[CANCER RESEARCH 50. 4533-4538, August 1, 1990]
Effect of Sulfonation on the Cell and Tissue Distribution of the Photosensitizer
Aluminum Phthalocyanine
Wai-Shun Chan,1 John F. Marshall, Rüssel Svensen, Joanne Bedwell, and Ian R. Hart
Biology of Metastasis Laboratory; Imperial Cancer Research Fund, Lincoln's Inn Fields, London, WC2A 3PX [W-S. C., J. F. M., I. R. HJ; Royal Institution of Great
Britain, 21 Albermarie Street, London, WIX 4BS [R. S.J; and The Rayne Institute, Faculty of Clinical Sciences, University College London, London,
United Kingdom [J. BJ
ABSTRACT
Aluminum sulfonated phthalocyanine has potential as a suitable pho-
tosensitizer for use in the photodynamic therapy of cancer. In the present
study, cellular uptake and retention of the individual mono-, di-, tri-, and
tetrasulfonated derivatives ( \IS, jIY) were examined in tissue culture
and in normal and neoplastic tissue of tumor-bearing mice. Uptake and
retention of the various derivatives by cells in tissue culture correlated
inversely with the degree of sulfonation. Accordingly, Colo 26 cells in
monola j er culture, 24 h after addition of 10 ;JMof appropriate photosen-
sitizer, had accumulated approximately 25-fold more VIS,IV than \IS ,1V-
and retained this species longer than more sulfonated derivatives. In
contrast to these in vitro results, it was found that Colo 26 growing s.c.
in BALB/c mice accumulated photosensitizer to a greater extent when
the degree of sulfonation increased, such that AlS«Pc > AlS3Pc > AlS2Pc
> AlS,Pc. By 24-48 h after the i.v. injection of 0.1 ml 2.27 mM solution
of individual photosensitizer, the relative ratios of tumoradjacent tissue
varied from >10:1 to <2:1, showing that selective tumor uptake may be
affected profoundly by the composition of the phthalocyanine compound.
The livers and spleens of both normal and tumor-bearing mice, unlike
other normal tissue, took up the sulfonated derivatives in an order that
provided a mirror image of that observed in neoplastic tissue. These
complex in vivo distribution and retention characteristics appear to be a
consequence of relative hydrophilicity/hydrophobicity properties of the
sulfonated species and indicate the extent to which these characteristics
may influence photosensitizer distribution and accumulation.
INTRODUCTION
Metallophthalocyanines are porphyrin-like, photoactivatable
dyes with strong red light absorption characteristics, which
have been considered as second generation photosensitizers for
the PDT2 of cancer (for review, see Refs. 1-4). Because most
metallo-Pc are poorly soluble in water, they are not suitable for
clinical administration. Problems of insolubility can be over
come by the use of specific carrier vehicles, such as entrapment
of monomeric form Pc in unilamellar vesicles (5), or by the
creation of water-soluble derivatives. This latter change can be
achieved by the addition of substituents like amino, carboxylic
acid, and sulfonate groups to the outer ring of the isoindole
units. To date, the sulfonated derivatives have been the most
commonly used, since their synthesis is relatively easy, although
subsequent purification may be difficult. One such sulfonated
derivative, AlSPc, that we have been investigating is capable of
photoinactivating cells in tissue culture (6), exhibits good tu
mor-localizing capacity (7, 8), and can be used to achieve
marked reduction in tumor burden of various murine tumors
of different histológica! origins (7). This dye, therefore, seems
to have considerable potential as a photosensitizer for use in
PDT.
Received 12/18/89; revised 4/6/90.
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' To whom requests for reprints should be addressed.
2 The abbreviations used are: PDT. photodynamic therapy; AIS.Pc, chloroal-
uminum sulfonated phthalocyanine with n sulfonate groups: AlSPc. a mixed
sulfonate preparation of chloroaluminum sulfonated phthalocyanine; ex/em, ex
citation/emission; HPLC, high pressure liquid chromatography; PBS, phosphate-
buffered saline; Pc, phthalocyanine(s).
However, the AlSPc used in our studies, and in studies from
other groups which also have demonstrated the possible utility
of this agent (9-11), consisted of a mixture of mono-, di-, tri-,
and tetrasulfonated derivatives. It would seem to be important
to know which derivative(s) is (are) responsible for the observed
biological activities. Some of the in vitro characteristics of the
individual species have been investigated (12-14), although to
date there is little information on the in vivo behavior of these
various agents (15) and nothing on their distribution patterns.
In this paper, we report not only the uptake of individual
derivatives of AlSPc by cells in vitro but also their in vivo uptake
and retention by normal and neoplastic tissue in tumor-bearing
mice.
MATERIALS AND METHODS
Photosensitizer Preparation. AlSPc was obtained from Ciba-Geigy
Dyestuffs and Chemicals (Basel, Switzerland). This material was a
complex mixture of mono- to tetrasulfonated derivatives; according to
the supplier, it had an average of three sulfonate groups. Individual
chloroaluminum mono-, di-, and trisulfonated derivatives (AlSiPc,
AlS2Pc, and AlS3Pc, respectively) were purchased from Porphyrin
Products (Logan, UT). Chloroaluminum tetrasulfonated Pc (AlS4Pc)
was prepared by condensation of aluminum trichloride with four equiv
alents of sulfophthalic acid (monosodium salt) using the modified
technique of Weber and Busch (16). Stock solutions of all of the dyes
were prepared at 2-4 mg/ml in PBS, except the water-insoluble AlSiPc,
which was dissolved to the same concentration in either 40% (v/v)
ethanohPBS (for in vivo studies) or in dimethylformamide (for in vitro
studies). Solutions were sonicated for 3-5 min, heated at 100°C for 5-
10 min, and then stored at 4°Cin darkness. Stock solutions were
measured spectrophotometrically (diode array spectrophotometer,
model 8452A; Hewlett-Packard, Palo Alto, CA) after 10 ^1 of stock
solution had been diluted in 9.990 ml 0.1 M NaOH [in the case of
AIS iPc, the diluent was the same volume of a 3:1 (v/v) mixture of
absolute ethanol:0.1 M NaOH]. Molarity of the AlS2Pc solution was
calculated from absorbance at 666 nm and a molar extinction coefficient
(17):
E = 1.5x 105M-'cm-'
In order to determine the molarity of the solutions of the other
derivatives, the area under the curve obtained by measuring absorbance
between 500 and 750 nm was compared to that obtained with AlS2Pc.
HPLC Analysis. Analysis of the individual Pc species was by re
verse-phase HPLC essentially as described elsewhere (18). Briefly, the
various sulfonated Pc were dissolved in 10 mM NaOH, buffered with
10 mM phosphate to pH 5, filtered (Waters HV 0.45 microfilters
SJHVD43N3), and then injected onto a reverse-phase column (Waters
NOVA-PAK C-18 radial compressed unit). Samples were resolved by
a gradient mode elution (0-80% methanol in 10 mM phosphate buffer)
over an 18-min run period. Eluted Pc were detected by absorption
measurements at 365 nm.
Tumor Cells. Colo 26 cells from a murine colorectal carcinoma,
syngeneic to BALB/c mice, were passaged routinely in E4 growth
medium containing 10% fetal calf serum exactly as detailed previously
(7).
Animals. Specific pathogen-free BALB/c mice were obtained from
the Imperial Cancer Research Fund breeding unit. For individual
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