Base Pairing between U3 Small Nucleolar RNA and the 5' End of 18S rRNA Is Required for Pre-rRNA Processing

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Molecular and Cellular Biology, September 1999, p. 6012-6019, Vol. 19, No. 9
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Base Pairing between U3 Small Nucleolar RNA and the 5' End of 18S rRNA Is Required for Pre-rRNA Processing

Kishor Sharma¹ and David Tollervey¹^,²^,^*

¹European Molecular Biology Laboratory, Gene Expression Programme, 69012 Heidelberg, Germany, and ² Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom

Received 15 March 1999/Returned for modification 23 April 1999/Accepted 28 May 1999

The loop of a stem structure close to the 5' end of the 18S rRNA is complementary to the box A region of the U3 small nucleolarRNA (snoRNA). Substitution of the 18S loop nucleotides inhibitedpre-rRNA cleavage at site A₁, the 5' end of the 18S rRNA, andat site A₂, located 1.9 kb away in internal transcribed spacer1. This inhibition was largely suppressed by a compensatory mutationin U3, demonstrating functional base pairing. The U3-pre-rRNAbase pairing is incompatible with the structure that forms inthe mature 18S rRNA and may prevent premature folding of the pre-rRNA.In the Escherichia coli pre-rRNA the homologous region of the16S rRNA is also sequestered, in that case by base pairing tothe 5' external transcribed spacer (5' ETS). Cleavage at siteA₀ in the yeast 5' ETS strictly requires base pairing betweenU3 and a sequence within the 5' ETS. In contrast, the U3-18S interactionis not required for A₀ cleavage. U3 therefore carries out at leasttwo functionally distinct base pair interactions with the pre-rRNA.The nucleotide at the site of A₁ cleavage was shown to be specifiedby two distinct signals; one of these is the stem-loop structurewithin the 18S rRNA. However, in contrast to the efficiency ofcleavage, the position of A₁ cleavage is not dependent on theU3-loop interaction. We conclude that the 18S stem-loop structureis recognized at least twice during pre-rRNAprocessing.

^* Corresponding author. Mailing address: Institute of Cell and Molecular Biology, University of Edinburgh, King's Buildings,Edinburgh EH9 3JR, United Kingdom. Phone: 44 131 650 7092. Fax:44 131 650 7040. E-mail: d.tollervey{at}ed.ac.uk.

Molecular and Cellular Biology, September 1999, p. 6012-6019, Vol. 19, No. 9
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

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