Arabidopsis thaliana LSM proteins function in mRNA splicing and degradation

Nucleic Acids Research

Volumn 41, Issue 12, 2013, Pages 6232-6249

  Golisz, Anna ^a   Sikorski, Pawel J ^a   Kruszka, Katarzyna ^a,b   Kufel, Joanna ^a  

^a UNIVERSITY OF WARSAW   (Poland)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PHOSPHODIESTERASE I; PROTEIN LSM; PROTEIN LSM1A; PROTEIN LSM1B; PROTEIN LSM2; PROTEIN LSM3A; PROTEIN LSM3B; PROTEIN LSM4; PROTEIN LSM5; PROTEIN LSM6A; PROTEIN LSM6B; PROTEIN LSM7; PROTEIN LSM8; SMALL NUCLEAR RNA; SPLEEN EXONUCLEASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; RNA DEGRADATION; RNA METABOLISM; RNA SPLICING; RNA STABILITY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL NUCLEUS; CYTOPLASM; GENE EXPRESSION REGULATION, PLANT; MUTATION; RNA SPLICING; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84880245179     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt296     Document Type: Article

References (80)

1. Tharun, S. (2009) Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int. Rev. Cell. Mol. Biol., 272, 149-189.
2. Boeck, R., Lapeyre, B., Brown, C.E. and Sachs, A.B. (1998) Capped mRNA degradation intermediates accumulate in the yeast spb8-2 mutant. Mol. Cell. Biol., 18, 5062-5072.
3. Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S. and Seraphin, B. (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J., 18, 3451-3462.
4. Mayes, A.E., Verdone, L., Legrain, P. and Beggs, J.D. (1999) Characterization of Sm-like proteins in yeast and their association with U6 snRNA. EMBO J., 18, 4321-4331.
5. Achsel, T., Brahms, H., Kastner, B., Bachi, A., Wilm, M. and Luhrmann, R. (1999) 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., 18, 5789-5802.
6. Bouveret, E., Rigaut, G., Shevchenko, A., Wilm, M. and Seraphin, B. (2000) A Sm-like protein complex that participates in mRNA degradation. EMBO J., 19, 1661-1671.
7. Tharun, S., He, W., Mayes, A.E., Lennertz, P., Beggs, J.D. and Parker, R. (2000) Yeast Sm-like proteins function in mRNA decapping and decay. Nature, 404, 515-518.
8. Tharun, S. and Parker, R. (2001) Targeting an mRNA for decapping: displacement of translation factors and association of the Lsm1p-7p complex on deadenylated yeast mRNAs. Mol. Cell, 8, 1075-1083.
9. Balagopal, V. and Parker, R. (2009) Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol., 21, 403-408.
10. Kufel, J., Allmang, C., Verdone, L., Beggs, J. and Tollervey, D. (2002) Lsm proteins are required for normal processing of pre-tRNAs and their efficient association with La-homologous protein Lhp1p. Mol. Cell. Biol., 22, 5248-5256.
11. Tomasevic, N. and Peculis, B.A. (2002) Xenopus LSm proteins bind U8 snoRNA via an internal evolutionarily conserved octamer sequence. Mol. Cell. Biol., 22, 4101-4112.
12. Kufel, J., Allmang, C., Petfalski, E., Beggs, J. and Tollervey, D. (2003) Lsm proteins are required for normal processing and stability of ribosomal RNAs. J. Biol. Chem., 278, 2147-2156.
13. Kufel, J., Allmang, C., Verdone, L., Beggs, J. and Tollervey, D. (2003) A complex pathway for 3′ processing of the yeast U3 snoRNA. Nucleic Acids Res., 31, 6788-6797.
14. Kufel, J., Bousquet-Antonelli, C., Beggs, J.D. and Tollervey, D. (2004) Nuclear pre-mRNA decapping and 5′ degradation in yeast require the Lsm2-8p complex. Mol. Cell. Biol., 24, 9646-9657.
15. Fernandez, C.F., Pannone, B.K., Chen, X., Fuchs, G. and Wolin, S.L. (2004) An Lsm2-Lsm7 complex in Saccharomyces cerevisiae associates with the small nucleolar RNA snR5. Mol. Biol. Cell, 15, 2842-2852.
