Yeast Rrp9p is an Evolutionarily Conserved U3 SnoRNP Protein Essential for Early Pre-rRNA Processing Cleavages and Requires Box C for Its Association

Overview

Journal RNA

Specialty Molecular Biology

Date 2000 Dec 6

PMID 11105764

Citations 39

Authors

J Venema

H R Vos

A W Faber

W J van Venrooij

H A Raue

Affiliations

Soon will be listed here.

Abstract

Pre-rRNA processing in eukaryotic cells requires participation of several snoRNPs. These include the highly conserved and abundant U3 snoRNP, which is essential for synthesis of 18S rRNA. Here we report the characterization of Rrp9p, a novel yeast U3 protein, identified via its homology to the human U3-55k protein. Epitope-tagged Rrp9p specifically precipitates U3 snoRNA, but Rrp9p is not required for the stable accumulation of this snoRNA. Genetic depletion of Rrp9p inhibits the early cleavages of the primary pre-rRNA transcript at A0, A1, and A2 and, consequently, production of 18S, but not 25S and 5.8S, rRNA. The hU3-55k protein can partially complement a yeast rrp9 null mutant, indicating that the function of this protein has been conserved. Immunoprecipitation of extracts from cells that coexpress epitope-tagged Rrp9p and various mutant forms of U3 snoRNA limits the region required for association of Rrp9p to the U3-specific box B/C motif. Box C is essential, whereas box B plays a supportive role.

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References

Lyman S, Gerace L, Baserga S . Human Nop5/Nop58 is a component common to the box C/D small nucleolar ribonucleoproteins. RNA. 1999; 5(12):1597-604. PMC: 1369881. DOI: 10.1017/s1355838299991288. View

Lafontaine D, Tollervey D . Nop58p is a common component of the box C+D snoRNPs that is required for snoRNA stability. RNA. 1999; 5(3):455-67. PMC: 1369773. DOI: 10.1017/s135583829998192x. View

Lafontaine D, Tollervey D . Synthesis and assembly of the box C+D small nucleolar RNPs. Mol Cell Biol. 2000; 20(8):2650-9. PMC: 85480. DOI: 10.1128/MCB.20.8.2650-2659.2000. View

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

Guarente L, Yocum R, Gifford P . A GAL10-CYC1 hybrid yeast promoter identifies the GAL4 regulatory region as an upstream site. Proc Natl Acad Sci U S A. 1982; 79(23):7410-4. PMC: 347349. DOI: 10.1073/pnas.79.23.7410. View

Tollervey D . A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J. 1987; 6(13):4169-75. PMC: 553900. DOI: 10.1002/j.1460-2075.1987.tb02763.x. View

Sikorski R, Hieter P . A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989; 122(1):19-27. PMC: 1203683. DOI: 10.1093/genetics/122.1.19. View

Li H, Zagorski J, Fournier M . Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol Cell Biol. 1990; 10(3):1145-52. PMC: 360983. DOI: 10.1128/mcb.10.3.1145-1152.1990. View

Kass S, Tyc K, Steitz J . The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell. 1990; 60(6):897-908. DOI: 10.1016/0092-8674(90)90338-f. View

10.

Lee S, Baserga S . Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing. Mol Cell Biol. 1999; 19(8):5441-52. PMC: 84386. DOI: 10.1128/MCB.19.8.5441. View

11.

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

12.

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

13.

Savino R, Gerbi S . In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J. 1990; 9(7):2299-308. PMC: 551956. DOI: 10.1002/j.1460-2075.1990.tb07401.x. View

14.

Kass S . The first pre-rRNA-processing event occurs in a large complex: analysis by gel retardation, sedimentation, and UV cross-linking. Mol Cell Biol. 1990; 10(9):4920-31. PMC: 361110. DOI: 10.1128/mcb.10.9.4920-4931.1990. View

15.

Jansen R, Hurt E, Kern H, Lehtonen H, Carmo-Fonseca M, Lapeyre B . Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast. J Cell Biol. 1991; 113(4):715-29. PMC: 2288999. DOI: 10.1083/jcb.113.4.715. View

16.

Raue H, Planta R . Ribosome biogenesis in yeast. Prog Nucleic Acid Res Mol Biol. 1991; 41:89-129. DOI: 10.1016/s0079-6603(08)60007-0. View

17.

Hughes J, Ares Jr M . Depletion of U3 small nucleolar RNA inhibits cleavage in the 5' external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 1991; 10(13):4231-9. PMC: 453175. DOI: 10.1002/j.1460-2075.1991.tb05001.x. View

18.

Gietz D, St Jean A, Woods R, Schiestl R . Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992; 20(6):1425. PMC: 312198. DOI: 10.1093/nar/20.6.1425. View

19.

Morrissey J, Tollervey D . Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol Cell Biol. 1993; 13(4):2469-77. PMC: 359567. DOI: 10.1128/mcb.13.4.2469-2477.1993. View

20.

Jansen R, Tollervey D, Hurt E . A U3 snoRNP protein with homology to splicing factor PRP4 and G beta domains is required for ribosomal RNA processing. EMBO J. 1993; 12(6):2549-58. PMC: 413493. DOI: 10.1002/j.1460-2075.1993.tb05910.x. View