Trm4 and Nsun2 RNA:m5C methyltransferases form metabolite-dependent, covalent adducts with previously methylated RNA

Biochemistry

Volumn 53, Issue 45, 2014, Pages 7132-7144

  Moon, Haley J ^a   Redman, Kent L ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; AMINO ACIDS; BIOMOLECULES; ENZYMES; MAMMALS; METABOLITES; NUCLEIC ACIDS; YEAST;

ACTIVE SITE RESIDUES; CATALYTIC MECHANISMS; COVALENT COMPLEX; METHYLTRANSFERASES; PH RANGE; RNA MOLECULES; S-ADENOSYLHOMOCYSTEINE;

RNA;

5 METHYLCYTOSINE; FUNGAL RNA; RNA METHYLTRANSFERASE; S ADENOSYLHOMOCYSTEINE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSFER RNA; TRM4P PROTEIN; UNCLASSIFIED DRUG; DNA ADDUCT; M(5)C RRNA METHYLTRANSFERASE; METHYLTRANSFERASE; NSUN2 PROTEIN, HUMAN; RNA;

ARTICLE; CONTROLLED STUDY; COVALENT BOND; MOUSE; NONHUMAN; PH; PROTEIN ASSEMBLY; PROTEIN FUNCTION; RNA METHYLATION; RNA PROCESSING; ANALYSIS; ANIMAL; DNA ADDUCT; HUMAN; METABOLISM; METHYLATION;

ANIMALS; DNA ADDUCTS; HUMANS; METHYLATION; METHYLTRANSFERASES; MICE; RNA;

EID: 84910663503     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500882b     Document Type: Article

References (60)

