Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-18T07:19:25.827Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro anti-Acanthamoeba activity of flavonoid glycosides isolated from Delphinium gracile, D. staphisagria, Consolida oliveriana and Aconitum napellus

Published online by Cambridge University Press:  24 June 2021

Rubén Martín-Escolano Open the ORCID record for Rubén Martín-Escolano [Opens in a new window] ,
Sonia Molero Romero ,
Jesus G. Díaz ,
Clotilde Marín Open the ORCID record for Clotilde Marín [Opens in a new window] ,
Manuel Sánchez-Moreno  and
Mª José Rosales
Rubén Martín-Escolano
Affiliation:
Laboratory of Molecular & Evolutionary Parasitology, RAPID group, School of Biosciences, University of Kent, Canterbury, CT2 7NJ, UK
Sonia Molero Romero
Affiliation:
Departamento de Parasitología, Instituto de Investigacion Biosanitaria Ibs, University of Granada, Severo Ochoa s/n, E-18071, Granada, Spain
Jesus G. Díaz
Affiliation:
Departamento de Química Orgánica, Instituto de Bio-Orgánica ‘Antonio González’, Universidad de La Laguna, Ctra. a la Esperanza 2, 38206-La Laguna, Tenerife, Spain
Clotilde Marín
Affiliation:
Departamento de Parasitología, Instituto de Investigacion Biosanitaria Ibs, University of Granada, Severo Ochoa s/n, E-18071, Granada, Spain
Manuel Sánchez-Moreno
Affiliation:
Departamento de Parasitología, Instituto de Investigacion Biosanitaria Ibs, University of Granada, Severo Ochoa s/n, E-18071, Granada, Spain
Mª José Rosales*
Affiliation:
Departamento de Parasitología, Instituto de Investigacion Biosanitaria Ibs, University of Granada, Severo Ochoa s/n, E-18071, Granada, Spain
*
Author for correspondence: Mª José Rosales, E-mail: mjrosale@ugr.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Acanthamoeba spp. are widely distributed in the environment and cause serious infections in humans. Treatment of Acanthamoeba infections is very challenging and not always effective which requires the development of more efficient drugs against Acanthamoeba spp. The purpose of the present study was to test medicinal plants that may be useful in the treatment of Acanthamoeba spp. Here we evaluated the trophozoital and cysticidal activity of 13 flavonoid glycosides isolated from Delphinium gracile, D. staphisagria, Consolida oliveriana and from Aconitum napellus subsp. Lusitanicum against the amoeba Acanthamoeba castellanii. AlamarBlue Assay Reagent® was used to determine the activity against trophozoites of A. castellanii, and cytotoxic using Vero cells. Cysticidal activity was assessed on treated cysts by light microscopy using a Neubauer chamber to quantify cysts and trophozoites. Flavonoids 1, 2, 3 and 4 showed higher trophozoital activity and selectivity indexes than the reference drug chlorhexidine digluconate. In addition, flavonoid 2 showed 100% cysticidal activity at a concentration of 50 μm, lower than those of the reference drug and flavonoid 3 (100 μm). These results suggest that flavonoids 2 and 3 might be used for the development of novel therapeutic approaches against Acanthamoeba infections after satisfactory in vivo evaluations.

