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Photodynamic therapy (PDT) has been used experimentally in cancer patients since 1976, with an estimated 3,000-4,000 patients treated world-wide, most since 1982. Phase III, comparative randomized clinical trials are under way for regulatory approval of Photofrin® II, a purified version of hematoporphyrin derivative (Hpd). Several recent advances in both the clinical application of PDT and basic understanding of mechanisms are noteworthy. For example, it is now recognized that the photosensitizer undergoes photobleaching during treatment which may provide a therapeutic advantage in treatment. Clinical trials using lower drug doses seem to be consistent with this expectation. Advances in light delivery systems and dosimetry have also been achieved. It is now clear that in at least some experimental animal tumors, destruction of the vasculature system in both the tumor and surrounding normal tissue is necessary for 'cure', a process which may involve release of inflammatory and other factors. It is unclear if this is relevant to humans. Because of the problem of cutaneous photosensitivity and other factors, a search for other photo-sensitizers is being carried out by several groups, with early encouraging results being reported for certain phthalocyanines, purpurins and others.
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In-vitro studies have been performed to compare the mode of action of porphyrin induced photodynamic therapy and hyperthermia. Parent and temperature resistant clones of Chinese hamster and mouse fibrosarcoma cells were treated with either PDT or hyperthermia. Quantitative survival curves obtained from these experiments indicate that temperature resistant cells are not cross resistant to PDT even though both treatments induce the synthesis of stress proteins. In-vivo studies were performed to evaluate the photosensitizing efficiency to mono-l-aspartyl chlorin e 6 (NPe6). Tumor response and normal skin response were determined using a murine tumor system. The studies indicate that NPe6 is an extremely effective tumor photosensitizer with rapid in-vivo clearance properties which may eliminate the side effects of prolonged and systemic skin photosensitivity.
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There is growing interest in photodynamic therapy as a method for the local control of certain human neoplawv.1 New photosensitizers for this form of therapy are currently undergoing experimental evaluation2,3,q. We have found that the purpurins are effective in the control of several experimental animal systems -5 In order to determine the effect of the purpurins on normal tissue, rat footpad and jejunum at therapeutic light levels and murine skin under sunlight equivalence were studied.
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The translocation and localization pattern of hematoporphyrin derivative (HpD) in human bladder tumor cells (MGH-U1) in culture was evaluated using fluorescence microscopy and interactive laser cytometry. The qualitative and quantitative fluorescence labelling patterns of HpD were compared with other fluorescent dyes specific for subcellular localization sites. Labelling of MGH-U1 cells with HpD initially showed fluorescence at the cell membrane. Later, diffuse perinuclear fluorescence was evident in these cells. This fluorescent staining pattern did not appear to be site-specific to either the mitochondria or endoplasmic reticulum but appeared to be generally distibuted to the cytomembranous structures of the cell. Lateral diffusion measurements indicated that the fluorescent components of HpD were bound to cellular lipids. These results suggest that HpD may localize in cells in vitro by a spontaneous diffusion process and be distributed to lipophilic sites within the cell.
