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In vitro anti-trypanosomal activity of elatol isolated from red seaweed Laurencia dendroidea

  • P. VEIGA-SANTOS (a1), K. J. PELIZZARO-ROCHA (a2), A. O. SANTOS (a2), T. UEDA-NAKAMURA (a1) (a3), B. P. DIAS FILHO (a1) (a3), S. O. SILVA (a1) (a3), D. B. SUDATTI (a4), E. M. BIANCO (a5), R. C. PEREIRA (a4) and C. V. NAKAMURA (a1) (a3)...

Summary

Chagas' disease is a debilitating but comparatively neglected illness that affects about 15 million people. There is an urgent need to develop new, more effective, and less-toxic compounds. In this study, we assessed the in vitro anti-trypanosomal activity of the sesquiterpene elatol from the Brazilian red seaweed Laurencia dendroidea. We used electron microscopy to evaluate the effect of elatol on the morphology and ultrastructure of the parasite. Elatol showed a dose-dependent effect against the epimastigote, trypomastigote, and amastigote forms, with IC50 values of 45·4, 1·38, and 1·01 μm, respectively. Observation of treated intracellular amastigotes by light microscopy demonstrated a total elimination of the infection at a dose of 3·0 μm. In addition, the compound did not affect the red blood cells, and the CC50 value for LLCMK2 cells was 27·0 μm. Transmission and scanning electron micrographs showed aberrant-shaped cells and breaks in the plasma membrane, prominent swollen mitochondria, and extensive formation of cytoplasmic vacuoles in all the forms. This is the first report of the anti-trypanosomal effect of the sesquiterpene elatol.

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Corresponding author

*Corresponding author: Programa de Pós-graduação em Ciências Farmacêuticas, Laboratório de Inovação Tecnológica no Desenvolvimento de Fármacos e Cosméticos, Bloco B-08, Universidade Estadual de Maringá, Av. Colombo 5790, CEP 87020-900, Maringá, Paraná, Brazil. Tel: +55 44 3041 5012. Fax: +55 44 3261 4860. E-mail: cvnakamura@uem.br

