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Selenium-induced apoptosis-like cell death in Plasmodium falciparum

Published online by Cambridge University Press:  19 August 2011

EKA W. SURADJI*
Affiliation:
Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan
TOSHIMITSU HATABU
Affiliation:
Gunma University Graduate School of Health Sciences, 3-39-15 Showa-machi, Maebashi 371-8514, Japan
KENJI KOBAYASHI
Affiliation:
Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan
CHIHO YAMAZAKI
Affiliation:
Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan
RIZKY ABDULAH
Affiliation:
Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan
MINATO NAKAZAWA
Affiliation:
Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan
JUNKO NAKAJIMA-SHIMADA
Affiliation:
Gunma University Graduate School of Health Sciences, 3-39-15 Showa-machi, Maebashi 371-8514, Japan
HIROSHI KOYAMA
Affiliation:
Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa-machi, Maebashi, Gunma 371-8511, Japan
*
*Corresponding author: Department of Public Health, Gunma University, Graduate School of Medicine, 3-39-22 Showa machi, Maebashi 371-8511, Japan. Tel: +81 27 220 8015. Fax: +81 27 220 8016. E-mail: [email protected]

Summary

Plasmodium falciparum has for some time been developing resistance against known anti-malarial drugs, and therefore a new drug is urgently needed. Selenium (Se), an essential trace element, in the form of inorganic Se, selenite (SeO32−), has been reported to have an anti-plasmodial effect, but its mechanism is still unclear. In the present study, we evaluated the anti-plasmodial effect of several Se compounds against P. falciparum in vitro. The anti-plasmodial effect of several Se compounds was analysed and their apoptosis-inducing activity was evaluated by morphological observation, DNA fragmentation assay and mitochondrial function analysis. SeO32−, methylseleninic acid, selenomethionine and selenocystine have anti-plasmodial effects with 50% inhibition concentration at 9, 10, 45, and 65 μm, respectively, while selenate and methylselenocysteine up to 100 μm have no effect on parasite growth. The effective Se compounds caused the parasites to become shrunken and pyknotic and significantly increased mitochondrial damage against P. falciparum compared to the untreated control. In conclusion, SeO32−, methylseleninic acid, selenomethionine and selenocystine have anti-plasmodial activities that induce apoptosis-like cell death in P. falciparum, and the anti-plasmodial effects of Se seem to be based on its chemical forms. The apoptosis-like cell-death mechanism in P. falciparum can be beneficial to respond to the growing problem of drug resistance.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Abdulah, R., Faried, A., Kobayashi, K., Yamazaki, C., Suradji, E. W., Ito, K., Suzuki, K., Murakami, M., Kuwano, H. and Koyama, H. (2009). Selenium enrichment of broccoli sprout extract increases chemosensitivity and apoptosis of LNCaP prostate cancer cells. BMC Cancer 9, 414. doi: 10.1186/1471-2407-9-414.CrossRefGoogle ScholarPubMed
Alexander, J. (2007). Selenium. Novartis Foundation Symposium 282, 143149, 149153, 212–148.CrossRefGoogle ScholarPubMed
Baritaud, M., Boujrad, H., Lorenzo, H. K., Krantic, S. and Susin, S. A. (2010). Histone H2AX: The missing link in AIF-mediated caspase-independent programmed necrosis. Cell Cycle 9, 31663173. doi: 10.4161/cc.9.16.12552.Google Scholar
Bebien, M., Kirsch, J., Mejean, V. and Vermeglio, A. (2002). Involvement of a putative molybdenum enzyme in the reduction of selenate by Escherichia coli. Microbiology 148, 38653872.Google Scholar