1. Motorin, Y., Lyko, F., and Helm, M. (2010) 5-Methylcytosine in RNA: Detection, enzymatic formation and biological functions Nucleic Acids Res. 38, 1415-1430
2. Tuorto, F., Liebers, R., Musch, T., Schaefer, M., Hofmann, S., Kellner, S., Frye, M., Helm, M., Stoecklin, G., and Lyko, F. (2012) RNA cytosine methylation by Dnmt2 and NSun2 promotes tRNA stability and protein synthesis Nat. Struct. Mol. Biol. 19, 900-905
3. Chernyakov, I., Whipple, J. M., Kotelawala, L., Grayhack, E. J., and Phizicky, E. M. (2008) Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5′-3′ exonucleases Rat1 and Xrn1 Genes Dev. 22, 1369-1380
4. Chan, C. T., Pang, Y. L., Deng, W., Babu, I. R., Dyavaiah, M., Begley, T. J., and Dedon, P. C. (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins Nat. Commun. 3, 937
5. Squires, J. E. and Preiss, T. (2010) Function and detection of 5-methylcytosine in eukaryotic RNA Epigenomics 2, 709-715
6. 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
7. Khoddami, V. and Cairns, B. R. (2013) Identification of direct targets and modified bases of RNA cytosine methyltransferases Nat. Biotechnol. 31, 458-464
8. Hussain, S., Sajini, A. A., Blanco, S., Dietmann, S., Lombard, P., Sugimoto, Y., Paramor, M., Gleeson, J. G., Odom, D. T., Ule, J., and Frye, M. (2013) NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs Cell Rep. 4, 255-261
9. Zhang, X., Liu, Z., Yi, J., Tang, H., Xing, J., Yu, M., Tong, T., Shang, Y., Gorospe, M., and Wang, W. (2012) The tRNA methyltransferase NSun2 stabilizes p16INK(4) mRNA by methylating the 3′-untranslated region of p16 Nat. Commun. 3, Article 712
10. Goll, M. G., Kirpekar, F., Maggert, K. A., Yoder, J. A., Hsieh, C. L., Zhang, X., Golic, K. G., Jacobsen, S. E., and Bestor, T. H. (2006) Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2 Science 311, 395-398
11. Purta, E., O'Connor, M., Bujnicki, J. M., and Douthwaite, S. (2008) YccW is the m5C methyltransferase specific for 23S rRNA nucleotide 1962 J. Mol. Biol. 383, 641-651
12. Motorin, Y. and Grosjean, H. (1999) Multisite-specific tRNA:m5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: Identification of the gene and substrate specificity of the enzyme RNA 5, 1105-1118
13. Brzezicha, B., Schmidt, M., Makalowska, I., Jarmolowski, A., Pienkowska, J., and Szweykowska-Kulinska, Z. (2006) 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. 34, 6034-6043
14. 5C methyltransferase Misu is multisite-specific RNA Biol. 9, 1331-1338
15. Frye, M. and Watt, F. M. (2006) The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors Curr. Biol. 16, 971-981
16. Hussain, S., Benavente, S. B., Nascimento, E., Dragoni, I., Kurowski, A., Gillich, A., Humphreys, P., and Frye, M. (2009) The nucleolar RNA methyltransferase Misu (NSun2) is required for mitotic spindle stability J. Cell Biol. 186, 27-40
17. Hussain, S., Tuorto, F., Menon, S., Blanco, S., Cox, C., Flores, J. V., Watt, S., Kudo, N. R., Lyko, F., and Frye, M. (2013) The mouse cytosine-5 RNA methyltransferase NSun2 is a component of the chromatoid body and required for testis differentiation Mol. Cell. Biol. 33, 1561-1570
18. Blanco, S., Kurowski, A., Nichols, J., Watt, F. M., Benitah, S. A., and Frye, M. (2011) The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate PLoS Genet. 7, e1002403
19. Abbasi-Moheb, L., Mertel, S., Gonsior, M., Nouri-Vahid, L., Kahrizi, K., Cirak, S., Wieczorek, D., Motazacker, M. M., Esmaeeli-Nieh, S., Cremer, K., Weissmann, R., Tzschach, A., Garshasbi, M., Abedini, S. S., Najmabadi, H., Ropers, H. H., Sigrist, S. J., and Kuss, A. W. (2012) Mutations in NSUN2 cause autosomal-recessive intellectual disability Am. J. Hum. Genet. 90, 847-855
20. Khan, M. A., Rafiq, M. A., Noor, A., Hussain, S., Flores, J. V., Rupp, V., Vincent, A. K., Malli, R., Ali, G., Khan, F. S., Ishak, G. E., Doherty, D., Weksberg, R., Ayub, M., Windpassinger, C., Ibrahim, S., Frye, M., Ansar, M., and Vincent, J. B. (2012) Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability Am. J. Hum. Genet. 90, 856-863
21. Martinez, F. J., Lee, J. H., Lee, J. E., Blanco, S., Nickerson, E., Gabriel, S., Frye, M., Al-Gazali, L., and Gleeson, J. G. (2012) Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome J. Med. Genet. 49, 380-385
22. Fahiminiya, S., Almuriekhi, M., Nawaz, Z., Staffa, A., Lepage, P., Ali, R., Hashim, L., Schwartzentruber, J., Abu, K. K., Zaineddin, S., Gamal, H., Majewski, J., and Ben-Omran, T. (2014) Whole exome sequencing unravels disease-causing genes in consanguineous families in Qatar Clin. Genet. 86, 134-141
