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Therapeutic Efficacy of Malachite Green-Based Photodynamic Therapy in Acute Myeloid Leukemia

Yıl 2023, Cilt: 13 Sayı: 2, 305 - 311, 22.03.2023
https://doi.org/10.16899/jcm.1251398

Öz

Aim: Acute myeloid leukemia (AML) is a disease characterized by relapse and treatment resistance in most patients. Therefore, there is a need for targeted therapies in AML. Photodynamic therapy (PDT) is a promising alternative for the treatment of malignant tumors. Also, PDT has the potential to be used individually or complementally in the treatment of leukemia. In this study, it was aimed to investigate possible the effect of malachite green (MG)-based PDT on acute myeloid leukemia cells.
Materials and Methods: Cells were incubated with 0.19, 0.39, 0.78,1.56, 3.125, and 6.25 µM MG for one hour and irradiated with 46.4 J/cm2 of light. The trypan blue test was used to assess the viability of cells, and the change in mitochondrial activity was determined by MTT. Morphological features were determined by Giemsa staining and scanning electron microscopy. Cell cycle and Annexin V/PI assays (measuring fluorescence emitted by staining reagents) were measured by flow cytometry.
Results: With the combination of MG and light, HL60 cell viability was found to be significantly reduced compared to the control group. Giemsa staining and SEM results showed that 3.125 μM MG-based PDT induced various morphological changes in cells typical for apoptosis. Late apoptosis was observed in cells treated with 3.125 μM MG combined PDT according to Annexin/PI staining, further showing that it caused an arrest in the subG1 phase of the cell cycle.
Conclusion: MG-based PDT has the potential to inactivate HL60 cells. Thus, MG-based PDT may ensure a promising approach for treating acute myeloid leukemia cells.

Destekleyen Kurum

A part of this study was supported by a research grant from the Scientific and Technological Research Council of Turkey-TUBİTAK

