Skip to main content
SpringerLink
Log in

Methods to Analyze Post-transcriptional Modifications Applied to Stable RNAs in Staphylococcus aureus

  • Chapter
  • First Online:
RNA Structure and Function

Part of the book series: RNA Technologies ((RNATECHN,volume 14))

  • 567 Accesses

Abstract

RNA modifications contribute to the various functions of RNAs in all living organisms. Some of these modifications are dynamic and contribute to the regulation of gene expression. In bacteria, their roles in stress, environmental adaptation, and in infections caused by pathogens have been recently fully recognized. In this review, we describe several methodologies including mass spectrometry, next-generation RNA sequencing methods, biochemical approaches, and cryo-EM structural analysis that are used to detect and localize the modifications in tRNAs and rRNAs. We illustrate how the combination of methods was necessary to avoid technical biases for a successful mapping of the modifications in tRNAs and rRNAs in Staphylococcus aureus.

R. Bahena-Ceron and J. Jaramillo-Ponce contributed equally in this chapter.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adachi H, DeZoysa MD, Yu YT (2019) Detection and Quantification of Pseudouridine in RNA. Methods Mol Biol 1870:219–235

    Article  CAS  PubMed  Google Scholar 

  • Agris PF (1996) The importance of being modified: roles of modified nucleosides and Mg2+ in RNA structure and function. Prog Nucleic Acid Res Mol Biol 53:79–129

    Article  CAS  PubMed  Google Scholar 

  • Antoine L, Bahena-Ceron R, Devi Bunwaree H et al (2021) RNA modifications in pathogenic bacteria: impact on host adaptation and virulence. Genes (basel) 12:1125

    Article  CAS  PubMed  Google Scholar 

  • Antoine L, Wolff P (2020) Mapping of posttranscriptional tRNA modifications by two-dimensional gel electrophoresis mass spectrometry. Methods Mol Biol 2113:101–110

    Article  CAS  PubMed  Google Scholar 

  • Antoine L, Wolff P, Westhof E et al (2019) Mapping post-transcriptional modifications in Staphylococcus aureus tRNAs by nanoLC/MSMS. Biochimie 164:60–69

    Article  CAS  PubMed  Google Scholar 

  • Apffel A, Chakel JA, Fischer S et al (1997) Analysis of oligonucleotides by HPLC-electrospray ionization mass spectrometry. Anal Chem 69:1320–1325

    Article  CAS  PubMed  Google Scholar 

  • Arimbasseri AG, Blewett NH, Iben JR et al (2015) RNA polymerase III output is functionally linked to tRNA dimethyl-G26 modification. PLoS Genet 11(12):e1005671

    Article  PubMed  PubMed Central  Google Scholar 

  • Aschenbrenner J, Werner S, Marchand V et al (2018) Engineering of a DNA polymerase for direct m(6) a sequencing. Angew Chem Int Ed Engl 57:417–421

    Article  CAS  PubMed  Google Scholar 

  • Atshan SS, Shamsudin MN, Lung LTT et al (2012) Improved method for the isolation of RNA from bacteria refractory to disruption, including S. aureus producing biofilm. Gene 494:219–224

    Article  CAS  PubMed  Google Scholar 

  • Bakin A, Ofengand J (1993) Four newly located pseudouridylate residues in Escherichia coli 23S ribosomal RNA are all at the peptidyltransferase center: analysis by the application of a new sequencing technique. Biochemistry 32:9754–9762

    Article  CAS  PubMed  Google Scholar 

  • Bastos MdCdF, Coutinho BG, Coelho MLV (2010) Lysostaphin: a staphylococcal bacteriolysin with potential clinical applications. Pharmaceuticals 3:1139–1161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begik O, Lucas MC, Pryszcz LP et al (2021) Quantitative profiling of pseudouridylation dynamics in native RNAs with nanopore sequencing. Nat Biotechnol 39:1278–1291

    Article  CAS  PubMed  Google Scholar 

  • Behm-Ansmant I, Helm M, Motorin Y (2011) Use of specific chemical reagents for detection of modified nucleotides in RNA. J Nucleic Acids 2011:408053

    Article  PubMed  PubMed Central  Google Scholar 

  • Behrens A, Rodschinka G, Nedialkova DD (2021) High-resolution quantitative profiling of tRNA abundance and modification status in eukaryotes by mim-tRNAseq. Mol Cell 81:1802–1815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belinite M, Khusainov I, Soufari H et al (2021) Stabilization of Ribosomal RNA of the Small Subunit by Spermidine in Staphylococcus aureus. Front Mol Biosci 8:738752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belousoff MJ, Eyal Z, Radjainia M et al (2017) Structural Basis for Linezolid Binding Site Rearrangement in the Staphylococcus aureus Ribosome. mBio 8:e00395-17