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In this study, we explore the possible utility of injecting hematoporphyrin derivative (HPD) directly into the tumor as a more effective means of porphyrin administration for photodynamic therapy. A subcutaneously implanted mouse bladder tumor was used as the model. Initially, we compared the tissue distribution of HPD in animals with HPD administered intraperitoneally (I.P.; 20 mg/kg. b.w.) and by direct intratumor injection (I.T., 0.4 mg/cm3 tumor). The concentrations of HPD in tumor and tissues were analyzed at various times after the injection, by 3H-HPD method and by a fluorometric method after dye extraction. Results indicated that at 3 to 96 hours after the administration, HPD levels in tumors were 3 to 15 times higher by I.T. than by I.P. injection, while the concentrations in skin and other tissues were 1.3 to 10 times lower. Consequently, ratios between tumor to skin HPD were up to 100 times higher for I.T. than I.P. injection. Subsequently, the photodynamic effect on tumors treated with I.T. injection of HPD was examined. Tumor cell killing, measured by cell survival, was observed in both the I.T. and I.P. groups to about the same extent, and was dependent on fluence and HPD dosage. There was no significant enhancement of cell killing observed in the I.T. injected tumors, despite 5 to 10 times higher porphyrin levels in these tumors. Histological examination of the effect of PDT on the blood vessels indicated that while cell death accompanied severe hemorrhage in the I.P. injected tumors, in the I.T. tumors there was much less hemorrhage and intact blood vessels remained. This observation suggests that with I.T. administration, direct photodynamic action may play a significant role in the tumor cell killing, in contrast to systemic administration, in which destruction of the blood vessels is believed to be the main cause of tumor destruction. This method of sensitizer administration may have utilities in the treatment of most single lesions that are accessible for direct injections as well as an experimental model for evaluating potencies of new photosensitizers and studying mechanisms involved in photo-destruction of tumors.
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We have investigated a novel and efficient delivery system utilizing photosensitizer-coupled-latex microspheres to photochemically target and kill phagocytic trabecular meshwork (TM) cells. TM cells are the most actively phagocytic cells within the anterior chamber of the eye and are located within an optically accessible discrete band. This delivery system, along with the property of cell photocytosis, will achieve double selectivity by combining preferential localization of the photosensitizer to the target cells with spatial localization of illumination on the target cells. All experiments were performed with preconfluent bovine TM cells, 3rd to 4th passage, plated in 15 mm wells. Chlorin e6 monoethylene diamine monoamide was conjugated to the surface of 1.0 Am MX Duke Scientific fluorescent latex microspheres. Spectroscopic analysis revealed an average of 1.3 x 10 -17 moles of chlorin e6 per microsphere. TM cells were incubated for 18 hours with 5 x 10 7 microspheres/ml in MEM with 10% FCS, washed with MEM, and irradiated through fresh media using an argon-pumped dye laser emitting .2 W at 660 nm. A dose-survival study indicated that energy doses of 10 J/cm2 or greater resulted in greater than 95% cell death as determined by ethidium bromide exclusion. Cell death could be demonstrated as early as 4 hours post-irradiation. TM cells incubated with a solution of chlorin e6 at a concentration equal to that conjugated to the microspheres showed no cell death. Unirradiated controls also showed no cell death.
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Increased selectivity and efficacy in photochemotherapy may be achieved by the use of monoclonal antibodies (Mabs) bound to chromophores. Due to their antigen recognition capabilities, Mabs can potentially deliver higher concentrations of chromophores to target tissue while sparing normal tissue. A brief review of the current status of antibody-mediated selective phototoxicity is presented.
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Rhodamine-123 (R123) and tetrabromo-R123 (TBR) have been evaluated in vitro as potential photosensitizers. R123 localizes selectively in mitochondria of MGH-V1 bladder carcinoma cells exposed to 10 pM R123 for 30 min, and under these conditions R123 is a weak photosensitizes. Incubation with R123 for longer times enhances its phototoxicity, and is associated with a modification of its intracellular localization. TBR is approximately 100 times more phototoxic than R123, as assessed either by 3H-thymidine uptake or vital staining. Actively proliferating cells are more sensitive to either R123 or TBR phototoxicity than are plateau-phase, confluent cultures.
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The binding of Rhodamine 123 (Rh123), Rhodamine 6G (R6G), and Rhodamine B (RhB) (from the cationic xanthene series) to isolated rat liver mitochondria maintained in State IV respiration in the presence of rotenone (NADH oxidase inhibitor) was monitored by following changes in the fluorescence signal of the dyes. Rh123 and Rh6G bind strongly with quenching, to 0.25 and 0.20, respectively, and red shift of emission maxima by 10 nm. RhB binds much less potently with slight emission enhancement of 1.2. For Rh123 added to 0.5 mg/ml mitochondria' protein, a sigmoidal relationship is obtained between percentage fluorescence quenching and log of Rh123 concentration with a 50% inflection point of 3.5x10-6M, estimating an apparent association constant of 2.9x 105M-1 for Rh123 binding. Addition of 7 uM RhB during Rh123 titration moves the sigmoidal inflection point to higher Rh123 concentrations, suggesting either RhB enhancement of binding of Rh123 fluorescence quenching by energy transfer to RhB bound. These results suggest that, to a great degree, the binding of the xanthene dyes to mitochondrial sites is specific, competitive, and probably cooperative.