23. Bujnicki, J. M., Feder, M., Ayres, C. L., and Redman, K. L. (2004) Sequence-structure-function studies of tRNA:m5C methyltransferase Trm4p and its relationship to DNA:m5C and RNA:m5U methyltransferases Nucleic Acids Res. 32, 2453-2463
24. Liu, Y. and Santi, D. V. (2000) m5C RNA and m5C DNA methyl transferases use different cysteine residues as catalysts Proc. Natl. Acad. Sci. U.S.A. 97, 8263-8265
25. Kealey, J. T. and Santi, D. V. (1991) Identification of the catalytic nucleophile of tRNA (m5U54)methyltransferase Biochemistry 30, 9724-9728
26. Kealey, J. T., Gu, X., and Santi, D. V. (1994) Enzymatic mechanism of tRNA (m5U54)methyltransferase Biochimie 76, 1133-1142
27. Walbott, H., Husson, C., Auxilien, S., and Golinelli-Pimpaneau, B. (2007) Cysteine of sequence motif VI is essential for nucleophilic catalysis by yeast tRNA m5C methyltransferase RNA 13, 967-973
28. King, M. Y. and Redman, K. L. (2002) RNA methyltransferases utilize two cysteine residues in the formation of 5-methylcytosine Biochemistry 41, 11218-11225
29. Foster, P. G., Nunes, C. R., Greene, P., Moustakas, D., and Stroud, R. M. (2003) The first structure of an RNA m5C methyltransferase, Fmu, provides insight into catalytic mechanism and specific binding of RNA substrate Structure 11, 1609-1620
30. Redman, K. L. (2006) Assembly of protein-RNA complexes using natural RNA and mutant forms of an RNA cytosine methyltransferase Biomacromolecules 7, 3321-3326
31. Hallberg, B. M., Ericsson, U. B., Johnson, K. A., Andersen, N. M., Douthwaite, S., Nordlund, P., Beuscher, A. E., and Erlandsen, H. (2006) The structure of the RNA m5C methyltransferase YebU from Escherichia coli reveals a C-terminal RNA-recruiting PUA domain J. Mol. Biol. 360, 774-787
32. Demirci, H., Larsen, L. H., Hansen, T., Rasmussen, A., Cadambi, A., Gregory, S. T., Kirpekar, F., and Jogl, G. (2010) Multi-site-specific 16S rRNA methyltransferase RsmF from Thermus thermophilus RNA 16, 1584-1596
33. Hikida, Y., Kuratani, M., Bessho, Y., Sekine, S. I., and Yokoyama, S. (2010) Structure of an archaeal homologue of the bacterial Fmu/RsmB/RrmB rRNA cytosine 5-methyltransferase Acta Crystallogr. D66, 1301-1307
34. Kuratani, M., Hirano, M., Goto-Ito, S., Itoh, Y., Hikida, Y., Nishimoto, M., Sekine, S., Bessho, Y., Ito, T., Grosjean, H., and Yokoyama, S. (2010) Crystal structure of Methanocaldococcus jannaschii Trm4 complexed with sinefungin J. Mol. Biol. 401, 323-333
35. Ishikawa, I., Sakai, N., Tamura, T., Yao, M., Watanabe, N., and Tanaka, I. (2004) Crystal structure of human p120 homologue protein PH1374 from Pyrococcus horikoshii Proteins 54, 814-816
36. Spahr, H., Habermann, B., Gustafsson, C. M., Larsson, N. G., and Hallberg, B. M. (2012) Structure of the human MTERF4-NSUN4 protein complex that regulates mitochondrial ribosome biogenesis Proc. Natl. Acad. Sci. U.S.A. 109, 15253-15258
37. Yakubovskaya, E., Guja, K. E., Mejia, E., Castano, S., Hambardjieva, E., Choi, W. S., and Garcia-Diaz, M. (2012) Structure of the essential MTERF4:NSUN4 protein complex reveals how an MTERF protein collaborates to facilitate rRNA modification Structure 20, 1940-1947
38. Sunita, S., Tkaczuk, K. L., Purta, E., Kasprzak, J. M., Douthwaite, S., Bujnicki, J. M., and Sivaraman, J. (2008) Crystal structure of the Escherichia coli 23S rRNA:m5C methyltransferase RlmI (YccW) reveals evolutionary links between RNA modification enzymes J. Mol. Biol. 383, 652-666
39. Lee, T. T., Agarwalla, S., and Stroud, R. M. (2005) A unique RNA fold in the RumA-RNA-cofactor ternary complex contributes to substrate selectivity and enzymatic function Cell 120, 599-611
40. Urbonavicius, J., Jager, G., and Bjork, G. R. (2007) Amino acid residues of the Escherichia coli tRNA(m5U54)methyltransferase (TrmA) critical for stability, covalent binding of tRNA and enzymatic activity Nucleic Acids Res. 35, 3297-3305
41. Conte, M. L. and Carroll, K. S. (2013) The chemistry of thiol oxidation and detection. In Oxidative Stress and Redox Regulation (Jakob, U. and Reichmann, D., Eds.) pp 1-42, Springer, Dordrecht, The Netherlands.
