Generation of singlet oxygen by porphyrin and phthalocyanine derivatives regarding the oxygen level

Authors

DOI:

https://doi.org/10.20883/medical.e752

Keywords:

photodynamic therapy, photosensitizers, hyperoxia, singlet oxygen

Abstract

Background. The principle of photodynamic effect is based on the combined action of photosensitiser, molecular oxygen and light, which produce various reactive oxygen species and are associated with significant cellular damage. Singlet oxygen is one of the most serious representatives, which is characterised by powerful oxidising properties. Moreover, concomitant hyperbaric oxygen treatment can support these effects. Therefore, the subject of our study was to compare the yields of singlet oxygen for four different photosensitizers in dependency on the oxygen concentration.

Material and methods. Four different photosensitizers 5,10,15,20-tetrakis(1-methyl-4-pyridinio)porphyrin tetra(p-toluenesulfonate), tetramethylthionine chloride, 5,10,15,20-tetrakis(4-sulfonatophenyl)porphyrin zinc(II) and zinc phthalocyanine disulfonate were investigated to determine the yield of singlet oxygen in PBS by Singlet Oxygen Sensor Green reagent under different partial pressures of oxygen (0.4 and 36 mg/l).

Results. There were no noticeable shifts in the excitation and emission fluorescence spectra regarding the oxygen concentration. Concerning the same molar concentration of photosensitizers the production of singlet oxygen was highest for 5,10,15,20-tetrakis(4-sulfonatophenyl)porphyrin zinc(II), where the rate of the fluorescence change was more than 3 times higher than that obtained for 5,10,15,20-tetrakis(1-methyl-4-pyridinio)porphyrin tetra(p-toluenesulfonate). On the other hand, zinc phthalocyanine disulfonate showed the lowest yield in singlet oxygen production.

Conclusions. Singlet oxygen production, within the range of oxygen concentrations achievable in tissues under normoxia or hyperoxia, does not depend on these concentrations. However, the singlet oxygen generation is significantly influenced by the type of photosensitizer, with the highest yield belonging to 5,10,15,20-tetrakis(4-sulfonatophenyl)porphyrin zinc(II).

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References

Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer. 2003 May; 3(5):380-7. DOI: 10.1038/nrc1071. PMID: 12724736. DOI: https://doi.org/10.1038/nrc1071

Berg K, Selbo PK, Weyergang A, Dietze A, Prasmickaite L, Bonsted A, Engesaeter BØ, Angell-Petersen E, Warloe T, Frandsen N, Høgset A. Porphyrin-related photosensitizers for cancer imaging and therapeutic applications. J Microsc. 2005 May; 218(Pt 2):133-47. DOI: 10.1111/j.1365-2818.2005.01471.x. PMID: 15857375. DOI: https://doi.org/10.1111/j.1365-2818.2005.01471.x

Kharkwal GB, Sharma SK, Huang YY, Dai T, Hamblin MR. Photodynamic therapy for infections: clinical applications. Lasers Surg Med. 2011 Sep; 43(7):755-67. DOI: 10.1002/lsm.21080. PMID: 22057503; PMCID: PMC3449167. DOI: https://doi.org/10.1002/lsm.21080

Gomes ATPC, Neves MGPMS, Cavaleiro JAS. Cancer, Photodynamic Therapy and Porphyrin-Type Derivatives. An Acad Bras Cienc. 2018; 90(1 Suppl 2):993-1026. DOI: 10.1590/0001-3765201820170811. PMID: 29873666. DOI: https://doi.org/10.1590/0001-3765201820170811

Roguin LP, Chiarante N, García Vior MC, Marino J. Zinc(II) phthalocyanines as photosensitizers for antitumor photodynamic therapy. Int J Biochem Cell Biol. 2019 Sep; 114:105575. DOI: 10.1016/j.biocel.2019.105575. Epub 2019 Jul 27. PMID: 31362060. DOI: https://doi.org/10.1016/j.biocel.2019.105575

