Anti-Acanthamoeba castellanii activity of alkaloid-enriched extracts and lycorine from the Amaryllidaceae species

Authors

  • Maressa Dietrich Rosa Department of Pathology, Health Sciences Center, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil
  • Jean Paulo de Andrade Department of Chemistry, Laboratory of Natural Products, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil
  • Adriana Oliveira Costa Faculty of Pharmacy, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
  • Raphael Conti Department of Chemistry, Laboratory of Natural Products, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil
  • Jaume Bastida Department of Biology, Healthcare and Environment, Group of Natural Products and Food Science, Faculty of Pharmacy, University of Barcelona, Barcelona, Spain
  • Warley de Souza Borges Department of Chemistry, Laboratory of Natural Products, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil
  • Cinthia Furst Department of Pathology, Health Sciences Center, Federal University of Espírito Santo, Vitória, Espírito Santo, Brazil https://orcid.org/0000-0001-9041-2401

DOI:

https://doi.org/10.1590/s2175-97902022e20459

Keywords:

Acanthamoeba castellanii, Cytotoxicity, MDCK cell, MTT, Amaryllidaceae alkaloids, Natural products

Abstract

Free-living amoebae of the genus Acanthamoeba are the causative agents of granulomatous encephalitis and keratitis, severe human infections. Bioactive compounds from plants are recognized as an alternative source for the development of new drugs. The Amaryllidaceae is a botanical family able to synthesize a very specific and consistent group of biologically active isoquinoline-like alkaloids. The alkaloidal fractions from the Brazilian species Hippeastrum canastrense, H. diniz-cruziae, H. puniceum, and Crinum x amabile, along with the alkaloid lycorine, were investigated against Acanthamoeba castellanii. The in vitro assays were performed with distinct concentrations of lycorine and alkaloidal fractions, while the cell viability was evaluated by the MTT method upon MDCK cells. Chlorhexidine 0.02% was used as the positive control. The effect of alkaloid fractions was concentration dependent, and 2000 μg mL-1 of H. canastrense and H. diniz-cruziae provided a 100% inhibition. At concentrations of 250, 500, and 1000 μg mL-1, the H. diniz-cruziae alkaloidal fraction showed the lowest cytotoxic effect (5%-7%) and remarkable anti-amoebic activity, demonstrating values of IC50 285.61 μg mL-1, low cytotoxicity (5%-7%), and selectivity index (7.0). Taken together, the results are indicative of the great potential that the alkaloids from H. diniz-cruziae have as new candidates for anti-amoebicidal compounds.

Downloads

Download data is not yet available.

References

Alvarenga LS, Freitas D, Hofling-Lima AL. Acanthamoeba keratitis. Braz Arch Ophthalmol. 2000;63(2):155-159. http://dx.doi.org/10.1590/S0004-27492000000200013

» https://doi.org/http://dx.doi.org/10.1590/S0004-27492000000200013

Amoros M, Simões CMO, Girre L. Synergistic effect of flavones and flavonols agains herpes simplex virus type 1 in cell culture. Comparison with the antiviral activity of propolis. J Nat Prod. 1992;55(12):1732-40.

Badria FA, Hetta MH, Sarhan RM, El-Din MHE. Lethal effects of Helianthemum lippii (L.) on Acanthamoeba castellanii cysts in vitro. Korean J Parasitol. 2014;52(3):243-249. http://doi.org/10.3347/kjp.2014.52.3.243

» https://doi.org/http://doi.org/10.3347/kjp.2014.52.3.243

Badisa RB, Darling-Reed SF, Joseph P, Cooperwood JF, Latinwo LM, Goodman CB. Selective cytotoxic activities of two novel synthetic drugs on human breast carcinoma MCF-7 cells. Anticancer Res. 2009;29(8):2993-2996.

Bastida J, Lavilla R, Viladomat F. Chemical and biological aspects of Narcissus alkaloids. In: Muñoz-Torrero, D (Ed) The Alkaloids. Elsevier Scientific Publishing. Amsterdam. The Netherlands. 2006, pp 87-179. https://doi.org/10.1016/S1099-4831(06)63003-4

» https://doi.org/https://doi.org/10.1016/S1099-4831(06)63003-4

Bessa CDPB, Andrade JP, Oliveira RS, Domingos E, Santos H, Romão W, et al. Identification of Alkaloids from Hippeastrum aulicum (Ker Gawl.) Herb. (Amaryllidaceae) Using CGC-MS and Ambient Ionization Mass Spectrometry (PS-MS and LS-MS). J Braz Chem Soc. 2017;28(5):819-830. http://dx.doi.org/10.21577/0103-5053.20160234

