Abstract
The 5' cap of a mammalian pre-mRNA has been shown to interact with splicing components at the adjacent 5' splice site for processing of the first exon and the removal of the first intron (E. Izaurralde, J. Lewis, C. McGuigan, M. Jankowska, E. Darzynkiewicz, and I.W. Mattaj, Cell 78:657-668, 1994). Likewise, it has been shown that processing of the last exon and removal of the last intron involve interaction between splicing components at the 3' splice site and the polyadenylation complex at the polyadenylation signal (M. Niwa, S. D. Rose, and S.M. Berget, Genes Dev. 4:1552-1559, 1990; M. Niwa and S. M. Berget, Genes Dev. 5:2086-2095, 1991). These findings suggest that the cap provides a function in first exon processing which is similar to the function of the 3' splice site at last exon processing. To determine whether caps and 3' splice sites function similarly, we compared the effects of the cap and the 3' splice site on the in vitro utilization of the simian virus 40 late polyadenylation signal. We show that the presence of a m7GpppG cap, but not a cap analog, can positively affect the efficiency of polyadenylation of a polyadenylation-only substrate. Cap analogs do not stimulate polyadenylation because they fail to bind titratable cap-binding factors. The failure of cap analogs to stimulate polyadenylation can be overcome if a 3' splice site is present upstream of the polyadenylation signal. These data indicate that factors interacting with the cap or the 3' splice site function similarly to affect polyadenylation signal, along with m7GpppG cap, is inhibitory to polyadenylation. This finding suggests that the interaction between the cap-binding complexes and splicing components at the 5' splice site may form a complex which is inhibitory to further processing if splicing of an adjacent intron is not achieved.
MeSH Terms
Base Sequence
Binding Sites
Dinucleoside Phosphates/metabolism
Exons
Guanosine Triphosphate/analogs & derivatives,metabolism
HeLa Cells
Humans
Introns
Molecular Structure
Poly A/genetics,metabolism
RNA Caps/chemistry,genetics,metabolism
RNA Precursors/chemistry,genetics,metabolism
RNA Processing, Post-Transcriptional
RNA Splicing
Chemicals
Dinucleoside Phosphates
RNA Caps
RNA Precursors
Poly A
5'-guanylylmethylenebisphosphonate
7-methyl-diguanosine triphosphate
Guanosine Triphosphate
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Cooke C
Graduate Group of Molecular Biology, University of Pennsylvania, Philadelphia 19104-6142, USA.
Alwine J C
References (28)
28 references, click to expand
-
Site-specific polyadenylation in a cell-free reaction.
Cell. 1984 Mar;36(3):581-91
PMID: 6230155
-
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
-
A sequence downstream of A-A-U-A-A-A is required for formation of simian virus 40 late mRNA 3' termini in frog oocytes.
Proc Natl Acad Sci U S A. 1985 Jun;82(12):3949-53
PMID: 2987956
-
Accurate cleavage and polyadenylation of exogenous RNA substrate.
Cell. 1985 Jul;41(3):845-55
PMID: 2408761
-
Cap-dependent RNA splicing in a HeLa nuclear extract.
Proc Natl Acad Sci U S A. 1985 Nov;82(22):7590-4
PMID: 3865180
-
A small nuclear ribonucleoprotein associates with the AAUAAA polyadenylation signal in vitro.
Cell. 1986 May 23;45(4):581-91
PMID: 2423249
-
Identification of a sequence element on the 3' side of AAUAAA which is necessary for simian virus 40 late mRNA 3'-end processing.
Mol Cell Biol. 1985 Oct;5(10):2713-9
PMID: 3016512
-
Preferential excision of the 5' proximal intron from mRNA precursors with two introns as mediated by the cap structure.
Proc Natl Acad Sci U S A. 1987 Aug;84(15):5187-91
PMID: 2440046
-
Association of poly(A) polymerase with U1 RNA.
J Biol Chem. 1988 Aug 15;263(23):11067-70
PMID: 2841316
-
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
-
How the messenger got its tail: addition of poly(A) in the nucleus.
Trends Biochem Sci. 1990 Jul;15(7):277-81
PMID: 1974368
-
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
-
Structure of spliceosomal snRNPs and their role in pre-mRNA splicing.
Biochim Biophys Acta. 1990 Nov 30;1087(3):265-92
PMID: 2147394
-
In vitro polyadenylation is stimulated by the presence of an upstream intron.
Genes Dev. 1990 Sep;4(9):1552-9
PMID: 1701407
-
Mutation of the AAUAAA polyadenylation signal depresses in vitro splicing of proximal but not distal introns.
Genes Dev. 1991 Nov;5(11):2086-95
PMID: 1657710
-
Simian virus 40 late mRNA leader sequences involved in augmenting mRNA accumulation via multiple mechanisms, including increased polyadenylation efficiency.
J Virol. 1991 Dec;65(12):6677-85
PMID: 1682508
-
The biochemistry of 3'-end cleavage and polyadenylation of messenger RNA precursors.
Annu Rev Biochem. 1992;61:419-40
PMID: 1353951
-
Are vertebrate exons scanned during splice-site selection?
Nature. 1992 Nov 19;360(6401):277-80
PMID: 1359430
-
Definition of the upstream efficiency element of the simian virus 40 late polyadenylation signal by using in vitro analyses.
Mol Cell Biol. 1992 Dec;12(12):5386-93
PMID: 1333042
-
Association with terminal exons in pre-mRNAs: a new role for the U1 snRNP?
Genes Dev. 1993 Apr;7(4):647-59
PMID: 8384583
-
Sequences within the last intron function in RNA 3'-end formation in cultured cells.
Mol Cell Biol. 1993 Jun;13(6):3359-69
PMID: 7684497
-
Upstream introns influence the efficiency of final intron removal and RNA 3'-end formation.
Genes Dev. 1994 Feb 1;8(3):363-75
PMID: 7906237
-
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
-
A nuclear cap binding protein complex involved in pre-mRNA splicing.
Cell. 1994 Aug 26;78(4):657-68
PMID: 8069914
-
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
-
Exon recognition in vertebrate splicing.
J Biol Chem. 1995 Feb 10;270(6):2411-4
PMID: 7852296
-
A complex protein assembly catalyzes polyadenylation of mRNA precursors.
Curr Opin Genet Dev. 1995 Apr;5(2):222-8
PMID: 7613093
-
Sequences on the 3' side of hexanucleotide AAUAAA affect efficiency of cleavage at the polyadenylation site.
Mol Cell Biol. 1984 Aug;4(8):1460-8
PMID: 6149460