A U1 snRNP-specific assembly pathway reveals the SMN complex as a versatile hub for RNP exchange

Nature Structural and Molecular Biology

Volumn 23, Issue 3, 2016, Pages 225-230

  So, Byung Ran ^a   Wan, Lili ^a   Zhang, Zhenxi ^a   Li, Pilong ^a   Babiash, Eric ^a   Duan, Jingqi ^a   Younis, Ihab ^a   Dreyfuss, Gideon ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SM; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; SURVIVAL MOTOR NEURON PROTEIN; TRANSCRIPTOME; U1 SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; GEMIN2 PROTEIN, HUMAN; NERVE PROTEIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE SILENCING; HUMAN; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; RNA BINDING; RNA METABOLISM; SIGNAL TRANSDUCTION; SPINAL MUSCULAR ATROPHY; CHEMISTRY; METABOLISM; MOLECULAR MODEL;

HUMANS; METABOLIC NETWORKS AND PATHWAYS; MODELS, MOLECULAR; NERVE TISSUE PROTEINS; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RNA-BINDING PROTEINS; SMN COMPLEX PROTEINS;

EID: 84959566655     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3167     Document Type: Article

References (58)

1. Mount, S.M., Pettersson, I., Hinterberger, M., Karmas, A., & Steitz, J.A. The U1 small nuclear RNA-protein complex selectively binds a 5' splice site in vitro. Cell 33, 509-518 (1983
2. Will, C.L., & Lührmann, R. Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 3, a003707 (2011
3. Berg, M.G., et al U1 snRNP determines mRNA length and regulates isoform expression. Cell 150 53-64 2012
4. Kaida, D., et al U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468 664-668 2010
5. Vorlová S., et al. Induction of antagonistic soluble decoy receptor tyrosine kinases by intronic polyA activation. Mol. Cell 43, 927-939 (2011
6. Almada, A.E., Wu, X., Kriz, A.J., Burge, C.B., & Sharp, P.A. Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature 499, 360-363 (2013
7. Ntini E., et al. Polyadenylation site-induced decay of upstream transcripts enforces promoter directionality. Nat. Struct. Mol. Biol. 20, 923-928 (2013
8. Baserga, S.J., & Steitz, J.A. The diverse world of small ribonucleoproteins. Cold Spring Harb. Monograph Arch. 24, 359-381 (1993
9. Battle D.J., et al. The SMN complex: an assembly machine for RNPs. Cold Spring Harb. Symp. Quant. Biol. 71, 313-320 (2006
10. Guthrie, C., & Patterson, B. Spliceosomal snRNAs. Annu. Rev. Genet. 22, 387-419 (1988
11. Yong, J., Golembe, T.J., Battle, D.J., Pellizzoni, L., & Dreyfuss, G. snRNAs contain specific SMN-binding domains that are essential for snRNP assembly. Mol. Cell. Biol. 24, 2747-2756 (2004
12. Kondo, Y., Oubridge, C., van Roon, A.M., & Nagai, K. Crystal structure of human U1 snRNP, a small nuclear ribonucleoprotein particle, reveals the mechanism of 5' splice site recognition. eLife 4, e04986 (2015
13. Leung, A.K., Nagai, K., & Li, J. Structure of the spliceosomal U4 snRNP core domain and its implication for snRNP biogenesis. Nature 473, 536-539 (2011
14. Pomeranz Krummel, D.A., Oubridge, C., Leung, A.K., Li, J., & Nagai, K. Crystal structure of human spliceosomal U1 snRNP at 5.5 Å resolution. Nature 458, 475-480 (2009
15. Raker, V.A., Hartmuth, K., Kastner, B., & Lührmann, R. Spliceosomal U snRNP core assembly: Sm proteins assemble onto an Sm site RNA nonanucleotide in a specific and thermodynamically stable manner. Mol. Cell. Biol. 19, 6554-6565 (1999
16. Urlaub, H., Raker, V.A., Kostka, S., & Lührmann, R. Sm protein-Sm site RNA interactions within the inner ring of the spliceosomal snRNP core structure. EMBO J. 20, 187-196 (2001
17. Weber, G., Trowitzsch, S., Kastner, B., Lührmann, R., & Wahl, M.C. Functional organization of the Sm core in the crystal structure of human U1 snRNP. EMBO J. 29, 4172-4184 (2010
18. Battle D.J., et al. The Gemin5 protein of the SMN complex identifies snRNAs. Mol. Cell 23, 273-279 (2006
19. Lau, C.K., Bachorik, J.L., & Dreyfuss, G. Gemin5-snRNA interaction reveals an RNA binding function for WD repeat domains. Nat. Struct. Mol. Biol. 16, 486-491 (2009
20. Yong, J., Kasim, M., Bachorik, J.L., Wan, L., & Dreyfuss, G. Gemin5 delivers snRNA precursors to the SMN complex for snRNP biogenesis. Mol. Cell 38, 551-562 (2010
21. Cauchi, R.J. SMN and Gemins: we are family or are we?: insights into the partnership between Gemins and the spinal muscular atrophy disease protein SMN. BioEssays 32, 1077-1089 (2010
22. Fischer, U., Englbrecht, C., & Chari, A. Biogenesis of spliceosomal small nuclear ribonucleoproteins. Wiley Interdiscip. Rev. RNA 2, 718-731 (2011
23. Chari A., et al. An assembly chaperone collaborates with the SMN complex to generate spliceosomal SnRNPs. Cell 135, 497-509 (2008
24. Grimm C., et al. Structural basis of assembly chaperone-mediated snRNP formation. Mol. Cell 49, 692-703 (2013
25. Zhang R., et al. Structure of a key intermediate of the SMN complex reveals Gemin2s crucial function in snRNP assembly. Cell 146, 384-395 (2011