» https://doi.org/http://dx.doi.org/10.21577/0103-5053.20160234

Berkov S, Bastida J, Sidjimova B, Viladomat F, Codina C. Phytochemical differentiation of Galanthus nivalis and Galanthus elwesii: a case study. Biochem Syst Ecol. 2008;36(8):638-645. hptts://doi.org/10.1016/j.bse.2008.04.002

» https://doi.org/hptts://doi.org/10.1016/j.bse.2008.04.002

Brown AC, Ross J, Jones DB, Collier SA, Ayers TL, Hoekstra RM. Risk Factors for Acanthamoeba Keratitis-A Multistate Case-Control Study, 2008-2011. Eye Contact Lens. 2018;44(Suppl 1):S173-S178. http://doi.org/10.1097/ICL.0000000000000365

» https://doi.org/http://doi.org/10.1097/ICL.0000000000000365

Çitoğlu G, Tanker M, Gümüşel B. Antiinflammatory effects of lycorine and haemanthidine. Phytother Res. 1998;12(3):205-206. https://doi.org/10.1002/(SICI)1099-1573(199805)12:3%3C205::AIDPTR203%3E3.0.CO;2-7

» https://doi.org/https://doi.org/10.1002/(SICI)1099-1573(199805)12:3%3C205::AIDPTR203%3E3.0.CO;2-7

Coen DM, Richman DD. Antiviral agents. In: Knipe D.M. & Howley P.M. (Eds), Fields Virology. 5th ed. Williams and Wilkins, Philadelphia, 2007, pp 447-485.

De Andrade J, Pigni NB, Torras-Claveria L, Ying G, Berko S, Reyes-Chilpa R, et al. Alkaloids from the Hippeastrum genus: chemistry and biological activity. Rev Latinoam Quím. 2012;40(2):83-98.

De Andrade JP, Giordani RB, Torras-Claveria L, Pigni, NB, Berkov S, Font-Bardia M, et al. The Brazilian Amaryllidaceae as a source of acetylcholinesterase inhibitory alkaloids. Phytochem Rev. 2016;15:147-160.

Duarte JL, Furst C, Klisiowicz DR, Klassen G, Costa AO. Morphological, genotypic, and physiological characterization of Acanthamoeba isolates from keratitis patients and the domestic environment in Vitoria, Espírito Santo, Brazil. Exp Parasitol. 2013;135(1):9-14. https://doi.org/10.1016/j.exppara.2013.05.013

» https://doi.org/https://doi.org/10.1016/j.exppara.2013.05.013

El-Sayed NM, Ismail, KA, Ahmed SAEG, Hetta MH. In vitro amoebicidal activity of ethanol extracts of Arachis hypogaea L., Curcuma longa L. and Pancratium maritimum L. on Acanthamoeba castellanii cysts. Parasitol Res. 2012;110(5):1985-1992. https://doi.org/10.1007/s00436-011-2727-3

» https://doi.org/https://doi.org/10.1007/s00436-011-2727-3

Giordani RB, Vieira PB, Weizenmann M, Rosemberg DB, Souza AP, Bonorino C, et al. Candimine-induced cell death of the amitochondriate parasite Trichomonas vaginalis J Nat Prod . 2010;73(12):2019-2023. https://doi.org/10.1021/np100449g

» https://doi.org/https://doi.org/10.1021/np100449g

Giordani RB, Vieira PB, Weizenmann M, Rosemberg DB, Souza AP, Bonorino C, et al. Lycorine induces cell death in the amitochondriate parasite, Trichomonas vaginalis, via an alternative non-apoptotic death pathway. Phytochemistry. 2011;72(7):645-50. hptts://doi.org/10.1016/j. phytochem.2011.01.023

» https://doi.org/hptts://doi.org/10.1016/j. phytochem.2011.01.023

Goze I, Alim A, Dag S, Tepe B, Polat. In vitro amoebicidal activity of Salvia staminea and Salvia caespitosa on Acanthamoeba castellanii and their cytotoxic potentials on corneal cells. J Ocul Pharmacol Ther. 2009;25(4):293-298. https://doi.org/10.1089/jop.2008.0132

» https://doi.org/https://doi.org/10.1089/jop.2008.0132

Hammersmith KM. Diagnosis and management of Acanthamoeba keratitis. Curr Opin Ophthalmol. 2006;17(4):327-331. https://doi.org/10.1097/01.icu.0000233949.56229.7d

» https://doi.org/https://doi.org/10.1097/01.icu.0000233949.56229.7d

Heredero-Bermejo I, Copa-Patiño JL, Soliveri J, Gómez R, Mata FJ, Pérez-Serrano J. In vitro comparative assessment of different viability assays in Acanthamoeba castellanii and Acanthamoeba polyphaga trophozoites. Parasitol Res . 2013;112(12):4087-4095. https://doi.org/10.1007/s00436-013-3599-5

