Xenopus U3 SnoRNA Docks on Pre-rRNA Through a Novel Base-pairing Interaction

Overview

Journal RNA

Specialty Molecular Biology

Date 2004 May 18

PMID 15146078

Citations 18

Authors

Anton V Borovjagin

Susan A Gerbi

Affiliations

Soon will be listed here.

Abstract

U3 small nucleolar RNA (snoRNA) is essential for rRNA processing to form 18S ribosomal RNA (rRNA). Previously, it has been shown that nucleolin is needed to load U3 snoRNA on pre-rRNA. However, as documented here, this is not sufficient. We present data that base-pairing between the U3 hinges and the external transcribed spacer (ETS) is critical for functional alignment of U3 on its pre-rRNA substrate. Additionally, the interaction between the U3 hinges and the ETS is proposed to serve as an anchor to hold U3 on the pre-rRNA substrate, while box A at the 5' end of U3 snoRNA swivels from ETS contacts to 18S rRNA contacts. Compensatory base changes revealed base-pairing between the 3' hinge of U3 snoRNA and region E1 of the ETS in Xenopus pre-rRNA; this novel interaction is required for 18S rRNA production. In contrast, base-pairing between the 5' hinge of U3 snoRNA and region E2 of the ETS is auxiliary, unlike the case in yeast where it is required. Thus, higher and lower eukaryotes use different interactions for functional association of U3 with pre-rRNA. The U3 hinge sequence varies between species, but covariation in the ETS retains complementarity. This species-specific U3-pre-rRNA interaction offers a potential target for a new class of antibiotics to prevent ribosome biogenesis in eukaryotic pathogens.

Citing Articles

Functional regions in the 5' external transcribed spacer of yeast pre-rRNA.

Chen J, Zhang L, Ye K RNA. 2020; 26(7):866-877.

PMID: 32213618 PMC: 7297118. DOI: 10.1261/rna.074807.120.

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.

Pre-Ribosomal RNA Processing in Human Cells: From Mechanisms to Congenital Diseases.

Aubert M, ODonohue M, Lebaron S, Gleizes P Biomolecules. 2018; 8(4).

PMID: 30356013 PMC: 6315592. DOI: 10.3390/biom8040123.

Maturation of the 90S pre-ribosome requires Mrd1 dependent U3 snoRNA and 35S pre-rRNA structural rearrangements.

Lackmann F, Belikov S, Burlacu E, Granneman S, Wieslander L Nucleic Acids Res. 2018; 46(7):3692-3706.

PMID: 29373706 PMC: 5909432. DOI: 10.1093/nar/gky036.

Arabidopsis small nucleolar RNA monitors the efficient pre-rRNA processing during ribosome biogenesis.

Zhu P, Wang Y, Qin N, Wang F, Wang J, Deng X Proc Natl Acad Sci U S A. 2016; 113(42):11967-11972.

PMID: 27708161 PMC: 5081647. DOI: 10.1073/pnas.1614852113.

References

Beltrame M, Henry Y, Tollervey D . Mutational analysis of an essential binding site for the U3 snoRNA in the 5' external transcribed spacer of yeast pre-rRNA. Nucleic Acids Res. 1994; 22(23):5139-47. PMC: 523791. DOI: 10.1093/nar/22.23.5139. View

Mougey E, Pape L . A U3 small nuclear ribonucleoprotein-requiring processing event in the 5' external transcribed spacer of Xenopus precursor rRNA. Mol Cell Biol. 1993; 13(10):5990-8. PMC: 364653. DOI: 10.1128/mcb.13.10.5990-5998.1993. View

Hughes J . Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA. J Mol Biol. 1996; 259(4):645-54. DOI: 10.1006/jmbi.1996.0346. View

Enright C, MAXWELL E, Eliceiri G . 5'ETS rRNA processing facilitated by four small RNAs: U14, E3, U17, and U3. RNA. 1996; 2(11):1094-9. PMC: 1369439. View

