In Vitro Antischistosomal Activity of the Argemone mexicana Methanolic Extract and Its Main Component Berberine
-
Joel Horacio ELIZONDO-LUÉVANO
,
Rocío CASTRO-RÍOS
,
Belén VICENTE
,
Pedro FERNÁNDEZ-SOTO
,
Julio LÓPEZ-ABAN
,
Antonio MURO
,
Abelardo CHÁVEZ-MONTES
Abstract
Background: Schistosomiasis has been identified as a major public health problem in tropical countries. The present study aimed to investigate the schistosomicidal effects of the methanolic extract of Argemone mexicana L. and its active component, berberine against Schistosoma mansoni on in-vitro experiments.
Methods: S. mansoni adults were used. Various concentrations of the methanolic extract (10 - 200 µg/ml) and berberine (2.5 - 50 µM) were tested from 24 to 72 h. The viability of S. mansoni was confirmed with an invertoscope-microscope. Furthermore, cytotoxic (Hemolysis test), and antioxidant (DPPH radical scavenging assay) capacities were determined.
Results: The viability tests on S. mansoni showed that A. mexicana at 50 μg/mL is lethal at 48 h and berberine at 10 μM is lethal at 24 h. The hemolytic activity at 1,000 μg/mL was 2.9% for A. mexicana and 90.2% for berberine. The antioxidant capacities shown by A. mexicana and berberine, were EC50 156.3 and 84.1 μg/mL, respectively.
Conclusion: The extract of A. mexicana and berberine demonstrated high antischistosomal activities in low concentration and short exposure time on the in-vitro model.
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2. Enk MJ, Lima ACL, Drummond SC, et al. The effect of the number of stool samples on the ob-served prevalence and the infection intensity with Schistosoma mansoni among a population in an area of low transmission. Acta Trop. 2008;108(2-3):222-28.
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4. Magalhães LG, Machado CB, Morais ER, et al. In vitro schistosomicidal activity of curcumin against Schistosoma mansoni adult worms. Parasitol Res. 2009;104(5):1197-201.
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6. Harvey A. Strategies for discovering drugs from previously unexplored natural products. Drug Dis-cov Today. 2000;5(7):294-300.
7. Brahmachari G, Gorai D, Roy R. Argemone mexicana: chemical and pharmacological aspects. Rev Bras Farmacogn. 2013;23(3):559-75.
8. Malebo HM, Wenzler T, Cal M, et al. Anti-protozoal activity of aporphine and protoberberine alkaloids from Annickia kummeriae (Engl. & Diels) Setten & Maas (Annonaceae). BMC Complement Altern Med. 2013;13:48.
9. Chang F-R, Khalil AT, Wu Y-C, et al. Cytotoxic Benzophenanthridine and Benzylisoquinoline Alka-loids from Argemone mexicana. Z Naturforsch C J Biosci. 2003;58(7-8):521-6.
10. Mahmoudv H, Sharififar F, Sharifi I, et al. In vitro inhibitory effect of Berberis vulgaris (Berberidaceae) and its main component, Berberine against different leishmania species. Iran J Parasitol. 2014;9(1):28-36.
11. Birdsall T, GS K. Berberine: Therapeutic potential of an alkaloid found in several medicinal plants. Alt Med Rev. 1997;2(2):94-103.
12. Singh B, Srivastava JS, Khosa RL, et al. Individual and combined effects of berberine and santonin on spore germination of some fungi. Folia Microbiol (Praha). 2001;46(2):137-42.
13. Dkhil MA, Moneim AEA, Al-Quraishy S. Berber-ine protects against Schistosoma mansoni-induced oxi-dative damage in renal and testicular tissues of mice. Pak J Zool. 2014;46(3):763-71.
14. Yepes E, Varela-M RE, López-Abán J, et al. Inhibi-tion of granulomatous inflammation and prophylac-tic treatment of schistosomiasis with a combination of edelfosine and Praziquantel. PLoS Negl Trop Dis. 2015;9(7):e0003893.
15. Elizondo-Luevano JH, Verde-Star J, González-Horta A, et al. In Vitro Effect of Methanolic Ex-tract of Argemone mexicana against Trichomonas vaginalis. Korean J Parasitol. 2020;58(2):135-45.
16. Yepes E, Varela-M RE, López-Abán J, et al. In vitro and in vivo anti-schistosomal activity of the al-kylphospholipid analog edelfosine. PLoS One. 2014;9(10):e109431.
