[CANCER RESEARCH 44, 5638-5643, December 1984]
Role of NADPH:Cytochrome c ReducÃ-aseand DT-Diaphorase in the
Biotransformation of Mitomycin C1
Susan R. Keyes, Paula M. Fracasso, David C. Heimbrook,2 Sara Rockwell, Stephen G. Silgar,3 and
Alan C. Sai-torelli4
Departments of Pharmacology [S. R. K., P. M. F., A. C. S.] and Therapeutic Radiology [S. R.J and Developmental Therapeutics Program, Comprehensive Cancer Center,
Yale University School of Medicine, New Haven 06510, and Department of Molecular Biophysics and Biochemistry, [S. G. S., D. C. H.¡Yale University,
New Haven 06511, Connecticut
ABSTRACT
Hypoxie cells of solid tumors are difficult to eradicate by X-
irradiation or chemotherapy; as an approach to this problem, our
laboratories are investigating the effects of the bioreductive
alkylating agent mitomycin C (MC) on hypoxic cells. This anti
biotic was preferentially toxic to EMT6 mouse mammary tumor
cells and V79 Chinese hamster lung fibroblasts under hypoxic
conditions, but it was equitoxic to Chinese hamster ovary cells
in the presence and absence of oxygen. All cell lines catalyzed
the formation of reactive metabolites under hypoxic conditions
and contained NADPH:cytochrome c reducÃ-aseand DT-diaphor-
ase, two enzymes which may be responsible for the cellular
activation of MC. Although a correlation existed between enzy
matic activities and the formation of reactive metabolites from
MC, there was no correspondence between these parameters
and the degree of cytotoxicity expressed by MC under hypoxic
conditions.
Purified NADPHrcytochrome c reducÃ-ase reduced MC in the
absence of oxygen, with addition of cytochrome P-450 enhanc
ing, but noi participating directly in, the reduction reaction. Ad
dition of NADP+ lo cell sonicates substantially reduced NADPH:-
cylochrome c reducÃ-ase activity, while Ihe formation of reactive
metabolites was affected only slightly; converse results were
observed using mersalyl. Exposure of cell sonicates lo dicumarol
inhibiled DT-diaphorase activity, while the rate of formation of
reactive metabolites of MC was enhanced. The findings suggest
that NADPH:cytochrome c reducÃ-ase and some as yet to be
identified enzyme(s) are important for the reductive activalion of
MC. DT-diaphorase and cytochrome P-450 are not directly in
volved in the activalion of MC, bul they appear lo modulate the
degree of activalion lo reaclive species, which are presumably
responsible for Ihe observed cytotoxicity.
INTRODUCTION
Solid neoplasms contain hypoxic tumor cell populations; since
oxygen-deficient cells are relatively refractory lo convenlional
radiolherapy and mosl chemolherapy, hypoxic cells have Ihe
potential to limit curability (13, 19). As an approach to the
circumvention of this problem, we have been studying the natu-
1This work was supported in part by American Cancer Society Grants CH-211
and PDT 145, USPHS Grant CA-02817, NIH Grants GM-31756 and AM-01160,
and American Heart Association Fellowship 11-104-812.
2 Present address: Department of Pharmacology, Yate University School of
Medicine, New Haven, CT 06510.
3 Present address: Department of Biochemistry, University of Illinois, Urbana, IL
61801.
4 To whom requests for reprints should be addressed.
Received May 21, 1984; accepted August 29, 1984.
rally occurring antibiolic, MC.5 This drug is aclive against a broad
range of transplantable animal (5) and human (2) tumors, is
preferentially cytotoxic to some hypoxic tumor cell lines in vitro
(11, 23, 27), and is also toxic to hypoxic tumor cells in vivo (25,
26).
Early studies have demonslraled lhal enzymalic bioactivalion
of MC results in cyloloxicily associated wilh cross-linking of
DNA (9). Using liver homogenales, the anaerobic production of
reaclive species from MC has been shown lo require NADPH
and to be catalyzed primarily by enzymes in the microsomal and
nuclear subcellular fractions (12, 28), and some alkylation prod
ucts have been identified (31). Limited studies with purified
enzymes have indicated that both NADPHxytochrome c reduc
Ã-aseand xanthine oxidase actÃ-valeMC under hypoxic conditions,
wilh Ihe concomilanl generalion of a reaclive eleclrophile (14,
21 ). Studies in our laboratories have suggested lhal cytochrome
P-450 might be involved in the anaerobic metabolism of MC (11,
12), and work by others on DT-diaphorase, an enzyme active in
the reduction of quiñones (6, 30), suggests that this enzyme
should also be considered as a possible activator of MC.
Although the mechanism by which MC is metabolically acti
vated has been examined extensively in bacteria and liver, little
is known about the bioaclivation of MC by neoplastic cells.
Previous investigations in our laboratories have demonslraled
that MC is more toxic to EMT6 and Sarcoma 180 tumor cells
under hypoxic conditions than in the presence of air, and lhal
sonicates of these cells are capable of generating a reactive
species from MC (11, 27). However, neilher Ihe enzyme(s) in
lumor cells responsible for activating MC nor the exact biochem
ical basis of Ihe enhanced cyloloxicily in Ihe absence of oxygen
has yet been characterized. The studies described in Ihis paper
were designed to address these issues.
MATERIALS AND METHODS
MC was supplied by the Bristol-Myers Co. (Syracuse, NY). Other
materials were obtained from the following sources: NADP*, NADH,
NADPH, glucose-6-phosphate dehydrogenase (type XII), glucose 6-phos-
phate, dicumarol, mersalyl, 2,6-dichlorophenolindophenol, dilaurylphos-
phatidylcholine, DEAE-cellulose, and 2',5'-ADP agarose (Sigma Chemi
cal Co., St. Louis, MO); fetal bovine serum and Waymouth's medium
(Grand Island Biological Co., Grand Island, NY); DEAE-Trisacryl M and
HA-Utrogel (LKB Instruments, Gaithersburg, MD); gases (Presto Welding
Service Center, North Haven, CT); and 4-<p-nitrobenzyl)pyridine (Aldrich
Chemical Co., Milwaukee, Wl). Chinese hamster V79 cells (subline V79-
8) and CHO cells (subline HA-1) were gifts of Dr. R. Michael Liskay and
Dr. Daniel S. Kapp, Department of Therapeutic Radiology, Yale University
School of Medicine.
5The abbreviations used are: MC, mitomycin C; CHO, Chinese hamster ovary.
CANCER RESEARCH VOL. 44 DECEMBER 1984
5638
Research.
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