Attomole quantification and global profile of RNA modifications: Epitranscriptome of human neural stem cells

Nucleic Acids Research

Volumn 44, Issue 3, 2016, Pages

  Basanta Sanchez, Maria ^a   Temple, Sally ^b   Ansari, Suraiya A ^b   D'Amico, Anna ^a   Agris, Paul F ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b Neural Stem Cell Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLADENOSINE; 1 METHYLGUANOSINE; 1 METHYLINOSINE; 2 THIOCYTIDINE; 2 THIOURIDINE; 2' O METHYLCYTIDINE; 2' O METHYLGUANOSINE; 2' O METHYLURIDINE; 3 METHYLURIDINE; 4 THIOURIDINE; 5 FORMYLCYTIDINE; 5 METHOXYURIDINE; 5 METHYLCYTIDINE; 5 METHYLURIDINE; 6 METHYLURIDINE; 6 N (3,3 DIMETHYLALLYL)ADENOSINE; 6 N METHYLADENOSINE; 7 METHYLGUANOSINE; ADENOSINE; CYTIDINE; DIHYDROURIDINE; EPITRANSCRIPTOME; GUANOSINE; INOSINE; N 2 METHYLGUANOSINE; N 4 ACETYLCYTIDINE; NUCLEOSIDE; TRANSCRIPTOME; UNCLASSIFIED DRUG; URIDINE; RNA;

ABSORPTION; ANIMAL CELL; ARTICLE; ATTOMOLE; CALCULATION; CONSTANTS AND COEFFICIENTS; CONTROLLED STUDY; EMBRYO; EXTINCTION COEFFICIENT; FEMTOMOLE; HUMAN; HUMAN CELL; LIMIT OF DETECTION; MOLECULAR WEIGHT; MOUSE; NEURAL STEM CELL; NONHUMAN; PHYSICAL PHENOMENA; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; RNA ANALYSIS; RNA EXTRACTION; RNA ISOLATION; RNA PROCESSING; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; CELL CULTURE; GENE EXPRESSION PROFILING; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; PROCEDURES;

CELLS, CULTURED; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GENE EXPRESSION PROFILING; HUMANS; LIMIT OF DETECTION; NEURAL STEM CELLS; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL; TANDEM MASS SPECTROMETRY; TRANSCRIPTOME;

EID: 84965002749     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv971     Document Type: Article

References (48)

