Lsm2 and Lsm3 bridge the interaction of the Lsm1-7 complex with Pat1 for decapping activation

Cell Research

Volumn 24, Issue 2, 2014, Pages 233-246

  Wu, Donghui ^a   Muhlrad, Denise ^b   Bowler, Matthew W ^c   Jiang, Shimin ^a   Liu, Zhou ^d   Parker, Roy ^b   Song, Haiwei ^a,d,e  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b UNIVERSITY OF COLORADO   (United States)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d ZHEJIANG UNIVERSITY   (China)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

decapping activation; Lsm; MRNA decay; Pat1; x ray crystallography

Indexed keywords

EUKARYOTA;

CAPPED RNA; LSM2 PROTEIN, S CEREVISIAE; LSM3 PROTEIN, S CEREVISIAE; PAT1 PROTEIN, S CEREVISIAE; RNA; RNA BINDING PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CHEMISTRY; GENETICS; METABOLISM; MUTAGENESIS; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; MUTAGENESIS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA; RNA CAPS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84893804491     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2013.152     Document Type: Article

References (69)

1. Coller J, Parker R. Eukaryotic mRNA decapping. Annu Rev Biochem 2004; 73:861-890.
2. Parker R, Song H. The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 2004; 11:121-127.
3. Wilson T, Treisman R. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3 AU-rich sequences. Nature 1988; 336:396-399.
4. Shyu AB, Belasco JG, Greenberg ME. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev 1991; 5:221-231.
5. Decker CJ, Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes Dev 1993; 7:1632-1643.
6. Arribas-Layton M, Wu D, Lykke-Andersen J, Song H. Structural and functional control of the eukaryotic mRNA decapping machinery. Biochim Biophys Acta 2013; 1829:580-589.
7. Hsu CL, Stevens A. Yeast cells lacking 53 exoribonuclease contain mRNA species that are poly(A) deficient and partially lack the 5 cap structure. Mol Cell Biol 1993; 13:4826-4835.
8. Beelman CA, Stevens A, Caponigro G, et al. An essential component of the decapping enzyme required for normal rates of mRNA turnover. Nature 1996; 382:642-646.
9. Dunckley T, Parker R. The DCP2 protein is required for mRNA decapping in Saccharomyces cerevisiae and contains a functional MutT motif. EMBO J 1999; 18:5411-5422.
10. Song MG, Kiledjian M. 3 Terminal oligo U-tract-mediated stimulation of decapping. Rna 2007; 13:2356-2365.
11. Rissland OS, Norbury CJ. Decapping is preceded by 3 uridylation in a novel pathway of bulk mRNA turnover. Nat Struct Mol Biol 2009; 16:616-623.
12. Fenger-Gron M, Fillman C, Norrild B, Lykke-Andersen J. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell 2005; 20:905-915.
13. Rehwinkel J, Behm-Ansmant I, Gatfield D, Izaurralde E. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 2005; 11:1640-1647.
14. Behm-Ansmant I, Rehwinkel J, Doerks T, et al. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 2006; 20:1885-1898.
15. Mullen TE, Marzluff WF. Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5 to 3 and 3 to 5. Genes Dev 2008; 22:50-65.
16. Geisler S, Lojek L, Khalil AM, Baker KE, Coller J. Decapping of long noncoding RNAs regulates inducible genes. Mol Cell 2012; 45:279-291.
17. Lai T, Cho H, Liu Z, et al. Structural basis of the PNRC2- mediated link between mRNA surveillance and decapping. Structure 2012; 20:2025-2037.
18. Balagopal V, Parker R. Polysomes, P bodies and stress granules: States and fates of eukaryotic mRNAs. Curr Opin Cell Biol 2009; 21:403-408.
19. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: At the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007; 8:9-22.
20. Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell 2007; 25:635-646.
21. Pilkington GR, Parker R. Pat1 contains distinct functional domains that promote P-body assembly and activation of decapping. Mol Cell Biol 2008; 28:1298-1312.
22. Nissan T, Rajyaguru P, She M, Song H, Parker R. Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Molecular cell 2010; 39:773-783.
23. Braun JE, Tritschler F, Haas G, et al. The C-terminal alphaalpha superhelix of Pat is required for mRNA decapping in metazoa. EMBO J 2010; 29:2368-2380.
24. Fischer N, Weis K. The DEAD box protein Dhh1 stimulates the decapping enzyme Dcp1. EMBO J 2002; 21:2788-2797.
25. Ozgur S, Chekulaeva M, Stoecklin G. Human Pat1b connects deadenylation with mRNA decapping and controls the assembly of processing bodies. Mol Cell Biol 2010; 30:4308-4323.
26. Totaro A, Renzi F, La Fata G, et al. The human Pat1b protein: A novel mRNA deadenylation factor identified by a new immunoprecipitation technique. Nucleic Acids Res 2011; 39:635-647.
27. Chowdhury A, Mukhopadhyay J, Tharun S. The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs. RNA 2007; 13:998-1016.
28. Bergman N, Moraes KC, Anderson JR, et al. Lsm proteins bind and stabilize RNAs containing 5 poly(A) tracts. Nat Struct Mol Biol 2007; 14:824-831.
29. Herrero AB, Moreno S. Lsm1 promotes genomic stability by controlling histone mRNA decay. EMBO J 2011; 30:2008- 2018.
30. Norbury CJ. 3 Uridylation and the regulation of RNA function in the cytoplasm. Biochem Soc Trans 2010; 38:1150-1153.
31. Heo I, Joo C, Cho J, et al. Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol Cell 2008; 32:276-284.