17. Eraky MA, Aly NS, Selem RF, et al. In vitro schis-tosomicidal activity of phytol and tegumental altera-tions induced in juvenile and adult stages of Schisto-soma haematobium. Korean J Parasitol. 2016;54(4):477-84.
18. Lakshmi G, Smitha N, Ammu S V, et al. Phyto-chemical profile, in vitro antioxidant and hemolytic activities of various leaf extract of Nymphaea Nouchali Linn: An in vitro study. Int J Pharm Pharm Sci. 2014;6(6):548-52.
19. Ledy G, Catalina L, Azucena O. Free radical scav-enging and cytotoxic activity of five commercial standardized extracts (red wine, green tea, pine bark, polygonum and pomegranate). Afr J Biotechnol. 2012;11(102):16725-30
20. Panic G, Duthaler U, Speich B, et al. Repurposing drugs for the treatment and control of helminth in-fections. Int J Parasitol Drugs Drug Resist. 2014;4(3):185-200.
21. Mølgaard P, Nielsen SB, Rasmussen DE, et al. Anthelmintic screening of Zimbabwean plants tra-ditionally used against schistosomiasis. J Eth-nopharmacol. 2001;74(3):257-64.
22. Keiser J, Chollet J, Xiao SH, et al. Mefloquine - An aminoalcohol with promising antischistosomal properties in mice. PLoS Negl Trop Dis. 2009;3(1):e350.
23. Elizondo-Luévano JH, Castro-Ríos R, Sánchez-García E, et al. In Vitro Study of Antiamoebic Ac-tivity of Methanol Extracts of Argemone mexicana on Trophozoites of Entamoeba histolytica HM1-IMSS. Can J Infect Dis Med Microbiol. 2018;2018:7453787.
24. Mahmoudvand H, Shakibaie M, Tavakoli R, et al. In vitro study of leishmanicidal activity of biogenic se-lenium nanoparticles against Iranian isolate of sensi-tive and glucantime- resistant Leishmania tropica. Iran J Parasitol. 2014;9(4):452-60.
25. Mahmoudvand H, Saedi Dezaki E, Sharififar F, et al. Protoscolecidal effect of Berberis vulgaris root ex-tract and its main compound, berberine in cystic echinococcosis. Iran J Parasitol. 2014;9(4):503-10.
26. Wright CW, Marshall SJ, Russell PF, et al. In vitro antiplasmodial, antiamoebic, and cytotoxic activities of some monomeric isoquinoline alkaloids. J Nat Prod. 2000;63(12):1638-40.
27. Grycová L, Dostál J, Marek R. Quaternary proto-berberine alkaloids. Phytochemistry. 2007;68(2):150-75.
28. Raghav D, Ashraf SM, Mohan L, et al. Berberine Induces Toxicity in HeLa Cells through Perturba-tion of Microtubule Polymerization by Binding to Tubulin at a Unique Site. Biochemistry. 2017;56(20):2594-611.
29. Doenhoff MJ, Cioli D, Utzinger J. Praziquantel: mechanisms of action, resistance and new deriva-tives for schistosomiasis. Curr Opin Infect Dis. 2008;21(6):659-67.
30. Hoffmann KF, Strand M. Molecular identification of a Schistosoma mansoni tegumental protein with simi-larity to cytoplasmic dynein light chains. J Biol Chem. 1996;271(42):26117-23.
31. Shuhua X, Binggui S, Utzinger J, et al. Ultrastruc-tural alterations in adult Schistosoma mansoni caused by artemether. Mem Inst Oswaldo Cruz. 2002;97(5):717-24.
32. Karimi G, Aghasizadeh M, Razavi M, et al. Protec-tive effects of aqueous and ethanolic extracts of Ni-gella sativa L. and Portulaca oleracea L. on free radical induced hemolysis of RBCs. Daru. 2011;19(4):295-300.
33. Fatehi M, Saleh TM, Fatehi-Hassanabad Z, et al. A pharmacological study on Berberis vulgaris fruit extract. J Ethnopharmacol. 2005; 102(1):46-52.
34. Hernández-Rodríguez P, Pabón Baquero LC, Ro-dríguez Álvarez MF. Propiedades químicas y bioló-gicas de Arbutus unedo: una planta con potencial me-dicinal. Rev Cuba de Farm. 2015;49(1):144-55.
35. Gouveia MJ, Brindley PJ, Rinaldi G, et al. Combina-tion Anthelmintic/Antioxidant Activity against Schis-tosoma mansoni. Biomolecules. 2019;9(2):54.
