Nucleolar localization signals of Box H/ACA small nucleolar RNAs

The two major families of small nucleolar RNAs (snoRNAs), Box C/D and Box H/ACA, are generated in the nucleoplasm and transported to the nucleolus where they function in rRNA processing and modification. We have investigated the sequences involved in the intranuclear transport of Box H/ACA snoRNAs by assaying the localization of injected fluorescent RNAs in Xenopus oocyte nuclear spreads. Our analysis of U17, U64 and U65 has revealed that disruption of either of the conserved sequence elements, Box H or Box ACA, eliminates nucleolar localization. In addition, the stem present at the base of the 3′ hairpin is required for efficient nucleolar localization of U65. Fragments or rearrangements of U65 that consist of Box H and Box ACA flanking either the 5′ or 3′ hairpin are targeted to the nucleolus. The targeting is dependent on the presence of the Box sequences, but not on their orientation. Our results indicate that in each of the two major families of snoRNAs, a motif composed of the signature conserved sequences and an adjacent structural element that tethers the sequence elements directs the nucleolar localization of the RNAs. We demonstrate that telomerase RNA is also targeted to the nucleolus by a Box ACA‐dependent mechanism.

[1]  R. Terns,et al.  Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli. , 1999, Molecular biology of the cell.

[2]  D. Tollervey,et al.  Nop58p is a common component of the box C+D snoRNPs that is required for snoRNA stability. , 1999, RNA.

[3]  Liang-Hu Qu,et al.  Seven Novel Methylation Guide Small Nucleolar RNAs Are Processed from a Common Polycistronic Transcript by Rat1p and RNase III in Yeast , 1999, Molecular and Cellular Biology.

[4]  Tamás Kiss,et al.  Elements essential for accumulation and function of small nucleolar RNAs directing site‐specific pseudouridylation of ribosomal RNAs , 1999, The EMBO journal.

[5]  Jeffrey B. Cheng,et al.  A Box H/ACA Small Nucleolar RNA-Like Domain at the Human Telomerase RNA 3′ End , 1999, Molecular and Cellular Biology.

[6]  M. Mann,et al.  Cbf5p, a potential pseudouridine synthase, and Nhp2p, a putative RNA-binding protein, are present together with Gar1p in all H BOX/ACA-motif snoRNPs and constitute a common bipartite structure. , 1998, RNA.

[7]  M. Caizergues-Ferrer,et al.  Nhp2p and Nop10p are essential for the function of H/ACA snoRNPs , 1998, The EMBO journal.

[8]  P J Shaw,et al.  Localization and processing from a polycistronic precursor of novel snoRNAs in maize. , 1998, Journal of cell science.

[9]  R. Singer,et al.  The snoRNA box C/D motif directs nucleolar targeting and also couples snoRNA synthesis and localization , 1998, The EMBO journal.

[10]  J. Brockenbrough,et al.  Nop5p Is a Small Nucleolar Ribonucleoprotein Component Required for Pre-18 S rRNA Processing in Yeast* , 1998, The Journal of Biological Chemistry.

[11]  E. Maxwell,et al.  In vitro assembly of the mouse U14 snoRNP core complex and identification of a 65-kDa box C/D-binding protein. , 1998, RNA.

[12]  D. Tollervey,et al.  The box H + ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase. , 1998, Genes & development.

[13]  A. Fatica,et al.  In Vivo Identification of Nuclear Factors Interacting with the Conserved Elements of Box C/D Small Nucleolar RNAs , 1998, Molecular and Cellular Biology.

[14]  Maurille J. Fournier,et al.  The Pseudouridine Residues of rRNA: Number, Location, Biosynthesis, and Function , 1998 .

[15]  D. Goldfarb,et al.  Nuclear transport of RNAs in microinjected Xenopus oocytes. , 1998, Methods in cell biology.

[16]  A. Matera,et al.  Human genes encoding U3 snRNA associate with coiled bodies in interphase cells and are clustered on chromosome 17p11.2 in a complex inverted repeat structure. , 1997, Nucleic acids research.

[17]  D. Tollervey,et al.  Function and synthesis of small nucleolar RNAs. , 1997, Current opinion in cell biology.

[18]  Tamás Kiss,et al.  Site-Specific Pseudouridine Formation in Preribosomal RNA Is Guided by Small Nucleolar RNAs , 1997, Cell.

[19]  J. Steitz,et al.  Sno Storm in the Nucleolus: New Roles for Myriad Small RNPs , 1997, Cell.

[20]  J. Ni,et al.  Small Nucleolar RNAs Direct Site-Specific Synthesis of Pseudouridine in Ribosomal RNA , 1997, Cell.

[21]  T. Kiss,et al.  The family of box ACA small nucleolar RNAs is defined by an evolutionarily conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation. , 1997, Genes & development.

