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Photophysical Properties of Protoporphyrin IX, Pyropheophorbide-A, and Photofrin® in Different Conditions

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Photophysical Properties of Protoporphyrin IX, Pyropheophorbide-A, and Photofrin® in Different Conditions pharmaceuticals Article Photophysical Properties of Protoporphyrin IX, Pyropheophorbide-a, and Photofrin® in Different Conditions Bauyrzhan Myrzakhmetov 1,2, Philippe Arnoux 1 , Serge Mordon 3 , Samir Acherar 4 , Irina Tsoy 2 and Céline Frochot 1,* 1 LRGP UMR 7274, CNRS, University of Lorraine, 54000 Nancy, France; [email protected] (B.M.); [email protected] (P.A.) 2 Department of Chemistry and Chemical Technology, M.Kh. Dulaty Taraz Regional University, Taraz 080012, Kazakhstan; [email protected] 3 ONCO-THAI U1189, INSERM, CHU Lille, University of Lille, 59000 Lille, France; [email protected] 4 LCPM UMR 7375, CNRS, University of Lorraine, 54000 Nancy, France; [email protected] * Correspondence: [email protected]; Tel.: +33-372743780 Abstract: Photodynamic therapy (PDT) is an innovative treatment of malignant or diseased tissues. The effectiveness of PDT depends on light dosimetry, oxygen availability, and properties of the photosensitizer (PS). Depending on the medium, photophysical properties of the PS can change leading to increase or decrease in fluorescence emission and formation of reactive oxygen species 1 (ROS) especially singlet oxygen ( O2). In this study, the influence of solvent polarity, viscosity, concentration, temperature, and pH medium on the photophysical properties of protoporphyrin ® IX, pyropheophorbide-a, and Photofrin were investigated by UV-visible absorption, fluorescence emission, singlet oxygen emission, and time-resolved fluorescence spectroscopies. Citation: Myrzakhmetov, B.; Arnoux, ® P.; Mordon, S.; Acherar, S.; Tsoy, I.; Keywords: photodynamic therapy; protoporphyrin IX; pyropheophorbide-a; Photofrin ; absorption; Frochot, C. Photophysical Properties fluorescence; singlet oxygen of Protoporphyrin IX, Pyropheophorbide-a, and Photofrin® in Different Conditions. Pharmaceuticals 2021, 14, 138. 1. Introduction https://doi.org/10.3390/ph14020138 Photodynamic therapy (PDT) is a targeted technique for the treatment of malignant or diseased tissues that relies on three non-toxic elements—a light-activated drug (photosensi- Academic Editor: Luís M. T. Frija tizer, PS), light, and molecular oxygen. Illumination of the PS induces the production of the triplet excited state 3PS* which is able to transfer protons, electrons, or energy, leading to Received: 26 January 2021 the formation of reactive oxygen species (ROS). ROS cause apoptosis or necrosis of tumor Accepted: 7 February 2021 cells by photochemical oxidation [1–3]. Published: 9 February 2021 A PS should ideally possess some valuable properties including (i) absorption peak in the near-infrared (NIR) region (700–1000 nm) of the UV-visible spectrum that provides Publisher’s Note: MDPI stays neutral enough penetration of light into deep tissues and energy to excite molecular oxygen to its with regard to jurisdictional claims in published maps and institutional affil- singlet state efficiently, (ii) minimal skin photosensitivity, (iii) no dark toxicity, (iv) selective iations. uptake by cancer tissues, thereby enabling the decrease of side effects [4,5], and (v) fast elimination. The self-assembly or aggregation of PS in aqueous environments can be caused by different reasons and is favored for amphiphilic PSs showing a negligible PDT activity due to the emission reduction of the 3PS* state in aggregated form [6,7]. The physico- Copyright: © 2021 by the authors. chemical properties of aggregates differ from those of monomers. They exhibit a broadened Licensee MDPI, Basel, Switzerland. Soret band and red-shifted Q bands in the UV-visible absorption spectra, low fluorescence This article is an open access article 1 distributed under the terms and intensity and lifetime [8–13], and low singlet oxygen ( O2) production. ® conditions of the Creative Commons The hematoporphyrin derivative (HPD) and its purified form Photofrin (PF) were Attribution (CC BY) license (https:// the first used PSs in PDT and PF was approved for the treatment of solid tumors [14–17]. PF creativecommons.org/licenses/by/ was also indicated as a specific and selective radiosensitizing agent by several in vitro and 4.0/). in vivo studies [18–22]. PF is being used for the treatment of esophageal and non-small-cell Pharmaceuticals 2021, 14, 138. https://doi.org/10.3390/ph14020138 https://www.mdpi.com/journal/pharmaceuticals Pharmaceuticals 2021, 14, x FOR PEER REVIEW 2 of 20 Pharmaceuticals 2021, 14, 138 2 of 20 and in vivo studies [18–22]. PF is being used for the treatment of esophageal and non-small-celllung and pancreatic lung and cancers pancreatic as well cancers as a possible as well therapyas a possible against