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In vitro schistosomicidal effects of aqueous and dichloromethane fractions from leaves and stems of Piper species and the isolation of an active amide from P. amalago L. (Piperaceae)

Published online by Cambridge University Press:  08 April 2013

V.S. Carrara
Affiliation:
Departamento de Farmácia, Universidade Estadual de Maringá, Maringá, PR, Brazil
S.C.H. Vieira
Affiliation:
Departamento de Farmácia, Universidade Estadual de Maringá, Maringá, PR, Brazil
R.G. de Paula
Affiliation:
Departamento de Bioquímica e Imunologia, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil
V. Rodrigues
Affiliation:
Departamento de Bioquímica e Imunologia, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil
L.G. Magalhães
Affiliation:
Núcleo de Pesquisas em Ciências Exatas e Tecnológicas, Universidade de Franca, Franca, SP, Brazil
D.A.G. Cortez
Affiliation:
Departamento de Farmácia, Universidade Estadual de Maringá, Maringá, PR, Brazil
A.A. Da Silva Filho*
Affiliation:
Departamento de Ciências Farmacêuticas, Faculdade de Farmácia, Universidade Federal de Juiz de Fora, Juiz de Fora, MG, Brazil

Abstract

Dichloromethane and aqueous fractions from leaves and stems of Piper arboreum Aubl., P. aduncum L., P. amalago L., P. crassinervium H.B. & K., P. diospyrifolium Kunth, P. hispidum Sw. and P. xylosteoides (Kunth) Steud. were tested against adult worms of Schistosoma mansoni. The in vitro activity was evaluated in terms of mortality, number of separated worms and number of worms with reduced motor activity. Most dichloromethane fractions from all Piper species showed moderate schistosomicidal activity, but aqueous fractions were not active. The dichloromethane fraction of P. amalago leaves (at 100 μg/ml) showed the highest activity, resulting in worm mortality, the separation of worm pairs and reduced motor activity. Chromatographic fractionation of the dichloromethane fraction of P. amalago leaves led to the isolation of its major compound, which was also tested against adults of S. mansoni. The isolated piperamide N-[7-(3′,4′-methylenedioxyphenyl)-2(Z),4(Z)-heptadienoyl] pyrrolidine, at 100 μm, resulted in the mortality of all adult worms after 24 h of incubation. The findings suggest that species of Piper are potential sources of schistosomicidal compounds.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2013 