    Google Scholar 

  • Beltrame CO, Côrtes MF, Bandeira PT et al (2015) Optimization of the RNeasy mini kit to obtain high-quality total RNA from sessile cells of Staphylococcus aureus. Braz J Med Biol Res 48:1071–1076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birkedal U, Christensen-Dalsgaard M, Krogh N et al (2015) Profiling of ribose methylations in RNA by high-throughput sequencing. Angew Chem Int Ed Engl 54:451–455

    Article  CAS  PubMed  Google Scholar 

  • Bleicher K, Bayer E (1994) Various factors influencing the signal intensity of oligonucleotides in electrospray mass spectrometry. Biol Mass Spectrom 23:320–322

    Article  CAS  PubMed  Google Scholar 

  • Boccaletto P, Stefaniak F, Ray A et al (2022) MODOMICS: a database of RNA modification pathways. 2021 update. Nucleic Acids Res 50:D231–D235

    Article  CAS  PubMed  Google Scholar 

  • Brielle R, Pinel-Marie ML, Chat S et al (2017) Purification, identification, and functional analysis of polysomes from the human pathogen Staphylococcus aureus. Methods 117:59–66

    Article  CAS  PubMed  Google Scholar 

  • Burakovsky DE, Prokhorova IV, Sergiev PV, a. (2012) Impact of methylations of m2G966/m5C967 in 16S rRNA on bacterial fitness and translation initiation. Nucleic Acids Res 40:7885–7895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai WM, Chionh YH, Hia F et al (2015) A platform for discovery and quantification of modified ribonucleosides in RNA: application to stress-induced reprogramming of tRNA modifications. Methods Enzymol 560:29–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castleberry CM, Rodicio LP, Limbach PA (2008) Electrospray ionization mass spectrometry of oligonucleotides. Curr Protoc Nucleic Acid Chem

    Google Scholar 

  • Cerutti P, Miller N (1967) Selective reduction of yeast transfer ribonucleic acid with sodium borohydride. J Mol Biol 26:55–66

    Article  CAS  PubMed  Google Scholar 

  • Chakraburtty K (1980) Recognition of E coli tRNAArg by arginyl tRNA synthetase. Nucleic Acids Res 8:4459–4472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charette M, Gray MW (2000) Pseudouridine in RNA: what, where, how, and why. IUBMB Life 49:341–351

    Article  CAS  PubMed  Google Scholar 

  • Chionh YH, Ho CH, Pruksakorn D et al (2013) A multidimensional platform for the purification of non-coding RNA species. Nucleic Acids Res 41:e168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cimicata G, Fridkin G, Bose T et al (2022) Structural studies reveal the role of helix 68 in the elongation step of protein biosynthesis. mBio 13:e0030622

    Google Scholar 

  • Cottilli P, Itoh Y, Nobe Y et al (2022) Cryo-EM structure and rRNA modification sites of a plant ribosome. Plant Commun 3:100342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crain PF (1990) Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry. Meth Enzymol 193:782–790

    Article  CAS  Google Scholar 

  • Dalluge JJ, Hashizume T, Sopchik AE, a. (1996) Conformational flexibility in RNA: the role of dihydrouridine. Nucleic Acids Res 24:1073–1079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Crécy-Lagard V, Jaroch M (2020) Functions of bacterial tRNA modifications: from ubiquity to diversity. Trends Microbiol 29:41–53

    Article  PubMed  PubMed Central  Google Scholar 

  • de Crecy-Lagard V, Ross RL, Jaroch M et al (2020) Survey and validation of tRNA modifications and their corresponding genes in bacillus subtilis sp subtilis strain 168. Biomolecules 10:977

    Article  PubMed  PubMed Central  Google Scholar 

  • Demirci H, Ft M, Belardinelli R et al (2010) Modification of 16S ribosomal RNA by the KsgA methyltransferase restructures the 30S subunit to optimize ribosome function. RNA 16(12):2319–2324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng X, Chen K, Luo GZ et al (2015) Widespread occurrence of N6-methyladenosine in bacterial mRNA. Nucleic Acids Res 43:6557–6567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deryusheva S, Choleza M, Barbarossa A et al (2012) Post-transcriptional modification of spliceosomal RNAs is normal in SMN-deficient cells. RNA 18:31–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dudley E, Tuytten R, Bond A et al (2005) Study of the mass spectrometric fragmentation of pseudouridine: comparison of fragmentation data obtained by matrix-assisted laser desorption/ionisation post-source decay, electrospray ion trap multistage mass spectrometry, and by a method utilising elect. Rapid Commun Mass Spectrom 19:3075–3085

