Fatty Acid Conjugates of Toluidine Blue O as Amphiphilic Photosensitizers: Synthesis, Solubility, Photophysics and Photochemical Properties
Journal
Photochemistry and photobiology
ISSN: 1751-1097
Titre abrégé: Photochem Photobiol
Pays: United States
ID NLM: 0376425
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
29
04
2020
revised:
07
06
2020
accepted:
25
06
2020
pubmed:
4
7
2020
medline:
7
8
2021
entrez:
4
7
2020
Statut:
ppublish
Résumé
Toluidine blue O (TBO) is a water-soluble photosensitizer that has been used in photodynamic antimicrobial and anticancer treatments, but suffers from limited solubility in hydrophobic media. In an effort to incrementally increase TBO's hydrophobicity, we describe the synthesis of hexanoic (TBOC6) and myristic (TBOC14) fatty acid derivatives of TBO formed in low to moderate percent yields by condensation with the free amine site. Covalently linking 6 and 14 carbon chains led to modifications of not only TBO's solubility, but also its photophysical and photochemical properties. TBOC6 and TBOC14 derivatives were more soluble in organic solvents and showed hypsochromic shifts in their absorption and emission bands. The solubility in phosphate buffer solution was low for both TBOC6 and TBOC14, but unexpectedly slightly greater in the latter. Both TBOC6 and TBOC14 showed decreased triplet excited-state lifetimes and singlet oxygen quantum yields in acetonitrile, which was attributed to heightened aggregation of these conjugates particularly at high concentrations due to the hydrophobic "tails." While in diluted aqueous buffer solution, indirect measurements showed similar efficiency in singlet oxygen generation for TBOC14 compared to TBO. This work demonstrates a facile synthesis of fatty acid TBO derivatives leading to amphiphilic compounds with a delocalized cationic "head" group and hydrophobic "tails" for potential to accumulate into biological membranes or membrane/aqueous interfaces in PDT applications.
Substances chimiques
Fatty Acids
0
Photosensitizing Agents
0
Tolonium Chloride
15XUH0X66N
Singlet Oxygen
17778-80-2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
71-79Informations de copyright
© 2020 American Society for Photobiology.
Références
Agostinis, P., K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson and J. Golab (2011) Photodynamic therapy of cancer: an update. CA Cancer J. Clin. 61, 250-281.
Baptista, M. S., J. Cadet, P. Di Mascio, A. A. Ghogare, A. Greer, M. R. Hamblin, C. Lorente, S. C. Nunez, M. S. Ribeiro, A. H. Thomas, M. Vignoni and T. M. Yoshimura (2017) Type I and II photosensitized oxidation reactions: guidelines and mechanistic pathways. Photochem. Photobiol. 93, 912-919.
Hamblin, M. R. and P. Mróz (2008) Advances in Photodynamic Therapy. Basic, Translational, and Clinical, pp. 41-58. Artech House, Norwood, MA.
Davies, M. J. (2005) The oxidative environment and protein damage. Biochim. Biophys. Acta Proteins Proteom. 1703, 93-109.
Agnez-Lima, L. F., J. T. Melo, A. E. Silva, A. H. S. Oliveira, A. R. S. Timoteo, K. M. Lima-Bessa, G. R. Martinez, M. H. Medeiros, P. Di Mascio and R. S. Galhardo (2012) DNA damage by singlet oxygen and cellular protective mechanisms. Mutat. Res. Rev. Mutat. 751, 15-28.
Bacellar, I., T. Tsubone, C. Pavani and M. Baptista (2015) Photodynamic efficiency: from molecular photochemistry to cell death. Int. J. Mol. Sci. 16, 20523-20559.
Castano, A. P., T. N. Demidova and M. R. Hamblin (2004) Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization. Photodiagn. Photodyn. Ther. 1, 279-293.
Callaghan, S. and M. O. Senge (2018) The good, the bad, and the ugly-controlling singlet oxygen through design of photosensitizers and delivery systems for photodynamic therapy. Photochem. Photobiol. Sci. 17, 1490-1514.