16. Watkins, N.J., Lemm, I., Ingelfinger, D., Schneider, C., Hossbach, M., Urlaub, H. and Luhrmann, R. (2004) Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol. Cell, 16, 789-798.
17. Eulalio, A., Rehwinkel, J., Stricker, M., Huntzinger, E., Yang, S.F., Doerks, T., Dorner, S., Bork, P., Boutros, M. and Izaurralde, E. (2007) Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev., 21, 2558-2570.
18. Mullen, T.E. and Marzluff, W.F. (2008) 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., 22, 50-65.
19. Verdone, L., Galardi, S., Page, D. and Beggs, J.D. (2004) Lsm proteins promote regeneration of pre-mRNA splicing activity. Curr. Biol., 14, 1487-1491.
20. Chowdhury, A., Mukhopadhyay, J. and Tharun, S. (2007) The decapping activator Lsm1p-7p-Pat1p complex has the intrinsic ability to distinguish between oligoadenylated and polyadenylated RNAs. RNA, 13, 998-1016.
21. Liu, Q., Liang, X.H., Uliel, S., Belahcen, M., Unger, R. and Michaeli, S. (2004) Identification and functional characterization of lsm proteins in Trypanosoma brucei. J. Biol. Chem., 279, 18210-18219.
22. Tkacz, I.D., Gupta, S.K., Volkov, V., Romano, M., Tulinski, P., Lebenthal, I. and Michaeli, S. (2010) Analysis of spliceosomal proteins in trypanosomatids reveals novel functions in mRNA processing. J. Biol. Chem., 285, 27982-27999.
23. Pillai, R.S., Will, C.L., Luhrmann, R., Schumperli, D. and Muller, B. (2001) Purified U7 snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J., 20, 5470-5479.
24. Pillai, R.S., Grimmler, M., Meister, G., Will, C.L., Luhrmann, R., Fischer, U. and Schumperli, D. (2003) Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev., 17, 2321-2333.
25. Albrecht, M. and Lengauer, T. (2004) Novel Sm-like proteins with long C-terminal tails and associated methyltransferases. FEBS Lett., 569, 18-26.
26. Anantharaman, V. and Aravind, L. (2004) Novel conserved domains in proteins with predicted roles in eukaryotic cell-cycle regulation, decapping, and RNA stability. BMC Genomics, 5, 45.
27. Decker, C.J. and Parker, R. (2006) CAR-1 and trailer hitch: driving mRNP granule function at the ER? J. Cell. Biol., 173, 159-163.
28. Decker, C.J., Teixeira, D. and Parker, R. (2007) Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol., 179, 437-449.
29. Wang, B.B. and Brendel, V. (2004) The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biol., 5, R102.
30. Cao, J., Shi, F., Liu, X., Jia, J., Zeng, J. and Huang, G. (2011) Genome-wide identification and evolutionary analysis of Arabidopsis Sm genes family. J. Biomol. Struct. Dyn., 28, 535-544.
31. Zhang, Z., Zhang, S., Zhang, Y., Wang, X., Li, D., Li, Q., Yue, M., Li, Q., Zhang, Y.E., Xu, Y. et al. (2011) Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell, 23, 396-411.
32. Xu, J. and Chua, N.H. (2009) Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell, 21, 3270-3279.
33. Perea-Resa, C., Hernandez-Verdeja, T., Lopez-Cobollo, R., Castellano Mdel, M. and Salinas, J. (2012) LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell, 24, 4930-4947.
34. Xiong, L., Gong, Z., Rock, C.D., Subramanian, S., Guo, Y., Xu, W., Galbraith, D. and Zhu, J.K. (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev. Cell, 1, 771-781.
35. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant, 15, 473-497.
36. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J., 16, 735-743.
37. Gloeckner, C.J., Boldt, K., Schumacher, A., Roepman, R. and Ueffing, M. (2007) A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics, 7, 4228-4234.
38. Nakagawa, T., Ishiguro, S. and Kimura, T. (2009) Gateway vectors for plant transformation. Plant Biotech., 26, 275-284.
39. Notredame, C., Higgins, D.G. and Heringa, J. (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol., 302, 205-217.
