Analysis of Sequence and Structural Features That Identify the B/C Motif of U3 Small Nucleolar RNA As the Recognition Site for the Snu13p-Rrp9p Protein Pair

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2006 Dec 6

PMID 17145781

Citations 20

Authors

A Clery

V Senty-Segault

F Leclerc

H A Raue

C Branlant

Affiliations

Soon will be listed here.

Abstract

The eukaryal Snu13p/15.5K protein binds K-turn motifs in U4 snRNA and snoRNAs. Two Snu13p/15.5K molecules bind the nucleolar U3 snoRNA required for the early steps of preribosomal processing. Binding of one molecule on the C'/D motif allows association of proteins Nop1p, Nop56p, and Nop58p, whereas binding of the second molecule on the B/C motif allows Rrp9p recruitment. To understand how the Snu13p-Rrp9p pair recognizes the B/C motif, we first improved the identification of RNA determinants required for Snu13p binding by experiments using the systematic evolution of ligands by exponential enrichment. This demonstrated the importance of a U.U pair stacked on the sheared pairs and revealed a direct link between Snu13p affinity and the stability of helices I and II. Sequence and structure requirements for efficient association of Rrp9p on the B/C motif were studied in yeast cells by expression of variant U3 snoRNAs and immunoselection assays. A G-C pair in stem II, a G residue at position 1 in the bulge, and a short stem I were found to be required. The data identify the in vivo function of most of the conserved residues of the U3 snoRNA B/C motif. They bring important information to understand how different K-turn motifs can recruit different sets of proteins after Snu13p association.

Citing Articles

Small but Mighty-The Emerging Role of snoRNAs in Hematological Malignancies.

Calvo Sanchez J, Kohn M Noncoding RNA. 2021; 7(4).

PMID: 34842767 PMC: 8629011. DOI: 10.3390/ncrna7040068.

Emerging Data on the Diversity of Molecular Mechanisms Involving C/D snoRNAs.

Baldini L, Charpentier B, Labialle S Noncoding RNA. 2021; 7(2).

PMID: 34066559 PMC: 8162545. DOI: 10.3390/ncrna7020030.

Synergistic defects in pre-rRNA processing from mutations in the U3-specific protein Rrp9 and U3 snoRNA.

Clerget G, Bourguignon-Igel V, Marmier-Gourrier N, Rolland N, Wacheul L, Manival X Nucleic Acids Res. 2020; 48(7):3848-3868.

PMID: 31996908 PMC: 7144924. DOI: 10.1093/nar/gkaa066.

Gene expression in life stages: Identifying a species-specific target for pest control applications.

Perkin L, Oppert B PeerJ. 2019; 7:e6946.

PMID: 31198628 PMC: 6535216. DOI: 10.7717/peerj.6946.

Mapping targets for small nucleolar RNAs in yeast.

Dudnakova T, Dunn-Davies H, Peters R, Tollervey D Wellcome Open Res. 2018; 3:120.

PMID: 30345388 PMC: 6171561. DOI: 10.12688/wellcomeopenres.14735.2.

References

Schultz A, Nottrott S, Hartmuth K, Luhrmann R . RNA structural requirements for the association of the spliceosomal hPrp31 protein with the U4 and U4atac small nuclear ribonucleoproteins. J Biol Chem. 2006; 281(38):28278-86. DOI: 10.1074/jbc.M603350200. View

Pluk H, Soffner J, Luhrmann R, van Venrooij W . cDNA cloning and characterization of the human U3 small nucleolar ribonucleoprotein complex-associated 55-kilodalton protein. Mol Cell Biol. 1998; 18(1):488-98. PMC: 121518. DOI: 10.1128/MCB.18.1.488. View

Samarsky D, Fournier M . Functional mapping of the U3 small nucleolar RNA from the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1998; 18(6):3431-44. PMC: 108924. DOI: 10.1128/MCB.18.6.3431. View