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References

Agra, M.F., Silva, K.N., Basílio, I.J.L.D., França, P.F. & Barbosa-Filho, J.M. (2008) Survey of medicinal plants used in the region Northeast of Brazil. Brazilian Journal of Pharmacognosy 18, 472508.Google Scholar
Alécio, A.C., Bolzani, V.S., Young, M.C.M., Kato, M.J. & Furlan, M. (1998) Antifungal amide from leaves of Piper hispidum . Journal of Natural Products 61, 637639.Google Scholar
Atjanasuppat, K., Wongkham, W., Meepowpan, P., Kittakoop, P., Sobhon, P., Bartlett, A. & Whitfield, P.J. (2009) In vitro screening for anthelmintic and antitumour activity of ethnomedicinal plants from Thailand. Journal of Ethnopharmacology 123, 475482.CrossRefGoogle ScholarPubMed
Bodiwala, H.S., Singh, G., Singh, R., Dey, C.S., Sharma, S.S., Bhutani, K.K. & Singh, I.P. (2007) Antileishmanial amides and lignans from Piper cubeba and Piper retrofractum . Journal of Natural Medicines 61, 418421.CrossRefGoogle Scholar
Botros, S.S., William, S., Beadle, J.R., Valiaeva, N. & Hostetler, K.Y. (2009) Antischistosomal activity of hexadecyloxypropyl cyclic 9-(S)-[3-hydroxy-2-(phosphonomethoxy) propyl]adenine and other alkoxyalkyl esters of acyclic nucleoside phosphonates assessed by schistosome worm killing in vitro . Antimicrobial Agents and Chemotherapy 53, 52845287.Google Scholar
Caixeta, S.C., Magalhães, L.G., Melo, N.I., Wakabayashi, K.A.L., Aguiar, G.P., Aguiar, D.P., Mantovani, A.L.L., Morais, J.A., Oliveira, P.F., Tavares, D.C., Groppo, M., Rodrigues, V., Cunha, W.R., Veneziani, R.C.S., Da Silva Filho, A.A. & Crotti, A.E.M. (2011) Chemical composition and in vitro schistosomicidal activity of the essential oil of Plectranthus neochilus grown in Brazil Southeast. Chemistry and Biodiversity 8, 21492157.Google Scholar
Carrara, V.S., Serra, L.Z., Cardozo-Filho, L., Cunha-Júnior, E.F., Torres-Santos, E.C. & Cortez, D.A.G. (2012) HPLC analysis of supercritical carbon dioxide and compressed propane extracts from Piper amalago L. with antileishmanial activity. Molecules 17, 1533.Google Scholar
Estevez, Y., Castillo, D., Pisango, T., Arevalo, J., Rojas, R., Alban, J., Deharo, E., Bourdy, G. & Sauvain, M. (2007) Evaluation of the leishmanicidal activity of plants used by Peruvian Chayahuita ethnic group. Journal of Ethnopharmacology 114, 254259.Google Scholar
Heckel, É. (1897) Les plantes médicinales et toxiques de la Guyane Française. 93 pp. Mâcon, Protat Frères.Google Scholar
Lago, J.H.G., Ramos, C.S., Casanova, D.C.C., Morandim, A.A., Bergamo, D.C.B., Cavalheiro, A.J., Bolzani, V.S., Furlan, M., Guimarães, S.E.F., Young, M.C.M. & Kato, M.J. (2004) Benzoic acid derivatives from Piper species and their fungitoxic activity against Cladosporium cladosporoides and C. sphaerospermum . Journal of Natural Products 67, 17831788.Google Scholar
Magalhães, L.G., Machado, C.B., Morais, E.R., Moreira, E.B., Soares, C.S., Silva, S.H., Da Silva Filho, A.A. & Rodrigues, V. (2009) In vitro schistosomicidal activity of curcumin against Schistosoma mansoni adult worms. Parasitology Research 104, 11971201.CrossRefGoogle ScholarPubMed
Magalhães, L.G., Souza, J.M., Wakabayashi, K.A.L., Laurentiz, R.S., Vinhólis, A.H., Rezende, K.C.S., Simaro, G.V., Bastos, J.K., Rodrigues, V., Esperandim, V.R., Ferreira, D.S., Crotti, A.E.M., Cunha, W.R. & Silva, M.L.A. (2012) In vitro efficacy of the essential oil of Piper cubeba L. (Piperaceae) against Schistosoma mansoni . Parasitology Research 110, 17471754.Google Scholar
Melek, F.R., Tadros, M.M., Yousif, F., Selim, M.A. & Hassan, M.H. (2011) Screening of marine extracts for schistosomicidal activity in vitro. Isolation of the triterpene glycosides echinosides A and B with potential activity from the sea cucumbers Actinopyga echinites and Holothuria polii . Pharmaceutical Biology 50, 490496.CrossRefGoogle Scholar
Melo, N.I., Magalhães, L.G., Carvalho, C.E., Wakabayashi, K.A.L., Aguiar, G.P., Ramos, R.C., Mantovani, A.L.L., Turatti, I.C.C., Rodrigues, V., Groppo, M., Cunha, W.R., Veneziani, R.C.S. & Crotti, A.E.M. (2011) Schistomicidal activity of the essential oil of Ageratum conyzoides L. (Asteraceae) against adult Schistosoma mansoni worms. Molecules 16, 762773.Google Scholar
Moraes, J., Nascimento, C., Lopes, P.O.M.V., Nakano, E., Yamaguchi, L.F., Kato, M.J. & Kawano, T. (2011) Schistosoma mansoni: In vitro schistosomicidal activity of piplartine. Experimental Parasitology 127, 357364.Google Scholar
Moraes, J., Carvalho, A.A.L., Nakano, E., Almeida, A.A.C., Marques, T.H.C., Andrade, L.N., Freitas, R.M. & Sousa, D.P. (2013) Anthelmintic activity of carvacryl acetate against Schistosoma mansoni . Parasitology Research 112, 603610.Google Scholar