40. Guindon, S. and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol., 52, 696-704.
41. Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol., 17, 540-552.
42. Chevenet, F., Brun, C., Banuls, A.L., Jacq, B. and Christen, R. (2006) Tree-Dyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics, 7, 439.
43. Tatusova, T.A. and Madden, T.L. (1999) BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett., 174, 247-250.
44. Souret, F.F., Kastenmayer, J.P. and Green, P.J. (2004) AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell, 15, 173-183.
45. Terzi, L.C. and Simpson, G.G. (2009) Arabidopsis RNA immunoprecipitation. Plant J., 59, 163-168.
46. Xia, Y., Nikolau, B.J. and Schnable, P.S. (1997) Developmental and hormonal regulation of the Arabidopsis CER2 gene that codes for a nuclear-localized protein required for the normal accumulation of cuticular waxes. Plant Physiol., 115, 925-937.
47. Zakrzewska-Placzek, M., Souret, F.F., Sobczyk, G.J., Green, P.J. and Kufel, J. (2010) Arabidopsis thaliana XRN2 is required for primary cleavage in the pre-ribosomal RNA. Nucleic Acids Res., 38, 4487-4502.
48. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. and Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
49. Bolstad, B.M., Irizarry, R.A., Astrand, M. and Speed, T.P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on bias and variance. Bioinformatics, 19, 185-193.
50. Usadel, B., Nagel, A., Steinhauser, D., Gibon, Y., Blasing, O.E., Redestig, H., Sreenivasulu, N., Krall, L., Hannah, M., Poree, F. et al. (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinformatics, 7, 535-543.
51. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol., 136, 2621-2632.
52. Spiller, M.P., Reijns, M.A. and Beggs, J.D. (2007) Requirements for nuclear localization of the Lsm2-8p complex and competition between nuclear and cytoplasmic Lsm complexes. J. Cell Sci., 120, 4310-4320.
53. Yu, J.H., Yang, W.H., Gulick, T., Bloch, K.D. and Bloch, D.B. (2005) Ge-1 is a central component of the mammalian cytoplasmic mRNA processing body. RNA, 11, 1795-1802.
54. Xu, J., Yang, J.Y., Niu, Q.W. and Chua, N.H. (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell, 18, 3386-3398.
55. Goeres, D.C., Van Norman, J.M., Zhang, W., Fauver, N.A., Spencer, M.L. and Sieburth, L.E. (2007) Components of the Arabidopsis mRNA decapping complex are required for early seedling development. Plant Cell, 19, 1549-1564.
56. Hatfield, L., Beelman, C.A., Stevens, A. and Parker, R. (1996) Mutations in trans-acting factors affecting mRNA decapping in Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 5830-5858.
57. Haas, G., Braun, J.E., Igreja, C., Tritschler, F., Nishihara, T. and Izaurralde, E. (2010) HPat provides a link between deadenylation and decapping in metazoa. J. Cell Biol., 189, 289-302.
58. Ozgur, S., Chekulaeva, M. and Stoecklin, G. (2010) Human Pat1b connects deadenylation with mRNA decapping and controls the assembly of processing bodies. Mol. Cell. Biol., 30, 4308-4323.
59. Totaro, A., Renzi, F., La Fata, G., Mattioli, C., Raabe, M., Urlaub, H. and Achsel, T. (2010) The human Pat1b protein: a novel mRNA deadenylation factor identified by a new immunoprecipitation technique. Nucleic Acids Res., 39, 635-647.
60. Garneau, N.L., Wilusz, J. and Wilusz, C.J. (2007) The highways and byways of mRNA decay. Nat. Rev. Mol. Cell. Biol., 8, 113-126.
61. Raghunathan, P.L. and Guthrie, C. (1998) RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr. Biol., 8, 847-855.
62. Bell, M., Schreiner, S., Damianov, A., Reddy, R. and Bindereif, A. (2002) p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J., 21, 2724-2735.
63. Lauber, J., Fabrizio, P., Teigelkamp, S., Lane, W.S., Hartmann, E. and Luhrmann, R. (1998) The HeLa 200 kDa U5 snRNP-specific protein and its homologue in Sacharomyces cerevisiae are members of the DEXH-box protein family of putative RNA helicase. EMBO J., 15, 4001-4015.
