Mol Gen Genet (1993) 239:72-76
© Springer-Verlag 1993
Mutations in the mutY gene of Escherichia coli enhance
the frequency of targeted G: C T: A transversions induced
by a single 8-oxoguanine residue in single-stranded DNA
Masaaki Moriya, Arthur P. Grollman
Department of Pharmacological Sciences, State University of New York at Stony Brook, Stony Brook, NY 11794-8651, USA
Received: 3 September 1992/Accepted: 23 December 1992
Abstract. Oxidative damage to guanine in DNA results in
the formation of 8-oxoguanine, which has been shown to
induce G ~ T transversions targeted to this site. The mu-
tagenicity of this lesion was studied in several mutator
strains of Escherichia coli, using single-stranded DNA
containing a single 8-oxoguanine residue. The frequen-
cies of targeted G ~ T transversions increased markedly
in rout Ystrains, while this mutagenic event was not affect-
ed in mutM or mutS strains. Introdution of a mutM muta-
tion into a mutY strain caused a somewhat higher fre-
quency of G~T transversions than that in the mut Y
strain and the effect of a routS mutation was marg!nal. We
conclude that the mutYgene plays a crucial role in pre-
venting targeted G ~ T mutations derived from misrepli-
cation of the 8-oxoguanine-containing template DNA.
Key words: Site-specific mutagenesis - Oxidative DNA
damage - 8-Hydroxyguanine - Mutator
Introduction
Cellular DNA is damaged by oxygen-free radicals
generated during endogenous oxidative processes or by
exposure to oxygen radical-forming agents (Saul et al.
1987; Ames 1989). Oxidative damage to DNA is thought
to play a significant role in spontaneous mutagenesis,
cancer and the aging process (Ames 1983, 1989; Ames
and Gold 1991). 8-Oxoguanine (8-oxoG) is created by
oxidative damage to DNA and is found in significant
quantities in cellular DNA (Ames and Gold 1991; Kasai
and Nishimura 1991).
In vitro primer extension studies showed that dCMP
or dAMP is incorporated opposite 8-oxoG; dAMP is
preferentially inserted by "replicative" DNA poly-
merases (a and 6) and dCMP by "repair" polymerases
Communicated by M. Sekiguchi
Correspondence to: M. Moriya
(I and 13) (Shibutani et al. 1991). In vivo studies using a
single 8-oxoG residue embedded in single-stranded (ss)
DNA revealed this lesion to be weakly mutagenic, induc-
ing targeted G~T transversions in Escherichia coli
(Wood et al. 1990; Moriya et al. 1991 ; Cheng et al. 1992)
and simian kidney cells (Moriya 1993). Michaels et al.
(1992) found that E. coli MutY protein, an adenine
DNA-glycosylase (Au et al. 1989), removes adenine from
an A: 8-oxoG pair in vitro, suggesting that the MutY
protein removes adenine misincorporated opposite
8-oxoG residues after DNA replication is completed. Ac-
cordingly, the weak in vivo mutagenicity of 8-oxoG em-
bedded in ssDNA may be ascribed to the activity of
MutY protein. In this paper, we show that 8-oxoG in
ssDNA is strongly mutagenic in mutY strains of E. coli.
We also report effects of other mutator genes on the
mutagenicity of this lesion.
Materials and methods
E. coli strains used in this study were ABl157 [thr-1,
ara-14, leuB6, A(gpt-proA)62, lacY1, tsx-33, SupE44,
9alK2, hisG4, rfbD1, rpsL31, kdgK51, xyl-5, mtl-1,
aroE3, thi-1, rac, )q, AB 1157-Y 11 (as AB 1157 but mut IT,
zgd:.'TnlO), RK1517 (as ABl157 but mutS::Tn5),
RK1517-Y33 (as RK1517 but mutY, nupG511::TnlO)
(Au et al. 1988), TT101 (as CC104 but mutM: :mini-tet)
(Michaels et al. 1991), TT101-mutY (as TT101 but
mutY: :mini-kan) and TT108 (as CC104 but mutY: :mini-
tet). CC104 is ara, A(gpt-lac)5, [F'lacI378, lacZ461,
proA+B +] (Cupples and Miller 1989). ABl157 was ob-
tained from B. Bachmann (Yale University, New Haven,
Conn.); the derivatives of CC104 were from M. Michaels
and J. Miller (UCLA, Los Angeles, Calif.); and the
others were from M. Modrich (Duke University, Dur-
ham, N.C.).
Construction of a circular ss phagemid vector con-
taining a single 8-oxoG at a specific site [hereafter called
ss pMS2(8-oxoG) and ss pMS2 (G) for control] and the
general procedure used in this study is shown schemati-