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PMID: 17942741 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A bipartite U1 site represses U1A expression by synergizing with PIE to inhibit nuclear polyadenylation.

RNA (New York, N.Y.) ·Vol. 13 ·No. 12 ·2007-12-00 ·Pages 2129-40

Guan F, Caratozzolo RM, Goraczniak R, Ho ES, Gunderson SI

Abstract

U1A protein negatively autoregulates itself by polyadenylation inhibition of its own pre-mRNA by binding as two molecules to a 3'UTR-located Polyadenylation Inhibitory Element (PIE). The (U1A)2-PIE complex specifically blocks U1A mRNA biosynthesis by inhibiting polyA tail addition, leading to lower mRNA levels. U1 snRNP bound to a 5'ss-like sequence, which we call a U1 site, in the 3'UTRs of certain papillomaviruses leads to inhibition of viral late gene expression via a similar mechanism. Although such U1 sites can also be artificially used to potently silence reporter and endogenous genes, no naturally occurring U1 sites have been found in eukaryotic genes. Here we identify a conserved U1 site in the human U1A gene that is, unexpectedly, within a bipartite element where the other part represses the U1 site via a base-pairing mechanism. The bipartite element inhibits U1A expression via a synergistic action with the nearby PIE. Unexpectedly, synergy is not based on stabilizing binding of the inhibitory factors to the 3'UTR, but rather is a property of the larger ternary complex. Inhibition targets the biosynthetic step of polyA tail addition rather than altering mRNA stability. This is the first example of a functional U1 site in a cellular gene and of a single gene containing two dissimilar elements that inhibit nuclear polyadenylation. Parallels with other examples where U1 snRNP inhibits expression are discussed. We expect that other cellular genes will harbor functional U1 sites.