Henras A, Henry Y, Bousquet-Antonelli C, Gelugne J, Caizergues-Ferrer M . Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs. EMBO J. 1998; 17(23):7078-90. PMC: 1171055. DOI: 10.1093/emboj/17.23.7078. View

Borovjagin A, Gerbi S . U3 small nucleolar RNA is essential for cleavage at sites 1, 2 and 3 in pre-rRNA and determines which rRNA processing pathway is taken in Xenopus oocytes. J Mol Biol. 1999; 286(5):1347-63. DOI: 10.1006/jmbi.1999.2527. View

Stevens S, Abelson J . Purification of the yeast U4/U6.U5 small nuclear ribonucleoprotein particle and identification of its proteins. Proc Natl Acad Sci U S A. 1999; 96(13):7226-31. PMC: 22060. DOI: 10.1073/pnas.96.13.7226. View

Sharma K, Tollervey D . Base pairing between U3 small nucleolar RNA and the 5' end of 18S rRNA is required for pre-rRNA processing. Mol Cell Biol. 1999; 19(9):6012-9. PMC: 84488. DOI: 10.1128/MCB.19.9.6012. View

Watkins N, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H . Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell. 2004; 16(5):789-98. DOI: 10.1016/j.molcel.2004.11.012. View

Cojocaru V, Nottrott S, Klement R, Jovin T . The snRNP 15.5K protein folds its cognate K-turn RNA: a combined theoretical and biochemical study. RNA. 2005; 11(2):197-209. PMC: 1370708. DOI: 10.1261/rna.7149605. View

10.

Charpentier B, Muller S, Branlant C . Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation. Nucleic Acids Res. 2005; 33(10):3133-44. PMC: 1142404. DOI: 10.1093/nar/gki630. View

11.

Li H, White S . RNA apatamers for yeast ribosomal protein L32 have a conserved purine-rich internal loop. RNA. 1997; 3(3):245-54. PMC: 1369477. View

12.

Nottrott S, Hartmuth K, Fabrizio P, Urlaub H, Vidovic I, Ficner R . Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5' stem-loop of U4 snRNA. EMBO J. 1999; 18(21):6119-33. PMC: 1171676. DOI: 10.1093/emboj/18.21.6119. View

13.

Kressler D, Linder P, de la Cruz J . Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol. 1999; 19(12):7897-912. PMC: 84875. DOI: 10.1128/MCB.19.12.7897. View

14.

Mao H, White S, Williamson J . A novel loop-loop recognition motif in the yeast ribosomal protein L30 autoregulatory RNA complex. Nat Struct Biol. 1999; 6(12):1139-47. DOI: 10.1038/70081. View

15.

Venema J, Tollervey D . Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet. 2000; 33:261-311. DOI: 10.1146/annurev.genet.33.1.261. View

16.

Ban N, Nissen P, Hansen J, Moore P, Steitz T . The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science. 2000; 289(5481):905-20. DOI: 10.1126/science.289.5481.905. View

17.

Lukowiak A, Granneman S, Mattox S, Speckmann W, Jones K, Pluk H . Interaction of the U3-55k protein with U3 snoRNA is mediated by the box B/C motif of U3 and the WD repeats of U3-55k. Nucleic Acids Res. 2000; 28(18):3462-71. PMC: 110750. DOI: 10.1093/nar/28.18.3462. View

18.

Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D . Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell. 2000; 102(5):615-23. DOI: 10.1016/s0092-8674(00)00084-2. View

19.

Wimberly B, Brodersen D, Clemons Jr W, Morgan-Warren R, Carter A, Vonrhein C . Structure of the 30S ribosomal subunit. Nature. 2000; 407(6802):327-39. DOI: 10.1038/35030006. View

20.

Watkins N, Segault V, Charpentier B, Nottrott S, Fabrizio P, Bachi A . A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell. 2000; 103(3):457-66. DOI: 10.1016/s0092-8674(00)00137-9. View