[CANCER RESEARCH 50. 1779-1785. March 15, 1990]
Multidrug Resistance Phenotype of Human BRO Melanoma Cells Transfected with
a Wild-Type Human mdrl Complementary DNA1
Carsten R. Lincke, Alexander M. van der Blick, Gerrit J. Schuurhuis, Trijntje van der Velde-Koerts,
Jaap J. M. Smit, and Piet Borst1
Division of Molecular Biology, The Netherlands Cancer Institute, 1066 CX Amsterdam, The Aether/ana's [C. R. L., A. M. v. d. B., T. \: d. V-K., J. J. M. S., P. B.];
Department of Biochemistry; L'niversity of Amsterdam, 1105 AZ Amsterdam, The Netherlands f( '. K. I..J; and Department of Oncology, Free L'nirersily of Amsterdam,
1007 MB Amsterdam, The Netherlands [G. J. S.¡
ABSTRACT
We have transfected a eukaryotic expression vector containing a mdr\
complementary DNA isolated from normal human liver into human BRO
melanoma cells to study the drug-resistant phenotype produced by the
exclusive overexpression of normal human mdr\ P-glycoprotein. The
drug resistance pattern of mdr\ -transfected clones includes relatively
high resistance to gramicidin D (about 300-fold), vincristine (about 100-
fold), and actinomycin D (about 100-fold) and a lower degree of resistance
to doxorubicin (about 10-fold), VP16-213 (about 10-fold), and colchicine
(about 6-fold). The transfectants did not exhibit resistance to trimetrex-
ate, CIS-platinum, mitomycin C, l-/3-i)-arabinofuranosylcytosine, bleo-
mycin, G418, or magainin-2-amide; they were slightly more sensitive to
verapamil (2-fold) but not to Triton \-100. As in other multidrug-
resistant cell lines, resistance to vincristine could be reversed by verapa
mil and, more effectively, by cyclosporin A. Chloroquine only marginally
increased drug sensitivity in mdr\ -transfected cells. Gramicidin D resist
ance was also reversed by verapamil, suggesting that the mechanism of
resistance to this polypeptide antibiotic is similar to that of other drugs
transported by P-glycoprotein. Thus, expression of the wild-type mdrl
complementary DNA induces a drug-resistant phenotype similar to that
induced by mdrl complementary DNAs isolated from drug-resistant cell
lines with relatively low colchicine resistance. As other cell lines may
display a different pattern of drug resistance, it is clear that other
resistance mechanisms or cell type-specific factors may modulate the
resistance. mdr\ -transfected cell lines provide a convenient tool for the
identification of P-glycoprotein-mediated phenomena.
INTRODUCTION
The MDR4 phenotype of mammalian cell lines selected for
drug resistance in vitro by exposure to a single chemotherapeu-
tic agent can be brought about by overproduction of a P-
glycoprotein (1-4). Direct experimental evidence for this has
been obtained by DNA- and chromosome-mediated transfer of
the MDR phenotype from drug-resistant to drug-sensitive re
cipient cells (5-9) and by transfection of cDNAs of a mouse
mdr gene (the homologue of hamster pgp2) and the human
mdr\ gene derived from drug-resistant cells (9-14). P-Glyco-
proteins appear to act as membrane-bound ATP-consuming
drug-efflux pumps, capable of transporting a wide variety of
structurally and functionally unrelated substances across the
plasma membrane (10, 15-17).
Received 8/2/89; revised 12/1/89.
The costs of publication of this article were defrayed in part by the payment
of page charges. This article must therefore be hereby marked advertisement in
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1This work was supported in part by Grant NKI 88-6 of The Netherlands
Cancer Foundation to P. B.
: Present address: Division of Biology. 156-29, California Institute of Tech
nology, Pasadena. CA 91125.
3To whom requests for reprints should be addressed, at the Division of
Molecular Biology, The Netherlands Cancer Institute. Plcsmanlaan 121. 1066
CX Amsterdam. The Netherlands.
