Partial methylation at Am100 in 18S rRNA of Baker's yeast reveals ribosome heterogeneity on the level of eukaryotic rRNA modification

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Buchhaupt, Markus ^a   Sharma, Sunny ^b   Kellner, Stefanie ^c   Oswald, Stefanie ^b   Paetzold, Melanie ^a   Peifer, Christian ^b   Watzinger, Peter ^b   Schrader, Jens ^a   Helm, Mark ^c   Entian, Karl Dieter ^b  

^a KARL WINNACKER INSTITUT   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBOZYME; RIBOSOME RNA; RNA 18S;

ARTICLE; CELL HETEROGENEITY; CHEMICAL MODIFICATION; CONTROLLED STUDY; FUNGAL CELL CULTURE; FUNGUS GROWTH; LIQUID CHROMATOGRAPHY; NONHUMAN; PLASMID; POLYSOME; RIBOSOME; RIBOSOME SUBUNIT; RNA CLEAVAGE; RNA GENE; RNA METHYLATION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SNORNA GENE; TANDEM MASS SPECTROMETRY; ULTRAVIOLET SPECTROSCOPY;

METHYLATION; RIBOSOMES; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE;

EID: 84896498492     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089640     Document Type: Article

References (38)

1. Anger AM, Armache JP, Berninghausen O, Habeck M, Subklewe M, et al. (2013) Structures of the human and Drosophila 80S ribosome. Nature 497: 80-85.
2. Ramagopal S (1992) Are eukaryotic ribosomes heterogeneous? Affirmations on the horizon. Biochem Cell Biol 70: 269-272.
3. Delaunay J, Mathieu C, Schapira G (1972) Eukaryotic ribosomal proteins. Interspecific and intraspecific comparisons by two-dimensional polyacrylamidegel electrophoresis. Eur J Biochem 31: 561-564.
4. Lambertsson AG (1975) The ribosomal proteins of Drosophila melanogaster. IV. Characterization by two-dimensional gel electrophoresis of the ribosomal proteins from nine postembryonic developmental stages. Mol Gen Genet 139: 133-144.
5. Gunderson JH, Sogin ML, Wollett G, Hollingdale M, de la Cruz VF, et al. (1987) Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238: 933-937. (Pubitemid 17163277)
6. Gilbert WV (2011) Functional specialization of ribosomes? Trends Biochem Sci 36: 127-132.
7. Xue S, Barna M (2012) Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 13: 355-369.
8. Machnicka MA, Milanowska K, Osman Oglou O, Purta E, Kurkowska M, et al. (2013) MODOMICS: a database of RNA modification pathways-2013 update. Nucleic Acids Res 41: D262-267.
9. Sharma S, Yang J, Watzinger P, Kötter P, Entian KD (2013) Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res 41: 9062-9076.
10. Castle JC, Armour CD, Lower M, Haynor D, Biery M, et al. (2010) Digital genome-wide ncRNA expression, including snoRNAs, across 11 human tissues using polyA-neutral amplification. PLoS One 5: e11779.
11. Hughes ME, Grant GR, Paquin C, Qian J, Nitabach MN (2012) Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res 22: 1266-1281.
12. Higa-Nakamine S, Suzuki T, Uechi T, Chakraborty A, Nakajima Y, et al. (2012) Loss of ribosomal RNA modification causes developmental defects in zebrafish. Nucleic Acids Res 40: 391-398.
13. Esguerra J (2008) High- resolution phenotypic profiling of a eukaryotic ribosome [PhD]. Gothenburg: University of Gothenburg.
14. Esguerra J, Warringer J, Blomberg A (2008) Functional importance of individual rRNA 29-O-ribose methylations revealed by high-resolution phenotyping. RNA 14: 649-656. (Pubitemid 351480877)
15. Andersen TE, Porse BT, Kirpekar F (2004) A novel partial modification at C2501 in Escherichia coli 23S ribosomal RNA. RNA 10: 907-913. (Pubitemid 38669763)
16. Hansen MA, Kirpekar F, Ritterbusch W, Vester B (2002) Posttranscriptional modifications in the A-loop of 23S rRNAs from selected archaea and eubacteria. RNA 8: 202-213. (Pubitemid 34288907)
