A single acetylation of 18 S rRNA is essential for biogenesis of the small ribosomal subunit in saccharomyces cerevisiae

Journal of Biological Chemistry

Volumn 289, Issue 38, 2014, Pages 26201-26212

  Ito, Satoshi ^a   Akamatsu, Yu ^a   Noma, Akiko ^a   Kimura, Satoshi ^a   Miyauchi, Kenjyo ^a   Ikeuchi, Yoshiho ^a,b   Suzuki, Takeo ^a   Suzuki, Tsutomu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b INSTITUTE OF INDUSTRIAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; BIOSYNTHESIS; YEAST;

ACETYL-COA; POST-TRANSCRIPTIONAL MODIFICATION; RIBOSOMAL SUBUNITS; RRNA PROCESSING;

RNA;

ACETYL COENZYME A; ACETYL COENZYME A SYNTHETASE 2; ACYLTRANSFERASE; ADENOSINE TRIPHOSPHATE; CYTIDINE DERIVATIVE; N4 ACETYLCYTIDINE; RECOMBINANT ENZYME; RECOMBINANT RIBOSOMAL RNA CYTIDINE ACETYLTRANSFERASE 1; RIBOSOMAL RNA CYTIDINE ACETYLTRANSFERASE 1; RNA 18S; RNA 23S; RNA ACETYLTRANSFERASE; SYNTHETASE; UNCLASSIFIED DRUG; FUNGAL RNA; RRA1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ACETYLATION; ARTICLE; BIOGENESIS; CATALYSIS; CELL LEVEL; CELL NUCLEUS; CONTROLLED STUDY; ENZYME INACTIVATION; ESSENTIAL GENE; KRE33 GENE; MASS SPECTROMETRY; NONHUMAN; PROTEIN DEPLETION; RNA PROCESSING; SACCHAROMYCES CEREVISIAE; SMALL RIBOSOMAL SUBUNIT; ENZYME SPECIFICITY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ACETYL COENZYME A; ACETYLATION; ACETYLTRANSFERASES; BASE SEQUENCE; CELL NUCLEUS; MOLECULAR SEQUENCE DATA; RIBOSOME SUBUNITS, SMALL; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, FUNGAL; RNA, RIBOSOMAL, 18S; RNA, RIBOSOMAL, 23S; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84907222762     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593996     Document Type: Article

References (54)