Becker, K., Rahlfs, S., Nickel, C. and Schirmer, R. H. (2003). Glutathione–functions and metabolism in the malarial parasite Plasmodium falciparum. Biological Chemistry 384, 551566. doi: 10.1515/BC.2003.063.Google Scholar
Breman, J. G. (2009). Eradicating malaria. Science Progress 92, 138. doi: 10.3184/003685009X440290Google Scholar
Budihardjo, I., Oliver, H., Lutter, M., Luo, X. and Wang, X. (1999). Biochemical pathways of caspase activation during apoptosis. Annual Review of Cell and Developmental Biology 15, 269290. doi: 1081-0706/99/1115-0269$08.00.CrossRefGoogle ScholarPubMed
Dame, J. B., Williams, J. L., Mccutchan, T. F., Weber, J. L., Wirtz, R. A., Hockmeyer, W. T., Maloy, W. L., Haynes, J. D., Schneider, I., Roberts, D., Sanders, G. S. and Reddy, E. P. (1984). Structure of the gene encoding the immunodominant surface antigen on the sporozoite of the human malaria parasite Plasmodium falciparum. Science 225, 593599. doi: 10.1126/science.6204383CrossRefGoogle ScholarPubMed
Davis, R. L. and Spallholz, J. E. (1996). Inhibition of selenite-catalyzed superoxide generation and formation of elemental selenium (Se(o)) by copper, zinc, and aurintricarboxylic acid (ATA). Biochemical Pharmacology 51, 10151020. doi: 10.1016/0006-2952(95)02435-2Google Scholar
Epstein, D. (1999). Malaria: failure, puzzle, challenge. Perspective in Health 4, 27.Google Scholar
Faried, A., Faried, L. S., Kimura, H., Sohda, M., Nakajima, M., Miyazaki, T., Kato, H., Kanuma, T. and Kuwano, H. (2006). Differential sensitivity of paclitaxel-induced apoptosis in human esophageal squamous cell carcinoma cell lines. Cancer Chemotherapy and Pharmacology 57, 301308. doi: 10.1007/s00280-005-0038-zGoogle Scholar
Hu, H., Jiang, C., Li, G. and Lu, J. (2005). PKB/AKT and ERK regulation of caspase-mediated apoptosis by methylseleninic acid in LNCaP prostate cancer cells. Carcinogenesis 26, 13741381. doi: 10.1093/carcin/bgi094Google Scholar
Jackson, M. I. and Combs, G. F. Jr. (2008). Selenium and anticarcinogenesis: underlying mechanisms. Current Opinion in Clinical Nutrition and Metabolic Care 11, 718726. doi: 10.1097/MCO.0b013e3283139674CrossRefGoogle ScholarPubMed
Jiang, C., Wang, Z., Ganther, H. and Lu, J. (2002). Distinct effects of methylseleninic acid versus selenite on apoptosis, cell cycle, and protein kinase pathways in DU145 human prostate cancer cells. Molecular Cancer Therapy 1, 10591066.Google Scholar
Kitahara, J., Seko, Y. and Imura, N. (1993). Possible involvement of active oxygen species in selenite toxicity in isolated rat hepatocytes. Archives of Toxicology 67, 497501.CrossRefGoogle ScholarPubMed
Le Chat, L., Sinden, R. E. and Dessens, J. T. (2007). The role of metacaspase 1 in Plasmodium berghei development and apoptosis. Molecular and Biochemical Parasitology 153, 4147. doi: 10.1016/j.molbiopara.2007.01.016 Google Scholar
Lee, S. O., Nadiminty, N., Wu, X. X., Lou, W., Dong, Y., Ip, C., Onate, S. A. and Gao, A. C. (2005). Selenium disrupts estrogen signaling by altering estrogen receptor expression and ligand binding in human breast cancer cells. Cancer Research 65, 34873492. doi: 10.1158/0008-5472.CAN-04-326Google Scholar
