Eukaryotic rRNA modification by yeast 5- methylcytosine-methyltransferases and human proliferation-associated antigen p120

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Bourgeois, Gabrielle ^a   Ney, Michel ^a   Gaspar, Imre ^b   Aigueperse, Christelle ^a   Schaefer, Matthias ^c   Kellner, Stefanie ^d   Helm, Mark ^d   Motorin, Yuri ^a  

^a Biopôle de l Université de Lorraine   (France)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE METHYLTRANSFERASE; CHIMERIC PROTEIN; METHYLTRANSFERASE; NOP2P PROTEIN; PROTEIN P120; RCM1P PROTEIN; RIBOSOME PROTEIN; RIBOSOME RNA; RNA 18S; RNA 25S; UNCLASSIFIED DRUG; 5 METHYLCYTOSINE; NOP2 PROTEIN, HUMAN; NOP2 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; PROTEIN BINDING; RNA, RIBOSOMAL, 25S; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSFER RNA METHYLTRANSFERASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MODIFICATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RNA SEQUENCE; YEAST; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

5-METHYLCYTOSINE; HUMANS; METHYLTRANSFERASES; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRNA METHYLTRANSFERASES;

EID: 84941313084     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133321     Document Type: Article

References (64)

1. Motorin Y, Helm M. RNA nucleotide methylation. Wiley Interdiscip Rev RNA 2011; 2(5):611-31. doi:10.1002/wrna.79 PMID: 21823225.
2. Salozhin SV, Prokhorchuk EB, Georgiev GP. Methylation of DNA-one of the major epigenetic markers. Biochemistry (Mosc) 2005; 70(5):525-32.
3. Smith JE, Cooperman BS, Mitchell P. Methylation sites in Escherichia coli ribosomal RNA: localization and identification of four new sites of methylation in 23S rRNA. Biochemistry 1992; 31(44):10825-34. PMID: 1384701.
4. Veldman GM, Klootwijk J, de Regt VC, Planta RJ, Branlant C, Krol A, et al. The primary and secondary structure of yeast 26S rRNA. Nucleic Acids Res 1981; 9(24):6935-52. PMID: 7335496.
5. Brand RC, Klootwijk J, Van Steenbergen TJ, De Kok AJ, Planta RJ. Secondary methylation of yeast ribosomal precursor RNA. Eur J Biochem 1977; 75(1):311-8. PMID: 405217.
6. Maden BE. Locations of methyl groups in 28 S rRNA of Xenopus laevis and man. Clustering in the conserved core of molecule. J Mol Biol 1988; 201(2):289-314. PMID: 3418702.
7. Sharma S, Yang J, Watzinger P, Kotter P, Entian KD. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res 2013; 41(19):9062-76. doi:10.1093/nar/gkt679 PMID: 23913415.
8. Gigova A, Duggimpudi S, Pollex T, Schaefer M, Kos M. A cluster of methylations in the domain IV of 25S rRNA is required for ribosome stability. RNA 2014; 20(10):1632-44. doi:10.1261/rna.043398.113 PMID: 25125595.
9. Motorin Y, Lyko F, Helm M. 5-methylcytosine in RNA: detection, enzymatic formation and biological functions. Nucleic Acids Res 2010; 38(5):1415-30. doi:10.1093/nar/gkp1117 PMID: 20007150.
10. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, et al. Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 2012; 40(11):5023-33. doi:10.1093/nar/gks144 PMID: 22344696.
11. Edelheit S, Schwartz S, Mumbach MR, Wurtzel O, Sorek R. Transcriptome-wide mapping of 5-methylcytidine RNA modifications in bacteria, archaea, and yeast reveals m5C within archaeal mRNAs. PLoS Genet 2013; 9(6):e1003602. doi:10.1371/journal.pgen.1003602 PMID: 23825970.
12. Brzezicha B, Schmidt M, Makalowska I, Jarmolowski A, Pienkowska J, Szweykowska-Kulinska Z. Identification of human tRNA:m5C methyltransferase catalysing intron-dependent m5C formation in the first position of the anticodon of the pre-tRNA Leu (CAA). Nucleic Acids Res 2006; 34(20):6034-43. PMID: 17071714.
13. Motorin Y, Grosjean H. Multisite-specific tRNA:m5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: identification of the gene and substrate specificity of the enzyme. RNA 1999; 5(8):1105-18. PMID: 10445884.