17. Belin S, Beghin A, Solano-Gonzalez E, Bezin L, Brunet-Manquat S, et al. (2009) Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS One 4: e7147.
18. Buchhaupt M, Peifer C, Entian KD (2007) Analysis of 29-O-methylated nucleosides and pseudouridines in ribosomal RNAs using DNAzymes. Anal Biochem 361: 102-108. (Pubitemid 46027002)
19. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368. (Pubitemid 33140562)
20. Schoemaker RJ, Gultyaev AP (2006) Computer simulation of chaperone effects of archaeal C/D box sRNA binding on rRNA folding. Nucleic Acids Res 34: 2015-2026. (Pubitemid 44314200)
21. Maden BE, Corbett ME, Heeney PA, Pugh K, Ajuh PM (1995) Classical and novel approaches to the detection and localization of the numerous modified nucleotides in eukaryotic ribosomal RNA. Biochimie 77: 22-29.
22. Yu YT, Shu MD, Steitz JA (1997) A new method for detecting sites of 29-Omethylation in RNA molecules. RNA 3: 324-331.
23. Hatin I, Fabret C, Namy O, Decatur WA, Rousset JP (2007) Fine-tuning of translation termination efficiency in Saccharomyces cerevisiae involves two factors in close proximity to the exit tunnel of the ribosome. Genetics 177: 1527-1537. (Pubitemid 350277050)
24. Sahoo T, del Gaudio D, German JR, Shinawi M, Peters SU, et al. (2008) Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat Genet 40: 719-721. (Pubitemid 351748873)
25. Heiss NS, Knight SW, Vulliamy TJ, Klauck SM, Wiemann S, et al. (1998) Xlinked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat Genet 19: 32-38. (Pubitemid 28242019)
26. Knight SW, Heiss NS, Vulliamy TJ, Greschner S, Stavrides G, et al. (1999) Xlinked dyskeratosis congenita is predominantly caused by missense mutations in the DKC1 gene. Am J Hum Genet 65: 50-58. (Pubitemid 30470448)
27. Dong XY, Guo P, Boyd J, Sun X, Li Q, et al. (2009) Implication of snoRNA U50 in human breast cancer. J Genet Genomics 36: 447-454.
28. Dong XY, Rodriguez C, Guo P, Sun X, Talbot JT, et al. (2008) SnoRNA U50 is a candidate tumor-suppressor gene at 6q14.3 with a mutation associated with clinically significant prostate cancer. Hum Mol Genet 17: 1031-1042.
29. Liao J, Yu L, Mei Y, Guarnera M, Shen J, et al. (2010) Small nucleolar RNA signatures as biomarkers for non-small-cell lung cancer. Mol Cancer 9: 198.
30. Mei YP, Liao JP, Shen J, Yu L, Liu BL, et al. (2012) Small nucleolar RNA 42 acts as an oncogene in lung tumorigenesis. Oncogene 31: 2794-2804.
31. Tanaka R, Satoh H, Moriyama M, Satoh K, Morishita Y, et al. (2000) Intronic U50 small-nucleolar-RNA (snoRNA) host gene of no protein-coding potential is mapped at the chromosome breakpoint t(3;6)(q27;q15) of human B-cell lymphoma. Genes Cells 5: 277-287. (Pubitemid 30253178)
32. Jack K, Bellodi C, Landry DM, Niederer RO, Meskauskas A, et al. (2011) rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol Cell 44: 660-666.
33. Gü ldener U, Heck S, Fielder T, Beinhauer J, Hegemann JH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24: 2519-2524. (Pubitemid 26237149)
34. Schiestl RH, Gietz RD (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet 16: 339-346. (Pubitemid 20034019)
35. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
36. McEntee CM, Hudson AP (1989) Preparation of RNA from unspheroplasted yeast cells (Saccharomyces cerevisiae). Anal Biochem 176: 303-306.
37. Sharma S, Watzinger P, Kötter P, Entian KD (2013) Identification of a novel methyltransferase, Bmt2, responsible for the N-1-methyl-adenosine base modification of 25S rRNA in Saccharomyces cerevisiae. Nucleic Acids Res 41: 5428-5443.
38. Kellner S, Seidu-Larry S, Burhenne J, Motorin Y, Helm M (2011) A multifunctional bioconjugate module for versatile photoaffinity labeling and click chemistry of RNA. Nucleic Acids Res 39: 7348-7360.