Home LiteratureArticle Details
PMID: 9716405 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The upstream sequence element of the C2 complement poly(A) signal activates mRNA 3' end formation by two distinct mechanisms.

Genes & development ·Vol. 12 ·No. 16 ·1998-08-15 ·Pages 2522-34

Moreira A, Takagaki Y, Brackenridge S, Wollerton M, Manley JL, Proudfoot NJ

Abstract

The poly(A) signal of the C2 complement gene is unusual in that it possesses an upstream sequence element (USE) required for full activity in vivo. We describe here in vitro experiments demonstrating that this USE enhances both the cleavage and poly(A) addition reactions. We also show that the C2 USE can be cross-linked efficiently to a 55-kD protein that we identify as the polypyrimidine tract-binding protein (PTB), implicated previously in modulation of pre-mRNA splicing. Mutation of the PTB-binding site significantly reduces the efficiency of the C2 poly(A) site both in vivo and in vitro. Furthermore, addition of PTB to reconstituted processing reactions enhances cleavage at the C2 poly(A) site, indicating that PTB has a direct role in recognition of this signal. The C2 USE, however, also increases the affinity of general polyadenylation factors independently for the C2 poly(A) signal as detected by enhanced binding of cleavage-stimulaton factor (CstF). Strikingly, this leads to a novel CstF-dependant enhancement of the poly(A) synthesis phase of the reaction. These studies both emphasize the interconnection between splicing and polyadenylation and indicate an unexpected flexibility in the organization of mammalian poly(A) sites.

MeSH Terms
Binding Sites Complement C2/genetics Humans Mutation Poly A/metabolism Polypyrimidine Tract-Binding Protein Promoter Regions, Genetic RNA Splicing RNA, Messenger/biosynthesis,metabolism,physiology RNA-Binding Proteins/genetics,metabolism,physiology Recombinant Proteins/metabolism Ribonucleoproteins/genetics,metabolism Transcriptional Activation mRNA Cleavage and Polyadenylation Factors
Chemicals
Complement C2 RNA, Messenger RNA-Binding Proteins Recombinant Proteins Ribonucleoproteins mRNA Cleavage and Polyadenylation Factors Polypyrimidine Tract-Binding Protein Poly A
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Moreira A
Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, UK.
Takagaki Y
Brackenridge S
Wollerton M
Manley J L
Proudfoot N J
References (75)
75 references, click to expand
  1. Cell-specific expression of the human complement protein factor B gene: evidence for the role of two distinct 5'-flanking elements.
    Cell. 1987 Jan 30;48(2):331-42 PMID: 3643061
  2. A polyadenylation factor subunit is the human homologue of the Drosophila suppressor of forked protein.
    Nature. 1994 Dec 1;372(6505):471-4 PMID: 7984242
  3. RNA14 and RNA15 proteins as components of a yeast pre-mRNA 3'-end processing factor.
    Science. 1994 Dec 9;266(5191):1702-5 PMID: 7992054
  4. CPSF recognition of an HIV-1 mRNA 3'-processing enhancer: multiple sequence contacts involved in poly(A) site definition.
    Genes Dev. 1995 Jan 1;9(1):72-83 PMID: 7828853
  5. Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins.
    Science. 1995 May 26;268(5214):1173-6 PMID: 7761834
  6. Upstream sequence elements enhance poly(A) site efficiency of the C2 complement gene and are phylogenetically conserved.
    EMBO J. 1995 Aug 1;14(15):3809-19 PMID: 7641699
  7. The 160-kD subunit of human cleavage-polyadenylation specificity factor coordinates pre-mRNA 3'-end formation.
    Genes Dev. 1995 Nov 1;9(21):2672-83 PMID: 7590244
  8. Regulation of alternative 3' splice site selection by constitutive splicing factors.
    RNA. 1995 May;1(3):234-45 PMID: 7489496
  9. Poly(A) site selection in the HIV-1 provirus: inhibition of promoter-proximal polyadenylation by the downstream major splice donor site.