References

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Bansemira, A., Justa, N., Michalikb, M., Lindequista, U. and Lalk, M. (2004). Extracts and sesquiterpene derivatives from the red alga Laurencia chondrioides with antibacterial activity against fish and human pathogenic bacteria. Chemistry and Biodiversity 1, 463467.
Brener, Z. (1962). Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi. Revista do Instituto de Medicina tropical de São Paulo 4, 389396.
Camargo, E. P. (1964). Growth and differentiation in Trypanosoma cruzi. Origen of metacyclic trypanosomes in liquid media. Revista do Instituto de Medicina tropical de São Paulo 6, 93–100.
Cassano, V. (2009). Taxonomia e filogenia do complexo Laurencia (Ceramiales, Rhodophyta), com ênfase no estado do Rio de Janeiro, Brasil. Ph.D. thesis. Instituto de Botânica da Secretaria de Estado do Meio Ambiente, São Paulo.
Coura, J. R. and Castro, S. L. (2002). A critical review on Chagas disease chemotherapy. Memórias do Instituto Oswaldo Cruz 97, 3–24.
Da Gama, B. A. P., Pereira, R. C., Soares, A. R., Teixeira, V. L. and Yoneshigue-Valentin, Y. (2003). Is the mussel test a good indicator of antifouling activity? A comparison between laboratory and field assays. Biofouling 19, 161169.
Dantas, A. P., Salomão, K., Barbosa, H. S. and Castro, S. L. (2006). The effect of Bulgarian propolis against Trypanosoma cruzi and during its interaction with host cells. Memórias do Instituto Oswaldo Cruz 101, 207211.
de Nys, R., Leya, T., Maximilien, R., Afsar, A., Nair, P. S. R. and Steinberg, P. D. (1996). The need of standardised broad scale biossay testing: a case study using the red algae Laurencia rigida. Biofouling 10, 213224.
Freile-Pelegrin, Y., Robledo, D., Chan-Bacab, M. J. and Ortega-Morales, B. O. (2008). Antileishmanial properties of tropical marine algae extracts. Fitoterapia 79, 374377. doi: 10.1016/j.fitote.2008.02.006.
Hay, M. E., Fenical, W. and Gustafson, K. (1987). Chemical-defense against diverse coral-reef herbivores. Ecology 68, 15811591.
Hay, M. E., Duffy, J. E. and Fenical, W. (1988). Seaweed chemical defenses: among-compound and among-herbivore variance. Proceedings of the 6th International Coral Reef Symposium 3, 4348.
Iliopoulou, D., Roussis, V., Pannecouque, C., De Clercq, E. and Vagias, C. (2002). Halogenated sesquiterpenes from the red alga Laurencia obtusa. Tetrahedron 58, 67496755. doi: 10.1016/S0040-4020(02)00687-7.
Izumi, E., Morello, L. G., Ueda-Nakamura, T., Yamada-Ogatta, S. F.; Dias-Filho, B. P., Cortez, D. A. G., Ferreira, I. C. P., Morgado-Días, J. A. and Nakamura, C. V. (2008). Trypanosoma cruzi: antiprotozoal activity of parthenolide obtained from Tanacetum parthenium (L.) Schultz Bip. (Asteraceae, Compositae) against epimastigote and amastigote forms. Experimental Parasitology 118, 324330. doi:10.1016/j.exppara.2007.08.015.
Kang, J. Y., Khan, M. N. A., Park, N. H., Cho, J. Y., Lee, M. C., Fujii, H. and Hong, Y. K. (2008). Antipyretic, analgesic, and anti-inflammatory activities of the seaweed Sargassum fulvellum and Sargassum thunbergii in mice. Journal of Ethnopharmacology 116, 187190. doi: 10.1016/j.jep.2007.10.032.
Kladi, M., Vagias, C., Stavri, M., Rahman, M. M., Gibbons, S. and Roussis, V. (2008). C15 acetogenins with antistaphylococcal activity from the red alga Laurencia glandulifera. Phytochemistry Letters 1, 3136. doi: 10.1016/j.phytol.2007.12.004.
König, G. M. and Wright, A. D. (1997). Sesquiterpene content of the antibacterial dichlormethane extract of the red alga Laurencia obtusa. Planta Medica 63, 186187. doi: 10.1055/S-2006-957643.
Luize, P. S., Tiuman, T. S., Morello, L. G., Maza, P. K., Ueda-Nakamura, T., Dias-Filho, B. P., Cortez, D. A. G., Mello, J. C. P. and Nakamura, C. V. (2005). Effects of medicinal plant extracts on growth of Leishmania (L.) amazonensis and Trypanosoma cruzi. Brazilian Journal of Pharmaceutical Sciences 41, 8594.