    Article  CAS  PubMed  Google Scholar 

  • Duval M, Simonetti A, Caldelari I et al (2015) Multiple ways to regulate translation initiation in bacteria: mechanisms, regulatory circuits, dynamics. Biochimie 114:18–29

    Article  CAS  PubMed  Google Scholar 

  • Easton LE, Shibata Y, Lukavsky PJ (2010) Rapid, nondenaturing RNA purification using weak anion-exchange fast performance liquid chromatography. RNA 16:647–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer N, Neumann P, Konevega AL et al (2015) Structure of the E. coli ribosome-EF-Tu complex at <3 a resolution by Cs-corrected cryo-EM. Nature 520:567–570

    Article  CAS  PubMed  Google Scholar 

  • França A, Melo LD, Cerca N (2011) Comparison of RNA extraction methods from biofilm samples of Staphylococcus epidermidis. BMC Res Notes 4:572

    Article  PubMed  PubMed Central  Google Scholar 

  • Frye M, Jaffrey SR, Pan T et al (2016) RNA modifications: what have we learned and where are we headed? Nat Rev Genet 17:365–372

    Article  CAS  PubMed  Google Scholar 

  • Garalde DR, Snell EA, Jachimowicz D et al (2018) Highly parallel direct RNA sequencing on an array of nanopores. Nat Methods 15:201–206

    Article  CAS  PubMed  Google Scholar 

  • Gehrke CW, Kuo KC (1990) Ribonucleoside analysis by reversed-phase high performance liquid chromatography. J Chromatogr Library 45(Part A):A3–A71

    Google Scholar 

  • Giessing AMB, Kirpekar F (2012) Mass spectrometry in the biology of RNA and its modifications. J Proteomics 75:3434–3449. https://doi.org/10.1016/j.jprot.2012.01.032

    Article  CAS  PubMed  Google Scholar 

  • Golubev A, Fatkhullin B, Khusainov I et al (2020) Cryo-EM structure of the ribosome functional complex of the human pathogen Staphylococcus aureus at 3.2 Å resolution. FEBS Lett 594:3551–3567

    Article  CAS  PubMed  Google Scholar 

  • Halfon Y, Matzov D, Eyal Z et al (2019) Exit tunnel modulation as resistance mechanism of S. aureus erythromycin resistant mutant. Sci Rep 9:11460

    Google Scholar 

  • Hansen MA, Kirpekar F, Ritterbusch W et al (2002) Posttranscriptional modifications in the A-loop of 23S rRNAs from selected archaea and eubacteria. RNA 8:202–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ho NW, Gilham PT (1971) Reaction of pseudouridine and inosine with N-cyclohexyl-N’-beta-(4-methylmorpholinium)ethylcarbodiimide. Biochemistry 10:3651–3657

    Article  CAS  PubMed  Google Scholar 

  • Houser WM, Butterer A, Addepalli B, a. (2015) Combining recombinant ribonuclease U2 and protein phosphatase for RNA modification mapping by liquid chromatography-mass spectrometry. Anal Biochem 478:52–58

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Zhang W, Katanski CD et al (2021) Interferon inducible pseudouridine modification in human mRNA by quantitative nanopore profiling. Genome Biol 22:330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igloi GL (1988) Interaction of tRNAs and of phosphorothioate-substituted nucleic acids with an organomercurial. Probing the chemical environment of thiolated residues by affinity electrophoresis. Biochemistry 27(10):3842–3849

    Google Scholar 

  • Igloi GL, Kössel H (1985) Affinity electrophoresis for monitoring terminal phosphorylation and the presence of queuosine in RNA. Application of polyacrylamide containing a covalently bound boronic acid. Nucleic Acids Res 13:6881–6898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igo-Kemenes T, Zachau HG (1969) On the specificity of the reduction of transfer ribonucleic acids with sodium borohydride. Eur J Biochem 10:549–556

    Article  CAS  PubMed  Google Scholar 

  • Incarnato D, Anselmi F, Morandi E et al (2017) High-throughput single-base resolution mapping of RNA 2΄-O-methylated residues. Nucleic Acids Res 45:1433–1441

