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PMID: 11509664 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Xenopus U3 snoRNA GAC-Box A' and Box A sequences play distinct functional roles in rRNA processing.

Molecular and cellular biology ·Vol. 21 ·No. 18 ·2001-09-00 ·Pages 6210-21

Borovjagin AV, Gerbi SA

Abstract

Mutations in the 5' portion of Xenopus U3 snoRNA were tested for function in oocytes. The results revealed a new cleavage site (A0) in the 3' region of vertebrate external transcribed spacer sequences. In addition, U3 mutagenesis uncoupled cleavage at sites 1 and 2, flanking the 5' and 3' ends of 18S rRNA, and generated novel intermediates: 19S and 18.5S pre-rRNAs. Furthermore, specific nucleotides in Xenopus U3 snoRNA that are required for cleavages in pre-rRNA were identified: box A is essential for site A0 cleavage, the GAC-box A' region is necessary for site 1 cleavage, and the 3' end of box A' and flanking nucleotides are required for site 2 cleavage. Differences between metazoan and yeast U3 snoRNA-mediated rRNA processing are enumerated. The data support a model where metazoan U3 snoRNA acts as a bridge to draw together the 5' and 3' ends of the 18S rRNA coding region within pre-rRNA to coordinate their cleavage.

MeSH Terms
Animals Base Sequence Gene Expression Regulation Molecular Sequence Data RNA Processing, Post-Transcriptional RNA, Ribosomal/genetics,metabolism RNA, Small Nucleolar/genetics,metabolism Sequence Analysis, RNA Xenopus laevis/genetics,metabolism
Chemicals
RNA, Ribosomal RNA, Small Nucleolar RNA, U3 small nucleolar
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Borovjagin A V
Division of Biology and Medicine, Brown University, Providence, Rhode Island 02912, USA.
Gerbi S A
References (55)
55 references, click to expand
  1. The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast.
    J Biol Chem. 1973 Feb 25;248(4):1412-6 PMID: 4568815
  2. Nucleolar factors direct the 2'-O-ribose methylation and pseudouridylation of U6 spliceosomal RNA.
    Mol Cell Biol. 1999 Oct;19(10):6906-17 PMID: 10490628
  3. Small nuclear RNAs and RNA processing.
    Prog Nucleic Acid Res Mol Biol. 1983;30:127-62 PMID: 6198692
  4. Two distinct recognition signals define the site of endonucleolytic cleavage at the 5'-end of yeast 18S rRNA.
    EMBO J. 1995 Oct 2;14(19):4883-92 PMID: 7588617
  5. Processing of the yeast pre-rRNA at sites A(2) and A(3) is linked.
    RNA. 1996 Jan;2(1):63-73 PMID: 8846297
  6. RNase III cleaves eukaryotic preribosomal RNA at a U3 snoRNP-dependent site.
    Cell. 1996 Apr 5;85(1):115-24 PMID: 8620530
  7. Accurate processing of a eukaryotic precursor ribosomal RNA by ribonuclease MRP in vitro.
    Science. 1996 Apr 12;272(5259):268-70 PMID: 8602511
  8. Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA.
    J Mol Biol. 1996 Jun 21;259(4):645-54 PMID: 8683571
  9. Small nucleolar RNA.
    Biochem Cell Biol. 1995 Nov-Dec;73(11-12):845-58 PMID: 8722000
  10. RRP5 is required for formation of both 18S and 5.8S rRNA in yeast.
    EMBO J. 1996 Oct 15;15(20):5701-14 PMID: 8896463
  11. Characterization of three sites of RNA 3' end formation in the Xenopus ribosomal gene spacer.
    Cell. 1986 May 9;45(3):431-43 PMID: 3453104
  12. Primary processing of mammalian rRNA involves two adjacent cleavages and is not species specific.
    Mol Cell Biol. 1987 Aug;7(8):2891-8 PMID: 3670298
  13. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA.
    EMBO J. 1987 Dec 20;6(13):4169-75 PMID: 3327689
  14. Nucleotide sequence determination and secondary structure of Xenopus U3 snRNA.
    Nucleic Acids Res. 1988 Mar 25;16(5):2127-48 PMID: 3357768
  15. Accurate processing of human pre-rRNA in vitro.
    Mol Cell Biol. 1989 Oct;9(10):4422-31 PMID: 2586517
  16. Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Mar;10(3):1145-52 PMID: 2406561
  17. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing.
    Cell. 1990 Mar 23;60(6):897-908 PMID: 2156625
  18. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing.
    EMBO J. 1990 Jul;9(7):2299-308 PMID: 2357971
  19. Xenopus borealis and Xenopus laevis 28S ribosomal DNA and the complete 40S ribosomal precursor RNA coding units of both species.
    Proc Biol Sci. 1991 Jul 22;245(1312):65-71 PMID: 1682930
  20. 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 Dec;10(13):4231-9 PMID: 1756730
  21. Preribosomal RNA processing in Xenopus oocytes does not include cleavage within the external transcribed spacer as an early step.
    Biochimie. 1991 Jun;73(6):805-12 PMID: 1764525
  22. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA.
    EMBO J. 1992 Apr;11(4):1531-42 PMID: 1563354
  23. Sequence requirements for maturation of the 5' terminus of human 18 S rRNA in vitro.
    J Biol Chem. 1992 May 5;267(13):9264-8 PMID: 1577760
  24. Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis.