36. Sun LL, Gao W, Zhang MM, et al. Composition and Antioxidant Activity of the Anthocyanins of the Fruit of Berberis heteropoda Schrenk. Molecules. 2014;19(11):19078-96.
2. Enk MJ, Lima ACL, Drummond SC, et al. The effect of the number of stool samples on the ob-served prevalence and the infection intensity with Schistosoma mansoni among a population in an area of low transmission. Acta Trop. 2008;108(2-3):222-28.
3. Cederberg S, Sikasunge CS, Andersson A, et al. Short communication: In vitro efficacy testing of praziquantel, ivermectin, and oxfendazole against Taenia solium cysts. J Parasitol Res. 2012;2012:363276.
4. Magalhães LG, Machado CB, Morais ER, et al. In vitro schistosomicidal activity of curcumin against Schistosoma mansoni adult worms. Parasitol Res. 2009;104(5):1197-201.
5. de Oliveira RN, Rehder VLG, Santos Oliveira AS, et al. Schistosoma mansoni: In vitro schistosomicidal ac-tivity of essential oil of Baccharis trimera (less) DC. Exp Parasitol. 2012;132(2):135-43.
6. Harvey A. Strategies for discovering drugs from previously unexplored natural products. Drug Dis-cov Today. 2000;5(7):294-300.
7. Brahmachari G, Gorai D, Roy R. Argemone mexicana: chemical and pharmacological aspects. Rev Bras Farmacogn. 2013;23(3):559-75.
8. Malebo HM, Wenzler T, Cal M, et al. Anti-protozoal activity of aporphine and protoberberine alkaloids from Annickia kummeriae (Engl. & Diels) Setten & Maas (Annonaceae). BMC Complement Altern Med. 2013;13:48.
9. Chang F-R, Khalil AT, Wu Y-C, et al. Cytotoxic Benzophenanthridine and Benzylisoquinoline Alka-loids from Argemone mexicana. Z Naturforsch C J Biosci. 2003;58(7-8):521-6.
10. Mahmoudv H, Sharififar F, Sharifi I, et al. In vitro inhibitory effect of Berberis vulgaris (Berberidaceae) and its main component, Berberine against different leishmania species. Iran J Parasitol. 2014;9(1):28-36.
11. Birdsall T, GS K. Berberine: Therapeutic potential of an alkaloid found in several medicinal plants. Alt Med Rev. 1997;2(2):94-103.
12. Singh B, Srivastava JS, Khosa RL, et al. Individual and combined effects of berberine and santonin on spore germination of some fungi. Folia Microbiol (Praha). 2001;46(2):137-42.
13. Dkhil MA, Moneim AEA, Al-Quraishy S. Berber-ine protects against Schistosoma mansoni-induced oxi-dative damage in renal and testicular tissues of mice. Pak J Zool. 2014;46(3):763-71.
14. Yepes E, Varela-M RE, López-Abán J, et al. Inhibi-tion of granulomatous inflammation and prophylac-tic treatment of schistosomiasis with a combination of edelfosine and Praziquantel. PLoS Negl Trop Dis. 2015;9(7):e0003893.
15. Elizondo-Luevano JH, Verde-Star J, González-Horta A, et al. In Vitro Effect of Methanolic Ex-tract of Argemone mexicana against Trichomonas vaginalis. Korean J Parasitol. 2020;58(2):135-45.
16. Yepes E, Varela-M RE, López-Abán J, et al. In vitro and in vivo anti-schistosomal activity of the al-kylphospholipid analog edelfosine. PLoS One. 2014;9(10):e109431.
17. Eraky MA, Aly NS, Selem RF, et al. In vitro schis-tosomicidal activity of phytol and tegumental altera-tions induced in juvenile and adult stages of Schisto-soma haematobium. Korean J Parasitol. 2016;54(4):477-84.
18. Lakshmi G, Smitha N, Ammu S V, et al. Phyto-chemical profile, in vitro antioxidant and hemolytic activities of various leaf extract of Nymphaea Nouchali Linn: An in vitro study. Int J Pharm Pharm Sci. 2014;6(6):548-52.
19. Ledy G, Catalina L, Azucena O. Free radical scav-enging and cytotoxic activity of five commercial standardized extracts (red wine, green tea, pine bark, polygonum and pomegranate). Afr J Biotechnol. 2012;11(102):16725-30
20. Panic G, Duthaler U, Speich B, et al. Repurposing drugs for the treatment and control of helminth in-fections. Int J Parasitol Drugs Drug Resist. 2014;4(3):185-200.
