Can the iron content of culture media impact on the leishmanicidal effect of artemisinin?

References

• WHO. Leishmaniasis: the disease. 2019. Available from: https://www.who.int/leishmaniasis/disease/en/
   Google Scholar
• Burza S, Croft SL, Boelaert M. Leishmaniasis. Lancet. 2018;392(10151):951–970.
   PubMed Web of Science ®Google Scholar
• Chakravarty J, Sundar S. Current and emerging medications for the treatment of leishmaniasis. Expert Opin Pharmacother. 2019;20(10):1251–1265.
   PubMed Web of Science ®Google Scholar
• Singh OP, Singh B, Chakravarty J, et al. Current challenges in treatment options for visceral leishmaniasis in India: a public health perspective. Infect Dis Poverty. 2016;5(1):19.
   PubMed Web of Science ®Google Scholar
• Croft SL, Sundar S, Fairlamb AH. Drug resistance in leishmaniasis. Clin Microbiol Rev. 2006;19(1):111–126.
   PubMed Web of Science ®Google Scholar
• Ponte-Sucre A, Gamarro F, Dujardin JC, et al. Drug resistance and treatment failure in leishmaniasis: a 21st century challenge. PLoS Negl Trop Dis. 2017;11(12):e0006052.
   PubMed Web of Science ®Google Scholar
• Kwofie KD, Sato K, Sanjoba C, et al. Oral activity of the antimalarial endoperoxide 6-(1,2,6,7-tetraoxaspiro[7.11]nonadec-4-yl)hexan-1-ol (N-251) against Leishmania donovani complex. PLoS Negl Trop Dis. 2019;13(3):e0007235.
   PubMed Web of Science ®Google Scholar
• Cortes S, Albuquerque A, Cabral LI, et al. In Vitro Susceptibility of Leishmania infantum to Artemisinin Derivatives and Selected Trioxolanes. Antimicrob Agents Chemother. 2015;59(8):5032–5035.
   PubMed Web of Science ®Google Scholar
• Sen R, Bandyopadhyay S, Dutta A, et al. Artemisinin triggers induction of cell-cycle arrest and apoptosis in Leishmania donovani promastigotes. J Med Microbiol. 2007;56(Pt 9):1213–1218.
   PubMed Web of Science ®Google Scholar
• De Sarkar S, Sarkar D, Sarkar A, et al. The leishmanicidal activity of artemisinin is mediated by cleavage of the endoperoxide bridge and mitochondrial dysfunction. Parasitology. 2019;146(4):511–520.
   PubMed Web of Science ®Google Scholar
• Geroldinger G, Tonner M, Hettegger H, et al. Mechanism of ascaridole activation in Leishmania. Biochem Pharmacol. 2017;132:48–62.
   PubMed Web of Science ®Google Scholar
• Geroldinger G, Tonner M, Quirgst J, et al. Activation of artemisinin and heme degradation in Leishmania tarentolae promastigotes: a possible link. Biochem Pharmacol. 2020;173:113737.
   PubMed Web of Science ®Google Scholar
• Monzote L, García M, Pastor J, et al. Essential oil from Chenopodium ambrosioides and main components: activity against Leishmania, their mitochondria and other microorganisms. Exp Parasitol. 2014;136:20–26.
   PubMed Web of Science ®Google Scholar
• Geroldinger G, Tonner M, Fudickar W, et al. Activation of anthracene endoperoxides in Leishmania and impairment of mitochondrial functions. Molecules. 2018;23(7):1680.
   Web of Science ®Google Scholar
• Copple IM, Mercer AE, Firman J, et al. Examination of the cytotoxic and embryotoxic potential and underlying mechanisms of next-generation synthetic trioxolane and tetraoxane antimalarials. Mol Med. 2012;18:1045–1055.
   PubMed Web of Science ®Google Scholar
• Loo CS, Lam NS, Yu D, et al. Artemisinin and its derivatives in treating protozoan infections beyond malaria. Pharmacol Res. 2017;117:192–217.
   PubMed Web of Science ®Google Scholar
• Efferth T, Benakis A, Romero MR, et al. Enhancement of cytotoxicity of artemisinins toward cancer cells by ferrous iron. Free Radic Biol Med. 2004;37(7):998–1009.
   PubMed Web of Science ®Google Scholar
• Meshnick SR, Yang YZ, Lima V, et al. Iron-dependent free radical generation from the antimalarial agent artemisinin (qinghaosu). Antimicrob Agents Chemother. 1993;37(5):1108–1114.
