Home LiteratureArticle Details
PMID: 10999605 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Effect of 3' terminal adenylic acid residue on the uridylation of human small RNAs in vitro and in frog oocytes.

RNA (New York, N.Y.) ·Vol. 6 ·No. 9 ·2000-09-00 ·Pages 1277-88

Chen Y, Sinha K, Perumal K, Reddy R

Abstract

It is known that several small RNAs including human and Xenopus signal recognition particle (SRP) RNA, U2 small nuclear RNA (snRNA) and 7SK RNAs are posttranscriptionally adenylated, whereas U6 snRNA and ribosomal 5S RNA are posttranscriptionally uridylated on their 3' ends. In this study, we provide evidence that a small fraction of U6 snRNA and 5S ribosomal RNA molecules from human as well as Xenopus oocytes contain a single posttranscriptionally added adenylic acid residue on their 3' ends. These data show that U6 snRNA and 5S rRNAs are posttranscriptionally modified on their 3' ends by both uridylation and adenylation. Although the SRP RNA, 7SK RNA, 5S RNA, and U6 snRNA with the uridylic acid residue on their 3' ends were readily uridylated, all these RNAs with posttranscriptionally added adenylic acid residue on their 3' ends were not uridylated in vitro, or when U6 snRNA with 3' A(OH) was injected into Xenopus oocytes. These results show that the presence of a single posttranscriptionally added adenylic acid residue on the 3' end of SRP RNA, U6 snRNA, 5S rRNA, or 7SK RNA prevents 3' uridylation. These data also show that adenylation and uridylation are two competing processes that add nucleotides on the 3' end of some small RNAs and suggest that one of the functions of the 3' adenylation may be to negatively affect the 3' uridylation of small RNAs.