Proje Numarası

1919B011902306

Kaynakça

  • 1. Hamblin MR. Photodynamic Therapy for Cancer: What’s Past is Prologue. Photochem Photobiol 2020; 96(3): 506-16.
  • 2. Martirosyan AS, Vardapetyan HR, Tiratsuyan SG, Hovhannisyan AA. Biphasic dose-response of antioxidants in hypericin-induced photohemolysis. Photodiagnosis Photodyn Ther 2011;8(3):282-87.
  • 3. Plaetzer K, Krammer B, Berlanda J, Berr F, Kiesslich T. Photophysics and photochemistry of photodynamic therapy: Fundamental aspects. Lasers Med Sci 2009; 24(29):259-68.
  • 4. Agostinis P, Berg K, Cengel KA et al. Photodynamic therapy of cancer: An update. CA Cancer J Clin 2011;V61(4):250-81. 2011.
  • 5. Fayter D, Corbett M, Heirs M, Fox D, Eastwood A. A systematic review of photodynamic therapy in the treatment of pre-cancerous skin conditions, Barrett's oesophagus and cancers of the biliary tract, brain, head and neck, lung, oesophagus and skin. Health Technol Assess 2010;14(37):1-288.
  • 6. Lo VC, Akens MK, Wise-Milestone L, Yee AJM, Wilson BC, Whyne CM. The benefits of photodynamic therapy on vertebral bone are maintained and enhanced by combination treatment with bisphosphonates and radiation therapy. J Orthop Res 2013; 31(9):1398-405.
  • 7. Irwin ME, Valle NRD, Chandra J. Redox control of leukemia: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2013;18(11):1349-83.
  • 8. Miller KD, Siegel RL, Lin CC et al. Cancer treatment and survivorship statistics. CA Cancer J Clin 2016; 66(4):271-89.
  • 9. Robertson CA, Evans DH, Abrahamse H. Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT. J Photochem Photobiol B Biol 2009;96(1):1-8.
  • 10. Juzeniene A, Moan J. The history of PDT in Norway: part one-identification of basic mechanisms of general PDT. Photodiagn Photodyn Ther 2007;4(1):3-11.
  • 11. Kwiatkowski S, Knap B, Przystupski D et al. Photodynamic therapy-mechanisms, photosensitizers and combinations. Biomed Pharmacother 2018;106:1098-107.
  • 12. Wang C, Cheng L, Liu Z. Upconversion nanoparticles for photodynamic therapy and other cancer therapeutics. Theranostics 2013;3(5):317-30.
  • 13. Sun X, Wong S, Liu X et al. Biosorption of malachite green from aqueous solutions onto aerobic granules: kinetic on equilibrium studies. Bioresour Technol 2008; 99 (9): 3475-83.
  • 14. Montes de Oca MN, Vara J,Milla L, Rivarola V, Ortiz CS. Physicochemical Properties and Photodynamic Activity of Novel Derivatives of Triarylmethane and Thiazine. Arch Pharm (Weinharm) 2013; 346 (4): 255-65
  • 15. Shimada T, Saito T, Okadome M et al. Secondary Leukemia After Chemotherapy and/or Radiotherapy for Gynecologic Neoplasia. Int J Gynecol Cancer 2014; 24(2): 178-83.
  • 16. Lv S, Li A, Wu H, Wang X. Observation of clinical efficacy and toxic and side effects of pirarubicin combined with cytarabine on acute myeloid leukemia. Oncol Lett 2019;17(3):3411-17.
  • 17. Lawitschka A, Peters C. Long-term Effects of Myeloablative Allogeneic Hematopoietic Stem Cell Transplantation in Pediatric Patients with Acute Lymphoblastic Leukemia. Curr Oncol Rep 2018; 20(9):74.
  • 18. Kennedy JC, Marcus SL, Pottier RH. Photodynamic Therapy (PDT) and Photodiagnosis (PD) Using Endogenous Photosensitization Induced by 5-Aminolevulinic Acid (ALA): Mechanisms and Clinical Results. J Clin Laser Med Surg 1996; 14(5): 289-304.
  • 19. Wang K, Yu B, Pathak JL. An update in clinical utilization of photodynamic therapy for lung cancer. J Cancer 2021;12(4); 1154-60.
  • 20. Sando Y, Matsuoka K, Sumii Y et al. Author Correction: 5-aminolevulinic acid-based photodynamic therapy can target aggressive adult T cell leukemia/lymphoma resistant to conventional chemotherapy. Sci Rep 2021; 11(1): 6420.
