Evolutionarily conserved roles of the dicer helicase domain in regulating RNA interference processing

Journal of Biological Chemistry

Volumn 289, Issue 41, 2014, Pages 28352-28362

  Kidwell, Mary Anne ^a   Chan, Jessica M ^a   Doudna, Jennifer A ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; ENZYMES; FUNGI;

CLEAVAGE ACTIVITIES; DOUBLE-STRANDED RNA; EVOLUTIONARY ORIGIN; HYDROLYTIC ACTIVITIES; REGULATORY FUNCTIONS; SCHIZOSACCHAROMYCES POMBE; SPOROTRICHUM THERMOPHILE; THERMOPHILIC FUNGUS;

RNA;

ADENOSINE TRIPHOSPHATE; DICER; DOUBLE STRANDED RNA; HELICASE; MICRORNA; RNA PRECURSOR; DNA HELICASE; FUNGAL PROTEIN; ISOENZYME; RECOMBINANT PROTEIN; RIBONUCLEASE III;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DICER GENE; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME SPECIFICITY; GENETIC CONSERVATION; GENETIC REGULATION; HYDROLYSIS; NONHUMAN; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA ANALYSIS; RNA CLEAVAGE; RNA INTERFERENCE; RNA PROCESSING; SCHIZOSACCHAROMYCES POMBE; SPOROTHRIX; SPOROTRICHUM THERMOPHILE; AMINO ACID SEQUENCE; ANIMAL; BACULOVIRIDAE; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SF9 CELL LINE; SIGNAL TRANSDUCTION; SPODOPTERA;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; BACULOVIRIDAE; BIOLOGICAL EVOLUTION; CONSERVED SEQUENCE; DNA HELICASES; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; HYDROLYSIS; ISOENZYMES; MICRORNAS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RIBONUCLEASE III; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; SF9 CELLS; SIGNAL TRANSDUCTION; SPODOPTERA; SPOROTHRIX; SUBSTRATE SPECIFICITY;

EID: 84907842170     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.589051     Document Type: Article

References (35)