   PubMed Web of Science ®Google Scholar
• Sen R, Saha P, Sarkar A, et al. Iron enhances generation of free radicals by Artemisinin causing a caspase-independent, apoptotic death in Leishmania donovani promastigotes. Free Radic Res. 2010;44(11):1289–1295.
   PubMed Web of Science ®Google Scholar
• Aucamp J, Zuma NH, N'Da DD. In vitro efficacy of synthesized artemisinin derivatives against Leishmania promastigotes. Bioorg Med Chem Lett. 2020;30(22):127581.
   PubMed Web of Science ®Google Scholar
• Basco LK, Le Bras J. In vitro activity of artemisinin derivatives against African isolates and clones of Plasmodium falciparum. Am J Trop Med Hyg. 1993;49(3):301–307.
   PubMed Web of Science ®Google Scholar
• Avery MA, Muraleedharan KM, Desai PV, et al. Structure-activity relationships of the antimalarial agent artemisinin. 8. design, synthesis, and CoMFA studies toward the development of artemisinin-based drugs against leishmaniasis and malaria. J Med Chem. 2003;46(20):4244–4258.
   PubMed Web of Science ®Google Scholar
• Machín L, Nápoles R, Gille L, et al. Leishmania amazonensis response to artemisinin and derivatives. Parasitol Int. 2021;80:102218.
   PubMed Web of Science ®Google Scholar
• Yang DM, Liew FY. Effects of qinghaosu (artemisinin) and its derivatives on experimental cutaneous leishmaniasis. Parasitology. 1993;106(1):7–11.
   PubMedGoogle Scholar
• Ganguly S, Bandyopadhyay S, Sarkar A, et al. Development of a semi-automated colorimetric assay for screening anti-leishmanial agents. J Microbiol Methods. 2006;66(1):79–86.
   PubMed Web of Science ®Google Scholar
• Dighal A, Mukhopadhyay D, Sengupta R, et al. Iron trafficking in patients with Indian Post kala-azar dermal leishmaniasis. PLoS Negl Trop Dis. 2020;14(2):e0007991.
   PubMed Web of Science ®Google Scholar
• Tenopoulou M, Kurz T, Doulias PT, et al. Does the calcein-AM method assay the total cellular 'labile iron pool' or only a fraction of it? Biochem J. 2007;403(2):261–266.
   PubMedGoogle Scholar
• Arnoult D, Akarid K, Grodet A, et al. On the evolution of programmed cell death: apoptosis of the unicellular eukaryote Leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ. 2002;9(1):65–81.
   PubMed Web of Science ®Google Scholar
• Dong Y, Vennerstrom JL. Mechanisms of in situ activation for peroxidic antimalarials. Redox Rep. 2003;8(5):284–288.
   PubMed Web of Science ®Google Scholar
• Mittra B, Andrews NW. IRONy OF FATE: role of iron-mediated ROS in Leishmania differentiation. Trends Parasitol. 2013;29(10):489–496.
   PubMed Web of Science ®Google Scholar
• Ortalli M, Varani S, Cimato G, et al. Evaluation of the pharmacophoric role of the O-O bond in synthetic antileishmanial compounds: comparison between 1,2-dioxanes and tetrahydropyrans. J Med Chem. 2020;63(21):13140–13158.
   PubMed Web of Science ®Google Scholar
• Mukanganyama S, Naik YS, Widersten M, et al. Proposed reductive metabolism of artemisinin by glutathione transferases in vitro. Free Radic Res. 2001;35(4):427–434.
   PubMed Web of Science ®Google Scholar
• Parapini S, Olliaro P, Navaratnam V, et al. Stability of the antimalarial drug dihydroartemisinin under physiologically relevant conditions: implications for clinical treatment and pharmacokinetic and in vitro assays. Antimicrob Agents Chemother. 2015;59(7):4046–4052.
   PubMed Web of Science ®Google Scholar
• Stockwin LH, Han B, Yu SX, et al. Artemisinin dimer anticancer activity correlates with heme-catalyzed reactive oxygen species generation and endoplasmic reticulum stress induction. Int J Cancer. 2009;125(6):1266–1275.
   PubMed Web of Science ®Google Scholar
• O’Neill PM, Barton VE, Ward SA. The molecular mechanism of action of artemisinin–the debate continues. Molecules. 2010;15(3):1705–1721.