Gulli M, Faubladier M, Sicard H, Caizergues-Ferrer M, Gas N . Ultrastructural changes in the Schizosaccharomyces pombe nucleolus following the disruption of the gar2+ gene, which encodes a nucleolar protein structurally related to nucleolin. Chromosoma. 1997; 105(7-8):542-52. DOI: 10.1007/BF02510491. View

Mereau A, Fournier R, Gregoire A, Mougin A, Fabrizio P, Luhrmann R . An in vivo and in vitro structure-function analysis of the Saccharomyces cerevisiae U3A snoRNP: protein-RNA contacts and base-pair interaction with the pre-ribosomal RNA. J Mol Biol. 1997; 273(3):552-71. DOI: 10.1006/jmbi.1997.1320. View

Ginisty H, Amalric F, Bouvet P . Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 1998; 17(5):1476-86. PMC: 1170495. DOI: 10.1093/emboj/17.5.1476. View

Hartshorne T . Distinct regions of U3 snoRNA interact at two sites within the 5' external transcribed spacer of pre-rRNAs in Trypanosoma brucei cells. Nucleic Acids Res. 1998; 26(11):2541-53. PMC: 147592. DOI: 10.1093/nar/26.11.2541. View

Lange T, Ezrokhi M, Borovjagin A, North M, Gerbi S . Nucleolar localization elements of Xenopus laevis U3 small nucleolar RNA. Mol Biol Cell. 1998; 9(10):2973-85. PMC: 25574. DOI: 10.1091/mbc.9.10.2973. View

10.

Ginisty H, Sicard H, Roger B, Bouvet P . Structure and functions of nucleolin. J Cell Sci. 1999; 112 ( Pt 6):761-72. DOI: 10.1242/jcs.112.6.761. View

11.

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

12.

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

13.

Hartshorne T, Toyofuku W . Two 5'-ETS regions implicated in interactions with U3 snoRNA are required for small subunit rRNA maturation in Trypanosoma brucei. Nucleic Acids Res. 1999; 27(16):3300-9. PMC: 148563. DOI: 10.1093/nar/27.16.3300. View

14.

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

15.

Ginisty H, Serin G, Roger B, Libante V, Amalric F, Bouvet P . Interaction of nucleolin with an evolutionarily conserved pre-ribosomal RNA sequence is required for the assembly of the primary processing complex. J Biol Chem. 2000; 275(25):18845-50. DOI: 10.1074/jbc.M002350200. View

16.

Borovjagin A, Gerbi S . The spacing between functional Cis-elements of U3 snoRNA is critical for rRNA processing. J Mol Biol. 2000; 300(1):57-74. DOI: 10.1006/jmbi.2000.3798. View

17.

Schnare M, Collings J, Spencer D, Gray M . The 28S-18S rDNA intergenic spacer from Crithidia fasciculata: repeated sequences, length heterogeneity, putative processing sites and potential interactions between U3 small nucleolar RNA and the ribosomal RNA precursor. Nucleic Acids Res. 2000; 28(18):3452-61. PMC: 110749. DOI: 10.1093/nar/28.18.3452. View

18.

Hanakahi L, Bu Z, Maizels N . The C-terminal domain of nucleolin accelerates nucleic acid annealing. Biochemistry. 2000; 39(50):15493-9. DOI: 10.1021/bi001683y. View

19.

Peculis B . snoRNA nuclear import and potential for cotranscriptional function in pre-rRNA processing. RNA. 2001; 7(2):207-19. PMC: 1370079. DOI: 10.1017/s1355838201001625. View

20.

Borovjagin A, Gerbi S . Xenopus U3 snoRNA GAC-Box A' and Box A sequences play distinct functional roles in rRNA processing. Mol Cell Biol. 2001; 21(18):6210-21. PMC: 87338. DOI: 10.1128/MCB.21.18.6210-6221.2001. View