    Genes Dev. 1995 Dec 1;9(23):3008-25 PMID: 7498796
  10. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA.
    RNA. 1995 Nov;1(9):924-38 PMID: 8548657
  11. An intron enhancer recognized by splicing factors activates polyadenylation.
    Genes Dev. 1996 Jan 15;10(2):208-19 PMID: 8566754
  12. Four factors are required for 3'-end cleavage of pre-mRNAs.
    Genes Dev. 1989 Nov;3(11):1711-24 PMID: 2558045
  13. A multicomponent complex is required for the AAUAAA-dependent cross-linking of a 64-kilodalton protein to polyadenylation substrates.
    Mol Cell Biol. 1990 Mar;10(3):1244-8 PMID: 2304466
  14. Sequences 5' to the polyadenylation signal mediate differential poly(A) site use in hepatitis B viruses.
    Genes Dev. 1990 May;4(5):764-76 PMID: 2379828
  15. How the messenger got its tail: addition of poly(A) in the nucleus.
    Trends Biochem Sci. 1990 Jul;15(7):277-81 PMID: 1974368
  16. A uridylate tract mediates efficient heterogeneous nuclear ribonucleoprotein C protein-RNA cross-linking and functionally substitutes for the downstream element of the polyadenylation signal.
    Mol Cell Biol. 1990 Dec;10(12):6397-407 PMID: 1701018
  17. A multisubunit factor, CstF, is required for polyadenylation of mammalian pre-mRNAs.
    Genes Dev. 1990 Dec;4(12A):2112-20 PMID: 1980119
  18. Interaction between the U1 snRNP-A protein and the 160-kD subunit of cleavage-polyadenylation specificity factor increases polyadenylation efficiency in vitro.
    Genes Dev. 1996 Feb 1;10(3):325-37 PMID: 8595883
  19. Purification and characterization of human cleavage factor Im involved in the 3' end processing of messenger RNA precursors.
    J Biol Chem. 1996 Mar 15;271(11):6107-13 PMID: 8626397
  20. Sequence similarity between the 73-kilodalton protein of mammalian CPSF and a subunit of yeast polyadenylation factor I.
    Science. 1996 Nov 29;274(5292):1514-7 PMID: 8929409
  21. Ending the message is not so simple.
    Cell. 1996 Nov 29;87(5):779-81 PMID: 8945502
  22. The end of the message--another link between yeast and mammals.
    Science. 1996 Nov 29;274(5292):1481-2 PMID: 8966619
  23. 3'-end-forming signals of yeast mRNA.
    Trends Biochem Sci. 1996 Dec;21(12):477-81 PMID: 9009831
  24. Transcription and polyadenylation in a short human intergenic region.
    Nucleic Acids Res. 1997 Jun 15;25(12):2326-36 PMID: 9171082
  25. RNA recognition by the human polyadenylation factor CstF.
    Mol Cell Biol. 1997 Jul;17(7):3907-14 PMID: 9199325
  26. Mutation of PTB binding sites causes misregulation of alternative 3' splice site selection in vivo.
    RNA. 1997 Jul;3(7):764-78 PMID: 9214659
  27. The 30-kD subunit of mammalian cleavage and polyadenylation specificity factor and its yeast homolog are RNA-binding zinc finger proteins.
    Genes Dev. 1997 Jul 1;11(13):1703-16 PMID: 9224719
  28. The HIV-1 5' LTR poly(A) site is inactivated by U1 snRNP interaction with the downstream major splice donor site.
    EMBO J. 1997 Sep 15;16(18):5752-63 PMID: 9312033
  29. Position-dependent sequence elements downstream of AAUAAA are required for efficient rabbit beta-globin mRNA 3' end formation.
    Cell. 1987 May 8;49(3):399-406 PMID: 3568131
  30. A 64 kd nuclear protein binds to RNA segments that include the AAUAAA polyadenylation motif.
    Cell. 1988 Jan 29;52(2):221-8 PMID: 2830023
  31. Separation and characterization of a poly(A) polymerase and a cleavage/specificity factor required for pre-mRNA polyadenylation.