Allison, R. R. and C. H. Sibata (2010) Oncologic photodynamic therapy photosensitizers: a clinical review. Photodiagn. Photodyn. 7, 61-75.
O’Connor, A. E., W. M. Gallagher and A. T. Byrne (2009) Porphyrin and nonporphyrin photosensitizers in oncology: preclinical and clinical advances in photodynamic therapy. Photochem. Photobiol. 85, 1053-1074.
Juzeniene, A., Q. Peng and J. Moana (2007) Milestones in the development of photodynamic therapy and fluorescence diagnosis. Photochem. Photobiol. Sci. 6, 1234-1245.
Dichiara, M., O. Prezzavento, A. Marrazzo, V. Pittala, L. Salerno, A. Rescifina and E. Amata (2017) Recent advances in drug discovery of phototherapeutic non-porphyrinic anticancer agents. Eur. J. Med. Chem. 142, 459-485.
Debele, T. A., S. Peng and H.-C. Tsai (2015) Drug carrier for photodynamic cancer therapy. Int. J. Mol. Sci. 16, 22094-22136.
Li, X., S. Lee and J. Yoon (2018) Supramolecular photosensitizers rejuvenate photodynamic therapy. Chem. Soc. Rev. 47, 1174-1188.
Lan, M., S. Zhao, W. Liu, C.-S. Lee, W. Zhang and P. Wang (2019) Photosensitizers for photodynamic therapy. Adv. Healthc. Mater. 8, 1900132.
Robinson-Duggon, J., F. Pérez-Mora, L. Dibona-Villanueva and D. Fuentealba (2018) Potential applications of cucurbit[n]urils inclusion complexes in photodynamic therapy. Isr. J. Chem. 58, 199-214.
Ma, X. and Y. Zhao (2014) Biomedical applications of supramolecular systems based on host-guest interactions. Chem. Rev. 115, 7794-7839.
Robinson-Duggon, J., F. Pérez-Mora, L. Valverde-Vásquez, D. Cortés-Arriagada, J. R. De la Fuente, G. Günther and D. Fuentealba (2017) Supramolecular reversible on-off switch for singlet oxygen using cucurbit[n]uril inclusion complexes. J. Phys. Chem. C 121, 21782-21789.
García, A. M., H. de Alwis Weerasekera, S. P. Pitre, B. McNeill, E. Lissi, A. M. Edwards and E. I. Alarcón (2016) Photodynamic performance of zinc phthalocyanine in HeLa cells: a comparison between DPCC liposomes and BSA as delivery systems. J. Photochem. Photobiol. B 163, 385-390.
Alarcón, E., A. M. Edwards, A. M. García, M. Muñoz, A. Aspee, C. D. Borsarelli and E. A. Lissi (2009) Photophysics and photochemistry of zinc phthalocyanine/bovine serum albumin adducts. Photochem. Photobiol. Sci. 8, 255-263.
Alarcón, E., A. M. Edwards, A. Aspée, F. E. Moran, C. D. Borsarelli, E. A. Lissi, D. González-Nilo, H. Poblete and J. C. Scaiano (2010) Photophysics and photochemistry of dyes bound to human serum albumin are determined by the dye localization. Photochem. Photobiol. Sci. 9, 93-102.
Alarcón, E., A. M. Edwards, A. Aspée, C. D. Borsarelli and E. A. Lissi (2009) Photophysics and photochemistry of rose bengal bound to human serum albumin. Photochem. Photobiol. Sci. 8, 933-943.
Jeong, H., M. Huh, S. J. Lee, H. Koo, I. C. Kwon, S. Y. Jeong and K. Kim (2011) Photosensitizer-conjugated human serum albumin nanoparticles for effective photodynamic therapy. Theranostics 1, 230-239.
Munoz, M. A., A. Pacheco, M. I. Becker, E. Silva, R. Ebensperger, A. M. García, A. E. De Ioannes and A. M. Edwards (2011) Different cell death mechanisms are induced by a hydrophobic flavin in human tumor cells after visible light irradiation. J. Photochem. Photobiol. B 103, 57-67.