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We have shown previously that the cationic cyanine dye, EDKC, which photosensitizes malignant cells in vitro and in vivo, blocks respiration in isolated murine liver mitochondria by preferentially inactivating Complex I mediated electron transport. The present work was directed towards examining whether the killing of malignant cells with EDKC and visible radiation was a result of irreparable damage to mitochondria of these cells. We report that EDKC selectively photosensitizes respiration of squamous carcinoma and melanoma cells in vitro. At 0.1 uM, the dye inhibited basal respiration, however, an uncoupler, FCCP, reverted the respiration rate to the control uncoupled rate. Furthermore, the basal respiration of control or EDKC treated cells was totally inhibited by oligomycin, an inhibitor of FoFiATPase, indicating that the respiration was coupled to phosphorylation. After irradiation with 700 + 20 nm light (14 J/cm2) in the presence of 0.1 uM dye, basal respiration was slightly enhanced compared to that of the dye treated cells, however, FCCP-stimulated respiration was drastically lowered. In addition, only 10-20% of the basal respiration was blocked by oligomycin, indicating that a major part of respiration was no longer coupled to phosphorylation. Furthermore, almost no recovery of the mitochondria! respiratory function was detected 6 hr after treatment. Respiration of an untransformed monkey kidney cell line (CV-1) was only minimally affected by ten fold higher dye concentration (1 uM) and 14 J/cm2 radiation.
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A copolymer of N-(2-hydroxypropyl)methacrylamide (HPMA) and N-methacryloylglycine p-nitrophenyl ester (MA-Gly-ONp) was synthesized by radical precipitation copolymerization. Galactosamine was coupled to the polymer by reaction with the active ester side chains. The remaining p-nitrophenyl groups were converted to amine functionalities via a polymeranalogous reaction with an excess of ethylene diamine. Chlorin e6 was activated using a mixed anhydride method and subsequently bound to the modified side chains of the polymer. The photodynamic activity of the conjugate with galactosamine as the targeting moiety was tested in vitro on a human hepatoma cell line: PLC/PRF/5 (Alexander cells). It appears that the conjugate enters the cell interior by receptor mediated pinocytosis via the asialoglycoprotein receptors present on the surface of the PLC cells. Photoactivation of the chlorin containing conjugate with red light proved cytotoxic to the cells. Structure tests comparing the HPMA copolymer-galactosamine-chlorin e6 conjugate and a nontargetable HPMA copolymer-chlorin e6 conjugate, with comparable chlorin e6 content, indicate that the targeted conjugate is more biologically active.
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A new method is described which enhances classical photodynamic action (PA) by adding electricity. Rather than producing singlet oxygen, the electrical enhancement of photodynamic action (EE-PA) drives the photochemical reactions towards the creation of superoxide, and other, oxygen radicals. The benefits of EE-PA over PA are illustrated by reviewing results from four groups of experiments where this process was used either to inactivate Herpes viruses, gliosarcomas, bacteria, or to enable charge transfer to oxidized hemoglobin. The experiments have suggested several advantages of EE-PA over traditional photodynamic action (PA).