Luize, P. S., Ueda-Nakamura, T., Dias-Filho, B. P., Cortez, D. A. G. and Nakamura, C. V. (2006). Activity of neolignans isolated from Piper regnellii (MIQ.) C. DC. var. pallescens (C. DC.) YUNCK against Trypanosoma cruzi. Biological Pharmaceutical Bulletin 29, 21262130.
Matsuhiro, B., Conte, A. F., Damonte, E. B., Kolender, A. A., Matulewicz, M. C., Mejías, E. G., Pujol, C. A. and Zúñiga, E. A. (2005). Structural analysis and antiviral activity of a sulfated galactan from the red seaweed Schizymenia binderi (Gigartinales, Rhodophyta). Carbohydrate Research 340, 23922402. doi:10.1016/j.carres.2005.08.004.
Mayer, A. M. S., Rodríguez, A. D., Berlinck, R. G. S. and Hamann, M. T. (2009). Marine pharmacology in 2005–6: Marine compounds with anthelmintic, antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems, and other miscellaneous mechanisms of action. Biochimica et Biophysica Acta 1790, 283308. doi: 10.1016/j.bbagen.2009.03.011.
Mendiola-Martínez, J., Hernández, H., Acuña, D., Esquivel, M., Scull, , Lizama, R. and Abreu-Payrol, J. (2005). Inhibiting activity of the in vitro growth of Plasmodium falciparum of extracts from algae of genus Laurencia. Revista Cubana de Medicina Tropical 57, 192195.
Menezes, D., Valentim, C., Oliveira, M. F. and Vannier-Santos, M. A. (2006). Putrescine analogue cytotoxicity against Trypanosoma cruzi. Parasitology Research 98, 99–105. doi: 10.1007/S00436-005-0010-1.
Menna-Barreto, R. F. S., Corrêa, J. R., Pinto, A. V., Soares, M. J. and Castro, S. L. (2007). Mitochondrial disruption and DNA fragmentation in Trypanosoma cruzi induced by naphthoimidazoles synthesized from β-lapachone. Parasitology Research 101, 895905. doi: 10.1007/s00436-007-0556-1.
Menna-Barreto, R. F. S., Gonçalves, R. S. L., Costa, E. M., Silva, R. S. F., Pinto, A. V., Oliveira, M. F. and de Castro, S. L. (2009). The activity on Trypanosoma cruzi of novel synthetic naphthoquinones is mediated by mitochondrial dysfunction. Free Radical Biology and Medicine 47, 644653. doi: 10.1016/j.freeradbiomed.2009.06.004.
Moo-Puc, R., Robledo, D. and Freile-Pelegrin, Y. (2008). Evaluation of selected tropical seaweeds for in vitro anti-trichomonal activity. Journal of Ethnopharmacology 120, 9297. doi: 10.1016/j.jep.2008.07.035.
Moreira, D. R. M., Leite, A. C. L., Santos, R. R. and Soares, M. B. P. (2009). Approaches for the development of new anti-Trypanosoma cruzi agents. Current Drug Targets 10, 212231.
Nara, T., Kamei, Y., Akiko, T., Annoura, T., Hirota, K., Iizumi, K., Dohmoto, Y., Ono, T. and Aoki, T. (2005). Inhibitory action of marine algae extracts on the Trypanosoma cruzi dihydroorotate dehydrogenase activity and on the protozoan growth in mammalian cells. Parasitology International 54, 5964. doi: 10.1016/j.parint.2004.11.001.
Orhan, I., Sener, B., Atici, T., Brun, R., Perozzo, R. and Tasdemir, D., (2006). Turkish freshwater and marine macrophyte extracts show in vitro anti-protozoal activity and inhibit FabI, a key enzyme of Plasmodium falciparum fatty acid biosynthesis. Phytomedicine 13, 388393. doi: 10.1016/j.phymed.2005.10.010.
Prata, A. (2001). Clinical and epidemiological aspects of Chagas disease. The Lancet Infectious Diseases 1, 91–100. doi: 10.1016/S1473-3099(01)00065-2.
Salas, C. A., Tapia, R. A., Ciudad, K., Armstrong, V., Orellana, M., Kemmerling, U., Ferreira, J., Maya, J. D. and Morello, A. (2008). Trypanosoma cruzi: Activities of lapachol and a- and b-lapachone derivatives against epimastigote and trypomastigote forms. Bioorganic & Medicinal Chemistry 16, 668674. doi:10.1016/j.bmc.2007.10.038.
Salgado, L. T., Viana, N. B., Andrade, L. R., Leal, R. N., Gama, B. A. P., Attias, M., Pereira, R. C. and Amado Filho, G. M. (2008). Intra-cellular storage, transport and exocytosis of halogenated compounds in marine red alga Laurencia obtusa. Journal of Structural Biology 162, 345355. doi: 10.1016/j.jsb.2008.01.015.
