Structure of precursor microRNA’s terminal loop regulates human Dicer’s dicing activity by switching DExH/D domain
Received date: 18 Oct 2014
Accepted date: 13 Nov 2014
Published date: 01 Apr 2015
Copyright
Almost all pre-miRNAs in eukaryotic cytoplasm are recognized and processed into double-stranded microRNAs by the endonuclease Dicer protein comprising of multiple domains. As a key player in the small RNA induced gene silencing pathway, the major domains of Dicer are conserved among different species with the exception of the N-terminal components. Human Dicer’s N-terminal domain has been shown to play an autoinhibitory function of the protein’s dicing activity. Such an auto-inhibition can be released when the human Dicer protein dimerizes with its partner protein, such as TRBP, PACT through the N-terminal DExH/D (ATPase-helicase) domain. The typical feature of a pre-miRNA contains a terminal loop and a stem duplex, which bind to human Dicer’s DExH/D (ATPase-helicase) domain and PAZ domain respectively during the dicing reaction. Here, we show that pre-miRNA’s terminal loop can regulate human Dicer’s enzymatic activity by interacting with the DExH/D (ATPase-helicase) domain. We found that various editing products of pre-miR-151 by the ADAR1P110 protein, an A-to-I editing enzyme that modifies pre-miRNAs sequence, have different terminal loop structures and different activity regulatory effects on human Dicer. Single particle electron microscopy reconstruction revealed that pre-miRNAs with different terminal loop structures induce human Dicer’s DExH/D (ATPase-helicase) domain into different conformational states, in correlation with their activity regulatory effects.
Zhongmin Liu , Jia Wang , Gang Li , Hong-Wei Wang . Structure of precursor microRNA’s terminal loop regulates human Dicer’s dicing activity by switching DExH/D domain[J]. Protein & Cell, 2015 , 6(3) : 185 -193 . DOI: 10.1007/s13238-014-0124-2
| 1 |
Ando Y, Maida Y, Morinaga A, Burroughs AM, Kimura R, Chiba J, Suzuki H, Masutomi K, Hayashizaki Y (2011) Two-step cleavage of hairpin RNA with 5’ overhangs by human DICER. BMC Mol Biol12: 6
|
| 2 |
Blow MJ, Grocock RJ, van Dongen S, Enright AJ, Dicks E, Futreal PA, Wooster R, Stratton MR (2006) RNA editing of human microRNAs. Genome Biol7: R27
|
| 3 |
Brennicke A, Marchfelder A, Binder S (1999) RNA editing. FEMS Microbiol Rev23: 297-316
|
| 4 |
Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell136: 642-655
|
| 5 |
Castilla-Llorente V, Nicastro G, Ramos A (2013) Terminal loopmediated regulation of miRNA biogenesis: selectivity and mechanisms. Biochem Soc Trans41: 861-865
|
| 6 |
Chendrimada TP, Gregory RI, Kumaraswamy E, Norman J, Cooch N, Nishikura K, Shiekhattar R (2005) TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing. Nature436: 740-744
|
| 7 |
Das AK, Carmichael GG (2007) ADAR editing wobbles the microRNA world. ACS Chem Biol2: 217-220
|
| 8 |
Grifflths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res36: D154-D158
|
| 9 |
Gu S, Jin L, Zhang Y, Huang Y, Zhang F, Valdmanis PN, Kay MA (2012) The loop position of shRNAs and pre-miRNAs is critical for the accuracy of dicer processing in vivo. Cell151: 900-911
|
| 10 |
He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet5: 522-531
|
| 11 |
Heo I, Joo C, Cho J, Ha M, Han J, Kim VN (2008) Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol Cell32: 276-284
|
| 12 |
Heo I, Ha M, Lim J, Yoon MJ, Park JE, Kwon SC, Chang H, Kim VN (2012) Mono-uridylation of pre-microRNA as a key step in the biogenesis of group II let-7 microRNAs. Cell151: 521-532
|
| 13 |
Kawahara Y, Zinshteyn B, Chendrimada TP, Shiekhattar R, Nishikura K (2007a) RNA editing of the microRNA-151 precursor blocks cleavage by the Dicer-TRBP complex. EMBO Rep8: 763-769