    Article  CAS  PubMed  Google Scholar 

  • Ishitani R, Yokoyama S, Nureki O (2008) Structure, dynamics, and function of RNA modification enzymes. Curr Opin Struct Biol 18:330–339

    Article  CAS  PubMed  Google Scholar 

  • Jenner LB, Demeshkina N, Yusupova G et al (2010) Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat Struct Mol Biol 17:555–560

    Article  CAS  PubMed  Google Scholar 

  • Jora M, Borland K, Abernathy S et al (2021) Chemical amination/imination of carbonothiolated nucleosides during RNA hydrolysis. Angew Chem Int Ed Engl 60:3961–3966

    Article  CAS  PubMed  Google Scholar 

  • Jora M, Burns AP, Ross RL et al (2018) Differentiating positional isomers of nucleoside modifications by higher-energy collisional dissociation mass spectrometry (HCD MS). J Am Soc Mass Spectrom 29:1745–1756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jora M, Lobue PA, Ross RL et al (2019) Detection of ribonucleoside modifications by liquid chromatography coupled with mass spectrometry. Biochim Biophys Acta Gene Regul Mech 1862:280–290

    Article  CAS  PubMed  Google Scholar 

  • Jühling F, Mörl M, Hartmann RK et al (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37:D159-162

    Article  PubMed  Google Scholar 

  • Kanwal F, Lu C (2019) A review on native and denaturing purification methods for non-coding RNA (ncRNA). J Chromatogr B Analyt Technol Biomed Life Sci 1120:71–79

    Article  CAS  PubMed  Google Scholar 

  • Kebarle P, Tang L (1993) From ions in solution to ions in the gas phase. Anal Chem 65:972A-986A

    CAS  Google Scholar 

  • Kellner S, Neumann J, Rosenkranz D et al (2014) Profiling of RNA modifications by multiplexed stable isotope labelling. Chem Commun 50:3516–3518

    Article  CAS  Google Scholar 

  • Khoddami V, Yerra A, Mosbruger TL et al (2019) Transcriptome-wide profiling of multiple RNA modifications simultaneously at single-base resolution. Proc Natl Acad Sci USA 116:6784–6789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khusainov I, Fatkhullin B, Pellegrino S et al (2020) Mechanism of ribosome shutdown by RsfS in Staphylococcus aureus revealed by integrative structural biology approach. Nat Commun 11:1656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khusainov I, Vicens Q, Ayupov R et al (2017) Structures and dynamics of hibernating ribosomes from Staphylococcus aureus mediated by intermolecular interactions of HPF. EMBO J 36:2073–2087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khusainov I, Vicens Q, Bochler A et al (2016) Structure of the 70S ribosome from human pathogen Staphylococcus aureus. Nucleic Acids Res 44:10491–10504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiesewetter S, Fischer W, Sprinzl M (1987) Sequences of three minor tRNAsArg from E. coli. Nucleic Acids Res 15:3184

    Google Scholar 

  • Klaholz BP (2019) Deriving and refining atomic models in crystallography and cryo-EM: the latest Phenix tools to facilitate structure analysis. Acta Crystallogr D Struct Biol 75:878–881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kowalak JA, Pomerantz SC, Crain PF et al (1993) A novel method for the determination of post-transcriptional modification in RNA by mass spectrometry. Nucleic Acids Res 21:4577–4585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kristen M, Plehn J, Marchand V et al (2020) Manganese Ions Individually Alter the Reverse Transcription Signature of Modified Ribonucleosides. Genes (basel) 11:950

    Article  CAS  PubMed  Google Scholar 

  • Kühlbrandt W (2014) Biochemistry. The resolution revolution. Science 343:1443–1444

    Article  PubMed  Google Scholar 

  • Li GW, Burkhardt D, Gross C et al (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maden BE, Corbett ME, Heeney PA et al (1995) Classical and novel approaches to the detection and localization of the numerous modified nucleotides in eukaryotic ribosomal RNA. Biochimie 77:22–29

    Article  CAS  PubMed  Google Scholar 

  • Marchand V, Blanloeil-Oillo F, Helm M et al (2016) Illumina-based RiboMethSeq approach for mapping of 2’-O-Me residues in RNA. Nucleic Acids Res 44:e135

    Article  PubMed  PubMed Central  Google Scholar 

  • Marchand V, Ayadi L, Ernst FGM et al (2018) AlkAniline-Seq: profiling of m(7) G and m(3) C RNA modifications at single nucleotide resolution. Angew Chem Int Ed Engl 57:16785–16790