Parmar, V.S., Jain, S.C., Bisht, K.S., Jain, R., Taneja, P., Jha, A., Tyagi, O.D., Prasad, A.K., Wengel, J., Olsen, C.E. & Boll, P.M. (1997) Phytochemistry of the genus Piper . Phytochemistry 46, 597673.Google Scholar
Parreira, N.A., Magalhães, L.G., Morais, D.R., Caixeta, S.C., de Sousa, J.P.B., Bastos, J.K., Cunha, W.R., Silva, M.L.A., Nanayakkara, N.P.D., Rodrigues, V. & Da Silva Filho, A.A. (2010) Antiprotozoal, schistosomicidal, and antimicrobial activities of the essential oil from the leaves of Baccharis dracunculifolia . Chemistry and Biodiversity 7, 9931001.Google Scholar
Patent 0503951-7 (2008) Process to obtain synthetic and semi-synthetic lignan derivatives, their antiparasitic activities and corresponding pharmaceutical formulations, including the therapeutic method using said lignan for the treatment of parasitosis. United States Patent Application 20080194678.Google Scholar
Pereira, A.C., Magalhães, L.G., Gonçalves, U.O., Luz, P.P., Moraes, A.C., Rodrigues, V., Guedes, P.M., Da Silva Filho, A.A., Cunha, W.R., Da Silva Filho, A.A., Cunha, W.R., Bastos, J.K., Nanayakkara, N.P. & Silva, M.L.A. (2011) Schistosomicidal and trypanocidal structure–activity relationships for ( ± )-licarin A and its ( − ) and (+) enantiomers. Phytochemistry 72, 14241430.Google Scholar
Ramalhete, C., Magalhães, L.G., Rodrigues, V., Silva, M., Da Silva Filho, A.A. & Ferreira, M.J.U. (2012) In vitro schistosomicidal activity of Balsaminol F and Karavilagenin C. Planta Medica 78, 19121917.Google Scholar
Rapado, L.N., Nakano, E., Ohlweiler, F.P., Kato, M.J., Yamaguchi, L.F., Pereira, C.A.B. & Kawano, T. (2011) Molluscicidal and ovicidal activities of plant extracts of the Piperaceae on Biomphalaria glabrata (Say, 1818). Journal of Helminthology 85, 6672.Google Scholar
Regasini, L.O., Cotinguiba, F., Passerini, G.D., Bolzani, V.S., Cicarelli, R.M.B., Kato, M.J. & Furlan, M. (2009) Trypanocidal activity of Piper arboreum and Piper tuberculatum (Piperaceae). Brazilian Journal of Pharmacognosy 9, 199203.Google Scholar
Silva, D.R., Nakamura, C.V., Dias-Filho, B.P.D., Ueda-Nakamura, T. & Cortez, D.A.G. (2009) In vitro antileishmanial activity of hydroethanolic extract, fractions, and compounds isolated from leaves of Piper ovatum Vahl against Leishmania amazonensis . Acta Protozoologica 48, 7381.Google Scholar
Silva, M.L.A., Coimbra, H.S., Pereira, A.C., Almeida, V.A., Lima, T.C., Costa, E.S., Vinhólis, A.H.C., Royo, V.A., Silva, R., Da Silva Filho, A.A., Cunha, W.R., Furtado, N.A.J.C., Martins, C.H.G., Carvalho, J.C.T. & Bastos, J.K. (2007) Evaluation of Piper cubeba extract, ( − )-cubebin and its semi-synthetic derivatives against oral pathogens. Phytotherapy Research 21, 420422.Google Scholar
Souza, V.A., Silva, R., Pereira, A.C., Royo, V.A., Saraiva, J., Montanheiro, M., Souza, G.H.B., Da Silva Filho, A.A., Grando, M.D., Donate, P.M., Bastos, J.K., Albuquerque, S. & Silva, M.L.A. (2005) Trypanocidal activity of ( − )-cubebin derivatives against free amastigote forms of Trypanosoma cruzi . Bioorganic and Medicinal Chemistry Letters 15, 303307.Google Scholar
Steinmann, P., Keiser, J., Bos, R., Tanner, M. & Utzinger, J. (2006) Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. The Lancet Infectious Diseases 6, 411425.Google Scholar
Stelma, F.F., Talla, I., Sow, S., Kongs, A., Niang, M., Polman, K., Deelder, A.M. & Gryseels, B. (1995) Efficacy and side effects of praziquantel in an epidemic focus of Schistosoma mansoni . American Journal of Tropical Medicine and Hygiene 53, 167170.Google Scholar
Tang, G., Chen, D., Oiu, B., Sheng, L., Wang, Y., Hu, G., Zhao, F., Ma, L., Huang, W., Huang, O., Xu, J., Long, C. & Li, J. (2011) Cytotoxic amide alkaloids from Piper boehmeriaefolium . Journal of Natural Products 74, 4549.Google Scholar
Veras, L.M., Guimarães, M.A., Campelo, Y.D., Vieira, M.M., Nascimento, C., Lima, D.F., Vasconcelos, L., Nakano, E., Kuckelhaus, S.S., Batista, M.C., Leite, J.R. & Moraes, J. (2012) Activity of epiisopiloturine against Schistosoma mansoni . Current Medicinal Chemistry 19, 20512058.Google Scholar
WHO (2011) Schistosomiasis: number of people treated worldwide in 2009. Weekly Epidemiological Record 86, 7380.Google Scholar
Yousif, F., Wassel, G., Boulos, L., Labib, T., Mahmoud, K., El-Hallouty, S., El Bardicy, S., Mahmoud, S., Ramzy, F., Gohar, L., El-Manawaty, M., El Gendy, M.A., Fayad, W. & El-Menshawi, B. (2012) Contribution to in vitro screening of Egyptian plants for schistosomicidal activity. Pharmaceutical Biology 50, 732739.Google Scholar