Paquette B, Boyle RW, Ali H, MacLennan AH, Truscott TG, van Lier JE. Sulfonated phthalimidomethyl aluminum phthalocyanine: the effect of hydrophobic substituents on the in vitro phototoxicity of phthalocyanines. Photochem Photobiol. 1991 Mar; 53(3):323-7. DOI: 10.1111/j.1751-1097.1991.tb03635.x. PMID: 2062879. DOI: https://doi.org/10.1111/j.1751-1097.1991.tb03635.x

Margaron P, Grégoire MJ, Scasnár V, Ali H, van Lier JE. Structure-photodynamic activity relationships of a series of 4-substituted zinc phthalocyanines. Photochem Photobiol. 1996 Feb; 63(2):217-23. DOI: 10.1111/j.1751-1097.1996.tb03017.x. PMID: 8657735. DOI: https://doi.org/10.1111/j.1751-1097.1996.tb03017.x

Colussi VC, Feyes DK, Mulvihill JW, Li YS, Kenney ME, Elmets CA, Oleinick NL, Mukhtar H. Phthalocyanine 4 (Pc 4) photodynamic therapy of human OVCAR-3 tumor xenografts. Photochem Photobiol. 1999 Feb; 69(2):236-41. PMID: 10048316. DOI: https://doi.org/10.1111/j.1751-1097.1999.tb03280.x

Nyman ES, Hynninen PH. Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy. J Photochem Photobiol B. 2004 Jan; 73(1-2):1-28. DOI: 10.1016/j.jphotobiol.2003.10.002. PMID: 14732247. DOI: https://doi.org/10.1016/j.jphotobiol.2003.10.002

Pineiro M, Pereira MM, Gonsalves A, Arnaut LG, Formosinho SJ. Singlet oxygen quantum yields from halogenated chlorins. J Photochem Photobiol A. 2001 Jan; 38(2):147-57. DOI: 10.1016/S1010-6030(00)00382-8. DOI: https://doi.org/10.1016/S1010-6030(00)00382-8

Daruwalla J, Christophi C. Hyperbaric oxygen therapy for malignancy: a review. World J Surg. 2006 Dec;30(12):2112-31. DOI: 10.1007/s00268-006-0190-6. PMID: 17102915. DOI: https://doi.org/10.1007/s00268-006-0190-6

Kizaka-Kondoh S, Inoue M, Harada H, Hiraoka M. Tumor hypoxia: a target for selective cancer therapy. Cancer Sci. 2003 Dec; 94(12):1021-8. DOI: 10.1111/j.1349-7006.2003.tb01395.x. PMID: 14662015. DOI: https://doi.org/10.1111/j.1349-7006.2003.tb01395.x

Niklas A, Brock D, Schober R, Schulz A, Schneider D. Continuous measurements of cerebral tissue oxygen pressure during hyperbaric oxygenation - HBO effects on brain edema and necrosis after severe brain trauma in rabbits. J Neurol Sci. 2004 Apr; 219(1-2):77-82. DOI: 10.1016/j.jns.2003.12.013. PMID: 15050441. DOI: https://doi.org/10.1016/j.jns.2003.12.013

Yamamoto N, Takada R, Maeda T, Yoshii T, Okawa A, Yagishita K. Microcirculation and tissue oxygenation in the head and limbs during hyperbaric oxygen treatment. Diving Hyperb Med. 2021 Dec 20;51(4):338-344. DOI: 10.28920/dhm51.4.338-344. PMID: 34897598; PMCID: PMC8920905. DOI: https://doi.org/10.28920/dhm51.4.338-344

Kubat P, Mosinger J. Photophysical properties of metal complexes of meso-tetrakis (4-sulphonatophenyl) porphyrin. J Photochem Photobiol A. 1996 May; 96(1–3):93-97. https://doi.org/10.1016/1010-6030(95)04279-2. DOI: https://doi.org/10.1016/1010-6030(95)04279-2

Griffiths J, Schofield J, Wainwright M, Brown SB. Some observations on the synthesis of polysubstituted zinc phthalocyanine sensitisers for photodynamic therapy. Dyes Pigm. 1997 33:65-78. DOI: https://doi.org/10.1016/S0143-7208(96)00037-X