64. Grainger, R.J. and Beggs, J.D. (2005) Prp8 protein: at the heart of the spliceosome. RNA, 11, 533-557.
65. Liu, S., Rauhut, R., Vornlocher, H.P. and Luhrmann, R. (2006) The network of protein-protein interactions within the human U4/U6.U5 tri-snRNP. RNA, 12, 1418-1430.
66. Johnson, M.A., Perez-Amador, M.A., Lidder, P. and Green, P.J. (2000) Mutants of Arabidopsis defective in a sequence-specific mRNA degradation pathway. Proc. Natl Acad. Sci. USA, 97, 13991-13996.
67. Perez-Amador, M.A., Abler, M.L., De Rocher, E.J., Thompson, D.M., van Hoof, A., LeBrasseur, N.D., Lers, A. and Green, P.J. (2000) Identification of BFN1, a bifunctional nuclease induced during leaf and stem senescence in Arabidopsis. Plant Physiol., 122, 169-180.
68. Gutierrez, R.A., Ewing, R.M., Cherry, J.M. and Green, P.J. (2002) Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch-and specific clock-controlled genes. Proc. Natl Acad. Sci. USA, 99, 11513-11158.
69. Seraphin, B. (1995) Sm and Sm-like proteins belong to a large family: identification of proteins of the U6 as well as the U1, U2, U4 and U5 snRNPs. EMBO J., 14, 2089-2098.
70. Chekanova, J.A., Gregory, B.D., Reverdatto, S.V., Chen, H., Kumar, R., Hooker, T., Yazaki, J., Li, P., Skiba, N., Peng, Q. et al. (2007) Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell, 131, 1340-1353.
71. Tkacz, I.D., Cohe, S., Salmon-Divon, M. and Michaeli, S. (2008) Identification of the heptameric Lsm complex that binds U6 snRNA in Trypanosoma brucei. Mol. Biochem. Parasitol., 160, 22-31.
72. Schmid, M. and Jensen, T.H. (2010) Nuclear quality control of RNA polymerase II transcripts. Wiley Interdiscip. Rev. RNA, 1, 474-485.
73. Kuai, L., Das, B. and Sherman, F. (2005) A nuclear degradation pathway controls the abundance of normal mRNAs in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 102, 13962-13967.
74. Houalla, R., Devaux, F., Fatica, A., Kufel, J., Barrass, D., Torchet, C. and Tollervey, D. (2006) Microarray detection of novel nuclear RNA substrates for the exosome. Yeast, 23, 439-454.
75. Song, M.G., Li, Y. and Kiledjian, M. (2010) Multiple mRNA decapping enzymes in mammalian cells. Mol. Cell, 40, 423-432.
76. Brannan, K., Kim, H., Erickson, B., Glover-Cutter, K., Kim, S., Fong, N., Kiemele, L., Hansen, K., Davis, R., Lykke-Andersen, J. et al. (2012) mRNA decapping factors and the exonuclease Xrn2 function in widespread premature termination of RNA polymerase II transcription. Mol. Cell, 46, 311-324.
77. Oeffinger, M., Zenklusen, D., Ferguson, A., Wei, K.E., El Hage, A., Tollervey, D., Chait, B.T., Singer, R.H. and Rout, M.P. (2009) Rrp17p is a eukaryotic exonuclease required for 5′ end processing of Pre-60S ribosomal RNA. Mol. Cell, 36, 768-781.
78. Gietz, D., St Jean, A., Woods, R.A. and Schiestl, R.H. (1992) Improved method for high efficient transformation of intact yeast cells. Nucleic Acids Res., 20, 1425.
79. Baudin, A., Ozier-Kalogeropoulos, O., Denouel, A., Lacroute, F. and Cullin, C. (1993) A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res., 21, 3329-3330.
80. Lau, D., Kunzler, M., Braunwarth, A., Hellmuth, K., Podtelejnikov, A., Mann, M. and Hurt, E. (2000) Purification of protein A-tagged yeast ran reveals association with a novel karyopherin beta family member, Pdr6p. J. Biol. Chem., 275, 467-471.