Vignoni, M., N. Walalawela, S. M. Bonesi, A. Greer and A. H. Thomas (2017) Lipophilic decyl chain-pterin conjugates with sensitizer properties. Mol. Pharm. 15, 798-807.
Walalawela, N., M. N. Urrutia, A. H. Thomas, A. Greer and M. Vignoni (2019) Alkane chain-extended pterin through a pendent carboxylic acid acts as triple functioning fluorophore, 1O2 sensitizer and membrane binder. Photochem. Photobiol. 95, 1160-1168.
Vignoni, M., M. N. Urrutia, H. C. Junqueira, A. Greer, A. Reis, M. S. Baptista, R. Itri and A. H. Thomas (2018) Photo-oxidation of unilamellar vesicles by a lipophilic pterin: deciphering biomembrane photodamage. Langmuir 34, 15578-15586.
Wilson, M., T. Burns, J. Pratten and G. Pearson (1995) Bacteria in supragingival plaque samples can be killed by low-power laser light in the presence of a photosensitizer. J. Appl. Bacteriol. 78, 569-574.
Wilson, M. and N. Mia (1993) Sensitisation of candida albicans to killing by low-power laser light. J. Oral Pathol. Med. 22, 354-357.
Wilson, M. and C. Yianni (1995) Killing of methicillin-resistant Staphylococcus aureus by low-power laser light. J. Med. Microbiol. 42, 62-66.
Herlin, P., J. Marnay, J. Jacob, J. Ollivier and A. Mandard (1983) A study of the mechanism of the toluidine blue dye test. Endoscopy 15, 4-7.
Eliezri, Y. D. (1988) The toluidine blue test: an aid in the diagnosis and treatment of early squamous cell carcinomas of mucous membranes. J. Am. Acad. Dermatol. 18, 1339-1349.
Epstein, J. B., C. Oakley, A. Millner, S. Emerton, E. van der Meij and N. Le (1997) The utility of toluidine blue application as a diagnostic aid in patients previously treated for upper oropharyngeal carcinoma. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 83, 537-547.
Tremblay, J. F., S. Dussault, G. Viau, F. Gad, M. Boushira and R. Bissonnette (2002) Photodynamic therapy with toluidine blue in Jurkat cells: cytotoxicity, subcellular localization and apoptosis induction. Photochem. Photobiol. Sci. 1, 852-856.
Blázquez-Castro, A., J. C. Stockert, F. Sanz-Rodríguez, A. Zamarrón and A. Juarranz (2009) Differential photodynamic response of cultured cells to methylene blue and toluidine blue: role of dark redox processes. Photochem. Photobiol. Sci. 8, 371-376.
Darzynkiewicz, Z. and S. P. Carter (1988) Photosensitizing effects of the tricyclic heteroaromatic cationic dyes pyronin Y and toluidine blue O (tolonium chloride). Can. Res. 48, 1295-1299.
Oleinick, N. L., R. L. Morris and I. Belichenko (2002) The role of apoptosis in response to photodynamic therapy: what, where, why, and how. Photochem. Photobiol. Sci. 1, 1-21.
Robinson-Duggon, J., N. Mariño-Ocampo, P. Barrias, D. Zúñiga-Núñez, G. Günther, A. M. Edwards, A. Greer and D. Fuentealba (2019) Mechanism of visible-light photooxidative demethylation of toluidine blue O. J. Phys. Chem. A 123, 4863-4872.
Wang, X. Q., Q. Lei, J. Y. Zhu, W. J. Wang, Q. Cheng, F. Gao, Y. X. Sun and X. Z. Zhang (2016) Cucurbit[8]uril regulated activatable supramolecular photosensitizer for targeted cancer imaging and photodynamic therapy. ACS Appl. Mater. Inter. 8, 22892-22899.
Kasimova, K. R., M. Sadasivam, G. Landi, T. Sarna and M. R. Hamblin (2014) Potentiation of photoinactivation of gram-positive and gram-negative bacteria mediated by six phenothiazinium dyes by addition of azide ion. Photochem. Photobiol. Sci. 13, 1541-1548.