14. Blagosklonny MV, Iglesias A, Zhan Z, Fojo T. Like p53, the proliferation-associated protein p120 accumulates in human cancer cells following exposure to anticancer drugs. Biochem Biophys Res Commun 1998; 244(2):368-73. PMID: 9514935.
15. Trere D, Migaldi M, Montanaro L, Pession A, Derenzini M. p120 expression provides a reliable indication of the rapidity of cell duplication in cancer cells independently of tumour origin. J Pathol 2000; 192 (2):216-20. PMID: 11004698.
16. Uchiyama B, Saijo Y, Kumano N, Abe T, Fujimura S, Ohkuda K, et al. Expression of nucleolar protein p120 in human lung cancer: difference in histological types as a marker for proliferation. Clin Cancer Res 1997; 3(10):1873-7. PMID: 9815576.
17. Frye M, Watt FM. The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr Biol 2006; 16(10):971-81. PMID: 16713953.
18. Frye M, Dragoni I, Chin SF, Spiteri I, Kurowski A, Provenzano E, et al. Genomic gain of 5p15 leads to over-expression of Misu (NSUN2) in breast cancer. Cancer Lett 2010; 289(1):71-80. doi:10.1016/j.canlet.2009.08.004PMID: 19740597.
19. Chi L, Delgado-Olguin P. Expression of NOL1/NOP2/sun domain (Nsun) RNA methyltransferase family genes in early mouse embryogenesis. Gene Expr Patterns 2013; 13(8):319-27doi:10.1016/j.gep.2013.06.003 PMID: 23816522.
20. Khan MA, Rafiq MA, Noor A, Hussain S, Flores JV, Rupp V, et al. Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability. Am J Hum Genet 2012; 90(5):856-63. doi:10.1016/j.ajhg.2012.03.023 PMID: 22541562.
21. Harris T, Marquez B, Suarez S, Schimenti J. Sperm motility defects and infertility in male mice with a mutation in Nsun7, a member of the Sun domain-containing family of putative RNA methyltransferases. Biol Reprod 2007; 77(2):376-82. PMID: 17442852.
22. Sakita-Suto S, Kanda A, Suzuki F, Sato S, Takata T, Tatsuka M. Aurora-B regulates RNA methyltransferase NSUN2. Mol Biol Cell 2007; 18(3):1107-17. PMID: 17215513.
23. Auxilien S, Guerineau V, Szweykowska-Kulinska Z, Golinelli-Pimpaneau B. The human tRNA m(5)C methyltransferase Misu is multisite-specific. RNA Biol 2012; 9(11):1331-8. doi:10.4161/rna.22180 PMID: 22995836.
24. Metodiev MD, Spahr H, Loguercio Polosa P, Meharg C, Becker C, Altmueller J, et al. NSUN4 is a dual function mitochondrial protein required for both methylation of 12S rRNA and coordination of mitoribosomal assembly. PLoS Genet 2014; 10(2):e1004110. doi:10.1371/journal.pgen.1004110 PMID: 24516400.
25. Reid R, Greene PJ, Santi DV. Exposition of a family of RNA m5C methyltransferases from searching genomic and proteomic sequences. Nucleic Acids Res 1999; 27(15):3138-45. PMID: 10454610.
26. Freeman JW, Hazlewood JE, Auerbach P, Busch H. Optimal loading of scraped HeLa cells with monoclonal antibodies to the proliferation-associated Mr 120, 000 nucleolar antigen. Cancer Res 1988; 48 (18):5246-50. PMID: 3044583.
27. Freeman JW, Busch RK, Gyorkey F, Gyorkey P, Ross BE, Busch H. Identification and characterization of a human proliferation-associated nucleolar antigen with a molecular weight of 120, 000 expressed in early G1 phase. Cancer Res 1988; 48(5):1244-51. PMID: 3422591.
28. Jhiang SM, Yaneva M, Busch H. Expression of human proliferation-associated nucleolar antigen p120. Cell Growth Differ 1990; 1(7):319-24. PMID: 2278884.
29. Ueki T, Nakayama Y, Sugao Y, Kohno K, Matsuo K, Sugimoto Y, et al. Significance of the expression of proliferation-associated nucleolar antigen p120 in human colorectal tumors. Hum Pathol 1997; 28 (1):74-9. PMID: 9013835.
30. Gorczyca W, Bruno S, Melamed MR, Darzynkiewicz Z. Cell cycle-related expression of p120 nucleolar antigen in normal human lymphocytes and in cells of HL-60 and MOLT-4 leukemic lines: effects of methotrexate, camptothecin, and teniposide. Cancer Res 1992; 52(12):3491-4. PMID: 1596908.