» https://doi.org/https://doi.org/10.1007/s00436-013-3599-5

Kaya GI, Sarykaya B, Onur MA, Somer NU, Viladomat F, Codina C, et al. Antiprotozoal alkaloids from Galanthus trojanus Phytochem Lett. 2011;4(3):301-305. http://doi.org/10.1016/j.phytol.2011.05.008

» https://doi.org/http://doi.org/10.1016/j.phytol.2011.05.008

Koch A, Tamez P, Pezzuto J, Soejarto D. Evaluation of plants used for antimalarial treatment by the Maasai of Kenya. J Ethnopharmacol. 2005;101(1-3):95-9. https;//doi: 10.1016/j. jep.2005.03.011. PMID: 15878245.

» https://doi.org/https;//doi: 10.1016/j. jep.2005.03.011

Kuźma Ł, Derda M, Hadaś E, Wysokinska H. Abietane diterpenoids from Salvia sclarea transformed roots as growth inhibitors of pathogenic Acanthamoeba spp. Parasitol Res . 2015;114(1):323-327. https://doi.org/10.1007/s00436-014-4211-3

» https://doi.org/https://doi.org/10.1007/s00436-014-4211-3

Labraña J, Moachoco AK, Kricsfalusy V, Brun R, Codina C, Viladomat F, et al. Alkaloids from Narcissus angustifolius subsp. transcarpathicus (Amaryllidaceae). Phytochemistry . 2002;60(8):847-852. https://doi.org/10.1016/S0031-9422(02)00154-1

» https://doi.org/https://doi.org/10.1016/S0031-9422(02)00154-1

Lamoral-Theys D, Decaestecker C, Mathieu V, Dubois J, Kornienko A, Kiss R, Evidente A, et al. Lycorine and its derivatives for anticancer drug design. Mini Rev Med Chem. 2010;10(1):41-50. https//doi.org/10.2174/138955710791112604

» https://doi.org/https//doi.org/10.2174/138955710791112604

Likhitwitayawuid K, Angerhofer CK, Chai H, Pezzuto JM, Cordell GA, Ruangrungsi N. Cytotoxic and antimalarial alkaloids from the bulbs of Crinum amabile J Nat Prod . 1993;56(8):1331-1338. https://doi.org/10.1021/np50098a017

» https://doi.org/https://doi.org/10.1021/np50098a017

Lorenzo-Morales J, Martim-Navarro CM, Lopéz-Arencibia A, Arnalich-Montiel F, Piñero JE, Valladares B. Acanthamoeba keratitis: an emerging disease gathering importance worldwide? Trends Parasitol. 2013;29(4):181-187. https://doi.org.10.1016/j.pt.2013.01.006

» https://doi.org/https://doi.org.10.1016/j.pt.2013.01.006

Lorenzo-Morales J, Khan NA, Walochnik J. An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite. 2015;22:10. https://doi.org/10.1051/parasite/2015010

» https://doi.org/https://doi.org/10.1051/parasite/2015010

Lukác M, Mrva M, Garajová M, Mojzisová G, Varinská L, Mojzis J, et al. Synthesis, self-aggregation and biological properties of alkylphosphocholine and alkylphosphohomocholine derivatives of cetyltrimethylammonium bromide, cetylpyridinium bromide, benzalkonium bromide (C16) and benzethonium chloride. ‎Eur J Med Chem. 2013;66:46-55. https://doi.org/10.1016/j.ejmech.2013.05.033

» https://doi.org/https://doi.org/10.1016/j.ejmech.2013.05.033

Luo Z, Wang F, Zhang J, Li X, Zhang M, Hao X, et al. Cytotoxic alkaloids from the whole plants of Zephyranthes candida J Nat Prod . 2012;75(12):2113-2120. https//doi.org/10.1021/np3005425

» https://doi.org/https//doi.org/10.1021/np3005425

Marciano-Cabral F, Cabral G. Acanthamoeba spp. as agents of disease in humans. Clin Microbiol Rev. 2003;16(2):273-307. https://doi.gov/10.1128/CMR.16.2.273-307.2003

» https://doi.org/https://doi.gov/10.1128/CMR.16.2.273-307.2003

McNulty J, Nair JJ, Bastida J, Pandey S, Griffin C. Structure-activity studies on the lycorine pharmacophore: a potent inducer of apoptosis in human leukemia cells. Phytochemistry . 2009;70(7):913-919. https//doi.org/10.1016/j.phytochem.2009.04.012

» https://doi.org/https//doi.org/10.1016/j.phytochem.2009.04.012

Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1-2):55-63. https://doi.org/10.1016/0022-1759(83)90303-4

» https://doi.org/https://doi.org/10.1016/0022-1759(83)90303-4

Nair JJ, Van Staden J. Traditional usage, phytochemistry and pharmacology of the South African medicinal plant Boophone disticha (L.f.) Herb. (Amaryllidaceae). J Ethnopharmacol . 2014;151(1):12-26. http://doi.org/10.1016/j.jep.2013.10.053.