Lippman, S. M., Klein, E. A., Goodman, P. J., Lucia, M. S., Thompson, I. M., Ford, L. G., Parnes, H. L., Minasian, L. M., Gaziano, J. M., Hartline, J. A., Parsons, J. K., Bearden, J. D. 3rd, Crawford, E. D., Goodman, G. E., Claudio, J., Winquist, E., Cook, E. D., Karp, D. D., Walther, P., Lieber, M. M., Kristal, A. R., Darke, A. K., Arnold, K. B., Ganz, P. A., Santella, R. M., Albanes, D., Taylor, P. R., Probstfield, J. L., Jagpal, T. J., Crowley, J. J., Meyskens, F. L. Jr, Baker, L. H. and Coltman, C. A. Jr. (2009). Effect of selenium and vitamin E on risk of prostate cancer and other cancers: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). The Journal of The American Medical Association 301, 3951. doi: 10.1001/jama.2008.864Google Scholar
Marinho-Filho, J. D., Bezerra, D. P., Araújo, A. J., Montenegro, R. C., Pessoa, C., Diniz, J. C., Viana, F. A., Pessoa, O. D., Silveira, E. R., de Moraes, M. O. and Costa-Lotufo, L. V. (2010). Oxidative stress induction by (+)-cordiaquinone J triggers both mitochondria-dependent apoptosis and necrosis in leukemia cells. Chemico-Biological Interactions 183, 369379. doi: 10.1016/j.cbi.2009.11.030CrossRefGoogle ScholarPubMed
Meslin, B., Barnadas, C., Boni, V., Latour, C., De Monbrison, F., Kaiser, K. and Picot, S. (2007). Features of apoptosis in Plasmodium falciparum erythrocytic stage through a putative role of PfMCA1 metacaspase-like protein. Journal of Infectious Diseases 195, 18521859. doi: 10.1086/518253Google Scholar
Menna-Barreto, R. F., Corrêa, J. R., Pinto, A. V., Soares, M. J. and de Castro, S. (2007). Mitochondrial disruption and DNA fragmentation in Trypanosoma cruzi induced by naphthoimidazoles synthesized from beta-lapachone. Parasitology Research 4, 895905. doi: 10.1007/s00436-007-0556-1Google Scholar
Muller, S. (2004). Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Molecular Microbiology 53, 12911305. doi: 10.1111/j.1365-2958.2004.04257.xCrossRefGoogle ScholarPubMed
Nian, H., Bisson, W. H., Dashwood, W. M., Pinto, J. T. and Dashwood, R. H. (2009). Alpha-keto acid metabolites of organoselenium compounds inhibit histone deacetylase activity in human colon cancer cells. Carcinogenesis 30, 14161423. doi: 10.1093/carcin/bgp147Google Scholar
Nyakeriga, A. M., Perlmann, H., Hagstedt, M., Berzins, K., Troye-Blomberg, M., Zhivotovsky, B., Perlmann, P. and Grandien, A. (2006). Drug-induced death of the asexual blood stages of Plasmodium falciparum occurs without typical signs of apoptosis. Microbes and Infection 8, 15601568. doi: 10.1016/j.micinf.2006.01.016Google Scholar
Orjih, A. U. (1997). Heme polymerase activity and the stage specificity of antimalarial action of chloroquine. The Journal of Pharmacology and Experimental Therapeutics 282, 108112. doi: 0022-3565/97/2821-0108Google Scholar
Ozben, T. (2006). Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Letters 580, 29032909. doi: 10.1016/j.febslet.2006.02.020Google Scholar
Picot, S., Burnod, J., Bracchi, V., Chumpitazi, B. F. and Ambroise-Thomas, P. (1997). Apoptosis related to chloroquine sensitivity of the human malaria parasite Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 590591. doi: 10.1016/S0035-9203(97)90039-0Google Scholar
Rogers, W. O., Sem, R., Tero, T., Chim, P., Lim, P., Muth, S., Socheat, D., Ariey, F. and Wongsrichanalai, C. (2009). Failure of artesunate-mefloquine combination therapy for uncomplicated Plasmodium falciparum malaria in southern Cambodia. Malaria Journal 8, 10. doi: 10.1186/1475-2875-8-10.CrossRefGoogle ScholarPubMed
Roth, E. F. Jr. (1987). Malarial parasite hexokinase and hexokinase-dependent glutathione reduction in the Plasmodium falciparum-infected human erythrocyte. Journal of Biological Chemistry 262, 1567815682.Google Scholar
Sashiyama, H., Shino, Y., Sakao, S., Shimada, H., Kobayashi, S., Ochiai, T. and Shirasawa, H. (2002). Alteration of integrin expression relates to malignant progression of human papillomavirus-immortalized esophageal keratinocytes. Cancer Letters 177, 2128. doi: 10.1016/S0304-3835(01)00771-6Google Scholar