    Article  CAS  PubMed  Google Scholar 

  • Marchand V, Ayadi L, Bourguignon-Igel V et al (2021a) AlkAniline-Seq: a highly sensitive and specific method for simultaneous mapping of 7-methyl-guanosine (m(7)G) and 3-methyl-cytosine (m(3)C) in RNAs by high-throughput sequencing. Meth Mol Biol 2298:77–95

    Article  CAS  Google Scholar 

  • Marchand V, Bourguignon-Igel V, Helm M et al (2021b) Mapping of 7-methylguanosine (m(7)G), 3-methylcytidine (m(3)C), dihydrouridine (D) and 5-hydroxycytidine (ho(5)C) RNA modifications by AlkAniline-Seq. Methods Enzymol 658:25–47

    Article  CAS  PubMed  Google Scholar 

  • Marchand V, Bourguignon-Igel V, Helm M et al (2022) Analysis of pseudouridines and other RNA modifications using HydraPsiSeq protocol. Methods 203:383–391

    Article  CAS  PubMed  Google Scholar 

  • Marchand V, Pichot F, Neybecker P et al (2020) HydraPsiSeq: a method for systematic and quantitative mapping of pseudouridines in RNA. Nucleic Acids Res 48:e110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchand V, Pichot F, Thuring K et al (2017) Next-generation sequencing-based ribomethseq protocol for analysis of tRNA 2’-O-methylation. Biomolecules 7:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Matzov D, Aibara S, Basu A et al (2017) The cryo-EM structure of hibernating 100S ribosome dimer from pathogenic Staphylococcus aureus. Nat Commun 8:723

    Article  PubMed  PubMed Central  Google Scholar 

  • McGinnis AC, Grubb EC, Bartlett MG (2013) Systematic optimization of ion-pairing agents and hexafluoroisopropanol for enhanced electrospray ionization mass spectrometry of oligonucleotides. Rapid Commun Mass Spectrom 27:2655–2664

    Article  CAS  PubMed  Google Scholar 

  • McKenna SA, Kim I, Puglisi EV et al (2007) Purification and characterization of transcribed RNAs using gel filtration chromatography. Nat Protoc 2:3270–3277

    Article  CAS  PubMed  Google Scholar 

  • Mcluckey SA, Van Berkel GJ, Glish GL (1992) Tandem mass spectrometry of small, multiply charged oligonucleotides. J Am Soc Mass Spectrom 3:60–70

    Article  CAS  PubMed  Google Scholar 

  • Mengel-Jørgensen J, Kirpekar F (2002) Detection of pseudouridine and other modifications in tRNA by cyanoethylation and MALDI mass spectrometry. Nucleic Acids Res 30:e135

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyer M, Masquida B (2016) Polyacrylamide gel electrophoresis for purification of large amounts of RNA. Methods Mol Biol 1320:59–65

    Article  PubMed  Google Scholar 

  • Mims BH, Prather NE, Murgola EJ (1985) Isolation and nucleotide sequence analysis of tRNAAlaGGC from Escherichia coli K-12. J Bacteriol 162:837–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyauchi K, Kimura S, Suzuki T (2013) A cyclic form of N 6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodification. Nat Chem Biol 9:105–111

    Article  CAS  PubMed  Google Scholar 

  • Miyauchi K, Ohara T, Suzuki T (2007) Automated parallel isolation of multiple species of non-coding RNAs by the reciprocal circulating chromatography method. Nucleic Acids Res 35:e24

    Article  PubMed  PubMed Central  Google Scholar 

  • Motorin Y, Helm M (2019) Methods for RNA modification mapping using deep sequencing: established and new emerging technologies. Genes (basel) 10:35

    Article  PubMed  Google Scholar 

  • Motorin Y, Helm M (2022) RNA nucleotide methylation: 2021 update. Wiley Interdiscip Rev RNA 13:e1691

    Article  CAS  PubMed  Google Scholar 

  • Motorin Y, Marchand V (2018) Detection and analysis of RNA ribose 2’-O-methylations: challenges and solutions. Genes (basel) 9:642

    Article  PubMed  Google Scholar 

  • Motorin Y, Marchand V (2021) Analysis of RNA modifications by second- and third-generation deep sequencing: 2020 update. Genes (basel) 12:278

    Article  CAS  PubMed  Google Scholar 

  • Motorin Y, Muller S, Behm-Ansmant I, a. (2007) Identification of modified residues in RNAs by reverse transcription-based methods. Meth Enzymol 425:21–53