Kwiatkowski S, Knap B, Przystupski D, Saczko J, Kędzierska E, Knap-Czop K, Kotlińska J, Michel O, Kotowski K, Kulbacka J. Photodynamic therapy - mechanisms, photosensitizers and combinations. Biomed Pharmacother. 2018 Oct;106:1098-1107. DOI: 10.1016/j.biopha.2018.07.049. Epub 2018 Jul 17. PMID: 30119176. DOI: https://doi.org/10.1016/j.biopha.2018.07.049

Gleadle J, Ratcliffe PJ. Hypoxia. In: Wiley J, editor. Encyclopedia of life sciences. Chichester: John Wiley & Sons; 2001. DOI: https://doi.org/10.1038/npg.els.0002125

Maier A, Tomaselli F, Anegg U, Rehak P, Fell B, Luznik S, Pinter H, Smolle-Jüttner FM. Combined photodynamic therapy and hyperbaric oxygenation in carcinoma of the esophagus and the esophago-gastric junction. Eur J Cardiothorac Surg. 2000 Dec;18(6):649-54; discussion 654-5. DOI: 10.1016/s1010-7940(00)00592-3. PMID: 11113670. DOI: https://doi.org/10.1016/S1010-7940(00)00592-3

Jirsa M Jr, Poucková P, Dolezal J, Pospísil J, Jirsa M. Hyperbaric oxygen and photodynamic therapy in tumour-bearing nude mice. Eur J Cancer. 1991;27(1):109. DOI: 10.1016/0277-5379(91)90075-o. PMID: 1826432. DOI: https://doi.org/10.1016/0277-5379(91)90075-O

Blake E, Allen J, Curnow A. The effects of protoporphyrin IX-induced photodynamic therapy with and without iron chelation on human squamous carcinoma cells cultured under normoxic, hypoxic and hyperoxic conditions. Photodiagnosis Photodyn Ther. 2013 Dec;10(4):575-82. DOI: 10.1016/j.pdpdt.2013.06.006. Epub 2013 Aug 8. PMID: 24284114. DOI: https://doi.org/10.1016/j.pdpdt.2013.06.006

Pola M, Kolarova H, Ruzicka J, Zholobenko A, Modriansky M, Mosinger J, Bajgar R. Effects of zinc porphyrin and zinc phthalocyanine derivatives in photodynamic anticancer therapy under different partial pressures of oxygen in vitro. Invest New Drugs. 2021 Feb;39(1):89-97. DOI: 10.1007/s10637-020-00990-7. Epub 2020 Aug 24. PMID: 32833137. DOI: https://doi.org/10.1007/s10637-020-00990-7

Förster T. Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys. 1948, 437, 55-75. DOI: https://doi.org/10.1002/andp.19484370105

Hu W, Yang F, Pietraszak N, Gu J, Huang J. Distance dependent energy transfer dynamics from a molecular donor to a zeolitic imidazolate framework acceptor. Phys Chem Chem Phys. 2020, 22, 25445-9. DOI: https://doi.org/10.1039/D0CP03995K

Lang K, Mosinger J, Wagnerová DM. Photophysical properties of porphyrinoid sensitizers non-covalently bound to host molecules; models for photodynamic therapy. Coord Chem Rev. 2004 Feb;248(3-4):321-50. doi: 10.1016/j.ccr.2004.02.004. DOI: https://doi.org/10.1016/j.ccr.2004.02.004

Ashkenazi S. Photoacoustic lifetime imaging of dissolved oxygen using methylene blue. J Biomed Opt. 2010 Jul-Aug;15(4):040501. DOI: 10.1117/1.3465548. PMID: 20799768. DOI: https://doi.org/10.1117/1.3465548

Beeby A, FitzGerald S, Stanley CF. A photophysical study of protonated (tetra-tert-butylphthalocyaninato)zinc. J Chem Soc Perkin Trans. 2001 Aug;2:1978-82. DOI: https://doi.org/10.1039/b102937c

Ogunsipe A, Chen JY, Nyokong T. Photophysical and photochemical studies of zinc(ii) phthalocyanine derivatives - effects of substituents and solvents. New J Chem. 2004 Jun;28:822-7. DOI: https://doi.org/10.1039/B315319C

Alwattar AH, Lumb MD, Birks, JB. Diffusion-controlled rate processes. In: Birks JB, editor. Organic Molecular Photophysics. New York: John Wiley & Sons; 1973. p. 403-454.