4The abbreviations used are: MDR. multidrug resistance; SDS, sodium do-
decyl sulfate; SSC, standard saline citrate (150 mM NaCI:15 mM sodium citrate.
pH 7); PBS. phosphate-buffered saline (137 mM NaCI:2.68 mM KCI:8.06 mM
NajHPO.:1.47 mM KH^O«); cDNA. complementary DNA; 1C,», concentration
of drug at 50% growth inhibition compared with cells grown in the absence of
drugs as determined in a 5-day growth inhibition assay in the continuous presence
of drugs.
The cross-resistance patterns and the relative resistance of
MDR cell lines that overexpress P-glycoprotein may vary con
siderably, but include resistance to colchicine, anthracyclines,
Vinca alkaloids, and actinomycin D in all cases examined so
far (1). In a few cases cross-resistance to various other drugs,
like melphalan (18, 19), methotrexate (20). and trimetrexate
(21) has been found in MDR cell lines selected for drug resist
ance in vitro. Furthermore, reversal of MDR by calcium channel
blockers like verapamil, most likely due to competition for
binding to P-glycoprotein, is consistently observed in MDR
cells (reviewed in Refs. 3 and 4).
Thus far, it is not clear what factors contribute to or deter
mine the variability of the MDR phenotype. A point mutation
in the human mdrl gene has been shown to selectively increase
the degree of resistance for the drug used for selection (22).
Other mechanisms expected to modulate the cross-resistance
pattern of MDR cells are the differential (over-)expression of
multiple or differentially spliced P-glycoprotein genes (23, 24)
that might differ in substrate specificity. "Atypical" MDR cell
lines have also been described. These do not overexpress P-
glycoprotein, and their cross-resistance patterns only partially
match the P-glycoprotein-mediated pattern (25-28). Although
this type of drug resistance can be due to altered topoisomerase
II activity (29, 30), this does not appear to explain the atypical
MDR phenotype of all cell lines described (27, 28). The cross-
resistance pattern of a MDR cell might also be a composite of
several of these mechanisms acting in concert.
To distinguish between effects mediated by the wild-type
mdr\ gene and those of other alterations we transfected a full-
length human mdrl cDNA from normal human liver into BRO
melanoma cells. Here we describe the MDR phenotype of these
transfectants.
MATERIALS AND METHODS
Cell Culture. The transfection of human BRO melanoma cells (31)
with a full-length mdrl cDNA was previously reported (32). This cDNA
was inserted into a eukaryotic expression vector providing the imme
diate early gene promoter-enhancer of human cytomegalovirus up
stream of the cDNA and, downstream, the hepatitis B virus polyade-
nylation signal, kindly provided by Dr. F. Meyer (Zurich, Switzerland).
BRO cells were grown in Dulbecco's modified Eagle's medium supple
mented with 4 mM l.-glutamine, penicillin (50 units/ml), streptomycin
(50 Mg/ml), and 10% fetal calf serum in the presence of 5% CO2.
Subculture was every 3 to 4 days. Transfected clones were selected and
expanded in the presence of 10 n\t vincristine. The non-small cell lung
carcinoma cell lines SW-1573, originally isolated by Dr. A. Leibovitz
(Temple, TX), and SW-1573-500 (33) were cultured as described (34).
The human ovarian carcinoma cell lines A2780 and 2780AD (35) were
obtained from Dr. R. F. Ozols (Bethesda. MD), and were grown in
RPMI 1640 with 10% fetal calf serum, the latter in the presence of 2
JIMdoxorubicin.
Chemicals. Doxorubicin (doxorubicin hydrochloride), chloroquinc.
colchicine, cytarabine (1-ß-D-arabinofuranosylcytosine), gramicidin D,
lidocaine. melphalan, and vincristine sulfate were purchased from
1779
Research.
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