    Article  CAS  Google Scholar 

  • Nakai C, Konishi A, Komatsu Y et al (1994) Sequence-specific cleavage of RNA by a hybrid ribonuclease H. FEBS Lett 339:67–72

    Article  CAS  PubMed  Google Scholar 

  • Nakamura K, Takeo K (1998) Affinity electrophoresis and its applications to studies of immune response. J Chromatogr B Biomed Sci Appl 715:125–136

    Article  CAS  PubMed  Google Scholar 

  • Nakayama H, Takahashi N, Isobe T (2011) Informatics for mass spectrometry-based RNA analysis. Mass Spectrom Rev 30:1000–1012

    Article  CAS  PubMed  Google Scholar 

  • Natchiar SK, Myasnikov AG, Hazemann I et al (2018) Visualizing the role of 2’-OH rRNA methylations in the human ribosome structure. Biomolecules 8:125

    Article  PubMed  PubMed Central  Google Scholar 

  • Natchiar SK, Myasnikov AG, Kratzat H et al (2017) Visualization of chemical modifications in the human 80S ribosome structure. Nature 551:472–477

    Article  CAS  PubMed  Google Scholar 

  • Ni J, Pomerantz C, Rozenski J et al (1996) Interpretation of oligonucleotide mass spectra for determination of sequence using electrospray ionization and tandem mass spectrometry. Anal Chem 68:1989–1999

    Article  CAS  PubMed  Google Scholar 

  • Nübel G, Sorgenfrei FA, Jäschke A (2017) Boronate affinity electrophoresis for the purification and analysis of cofactor-modified RNAs. Methods 117:14–20

    Article  PubMed  Google Scholar 

  • Ohira T, Minowa K, Sugiyama K et al (2022) Reversible RNA phosphorylation stabilizes tRNA for cellular thermotolerance. Nature 605:372–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patteson KG, Rodicio LP, Limbach PA (2001) Identification of the mass-silent post-transcriptionally modified nucleoside pseudouridine in RNA by matrix-assisted laser desorption/ionization mass spectrometry. Nucleic Acids Res 29:49–49

    Article  Google Scholar 

  • Peattie DA (1979) Direct chemical method for sequencing RNA. Proc Natl Acad Sci USA 76:1760–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrov A, Wu T, Puglisi EV et al (2013) RNA purification by preparative polyacrylamide gel electrophoresis. Meth Enzymol 530:315–330

    Article  CAS  Google Scholar 

  • Pichot F, Marchand V, Helm M et al (2021) Non-redundant tRNA reference sequences for deep sequencing analysis of tRNA abundance and epitranscriptomic RNA modifications. Genes (basel) 12:81

    Article  CAS  PubMed  Google Scholar 

  • Piekna-Przybylska D, Decatur WA, Fournier MJ (2008) The 3D rRNA modification maps database: with interactive tools for ribosome analysis. Nucleic Acids Res 36:D178-183

    Article  CAS  PubMed  Google Scholar 

  • Polikanov YS, Melnikov SV, Soll D et al (2015) Structural insights into the role of rRNA modifications in protein synthesis and ribosome assembly. Nat Struct Mol Biol 22:342–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polo LM, Limbach PA (2001) Analysis of Oligonucleotides by Electrospray Ionization Mass Spectrometry. Curr Protoc Nucleic Acid Chem

    Google Scholar 

  • Pomerantz SC, McCloskey JA (1990) Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry. Methods Enzymol 193:796–824

    Article  CAS  PubMed  Google Scholar 

  • Potapov V, Fu X, Dai N et al (2018) Base modifications affecting RNA polymerase and reverse transcriptase fidelity. Nucleic Acids Res 46:5753–5763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potier N, van Dorsselaer A, Cordier Y et al (1994) Negative electrospray ionization mass spectrometry of synthetic and chemically modified oligonucleotides. Nucleic Acids Res 22:3895–3903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poulson R (1973) Isolation, Purification and Fractionation of RNA. The ribonucleic acids, pp 243–261

    Google Scholar 

  • Rebane A, Roomere H, Metspalu A (2002) Locations of several novel 2’-O-methylated nucleotides in human 28S rRNA. BMC Mol Biol 3:1

    Article  PubMed  PubMed Central  Google Scholar 

  • Roost C, Lynch SR, Batista PJ et al (2015) Structure and thermodynamics of N6-methyladenosine in RNA: a spring-loaded base modification. J Am Chem Soc 137:2107–2115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ross R, Cao X, Yu N et al (2016) Sequence mapping of transfer RNA chemical modifications by liquid chromatography tandem mass spectrometry. Methods (san Diego, Calif) 107:73–78