» https://doi.org/http://doi.org/10.1016/j.jep.2013.10.053

Osorio EJ, Berkov S, Brun R, Codina C, Viladomat F, Cabezas F, et al. In vitro antiprotozoal activity of alkaloids from Phaedranassa dubia (Amaryllidaceae). Phytochem Lett . 2010;3(3):161-163. https://doi.org/10.1016/j.phytol.2010.06.004

» https://doi.org/https://doi.org/10.1016/j.phytol.2010.06.004

Pagliosa LB, Monteiro SC, Silva KB, Andrade JP, Dutilh J, Bastida J, et al. Effect of isoquinoline alkaloids from two Hippeastrum species on in vitro acetylcholinesterase activity. Phytomedicine. 2010;17(8):698-701. https://doi.org/10.1016/j.phymed.2009.10.003

» https://doi.org/https://doi.org/10.1016/j.phymed.2009.10.003

Radford CF, Bacon AS, Dart JK, Minassian DC. Risk factors for Acanthamoeba keratitis in contact lens users: a case-control study. BMJ. 1995;310(6994):1567-70. https://doi. org/10.1136/bmj.310.6994.1567

» https://doi.org/https://doi. org/10.1136/bmj.310.6994.1567

Reyes-Chilpa R, Berkov S, Hernández-Ortega S, Jankowski CK, Arseneau S, Clotet-Codina I, et al. Acetylcholinesterase-inhibiting Alkaloids from Zephyranthes concolor Molecules. 2011;16(11):9520-33. https://www.mdpi.com/1420-3049/16/11/9520

» https://www.mdpi.com/1420-3049/16/11/9520

Sauter IP, Santos JC, Apel MA, Cibulski SP, Roehe PM, Von Poser GL, et al. Amoebicidal activity and chemical composition of Pterocaulon polystachyum (Asteraceae) essential oil. Parasitol Res . 2011;109(5):1367-1371. https://doi.org/10.1007/s00436-011-2383-7

» https://doi.org/https://doi.org/10.1007/s00436-011-2383-7

Schuster FL, Visvesvara GS. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. Int J Parasitol. 2004;34(9):1001-1027. https://doi.org/10.1016/j.ijpara.2004.06.004

» https://doi.org/https://doi.org/10.1016/j.ijpara.2004.06.004

Sener B, Orhan I, Satayavivad J. Antimalarial activity screening of some alkaloids and the plant extracts from Amaryllidaceae. Phytotherapy Res. 2003;17(10):1220-1223. https://doi.org/10.1002/ptr.1346

» https://doi.org/https://doi.org/10.1002/ptr.1346

Sifaoui I, López-Arencibia A, Ticona JC, Martín-Navarro CM, Reyes-Batle M, Mejri M, et al. Bioassay guided isolation and identification of anti Acanthamoeba compounds from Tunisian olive leaf extracts. Exp Parasitol . 2014;145(Suppl):111-114. https://doi.org/10.1016/j. exppara.2014.02.018

» https://doi.org/https://doi.org/10.1016/j. exppara.2014.02.018

Turner NA, Russell AD, Furr JR, Lloyd D. Emergence of resistance to biocides during differentiation of Acanthamoeba castellanii J Antimicrob Chemoth. 2000;46(1):27-34. https://doi.org/10.1093/jac/46.1.27

» https://doi.org/https://doi.org/10.1093/jac/46.1.27

Toriizuka Y, Kinoshita E, Kogure N, Kitajima M, Ishiyama A, Otoguro K, et al. New lycorine-type alkaloid from Lycoris traubii and evaluation of antitrypanosomal and antimalarial activities of lycorine derivatives. Bioorg Med Chem. 2008;16(24):10182-10189. https://doi.org/10.1016/j.bmc.2008.10.061

» https://doi.org/https://doi.org/10.1016/j.bmc.2008.10.061

Downloads

Published

2022-12-23

Issue

Vol. 58 (2022)

Section

Original Article

License

Copyright (c) 2022 Brazilian Journal of Pharmaceutical Sciences

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

All content of the journal, except where identified, is licensed under a Creative Commons attribution-type BY.

The on line journal has open and free access.

How to Cite

Anti-Acanthamoeba castellanii activity of alkaloid-enriched extracts and lycorine from the Amaryllidaceae species. (2022). Brazilian Journal of Pharmaceutical Sciences, 58. https://doi.org/10.1590/s2175-97902022e20459

Funding data