|
| 14 |
Kawahara Y, Zinshteyn B, Sethupathy P, Iizasa H, Hatzigeorgiou AG, Nishikura K (2007b) Redirection of silencing targets by adenosine-to-inosine editing of miRNAs. Science315: 1137-1140
|
| 15 |
Lau P-W, Guiley KZ, De N, Potter CS, Carragher B, MacRae IJ (2012) The molecular architecture of human Dicer. Nat Struct Mol Biol19: 436-440
|
| 16 |
Lee Y, Hur I, Park S-Y, Kim Y-K, Suh MR, Kim AVN (2006) The role of PACT in the RNA silencing pathway. EMBO J25: 522-532
|
| 17 |
Ma E, MacRae IJ, Kirsch JF, Doudna JA (2008) Autoinhibition of human dicer by its internal helicase domain. J Mol Biol380: 237-243
|
| 18 |
MacRae IJ, Ma E, Zhou M, Robinson CV, Doudna JA (2008) In vitro reconstitution of the human RISC-loading complex. Proc Natl Acad Sci USA105(2): 512-517
|
| 19 |
Nishikura K (2010) Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem79: 321-349
|
| 20 |
Ota H, Sakurai M, Gupta R, Valente L, Wulff BE, Ariyoshi K, Iizasa H, Davuluri RV, Nishikura K (2013) ADAR1 forms a complex with Dicer to promote microRNA processing and RNA-induced gene silencing. Cell153: 575-589
|
| 21 |
Park JE, Heo I, Tian Y, Simanshu DK, Chang H, Jee D, Patel DJ, Kim VN (2011) Dicer recognizes the 5′ end of RNA for efficient and accurate processing. Nature475: 201-205
|
| 22 |
Scheres SHW (2012) RELION: implementationofaBayesianapproach to cryo-EM structure determination. J Struct Biol180: 519-530
|
| 23 |
Schraml E, Grillari J (2012) From cellular senescence to age associated diseases: the miRNA connection. Longev Heal1: 1-15
|
| 24 |
Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, Leith A, Frank J (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc3: 1941-1974
|
| 25 |
Su AAH, Randau L (2011) A-to-I and C-to-U editing within transfer RNAs. Biochemistry76: 932-937
|
| 26 |
Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ (2007) EMAN2: an extensible image processing suite for electron microscopy. J Struct Biol157: 38-46
|
| 27 |
Taylor DW, Ma E, Shigematsu H, Cianfrocco MA, Noland CL, Nagayama K, Nogales E, Doudna JA, Wang H-W (2013) Substrate-speciflc structural rearrangements of human Dicer. Nat Struct Mol Biol: 662-670
|
| 28 |
Tsutsumi A, Kawamata T, Izumi N, Seitz H, Tomari Y (2011) Recognition of the pre-miRNA structure by Drosophila Dicer-1. Nat Struct Mol Biol18: 1153-1158
|
| 29 |
van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol116: 17-24
|
| 30 |
Wang HW, Noland C, Siridechadilok B, Taylor DW, Ma E, Felderer K, Doudna JA, Nogales E (2009) Structural insights into RNA processing by the human RISC-loading complex. Nat Struct Mol Biol16: 1148-1153
|
| 31 |
Xie M, Li M, Vilborg A, Lee N, Shu MD, Yartseva V, Sestan N, Steitz JA (2013) Mammalian 5′-capped microRNA precursors that generate a single microRNA. Cell155: 1568-1580
|
| 32 |
Yang W, Chendrimada TP, Wang Q, Higuchi M, Seeburg PH, Shiekhattar R, Nishikura K (2006) Modulation of microRNA processing and expression through RNA editing by ADAR deaminases. Nat Struct Mol Biol13: 13-21
|
| 33 |
Zhang X, Zeng Y (2010) The terminal loop region controls microRNA processing by Drosha and Dicer. Nucleic Acids Res38: 7689-7697
|
| 34 |
Zhang H, Kolb FA, Vincent Brondani EBA, Filipowicz W (2002) Human Dicer preferentially cleaves dsRNAs at their termini without ATP. EMBO J21: 5875-5885
|
| 35 |
Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W (2004) Single processing center models for human Dicer and bacterial RNase III. Cell118: 57-68
|
| 36 |
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res31: 3406-3415
|
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|
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