1. Warner, J. R. (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440
2. Venema, J., and Tollervey, D. (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33, 261-311
3. Henras, A. K., Soudet, J., Gérus, M., Lebaron, S., Caizergues-Ferrer, M., Mougin, A., and Henry, Y. (2008) The post-transcriptional steps of eu-karyotic ribosome biogenesis. Cell. Mol. Life Sci. 65, 2334-2359
4. Fromont-Racine, M., Senger, B., Saveanu, C., and Fasiolo, F. (2003) Ribo-some assembly in eukaryotes. Gene 313, 17-42
5. Woolford, J. L., Jr., and Baserga, S. J. (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195, 643-681
6. Mullineux, S. T., and Lafontaine, D. L. (2012) Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie 94, 1521-1532
7. Granneman, S., and Baserga, S. J. (2004) Ribosome biogenesis: of knobs and RNA processing. Exp. Cell Res. 296, 43-50
8. Reichow, S. L., Hamma, T., Ferré-D'Amaré, A. R., and Varani, G. (2007) The structure and functionof small nucleolar ribonucleoproteins. Nucleic Acids Res. 35, 1452-1464
9. Kos, M., and Tollervey, D. (2010) Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell 37, 809-820
10. Piekna-Przybylska, D., Decatur, W. A., and Fournier, M. J. (2008) The 3D rRNA modification maps database: with interactive tools for ribosome analysis. Nucleic Acids Res. 36, D178-D183
11. Eschrich, D., Buchhaupt, M., Kötter, P., and Entian, K. D. (2002) Nep1p (Emg1p), a novel protein conserved in eukaryotes and archaea, is involved in ribosome biogenesis. Curr. Genet. 40, 326-338
12. Wurm, J. P., Meyer, B., Bahr, U., Held, M., Frolow, O., Kötter, P., Engels, J. W., Heckel, A., Karas, M., Entian, K. D., and Wöhnert, J. (2010) The ribosome assembly factor Nep1 responsible for Bowen-Conradi syndrome is a pseudouridine-N1-specific methyltransferase. Nucleic Acids Res. 38, 2387-2398
13. Brand, R. C., Klootwijk, J., Planta, R. J., and Maden, B. E. (1978) Biosynthesis of a hypermodified nucleotide in Saccharomyces carlsbergen-sis 17 S and HeLa-cell 18 S ribosomal ribonucleic acid. Biochem. J. 169, 71-77
14. Armistead, J., Khatkar, S., Meyer, B., Mark, B. L., Patel, N., Coghlan, G., Lamont, R. E., Liu, S., Wiechert, J., Cattini, P. A., Koetter, P., Wroge-mann, K., Greenberg, C. R., Entian, K. D., Zelinski, T., and Triggs-Raine B (2009) Mutation of a gene essential for ribosome biogenesis, EMG1, causes Bowen-Conradi syndrome. Am. J. Hum. Genet. 84, 728-739
15. White, J., Li, Z., Sardana, R., Bujnicki, J. M., Marcotte, E. M., and Johnson, A. W. (2008) Bud23 methylates G1575 of 18 S rRNA and is required for efficient nuclear export of pre-40 S subunits. Mol. Cell. Biol. 28, 3151-3161
16. Lafontaine, D., Vandenhaute, J., and Tollervey, D. (1995) The 18 S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 9, 2470-2481
17. Thomas, G., Gordon, J., and Rogg, H. (1978) N4-acetylcytidine: a previously unidentified labile component of the small subunit of eukaryotic ribosomes. J. Biol. Chem. 253, 1101-1105
18. McCarroll, R., Olsen, G. J., Stahl, Y. D., Woese, C. R., and Sogin, M. L. (1983) Nucleotide sequence of the Dictyostelium discoideum small-sub-unit ribosomal ribonucleic acid inferred from the gene sequence: evolutionary Implication. Biochemistry 22, 5858-5868
19. Sanchez-Diaz, A., Kanemaki, M., Marchesi, V., and Labib, K. (2004) Rapid depletion of budding yeast proteins by fusion to a heat-inducible degron. Sci. STKE 2004, PL8
20. Takahashi, H., McCaffery, J. M., Irizarry, R. A., and Boeke, J. D. (2006) Nucleocytosolic acetyl-coenzyme a synthetase is required for histone acetylation and global transcription. Mol. Cell 23, 207-217