  • 21. Xu Y, Wang D, ZhuangZ et al. Hypericin-based photodynamic therapy induces apoptosis in K562 human leukemia cells through JNK pathway modulation. Mol Med Rep 2015; 12(5):6475-82.
  • 22. Zhang S, Zhang Z, Jiang D. Photodynamic therapy of different photosensitizers in leukemia. Proc. SPIE 4536, International Workshop on Photonics and Imaging in Biology and Medicine, (12 April 2002); https://doi.org/10.1117/12.462525
  • 23. Smetana K, Cajthamlová H, Grebenová D, Hrkal Z. The 5-aminolaevulinic acid-based photodynamic effects on nuclei and nucleoli of HL-60 leukemic granulocytic precursors. J Photochem Photobiol B Biol 2000; 59(1-3): 80-6.
  • 24. Lilge L, Molpus K, Hasan T, Wilson BC. Light dosimetry for intraperitoneal photodynamic therapy in a murine xenograft model of human epithelial ovarian carcinoma. Photochem Photobiol 1998; 68(3):281-8.
  • 25. Wormald R, Evans J, Smeeth L, Henshaw K. Photodynamic therapy for neovascular age-related macular degeneration. Cochrane Database Syst Rev 2003;(2):CD002030. doi: 10.1002/14651858.CD002030.
  • 26. Yuan M, Liu C, Li J et al. The effects of photodynamic therapy on leukemia cells mediated by KillerRed, a genetically encoded fluorescent protein photosensitizer. BMC Cancer 2019; 19(1): 934.
  • 27. Salmerón ML, Quintana-Aguiar J, De La Rosa JV et al. Phenalenone-photodynamic therapy induces apoptosis on human tumor cells mediated by caspase-8 and p38-MAPK activation. Mol Carcinog 2018; 57(11): 1525-39.
  • 28. Sun D, Lu Y, Zhang SJ, Wang KG, Li Y. The effect of ellagic acid on photodynamic therapy in leukemia cells. Gen Physiol Biophys 2018; 37(3); 319-28.
  • 29. Cisáriková A, Barbieriková Z, Janovec L et al. Acridin-3,6-dialkyldithiourea hydrochlorides as new photosensitizers for photodynamic therapy of mouse leukemia cells. Bioorg Med Chem 2016; 24(9): 2011-22.
  • 30. Feuser PE, Gaspar PC, Jacques AV et al. Synthesis of ZnPc loaded poly(methyl methacrylate) nanoparticles via miniemulsion polymerization for photodynamic therapy in leukemic cells. Mater Sci Eng C Mater Biol Appl 2016; 60: 458-66.
  • 31. Philchenkov AA, Shishko ED, Zavelevich MP et al. Photodynamic responsiveness of human leukemia Jurkat/A4 cells with multidrug resistant phenotype. Exp Oncol 2014; 36(4): 241-5.
  • 32. Zhang S, Sun D, Hao J, Wei YF, Yin LF, Liu X. The effect of dietary soyabean isoflavones on photodynamic therapy in K562 leukemia cells. J Photochem Photobiol B Biol 2012; 110, 28-33.
  • 33. Ettorre A, Frosali S, Andreassi M, Di Stefano A. Lycopene phytocomplex, but not pure lycopene, is able to trigger apoptosis and improve the efficacy of photodynamic therapy in HL60 human leukemia cells. Exp Biol Med 2010; 235(9): 1114-25.
  • 34. Čunderlíková B, Vasovič V, Sieber F, Furre T, Nesland JM, Peng Q. Hexaminolevulinate-based photodynamic purging of leukemia cells from BM. Bone Marrow Transplant 2010;45(10): 1553-61.
  • 35. Chen YJ, Huang WP, Yang YC et al. Platonin induces autophagy-associated cell death in human leukemia cells. Autophagy 2009; 5(2), 173-83.
  • 36. Zhang SJ, Zhang ZX. 5-aminolevulinic acid-based photodynamic therapy in leukemia cell HL60. Photochem Photobiol 2004; 79(6): 545-50.
  • 37. Di Stefano A, Ettorre A, Sbrana S, Giovani C, Neri P. Purpurin-18 in combination with light leads to apoptosis or necrosis in HL60 leukemia cells. Photochem Photobiol 2001;73(3): 290-96.
  • 38. Grebenová D, Cajthamlová H, Holada K, Marinov J, Jirsa M, Hrkal Z. Photodynamic effects of meso-tetra (4-sulfonatophenyl)porphine on human leukemia cells HEL and HL60, human lymphocytes and bone marrow progenitor cells. J Photochem Photobiol B Biol 1997;39(3); 269-78.