   PubMed Web of Science ®Google Scholar
• Antoine T, Fisher N, Amewu R, et al. Rapid kill of malaria parasites by artemisinin and semi-synthetic endoperoxides involves ROS-dependent depolarization of the membrane potential. J Antimicrob Chemother. 2014;69(4):1005–1016.
   PubMed Web of Science ®Google Scholar
• Taylor MC, Kelly JM. Iron metabolism in trypanosomatids, and its crucial role in infection. Parasitology. 2010;137(6):899–917.
   PubMed Web of Science ®Google Scholar
• Kaiser M, Wittlin S, Nehrbass-Stuedli A, et al. Peroxide bond-dependent antiplasmodial specificity of artemisinin and OZ277 (RBx11160). Antimicrob Agents Chemother. 2007;51(8):2991–2993.
   PubMed Web of Science ®Google Scholar
• Tilley L, Straimer J, Gnädig NF, et al. Artemisinin action and resistance in Plasmodium falciparum. Trends Parasitol. 2016;32(9):682–696.
   PubMed Web of Science ®Google Scholar
• Kwok JC, Richardson DR. The iron metabolism of neoplastic cells: alterations that facilitate proliferation? Crit Rev Oncol Hematol. 2002;42(1):65–78.
   PubMed Web of Science ®Google Scholar
• Ooko E, Saeed ME, Kadioglu O, et al. Artemisinin derivatives induce iron-dependent cell death (ferroptosis) in tumor cells. Phytomedicine. 2015;22(11):1045–1054.
   PubMed Web of Science ®Google Scholar
• Shterman N, Kupfer B, Moroz C. Comparison of transferrin receptors, iron content and isoferritin profile in normal and malignant human breast cell lines. Pathobiology. 1991;59(1):19–25.
   PubMed Web of Science ®Google Scholar
• Konstat-Korzenny E, Ascencio-Aragón JA, Niezen-Lugo S, et al. Artemisinin and its synthetic derivatives as a possible therapy for cancer. Med Sci (Basel). 2018;6(1):19.
   Google Scholar
• Tangnitipong S, Thaptimthong T, Srihirun S, et al. Extracellular heme enhances the antimalarial activity of artemisinin. Biol Pharm Bull. 2012;35(1):29–33.
   PubMed Web of Science ®Google Scholar
• Pagura L, Tevere E, Merli ML, et al. A new model for Trypanosoma cruzi heme homeostasis depends on modulation of TcHTE protein expression. J Biol Chem. 2020;295(38):13202–13212.
   PubMed Web of Science ®Google Scholar
• Huynh C, Andrews NW. Iron acquisition within host cells and the pathogenicity of Leishmania. Cell Microbiol. 2008;10(2):293–300.
   PubMed Web of Science ®Google Scholar
• D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol. 2007;8:813–824.
   PubMed Web of Science ®Google Scholar
• Jaeger T, Flohé L. The thiol-based redox networks of pathogens: unexploited targets in the search for new drugs. Biofactors. 2006;27(1–4):109–120.
   PubMed Web of Science ®Google Scholar
• Dodd S, Dean O, Copolov DL, et al. N-acetylcysteine for antioxidant therapy: pharmacology and clinical utility. Expert Opin Biol Ther. 2008;8(12):1955–1962.
   PubMed Web of Science ®Google Scholar
• Debrabant A, Lee N, Bertholet S, et al. Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol. 2003;33(3):257–267.
   PubMed Web of Science ®Google Scholar
• Dixon SJ, Stockwell BR. The hallmarks of ferroptosis. Annu Rev Cancer Biol. 2019;3(1):35–54.
   Google Scholar
• Li J, Cao F, Yin HL, et al. Ferroptosis: past, present and future. Cell Death Dis. 2020;11(2):88.
   PubMed Web of Science ®Google Scholar
• Anderson GJ, Frazer DM. Current understanding of iron homeostasis. Am J Clin Nutr. 2017;106(6):1559S–1566S.
   PubMed Web of Science ®Google Scholar
• Gonciarz RL, Collisson EA, Renslo AR. Ferrous iron-dependent pharmacology. Trends Pharmacol Sci. 2021;42(1):7–18.
   PubMed Web of Science ®Google Scholar
• Kakhlon O, Cabantchik ZI. The labile iron pool: characterization, measurement, and participation in cellular processes. Free Radic Biol Med. 2002;33(8):1037–1046.
   PubMed Web of Science ®Google Scholar