1. Niu, Y., Zhao, X., Wu, Y., Li, M., Wang, X. and Yang, Y. (2013) N6-methyl- Adenosine (m6A) in RNA: An Old Modification with A Novel Epigenetic Function. Genomics Proteomics Bioinformatics, 11, 8-17.
2. Satterlee, J.S., Basanta-Sanchez, M., Blanco, S., Li, J.B., Meyer, K., Pollock, J., Sadru-Vakili, G. and Rybak-Wolf, A. (2014) Novel RNA Modifications in the Nervous System: Form and Function. J. Neurosci., 34, 15170-15177.
3. Agris, P.F. (2015) The importance of being modified: An unrealized code to RNA structure and function. RNA, 21, 552-554.
4. Saletore, Y., Meyer, K., Korlach, J., Vilfan, I.D., Jaffrey, S. and Mason, C.E. (2012) The birth of the Epitranscriptome: deciphering the function of RNA modifications. Genome Biol., 13, 175.
5. Kellner, S., Burhenne, J. and Helm, M. (2010) Detection of RNA modifications. RNA Biol., 7, 237-247.
6. Cantara, W.A., Crain, P.F., Rozenski, J., McCloskey, J.A., Harris, K.A., Zhang, X., Vendeix, F.A.P, Fabris, D. and Agris, P.F. (2011) The RNA modification database, RNAMDB: 2011 update. Nucleic Acids Res., 39, D195-D201.
7. Machnicka, M.A., Milanowska, K., Oglou, O.O., Purta, E., Kurkowska, M., Olchowik, A., Januszewski, W., Kalinowski, S., Dunin-Horkawicz, S, Rother, K.M. et al. (2013) MODOMICS: A database of RNA modification pathways-2013 update. Nucleic Acids Res., 41, D262-D267.
8. Agris, P.F. (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.
9. Chan, C.T.Y., Dyavauah, M., DeMott, M.S., Taghizadeh, K., Dedon, P.C. and Begley, T.J. (2010) A Quantitative Systems Approach Reveals Dynamic Control of tRNA Modifications during Cellular Stress. Plos Genet., 6, e1001247.
10. Begley, U., Dyavaiah, M., Patil, A., Rooney, J.P., DiRenzo, D., Young, C.M., Conklin, D.S., Zitomer, R.S. and Begley, T.J. (2007) Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol. Cell, 28, 860-870.
11. Russell, S.P. and Limbach, P.A. (2013) Evaluating the reproducibility of quantifying modified nucleosides from ribonucleic acids by LC-UV-MS. J. Chromatogr. B, 923-924, 74-82.
12. Lui, L. and Lowe, T. (2013) Small nucleolar RNAs and RNA-guided post- Transcriptional modification. Essays Biochem., 54, 53-77.
13. Li, S.C., Tsai, K.W., Pan, H.W., Jeng, Y.M., Ho, M.R. and Li, W.H. (2012) MicroRNA 3' end nucleotide modification patterns and arm selection preference in liver tissues. BMC Syst. Biol., 6, S14.
14. Meyer, K.D., Saletore, Y., Zumbo, P., Elemento, O., Mason, C.E. and Jaffrey, S.R. (2012) Comprehensive Analysis of mRNA Methylation Reveals Enrichment in 3'UTRs and near Stop Codons. Cell, 149, 1635-1646.
15. Carlile, T.M., Rojas-Duran, M.F., Zinshteyn, B., Shin, H., Bartoli, K.M. and Gilbert, W.V. (2014) Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells. Nature, 515, 143-146.
16. Linder, B., Grozhik, A.V., Olarerin-George, A.O., Meydan, C., Mason, C.E. and Jaffrey, S.R. (2015) Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome. Nat. Meth., 12, 767-772.
17. Gaston, K.W. and Limbach, P.A. (2014) The identification and characterization of non-coding and coding RNAs and their modified nucleosides by mass spectrometry. RNA Biol., 11, 1568-1585.
18. Davis, G.E., Gehrke, C.W., Kuo, K.C. and Agris, P.F. (1979) Major and modified nucleosides in tRNA hydrolysates by high performance liquid chromatography. J. Chromatogr., 173, 281-298.
19. Gehrke, C.W., Kuo, K.C., McCune, R.A., Gerhardt, K.O. and Agris, P.F. (1982) Quantitative enzymatic hydrolysis of tRNAs: Reversed-phase high-performance liquid chromatography of tRNA nucleosides. J. Chromatogr. B, 230, 297-308.
20. Su, D., Chan, C.T., Gu, C., Lim, K.S., Chionh, Y.H., McBee, M.E., Russell, B.S., Babu, I.R., Begley, T.J. and Dedon, P.C. (2014) Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry. Nat. Protoc., 9, 828-841.
21. Rose, R.E., Quinn, R., Sayre, J.L. and Fabris, D. (2015) Profiling ribonucleotide modifications at full- Transcriptome level: A step toward MS-based epitranscriptomics. RNA, 21, 1361-1374.
22. Wang, Y., Li, Y., Toth, J.I., Petroski, M.D., Zhang, Z. and Zhao, J.C. (2014) N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat. Cell Biol., 16, 191-198.
23. Chen, T., Hao, Y., Zhang, Y., Li, M., Wang, M., Han, W., Wu, Y., Lv, Y., Hao, J., Wang, L. et al. (2015) m6A RNA Methylation Is Regulated by MicroRNAs and Promotes Reprogramming to Pluripotency. Cell Stem Cell, 16, 289-301.
24. Edelheit, S., Schwartz, S., Mumbach, M.R., Wurtzel, O. and Sorek, R. (2013) Transcriptome-WideMapping of 5-methylcytidine RNA Modifications in Bacteria, Archaea, and Yeast Reveals m5C within Archaeal mRNAs. PLoS Genet., 9, e1003602.
25. Cavaluzzi, M.J. and Borer, P.N. (2004) Revised UV extinction coefficients for nucleoside-5-monophosphates and unpaired DNA and RNA. Nucleic Acids Res., 32, e13.