21. Chomczynski, P., and Sacchi, N. (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat. Protoc. 1, 581-585
22. Miyauchi, K., Ohara, T., and Suzuki, T. (2007) Automated parallel isolation of multiple species of non-coding RNAs by the reciprocal circulating chromatography method. Nucleic Acids Res. 35, e24
23. Miyauchi, K., Kimura, S., and Suzuki, T. (2013) A cyclic form of N6-threonylcarbamoyladenosine as a widely distributed tRNA hypermodifi-cation. Nat. Chem. Biol. 9, 105-111
24. Suzuki, T., Ikeuchi, Y., Noma, A., Suzuki, T., and Sakaguchi, Y. (2007) Mass spectrometric identification and characterization of RNA-modify-ing enzymes. Methods Enzymol. 425, 211-229
25. Inada, T., Winstall, E., Tarun, S. Z., Jr., Yates, J. R., 3rd, Schieltz, D., and Sachs, A.B. (2002) One-step affinity purificationofthe yeast ribosome and its associated proteins and mRNAs. RNA 8, 948-958
26. Sampson, J. R., and Uhlenbeck, O. C. (1988) Biochemical and physical characterizationof an unmodified yeast phenylalanine transfer RNA transcribed in vitro. Proc. Natl. Acad. Sci. U.S.A. 85, 1033-1037
27. Machnicka, M. A., Milanowska, K., Osman Oglou, O., Purta, E., Kurkowska, M., Olchowik, A., Januszewski, W., Kalinowski, S., Dunin-Horkawicz, S., Rother, K. M., Helm, M., Bujnicki, J. M., Grosjean, H. (2013) MODOMICS: a database of RNA modification pathways: 2013 update. Nucleic Acids Res. 41, D262-D267
28. Ikeuchi, Y., Kitahara, K., and Suzuki, T. (2008) The RNA acetyltransferase driven by ATP hydrolysis synthesizes N4-acetylcytidine of tRNA anti-codon. EMBO J. 27, 2194-2203
29. Pagé, N., Gérard-Vincent, M., Ménard, P., Beaulieu, M., Azuma, M., Dijkgraaf, G. J., Li, H., Marcoux, J., Nguyen, T., Dowse, T., Sdicu, A. M., and Bussey, H. (2003) A Saccharomyces cerevisiae genome-wide mutant screen for altered sensitivity to K1 killer toxin. Genetics 163, 875-894
30. Grandi, P., Rybin, V., Bassler, J., Petfalski, E., Strauss, D., Marzioch, M., Schäfer, T., Kuster, B., Tschochner, H., Tollervey, D., Gavin, A. C., and Hurt, E. (2002) 90 S pre-ribosomes include the 35 S pre-rRNA, the U3 snoRNP, and 40 S subunit processing factors but predominantly lack 60 S synthesis factors. Mol. Cell 10, 105-115
31. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weiss-man, J. S., and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691
32. Li, Z., Lee, I., Moradi, E., Hung, N. J., Johnson, A. W., and Marcotte, E. M. (2009) Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol. 7, e1000213
33. Strunk, B. S., and Karbstein, K. (2009) Powering through ribosome assembly. RNA 15, 2083-2104
34. Hughes, J. M., and Ares, M., Jr. (1991) Depletion of U3 small nucleolar RNA inhibits cleavage in the 5' external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18 S ribosomal RNA. EMBOJ. 10, 4231-4239
35. Pendrak, M. L., and Roberts, D. D. (2011) Ribosomal RNA processing in Candida albicans. RNA 17, 2235-2248
36. Chypre, M., Zaidi, N, and Smans, K. (2012) ATP-citrate lyase: a mini-review. Biochem. Biophys. Res. Commun. 422, 1-4
37. Pronk, J. T., Yde Steensma, H., and Van Dijken, J. P. (1996) Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 12, 1607-1633
38. Starai, V. J., and Escalante-Semerena, J. C. (2004) Acetyl-coenzyme A synthetase (AMP forming). Cell. Mol. Life Sci. 61, 2020-2030
39. Kratzer, S., and Schüller, H. J. (1995) Carbon source-dependent regulation of the acetyl-coenzyme A synthetase-encoding gene ACS1 from Saccharomyces cerevisiae. Gene 161, 75-79