Akut Miyeloid Lösemide Malahit Yeşili-Bazlı Fotodinamik Tedavinin Terapötik Etkinliği

Yıl 2023, Cilt: 13 Sayı: 2, 305 - 311, 22.03.2023
https://doi.org/10.16899/jcm.1251398

Öz

Amaç: Akut miyeloid lösemi (AML), çoğu hastada nüks ve tedavi direnci ile karakterize bir hastalıktır. Bu yüzden AML de hedefleme tedavilerine ihtiyaç vardır. Fotodinamik tedavi (FDT), malign tümörlerin tedavisi için umut verici bir alternatiftir. Aynı zamanda FDT, lösemi tedavisinde tek başına veya tamamlayıcı olarak kullanılma potansiyeline sahiptir. Bu çalışmada malahit yeşili (MG) aracılı FDT'nin akut miyeloid lösemi hücreleri üzerindeki olası etkisinin araştırılması amaçlanmıştır.
Gereç ve Yöntem: Hücreler 0.19, 0.39, 0.78, 1.56, 3.125 ve 6.25 μM MG ile bir saat süreyle inkübe edildi ve 46.4 J/cm2 ışık ışınına tabi tutuldu. Hücrelerin canlılığını değerlendirmek için tripan mavisi testi kullanıldı ve mitokondriyal aktivite değişikliği MTT ile belirlendi. Morfolojik özellikler Giemsa boyama ve taramalı elektron mikroskobu ile belirlenmiştir. Hücre döngüsü ve Annexin V/PI testleri (boyama reaktifleri tarafından yayılan floresan ölçümü) akım sitometrisi ile ölçüldü.
Bulgular: MG ve ışık kombinasyonu ile HL60 hücre canlılığının kontrol grubuna göre anlamlı derecede azaldığı bulunmuştur. Giemsa boyama ve SEM sonuçları, 3.125 μM MG aracılı FDT’nin,hücrelerde apoptoz için tipik olan çeşitli morfolojik değişikliği indüklediğini göstermiştir. Annexin/PI boyamasına göre 3.125 μM MG kombine FDT ile tedavi edilen hücrelerde geç apoptoz gözlenmiş, ayrıca hücre döngüsünde subG1 fazında bir durmaya neden olduğunu göstermiştir.
Sonuç: MG aracılı FDT, HL60 hücrelerini inaktive etme potansiyeline sahiptir. Bu nedenle, MG bazlı FDT, akut miyeloid lösemi hücreleri için umut verici bir yaklaşım sağlayabilir.

