The MID-PIWI module of Piwi proteins specifies nucleotide- and strand-biases of piRNAs

RNA

Volumn 20, Issue 6, 2014, Pages 773-781

  Cora, Elisa ^a,b   Pandey, Radha R ^a,b   Xiol, Jordi ^a,b,d   Taylor, Josh ^a,b   Sachidanandam, Ravi ^c   McCarthy, Andrew A ^a,b   Pillai, Ramesh S ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b UNIV GRENOBLE ALPES   (France)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

MID; PiRNA; Piwi; Strand bias; U1 bias

Indexed keywords

ADENOSINE PHOSPHATE; ALANINE TRANSFER RNA; ARGONAUTE PROTEIN; ASPARAGINE TRANSFER RNA; GLUTAMIC ACID TRANSFER RNA; GLUTAMINE TRANSFER RNA; PIWI INTERACTING RNA; PIWI PROTEIN; PROLINE TRANSFER RNA; TYROSINE TRANSFER RNA; URIDINE; URIDINE PHOSPHATE;

5' UNTRANSLATED REGION; ARTICLE; BOMBYX MORI; CELL GRANULE; CONTROLLED STUDY; CRYSTALLIZATION; DROSOPHILA; GEL PERMEATION CHROMATOGRAPHY; HYDROGEN BOND; IN VITRO STUDY; NEUROSPORA CRASSA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA BINDING; RNA SEQUENCE; STEREOSPECIFICITY; X RAY FLUORESCENCE;

MID; PIRNA; PIWI; STRAND-BIAS; U1-BIAS;

ANIMALS; ARGONAUTE PROTEINS; BOMBYX; CELL LINE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; MICE; NUCLEOTIDES; RNA, SMALL INTERFERING;

EID: 84901444470     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.044701.114     Document Type: Article

References (44)

