Anticancer properties of a new platinum (IV) agent on HT1080 cancer stem-like cells: an in vitro study
-
Seyede Masoome Sajjadi Mohri
,
Vahideh Montazeri
,
Shima Aliebrahimi
,
Anita Abedi
,
Marzieh Zare Dehnavi
,
Akram Jamshidzadeh
,
Seyed Nasser Ostad
Abstract
According to the cancer stem cell (CSC) theory, a subpopulation of cells demonstrating stem-like cell properties is responsible for tumorigenicity, self-renewal capacity, therapy resistance, and recurrence. Due to CSCs’ resistance, it’s demanded to develop drugs having appropriate efficacy. Despite cisplatin is a potent antitumor agent widely used in the treatment of different cancers, its severe side effects and resistance remain a challenge in the clinic. Research has shown that platinum (IV) has considerably fewer side effects and drug resistance. In this study, toxicity and effectiveness of [Pt(dpyam)Cl4] where dpyam is 2,2'-dipyridylamine, as a platinum (IV) agent, has been investigated to find a reliable alternative for cisplatin. To this aim, cancer stem-like cells (CS-LCs) with CD44+/CD133+ phenotype were isolated from HT1080 cells. EJ138, HT1080, and its CS-LCs were selected to compare the effectiveness of Pt (IV) complex versus cisplatin. MTT, apoptosis, and cell cycle analysis were carried out to evaluate drug toxicity. Sphere and colony formation assays confirmed the potentiality of Pt (IV) complex and cisplatin to target stemness characteristics in CS-LCs. Although toxicity results were in favor of cisplatin, the anti-cancer activity of the synthesized Pt (IV) complex was also considerable. Regarding other studies that proposed high selective toxicity of Pt (IV), they could be a volunteer for additional improvements.
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31. Nassar D, Blanpain C. Cancer stem cells: Basic concepts and therapeutic implications. Annu Rev Pathol 2016;11(1):47-76.
32. Genadry KC, Pietrobono S, Rota R, Linardic CM. Soft tissue sarcoma cancer stem cells: An overview. Front Oncol 2018;8:475.
33. Choy H, Park C, Yao M. Current status and future prospects for satraplatin, an oral platinum analogue. Clin Cancer Res 2008;14(6):1633-8.
34. Sarin N, Engel F, Kalayda GV, Mannewitz M, Cinatl J, Jr., Rothweiler F, et al. Cisplatin resistance in non-small cell lung cancer cells is associated with an abrogation of cisplatin-induced G2/M cell cycle arrest. PLoS One 2017;12(7):e0181081.
35. Montazeri V, Ghahremani MH, Montazeri H, Hasanzad M, Safavi M, Ayati M, et al. A preliminary study of NER and MMR pathways involved in chemotherapy response in bladder transitional cell carcinoma: Impact on progression-free survival. Iran J Pharm Res 2020;19(1):355-65.
36. Aghmasheh S, Ostad SN, Abedi A. Pharmacological properties of Pt (II) and Pt (IV) complexes with 2, 2′-dipyridylamine; the comparative in vitro thereof. Cell Biochem Biophys 2020;78(4):521-9.
37. Zhang D, Piao H-L, Li Y-H, Qiu Q, Li D-J, Du M-R, et al. Inhibition of AKT sensitizes chemoresistant ovarian cancer cells to cisplatin by abrogating S and G2/M arrest. Exp Mol Pathol 2016;100(3):506-13.
38. Fujii H, Honoki K, Tsujiuchi T, Kido A, Yoshitani K, Takakura Y. Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int J Oncol 2009;34(5):1381-6.
2. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63(18):5821-8.
3. Beck B, Blanpain C. Unravelling cancer stem cell potential. Nat Rev Cancer 2013;13(10):727-38.
4. Zabala M, Lobo N, Qian D, van Weele L, Heiser D, Clarke M, et al. Overview: Cancer stem cell self-renewal. In: Cancer stem cells. 2016, Academic Press. p. 25-58.
5. Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: An evolving concept. Nat Rev Cancer 2012;12(2):133-43.
6. Clarke MF, Hass AT. Cancer stem cells. 2nd ed. Encyclopedia of Molecular Cell Biology and Molecular Medicine, 2006: 221-240.
7. Feng BH, Liu AG, Gu WG, Deng L, Cheng XG, Tong TJ, et al. CD133+ subpopulation of the HT1080 human fibrosarcoma cell line exhibits cancer stem-like characteristics. Oncol Rep 2013;30(2):815-23.
8. Li Z. CD133: A stem cell biomarker and beyond. Exp Hematol Oncol 2013;2(1):1-8.
9. Warrier S, Pavanram P, Raina D, Arvind M. Study of chemoresistant CD133+ cancer stem cells from human glioblastoma cell line U138MG using multiple assays. Cell Biol Int 2012;36(12):1137-43.
10. Babjuk M, Böhle A, Burger M, Capoun O, Cohen D, Compérat EM, et al. EAU guidelines on non–muscle-invasive urothelial carcinoma of the bladder: Update 2016. Eur Urol 2017;71(3):447-61.
11. Hernández P, Alem D, Nieves M, Cerecetto H, González M, Martínez-López W, et al. Chemosensitizer effect of cisplatin-treated bladder cancer cells by phenazine-5, 10-dioxides. Environ Toxicol Pharmacol 2019;69:9-15.
12. Eastman A. The mechanism of action of cisplatin: From adducts to apoptosis. In Cisplatin. Chemistry and biochemistry of a leading anticancer drug. Verlag Helvetica Chimica Acta, 1999:111-34.
13. Dasari S, Tchounwou PB. Cisplatin in cancer therapy: Molecular mechanisms of action. Eur J Pharmacol 2014;740:364-78.
14. Chen S-H, Chang J-Y. New insights into mechanisms of cisplatin resistance: From tumor cell to microenvironment. Int J Mol Sci 2019;20(17):4136.
15. Zhu H, Luo H, Zhang W, Shen Z, Hu X, Zhu X. Molecular mechanisms of cisplatin resistance in cervical cancer. Drug Des Devel Ther 2016;10:1885.
16. Martin LP, Hamilton TC, Schilder RJ. Platinum resistance: The role of DNA repair pathways. Clin Cancer Res 2008;14(5):1291-5.
17. Loh S, Mistry P, Kelland L, Abel G, Harrap K. Reduced drug accumulation as a major mechanism of acquired resistance to cisplatin in a human ovarian carcinoma cell line: Circumvention studies using novel platinum (II) and (IV) ammine/amine complexes. Br J Cancer 1992;66(6):1109-15.
18. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, et al. Molecular mechanisms of cisplatin resistance. Oncogene 2012;31(15):1869-83.
19. Kartalou M, Essigmann JM. Mechanisms of resistance to cisplatin. Mutat Res 2001;478(1):23-43.
20. Kaufman DS, Shipley WU, Feldman AS. Bladder cancer. Lancet 2009;374(9685):239-49.
21. Dobruch J, Daneshmand S, Fisch M, Lotan Y, Noon AP, Resnick MJ, et al. Gender and bladder cancer: A collaborative review of etiology, biology, and outcomes. Eur Urol 2016;69(2):300-10.
22. Amable L. Cisplatin resistance and opportunities for precision medicine. Pharmacol Res 2016;106:27-36.
23. Mankin HJ, Hornicek FJ. Diagnosis, classification, and management of soft tissue sarcomas. Cancer Control 2005;12(1):5-21.
24. Coindre J-M. Grading of soft tissue sarcomas: Review and update. Arch Pathol Lab Med 2006;130(10):1448-53.
25. Augsburger D, Nelson PJ, Kalinski T, Udelnow A, Knösel T, Hofstetter M, et al. Current diagnostics and treatment of fibrosarcoma -perspectives for future therapeutic targets and strategies. Oncotarget 2017;8(61):104638-53.