Proje Numarası

1919B011902306

Kaynakça

  • 1. Hamblin MR. Photodynamic Therapy for Cancer: What’s Past is Prologue. Photochem Photobiol 2020; 96(3): 506-16.
  • 2. Martirosyan AS, Vardapetyan HR, Tiratsuyan SG, Hovhannisyan AA. Biphasic dose-response of antioxidants in hypericin-induced photohemolysis. Photodiagnosis Photodyn Ther 2011;8(3):282-87.
  • 3. Plaetzer K, Krammer B, Berlanda J, Berr F, Kiesslich T. Photophysics and photochemistry of photodynamic therapy: Fundamental aspects. Lasers Med Sci 2009; 24(29):259-68.
  • 4. Agostinis P, Berg K, Cengel KA et al. Photodynamic therapy of cancer: An update. CA Cancer J Clin 2011;V61(4):250-81. 2011.
  • 5. Fayter D, Corbett M, Heirs M, Fox D, Eastwood A. A systematic review of photodynamic therapy in the treatment of pre-cancerous skin conditions, Barrett's oesophagus and cancers of the biliary tract, brain, head and neck, lung, oesophagus and skin. Health Technol Assess 2010;14(37):1-288.
  • 6. Lo VC, Akens MK, Wise-Milestone L, Yee AJM, Wilson BC, Whyne CM. The benefits of photodynamic therapy on vertebral bone are maintained and enhanced by combination treatment with bisphosphonates and radiation therapy. J Orthop Res 2013; 31(9):1398-405.
  • 7. Irwin ME, Valle NRD, Chandra J. Redox control of leukemia: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 2013;18(11):1349-83.
  • 8. Miller KD, Siegel RL, Lin CC et al. Cancer treatment and survivorship statistics. CA Cancer J Clin 2016; 66(4):271-89.
  • 9. Robertson CA, Evans DH, Abrahamse H. Photodynamic therapy (PDT): a short review on cellular mechanisms and cancer research applications for PDT. J Photochem Photobiol B Biol 2009;96(1):1-8.
  • 10. Juzeniene A, Moan J. The history of PDT in Norway: part one-identification of basic mechanisms of general PDT. Photodiagn Photodyn Ther 2007;4(1):3-11.
  • 11. Kwiatkowski S, Knap B, Przystupski D et al. Photodynamic therapy-mechanisms, photosensitizers and combinations. Biomed Pharmacother 2018;106:1098-107.
  • 12. Wang C, Cheng L, Liu Z. Upconversion nanoparticles for photodynamic therapy and other cancer therapeutics. Theranostics 2013;3(5):317-30.
  • 13. Sun X, Wong S, Liu X et al. Biosorption of malachite green from aqueous solutions onto aerobic granules: kinetic on equilibrium studies. Bioresour Technol 2008; 99 (9): 3475-83.
  • 14. Montes de Oca MN, Vara J,Milla L, Rivarola V, Ortiz CS. Physicochemical Properties and Photodynamic Activity of Novel Derivatives of Triarylmethane and Thiazine. Arch Pharm (Weinharm) 2013; 346 (4): 255-65
  • 15. Shimada T, Saito T, Okadome M et al. Secondary Leukemia After Chemotherapy and/or Radiotherapy for Gynecologic Neoplasia. Int J Gynecol Cancer 2014; 24(2): 178-83.
  • 16. Lv S, Li A, Wu H, Wang X. Observation of clinical efficacy and toxic and side effects of pirarubicin combined with cytarabine on acute myeloid leukemia. Oncol Lett 2019;17(3):3411-17.
  • 17. Lawitschka A, Peters C. Long-term Effects of Myeloablative Allogeneic Hematopoietic Stem Cell Transplantation in Pediatric Patients with Acute Lymphoblastic Leukemia. Curr Oncol Rep 2018; 20(9):74.
  • 18. Kennedy JC, Marcus SL, Pottier RH. Photodynamic Therapy (PDT) and Photodiagnosis (PD) Using Endogenous Photosensitization Induced by 5-Aminolevulinic Acid (ALA): Mechanisms and Clinical Results. J Clin Laser Med Surg 1996; 14(5): 289-304.
  • 19. Wang K, Yu B, Pathak JL. An update in clinical utilization of photodynamic therapy for lung cancer. J Cancer 2021;12(4); 1154-60.
  • 20. Sando Y, Matsuoka K, Sumii Y et al. Author Correction: 5-aminolevulinic acid-based photodynamic therapy can target aggressive adult T cell leukemia/lymphoma resistant to conventional chemotherapy. Sci Rep 2021; 11(1): 6420.
  • 21. Xu Y, Wang D, ZhuangZ et al. Hypericin-based photodynamic therapy induces apoptosis in K562 human leukemia cells through JNK pathway modulation. Mol Med Rep 2015; 12(5):6475-82.
  • 22. Zhang S, Zhang Z, Jiang D. Photodynamic therapy of different photosensitizers in leukemia. Proc. SPIE 4536, International Workshop on Photonics and Imaging in Biology and Medicine, (12 April 2002); https://doi.org/10.1117/12.462525
