Eukaryotic DNA Replication

Eukaryotic DNA replication is SLOW compared to E. coli DNA replication: only about 75 nucleotides/second. Our deepest understanding of eukaryotic DNA replication comes from studying a model replication system using the small DNA tumor virus SV40 (monkey cells are the host for SV40). A double hexamer of T antigen (Tumor antigen: a virus-encoded origin-binding protein) formed in the presence of ATP binds to the SV40 origin and causes structural distortion of the DNA. This stable initiator protein-DNA complex then binds the cellular replication protein A (RPA), a three-subunit single-stranded DNA-binding protein. This allows more extensive unwinding of the DNA mediated by the DNA helicase function of SV40 T antigen (T antigen is a 3'-to-5' helicase that tracks along the leading strand template). The T antigen-RPA complex binds polymerase alpha (pol alpha)/primase and a nascent RNA-DNA is synthesized at the origin. The cellular replication factor C (RFC) binds to the 3' end of the nascent DNA strand and loads proliferating cell nuclear antigen (PCNA) and DNA polymerase delta (pol delta) on to the template, thereby replacing pol alpha. The processive RFC/PCNA/pol delta complex then extends the nascent DNA strands to form the continuously synthesized leading-strand complex. Thus, initiation of leading-strand DNA replication requires a switch from pol alpha to pol delta. The lagging strands is synthesized discontinuously: primed by pol alpha/primase and extended by pol delta. A 5'-to-3' exonuclease (FEN-1) and RNaseH1 are required to remove RNA primers, and DNA ligase I is required to join Okazaki fragments into completed DNA strands. The swivel for DNA replication is eukaryotic topoisomerase I. The final replication products are covalently closed interlinked circular molecules. Interlinked daughter molecules are decatenated by topoisomerase IIa or IIb.

These are figures and tables found in the review article: T. A. Baker and S. P. Bell (1998) Polymerases and the Replisome: Machines within Machines. Cell 92: 295-305.

Proteins that perform analogous functions at the replication fork (Table 1).

Initiation proteins (Table 2).

Proteins required for SV40 DNA replication in vitro

 Factor

Mol. Wt. (kD)

 Function(s)
T antigen

90
origin recognition protein, 3'-to-5' helicase on leading strand template (stimulated by RPA).
RPA

70, 34, 11
binds ssDNA, promotes origin unwinding, stimulates T antigen helicase activity, stimulates pol alpha/primase, cooperates with RFC and PCNA to stimulate pol delta to produce long DNA products. Also prevents pol alpha/primase from rebinding to newly synthesized strands.
DNA polymerase alpha/primase

167, 79, 62, 48
initiates leading- and lagging-strand synthesis, primers have about 10 nucleotides of RNA at the 5' end and about 30 nucleotides of DNA at the 3' end. Priming on the lagging strand template is very frequent, with placement of primers about 50 nucleotides apart. pol alpha does NOT have 3'-to-5' exonuclease (editing) activity. p167 has polymerizing activity and p48 has primase activity. Requires RPA for stable attachment to its primed site.
DNA polymerase delta

125, 55, 40
completes leading- and lagging-strand synthesis, the 125 kD subunit has polymerization and 3'-to-5' exonuclease (editing) activity. p40 interacts with PCNA.
DNA polymerase epsilon

255, 79, 29, 23
pol epsilon is NOT required for SV40 DNA replication, but deletion of the gene for p255 in yeast is lethal, although a p255 mutant only lacking polymerization is not. Its role is replication is currently not known. p255 has polymerase and 3'-to-5' exonuclease activities.
RFC

140, 40, 38, 37, 36
loads PCNA onto DNA, DNA-dependent ATPase (stimulated by PCNA), binds to primer terminus (3'-OH), binding requires ATP. Involved in polymerase switching: it disrupts the contacts between RPA and pol alpha/primase. This allows pol delta to couple to PCNA.
PCNA