31. Fonagy A, Swiderski C, Dunn M, Freeman JW. Antisense-mediated specific inhibition of P120 protein expression prevents G1- To S-phase transition. Cancer Res 1992; 52(19):5250-6. PMID: 1394129.
32. Perlaky L, Valdez BC, Busch RK, Larson RG, Jhiang SM, Zhang WW, et al. Increased growth of NIH/3T3 cells by transfection with human p120 complementary DNA and inhibition by a p120 antisense construct. Cancer Res 1992; 52(2):428-36. PMID: 1728415.
33. Valdez BC, Perlaky L, Saijo Y, Henning D, Zhu C, Busch RK, et al. A region of antisense RNA from human p120 cDNA with high homology to mouse p120 cDNA inhibits NIH 3T3 proliferation. Cancer Res 1992; 52(20):5681-6. PMID: 1394192.
34. Valdez BC, Perlaky L, Henning D, Saijo Y, Chan PK, Busch H. Identification of the nuclear and nucleolar localization signals of the protein p120. Interaction with translocation protein B23. J Biol Chem 1994; 269(38):23776-83. PMID: 8089149.
35. Gustafson WC, Taylor CW, Valdez BC, Henning D, Phippard A, Ren Y, et al. Nucleolar protein p120 contains an arginine-rich domain that binds to ribosomal RNA. Biochem J 1998; 331 ((Pt 2)):387-93. PMID: 9531475.
36. Lafontaine D, Vandenhaute J, Tollervey D. The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev 1995; 9(20):2470-81. PMID: 7590228.
37. Kressler D, Rojo M, Linder P, Cruz J. Spb1p is a putative methyltransferase required for 60S ribosomal subunit biogenesis in Saccharomyces cerevisiae. Nucleic Acids Res 1999; 27(23):4598-608. PMID: 10556316.
38. White J, Li Z, Sardana R, Bujnicki JM, Marcotte EM, Johnson AW. Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol Cell Biol 2008; 28(10):3151- 61. doi:10.1128/MCB.01674-07 PMID: 18332120.
39. Letoquart J, Huvelle E, Wacheul L, Bourgeois G, Zorbas C, Graille M, et al. Structural and functional studies of Bud23-Trm112 reveal 18S rRNA N7-G1575 methylation occurs on late 40S precursor ribosomes. Proc Natl Acad Sci USA 2014; 111(51):E5518-26. doi:10.1073/pnas.1413089111 PMID: 25489090.
40. Meyer B, Wurm JP, Kotter P, Leisegang MS, Schilling V, Buchhaupt M, et al. The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of Psi1191 in yeast 18S rRNA. Nucleic Acids Res 2011; 39(4):1526- 37. doi:10.1093/nar/gkq931 PMID: 20972225.
41. Thomas SR, Keller CA, Szyk A, Cannon JR, Laronde-Leblanc NA. Structural insight into the functional mechanism of Nep1/Emg1 N1-specific pseudouridine methyltransferase in ribosome biogenesis. Nucleic Acids Res 2011; 39(6):2445-57. doi:10.1093/nar/gkq1131 PMID: 21087996.
42. Wurm JP, Meyer B, Bahr U, Held M, Frolow O, Kotter P, et al. The ribosome assembly factor Nep1 responsible for Bowen-Conradi syndrome is a pseudouridine-N1-specific methyltransferase. Nucleic Acids Res 2010; 38(7):2387-98. doi:10.1093/nar/gkp1189 PMID: 20047967.
43. Hong B, Brockenbrough JS, Wu P, Aris JP. Nop2p is required for pre-rRNA processing and 60S ribosome subunit synthesis in yeast. Mol Cell Biol 1997; 17(1):378-88. PMID: 8972218.
44. de Beus E, Brockenbrough JS, Hong B, Aris JP. Yeast NOP2 encodes an essential nucleolar protein with homology to a human proliferation marker. J Cell Biol 1994; 127(6 Pt 2):1799-813. PMID: 7806561.
45. Ito H, Fukuda Y, Murata K, Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol 1983; 153(1):163-8. PMID: 6336730.
46. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, et al. Global analysis of protein localization in budding yeast. Nature 2003; 425(6959):686-91. PMID: 14562095.