32. Hagan JP, Piskounova E, Gregory RI. Lin28 recruits the TUTase Zcchc11 to inhibit let-7 maturation in mouse embryonic stem cells. Nat Struct Mol Biol 2009; 16:1021-1025.
33. Heo I, Joo C, Kim YK, et al. TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation. Cell 2009; 138:696-708.
34. Lehrbach NJ, Armisen J, Lightfoot HL, et al. LIN-28 and the poly(U) polymerase PUP-2 regulate let-7 microRNA processing in Caenorhabditis elegans. Nat Struct Mol Biol 2009; 16:1016-1020.
35. van Wolfswinkel JC, Claycomb JM, Batista PJ, et al. CDE-1 affects chromosome segregation through uridylation of CSR- 1-bound siRNAs. Cell 2009; 139:135-148.
36. Zaric B, Chami M, Remigy H, et al. Reconstitution of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function. J Biol Chem 2005; 280:16066-16075.
37. Deshmukh MV, Jones BN, Quang-Dang DU, et al. mRNA decapping is promoted by an RNA-binding channel in Dcp2. Mol Cell 2008; 29:324-336.
38. Wang Z, Kiledjian M. Functional link between the mammalian exosome and mRNA decapping. Cell 2001; 107:751-762.
39. Bouveret E, Rigaut G, Shevchenko A, Wilm M, Seraphin B. A Sm-like protein complex that participates in mRNA degradation. EMBO J 2000; 19:1661-1671.
40. Tharun S, He W, Mayes AE, et al. Yeast Sm-like proteins function in mRNA decapping and decay. Nature 2000; 404:515-518.
41. Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 2003; 300:805-808.
42. Holm L, Rosenstrom P. Dali server: Conservation mapping in 3D. Nucleic Acids Res 2010; 38:545-549.
43. Naidoo N, Harrop SJ, Sobti M, et al. Crystal structure of Lsm3 octamer from Saccharomyces cerevisiae: Implications for Lsm ring organisation and recruitment. J Mol Biol 2008; 377:1357-1371.
44. Wu D, Jiang S, Bowler MW, Song H. Crystal Structures of Lsm3, Lsm4 and Lsm5/6/7 from Schizosaccharomyces pombe. PLoS ONE 2012; 7:e36768.
45. Pannone BK, Kim SD, Noe DA, Wolin SL. Multiple functional interactions between components of the Lsm2-Lsm8 complex, U6 snRNA, and the yeast La protein. Genetics 2001; 158:187-196.
46. Muhlrad D, Decker CJ, Parker R. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 53 digestion of the transcript. Genes Dev 1994; 8:855-866.
47. Hatfield L, Beelman CA, Stevens A, Parker R. Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol Cell Biol 1996; 16:5830-5838.
48. Cao D, Parker R. Computational modeling of eukaryotic mRNA turnover. RNA 2001; 7:1192-1212.
49. He W, Parker R. The yeast cytoplasmic LsmI/Pat1p complex protects mRNA 3 termini from partial degradation. Genetics 2001; 158:1445-1455.
50. Achsel T, Brahms H, Kastner B, et al. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J 1999; 18:5789-5802.
51. Mayes AE, Verdone L, Legrain P, Beggs JD. Characterization of Sm-like proteins in yeast and their association with U6 sn- RNA. EMBO J 1999; 18:4321-4331.
52. Salgado-Garrido J, Bragado-Nilsson E, Kandels-Lewis S, Seraphin B. Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J 1999; 18:3451-3462.
53. Pomeranz Krummel DA, Oubridge C, Leung AK, Li J, Nagai K. Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 2009; 458:475-480.
54. Leung AK, Nagai K, Li J. Structure of the spliceosomal U4 snRNP core domain and its implication for snRNP biogenesis. Nature 2011; 473:536-539.
55. Mund M, Neu A, Ullmann J, Neu U, Sprangers R. Structure of the LSm657 complex: An assembly intermediate of the LSm1- and LSm2-8 rings. J Mol Biol 2011; 414:165-176.
56. Arnold K, Bordoli L, Kopp J, Schwede T. The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 2006; 22:195-201.
57. Stevens SW, Ryan DE, Ge HY, et al. Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol Cell 2002; 9:31-44.
58. Wu D, Lim SC, Dong Y, et al. Structural basis of substrate binding specificity revealed by the crystal structures of polyamine receptors SpuD and SpuE from Pseudomonas aeruginosa. J Mol Biol 2012; 416:697-712.
59. Bowler MW, Guijarro M, Petitdemange S, et al. Diffraction cartography: Applying microbeams to macromolecular crystallography sample evaluation and data collection. Acta Crystallogr D Biol Crystallogr 2010; 66:855-864.
60. Gabadinho J, Beteva A, Guijarro M, et al. MxCuBE: A synchrotron beamline control environment customized for macromolecular crystallography experiments. J Synchrotron Radiat 2010; 17:700-707.
61. Brockhauser S, Svensson O, Bowler MW, et al. The use of workflows in the design and implementation of complex experiments in macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2012; 68:975-984.
62. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 1993; 26:795-800.
63. Potterton E, Briggs P, Turkenburg M, Dodson E. A graphical user interface to the CCP4 program suite. Acta Crystallogr D Biol Crystallogr 2003; 59:1131-1137.
64. Zwart PH, Afonine PV, Grosse-Kunstleve RW, et al. Automated structure solution with the PHENIX suite. Methods Mol Biol 2008; 426:419-435.
65. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 1991; 47 (Part 2):110-119.
66. Emsley P, Cowtan K. Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 2004; 60:2126-2132.
67. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 1997; 53:240-255.
68. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001; 98:10037-10041.
69. Zhang S, Williams CJ, Wormington M, Stevens A, Peltz SW. Monitoring mRNA decapping activity. Methods 1999; 17:46-51.