Mechanistic insights into small RNA recognition and modification by the HEN1 methyltransferase

Biochemical Journal

Volumn 453, Issue 2, 2013, Pages 281-290

  Plotnikova, Alexandra ^a,b   Baranauske, Simona ^a   Osipenko, Aleksandr ^a   Klimašauskas, Saulius ^a   Vilkaitis, Giedrius ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

^b GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

Author keywords

2 O ribose methylation; Enzyme kinetics; Methyltransferase; miRNA; RNA modification; siRNA

Indexed keywords

HEN1 METHYLTRANSFERASE; ISOTOPE; METHYLTRANSFERASE; MICRORNA; NUCLEIC ACID BASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; ENZYME KINETICS; ENZYME MODIFICATION; ENZYME SUBSTRATE COMPLEX; METHYLATION; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; STEADY STATE;

ARABIDOPSIS; CATALYSIS; KINETICS; METHYLTRANSFERASES; RNA; SUBSTRATE SPECIFICITY;

ARABIDOPSIS THALIANA;

EID: 84879557109     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121699     Document Type: Article

References (31)

1. Ghildiyal, M. and Zamore, P. D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10, 94-108
2. Kim, Y.-K., Heo, I. and Kim, V. N. (2010) Modifications of small RNAs and their associated proteins. Cell 143, 703-709
3. Ji, L. and Chen, X. (2012) Regulation of small RNA stability: methylation and beyond. Cell Res. 22, 624-636
4. Horwich, M. D., Li, C., Matranga, C., Vagin, V., Farley, G., Wang, P. and Zamore, P. D. (2007) The Drosophila RNA methyltransferase, DmHen1, modifies germline piRNAs and single-stranded siRNAs in RISC. Curr. Biol. 17, 1265-1272 (Pubitemid 47043434)
5. Kirino, Y. and Mourelatos, Z. (2007) The mouse homolog of HEN1 is a potential methylase for Piwi-interacting RNAs. RNA 13, 1397-1401 (Pubitemid 47347410)
6. Saito, K., Sakaguchi, Y., Suzuki, T., Suzuki, T., Siomi, H. and Siomi, M. C. (2007) Pimet, the Drosophila homolog of HEN1, mediates 2′-O- methylation of Piwi-interacting RNAs at their 3′ ends. Genes Dev. 21, 1603-1608 (Pubitemid 47026364)
7. Huang, R. H. (2012) Unique 2′-O-methylation by Hen1 in eukaryotic RNA interference and bacterial RNA repair. Biochemistry 51, 4087-4095
8. Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R. W., Steward, R. and Chen, X. (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932-935 (Pubitemid 40229231)
9. Yang, Z., Ebright, Y. W., Yu, B. and Chen, X. (2006) HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res. 34, 667-675 (Pubitemid 43240253)
10. Abe, M., Yoshikawa, T., Nosaka, M., Sakakibara, H., Sato, Y., Nagato, Y. and Itoh, J. (2010) WAVY LEAF1, an ortholog of Arabidopsis HEN1, regulates shoot development by maintaining MicroRNA and trans-acting small interfering RNA accumulation in rice. Plant Physiol. 154, 1335-1346
11. Yu, B., Bi, L., Zhai, J., Agarwal, M., Li, S., Wu, Q., Ding, S.-W., Meyers, B. C., Vaucheret, H. and Chen, X. (2010) siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Res. 38, 5844-5850
12. Vilkaitis, G., Plotnikova, A. and Klimasauskas, S. (2010) Kinetic and functional analysis of the small RNA methyltransferase HEN1: the catalytic domain is essential for preferential modification of duplex RNA. RNA 16, 1935-1942
13. Park, W., Li, J., Song, R., Messing, J. and Chen, X. (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana . Curr. Biol. 12, 1484-1495 (Pubitemid 35036646)
