[CANCER RESEARCH 45, 2450-2455, June 1985]
Evidencefrom Rat Hepatocytesof an UnrecognizedPathwayof 5-Fluorouracil
Metabolismwiththe Formationof a GlucuronideDerivative1
Jean-Pierre Sommadossi,2 David S. Cross, David A. Gewirtz, I. David Goldman, Jean-Paul Cano, and
Robert B. Diasio3
Department ot Pharmacology and Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, Alabama 35294 [J-P. S., R. B. D.J; Departments of
Medicine and Pharmacology, Medical College of Virginia, Richmond, Virginia 23298 [D. S. C., D. A. G., I. D. G.J; and The Institut National de la Sante et de la Recherche
Medicale U278, Laboratoire de Pharmacocinetique et Toxicocinetique, 73385 Marseille Cedex 5, France [J-P. S., J.-P. C.]
ABSTRACT
Isolated rat hepatocytes in suspension were exposed to [3H]-
5-fluorouracil for intervals over 2 h, following which the cells
were removed from the media and sonicated, and the cytoplasm
was sampled. High-performance liquid chromatography was
used to separate 5-fluorouracil (FUra) from its known anabolites
and catabolites, with subsequent quantitation of these metabo
lites by measurement of radioactivity. As the extracellular con
centration of FUra was increased above 30 UM, the intracellular
levels of FUra increased, with detection of a new peak of radio
activity distinct from any of the known anabolites or catabolites.
This new metabolite, "G," increased in concentration as the
extracellular concentration of FUra was raised above 1 mw.
Inhibition of FUra catabolism by 2 mw thymine resulted in a
further increase in intracellular FUra (approaching the extracel
lular FUra concentration) and was accompanied by a further
increase in the intracellular concentration of "G," demonstrating
that "G" was not formed via the catabolic pathway. The increase
in intracellular FUra and "G" was not accompanied by an increase
in intracellular anabolites, suggesting that "G" was formed via a
novel metabolic pathway. "G" was retained within the hepato
cytes, although it was not bound to intracellular macromolecules.
"G" was converted to FUra in the presence of ß-o-glucuronidase;
this reaction was inhibited with the addition of saccharo-1,4-/3-
lactone, a specific inhibitor of the 0-D-glucuronidase. This data,
together with evidence from hepatocyte homogenates in which
formation of "G" was shown to be dependent on the concentra
tion of uridine-5'-diphosphoglucuronic acid, demonstrates that
"G" is a glucuronide of FUra. The formation of "G" suggests that
FUra is metabolized via a previously unrecognized metabolic
pathway.
INTRODUCTION
Since the synthesis of FUra4 25 years ago, most studies of
fluoropyrimidine metabolism have concentrated on anabolism,
focusing on the conversion of FUra or its nucleosides to ribosyl
or deoxyribosyl nucleotides and the subsequent effects on DNA
or RNA synthesis or function (2, 12-15, 19, 22, 23, 28). In
1This work was supported by NIH Grants CA 23412, CA 40530, CA 16906,
and AM 18976.
2 Supported in part by the National Cancer Institute, Scientist Exchange Program
G 50111 (United States-France Cancer Program).
3 To whom requests for reprints should be addressed, at Division of Clinical
Pharmacology, University of Alabama in Birmingham, Birmingham, AL 35294.
4 The abbreviations used are: FUra, 5-fluorouracil; FUH2, dihydrofluorouracil;
PUPA, a-fluoro-0-ureidopropionic acid; FBAL, «-fluoro-0-alanine; "G," unknown
metabolite of FUra thought to be a glucuronide derivative of FUra; HPLC, high-
performance liquid chromatography; UDPGA, uridine 5'-diphosphoglucuronic acid.
Received 10/22/84; revised 2/14/85; accepted 2/21/85.
contrast, until recently, there have been few studies (3, 4, 21)
that have examined FUra catabolism, despite the fact that, in
humans, approximately 90% of administered FUra is metabolized
via the pyrimidine catabolic pathway (2), with the major site of
FUra catabolism believed to be in the liver (7).
The development of a highly specific HPLC methodology that
can rapidly resolve all of the known anabolites and catabolites
of FUra has permitted a reexamination of fluoropyrimidine me
tabolism (26). We have recently demonstrated the usefulness of
the isolated rat hepatocyte model for studying fluoropyrimidine
metabolism because of its excellent agreement with the meta
bolic fate of FUra in humans (6). In a previously reported study
(26), hepatocytes in suspension were exposed to 30 fiM FUra [a
concentration corresponding to that found after systemic admin
istration of FUra (2, 6)]. Intracellular and extracellular FUra and
its metabolites were quantitated, demonstrating a transport-
limited, rapid, and complete conversion of FUra to FUH2, with
FUH2 being the major intracellular catabolite, with subsequent
conversion to FUPA and then to FBAL, but with no evidence for
FUra anabolism (26).
In order to better understand the metabolism of FUra at the
hepatic site with concentrations more representative of FUra
levels achieved following various clinical regimens, including i.v.
bolus injection (2), studies were undertaken with FUra concen
trations higher than 30 /*M. In the present study, we demonstrate
that, as extracellular FUra is increased, the catabolic enzyme
dihydrouracil dehydrogenase (EC 1.3.1.2) becomes saturated,
resulting in increased intracellular levels of FUra. However, this
is not accompanied by evidence of increased anabolism. Most
notable is the appearance of a new metabolite distinct from any
of the known anabolites or catabolites of FUra that appears to
be a glucuronide of the FUra base formed via a previously
unrecognized metabolic pathway.
MATERIALS AND METHODS
Chemicals
[6-3H]FUra (20 Ci/mmol) was obtained from Moravek Biochemicals,
Inc. (City of Industry, CA) and purified by the HPLC technique described
below. [Carboxyl-14C]inulin (2.5 Ci/g) was purchased from Amersham-
Searie Corp. (Irvine, CA). FUra and authentic standards of FUH2, FUPA,
and FBAL were kindly supplied by Hoffmann-La Roche Laboratories
(Nutley, NJ and Basel, Switzerland). /3-o-Glucuronidase (from bovine
liver, type B-3), saccharo-1,4-0-lactone, and thymine were purchased
from Sigma Chemical Co. (St. Louis, MO). All other chemicals used were
reagent grade.
CANCER RESEARCH VOL. 45 JUNE 1985
2450
Research.
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