    Article  CAS  PubMed  Google Scholar 

  • Samatova E, Daberger J, Liutkute M et al (2020) Translational control by ribosome pausing in bacteria: how a non-uniform pace of translation affects protein production and folding. Front Microbiol 11:619430

    Article  PubMed  Google Scholar 

  • Schaefer M, Kapoor U, Jantsch MF (2017) Understanding RNA modifications: the promises and technological bottlenecks of the ‘epitranscriptome.’ Open Biol 7:1–14

    Article  Google Scholar 

  • Schaefer M, Pollex T, Hanna K et al (2009) RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res 37:e12

    Article  PubMed  Google Scholar 

  • Schwartz S, Bernstein DA, Mumbach MR et al (2014) Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 159:148–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Squires JE, Patel HR, Nousch M et al (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 40:5023–5033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stern S, Moazed D, Noller HF (1988) Structural analysis of RNA using chemical and enzymatic probing monitored by primer extension. Methods Enzymol 164:481–489

    Article  CAS  PubMed  Google Scholar 

  • Stojković V, Myasnikov AG, Young ID et al (2020) Assessment of the nucleotide modifications in the high-resolution cryo-electron microscopy structure of the Escherichia coli 50S subunit. Nucleic Acids Res 48:2723–2732

    Article  PubMed  PubMed Central  Google Scholar 

  • Stults JT, Marsters JC, Carr SA (1991) Improved electrospray ionization of synthetic oligodeoxynucleotides. Rapid Commun Mass Spectrom 5:359–363

    Article  CAS  Google Scholar 

  • Su D, Chan CTY, Gu C et al (2014) Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry. Nat Protoc 9:828–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T, Suzuki T (2007) Chaplet column chromatography: isolation of a large set of individual RNAs in a single step. Meth Enzymol 425:231–239

    Article  CAS  Google Scholar 

  • Taoka M, Ikumi M, Nakayama H et al (2010) In-gel digestion for mass spectrometric characterization of RNA from fluorescently stained polyacrylamide gels. Anal Chem 82:7795–7803

    Article  CAS  PubMed  Google Scholar 

  • Thakur P, Jora M, Zhao R et al (2021) Mass spectrometry-based methods for characterization of hypomodifications in transfer RNA. Springer. Epitranscriptomics, pp 555–592

    Google Scholar 

  • Thomas B, Akoulitchev AV (2006) Mass spectrometry of RNA. Trends Biochem Sci 31:173–181

    Article  CAS  PubMed  Google Scholar 

  • Thuring K, Schmid K, Keller P et al (2016) Analysis of RNA modifications by liquid chromatography-tandem mass spectrometry. Methods 107:48–56

    Article  PubMed  Google Scholar 

  • Tollerson R 2nd, Ibba M (2020) Translational regulation of environmental adaptation in bacteria. J Biol Chem 295:10434–10445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuorto F, Legrand C, Cirzi C et al (2018) Queuosine-modified tRNAs confer nutritional control of protein translation. EMBO J 37:e99777

    Article  PubMed  PubMed Central  Google Scholar 

  • Ty H, Kharlamova A, Liu J et al (2008) Ion trap collision-induced dissociation of multiply deprotonated RNA: c/y-Ions versus (a-B)/w-Ions. J Am Soc Mass Spectrom 19:1832–1840

    Article  Google Scholar 

  • Wang J, Natchiar SK, Moore PB et al (2021) Identification of Mg(2+) ions next to nucleotides in cryo-EM maps using electrostatic potential maps. Acta Crystallogr D Struct Biol 77:534–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson ZL, Ward FR, Méheust R et al (2020) Structure of the bacterial ribosome at 2 Å resolution. Elife 9:e60482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werner S, Galliot A, Pichot F et al (2021) NOseq: amplicon sequencing evaluation method for RNA m6A sites after chemical deamination. Nucleic Acids Res 49:e23

    Article  CAS  PubMed  Google Scholar 

  • Werner S, Schmidt L, Marchand V et al (2020) Machine learning of reverse transcription signatures of variegated polymerases allows mapping and discrimination of methylated purines in limited transcriptomes. Nucleic Acids Res 48:3734–3746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wetzel C, Limbach PA (2016) Mass spectrometry of modified RNAs: recent developments. Analyst 141:16–23