MeSH Terms
Adenosine Monophosphate/metabolism Alu Elements/physiology Animals HeLa Cells Humans Oocytes RNA Processing, Post-Transcriptional RNA, Ribosomal, 5S/metabolism RNA, Small Nuclear/chemistry,metabolism Signal Recognition Particle/genetics Transfection Uridine/metabolism Uridine Monophosphate/metabolism Xenopus
Chemicals
RNA, Ribosomal, 5S RNA, Small Nuclear Signal Recognition Particle Adenosine Monophosphate Uridine Monophosphate Uridine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chen Y
Department of Pharmacology, Baylor College of Medicine, Houston, Texas 77030, USA.
Sinha K
Perumal K
Reddy R
References (54)
54 references, click to expand
  1. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  2. Post-transcriptional adenylation of signal recognition particle RNA is carried out by an enzyme different from mRNA Poly(A) polymerase.
    J Biol Chem. 1999 Oct 22;274(43):30826-31 PMID: 10521474
  3. Association of the lupus antigen La with a subset of U6 snRNA molecules.
    Nucleic Acids Res. 1985 Apr 11;13(7):2617-29 PMID: 2582364
  4. Animal mitochondrial DNA: an extreme example of genetic economy.
    Int Rev Cytol. 1985;93:93-145 PMID: 3891661
  5. Formation of the 3' end of U1 snRNA is directed by a conserved sequence located downstream of the coding region.
    EMBO J. 1985 Jul;4(7):1827-37 PMID: 2411548
  6. U6 small nuclear RNA is transcribed by RNA polymerase III.
    Proc Natl Acad Sci U S A. 1986 Nov;83(22):8575-9 PMID: 3464970
  7. The capped U6 small nuclear RNA is transcribed by RNA polymerase III.
    J Biol Chem. 1987 Jan 5;262(1):75-81 PMID: 3793736
  8. Accurate and efficient 3' processing of U2 small nuclear RNA precursor in a fractionated cytoplasmic extract.
    Mol Cell Biol. 1987 Sep;7(9):3131-7 PMID: 3670307
  9. The exosome: a proteasome for RNA?
    Cell. 1999 Nov 12;99(4):347-50 PMID: 10571176
  10. Evolutionary conservation of post-transcriptional 3' end adenylation of small RNAs: S. cerevisiae signal recognition particle RNA and U2 small nuclear RNA are post-transcriptionally adenylated.
    Mol Cell Biochem. 2000 May;208(1-2):99-109 PMID: 10939633
  11. [Biochemical research on oogenesis. 7. Synthesis and maturation of 5S RNA in the small oocytes of Xenopus laevis].
    Biochimie. 1973;55(9):1137-51 PMID: 4799005
  12. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  13. Use of in vitro 32P labeling in the sequence analysis of nonradioactive tRNAs.
    Methods Enzymol. 1979;59:58-109 PMID: 220499
  14. Faithful transcription of eukaryotic genes by RNA polymerase III in systems reconstituted with purified DNA templates.
    J Biol Chem. 1979 Jul 10;254(13):6163-73 PMID: 447704
  15. Specific labeling of 3' termini of RNA with T4 RNA ligase.
    Methods Enzymol. 1980;65(1):65-74 PMID: 6154874
  16. Terminal uridylyl transferase of Vigna unguiculata: purification and characterization of an enzyme catalyzing the addition of a single UMP residue to the 3'-end of an RNA primer.
    Nucleic Acids Res. 1981 Jun 11;9(11):2433-53 PMID: 6269049
  17. Newly synthesized small nuclear RNAs appear transiently in the cytoplasm.
    J Mol Biol. 1988 Jan 20;199(2):259-67 PMID: 3351925
  18. Upstream regulatory elements are necessary and sufficient for transcription of a U6 RNA gene by RNA polymerase III.
    EMBO J. 1988 Feb;7(2):503-12 PMID: 3366121
  19. Uridylation of U6 RNA in a nuclear extract in Ehrlich ascites tumor cells.
    J Biochem. 1988 Dec;104(6):991-4 PMID: 3243771
  20. Gamma-monomethyl phosphate: a cap structure in spliceosomal U6 small nuclear RNA.
    Proc Natl Acad Sci U S A. 1989 Nov;86(21):8280-3 PMID: 2813391
  21. Determination of RNA-protein and RNA-ribonucleoprotein interactions by nuclease probing.
    Methods Enzymol. 1989;180:454-68 PMID: 2482428
  22. An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus.
    Science. 1990 Aug 17;249(4970):786-90 PMID: 2143847
  23. Ribonucleases, tRNA nucleotidyltransferase, and the 3' processing of tRNA.
    Prog Nucleic Acid Res Mol Biol. 1990;39:209-40 PMID: 2247609
  24. Nuclear processing of the 3'-terminal nucleotides of pre-U1 RNA in Xenopus laevis oocytes.
    Mol Cell Biol. 1992 Apr;12(4):1553-60 PMID: 1549111
  25. Cyclic 2',3'-phosphates and nontemplated nucleotides at the 3' end of spliceosomal U6 small nuclear RNA's.
    Science. 1992 Jan 17;255(5042):327-30 PMID: 1549778
  26. 3'-end-dependent formation of U6 small nuclear ribonucleoprotein particles in Xenopus laevis oocyte nuclei.
    Mol Cell Biol. 1992 Jul;12(7):3032-40 PMID: 1535684
