[CANCER RESEARCH 45, 6328-6330, December 1985]
Photoenhancement of Lipid Peroxidation Associated with the Generation of
Reactive Oxygen Species in Hepatic Microsomes of Hematoporphyrin
Derivative-treated Rats1
Mukul Das,2 Hasan Mukhtar, Emily R. Greenspan, and David R. Bickers
Department of Dermatology, University Hospitals of Cleveland, Case Western Reserve University, and Veterans Administration Medical Center, Cleveland, Ohio 44106
ABSTRACT
Hepatic microsomes prepared from rats pretreated with he-
matoporphyrin derivative (HPD) undergo rapid enhancement of
lipid peroxidation in the presence of solar radiation (~400 nm).
Quenchers of singlet oxygen, including 2,5-dimethylfuran, histi-
dine, and 0-carotene, and inhibitors of the hydroxyl radical,
including benzoate, mannitol, and ethanol, largely protected
against the enhancement of lipid peroxidation caused by HPD
photosensitization. Catalase, a scavenger of hydrogen peroxide
and Superoxide dismutase, a scavenger of Superoxide anión,
had little or no protective effect against HPD-photosensitized
enhancement of lipid peroxidation. Our data indicate that in vitro
irradiation of hepatic microsomes prepared from HPD-treated
rats results in the generation of both singlet oxygen and hydroxyl
radical. These reactive moitiésare associated with a rapid in
crease in microsomal lipid peroxidation which may explain the
unique susceptibility of membranous components of cells to this
type of phototoxic injury.
INTRODUCTION
HPD,3 a mixture of several porphyrin moitiésprepared from
hematoporphyrin, is being increasingly used as an approach to
the management of malignant tumors (1, 2). It is believed that
malignant cells may selectively take up porphyrins and that
porphyrin photosensitization generates reactive oxygen species
which can result in the oxidation of essential cellular components
including proteins, lipids, amino acids, and nucleotides (3, 4).
Although the subcellular site of porphyrin-induced cytotoxicity
has not been ascertained, prior studies have shown that HPD
photosensitization results in the destruction of mitochondria!
cytochrome c oxidase (5). Furthermore, studies from our labo
ratory have verified that the microsomal hemeprotein, cyto
chrome P-450, is destroyed by HPD photosensitization (6).
Lipid peroxidation has been broadly defined as the oxidative
deterioration of polyunsaturated lipids (7). The peroxidation of
lipids can be highly catastrophic to the integrity of cellular mem
branes and to membrane-bound enzymes (8, 9). It is believed
that lipid peroxidation of biomembranes is one mechanism
whereby a foreign chemical may be toxic to cells, and this has
evoked considerable interest in understanding the mechanism of
this phenomenon in various biological systems (8, 9). Since lipid
peroxidation is thought to be an essential marker for microsomal
membrane damage, we attempted to determine whether HPD
Received 1/8/85; revised 8/23/85; accepted 9/9/85.
1 Supported by NIH Grants CA 34368, ES-1900, and CA-38028 and by research
funds from the Veterans Administration.
1 Recipient of the Burroughs Wellcome Fund fellowship award from the Derma
tology Foundation. To whom requests for reprints should be addressed, at Veterans
Administration Medical Center, 10701 East Boulevard, Cleveland, OH 44106.
3 The abbreviations used are: HPD, hematoporphyrin derivative; 2,5-DMF, 2,5-
dimethylfuran; D;.O. deuterium oxide; MDA, malonyldialdehyde.
photosensitization could alter endogenous lipid peroxidation. Our
studies indicate that hepatic microsomal lipid peroxidation is
significantly enhanced by reactive oxygen species generated
during HPD photosensitization. These results suggest that en
hancement of lipid peroxidation in microsomal membranes may
contribute to cell cytotoxicity evoked by HPD-induced photosen
sitization. Such a response could play a role in the antineoplastic
effect of photoradiation therapy with this compound.
MATERIALS AND METHODS
Chemicals. Histidine, 2,5-dimethylfuran, 0-carotene, Superoxide dis
mutase, catalase, mannitol, benzoate, and D2O were obtained from
Sigma Chemical Company, St. Louis, MO. Hematoporphyrin dihydro-
chloride was a product of Porphyrin Products, Logan, UT. All other
chemicals were of highest purity commercially available. HPD was pre
pared essentially by the method of Lipson ef a/. (10) as described earlier
(6).
Animals and Preparation of Hepatic Microsomes. Adult male Spra-
gue-Dawley rats (100 ±10 g) were obtained from Holtzman Rat Farm,
Madison, Wl. Rats were given injections i.p. of HPD (20, 40, 60, 80 mg/
kg of body weight). In most of the experiments performed, a HPD dose
of 80 mg/kg of body weight was used as described by Gibson and Hilf
(5). The control animals received an equal volume of vehicle. The animals
were kept in the dark and were sacrificed by cervical dislocation 2 h after
treatment with HPD. Hepatic microsomes were prepared according to
the conventional method (11). The twice washed microsomal pellet was
suspended in 0.1 M phosphate buffer prepared in D20 containing 10~4 M
MgCI2. The protein concentration in the samples was determined ac
cording to the method of Lowry ef a/. (12) using bovine serum albumin
as reference standard.
Exposure of Microsomes from HPD-treated Rats to UV Light. The
microsomal suspension was brought to a protein concentration of 1 mg/
ml. Photooxidation was performed using a Model B-1000-A black-ray
long-wave UV lamp which has an emission spectrum between 380 and
420 nm; light intensity was determined using a black-ray long-wave UV
meter (Ultraviolet Products, Inc.). The HPD-treated microsomes were
exposed to the UV light source at an intensity of 50 W/m2 at 0-4°C (the
reaction vessel was immersed in crushed ice throughout the incubation).
Assay of Lipid Peroxidation. Lipid peroxidation in hepatic microsomal
preparations from control and HPD-treated rats was assessed by mea
suring the formation of MDA as described by Wright ef al. (13). The
following modifications were made. Lipid peroxidation was measured by
incubating 0.5-0.7 mg of microsomal protein in 0.6 ml of Ca2+-free 0.1
M phosphate buffer, pH 7.4, containing 10~4 M MgCI2 for 10 min at 37°C.
The reaction was terminated by the addition of 0.6 ml of 10% (w/v)
trichloroacetic acid. One ml of 0.5% (w/v) 2-thiobarbituric acid was added
to the reaction mixture which was then heated for 10 min in a boiling
water bath. Samples were cooled under running tap water and centri-
fuged, and the levels of MDA were measured by estimating the formation
of color at 535 nm. The concentration of MDA was calculated by using
a molar extinction coefficient of 1.5 x 10* M~V
All buffers used in this study were prepared in D2O unless otherwise
stated. Quenchers of activated oxygen were also prepared in D2O buffer.
CANCER RESEARCH VOL. 45 DECEMBER 1985
6328
Research.
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