MeSH Terms
3' Untranslated Regions/genetics Animals Base Sequence Binding Sites Cell Nucleus/metabolism Cloning, Molecular Conserved Sequence DNA, Complementary/genetics Gene Expression Regulation Homeostasis Humans Mammals Molecular Sequence Data Plasmids/genetics Poly A/antagonists & inhibitors,metabolism RNA, Messenger/genetics RNA-Binding Proteins/chemistry,genetics,metabolism Ribonucleoprotein, U1 Small Nuclear/chemistry,genetics,metabolism Sequence Alignment Sequence Homology, Nucleic Acid
Chemicals
3' Untranslated Regions DNA, Complementary RNA, Messenger RNA-Binding Proteins Ribonucleoprotein, U1 Small Nuclear U1A protein Poly A
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Guan Fei
Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey 08854, USA.
Caratozzolo Rose M
Goraczniak Rafal
Ho Eric S
Gunderson Samuel I
References (37)
37 references, click to expand
  1. Inhibiting expression of specific genes in mammalian cells with 5' end-mutated U1 small nuclear RNAs targeted to terminal exons of pre-mRNA.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8264-9 PMID: 12826613
  2. The snRNP-associated U1A levels change following IL-6 stimulation of human B-cells.
    Mol Immunol. 2003 Mar;39(13):809-14 PMID: 12617996
  3. Preparation and fractionation of mammalian extracts active in pre-mRNA splicing.
    Methods Enzymol. 1990;181:3-19 PMID: 2381324
  4. Formation of mRNA 3' ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis.
    Microbiol Mol Biol Rev. 1999 Jun;63(2):405-45 PMID: 10357856
  5. U1A inhibits cleavage at the immunoglobulin M heavy-chain secretory poly(A) site by binding between the two downstream GU-rich regions.
    Mol Cell Biol. 2004 Jul;24(14):6162-71 PMID: 15226420
  6. Sequences homologous to 5' splice sites are required for the inhibitory activity of papillomavirus late 3' untranslated regions.
    Mol Cell Biol. 1994 Aug;14(8):5278-89 PMID: 8035806
  7. Elevated levels of the 64-kDa cleavage stimulatory factor (CstF-64) in lipopolysaccharide-stimulated macrophages influence gene expression and induce alternative poly(A) site selection.
    J Biol Chem. 2005 Dec 2;280(48):39950-61 PMID: 16207706
  8. Non-snRNP U1A levels decrease during mammalian B-cell differentiation and release the IgM secretory poly(A) site from repression.
    RNA. 2006 Jan;12(1):122-32 PMID: 16373497
  9. UTRdb and UTRsite: specialized databases of sequences and functional elements of 5' and 3' untranslated regions of eukaryotic mRNAs. Update 2002.
    Nucleic Acids Res. 2002 Jan 1;30(1):335-40 PMID: 11752330
  10. A history of poly A sequences: from formation to factors to function.
    Prog Nucleic Acid Res Mol Biol. 2002;71:285-389 PMID: 12102557
  11. Activity of the human papillomavirus type 16 late negative regulatory element is partly due to four weak consensus 5' splice sites that bind a U1 snRNP-like complex.
    J Virol. 2003 May;77(9):5167-77 PMID: 12692219
  12. Use of modified U1 snRNAs to inhibit HIV-1 replication.
    Nucleic Acids Res. 2007;35(1):247-55 PMID: 17158512
  13. Protein functions in pre-mRNA splicing.
    Curr Opin Cell Biol. 1997 Jun;9(3):320-8 PMID: 9159080
  14. The human U1 snRNP-specific U1A protein inhibits polyadenylation of its own pre-mRNA.
    Cell. 1993 Mar 26;72(6):881-92 PMID: 8458082
  15. The Caenorhabditis elegans histone hairpin-binding protein is required for core histone gene expression and is essential for embryonic and postembryonic cell division.
    J Cell Sci. 2002 Feb 15;115(Pt 4):857-66 PMID: 11865041
  16. Mechanisms of alternative pre-messenger RNA splicing.
    Annu Rev Biochem. 2003;72:291-336 PMID: 12626338
  17. Widespread mRNA polyadenylation events in introns indicate dynamic interplay between polyadenylation and splicing.
    Genome Res. 2007 Feb;17(2):156-65 PMID: 17210931
  18. The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation.
    Cell. 1996 Nov 29;87(5):941-52 PMID: 8945520
  19. Regulation of nuclear poly(A) addition controls the expression of immunoglobulin M secretory mRNA.
    EMBO J. 2001 Nov 15;20(22):6443-52 PMID: 11707415
  20. Identification of alternate polyadenylation sites and analysis of their tissue distribution using EST data.
    Genome Res. 2001 Sep;11(9):1520-6 PMID: 11544195
  21. Modulation of P-element pre-mRNA splicing by a direct interaction between PSI and U1 snRNP 70K protein.
    Mol Cell. 2001 Aug;8(2):363-73 PMID: 11545738
  22. Computational analysis of 3'-ends of ESTs shows four classes of alternative polyadenylation in human, mouse, and rat.
    Genome Res. 2005 Mar;15(3):369-75 PMID: 15741508
  23. Involvement of the carboxyl terminus of vertebrate poly(A) polymerase in U1A autoregulation and in the coupling of splicing and polyadenylation.
    Genes Dev. 1997 Mar 15;11(6):761-73 PMID: 9087430
  24. The cap-to-tail guide to mRNA turnover.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):237-46 PMID: 11283721
  25. Reduction of target gene expression by a modified U1 snRNA.
    Mol Cell Biol. 2001 Apr;21(8):2815-25 PMID: 11283260
  26. Regulation of splicing at an intermediate step in the formation of the spliceosome.
    Genes Dev. 1994 Jan;8(2):211-20 PMID: 8299940
  27. Determinants within an 18-amino-acid U1A autoregulatory domain that uncouple cooperative RNA binding, inhibition of polyadenylation, and homodimerization.
    Mol Cell Biol. 2003 May;23(9):3163-72 PMID: 12697817
  28. A large-scale analysis of mRNA polyadenylation of human and mouse genes.
    Nucleic Acids Res. 2005 Jan 12;33(1):201-12 PMID: 15647503
  29. Intracellular distribution of the U1A protein depends on active transport and nuclear binding to U1 snRNA.
    J Cell Biol. 1992 Jul;118(1):11-21 PMID: 1618898
  30. Regulation of alternative polyadenylation by U1 snRNPs and SRp20.
    Mol Cell Biol. 1998 Sep;18(9):4977-85 PMID: 9710581
  31. Regulation of mRNA stability in mammalian cells.
    Gene. 2001 Mar 7;265(1-2):11-23 PMID: 11255003
  32. The human U1A snRNP protein regulates polyadenylation via a direct interaction with poly(A) polymerase.
    Cell. 1994 Feb 11;76(3):531-41 PMID: 8313473
  33. Downstream sequence elements with different affinities for the hnRNP H/H' protein influence the processing efficiency of mammalian polyadenylation signals.
    Nucleic Acids Res. 2002 Apr 15;30(8):1842-50 PMID: 11937639
  34. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  35. U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase.
    Mol Cell. 1998 Jan;1(2):255-64 PMID: 9659922
  36. Stem-loop 1 of the U1 snRNP plays a critical role in the suppression of HIV-1 polyadenylation.
    RNA. 2000 Feb;6(2):170-7 PMID: 10688356
  37. Analysis of a noncanonical poly(A) site reveals a tripartite mechanism for vertebrate poly(A) site recognition.
    Genes Dev. 2005 Jun 1;19(11):1315-27 PMID: 15937220
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1469-9001
Published
2007-12-00
Epub
2007-00-17
Pages
2129-40
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC2080603
Subset
IM
Grants
NIGMS NIH HHS · R01 GM057286 · United States
NIGMS NIH HHS · GM057286 · United States
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