Battogtokh, G., H. B. Liu, S. M. Bae, P. K. Chaturvedi, Y. W. Kim, I. W. Kim and W. S. Ahn (2012) Synthesis of chlorin-based unsaturated fatty acid conjugates: their in vitro phototoxicity on TC-1 cancer cell line. J. Photochem. Photobiol. B 110, 50-57.
Ngen, E. J., P. Rajaputra and Y. You (2009) Evaluation of delocalized lipophilic cationic dyes as delivery vehicles for photosensitizers to mitochondria. Bioorg. Med. Chem. 17, 6631-6640.
Rajaputra, P., G. Nkepang, R. Watley and Y. You (2013) Synthesis and in vitro biological evaluation of lipophilic cation conjugated photosensitizers for targeting mitochondria. Bioorg. Med. Chem. 21, 379-387.
McKamey, M. R. and L. A. Spitznagle (1975) Chromatographic, mass spectral, and visible light absorption characteristics of toluidine blue O and related dyes. J. Pharm. Sci. 64, 1456-1462.
Frisch, M. J., G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G. A. Petersson, H. Nakatsuji, M. Caricato, X. Li, H. P. Hratchian, A. F. Izmaylov, J. Bloino, G. Zheng, J. L. Sonnenberg, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, J. A. Montgomery, J. E. Peralta, F. Ogliaro, M. Bearpark, J. J. Heyd, E. Brothers, K. N. Kudin, V. N. Staroverov, R. Kobayashi, J. Normand, K. Raghavachari, A. Rendell, J. C. Burant, S. S. Iyengar, J. Tomasi, M. Cossi, N. Rega, J. M. Millam, M. Klene, J. E. Knox, J. B. Cross, V. Bakken, C. Adamo, J. Jaramillo, R. Gomperts, R. E. Stratmann, O. Yazyev, A. J. Austin, R. Cammi, C. Pomelli, J. W. Ochterski, R. L. Martin, K. Morokuma, V. G. Zakrzewski, G. A. Voth, P. Salvador, J. J. Dannenberg, S. Dapprich, A. D. Daniels, J. B. Farkas, J. V. Foresman, J. C. Ortiz and D. J. Fox (2009) Gaussian 09, revision E.01. Gaussian, Inc, Wallingford, CT.
Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98, 5648-5652.
Lee, C., W. Yang and R. G. Parr (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 37, 785-789.
Petersson, G. A. and M. A. Al-Laham (1991) A complete basis set model chemistry. II. Open-shell systems and the total energies of the first-row atoms. J. Chem. Phys. 94, 6081-6090.
Petersson, G. A., A. Bennett, T. G. Tensfeldt, M. A. Al-Laham, W. A. Shirley and J. Mantzaris (1988) A complete basis set model chemistry. I. The total energies of closed-shell atoms and hydrides of the first-row elements. J. Chem. Phys. 89, 2193-2218.
Stratmann, R. E., G. E. Scuseria and M. J. Frisch (1998) An efficient implementation of time-dependent density-functional theory for the calculation of excitation energies of large molecules. J. Chem. Phys. 109, 8218-8224.
Furche, F. and R. Ahlrichs (2002) Adiabatic time-dependent density functional methods for excited state properties. J. Chem. Phys. 117, 7433-7447.
Maurizio, C., R. Nadia, S. Giovanni and B. Vincenzo (2003) Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model. J. Comput. Chem. 24, 669-681.
Scholtbach, K., I. Venegas, C. Bohne and D. Fuentealba (2015) Time-resolved fluorescence anisotropy as a tool to study guest-cucurbit[n]uril-protein ternary supramolecular interactions. Photochem. Photobiol. Sci. 14, 842-852.
Pace, T. C. S., M. Nishijima, T. Wada, Y. Inoue and C. Bohne (2009) Photophysical studies on the supramolecular photochirogenesis for the photocyclodimerization of 2-anthracenecarboxylate within human serum albumin. J. Phys. Chem. B 113, 10445-10453.
Fuentealba, D., H. Kato, M. Nishijima, G. Fukuhara, T. Mori, Y. Inoue and C. Bohne (2013) Explaining the highly enantiomeric photocyclodimerization of 2-anthracenecarboxylate bound to human serum albumin using time-resolved anisotropy studies. J. Am. Chem. Soc. 135, 203-209.
