OXIDATIVE STRESS INDUCED BY DRUG BIOTRANSFORMATION 519
Copyright © 2004 John Wiley & Sons, Ltd. J. Appl. Toxic
* Correspondence to: M. E. Letelier, Laboratorio de Farmacología,
Facultad de Ciencias Químicas y Farmacéuticas, Universidad de Chile,
Olivos 1007, Independencia, Santiago, Chile.
E-mail: mel@ciq.uchile.cl
Liver Microsomal Biotransformation of
Nitro-aryl Drugs: Mechanism for Potential
Oxidative Stress Induction
M. E. Letelier,* P. Izquierdo, L. Godoy, A. M. Lepe and M. Faúndez
Laboratorio de Farmacología, Departamento de Química Farmacológica y Toxicológica, Facultad de Ciencias Químicas y
Farmacéuticas, Universidad de Chile, Olivos 1007, Independencia, Santiago, Chile
Key words: biotransformation; liver microsomes; oxidative stress; nitro-aryl drugs; nitrofurantoin/nifurtimox; microsomal
reduction; nitro-aryl drug reduction.
Toxic effects of several nitro-aryl drugs are attributed to the nitro-reduction that may be suffered in vivo, a
reaction that may be catalysed by different reductases. One of these enzymes is NADPH–cytochrome P450
reductase, which belongs to the cytochrome P450 oxidative system mainly localized in the endoplasmic reticulum
of the hepatic cell. This system is responsible for the biotransformation of oxidative lipophilic compounds, so
that oxidative and reductive metabolic pathways of lipophilic nitro-aryl drugs can take place simultaneously.
Because of the affinity of nitro-aryl drugs (xenobiotics) for the endoplasmic reticulum, we propose this subcellular
organelle as a good biological system for investigating the toxicity induced by the biotransformation of these
or another compounds.
In this work we used rat liver microsomes to assess the oxidative stress induced by nitro-aryl drug bio-
transformation. Incubation of microsomes of rat liver with nifurtimox and nitrofurantoin in the presence
of NADPH induced lipoperoxidation, UDP-glucuronyltransferase activation and an increase in the basal
microsomal oxygen consumption. Nitro-aryl-1,4-dihydropyridines did not elicit these prooxidant effects; fur-
thermore, they inhibited lipoperoxidation and oxygen consumption induced by Fe
3+
/ascorbate. Nifurtimox and
nitrofurantoin modified the maximum absorption of cytochrome P450 oxidase and inhibited p-nitroanisole O-
demethylation, an oxidative reaction catalysed by the cytochrome P450 system, signifying that oxidation may
proceed in a similar way to that described for nitro-aryl-1,4-dihydropyridines. Thus the balance between
lipophilic nitro-aryl drug oxidation and reduction may be involved in the potential oxidative stress induced by
biotransformation.
INTRODUCTION
Nitro-aryl compounds have enjoyed widespread use in
medicine as antibiotics, radiosensitizers and antibacterial
and antiprotozoal agents. Under aerobic conditions, one
of the biotransformation pathways of these compounds
appears to be reduction of the nitro group, a reaction that
leads to a ‘futile metabolism’. Nitro-aryl reduction has been
described in different subcellular organelles — microsomes,
mitochondria and cytosol — and there is direct proof that
a one-electron reduction can provoke the formation of
a superoxide anion (O
2
·
-
) and a hydroxyl radical (
·
OH)
(Moreno et al., 1984; Docampo et al., 1988; Iwata et al.,
1992). It is widely accepted that the generation of reactive
oxygen species (ROS) without their efficient removal can
lead to oxidative modification of proteins, lipids and DNA,
which may alter their biological functions (Neuzil et al.,
1993). The nitro-anion radical (NO
2
·
-
), the first intermedi-
ate of the nitro-reduction pathway, can react with mole-
cular oxygen to regenerate the original nitro-compound,
forming O
2
·
-
and
·
OH as by-products. Accordingly, it has
been suggested that intracellular reduction of nifurtimox
explains both its trypanocide action and its toxicity in
mammals (Núñez-Vergara et al., 1997; Docampo, 1990). A
similar hypothesis has been proposed to explain the toxic-
ity of nitrofurantoin, an antibacterial drug (Hoener et al.,
1989; Foth, 1995; Amit et al., 2002). However, the -NO
2
·
-
intermediate may continue in the reductive pathway lead-
ing to the nitroso-derivative (Wardman, 1985; Docampo
et al., 1988; Orna and Mason, 1989) with no apparent
toxicological consequences. Nevertheless, not all nitro-
compounds seem to suffer nitro-reduction as an important
metabolic pathway. Thus, the adverse effects described
for nitro-aryl dihydropyridines (N-1,4-DHPs), which are
calcium channel antagonists, have not been associated
with oxidative stress (Messerli, 2002); moreover, these
drugs are administered to cardiovascular patients over long
periods and different authors have demonstrated that
N-1,4-DHPs can induce antioxidant protective effects in
cardiac and liver membranes and brain slices (Janero and
Burghardt, 1988; Engineer and Sridhar, 1989; Díaz-Araya
et al., 1998).