Quina FH, Silva GTM. The photophysics of photosensitization: A brief overview. J Photochem Photobiol. 2021 Sep; 7:100042. DOI: 10.1016/j.jpap.2021.100042. DOI: https://doi.org/10.1016/j.jpap.2021.100042

Haouzi P, Gueguinou M, Sonobe T, Judenherc-Haouzi A, Tubbs N, Trebak M, Cheung J, Bouillaud F. Revisiting the physiological effects of methylene blue as a treatment of cyanide intoxication. Clin Toxicol (Phila). 2018 Sep; 56(9): 828-840. DOI: 10.1080/15563650.2018.1429615. Epub 2018 Feb 16. PMID: 29451035; PMCID: PMC6086742. DOI: https://doi.org/10.1080/15563650.2018.1429615

Lu G, Nagbanshi M, Goldau N, Mendes Jorge M, Meissner P, Jahn A, Mockenhaupt FP, Müller O. Efficacy and safety of methylene blue in the treatment of malaria: a systematic review. BMC Med. 2018 Apr; 16(1):59. DOI: 10.1186/s12916-018-1045-3. PMID: 29690878; PMCID: PMC5979000. DOI: https://doi.org/10.1186/s12916-018-1045-3

Zhang LZ, Tang GQ. The binding properties of photosensitizer methylene blue to herring sperm DNA: a spectroscopic study. J Photochem Photobiol B. 2004 May; 74(2-3):119-25. DOI: 10.1016/j.jphotobiol.2004.03.005. PMID: 15157907. DOI: https://doi.org/10.1016/j.jphotobiol.2004.03.005

Klosowski EM, de Souza BTL, Mito MS, Constantin RP, Mantovanelli GC, Mewes JM, Bizerra PFV, Menezes PVMDC, Gilglioni EH, Utsunomiya KS, Marchiosi R, Dos Santos WD, Filho OF, Caetano W, Pereira PCS, Gonçalves RS, Constantin J, Ishii-Iwamoto EL, Constantin RP. The photodynamic and direct actions of methylene blue on mitochondrial energy metabolism: A balance of the useful and harmful effects of this photosensitizer. Free Radic Biol Med. 2020 Jun; 153:34-53. DOI: 10.1016/j.freeradbiomed.2020.04.015. Epub 2020 Apr 18. PMID: 32315767. DOI: https://doi.org/10.1016/j.freeradbiomed.2020.04.015

Pucelik B, Sułek A, Barzowska A, Dąbrowski JM. Recent advances in strategies for overcoming hypoxia in photodynamic therapy of cancer. Cancer Lett. 2020 Nov; 492:116-135. https://doi.org/10.1016/j.canlet.2020.07.007. DOI: https://doi.org/10.1016/j.canlet.2020.07.007

Larue L, Myrzakhmetov B, Ben-Mihoub A, Moussaron A, Thomas N, Arnoux P, Baros F, Vanderesse R, Acherar S, Frochot C. Fighting Hypoxia to Improve PDT. Pharmaceuticals. 2019; 12(4): 163. https://doi.org/10.3390/ph12040163. DOI: https://doi.org/10.3390/ph12040163

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Published

2022-12-27

How to Cite

1.
Pola M, Kolarova H, Bajgar R. Generation of singlet oxygen by porphyrin and phthalocyanine derivatives regarding the oxygen level. JMS [Internet]. 2022 Dec. 27 [cited 2024 Mar. 29];91(4):e752. Available from: https://jms.ump.edu.pl/index.php/JMS/article/view/752

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Section

Original Papers
Received 2022-10-10
Accepted 2022-11-18
Published 2022-12-27