26. Brandmayr, C., Wagner, M., Brückl, T., Globisch, D., Pearson, D., Kneuttinger, A.C., Reiter, V., Hienzsch, A., Koch, S., Thoma, I. et al. (2012) Isotope-Based Analysis of Modified tRNA Nucleosides Correlates Modification Density with Translational Efficiency. Angew. Chem. Int. Ed. Engl., 51, 11162-11165.
27. Laourdakis, C.D., Merino, E.F., Neilson, A.P. and Cassera, M.B. (2014) Comprehensive quantitative analysis of purines and pyrimidines in the human malaria parasite using ion-pairing ultra-performance liquid chromatography-mass spectrometry. J. Chromatogr. B, 967, 127-133.
28. Kellner, S., Ochel, A., Thuring, K., Spenkuch, F., Neumann, J., Sharma, S., Entian, K.-D., Schneider, D. and Helm, M. (2014) Absolute and relative quantification of RNA modifications via biosynthetic isotopomers. Nucleic Acids Res., 42, e142.
29. Shrivastava, A. and Gupta, V. (2011) Methods for the determination of limit of detection and limit of quantitation of the analytical methods. Chronicles of Young Scientists, 2, 21-25.
30. Fasano, C.A., Chambers, S.M., Lee, G., Tomishima, M.J. and Studer, L. (2010) Efficient derivation of functional floor plate tissue from human embryonic stem cells. Cell Stem Cell, 6, 336-347.
31. Van de Leemput, J., Boles, N.C., Kiehl, T.R., Corneo, B., Lederman, P., Menon, V., Lee, C., Martinez, R.A., Levi, B.P., Thompson, C.L. et al. (2014) CORTECON: A Temporal Transcriptome Analysis of In Vitro Human Cerebral Cortex Development from Human Embryonic Stem Cells. Neuron, 83, 51-68.
32. Chambers, S.M., Fasano, C.A., Papapetrou, E.P., Tomishima, M., Sadelain, M. and Studer, L. (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol., 27, 275-280.
33. Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S.N. et al. (2008) An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature, 455, 351-357.
34. Qian, X., Davis, A.A., Goderie, S.K. and Temple, S. (1997) FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron, 18, 81-93.
35. Crain, P.F. (1990) Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry. Meth. Enzymol., 193, 782-790.
36. Luo, G.-Z., MacQueen, A., Zheng, G., Duan, H., Dore, L.C., Lu, Z., Liu, J., Chen, K., Jia, G., Bergelson, J. et al. (2014) Unique features of the m6A methylome in Arabidopsis thaliana. Nat. Commun., 5, 5630.
37. Shih, P., Pedersen, L.G., Gibbs, P.R. and Wolfenden, R. (1998) Hydrophobicities of the nucleic acid bases: distribution coefficients from water to cyclohexane. J. Mol. Biol., 280, 421-430.
38. Quinn, R., Basanta-Sanchez, M., Rose, R.E. and Fabris, D. (2013) Direct infusion analysis of nucleotide mixtures of very similar or identical elemental composition. J. Mass Spectrom., 48, 703-712.
39. Dominissini, D., Moshitch-Moshkovitz, S., Salmon-Divon, M., Amariglio, N. and Rechavi, G. (2013) Transcriptome-wide mapping of N6-methyladenosine by m6A-seq based on immunocapturing and massively parallel sequencing. Nat. Protoc., 8, 176-189.
40. Alarcón, C.R., Lee, H., Goodarzi, H., Halberg, N. and Tavazoie, S.F. (2015) N6-methyladenosine marks primary microRNAs for processing. Nature, 519, 482-485.
41. Squires, J.E., Patel, H.R., Nousch, M., Sibbritt, T., Humphreys, D.T., Parker, B.J., Suter, C.M. and Preiss, T. (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res., 40, 5023-5033.
42. Cavaillé, J., Buiting, K., Kiefmann, M., Lalande, M., Brannan, C.I., Horsthemke, B., Bachellerie, J.P., Brosius, J. and Hüttenhofer, A. (2000) Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. PNAS, 97, 14311-14316.
43. Nestler, E.J. (2005) The Neurobiology of Cocaine Addiction. Sci. Pract. Perspect., 3, 4-10.
44. Martin, C.B.P., Ramond, F., Farrington, D.T., Aguiar, A.S. Jr., Chevarin, C., Berthiau, A.S., Caussanel, S., Lanfumey, L., Herrick-Davis, K., Hamon, M. et al. (2013) RNA splicing and editing modulation of 5-HT2C receptor function: Relevance to anxiety and aggression in VGV mice. Mol. Psychiatry, 18, 656-665.
45. Agris, P.F. (2008) Bringing order to translation: The contributions of transfer RNA anticodon-domain modifications. EMBO Rep., 9, 629-635.
46. Blanco, S., Dietmann, S., Flores, J.V., Hussain, S., Kutter, C., Humphreys, P., Lukk, M., Lombard, P., Treps, L., Popis, M. et al. (2014) Aberrant methylation of tRNAs links cellular stress to neuro-developmental disorders. EMBO J., 33, 2020-2039.
47. Li, J.B. and Church, G.M. (2013) Deciphering the functions and regulation of brain-enriched A- To-I RNA editing. Nat. Neurosci., 16, 1518-1522.
48. Li, S. and Mason, C.E. (2014) The Pivotal Regulatory Landscape of RNA Modifications. Annu. Rev.Genomics Hum. Genet., 15, 127-150.