26. Abedi A, Amani V, Safari N, Ostad SN, Notash B. From proton transferred to cyclometalated platinum (IV) complex: Crystal structure and biological activity. J Organomet Chem 2015;799:30-7.
27. Kelland LR, Murrer BA, Abel G, Giandomenico CM, Mistry P, Harrap KR. Ammine/amine platinum (IV) dicarboxylates: A novel class of platinum complex exhibiting selective cytotoxicity to intrinsically cisplatin-resistant human ovarian carcinoma cell lines. Cancer Res 1992;52(4):822-8.
28. Shahsavar F, Bozorgmehr M, Mirzadegan E, Abedi A, Mehri Lighvan Z, Mohammadi F, et al. A novel platinum-based compound with preferential cytotoxic activity against a panel of cancer cell lines. Anticancer Agents Med Chem 2016;16(3):393-403.
29. Wosikowski K, Lamphere L, Unteregger G, Jung V, Kaplan F, Xu JP, et al. Preclinical antitumor activity of the oral platinum analog satraplatin. Cancer Chemother Pharmacol 2007;60(4):589-600.
30. Kozubík A, Horváth V, Švihálková-Šindlerová L, Souček K, Hofmanová J, Sova P, et al. High effectiveness of platinum (IV) complex with adamantylamine in overcoming resistance to cisplatin and suppressing proliferation of ovarian cancer cells in vitro. Biochem Pharmacol 2005;69(3):373-83.
31. Nassar D, Blanpain C. Cancer stem cells: Basic concepts and therapeutic implications. Annu Rev Pathol 2016;11(1):47-76.
32. Genadry KC, Pietrobono S, Rota R, Linardic CM. Soft tissue sarcoma cancer stem cells: An overview. Front Oncol 2018;8:475.
33. Choy H, Park C, Yao M. Current status and future prospects for satraplatin, an oral platinum analogue. Clin Cancer Res 2008;14(6):1633-8.
34. Sarin N, Engel F, Kalayda GV, Mannewitz M, Cinatl J, Jr., Rothweiler F, et al. Cisplatin resistance in non-small cell lung cancer cells is associated with an abrogation of cisplatin-induced G2/M cell cycle arrest. PLoS One 2017;12(7):e0181081.
35. Montazeri V, Ghahremani MH, Montazeri H, Hasanzad M, Safavi M, Ayati M, et al. A preliminary study of NER and MMR pathways involved in chemotherapy response in bladder transitional cell carcinoma: Impact on progression-free survival. Iran J Pharm Res 2020;19(1):355-65.
36. Aghmasheh S, Ostad SN, Abedi A. Pharmacological properties of Pt (II) and Pt (IV) complexes with 2, 2′-dipyridylamine; the comparative in vitro thereof. Cell Biochem Biophys 2020;78(4):521-9.
37. Zhang D, Piao H-L, Li Y-H, Qiu Q, Li D-J, Du M-R, et al. Inhibition of AKT sensitizes chemoresistant ovarian cancer cells to cisplatin by abrogating S and G2/M arrest. Exp Mol Pathol 2016;100(3):506-13.
38. Fujii H, Honoki K, Tsujiuchi T, Kido A, Yoshitani K, Takakura Y. Sphere-forming stem-like cell populations with drug resistance in human sarcoma cell lines. Int J Oncol 2009;34(5):1381-6.
| Files | ||
| Issue | Vol 60 No 12 (2022) | |
| Section | Articles | |
| DOI | https://doi.org/10.18502/acta.v60i12.11828 | |
| Keywords | ||
| Cancer stem-like cells Platinum (IV) Cisplatin Cytotoxicity Self-renewal | ||
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How to Cite
1.
Sajjadi Mohri SM, Montazeri V, Aliebrahimi S, Abedi A, Zare Dehnavi M, Jamshidzadeh A, Ostad SN. Anticancer properties of a new platinum (IV) agent on HT1080 cancer stem-like cells: an in vitro study. Acta Med Iran. 2023;60(12):756-764.