    Cell. 1988 Mar 11;52(5):731-42 PMID: 2830992
  32. Two proteins crosslinked to RNA containing the adenovirus L3 poly(A) site require the AAUAAA sequence for binding.
    EMBO J. 1988 Oct;7(10):3159-69 PMID: 3181133
  33. Multiple forms of poly(A) polymerases purified from HeLa cells function in specific mRNA 3'-end formation.
    Mol Cell Biol. 1989 Oct;9(10):4229-38 PMID: 2555686
  34. Efficiency of utilization of the simian virus 40 late polyadenylation site: effects of upstream sequences.
    Mol Cell Biol. 1989 Oct;9(10):4248-58 PMID: 2573828
  35. Sequences upstream of AAUAAA influence poly(A) site selection in a complex transcription unit.
    Mol Cell Biol. 1989 Nov;9(11):4951-61 PMID: 2601703
  36. Biochemical characterization of U2 snRNP auxiliary factor: an essential pre-mRNA splicing factor with a novel intranuclear distribution.
    EMBO J. 1991 Jan;10(1):207-14 PMID: 1824937
  37. Poly(A) site efficiency reflects the stability of complex formation involving the downstream element.
    EMBO J. 1991 Jan;10(1):215-9 PMID: 1671216
  38. Involvement of long terminal repeat U3 sequences overlapping the transcription control region in human immunodeficiency virus type 1 mRNA 3' end formation.
    Mol Cell Biol. 1991 Mar;11(3):1624-30 PMID: 1996111
  39. The human immunodeficiency virus type 1 polyadenylylation signal: a 3' long terminal repeat element upstream of the AAUAAA necessary for efficient polyadenylylation.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2108-12 PMID: 1848693
  40. Site-directed ribose methylation identifies 2'-OH groups in polyadenylation substrates critical for AAUAAA recognition and poly(A) addition.
    Cell. 1991 Apr 5;65(1):125-33 PMID: 1901516
  41. Molecular analyses of two poly(A) site-processing factors that determine the recognition and efficiency of cleavage of the pre-mRNA.
    Mol Cell Biol. 1991 May;11(5):2432-8 PMID: 2017162
  42. Efficient polyadenylation within the human immunodeficiency virus type 1 long terminal repeat requires flanking U3-specific sequences.
    J Virol. 1991 Jun;65(6):3340-3 PMID: 1851882
  43. Characterization of cDNAs encoding the polypyrimidine tract-binding protein.
    Genes Dev. 1991 Jul;5(7):1224-36 PMID: 1906035
  44. Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing.
    Genes Dev. 1991 Jul;5(7):1237-51 PMID: 1906036
  45. Primary structure and expression of bovine poly(A) polymerase.
    Nature. 1991 Sep 19;353(6341):229-34 PMID: 1896071
  46. Purification of the cleavage and polyadenylation factor involved in the 3'-processing of messenger RNA precursors.
    J Biol Chem. 1991 Oct 15;266(29):19768-76 PMID: 1918081
  47. Regulation of polyadenylation in hepatitis B viruses: stimulation by the upstream activating signal PS1 is orientation-dependent, distance-independent, and additive.
    Nucleic Acids Res. 1991 Dec 11;19(23):6449-56 PMID: 1754382
  48. Transcriptional termination between the closely linked human complement genes C2 and factor B: common termination factor for C2 and c-myc?
    EMBO J. 1991 Dec;10(13):4197-207 PMID: 1756727
  49. Cleavage and polyadenylation factor CPF specifically interacts with the pre-mRNA 3' processing signal AAUAAA.
    EMBO J. 1991 Dec;10(13):4241-9 PMID: 1756731
  50. Isolation and expression of cDNA clones encoding mammalian poly(A) polymerase.
    EMBO J. 1991 Dec;10(13):4251-7 PMID: 1756732
  51. The human 64-kDa polyadenylylation factor contains a ribonucleoprotein-type RNA binding domain and unusual auxiliary motifs.
    Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1403-7 PMID: 1741396
  52. Regulation of polyadenylation in human immunodeficiency virus (HIV): contributions of promoter proximity and upstream sequences.