36
processivity factor for pol delta and pol epsilon, homotrimeric ring-shaped structure (like E. coli DNA pol III beta subunit), binds also to RFC, FEN-1, DNA ligase I, nucleotide excision repair protein XPG, and a number of other proteins.
Topoisomerase I

110
relieves torsional strain in front of replication forks.
Topoisomerase IIa and/or IIb

170 (IIa), 180 (IIb)
segregates catenated (interlinked) covalently closed circles.
FEN-1

43
5'-to-3' exo/endonuclease (flap endonuclease), removes RNA primers from the 5' ends of Okazaki fragments, but cannot degrade a 5'-triphosphorylated ribonucleotide annealed to ssDNA (in such a situation, RNaseHI is required), binding to PCNA stimulates activity 10-fold (Figure B5). FEN-1 can also remove mismatched sequences synthesized by pol alpha/primase.
RNaseH1

89
endonuclease, cleaves RNA primer leaving a single ribonucleotide on the 5' end of the DNA strand.
DNA ligase I

125
ligates Okazaki fragments, binds to PCNA. (Note: Unlike E. coli, which has only one DNA ligase, there are at least four known human DNA ligases). Uses ATP as an energy cofactor.

These are the figures in the review article: R. A. Bambara, R. S. Murante, and L. A. Henricksen (1997) Enzymes and reactions at the eukaryotic DNA replication fork. J. Biol. Chem. 272: 4647-4650. Click here for copy of paper.

DNA polymerase switching and processing of an Okazaki fragment (Figure 1).

Removal of a displaced Okazaki initiator RNA by FEN-1 nuclease (Figure 2).

FEN-1 assay (Figure B4) Note: the 5'-to-3' exonuclease activity of E. coli DNA polymerase I also cleaves flap substrates!

FEN-1 may remove mismatches synthesized by pol alpha (Figure B6)

The Ends of Eukaryotic Chromosomes (Telomeres)

Eukaryotic chromosomes are linear DNA molecules. The ends (telomeres) are specialized sequences involved in chromosome stability. Telomeric DNA consists of tandem repeats of simple sequences. These sequences are usually short and rich in G residues on one strand. For example, the ciliate Tetrahymena contains tandem TTGGGG repeats, whereas humans and other mammals contain TTAGGG repeats. The orientation of the telomere sequences is also conserved; the G-rich strand runs 5'-to-3' toward the end of the chromosome and thus makes up the molecular 3' end of the chromosome. In most organisms the number of repeats on any given end is not fixed, giving telomeres a typical heterogeneous or "fuzzy" appearance in Southern blots. The tract length of these repeated sequences ranges from 38 base pairs in ciliates, like Oxytricha, up to tens of kilobase pairs in mammalian cells, each organism having a characteristic mean length. The length of the simple telomere repeat tracts is maintained by the enzyme telomerase. Telomerase is a specialized DNA polymerase that adds telomeric sequences onto chromosome ends. This de novo addition of sequences balances the loss of repeats during each round of replication of linear DNA molecules (DNA polymerases cannot synthesize DNA on template sequences at the very 3' end of linear chromosomes as shown in Figure J1).

Telomerase

Telomerase is a ribonucleoprotein enzyme that contains both essential proteins and an essential RNA component. The RNA component provides the template for the telomeric repeats that are synthesized de novo onto chromosome ends. For example, the Tetrahymena telomerase RNA is 160 nucleotides long and contains nine potential template nucleotides CAAACCCCAA. The redundancy in the template region allows base pairing of the growing telomere with the RNA and still leaves a region that can serve as a template.

Telomerase RNA Components

 Organism

Telomere sequence

RNA template sequence

 RNA Size

 Tetrahymena

TTGGGG

CAACCCCAA

160

Oxytricha

TTTTGGGG

CAAAACCCCAAAACC

190

Human

TTAGGG

CUAACCCUAAC

450

Mouse

TTAGGG

CCUAACCCU

450

Mechanism of telomerase elongation (Figure J2).