1. Boland A, Huntzinger E, Schmidt S, Izaurralde E, Weichenrieder O.2011. Crystal structure of the MID-PIWI lobe of a eukaryoticArgonaute protein. Proc Natl Acad Sci 108: 10466-10471.
2. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R,Hannon GJ. 2007. Discrete small RNA-generating loci as master regulatorsof transposon activity in Drosophila. Cell 128: 1089-1103. (Pubitemid 46427877)
3. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X,Murray LW, Arendall WB III, Snoeyink J, Richardson JS, et al.2007. MolProbity: all-atom contacts and structure validation forproteins and nucleic acids. Nucleic Acids Res 35: W375-W383.
4. de La Fortelle E, Bricogne G. 1997. Maximum-likelihood heavy-atomparameter refinement from multiple isomorphous replacementand multiwavelength anomalous diffraction methods. In Methodsin Enzymology, Macromolecular Crystallography (ed. Sweet RM,Carter WC), Vol. 276, pp. 472-494. Academic Press, Waltham, MA. (Pubitemid 27085618)
5. Emsley P, Cowtan K. 2004. Coot: model-building tools for moleculargraphics. Acta Crystallogr 60: 2126-2132.
6. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms ofpost-transcriptional regulation by microRNAs: Are the answers insight? Nat Rev Genet 9: 102-114.
7. Frank F, Sonenberg N, Nagar B. 2010. Structural basis for 5′-nucleotidebase-specific recognition of guide RNA by human AGO2. Nature465: 818-822.
8. Frank F, Hauver J, Sonenberg N, Nagar B. 2012. Arabidopsis ArgonauteMID domains use their nucleotide specificity loop to sort smallRNAs. EMBO J 31: 3588-3595.
9. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: an expandinguniverse. Nat Rev Genet 10: 94-108.
10. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y,Nagami T, Siomi H, Siomi MC. 2007. A slicer-mediated mechanismfor repeat-associated siRNA 5′ end formation in Drosophila. Science315: 1587-1590. (Pubitemid 46449477)
11. Heo I, Kim VN. 2009. Regulating the regulators: posttranslational modificationsof RNA silencing factors. Cell 139: 28-31.
12. Kabsch W. 2010. XDS. Acta Cryst D66: 125-132.
13. Kawamata T, Tomari Y. 2010. Making RISC. Trends Biochem Sci 35:368-376.
14. Kawaoka S, Hayashi N, Suzuki Y, Abe H, Sugano S, Tomari Y, Shimada T, Katsuma S. 2009. The Bombyx ovary-derived cell line endogenouslyexpresses PIWI/PIWI-interacting RNA complexes. RNA 15: 1258-1264.
15. Kawaoka S, Izumi N, Katsuma S, Tomari Y. 2011. 3′ end formation ofPIWI-interacting RNAs in vitro. Mol Cell 43: 1015-1022.
16. Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S,Klein PS, Rigoutsos I, Jongens TA, Mourelatos Z. 2009. Argininemethylation of Piwi proteins catalysed by dPRMT5 is required forAgo3 and Aub stability. Nat Cell Biol 11: 652-658.
17. Li XZ, Roy CK, Dong X, Bolcun-Filas E, Wang J, Han BW, Xu J,Moore MJ, Schimenti JC, Weng Z, Zamore PD. 2013. An ancienttranscription factor initiates the burst of piRNA production duringearly meiosis in mouse testes. Mol Cell 50: 67-81.
18. Luteijn MJ, Ketting RF. 2013. PIWI-interacting RNAs: from generationto transgenerational epigenetics. Nat Rev Genet 14: 523-534.
19. Ma JB, Yuan YR, Meister G, Pei Y, Tuschl T, Patel DJ. 2005. Structuralbasis for 5′-end-specific recognition of guide RNA by the A. fulgidusPiwi protein. Nature 434: 666-670. (Pubitemid 40488561)
20. Malone CD, Hannon GJ. 2009. Small RNAs as guardians of the genome.Cell 136: 656-668.
21. McCarthy AA, Brockhauser S, Nurizzo D, Theveneau P, Mairs T,Spruce D, Guijarro M, Lesourd M, Ravelli RBG, McSweeney S.2009. A decade of user operation on the macromolecular crystallographyMAD beamline ID14-4 at the ESRF. J Synchrotron Radiat 16:803-812.
22. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC,Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr40: 658-674. (Pubitemid 47080256)
23. Meister G. 2013. Argonaute proteins: functional insights and emergingroles. Nat Rev Genet 14: 447-459.
24. Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H,Long C, et al. 2008. Sorting of small RNAs into Arabidopsis argonautecomplexes is directed by the 5′ terminal nucleotide. Cell133: 116-127.
25. Morris RJ, Zwart PH, Cohen S, Fernandez FJ, Kakaris M, Kirillova O,Vonrhein C, Perrakis A, Lamzin VS. 2004. Breaking good resolutionswith ARP/wARP. J Synchrotron Radiat 11: 56-59.
26. Morris GM, Huey R, LindstromW, Sanner MF, Belew RK, Goodsell DS, Olson AJ. 2009. AutoDock4 and AutoDockTools4: automated dockingwith selective receptor flexibility. J Comput Chem 30: 2785-2791.
27. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecularstructures by the maximum-likelihood method. ActaCrystallogr 53: 240-255.
28. Nakanishi K, Weinberg DE, Bartel DP, Patel DJ. 2012. Structure of yeastArgonaute with guide RNA. Nature 486: 368-374.
29. Olivieri D, Senti KA, Subramanian S, Sachidanandam R, Brennecke J.2012. The cochaperone shutdown defines a group of biogenesis factorsessential for all piRNA populations in Drosophila. Mol Cell 47:954-969.
30. Panjikar S, Parthasarathy V, Lamzin VS, Weiss MS, Tucker PA. 2005.Auto-rickshaw: an automated crystal structure determination platformas an efficient tool for the validation of an X-ray diffraction experiment.Acta Crystallogr 61: 449-457.
31. Parker JS, Barford D. 2006. Argonaute: a scaffold for the function ofshort regulatory RNAs. Trends Biochem Sci 31: 622-630. (Pubitemid 44635269)
32. Parker JS, Roe SM, Barford D. 2005. Structural insights into mRNA recognitionfrom a PIWI domain-siRNA guide complex. Nature 434:663-666. (Pubitemid 40488560)
33. Patel DJ, Ma JB, Yuan YR, Ye K, Pei Y, Kuryavyi V, Malinina L, Meister G,Tuschl T. 2006. Structural biology ofRNAsilencing and its functionalimplications. Cold Spring Harb Symp Quant Biol 71: 81-93.
34. Rao ST, Rossmann MG. 1973. Comparison of super-secondary structuresin proteins. J Mol Biol 76: 241-256.
35. Reuter M, Berninger P, Chuma S, Shah H, Hosokawa M, Funaya C,Antony C, Sachidanandam R, Pillai RS. 2011. Miwi catalysis is requiredfor piRNA amplification-independent LINE1 transposon silencing.Nature 480: 264-267.
36. Rudel S, Wang Y, Lenobel R, Korner R, Hsiao HH, Urlaub H, Patel D,Meister G. 2011. Phosphorylation of human Argonaute proteins affectssmall RNA binding. Nucleic Acids Res 39: 2330-2343.
37. Schirle NT, MacRae IJ. 2012. The crystal structure of human Argonaute2.Science 336: 1037-1040.
38. Schneider TR, Sheldrick GM. 2002. Substructure solution withSHELXD. Acta Crystallogr 58: 1772-1779.
39. Simon B, Kirkpatrick JP, Eckhardt S, Reuter M, Rocha EA, Andrade-Navarro MA, Sehr P, Pillai RS, Carlomagno T. 2011. Recognitionof 2′-O-methylated 3′-end of piRNA by the PAZ domain of a Piwiprotein. Structure 19: 172-180.
40. Tian Y, Simanshu DK, Ma JB, Patel DJ. 2011. Structural basis for piRNA2′-O-methylated 3′-end recognition by Piwi PAZ (Piwi/Argonaute/Zwille) domains. Proc Natl Acad Sci 108: 903-910.
41. Till S, Lejeune E, Thermann R, Bortfeld M, Hothorn M, Enderle D,Heinrich C, Hentze MW, Ladurner AG. 2007. A conserved motifin Argonaute-interacting proteins mediates functional interactionsthrough the Argonaute PIWI domain. Nat Struct Mol Biol 14:897-903. (Pubitemid 47525180)
42. Trott O, Olson AJ. 2010. AutoDock Vina: improving the speed and accuracyof docking with a new scoring function, efficient optimization,and multithreading. J Comput Chem 31: 455-461.
43. Wang Y, Juranek S, Li H, Sheng G,Wardle GS, Tuschl T, Patel DJ. 2009.Nucleation, propagation and cleavage of target RNAs in Ago silencingcomplexes. Nature 461: 754-761.
44. Xiol J, Cora E, Koglgruber R, Chuma S, Subramanian S, Hosokawa M,Reuter M, Yang Z, Berninger P, Palencia A, et al. 2012. A role forFkbp6 and the chaperone machinery in piRNA amplification andtransposon silencing. Mol Cell 47: 970-979.