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In photochemotherapy, as exemplified by the photodynamic therapy of tumors, a photosensitizing drug is administered to the patient; then, after a period of time to permit the most effective anatomical distribution of the drug, the diseased area is illuminated using an appropriate source of light of wavelengths absorbed by the sensitizer. In the tumor case, this results in the photochemical alteration of critical kinds of biornolecules in the diseased tissue, which interferes with the normal activities of certain cell organelles. This, in turn, leads to the injury or death of diseased cells in the treated area. This paper briefly reviews the reactive chemical species that can be formed in biological systems by illuminated sensitizers (triplet states of sensitizer molecules, free radicals of sensitizers and cellular components, singlet oxygen, superoxide, hydrogen peroxide, hydroxyl radical) and the kinds of biochemical changes they produce in essential cellular molecules (nucleic acids, proteins, unsaturated lipids, etc.). Also reviewed are the effects of these molecular changes on the structure and function of mammalian cell organelles (membranes, mitochondria, nuclear components, etc.) and the mechanisms of the resulting injury or killing of the cells.
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Photosensitized oxidation is the key chemical process which causes cell toxicity in photodynamic therapy. The process is initiated by absorption of light by a sensitizer (Sens) to convert the sensitizer to an electronically excited state (Sens*). There are two principal reaction mechanisms, referred to as Type I or II, depending on whether the initial interaction of Sens* is with substrate or solvent, or with oxygen, respectively. The route actually adopted depends on oxygen and substrate concentration, and on substrate and sensitizer reactivity. Sensitizers may be dyes, pigments such as porphyrins, aromatic hydrocarbons, ketones or quinones, or a variety of other light-absorbing materials. Most types of photodynamic action involve absorption of visible light, although near-UV or infrared light can also be used in some cases.
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Naphthalocyanines are a new class of photodynamic sensitizers that strongly absorb far red light. Using silicon as the central metal atom in the tetrapyrrole ring provides two ligand sites that are perpendicular to the ring plane. These axial sites are thereby useful for synthetically attaching organic residues designed to convey specific solubility properties. Thus by attaching polyethylene glycol units, the resulting molecules show significant water solubility; attaching branched alkyl chains conveys useful lipid solubility.
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Due to the encouraging results with hematoporphyrin in photochemotherapy the porphyrin system gained predominant importance for this important medicinal application. By some convenient chemical reactions hematoporphyrin can be converted to improved derivatives, which are homogeneous, stable, and excellently soluble. Novel enlarged "porphyrinoids" with two, four, and eight additional double bonds inserted into the porphyrin ring system were synthesized. With intensive VIS absorption bands, shifted up to 300 nm to longer wave lengths compared with the normal porphyrins, these porphyrinoids may be promising for more selective and penetrating phototherapy. All the new porphyrin derivatives were shown to be efficient photosensitizers with respect to the production of singlet oxygen.
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For the last several years our research group has concentrated some effort on the xanthene dyes, in particular Rose Bengal. Rose Bengal, 2,4,5,7-tetraiodo-3,'4',5',6'- tetrachlorofluorescein3, was originally synthesized by Gnehm4 as a fabric dye to mimic the red colors in "bengalis"5. Its name is connected to the red symbolic spot worn at the part of the hair by Bengali women to symbolize marriage. Much of the history of Rose Bengal has been reviewed elsewhere7,8.
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Extraction procedures to quantitate Photofrin® II concentration in tissues correlated with fluorescence measurements from instrumentation developed for in vivo fluorimetry were applied for the detection of low drug .levels in occult metastases of the lymph nodes. A sensitive fluorimeter was developed to overcome the limitation of natural background autofluorescence signals. The new device circumvents this limitation by reliably subtracting the normal tissue background signal from the combined fluorescence of DHE and natural background at 630. These techniques have been initially applied to detect low levels of drug in DBA mice bearing the SMT-F tumor, which has been extensively studied in our laboratory. The data show the ability of the techniques to detect very low levels of porphyrin in the tumors after low, non-therapeutic doses of injected photosensitizer. The Pollard rat prostatic adenocarcinoma (PA-III) model was chosen for this study because of its characteristic pattern of metastases involving only ipsilateral lymph nodes. Early studies on this lymph node model have shown the ability of the detection device to measure low levels of drug in non-palpable occult metastases in the nodes. The findings show that the detection of small numbers of metastatic cells is possible (<100 cells) with injected DHE doses of 0.25 mg/kg.