    Article  CAS  PubMed  Google Scholar 

  • Wolff P, Villette C, Zumsteg J et al (2020) Comparative patterns of modified nucleotides in individual tRNA species from a mesophilic and two thermophilic archaea. RNA 26:1957–1975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright A, Deane-Alder K, Marschall E et al (2020) Characterization of the core ribosomal binding region for the oxazolidone family of antibiotics using cryo-EM. ACS Pharmacol Transl Sci 3:425–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xing F, Hiley SL, Hughes TR et al (2004) The specificities of four yeast dihydrouridine synthases for cytoplasmic tRNAs. J Biol Chem 279:17850–17860

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Sharma S, Watzinger P et al (2016) Mapping of complete set of ribose and base modifications of yeast rRNA by RP-HPLC and mung bean nuclease assay. PLoS ONE 11:e0168873

    Article  PubMed  PubMed Central  Google Scholar 

  • Yokogawa T, Kitamura Y, Nakamura D et al (2010) Optimization of the hybridization-based method for purification of thermostable tRNAs in the presence of tetraalkylammonium salts. Nucleic Acids Res 38:e89

    Article  PubMed  Google Scholar 

  • Yoluç Y, Ammann G, Barraud P et al (2021) Instrumental analysis of RNA modifications. Crit Rev Biochem Mol Biol 56:178–204

    Article  PubMed  Google Scholar 

  • Zheng C, Black KA, Dos Santos PC (2017) Diverse mechanisms of sulfur decoration in bacterial tRNA and their cellular functions. Biomolecules 7:33

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Centre National de la Recherche Scientifique (CNRS), by the French National Research Agency ANR (ANR-21-CE12-0030-01 to [SM]), by the Region Grand Est (N°18P-09227- EpiRNA), and the previous French National Program Investissement d’Avenir (Labex NetRNA) (ANR-10-LABX-0036_NETRNA). This work of the Interdisciplinary Thematic Institute IMCBio, as part of the ITI 2021–2028 program of the University of Strasbourg, CNRS, and Inserm, was supported by IdEx Unistra (ANR-10-IDEX-0002), by SFRI-STRAT’US project (20-SFRI-0012), and EUR IMCBio (IMCBio ANR-17-EURE-0023) under the framework of the France 2030 Program. [HK] is supported by a fellowship from Fondation de la Recherche Médicale (FRM). [BPK] acknowledges support by CNRS, Association pour la Recherche sur le Cancer (ARC), Institut National du Cancer (INCa_16099), the Fondation pour la Recherche Médicale (FRM) and ANR.

Author information

Authors and Affiliations

  1. Architecture Et Réactivité de L’ARN, CNRS, Université de Strasbourg, 9002, Strasbourg, France

    Roberto Bahena-Ceron, Jose Jaramillo-Ponce, Hiroki Kanazawa, Laura Antoine, Philippe Wolff, Pascale Romby & Stefano Marzi

  2. Université de Lorraine, CNRS, IMoPA (UMR7365), 54000, Nancy, France

    Virginie Marchand & Yuri Motorin

  3. Université de Lorraine, CNRS, INSERM, IBSLor (UAR2008/US40), F54000, Nancy, France

    Virginie Marchand & Yuri Motorin

  4. Centre for Integrative Biology (CBI), Department of Integrated Structural Biology, IGBMC (Institute of Genetics and of Molecular and Cellular Biology), 1 Rue Laurent Fries, Illkirch, France

    Bruno P. Klaholz

  5. Centre National de La Recherche Scientifique (CNRS) UMR 7104, Illkirch, France

    Bruno P. Klaholz

  6. Institut National de La Santé Et de La Recherche Médicale (Inserm) U964, Illkirch, France

    Bruno P. Klaholz

  7. Université de Strasbourg, Strasbourg, France

    Bruno P. Klaholz

Authors
  1. Roberto Bahena-Ceron
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jose Jaramillo-Ponce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroki Kanazawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura Antoine
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philippe Wolff
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Virginie Marchand
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bruno P. Klaholz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuri Motorin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Pascale Romby
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Stefano Marzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefano Marzi .

Editor information

Editors and Affiliations

  1. NanoBioMedical Centre of Adam Mickiewicz University, Poznań, Poland

    Jan Barciszewski

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bahena-Ceron, R. et al. (2023). Methods to Analyze Post-transcriptional Modifications Applied to Stable RNAs in Staphylococcus aureus. In: Barciszewski, J. (eds) RNA Structure and Function. RNA Technologies, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-031-36390-0_11

Download citation

Publish with us

Policies and ethics

Search

Navigation