Tang, H., D. Fuentealba, Y. H. Ko, N. Selvapalam, K. Kim and C. Bohne (2011) Guest binding dynamics with cucurbit[7]uril in the presence of cations. J. Am. Chem. Soc. 133, 20623-20633.
Das, K. G., P. T. Funke and A. K. Bose (1964) Mass spectral studies. III. Fragmentation of aromatic amides. J. Am. Chem. Soc. 86, 3729-3732.
Claridge, T. D. (2016) High-Resolution NMR Techniques in Organic Chemistry. Elsevier, Oxford.
Chen, Y., W. R. Potter, J. R. Missert, J. Morgan and R. K. Pandey (2007) Comparative in vitro and in vivo studies on long-wavelength photosensitizers derived from bacteriopurpurinimide and bacteriochlorin p6: fused imide ring enhances the in vivo PDT efficacy. Bioconjug. Chem. 18, 1460-1473.
Henderson, B. W., D. A. Bellnier, W. R. Greco, A. Sharma, R. K. Pandey, L. A. Vaughan, K. R. Weishaupt and T. J. Dougherty (1997) An in vivo quantitative structure-activity relationship for a congeneric series of pyropheophorbide derivatives as photosensitizers for photodynamic therapy. Cancer Res. 57, 4000-4007.
Bhal, S. K., K. Kassam, I. G. Peirson and G. M. Pearl (2007) The rule of five revisited: applying log D in place of log P in drug-likeness filters. Mol. Pharm. 4, 556-560.
Tetko, I. V. and G. I. Poda (2004) Application of ALOGPS 2.1 to predict log D distribution coefficient for Pfizer proprietary compounds. J. Med. Chem. 47, 5601-5604.
Zamora, W. J., C. Curutchet, J. M. Campanera and F. J. Luque (2017) Prediction of pH-dependent hydrophobic profiles of small molecules from Miertus-Scrocco-Tomasi continuum solvation calculations. J. Phys. Chem. B 121, 9868-9880.
Tsonopoulos, C. (1999) Thermodynamic analysis of the mutual solubilities of normal alkanes and water. Fluid Phase Equilib. 156, 21-33.
McWilliams, A. D. S., S. Ergülen, M. M. Ogle, C. A. de los Reyes, M. Pasquali and A. A. Martí (2020) Fluorescent surfactants from common dyes - rhodamine B and eosin Y. Pure Appl. Chem. 92, 265-274.
Dong, L., Z. Xu, W. Qiao, Z. Li and L. Cheng (2007) Synthesis and properties of a novel fluorescent surfactant. Energ. Sourc. Part A 29, 1407-1413.
Wang, J., Z. Xu, Y. Zhao, W. Qiao and Z. Li (2007) Synthesis and characterization of novel fluorescent surfactants. Dyes Pigm. 74, 103-107.
Chen, J., T. C. Cesario and P. M. Rentzepis (2010) Time resolved spectroscopic studies of methylene blue and phenothiazine derivatives used for bacteria inactivation. Chem. Phys. Lett. 498, 81-85.
Kimani, S., G. Ghosh, A. Ghogare, B. Rudshteyn, D. Bartusik, T. Hasan and A. Greer (2012) Synthesis and characterization of mono-, di-, and tri-poly(ethylene glycol) chlorin e6 conjugates for the photokilling of human ovarian cancer cells. J. Org. Chem. 77, 10638-10647.
Li, Y.-C., S. Rissanen, M. Stepniewski, O. Cramariuc, T. Róg, S. Mirza, H. Xhaard, M. Wytrwal, M. Kepczynski and A. Bunker (2012) Study of interaction between peg carrier and three relevant drug molecules: piroxicam, paclitaxel, and hematoporphyrin. J. Phys. Chem. B 116, 7334-7341.
Pottier, R., R. Bonneau and J. Joussot-Dubien (1975) pH dependence of singlet oxygen production in aqueous solutions using toluidine blue as a photosensitizer. Photochem. Photobiol. 22, 59-61.