[CANCER RESEARCH54, 41)72-4076, August 1, 19941
murine tumors (4) and melanoma xenografts (5) and is significantly
more effective than DTIC in inhibiting the growth of the Walker
tumor in rats (6). Like DTIC, CB1O-277 requires activation by oxi
dative N-demethylation, but the overall production of the putative
active monomethyl metabolite in rats was iS-fold greater than that for
DTIC, suggesting that species-dependent activation is less likely to be
a problem in humans (6). Thus, due to the structural similarities to
DTIC, the improved in vitro stability and solubility, and the possibil
ity of improved metabolic activation, CB1O-277 was selected for
clinical trial by the Cancer Research Campaign (UK) Clinical Trial
Committee (7).
With respect to the mechanisms of antitumor action, there is a
considerable amount of evidence to indicate that the cell-killing
effects of DTIC, CB1O-277, and related methylating agents are me
diated mainly by the formation of 06-MedG in DNA and that the
principal mechanism of resistance is via the DNA repair protein
ATase. This protein acts by the stoichiometric transfer of the methyl
group from the 06-position of guanine in alkylated DNA to a cysteine
residue in the protein itself, in an autoinactivating reaction (5, 8—12).
The strongest evidence for the cytotoxic effects of 06-alkylguanine in
DNA comes from experiments which show that the expression of a
transfected prokaryotic or eukaryotic ATase complementary DNA in
mammalian cells protects them against the toxic effects of these
agents (13—17). .
We recently demonstrated a wide interindividual variation in the
depletion of lymphocyte ATase during a 24-h continuous infusion of
CB1O-277 (18). These findings can be attributed to the CBiO-277-
mediated formation of 06-MedG in lymphocyte DNA, and the sub
sequent repair of this adduct by ATase is manifested as a depletion of
ATase activity in lymphocyte extracts. The relationship between the
ability to activate CB1O-277, which is reflected in the formation of
06-MedG in DNA, and the wide range of clinical responses seen
among patients with metastatic melanoma receiving this drug has not
been explored. The aims of the present study are therefore to examine
whether there is a correlation between 06-MedG accumulation in
leukocyte DNA and lymphocyte ATase activity and also to assess
whether there is any relationship between 06-MedG formation and
clinical response.
MATERIALS AND METhODS
Patients and Blood Samples. CB1O-277 (sodium salt, Mr 215) was sup
plied as a lyophilized, pyrogen- and preservative-free powder (in 1000-mg
vials) by the Developmental Therapeutics Program, National Cancer Institute
(Bethesda, MD). All nine patients had metastatic melanoma, and details of the
individuals studied as reported previously (18) are shown in Table 1. Each
patient received CB1O-277 (12 mg/m2) by continuous iv. infusion over 24 h
and the treatment was repeated every 4 weeks. Serial blood samples (20 ml)
were collected at various times during the infusion and for 24 h after comple
tion of the first cycle of CB1O-277. Blood samples were dispensed into two
universal containers (10 ml each) containing 0.5 ml of 0.5% EDTA, pH 8.0.
One container was stored at —20°C prior to DNA extraction and radioimmu
noassay for 06-MedG levels (see below). The second container was kept at
4072
Relationships between the Formation of 06-Methyldeoxyguanosine by 1-p-Carboxyl
3,3-dimethylphenyltriazene in DNA and 06-AlkylguanineDNA
Alkyltransferase in Human Peripheral Leukocytes1
Slow Ming Lee,2 Peter J. O'Connor, Nicholas Thatcher, Derek Crowther, Geoffrey P. Margison, and
Donald P. Cooper
CRC Department of Carcinogenesis, Paterson Institute for Cancer Research (S. M. L., P. J. 0., G. P. M., D. P. C.J, and CRC Department ofMedical Oncology, Christie Hospital
National Health Service Trust [S. M. L., N. T., D. C.], Manchester, M20 9BX, UK
ABSTRACT
There is increasing experimental evidence to indicate that 06-meth
yldeoxyguanosine (06-MedG) formation in DNA is a critical cytotoxic
event following exposure to certain antitumor alkylating agents and that
the DNA repair protein O@-alkylguanine-DNA-alkyltransferase(ATase)
can confer resistance to these agents. We recently demonstrated a wide
interindividual variation in the depletion and subsequent regeneration of
ATase in peripheral blood lymphocytes of patients treated with 24-h
continuous infusion of 1-p-carboxyl-3,3-dimethylphenyltnazene (CB1O-
277) for metastatic melanoma. We have now measured the formation of
O't-MedG in the DNA of peripheral leukocytes of nine patients receiving
this treatment regimen. This lesion could be detected in DNA within 1h
and a progressive increase in adduct levels occurred during the CB1O-277
infusion and for 24 h after completion. Considerable interindividual var
iation was observed in the peak O'@-ModG levels, with values ranging from
3.0 to 23.8 @unol O'-MedG/mol deoxyguanosine (mean, 12.3 ±6.4 @.tmol
06-MedG/mol deoxyguanosine) following the first treatment cycle, possi
bly as a consequence of differences in the capacity of patients to metab
olize CB1O-277 to a methylating agent. There was, nevertheless, a clear
temporal relationship between the progressive formation of leukocyte
O@-MedGand lymphocyte ATase depletion. Repeated-measures regres
sion showed that this was statisticaHy significant (P < 0.001) during the
CB1O.277 infusion. A significant inverse correlation was also seen between
pretreatment lymphocyte ATase activity and peak O'@-MedGlevels in
leukocyte DNA (r = —0.73)and the area under the leukocyte O'@-MedG
concentration-time curve (r —0.76).Metabolism of CB1O-277 to a
methylating agent could be one factor that combines with DNA repair
capacity to determine clinical response, because the two responses oh
served in this series occurred in the two patients with the highest leukocyte
O@-MedGlevels and also the lowest pretreatment ATase activity. Hema
tological toxicity developed in the same two patients.
INTRODUCTION
The treatment of metastatic melanoma remains unsatisfactory. Al
though DTIC3 is still regarded as the most effective chemotherapeutic
agent and regularly produces a response rate of 20%, only 4% of
patients (jrimarily those with soft tissue metastasis) show a complete
response and responses are rare in cases with visceral metastasis (i,
2). It has been suggested that one possible reason for the relatively
poor clinical activity of DTIC may be the relatively inefficient met
abolic activation, compared to murine models. Thus, following equiv
alent doses, the plasma levels of the active monomethyl metabolite
5-(3-methyl-1-triazeno)imidazole-4-carboxamide are much lower in
rats and humans than in mice (3). Another triazene, CB1O-277 (Fig.
1), has been shown to have marked activity against experimental
Received 1/10/94; accepted 5/24/94.
I Supported by funds from the Christie Hospital (National Health Service) Trust
Endowment Fund, North West Regional Health Authority, and the Cancer Research
Campaign (UK).
2 To whom requests for reprints should be addressed.
3 The abbreviations used are: DTIC (dacarbazine), 5-(3,3-dimethyl-1-triazeno)imida
zole-4-carboxamide; ATase, O―-alkylguanine-DNA alkyltransferase; AUC, area under
the concentration-time curve; CB1O-277, 1-p-carboxyl-3,3-dimethylphenyltriazene;
O―-MedG,O―-methyldeoxyguanosine.
Research.
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