  • 23. Smetana K, Cajthamlová H, Grebenová D, Hrkal Z. The 5-aminolaevulinic acid-based photodynamic effects on nuclei and nucleoli of HL-60 leukemic granulocytic precursors. J Photochem Photobiol B Biol 2000; 59(1-3): 80-6.
  • 24. Lilge L, Molpus K, Hasan T, Wilson BC. Light dosimetry for intraperitoneal photodynamic therapy in a murine xenograft model of human epithelial ovarian carcinoma. Photochem Photobiol 1998; 68(3):281-8.
  • 25. Wormald R, Evans J, Smeeth L, Henshaw K. Photodynamic therapy for neovascular age-related macular degeneration. Cochrane Database Syst Rev 2003;(2):CD002030. doi: 10.1002/14651858.CD002030.
  • 26. Yuan M, Liu C, Li J et al. The effects of photodynamic therapy on leukemia cells mediated by KillerRed, a genetically encoded fluorescent protein photosensitizer. BMC Cancer 2019; 19(1): 934.
  • 27. Salmerón ML, Quintana-Aguiar J, De La Rosa JV et al. Phenalenone-photodynamic therapy induces apoptosis on human tumor cells mediated by caspase-8 and p38-MAPK activation. Mol Carcinog 2018; 57(11): 1525-39.
  • 28. Sun D, Lu Y, Zhang SJ, Wang KG, Li Y. The effect of ellagic acid on photodynamic therapy in leukemia cells. Gen Physiol Biophys 2018; 37(3); 319-28.
  • 29. Cisáriková A, Barbieriková Z, Janovec L et al. Acridin-3,6-dialkyldithiourea hydrochlorides as new photosensitizers for photodynamic therapy of mouse leukemia cells. Bioorg Med Chem 2016; 24(9): 2011-22.
  • 30. Feuser PE, Gaspar PC, Jacques AV et al. Synthesis of ZnPc loaded poly(methyl methacrylate) nanoparticles via miniemulsion polymerization for photodynamic therapy in leukemic cells. Mater Sci Eng C Mater Biol Appl 2016; 60: 458-66.
  • 31. Philchenkov AA, Shishko ED, Zavelevich MP et al. Photodynamic responsiveness of human leukemia Jurkat/A4 cells with multidrug resistant phenotype. Exp Oncol 2014; 36(4): 241-5.
  • 32. Zhang S, Sun D, Hao J, Wei YF, Yin LF, Liu X. The effect of dietary soyabean isoflavones on photodynamic therapy in K562 leukemia cells. J Photochem Photobiol B Biol 2012; 110, 28-33.
  • 33. Ettorre A, Frosali S, Andreassi M, Di Stefano A. Lycopene phytocomplex, but not pure lycopene, is able to trigger apoptosis and improve the efficacy of photodynamic therapy in HL60 human leukemia cells. Exp Biol Med 2010; 235(9): 1114-25.
  • 34. Čunderlíková B, Vasovič V, Sieber F, Furre T, Nesland JM, Peng Q. Hexaminolevulinate-based photodynamic purging of leukemia cells from BM. Bone Marrow Transplant 2010;45(10): 1553-61.
  • 35. Chen YJ, Huang WP, Yang YC et al. Platonin induces autophagy-associated cell death in human leukemia cells. Autophagy 2009; 5(2), 173-83.
  • 36. Zhang SJ, Zhang ZX. 5-aminolevulinic acid-based photodynamic therapy in leukemia cell HL60. Photochem Photobiol 2004; 79(6): 545-50.
  • 37. Di Stefano A, Ettorre A, Sbrana S, Giovani C, Neri P. Purpurin-18 in combination with light leads to apoptosis or necrosis in HL60 leukemia cells. Photochem Photobiol 2001;73(3): 290-96.
  • 38. Grebenová D, Cajthamlová H, Holada K, Marinov J, Jirsa M, Hrkal Z. Photodynamic effects of meso-tetra (4-sulfonatophenyl)porphine on human leukemia cells HEL and HL60, human lymphocytes and bone marrow progenitor cells. J Photochem Photobiol B Biol 1997;39(3); 269-78.
Toplam 38 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm Orjinal Araştırma
Yazarlar

Serçin Özlem Çalışkan 0000-0001-8464-5487

Ömer Furkan Duran 0000-0002-2490-6435

Cem Aslan 0000-0003-1244-7320

Hüsne Özen 0000-0002-2389-6941

Metin Çalışkan 0000-0002-9243-4943

Rahşan Ilıkçı Sağkan 0000-0003-3844-6158

Proje Numarası 1919B011902306
Erken Görünüm Tarihi 23 Ocak 2023
Yayımlanma Tarihi 22 Mart 2023
Kabul Tarihi 13 Mart 2023
Yayımlandığı Sayı Yıl 2023 Cilt: 13 Sayı: 2

Kaynak Göster

AMA Özlem Çalışkan S, Duran ÖF, Aslan C, Özen H, Çalışkan M, Ilıkçı Sağkan R. Therapeutic Efficacy of Malachite Green-Based Photodynamic Therapy in Acute Myeloid Leukemia. J Contemp Med. Mart 2023;13(2):305-311. doi:10.16899/jcm.1251398