[22]  J. Brown,et al.  Intracellular localization and unique conserved sequences of three small nucleolar RNAs. , 1997, Nucleic acids research.

[23]  J Ofengand,et al.  Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts. , 1997, Journal of molecular biology.

[24]  J. Gall,et al.  "Micronucleoli" in the Xenopus germinal vesicle. , 1997, Chromosoma.

[25]  E. Maxwell,et al.  5'ETS rRNA processing facilitated by four small RNAs: U14, E3, U17, and U3. , 1996, RNA.

[26]  Laurie Smith,et al.  The RNA World of the Nucleolus: Two Major Families of Small RNAs Defined by Different Box Elements with Related Functions , 1996, Cell.

[27]  C. Murphy,et al.  The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes. , 1996, RNA.

[28]  J. Bachellerie,et al.  Intron-encoded, antisense small nucleolar RNAs: the characterization of nine novel species points to their direct role as guides for the 2'-O-ribose methylation of rRNAs. , 1996, Journal of molecular biology.

[29]  Tamás Kiss,et al.  Site-Specific Ribose Methylation of Preribosomal RNA: A Novel Function for Small Nucleolar RNAs , 1996, Cell.

[30]  W. Filipowicz,et al.  Characterization of the intron-encoded U19 RNA, a new mammalian small nucleolar RNA that is not associated with fibrillarin , 1996, Molecular and cellular biology.

[31]  D. Tollervey,et al.  Processing of pre‐ribosomal RNA in Saccharomyces cerevisiae , 1995, Yeast.

[32]  J. Ofengand,et al.  The pseudouridine residues of ribosomal RNA. , 1995, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[33]  M. Terns,et al.  A common maturation pathway for small nucleolar RNAs. , 1995, The EMBO journal.

[34]  M. Fournier,et al.  The small nucleolar RNAs. , 1995, Annual review of biochemistry.

[35]  J. Ofengand,et al.  Pseudouridine and O2'-methylated nucleosides. Significance of their selective occurrence in rRNA domains that function in ribosome-catalyzed synthesis of the peptide bonds in proteins. , 1995, Biochimie.

[36]  F. Cecconi,et al.  The Xenopus intron-encoded U17 snoRNA is produced by exonucleolytic processing of its precursor in oocytes. , 1995, Nucleic acids research.

[37]  G. Blobel,et al.  NAP57, a mammalian nucleolar protein with a putative homolog in yeast and bacteria [published erratum appears in J Cell Biol 1998 Jan 26;140(2):447] , 1994, The Journal of cell biology.

[38]  Andrei V Bakin,et al.  Clustering of pseudouridine residues around the peptidyltransferase center of yeast cytoplasmic and mitochondrial ribosomes. , 1994, Biochemistry.

[39]  M. Terns,et al.  Retention and 5' cap trimethylation of U3 snRNA in the nucleus. , 1994, Science.

[40]  S. Turley,et al.  Selective induction of anti‐fibrillarin autoantibodies by silver nitrate in mice , 1994, Clinical and experimental immunology.

[41]  F. Cecconi,et al.  U17XS8, a small nucleolar RNA with a 12 nt complementarity to 18S rRNA and coded by a sequence repeated in the six introns of Xenopus laevis ribosomal protein S8 gene. , 1994, Nucleic acids research.

[42]  W. Boelens,et al.  Nuclear export of different classes of RNA is mediated by specific factors , 1994, The Journal of cell biology.

[43]  D. Eichler,et al.  Processing of eukaryotic ribosomal RNA. , 1994, Progress in nucleic acid research and molecular biology.

[44]  U. Scheer,et al.  The nucleolus. , 1994, Current opinion in cell biology.

[45]  B. Sollner-Webb,et al.  Novel intron-encoded small nucleolar RNAs , 1993, Cell.

[46]  R. Tuma,et al.  Identification and characterization of a sphere organelle protein , 1993, The Journal of cell biology.

[47]  C. Murphy,et al.  Chapter 8 Lampbrush Chromosomes , 1991 .

[48]  B. Maden The numerous modified nucleotides in eukaryotic ribosomal RNA. , 1990, Progress in nucleic acid research and molecular biology.

[49]  D. Tollervey,et al.  A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. , 1989, The EMBO journal.

[50]  H. Busch,et al.  Human U3 small nucleolar RNA genes are localized to the nucleoplasm. , 1987, Biochemical and biophysical research communications.

[51]  Professor Dr. Harold Garnet Callan Lampbrush Chromosomes , 1986, Molecular Biology, Biochemistry and Biophysics.

[52]  Prof. Dr. Asen A. Hadjiolov The Nucleolus and Ribosome Biogenesis , 1985, Cell Biology Monographs.