  27. Formation of the 3' end of sea urchin U1 small nuclear RNA occurs independently of the conserved 3' box and on transcripts initiated from a histone promoter.
    Mol Cell Biol. 1992 Sep;12(9):4132-41 PMID: 1508209
  28. Transcription and replication of animal mitochondrial DNAs.
    Int Rev Cytol. 1992;141:217-32 PMID: 1452432
  29. Poly(U)-binding protein inhibits Drosophila pre-5 S RNA 3'-exonuclease digestion.
    J Biol Chem. 1993 Jun 5;268(16):11553-7 PMID: 8389357
  30. Methylphosphate cap structure increases the stability of 7SK, B2 and U6 small RNAs in Xenopus oocytes.
    Nucleic Acids Res. 1993 Oct 11;21(20):4756-61 PMID: 8233824
  31. Characterization of two classes of ribonucleoprotein complexes possibly involved in RNA editing from Leishmania tarentolae mitochondria.
    EMBO J. 1994 Apr 1;13(7):1664-72 PMID: 7512500
  32. No end yet to messenger RNA 3' processing!
    Cell. 1995 Jun 16;81(6):829-32 PMID: 7781059
  33. A complex protein assembly catalyzes polyadenylation of mRNA precursors.
    Curr Opin Genet Dev. 1995 Apr;5(2):222-8 PMID: 7613093
  34. A possible role for the guide RNA U-tail as a specificity determinant in formation of guide RNA-messenger RNA chimeras in mitochondrial extracts of Crithidia fasciculata.
    Mol Biochem Parasitol. 1995 Jul;73(1-2):211-22 PMID: 8577329
  35. Mechanism and evolution of RNA editing in kinetoplastida.
    Biochim Biophys Acta. 1996 Jun 3;1307(1):39-54 PMID: 8652667
  36. Trypanosome RNA editing: resolved.
    Science. 1996 Aug 30;273(5279):1182-3 PMID: 8787123
  37. Identification and characterization of a nuclease specific for the 3' end of the U6 small nuclear RNA.
    J Biol Chem. 1997 Jan 10;272(2):984-91 PMID: 8995392
  38. RNA editing in kinetoplastid protozoa.
    Microbiol Mol Biol Rev. 1997 Mar;61(1):105-20 PMID: 9106367
  39. Formation of 2',3'-cyclic phosphates at the 3' end of human U6 small nuclear RNA in vitro. Identification of 2',3'-cyclic phosphates at the 3' ends of human signal recognition particle and mitochondrial RNA processing RNAs.
    J Biol Chem. 1997 Aug 29;272(35):21989-93 PMID: 9268336
  40. Nuclear transport of RNAs in microinjected Xenopus oocytes.
    Methods Cell Biol. 1998;53:559-89 PMID: 9348525
  41. The mechanism of U insertion/deletion RNA editing in kinetoplastid mitochondria.
    Nucleic Acids Res. 1997 Oct 1;25(19):3751-9 PMID: 9380494
  42. The exosome: a conserved eukaryotic RNA processing complex containing multiple 3'-->5' exoribonucleases.
    Cell. 1997 Nov 14;91(4):457-66 PMID: 9390555
  43. Adenylation of small RNAs in human cells. Development of a cell-free system for accurate adenylation on the 3'-end of human signal recognition particle RNA.
    J Biol Chem. 1998 Mar 20;273(12):6853-9 PMID: 9506988
  44. A highly specific terminal uridylyl transferase modifies the 3'-end of U6 small nuclear RNA.
    Nucleic Acids Res. 1998 Jul 1;26(13):3119-26 PMID: 9628908
  45. In vivo expression of a variant human U6 RNA from a unique, internal promoter.
    Biochemistry. 1998 Sep 15;37(37):12943-51 PMID: 9737874
  46. Polyadenylation of stable RNA precursors in vivo.
    Proc Natl Acad Sci U S A. 1998 Oct 13;95(21):12158-62 PMID: 9770456
  47. Accurate 3' end processing and adenylation of human signal recognition particle RNA and alu RNA in vitro.
    J Biol Chem. 1998 Dec 25;273(52):35023-31 PMID: 9857035
  48. Mapping contacts between gRNA and mRNA in trypanosome RNA editing.
    Nucleic Acids Res. 1999 Feb 1;27(3):778-87 PMID: 9889273
  49. 3'-Terminal RNA structures and poly(U) tracts inhibit initiation by a 3'-->5' exonuclease in vitro.
    Nucleic Acids Res. 1999 Feb 15;27(4):1159-67 PMID: 9927751
  50. Characterization of Sm-like proteins in yeast and their association with U6 snRNA.
    EMBO J. 1999 Aug 2;18(15):4321-31 PMID: 10428970
  51. The yeast exosome and human PM-Scl are related complexes of 3' --> 5' exonucleases.
    Genes Dev. 1999 Aug 15;13(16):2148-58 PMID: 10465791
  52. Functions of the exosome in rRNA, snoRNA and snRNA synthesis.
    EMBO J. 1999 Oct 1;18(19):5399-410 PMID: 10508172
  53. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3'-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro.
    EMBO J. 1999 Oct 15;18(20):5789-802 PMID: 10523320
  54. Poliovirus replicase stimulation by terminal uridylyl transferase.
    J Biol Chem. 1985 Jun 25;260(12):7628-35 PMID: 2987262
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1355-8382
Published
2000-09-00
Pages
1277-88
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC1370001
Subset
IM
Grants
NIGMS NIH HHS · GM 38320 · United States
NIGMS NIH HHS · GM 52901 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com