42. Strausberg, R. L., Feingold, E. A., Grouse, L. H., Derge, J. G., Klausner, R. D., Collins, F. S., Wagner, L., Shenmen, C. M., Schuler, G. D., Altschul, S. F., Zeeberg, B., Buetow, K. H., Schaefer, C. F., Bhat, N. K., Hopkins, R. F., Jordan, H., Moore, T., Max, S. I., Wang, J., Hsieh, F., Diatchenko, L., Marusina, K., Farmer, A. A., Rubin, G. M., Hong, L., Stapleton, M., Soares, M. B., Bonaldo, M. F., Casavant, T. L., Scheetz, T. E., Brownstein, M. J., Usdin, T. B., Toshiyuki, S., Carninci, P., Prange, C., Raha, S. S., Loquellano, N. A., Peters, G. J., Abramson, R. D., Mullahy, S. J., Bosak, S. A., McEwan, P. J., McKernan, K. J., Malek, J. A., Gunaratne, P. H., Richards, S., Worley, K. C., Hale, S., Garcia, A. M., Gay, L. J., Hulyk, S. W., Villalon, D. K., Muzny, D. M., Sodergren, E. J., Lu, X., Gibbs, R. A., Fahey, J., Helton, E., Ketteman, M., Madan, A., Rodrigues, S., Sanchez, A., Whiting, M., Madan, A., Young, A. C., Shevchenko, Y., Bouffard, G. G., Blakesley, R. W., Touchman, J. W., Green, E. D., Dickson, M. C., Rodriguez, A. C., Grimwood, J., Schmutz, J., Myers, R. M., Butterfield, Y. S., Krzywinski, M. I., Skalska, U., Smailus, D. E., Schnerch, A., Schein, J. E., Jones, S. J., and Marra, M. A. (2002) Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences Proc. Natl. Acad. Sci. U.S.A. 99, 16899-16903
43. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures Protein Expression Purif. 41, 207-234
44. Lee, J. E., Cornell, K. A., Riscoe, M. K., and Howell, P. L. (2001) Expression, purification, crystallization and preliminary X-ray analysis of Escherichia coli 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase Acta Crystallogr. D57, 150-152
45. Rio, D. C., Ares, M., Jr., Hannon, G. J., and Nilsen, T. W. (2011) Removing rRNA from deproteinized, phenol-extracted total RNA. In RNA a Laboratory Manual, pp 48-50, Cold Spring Harbor Laboratory Press, Plainview, NY.
46. Subach, O. M., Khoroshaev, A. V., Gerasimov, D. N., Baskunov, V. B., Shchyolkina, A. K., and Gromova, E. S. (2004) 2-Pyrimidinone as a probe for studying the EcoRII DNA methyltransferase-substrate interaction Eur. J. Biochem. 271, 2391-2399
47. Hurd, P. J., Whitmarsh, A. J., Baldwin, G. S., Kelly, S. M., Waltho, J. P., Price, N. C., Connolly, B. A., and Hornby, D. P. (1999) Mechanism-based inhibition of C5-cytosine DNA methyltransferases by 2-H pyrimidinone J. Mol. Biol. 286, 389-401
48. van Bemmel, D. M., Brank, A. S., Eritja, R., Marquez, V. E., and Christman, J. K. (2009) DNA (Cytosine-C5) methyltransferase inhibition by oligodeoxyribonucleotides containing 2-(1H)-pyrimidinone (zebularine aglycon) at the enzymatic target site Biochem. Pharmacol. 78, 633-641
49. Zhou, L., Cheng, X., Connolly, B. A., Dickman, M. J., Hurd, P. J., and Hornby, D. P. (2002) Zebularine: A novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases J. Mol. Biol. 321, 591-599
50. Ben-Kasus, T., Ben-Zvi, Z., Marquez, V. E., Kelley, J. A., and Agbaria, R. (2005) Metabolic activation of zebularine, a novel DNA methylation inhibitor, in human bladder carcinoma cells Biochem. Pharmacol. 70, 121-133
51. Hendricks, C. L., Ross, J. R., Pichersky, E., Noel, J. P., and Zhou, Z. S. (2004) An enzyme-coupled colorimetric assay for S-adenosylmethionine-dependent methyltransferases Anal. Biochem. 326, 100-105
52. Chervin, S. M., Kittendorf, J. D., and Garcia, G. A. (2007) Probing the intermediacy of covalent RNA enzyme complexes in RNA modification enzymes Methods Enzymol. 425, 121-137
53. Alian, A., Lee, T. T., Griner, S. L., Stroud, R. M., and Finer-Moore, J. (2008) Structure of a TrmA-RNA complex: A consensus RNA fold contributes to substrate selectivity and catalysis in m5U methyltransferases Proc. Natl. Acad. Sci. U.S.A. 105, 6876-6881
54. Wu, P., Brockenbrough, J. S., Paddy, M. R., and Aris, J. P. (1998) NCL1, a novel gene for a non-essential nuclear protein in Saccharomyces cerevisiae Gene 220, 109-117
55. Phizicky, E. M. and Hopper, A. K. (2010) tRNA biology charges to the front Genes Dev. 24, 1832-1860
56. Gu, X. and Santi, D. V. (1992) Covalent adducts between tRNA (m5U54)-methyltransferase and RNA substrates Biochemistry 31, 10295-10302
57. Dong, A., Yoder, J. A., Zhang, X., Zhou, L., Bestor, T. H., and Cheng, X. (2001) Structure of human DNMT2, an enigmatic DNA methyltransferase homolog that displays denaturant-resistant binding to DNA Nucleic Acids Res. 29, 439-448
58. Schaefer, M., Pollex, T., Hanna, K., Tuorto, F., Meusburger, M., Helm, M., and Lyko, F. (2010) RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage Genes Dev. 24, 1590-1595
59. Jurkowski, T. P., Meusburger, M., Phalke, S., Helm, M., Nellen, W., Reuter, G., and Jeltsch, A. (2008) Human DNMT2 methylates tRNA(Asp) molecules using a DNA methyltransferase-like catalytic mechanism RNA 14, 1663-1670
60. Ivanetich, K. M. and Santi, D. V. (1992) 5,6-Dihydropyrimidine adducts in the reactions and interactions of pyrimidines with proteins Prog. Nucleic Acid Res. Mol. Biol. 42, 127-156