Abstract
DNA primase-dependent synthesis of oligoribonucleotides 10-15 nucleotides long was observed in the presence of ATP, UTP, GTP, and CTP by using the purified components of the simian virus 40 (SV40) DNA replication system. The DNA primase-catalyzed reaction required the SV40 large tumor antigen (T antigen), DNA polymerase alpha (pol-alpha), the three-subunit human single-stranded DNA binding protein (HSSB), and topoisomerase I. The synthesis of small RNAs was unaffected by the addition of activator 1, proliferating cell nuclear antigen, and DNA polymerase delta, proteins that can support extensive leading-strand synthesis. The RNA primers were derived predominantly from transcription of the lagging-strand template, even after prolonged incubation, indicating that the leading strand did not serve as a template. When the four dNTPs were added after oligoribonucleotide synthesis, pol-alpha extended the RNA primers hybridized to SV40 DNA. Pulse-chase experiments revealed that the small RNA chains were elongated to Okazaki-sized products. T7 DNA polymerase was also shown to rapidly extend oligoribonucleotide primers in the presence of aphidicolin or antibodies against pol-alpha, conditions under which pol-alpha was markedly inhibited. These findings suggest that interactions between T antigen, pol-alpha-primase, and HSSB position the pol-alpha-primase complex on the lagging-strand template for RNA primer synthesis.
MeSH Terms
Antigens, Polyomavirus Transforming/physiology
DNA Polymerase II/metabolism
DNA Primase
DNA Replication
DNA Topoisomerases, Type I/metabolism
DNA, Viral/biosynthesis
DNA-Binding Proteins/metabolism
In Vitro Techniques
Oligoribonucleotides/biosynthesis
RNA Nucleotidyltransferases/metabolism
Simian virus 40/genetics
Templates, Genetic
Virus Replication
Chemicals
Antigens, Polyomavirus Transforming
DNA, Viral
DNA-Binding Proteins
Oligoribonucleotides
DNA Primase
RNA Nucleotidyltransferases
DNA Polymerase II
DNA Topoisomerases, Type I
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Murakami Y
Graduate Program in Molecular Biology, Sloan-Kettering Institute, New York, NY 10021.
Eki T
Hurwitz J
References (21)
21 references, click to expand
-
Replication factors required for SV40 DNA replication in vitro. II. Switching of DNA polymerase alpha and delta during initiation of leading and lagging strand synthesis.
J Biol Chem. 1991 Jan 25;266(3):1961-8
PMID: 1671046
-
T-antigen-DNA polymerase alpha complex implicated in simian virus 40 DNA replication.
Mol Cell Biol. 1986 Nov;6(11):4077-87
PMID: 3025630
-
Three domains in the simian virus 40 core origin orchestrate the binding, melting, and DNA helicase activities of T antigen.
J Virol. 1990 Feb;64(2):509-18
PMID: 2153220
-
Binding and unwinding--how T antigen engages the SV40 origin of DNA replication.
Cell. 1990 Jan 26;60(2):181-4
PMID: 2153460
-
Two DNA polymerases may be required for synthesis of the lagging DNA strand of simian virus 40.
J Virol. 1990 Dec;64(12):5912-8
PMID: 2173773
-
Structure and function of SV40 large-T antigen.
Philos Trans R Soc Lond B Biol Sci. 1987 Dec 15;317(1187):455-69
PMID: 2450379
-
RNA unwinding activity of SV40 large T antigen.
Cell. 1989 Jun 16;57(6):955-63
PMID: 2472217
-
Initiation of eukaryotic DNA replication in vitro.
Annu Rev Cell Biol. 1989;5:197-245
PMID: 2557059
-
Synthesis of DNA containing the simian virus 40 origin of replication by the combined action of DNA polymerases alpha and delta.
Proc Natl Acad Sci U S A. 1989 Oct;86(19):7361-5
PMID: 2571990
-
Complete enzymatic synthesis of DNA containing the SV40 origin of replication.
J Biol Chem. 1988 Dec 25;263(36):19723-33
PMID: 2848839
-
In vitro replication of duplex circular DNA containing the simian virus 40 DNA origin site.
Proc Natl Acad Sci U S A. 1985 Sep;82(17):5710-4
PMID: 2994044
-
Synthesis by the DNA primase of Drosophila melanogaster of a primer with a unique chain length.
Proc Natl Acad Sci U S A. 1982 Aug;79(15):4585-8
PMID: 6812052
-
Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase delta.
J Biol Chem. 1991 Jan 5;266(1):594-602
PMID: 1670772
-
Initiation of simian virus 40 DNA synthesis in vitro.
Mol Cell Biol. 1991 May;11(5):2350-61
PMID: 1673224
-
Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase.
Mol Cell Biol. 1991 Apr;11(4):2108-15
PMID: 1848671
-
Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin.
Nature. 1990 Aug 9;346(6284):534-9
PMID: 2165567
-
Studies on the initiation and elongation reactions in the simian virus 40 DNA replication system.
Proc Natl Acad Sci U S A. 1990 Dec;87(24):9712-6
PMID: 2175912
-
Animal virus DNA replication.
Annu Rev Biochem. 1989;58:671-717
PMID: 2549858
-
Multiple functions of human single-stranded-DNA binding protein in simian virus 40 DNA replication: single-strand stabilization and stimulation of DNA polymerases alpha and delta.
Proc Natl Acad Sci U S A. 1989 Dec;86(24):9757-61
PMID: 2557626
-
Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases, alpha and delta.
EMBO J. 1989 Dec 1;8(12):3883-9
PMID: 2573521
-
SV40 T antigen binds directly to the large subunit of purified DNA polymerase alpha.
EMBO J. 1990 Oct;9(10):3329-36
PMID: 1698613