Spallholz, J. E., Palace, V. P. and Reid, T. W. (2004). Methioninase and selenomethionine but not Se-methylselenocysteine generate methylselenol and superoxide in an in vitro chemiluminescent assay: implications for the nutritional carcinostatic activity of selenoamino acids. Biochemical Pharmacology 67, 547554. doi: 10.1016/j.bcp.2003.09.004Google Scholar
Spallholz, J. E., Shriver, B. J. and Reid, T. W. (2001). Dimethyldiselenide and methylseleninic acid generate superoxide in an in vitro chemiluminescence assay in the presence of glutathione: implications for the anticarcinogenic activity of L-selenomethionine and L-Se-methylselenocysteine. Nutrition and Cancer 40, 3441. doi: 10.1207/S15327914NC401_8Google Scholar
Suzuki, K. T., Kurasaki, K. and Suzuki, N. (2007). Selenocysteine beta-lyase and methylselenol demethylase in the metabolism of Se-methylated selenocompounds into selenide. Biochimica et Biophysica Acta 1770, 10531061. doi: 10.1016/j.bbagen.2007.03.007Google Scholar
Suzuki, K. T. and Ogra, Y. (2002). Metabolic pathway for selenium in the body: speciation by HPLC-ICP MS with enriched Se. Food Additives and Contaminants 19, 974983. doi: 10.1080/02652030210153578Google Scholar
Suzuki, K. T., Tsuji, Y., Ohta, Y. and Suzuki, N. (2008). Preferential organ distribution of methylselenol source Se-methylselenocysteine relative to methylseleninic acid. Toxicology and Applied Pharmacology 227, 7683. doi: 10.1016/j.taap.2007.10.001CrossRefGoogle ScholarPubMed
Taguchi, N., Hatabu, T., Yamaguchi, H., Suzuki, M., Sato, K. and Kano, S. (2004). Plasmodium falciparum: selenium-induced cytotoxicity to P. falciparum. Experimental Parasitology 106, 5055. doi: 10.1016/j.exppara.2004.01.005Google Scholar
Totino, P. R., Daniel-Ribeiro, C. T., Corte-Real, S. and De Fatima Ferreira-Da-Cruz, M. (2008). Plasmodium falciparum: erythrocytic stages die by autophagic-like cell death under drug pressure. Experimental Parasitology 118, 478486. doi: 10.1016/j.exppara.2007.10.017Google Scholar
Thanh, N. V., Toan, T. Q., Cowman, A. F., Casey, G. J., Phuc, B. Q., Tien, N. T., Hung, N. M. and Biggs, B. A. (2010). Monitoring for Plasmodium falciparum drug resistance to artemisinin and artesunate in Binh Phuoc Province, Vietnam: 1998–2009. Malaria Journal 9, 181. doi: 10.1186/1475-2875-9-181.CrossRefGoogle ScholarPubMed
Vermeulen, K., Van Bockstaele, D. R. and Berneman, Z. N. (2005). Apoptosis: mechanisms and relevance in cancer. Annals of Hematology 84, 627639. doi: 10.1007/s00277-005-1065-xGoogle Scholar
Wang, Z., Jiang, C. and Lu, J. (2002). Induction of caspase-mediated apoptosis and cell-cycle G1 arrest by selenium metabolite methylselenol. Molecular Carcinogenesis 34, 113120. doi: 10.1002/mc.10056CrossRefGoogle ScholarPubMed
Wells, V. and Mallucci, L. (2009). Phosphoinositide 3-kinase targeting by the beta galactoside binding protein cytokine negates akt gene expression and leads aggressive breast cancer cells to apoptotic death. Breast Cancer Research 11, R2. doi: 10.1186/bcr2217Google Scholar
Yan, L. and Spallholz, J. E. (1993). Generation of reactive oxygen species from the reaction of selenium compounds with thiols and mammary tumor cells. Biochemical Pharmacology 45, 429437. doi: 10.1016/0006-2952(93)90080-GGoogle Scholar
Zeng, H., Briske-Anderson, M., Idso, J. P. and Hunt, C. D. (2006). The selenium metabolite methylselenol inhibits the migration and invasion potential of HT1080 tumor cells. Journal of Nutrition 136, 15281532.Google Scholar