Schaeffer, D. J. and Krylov, V. S. (2000). Anti-HIV activity of extracts and compounds from algae and cyanobacteria. Ecotoxicology and Environmental Safety 45, 208227. doi: 10.1006/eesa.1999.1862.
Schmunis, G. A. (2007). Epidemiology of Chagas disease in non-endemic countries: the role of international migration. Memórias do Instituto Oswaldo Cruz 102, 7585.
Sims, J. J., Lin, G. H. Y. and Wing, R. M. (1974). Marine natural products: elatol, a halogenated sesquiterpene alcohol from the red alga Laurencia elata. Tetrahedron Letters 39, 34873490.
Steinberg, P. D., De Ny, R. and Kjelleberg, S. (1998). Chemical inhibition of epibiota by Australian seaweeds. Biofouling 12, 227244.
Sudatti, D. B., Rodrigues, S. V., Coutinho, R., Gama, B. A. P., Salgado, L. T., Amado Filho, G. M. and Pereira, R. C. (2008). Transport and defensive role of elatol at the surface of the red seaweed Laurencia obtusa (CERAMIALES, RHODOPHYTA). Journal of Phycology 44, 584591. doi: 10.1111/j.1529-8817.2008.00507.X.
Tonin, T. D., Barbosa, V. A., Bocca, C. C., Ramos, E. R. F., Nakamura, C. V., Costa, W. F., Basso, E. A., Ueda-Nakamura, T. and Sarragiotto, M. H. (2009). Comparative study of the trypanocidal activity of the methyl 1-nitrophenyl-1,2,3,4-9H-tetrahydro-β-carboline-3-carboxylate derivatives and benznidazole using theoretical calculations and cyclic voltammetry. European Journal of Medicinal Chemistry 44, 17451750. doi:10.1016/j.ejmech.2008.03.044.
Topcu, G., Anydoqmus, Z., Imre, S., Goren, A. C., Pezzuto, J. M., Clement, J. A. and Kingston, D. G. (2003). Brominated sesquiterpenes from the red alga Laurencia obtusa. Journal of Natural Products 66, 15051508.
Urbina, J. A. and Docampo, R. (2003). Specific chemotherapy of Chagas disease: controversies and advances. TRENDS in Parasitology 19, 495501. doi:10.1016/j.pt.2003.09.001.
Urbina, J. A. (2009). Ergosterol biosynthesis and drug development for Chagas disease. Memórias do Instituto Oswaldo Cruz 104, 311318.
Vairappan, C. S., Suzuki, M., Abe, T. and Masuda, M. (2001). Antibacterial halogenated metabolites from the Malaysian Laurencia species. Phytochemistry 58, 291297.doi: S0031-9422(01)00260-6.
Vairappan, C. S. (2003). Potent antibacterial activity of halogenated metabolites from Malaysian red algae, Laurencia majuscule (Rhodomelaceae, Ceramiales). Biomolecular Engineering 20, 255259. doi:10.1016/S1389-0344(03)00067-4.
Valdez, R. H., Tonin, L. T. D., Ueda-Nakamura, T., Dias-Filho, B. P. D., Morgado-Díaz, J. A., Sarragiotto, M. H. and Nakamura, C. V. (2009). Biological activity of 1,2,3,4-tetrahydro-β-carboline-3-carboxamides against Trypanosoma cruzi. Acta Tropica 110, 7–14. doi: 10.1016/j.actatropica.2008.11.008.
Van-Hellemond, J. J., Opperdoes, F. R. and Tielens, A. G. (2005). The extraordinary mitochondrion and unusual citric acid cycle in Trypanosoma brucei. Biochemical Society Transactions 33, 967971.
Wang, B., Zhang, W., Duan, X. and Li, X. (2009). In vitro antioxidative activities of extract and semi-purified fractions of the marine red alga, Rhodomela confervoides (Rhodomelaceae). Food Chemistry 113, 11011105. doi: 10.1016/j.foodchem.2008.08.078.
WHO/TDR – World Health Organization (2006). Report of the Scientific Working Group on Chagas disease, Buenos Aires, Argentina, p. 7.
Wright, A. D., König, G. M., Angerhofer, C. K., Greenidge, P., Linden, A. and Desqueyroux-Faundez, R. (1996). Anti-malarial activity: the search for marine-derived natural products with selective anti-malarial activity. Journal of Natural Products 59, 710716.

Keywords

In vitro anti-trypanosomal activity of elatol isolated from red seaweed Laurencia dendroidea

  • P. VEIGA-SANTOS (a1), K. J. PELIZZARO-ROCHA (a2), A. O. SANTOS (a2), T. UEDA-NAKAMURA (a1) (a3), B. P. DIAS FILHO (a1) (a3), S. O. SILVA (a1) (a3), D. B. SUDATTI (a4), E. M. BIANCO (a5), R. C. PEREIRA (a4) and C. V. NAKAMURA (a1) (a3)...

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