 59: 487-517. https://doi.org/10.1146/annurev.micro.59.030804.121336.
• Yang H, Jossinet F, Leontis NB, Chen L, Westbrook J, Berman H, Westhof E (2003) Tools for the automatic identification and classification of RNA base pairs. Nucleic Acids Res 31: 3450-3460. https://doi.org/10.1093/nar/gkg529.
• Zhang JC, Styblinski M.A. (1995) Yield and Variability Optimization of Integrated Circuits. Springer Science, New York: 199-202. ISBN 978-1-4613-5935-7
• Zhang S, Sun L, Kragler F (2009) The phloem-delivered RNA pool contains small noncoding RNAs and interferes with translation. Plant Physiol 150: 378-387. https://doi.org/10.1104/pp.108.134767.
• Zok T, Popenda M, Szachniuk M (2014) MCQ4Structures to compute similarity of molecule structures. Central Eur J Operations Res 22: 457-474. https://doi.org/10. 1007/s10100-013-0296-5

Identifiers

DOI

10.18388/abp.2016_1331