21. Mølgaard P, Nielsen SB, Rasmussen DE, et al. Anthelmintic screening of Zimbabwean plants tra-ditionally used against schistosomiasis. J Eth-nopharmacol. 2001;74(3):257-64.
22. Keiser J, Chollet J, Xiao SH, et al. Mefloquine - An aminoalcohol with promising antischistosomal properties in mice. PLoS Negl Trop Dis. 2009;3(1):e350.
23. Elizondo-Luévano JH, Castro-Ríos R, Sánchez-García E, et al. In Vitro Study of Antiamoebic Ac-tivity of Methanol Extracts of Argemone mexicana on Trophozoites of Entamoeba histolytica HM1-IMSS. Can J Infect Dis Med Microbiol. 2018;2018:7453787.
24. Mahmoudvand H, Shakibaie M, Tavakoli R, et al. In vitro study of leishmanicidal activity of biogenic se-lenium nanoparticles against Iranian isolate of sensi-tive and glucantime- resistant Leishmania tropica. Iran J Parasitol. 2014;9(4):452-60.
25. Mahmoudvand H, Saedi Dezaki E, Sharififar F, et al. Protoscolecidal effect of Berberis vulgaris root ex-tract and its main compound, berberine in cystic echinococcosis. Iran J Parasitol. 2014;9(4):503-10.
26. Wright CW, Marshall SJ, Russell PF, et al. In vitro antiplasmodial, antiamoebic, and cytotoxic activities of some monomeric isoquinoline alkaloids. J Nat Prod. 2000;63(12):1638-40.
27. Grycová L, Dostál J, Marek R. Quaternary proto-berberine alkaloids. Phytochemistry. 2007;68(2):150-75.
28. Raghav D, Ashraf SM, Mohan L, et al. Berberine Induces Toxicity in HeLa Cells through Perturba-tion of Microtubule Polymerization by Binding to Tubulin at a Unique Site. Biochemistry. 2017;56(20):2594-611.
29. Doenhoff MJ, Cioli D, Utzinger J. Praziquantel: mechanisms of action, resistance and new deriva-tives for schistosomiasis. Curr Opin Infect Dis. 2008;21(6):659-67.
30. Hoffmann KF, Strand M. Molecular identification of a Schistosoma mansoni tegumental protein with simi-larity to cytoplasmic dynein light chains. J Biol Chem. 1996;271(42):26117-23.
31. Shuhua X, Binggui S, Utzinger J, et al. Ultrastruc-tural alterations in adult Schistosoma mansoni caused by artemether. Mem Inst Oswaldo Cruz. 2002;97(5):717-24.
32. Karimi G, Aghasizadeh M, Razavi M, et al. Protec-tive effects of aqueous and ethanolic extracts of Ni-gella sativa L. and Portulaca oleracea L. on free radical induced hemolysis of RBCs. Daru. 2011;19(4):295-300.
33. Fatehi M, Saleh TM, Fatehi-Hassanabad Z, et al. A pharmacological study on Berberis vulgaris fruit extract. J Ethnopharmacol. 2005; 102(1):46-52.
34. Hernández-Rodríguez P, Pabón Baquero LC, Ro-dríguez Álvarez MF. Propiedades químicas y bioló-gicas de Arbutus unedo: una planta con potencial me-dicinal. Rev Cuba de Farm. 2015;49(1):144-55.
35. Gouveia MJ, Brindley PJ, Rinaldi G, et al. Combina-tion Anthelmintic/Antioxidant Activity against Schis-tosoma mansoni. Biomolecules. 2019;9(2):54.
36. Sun LL, Gao W, Zhang MM, et al. Composition and Antioxidant Activity of the Anthocyanins of the Fruit of Berberis heteropoda Schrenk. Molecules. 2014;19(11):19078-96.
| Files | ||
| Issue | Vol 16 No 1 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v16i1.5518 | |
| Keywords | ||
| Anthelmintics Medicinal plants Papaveraceae Schistosoma mansoni | ||
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How to Cite
1.
ELIZONDO-LUÉVANO J, CASTRO-RÍOS R, VICENTE B, FERNÁNDEZ-SOTO P, LÓPEZ-ABAN J, MURO A, CHÁVEZ-MONTES A. In Vitro Antischistosomal Activity of the Argemone mexicana Methanolic Extract and Its Main Component Berberine. Iran J Parasitol. 2021;16(1):91-100.