    Mol Cell Biol. 1993 Apr;13(4):2469-77 PMID: 8455623
  25. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte.
    Cell. 1993 Jun 18;73(6):1233-45 PMID: 8513505
  26. A U3 small nuclear ribonucleoprotein-requiring processing event in the 5' external transcribed spacer of Xenopus precursor rRNA.
    Mol Cell Biol. 1993 Oct;13(10):5990-8 PMID: 8413202
  27. Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Dec;13(12):7935-41 PMID: 8247008
  28. The RNA of RNase MRP is required for normal processing of ribosomal RNA.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):659-63 PMID: 8290578
  29. The 5' end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site.
    EMBO J. 1994 May 15;13(10):2452-63 PMID: 7515008
  30. Requirement for intron-encoded U22 small nucleolar RNA in 18S ribosomal RNA maturation.
    Science. 1994 Dec 2;266(5190):1558-61 PMID: 7985025
  31. Birth of the snoRNPs: the evolution of RNase MRP and the eukaryotic pre-rRNA-processing system.
    Trends Biochem Sci. 1995 Feb;20(2):78-82 PMID: 7701567
  32. U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing.
    Genes Dev. 1995 Oct 1;9(19):2433-43 PMID: 7557394
  33. Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis.
    EMBO J. 1995 Sep 1;14(17):4350-6 PMID: 7556076
  34. 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 Oct 31;273(3):552-71 PMID: 9356246
  35. Functional separation of pre-rRNA processing steps revealed by truncation of the U3 small nucleolar ribonucleoprotein component, Mpp10.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13536-41 PMID: 9391061
  36. Functional mapping of the U3 small nucleolar RNA from the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1998 Jun;18(6):3431-44 PMID: 9584183
  37. Conserved boxes C and D are essential nucleolar localization elements of U14 and U8 snoRNAs.
    EMBO J. 1998 Jun 1;17(11):3176-87 PMID: 9606199
  38. Nucleolar localization elements of Xenopus laevis U3 small nucleolar RNA.
    Mol Biol Cell. 1998 Oct;9(10):2973-85 PMID: 9763456
  39. Essential structural features in the Schizosaccharomyces pombe pre-rRNA 5' external transcribed spacer.
    J Mol Biol. 1999 Feb 26;286(3):695-708 PMID: 10024444
  40. 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 Mar 12;286(5):1347-63 PMID: 10064702
  41. The 5' end of the 18S rRNA can be positioned from within the mature rRNA.
    RNA. 1999 May;5(5):678-86 PMID: 10334338
  42. The roles of Rrp5p in the synthesis of yeast 18S and 5.8S rRNA can be functionally and physically separated.
    RNA. 1999 Jun;5(6):779-93 PMID: 10376877
  43. 5'ETS rRNA processing facilitated by four small RNAs: U14, E3, U17, and U3.
    RNA. 1996 Nov;2(11):1094-9 PMID: 8903340
  44. Formation of the 5' end pseudoknot in small subunit ribosomal RNA: involvement of U3-like sequences.
    RNA. 1997 Apr;3(4):337-43 PMID: 9085841
  45. Three small nucleolar RNAs that are involved in ribosomal RNA precursor processing.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):4972-7 PMID: 9144174
  46. Ribosome synthesis in Saccharomyces cerevisiae.
    Annu Rev Genet. 1999;33:261-311 PMID: 10690410
  47. Rcl1p, the yeast protein similar to the RNA 3'-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis.
    EMBO J. 2000 May 2;19(9):2115-26 PMID: 10790377
  48. The spacing between functional Cis-elements of U3 snoRNA is critical for rRNA processing.
    J Mol Biol. 2000 Jun 30;300(1):57-74 PMID: 10864498
  49. Dhr1p, a putative DEAH-box RNA helicase, is associated with the box C+D snoRNP U3.
    Mol Cell Biol. 2000 Oct;20(19):7238-46 PMID: 10982841
  50. Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli.
    Mol Biol Cell. 1999 Jul;10(7):2131-47 PMID: 10397754
  51. Yeast Rnt1p is required for cleavage of the pre-ribosomal RNA in the 3' ETS but not the 5' ETS.
    RNA. 1999 Jul;5(7):909-17 PMID: 10411134
  52. Imp3p and Imp4p, two specific components of the U3 small nucleolar ribonucleoprotein that are essential for pre-18S rRNA processing.
    Mol Cell Biol. 1999 Aug;19(8):5441-52 PMID: 10409734
  53. Base pairing between U3 small nucleolar RNA and the 5' end of 18S rRNA is required for pre-rRNA processing.
    Mol Cell Biol. 1999 Sep;19(9):6012-9 PMID: 10454548
  54. Two 5'-ETS regions implicated in interactions with U3 snoRNA are required for small subunit rRNA maturation in Trypanosoma brucei.
    Nucleic Acids Res. 1999 Aug 15;27(16):3300-9 PMID: 10454637
  55. Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA.
    Proc Natl Acad Sci U S A. 1978 Aug;75(8):3593-7 PMID: 358189
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2001-09-00
Pages
6210-21
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC87338
Subset
IM
Grants
NIGMS NIH HHS · R01 GM061945 · United States
NIGMS NIH HHS · GM 61945 · United States
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