26. Will, C.L., & Lührmann, R. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 13, 290-301 (2001
27. Matera, A.G., & Wang, Z. A day in the life of the spliceosome. Nat. Rev. Mol. Cell Biol. 15, 108-121 (2014
28. Hamm, J., Dathan, N.A., Scherly, D., & Mattaj, I.W. Multiple domains of U1 snRNA, including U1 specific protein binding sites, are required for splicing. EMBO J. 9, 1237-1244 (1990
29. Nelissen, R.L., Will, C.L., van Venrooij, W.J., & Lührmann, R. The association of the U1-specific 70K and C proteins with U1 snRNPs is mediated in part by common U snRNP proteins. EMBO J. 13, 4113-4125 (1994
30. Yong, J., Pellizzoni, L., & Dreyfuss, G. Sequence-specific interaction of U1 snRNA with the SMN complex. EMBO J. 21, 1188-1196 (2002
31. Wan, L., Ottinger, E., Cho, S., & Dreyfuss, G. Inactivation of the SMN complex by oxidative stress. Mol. Cell 31, 244-254 (2008
32. Wan L., et al. The survival of motor neurons protein determines the capacity for snRNP assembly: biochemical deficiency in spinal muscular atrophy. Mol. Cell. Biol. 25, 5543-5551 (2005
33. Younis I., et al. Minor introns are embedded molecular switches regulated by highly unstable U6ata U6atac snRNA. eLife 2, e00780 (2013
34. Kohtz J.D., et al. Protein-protein interactions and 5'-splice-site recognition in mammalian mRNA precursors. Nature 368, 119-124 (1994
35. Cléry, A., Blatter, M., & Allain, F.H. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 18, 290-298 (2008
36. Cho S., et al. Interaction between the RNA binding domains of Ser-Arg splicing factor 1 and U1-70K snRNP protein determines early spliceosome assembly. Proc. Natl. Acad. Sci. USA 108, 8233-8238 (2011
37. Burghes, A.H., & Beattie, C.E. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat. Rev. Neurosci. 10, 597-609 (2009
38. Lorson C.L., et al. SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat. Genet. 19, 63-66 (1998
39. Pellizzoni, L., Yong, J., & Dreyfuss, G. Essential role for the SMN complex in the specificity of snRNP assembly. Science 298, 1775-1779 (2002
40. Young, P.J., et al. The exon 2b region of the spinal muscular atrophy protein, SMN, is involved in self-Association and SIP1 binding. Hum. Mol. Genet. 9, 2869-2877 (2000
41. Bedford, M.T., & Clarke, S.G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13 (2009
42. Tripsianes K., et al. Structural basis for dimethylarginine recognition by the Tudor domains of human SMN and SPF30 proteins. Nat. Struct. Mol. Biol. 18, 1414-1420 (2011
43. Liu, K., et al. Crystal structure of TDRD3 and methyl-Arginine binding characterization of TDRD3, SMN and SPF30. PLoS One 7, e30375 (2012
44. Yong, J., Wan, L., & Dreyfuss, G. Why do cells need an assembly machine for RNA-protein complexes? Trends Cell Biol. 14, 226-232 (2004
45. Ling, S.C., Polymenidou, M., & Cleveland, D.W. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron 79, 416-438 (2013
46. Piazzon N., et al. Implication of the SMN complex in the biogenesis and steady state level of the signal recognition particle. Nucleic Acids Res. 41, 1255-1272 (2013
47. Cheng, D., Côté, J., Shaaban, S., & Bedford, M.T. The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol. Cell 25, 71-83 (2007
48. Lorson, C.L., & Androphy, E.J. The domain encoded by exon 2 of the survival motor neuron protein mediates nucleic acid binding. Hum. Mol. Genet. 7, 1269-1275 (1998
49. OReilly, D., et al. Differentially expressed, variant U1 snRNAs regulate gene expression in human cells. Genome Res. 23, 281-291 (2013
50. Shukla, S., & Parker, R. Quality control of assembly-defective U1 snRNAs by decapping and 5'-To-3' exonucleolytic digestion. Proc. Natl. Acad. Sci. USA 111, E3277-E3286 (2014
51. Gabanella F., et al. Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS One 2, e921 (2007
52. Li, D.K., Tisdale, S., Lotti, F., & Pellizzoni, L. SMN control of RNP assembly: from post-Transcriptional gene regulation to motor neuron disease. Semin. Cell Dev. Biol. 32, 22-29 (2014
53. Tisdale S., et al. SMN is essential for the biogenesis of U7 small nuclear ribonucleoprotein and 3'-end formation of histone mRNAs. Cell Reports 5, 1187-1195 (2013
54. Zhang Z., et al. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 133, 585-600 (2008
55. Zhang Z., et al. Dysregulation of synaptogenesis genes antecedes motor neuron pathology in spinal muscular atrophy. Proc. Natl. Acad. Sci. USA 110, 19348-19353 (2013
56. Sun S., et al. ALS-causative mutations in FUS/TLS confer gain and loss of function by altered association with SMN and U1-snRNP. Nat. Commun. 6, 6171 (2015
57. Tsuiji H., et al. Spliceosome integrity is defective in the motor neuron diseases ALS and SMA. EMBO Mol. Med. 5, 221-234 (2013
58. Yamazaki T., et al. FUS-SMN protein interactions link the motor neuron diseases ALS and SMA. Cell Reports 2, 799-806 (2012