14. Huang, Y., Ji, L., Huang, Q., Vassylyev, D. G., Chen, X. and Ma, J.-B. (2009) Structural insights into mechanisms of the small RNA methyltransferase HEN1. Nature 461, 823-827
15. Tkaczuk, K. L., Obarska, A. and Bujnicki, J. M. (2006) Molecular phylogenetics and comparative modeling of HEN1, a methyltransferase involved in plant microRNA biogenesis. BMC Evol. Biol. 6, 6
16. Yang, Z., Vilkaitis, G., Yu, B., Klimasauskas, S. and Chen, X. (2007) Approaches for studying microRNA and small interfering RNA methylation in vitro and in vivo. Methods Enzymol. 427, 139-154
17. Chen, X. (2010) Small RNAs: secrets and surprises of the genome. Plant J. 61, 941-958
18. Katiyar-Agarwal, S. and Jin, H. (2010) Role of small RNAs in host-microbe interactions. Annu. Rev. Phytopathol. 48, 225-246
19. Meng, Y., Shao, C., Wang, H. and Chen, M. (2011) The regulatory activities of plant microRNAs: a more dynamic perspective. Plant Physiol. 157, 1583-1595
20. Chen, H.-M., Chen, L.-T., Patel, K., Li, Y.-H., Baulcombe, D. C. and Wu, S.-H. (2010) 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. U.S.A. 107, 15269-15274
21. Manavella, P. A., Koenig, D. and Weigel, D. (2012) Plant secondary siRNA production determined by microRNA-duplex structure. Proc. Natl. Acad. Sci. U.S.A. 109, 2461-2466
22. Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., Sullivan, C. M., Gilbert, S. D., Montgomery, T. A. and Carrington, J. C. (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17, 997-1003
23. Rose, I. A. (1980) The isotope trapping method: desorption rates of productive E·S complexes. Methods Enzymol. 64, 47-59
24. Vilkaitis, G., Merkiene, E., Serva, S., Weinhold, E. and Klimasauskas, S. (2001) The mechanism of DNA cytosine-5 methylation. Kinetic and mutational dissection of HhaI methyltransferase. J. Biol. Chem. 276, 20924-20934
25. Chan, C. M., Zhou, C., Brunzelle, J. S. and Huang, R. H. (2009) Structural and biochemical insights into 2′-O-methylation at the 3′-terminal nucleotide of RNA by Hen1. Proc. Natl. Acad. Sci. U.S.A. 106, 17699-17704
26. Kurth, H. M. and Mochizuki, K. (2009) 2′-O-methylation stabilizes Piwi-associated small RNAs and ensures DNA elimination in Tetrahymena. RNA 15, 675-685
27. Jain, R. and Shuman, S. (2010) Bacterial Hen1 is a 3′ terminal RNA ribose 2′-O-methyltransferase component of a bacterial RNA repair cassette. RNA 16, 316-323
28. Urig, S., Gowher, H., Hermann, A., Beck, C., Fatemi, M., Humeny, A. and Jeltsch, A. (2002) The Escherichia coli dam DNA methyltransferase modifies DNA in a highly processive reaction. J. Mol. Biol. 319, 1085-1096 (Pubitemid 34729420)
29. Zinoviev, V. V., Evdokimov, A. A., Malygin, E. G., Schlagman, S. L. and Hattman, S. (2003) Bacteriophage T4 Dam DNA-(N6-adenine)-methyltransferase. Processivity and orientation to the methylation target. J. Biol. Chem. 278, 7829-7833 (Pubitemid 36800516)
30. Vilkaitis, G., Suetake, I., Klimasauskas, S. and Tajima, S. (2005) Processive methylation of hemimethylated CpG sites by mouse Dnmt1 DNA methyltransferase. J. Biol. Chem. 280, 64-72 (Pubitemid 40164965)
31. Holz-Schietinger, C. and Reich, N. O. (2010) The inherent processivity of the human de novo methyltransferase 3A (DNMT3A) is enhanced by DNMT3L. J. Biol. Chem. 285, 29091-29100