    EMBO J. 1992 Apr;11(4):1513-24 PMID: 1373376
  53. Varied poly(A) site efficiency in the adenovirus major late transcription unit.
    J Biol Chem. 1992 Apr 25;267(12):8175-81 PMID: 1575826
  54. Separation of factors required for cleavage and polyadenylation of yeast pre-mRNA.
    Mol Cell Biol. 1992 Aug;12(8):3470-81 PMID: 1352851
  55. Characterization of the multisubunit cleavage-polyadenylation specificity factor from calf thymus.
    J Biol Chem. 1992 Jul 25;267(21):14804-11 PMID: 1634525
  56. Activation of HIV-1 pre-mRNA 3' processing in vitro requires both an upstream element and TAR.
    EMBO J. 1992 Dec;11(12):4419-28 PMID: 1425577
  57. Assembly of a processive messenger RNA polyadenylation complex.
    EMBO J. 1993 Feb;12(2):585-94 PMID: 8440247
  58. Upstream and downstream cis-acting elements for cleavage at the L4 polyadenylation site of adenovirus-2.
    Nucleic Acids Res. 1994 Jan 25;22(2):222-31 PMID: 8121807
  59. Sequence elements upstream of the 3' cleavage site confer substrate strength to the adenovirus L1 and L3 polyadenylation sites.
    Mol Cell Biol. 1994 Jul;14(7):4682-93 PMID: 7911973
  60. 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
  61. Sequence and position requirements for uridylate-rich downstream elements of polyadenylation signals.
    Nucleic Acids Res. 1994 Jul 11;22(13):2525-31 PMID: 7518915
  62. Smooth muscle-specific switching of alpha-tropomyosin mutually exclusive exon selection by specific inhibition of the strong default exon.
    EMBO J. 1994 Aug 15;13(16):3861-72 PMID: 8070413
  63. Direct interaction of the U1 snRNP-A protein with the upstream efficiency element of the SV40 late polyadenylation signal.
    Genes Dev. 1994 Mar 1;8(5):576-86 PMID: 7926751
  64. The 64-kilodalton subunit of the CstF polyadenylation factor binds to pre-mRNAs downstream of the cleavage site and influences cleavage site location.
    Mol Cell Biol. 1994 Oct;14(10):6647-54 PMID: 7935383
  65. Characterization of cleavage and polyadenylation specificity factor and cloning of its 100-kilodalton subunit.
    Mol Cell Biol. 1994 Dec;14(12):8183-90 PMID: 7969155
  66. Mechanism and regulation of mRNA polyadenylation.
    Genes Dev. 1997 Nov 1;11(21):2755-66 PMID: 9353246
  67. Human pre-mRNA cleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits.
    Mol Cell. 1998 Jan;1(2):243-53 PMID: 9659921
  68. 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
  69. 3' non-coding region sequences in eukaryotic messenger RNA.
    Nature. 1976 Sep 16;263(5574):211-4 PMID: 822353
  70. Purification with monoclonal antibody of a predominant leukocyte-common antigen and glycoprotein from rat thymocytes.
    Eur J Immunol. 1979 Feb;9(2):155-9 PMID: 374095
  71. 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
  72. Requirement of a downstream sequence for generation of a poly(A) addition site.
    Cell. 1984 Jul;37(3):993-9 PMID: 6744418
  73. A sequence downstream of AAUAAA is required for rabbit beta-globin mRNA 3'-end formation.
    Nature. 1984 Nov 29-Dec 5;312(5993):473-4 PMID: 6095108
  74. The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3' termini.
    Nucleic Acids Res. 1985 Feb 25;13(4):1347-68 PMID: 2987822
  75. Sequences capable of restoring poly(A) site function define two distinct downstream elements.
    EMBO J. 1986 Nov;5(11):2907-13 PMID: 3024967
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
1998-08-15
Pages
2522-34
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC317083
Subset
IM
Grants
NIGMS NIH HHS · GM 28983 · United States
Wellcome Trust · United Kingdom
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