1. Wilson, R. C., and Doudna, J. A. (2013) Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 42, 217-239
2. Ambros, V., Bartel, B., Bartel, D. P., Burge, C. B., Carrington, J. C., Chen, X., Dreyfuss, G., Eddy, S. R., Griffiths-Jones, S., Marshall, M., Matzke, M., Ruvkun, G., and Tuschl, T. (2003) A uniform system for microRNA annotation. RNA 9, 277-279
3. Bazzini, A. A., Lee, M. T., and Giraldez, A. J. (2012) Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336, 233-237
4. Djuranovic, S., Nahvi, A., and Green, R. (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336, 237-240
5. Cerutti, H., and Casas-Mollano, J. A. (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50, 81-99
6. Moran, Y., Praher, D., Fredman, D., and Technau, U. (2013) The evolution of microRNA pathway protein components in cnidaria. Mol. Biol. Evol. 30, 2541-2552
7. Zhang, H., Kolb, F. A., Jaskiewicz, L., Westhof, E., and Filipowicz, W. (2004) Single processing center models for human dicer and bacterial RNase III. Cell 118, 57-68
8. Macrae, I. J., Zhou, K., Li, F., Repic, A., Brooks, A. N., Cande, W. Z., Adams, P. D., and Doudna, J. A. (2006) Structural basis for double-stranded RNA processing by Dicer. Science 311, 195-198
9. Ma, E., MacRae, I. J., Kirsch, J. F., and Doudna, J. A. (2008) Autoinhibition of human Dicer by its internal helicase domain. J. Mol. Biol. 380, 237-243
10. Chakravarthy, S., Sternberg, S. H., Kellenberger, C. A., and Doudna, J. A. (2010) Substrate-specific kinetics of dicer-catalyzed RNA processing. J. Mol. Biol. 404, 392-402
11. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J., and Carthew, R. W. (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81
12. Tsutsumi, A., Kawamata, T., Izumi, N., Seitz, H., and Tomari, Y. (2011) Recognition of the pre-miRNA structure by Drosophila Dicer-1. Nat. Struct. Mol. Biol. 18, 1153-1158
13. Cenik, E. S., Fukunaga, R., Lu, G., Dutcher, R., Wang, Y., Tanaka Hall, T. M., and Zamore, P. D. (2011) Phosphate and R2D2 restrict the substrate specificity of Dicer-2, an ATP-driven ribonuclease. Mol. Cell 42, 172-184
14. Welker, N. C., Pavelec, D. M., Nix, D. A., Duchaine, T. F., Kennedy, S., and Bass, B. L. (2010) Dicer's helicase domain is required for accumulation of some, but not all, C. elegans endogenous siRNAs. RNA 16, 893-903
15. Lau, P. W., Guiley, K. Z., De, N., Potter, C. S., Carragher, B., and MacRae, I. J. (2012) The molecular architecture of human Dicer. Nat. Struct. Mol. Biol. 19, 436-440
16. Ferré-D'Amaré, A. R., and Doudna, J. A. (1996) Use of cis- and transribozymes to remove 5'' and 3'' heterogeneities from milligrams of in vitro transcribed RNA. Nucleic Acids Res. 24, 977-978
17. Lindner, K., Gregán, J., Montgomery, S., and Kearsey, S. E. (2002) Essential role of MCM proteins in premeiotic DNA replication. Mol. Biol. Cell 13, 435-444
18. Beeson, W. T., 4th, Iavarone, A. T., Hausmann, C. D., Cate, J. H., and Marletta, M. A. (2011) Extracellular aldonolactonase from Myceliophthora thermophila. Appl. Environ. Microbiol. 77, 650-656
19. Sasaki, T., and Shimizu, N. (2007) Evolutionary conservation of a unique amino acid sequence in human DICER protein essential for binding to Argonaute family proteins. Gene 396, 312-320
20. Lee, H. C., Li, L., Gu, W., Xue, Z., Crosthwaite, S. K., Pertsemlidis, A., Lewis, Z. A., Freitag, M., Selker, E. U., Mello, C. C., and Liu, Y. (2010) Diverse pathways generate MicroRNA-like RNAs and dicer-independent small interfering RNAs in fungi. Mol. Cell 38, 803-814
21. De, N., Young, L., Lau, P. W., Meisner, N. C., Morrissey, D. V., and Mac-Rae, I. J. (2013) Highly complementary target RNAs promote release of guide RNAs from human Argonaute2. Mol. Cell 50, 344-355
22. Ma, E., Zhou, K., Kidwell, M. A., and Doudna, J. A. (2012) Coordinated activities of human dicer domains in regulatory RNA processing. J. Mol. Biol. 422, 466-476
23. Lee, H. Y., and Doudna, J. A. (2012) TRBP alters human precursor microRNA processing in vitro. RNA 18, 2012-2019
24. Gee, P., Chua, P. K., Gevorkyan, J., Klumpp, K., Najera, I., Swinney, D. C., and Deval, J. (2008) Essential role of the N-terminal domain in the regulation of RIG-I ATPase activity. J. Biol. Chem. 283, 9488-9496
25. Provost, P., Silverstein, R. A., Dishart, D., Walfridsson, J., Djupedal, I., Kniola, B., Wright, A., Samuelsson, B., Radmark, O., and Ekwall, K. (2002) Dicer is required for chromosome segregation and gene silencing in fission yeast cells. Proc. Natl. Acad. Sci. U.S.A. 99, 16648-16653
26. Catalanotto, C., Pallotta, M., ReFalo, P., Sachs, M. S., Vayssie, L., Macino, G., and Cogoni, C. (2004) Redundancy of the two dicer genes in transgeneinduced posttranscriptional gene silencing in Neurospora crassa. Mol. Cell. Biol. 24, 2536-2545
27. Kadotani, N., Nakayashiki, H., Tosa, Y., and Mayama, S. (2004) One of the two Dicer-like proteins in the filamentous fungi Magnaporthe oryzae genome is responsible for hairpin RNA-triggered RNA silencing and related small interfering RNA accumulation. J. Biol. Chem. 279, 44467-44474
28. Taylor, D. W., Ma, E., Shigematsu, H., Cianfrocco, M. A., Noland, C. L., Nagayama, K., Nogales, E., Doudna, J. A., and Wang, H. W. (2013) Substrate- specific structural rearrangements of human Dicer. Nat. Struct. Mol. Biol. 20, 662-670
29. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J. A., and Imler, J. (2006) Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat. Immunol. 7, 590-597
30. de Jong, D., Eitel, M., Jakob, W., Osigus, H. J., Hadrys, H., Desalle, R., and Schierwater, B. (2009) Multiple dicer genes in the early-diverging metazoa. Mol. Biol. Evol. 26, 1333-1340
31. Mukherjee, K., Campos, H., and Kolaczkowski, B. (2013) Evolution of animal and plant dicers: early parallel duplications and recurrent adaptation of antiviral RNA binding in plants. Mol. Biol. Evol. 30, 627-641
32. Kowalinski, E., Lunardi, T., McCarthy, A. A., Louber, J., Brunel, J., Grigorov, B., Gerlier, D., and Cusack, S. (2011) Structural basis for the activation of innate immune pattern-recognition receptor RIG-I by viral RNA. Cell 147, 423-435
33. Luo, D., Ding, S. C., Vela, A., Kohlway, A., Lindenbach, B. D., and Pyle, A. M. (2011) Structural insights into RNA recognition by RIG-I. Cell 147, 409-422
34. Jiang, F., Ramanathan, A., Miller, M. T., Tang, G. Q., Gale, M., Jr., Patel, S. S., and Marcotrigiano, J. (2011) Structural basis of RNA recognition and activation by innate immune receptor RIG-I. Nature 479, 423-427
35. Civril, F., Bennett, M., Moldt, M., Deimling, T., Witte, G., Schiesser, S., Carell, T., and Hopfner, K. (2011) The RIG-I ATPase domain structure reveals insights into ATP-dependent antiviral signalling. EMBO Rep. 12, 1127-1134