40. Bruenger, E., Kowalak, J. A., Kuchino, Y., McCloskey, J. A., Mizushima, H, Stetter, K. O., and Crain, P. F. (1993) 5S rRNA modification in the hyper-thermophilic archaea Sulfolobus solfataricus and Pyrodictium occultum. FASEBJ. 7, 196-200
41. Gupta, R. (1984) Halobacterium volcanii tRNAs. Identification of 41 tRNAs covering all amino acids and the sequences of 33 class I tRNAs. J. Biol. Chem. 259, 9461-9471
42. Noon, K. R., Bruenger, E., and McCloskey, J. A. (1998) Posttranscriptional modifications in 16 S and 23 S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus. J. Bacteriol. 180, 2883-2888
43. Waters, K., Yang, A. Z., and Reinke, V. (2010) Genome-wide analysis of germ cell proliferation in C. elegans identifies VRK-1 as a key regulator of CEP-1/p53. Dev. Biol. 344, 1011-1025
44. Peter, A., Schottler, P., Werner, M., Beinert, N., Dowe, G., Burkert, P., Mourkioti, F., Dentzer, L., He, Y., Deak, P., Benos, P. V., Gatt, M. K., Murphy, L., Harris, D., Barrell, B., Ferraz, C, Vidal, S., Brun, C, Demaille, J., Cadieu, E., Dreano, S., Gloux, S., Lelaure, V., Mottier, S., Galibert, F., Borkova, D., Miñana, B., Kafatos, F. C, Bolshakov, S., Siden-Kiamos, I., Papagiannakis, G., Spanos, L., Louis, C, Madueno, E., de Pablos, B., Modolell, J., Bucheton, A., Callister, D., Campbell, L., Henderson, N. S., McMillan, P. J., Salles, C, Tait, E., Valenti, P., Saunders, R. D., Billaud, A., Pachter, L., Klapper, R., Janning, W., Glover, D. M., and Ashburner, M. (2002) Mapping and identification of essential gene functions on the X chromosome of Drosophila. EMBO Rep. 3, 34-38
45. Lv, J., Liu, H, Wang, Q., Tang, Z., Hou, L., and Zhang, B. (2003) Molecular cloning of a novel human gene encoding histone acetyltransferase-like protein involved in transcriptional activation of hTERT. Biochem. Biophys. Res. Commun. 311, 506-513
46. Chimnaronk, S., Suzuki, T., Manita, T., Ikeuchi, Y., Yao, M., Suzuki, T., and Tanaka, I. (2009) RNA helicase module in an acetyltransferase that modifies a specific tRNA anticodon. EMBOJ. 28, 1362-1373
47. Shen, Q., Zheng, X., McNutt, M. A., Guang, L., Sun, Y., Wang, J., Gong, Y., Hou, L., and Zhang, B. (2009) NAT10, a nucleolar protein, localizes to the midbody and regulates cytokinesis and acetylation of microtubules. Exp. Cell Res. 315, 1653-1667
48. Larrieu, D., Britton, S., Demir, M., Rodriguez, R., and Jackson, S. P. (2014) Chemical inhibition of NAT10 corrects defects of laminopathic cells. Science 344, 527-532
49. Tan, T. Z., Miow, Q. H, Huang, R. Y., Wong, M. K., Ye, J., Lau, J. A., Wu, M. C, Bin Abdul Hadi, L. H., Soong, R., Choolani, M., Davidson, B., Ne-sland, J. M., Wang, L. Z., Matsumura, N., Mandai, M., Konishi, I., Goh, B. C, Chang, J. T., Thiery, J. P., and Mori, S. (2013) Functional genomics identifies five distinct molecular subtypes with clinical relevance and pathways for growth control in epithelial ovarian cancer. EMBO Mol. Med. 5, 983-998
50. Perez-Fernandez, J., Roman, A., De Las Rivas, J., Bustelo, X. R., and Dosil, M. (2007) The 90 S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 27, 5414-5429
51. Holcik, M., and Sonenberg, N. (2005) Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6, 318-327
52. McCarthy, J. E. (1998) Posttranscriptional control of gene expression in yeast. Microbiol Mol. Biol. Rev. 62, 1492-1553
53. Cai, L., Sutter, B. M., Li, B., and Tu, B. P. (2011) Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 42, 426-437
54. McLuckey, S. A., Van Berkel, G. J., and Glish, G. L. (1992) Tandem mass-spectrometryof small, multiply charged oligonucleotides. J. Am. Soc. Mass Spectrom. 3, 60-70