therapy Karposi’s against sarcoma Karposi’s and sarcomabrain, breast, and brain, skin, andbreast, bladder skin, cancersand bladder [23]. cancers [23]. TheThe selective selective accumulation accumulation of of protoporphyrin protoporphyrin IX (PpIX) in the tumor cells following administrationadministration of 5-aminolevulinic acidacid (5-ALA)(5-ALA) hashas mademade this this PS PS precursor precursor very very popular popu- larfor for skin skin cancer cancer PDT PDT and and fluorescent fluorescent diagnostics diagnostics of of tumor tumor tissues tissues [[24,25].24,25]. Topical, Topical, oral, oral, oror intravenous administration administration of of 5-ALA 5-ALA prodrug prodrug in in excess leading to the formation and accumulationaccumulation of of PpIX PpIX inin vivo [26][26] is used by dermatologists to treat several malignant neoplasmsneoplasms of of the the skin, such as Bowe Bowenn disease or actinic keratosis [27]. [27]. Pyropheophorbide-aPyropheophorbide-a (PPa) (PPa) is is a natural second-generation bacteriochlorin PS which 1 1 presentspresents aa significantsignificant absorption absorption in in the the far-red far-red spectral spectral region region and highand highO2 formation O2 formation upon uponlight illumination,light illumination, suggesting sugge itsting for PDTit for [PDT28,29 [28,29].]. ThisThis study aimed toto exploreexplore thethe differentdifferent parameters parameters (i.e., (i.e., solvent solvent polarity, polarity, concentra- concen- tration,tion, temperature, temperature, and and pH medium)pH medium) that influencethat influence the photophysical the photophysical properties properties (absorption, (ab- 1 1 sorption,fluorescence fluorescence emission, emission, and O2 formation) and O2 formation) of the three of the PSs three (PpIX, PSs PPa, (PpIX, and PPa, PF). and PF). 2.2. Results Results and and Discussion Discussion ChemicalChemical structures of PpIX, PPa, andand PFPF areare shownshown inin FigureFigure1 .1. PpIX PpIX has has two two ioniz- ion- izableable propionate propionate groups groups and and ahydrophobic a hydrophobic ring ring core, core, which which gives gives it amphiphilic it amphiphilic properties prop- ertiesleading leading to an to aggregation an aggregation through throughπ–π stackingπ–π stacking interaction interaction and vesicleand vesicle formation formation [30]. [30].PPa hasPPa onlyhas only one propionateone propionate group group and and a hydrophobic a hydrophobic ring ring core, core, it can it can also also aggregate aggre- gatein aqueous in aqueous solutions solutions [31]. [31]. PF is PF composed is composed of monomers, of monomers, dimers, dimers, and someand some very largevery largeoligomers oligomers [32]. [32]. Figure 1. ChemicalChemical structures structures of pr protoporphyrinotoporphyrin IX (PpIX) ( A), pyropheophorbide-a (PPa) (B), and Photofrin®(® (PF) (C). 2.1.2.1. Influence Influence of of the the Solvent Solvent TheThe structure ofof thethe molecule, molecule, ionic ionic strength, strength, pH, pH, and and temperature temperature should should play aplay main a mainrole in role the in photophysical the photophysical properties properties [33]. UV-visible [33]. UV-visible absorption absorption spectra spectra of PSs presented of PSs pre- in sentedFigure 2in, wereFigure recorded 2, were in recorded different in solvents. different ET(30) solvents. is a solventET(30) is polarity a solvent parameter polarity that pa- rametercharacterized that characterized the polarity of the the polarity different of solvents. the different The biggersolvents. the The ET(30) bigger value, the the ET more (30) value,solvent the polarity more solvent it is associated polarity with. it is associated with. Pharmaceuticals 2021, 14, x FOR PEER REVIEW 3 of 20 As expected, UV-visible absorption spectra of PpIX (Figure 2A) exhibited an intense Soret band centered at around 406 nm and four weaker Q bands in the visible range in toluene, ethyl acetate (AcOEt), ethanol (EtOH), and methanol (MeOH). These similar spectra are typical of monomeric PpIX. Nevertheless, in glycerol, water, phos- phate-buffered solution (PBS), and fetal bovine serum (FBS), the Soret band was split into two bands [34]. This can be explained by the fact that PpIX is aggregated in aqueous so- lutions. In polar solvents the QI band was red-shifted compared to the QI band in less polar solvents (629 nm and 641 nm in EtOH and PBS, respectively) (Table 1), and the in- tensity decreased drastically. In the literature, it is often claimed that PpIX should be ex- Pharmaceuticals 2021, 14, 138 cited in vitro or in vivo at 630 nm. This wavelength of excitation is based on the absorp-3 of 20 tion spectrum in EtOH. As it can be seen in Table 1 in water, PBS, and FBS, the QI band was located at 641, 641, and 640 nm, respectively. FigureFigure 2. 2. UV-visibleUV-visible absorption absorption spectra spectra
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