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Simultaneous exposure to the lipophilic photosensitizer, merocyanine 540, and light in the presence of serum (or certain serum components) and oxygen kills leukemia cells, lymphoma cells, neuroblastoma cells, cell-free enveloped viruses, cell-associated enveloped viruses, and virus-infected cells. The same treatment spares pluripotent hematopoietic stem cells, mature erythrocytes, factor VIII, von Willebrand factor, and probably other blood components. Merocyanine 540-mediated photosensitization is now being evaluated clinically as a means to eliminate residual tumor cells from autologous remission bone marrow grafts and preclinically as a means to inactivate pathogenic viruses in blood products.
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Benzoporphyrin derivative (BPD), synthesized from protoporphyrin and involving the formation of Diels-Alder adducts, contains four components, mono and di-acid derivatives of either ring A or ring B fused porphyrins. These compounds have been isolated and tested individually as photosensitizers both in vitro and in vivo. All forms of BPD are potent photosensiters in vitro and have a strong absorption peak at about 690 nm. 3H-BPDs were tested for biodistribution in tumor bearing mice. Distribution appeared to be similar to distribution data published by others for dihematoporphyrin ethers, with the exception that levels in skin were lower for BPD. Extraction of 3H-BPD from tissue, followed by in vitro testing of extracts for photosensitizing activity, indicated that BPD is aTly degraded in vivo. When BPDs were compared to Photofrin II for causing skin photosensitivity following intravenous administration, it was found that monoacid derivatives caused photosensitivity at 3 hours but not after 24 hours. The diacid forms did not cause appreciable skin photosensitivity even at 3 hours. Photodynamic therapy of tumors in mice with BPD showed that these compounds had comparable efficacy to Photofrin II under the experimental conditions used here.
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The photochemical and photophysical properties of purpurins have been investigated. Photophysical measurements indicate that these sensitizers have high quantum yields of long lived triplet excited states which efficiently quench molecular oxygen, giving rise to singlet oxygen. Irradiation of purpurins in light leads to oxidative cleavage of the isocyclic ring to form the corresponding formyl chlorins. In aqueous solutions, it appears that this species then undergoes hydration with a corresponding blue shift in the absorption of band I in the visible spectrum.
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The replament of the oxygen atom in benzophenoxazines with sulfur leads to the corresponding phenothiazinium ehromophorus The effect that this change, as well as other structural alterations, has on photosensitized singlet oxygen formation partitioning coefficient, and in-vitro phototoxicity is presented. A brief discussion concerning how structural modifications can bring about changes in these parameters is also presented. Preliminary results suggest that some phenothiazines could be promising photosensitizers for photodynamic therapy.
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We have investigated the malignant cell selective phototoxicity of some triarylmethane dyes including Victoria Blue BO (VB-BO), Victoria Blue R (VB-R), and Malachite Green (MG). Phototoxicity was studied in human squamous (FaDu) and colon (CX-1) carcinoma, and in human and murine melanoma (NEL, B-16) cell lines, as well as in non-malignant monkey kidney cells (CV-1). Cultured cells were exposed to varying concentrations of the dyes for 60 min, washed with PBS, irradiated after an efflux time of 90 min in culture media, and placed in a colony forming assay. VB-BO was the most effective photosensitizer, giving 90% killing of malignant cells such as B-16 when treated with 5x10-8 M dye and 13 J/cm2 light. CV-1 cells were unaffected under these conditions. VB-R was about 10 fold less effective, while MG had minimal phototoxicity in this assay. VB-BO was studied in vivo, using subcutaneous FaDu tumors in nude mice. At a dose of 3 mg/kg followed 4 hrs later by dye laser irradiation under conditions which did not produce hyperthermia, there was an 80% complete remission rate without significant phototoxicity to overlying or adjacent normal skin. The triarylmethanes are a novel class of photosensitizers which may have promise in vitro and in vivo.
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