47. Marchand V, Santerre M, Aigueperse C, Fouillen L, Saliou JM, VanDorsselaer A, et al. Identification of protein partners of the human immunodeficiency virus 1 tat/rev exon 3 leads to the discovery of a new HIV-1 splicing regulator, protein hnRNP K. RNA Biol 2011; 8(2):325-42. PMID: 21368586.
48. Studier FW. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 2005; 41(1):207-34. PMID: 15915565.
49. Schaefer M, Pollex T, Hanna K, Lyko F. RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res 2009; 37(2):e12. doi:10.1093/nar/gkn954 PMID: 19059995.
50. Kellner S, Ochel A, Thuring K, Spenkuch F, Neumann J, Sharma S, et al. Absolute and relative quantification of RNA modifications via biosynthetic isotopomers. Nucleic Acids Res 2014; 42(18):e142. doi:10.1093/nar/gku733 PMID: 25129236.
51. Koonin EV. Prediction of an rRNA methyltransferase domain in human tumor-specific nucleolar protein P120. Nucleic Acids Res 1994; 22(13):2476-8. PMID: 8041608.
52. Hong B, Wu K, Brockenbrough JS, Wu P, Aris JP. Temperature sensitive nop2 alleles defective in synthesis of 25S rRNA and large ribosomal subunits in Saccharomyces cerevisiae. Nucleic Acids Res 2001; 29(14):2927-37. PMID: 11452018.
53. King MY, Redman KL. RNA methyltransferases utilize two cysteine residues in the formation of 5- methylcytosine. Biochemistry 2002; 41(37):11218-25. PMID: 12220187.
54. Lafontaine DL, Preiss T, Tollervey D. Yeast 18S rRNA dimethylase Dim1p: A quality control mechanism in ribosome synthesis? Mol Cell Biol 1998; 18(4):2360-70. PMID: 9528805.
55. Schilling V, Peifer C, Buchhaupt M, Lamberth S, Lioutikov A, Rietschel B, et al. Genetic interactions of yeast NEP1 (EMG1), encoding an essential factor in ribosome biogenesis. Yeast 2012; 29(5):167-83. doi:10.1002/yea.2898 PMID: 22588997.
56. Leulliot N, Bohnsack MT, Graille M, Tollervey D, Van Tilbeurgh H. The yeast ribosome synthesis factor Emg1 is a novel member of the superfamily of alpha/beta knot fold methyltransferases. Nucleic Acids Res 2008; 36(2):629-39. PMID: 18063569.
57. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F. Ribosome assembly in eukaryotes. Gene 2003; 313:17-42. PMID: 12957375.
58. Harnpicharnchai P, Jakovljevic J, Horsey E, Miles T, Roman J, Rout M, et al. Composition and functional characterization of yeast 66S ribosome assembly intermediates. Mol Cell 2001; 8(3):505-15. PMID: 11583614.
59. Ferreira-Cerca S, Poll G, Kuhn H, Neueder A, Jakob S, Tschochner H, et al. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol Cell 2007; 28(3):446-57. PMID: 17996708.
60. Talkish J, Zhang J, Jakovljevic J, Horsey EW, Woolford JL Jr. Hierarchical recruitment into nascent ribosomes of assembly factors required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res 2012; 40(17):8646-61. PMID: 22735702.
61. Leulliot N, Chaillet M, Durand D, Ulryck N, Blondeau K, van Tilbeurgh H. Structure of the yeast tRNA m7G methylation complex. Structure 2008; 16(1):52-61. doi:10.1016/j.str.2007.10.025 PMID: 18184583.
62. Spahr H, Habermann B, Gustafsson CM, Larsson NG, Hallberg BM. Structure of the human MTERF4- NSUN4 protein complex that regulates mitochondrial ribosome biogenesis. Proc Natl Acad Sci USA 2012; 109(38):15253-8. PMID: 22949673.
63. Yakubovskaya E, Guja KE, Mejia E, Castano S, Hambardjieva E, Choi WS, et al. Structure of the essential MTERF4:NSUN4 protein complex reveals how an MTERF protein collaborates to facilitate rRNA modification. Structure 2012; 20(11):1940-7. doi:10.1016/j.str.2012.08.027 PMID: 23022348.
64. Hussain S, Sajini AA, Blanco S, Dietmann S, Lombard P, Sugimoto Y, et al. NSun2-mediated cytosine- 5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep 2013; 4(2):255-61. doi:10.1016/j.celrep.2013.06.029 PMID: 23871666.