Keywords

Acanthamoeba castellaniiamoebicidalchlorhexidine digluconatecysticidalflavonoids
Type
Research Article
Information
Parasitology , Volume 148 , Issue 11 , September 2021 , pp. 1392 - 1400
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bang, S, Edell, E, Eghrari, AO and Gottsch, JD (2010) Treatment with voriconazole in 3 eyes with resistant Acanthamoeba keratitis. American Journal of Ophthalmology 149, 66–69.CrossRefGoogle ScholarPubMed
Banich, A, Bu, P, Jacob, G, Fox, I, Zhang, X, Perlman, J and Bouchar, C (2003) Penetration of chlorhexidine into the rabbit anterior chamber following topical administration. Investigative Ophthalmology 44, U317, Meeting Abstract, 3769.Google Scholar
Carmona, AJ, Perez, P, Paz, D, Herz, W and Dı, G (2008). Acylated flavonol glycosides from Delphinium staphisagria. 1, 125–129.Google Scholar
Carvalho, FRS, Foronda, AS, Mannis, MJ, Höfling-Lima, AL, Belfort, R and De Freitas, D (2009) Twenty years of Acanthamoeba keratitis. Cornea 28, 516–519.CrossRefGoogle ScholarPubMed
Cordingley, JS, Wills, RA and Villemez, CL (1996) Osmolarity is an independent trigger of Acanthamoeba castellanli differentiation. Journal of Cellular Biochemistry 61, 167–171.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Degerli, S, Tepe, B, Celiksoz, A, Berk, S and Malatyali, E (2012) In vitro amoebicidal activity of Origanum syriacum and Origanum laevigatum on Acanthamoeba castellanii cysts and trophozoites. Experimental Parasitology 131, 20–24.CrossRefGoogle ScholarPubMed
Derda, M, Thiem, B, Budzianowski, J, Hadaś, E, Wojt, WJ and Wojtkowiak-Giera, A (2013) The evaluation of the amebicidal activity of Eryngium planum extracts. Acta Poloniae Pharmaceutica – Drug Research 70, 1027–1034.Google ScholarPubMed
Díaz, J, García Ruiz, J, Rachid Días, B, Gavín Sazatornil, J and Werner, H (2005) Flavonol 3,7-glycosides and dihydroxyphenethyl glycosides from Aconitum napellus subsp. Biochemical Systematics and Ecology 33, 201–205.CrossRefGoogle Scholar
Diaz, JG and Herz, W (2010) Phytochemistry acylated flavonol tetraglycosides from Delphinium gracile. Phytochemistry 71, 463–468.CrossRefGoogle ScholarPubMed
Ehlers, N and Hjortdal, J (2004) Are cataract and iris atrophy toxic complications of medical treatment of Acanthamoeba keratitis? Acta Ophthalmologica Scandinavica 82, 228–231.CrossRefGoogle ScholarPubMed
El-Sayed, NM, Ismail, KA, Ahmed, SAEG and Hetta, MH (2012) In vitro amoebicidal activity of ethanol extracts of Arachis hypogaea L., Curcuma longa L. and Pancratium maritimum L. on Acanthamoeba castellanii cysts. Parasitology Research 110, 1985–1992.CrossRefGoogle Scholar
Ferrari, G, Matuska, S and Rama, P (2011) Double-biguanide therapy for resistant Acanthamoeba keratitis. Case Reports in Ophthalmology 2, 338–342.CrossRefGoogle ScholarPubMed
Ghazouani, N, Sifaoui, I, Bachrouch, O, Abderrabba, M, Pinero, JE and Lorenzo-Morales, J (2017) Essential oil composition and anti Acanthamoeba studies of Teucrium ramosissimum. Experimental Parasitology 183, 207–211.CrossRefGoogle ScholarPubMed
Greub, G and Raoult, D (2004) Microorganisms resistant to free-living amoebae. Clinical Microbiology Reviews 17, 413–433.CrossRefGoogle ScholarPubMed
Gupta, SS and Miescke, KJ (213AD) Drugs for parasitic infections. doi: 10.1016/0378-3758(85)90065-5.CrossRefGoogle Scholar
Hajaji, S, Sifaoui, I, López-Arencibia, A, Reyes-Batlle, M, Valladares, B, Pinero, JE, Lorenzo-Morales, J and Akkari, H (2017) Amoebicidal activity of α-bisabolol, the main sesquiterpene in chamomile (Matricaria recutita L.) essential oil against the trophozoite stage of Acanthamoeba castellani Neff. Acta Parasitologica 62, 290–295.CrossRefGoogle ScholarPubMed
Khan, NA (2006) Acanthamoeba: biology and increasing importance in human health. FEMS Microbiology Reviews 30, 564–595.CrossRefGoogle ScholarPubMed
Marín, C, Ramírez-Macías, I, López-Céspedes, A, Olmo, F, Villegas, N, Díaz, JG, Rosales, MJ, Gutiérrez-Sánchez, R and Sánchez-Moreno, M (2011) In vitro and in vivo trypanocidal activity of flavonoids from Delphinium staphisagria against Chagas disease. Journal of Natural Products 74, 744–750.CrossRefGoogle ScholarPubMed
Marín, C, Díaz, JG, Irure Maiques, D, Ramírez-Macías, I, Rosales, MJ, Guitierrez-Sánchez, R, Cañas, R and Sánchez-Moreno, M (2017) Antitrypanosomatid activity of flavonoid glycosides isolated from Delphinium gracile, D. staphisagria, Consolida oliveriana and from Aconitum napellus subsp. Lusitanicum. Phytochemistry Letters 19, 196–209.CrossRefGoogle Scholar
Martín-Navarro, CM, Lorenzo-Morales, J, Cabrera-Serra, MG, Rancel, F, Coronado-Álvarez, NM, Piñero, JE and Valladares, B (2008) The potential pathogenicity of chlorhexidine- sensitive Acanthamoeba strains isolated from contact lens cases from asymptomatic individuals in Tenerife, Canary Islands, Spain. Journal of Medical Microbiology 57, 1399–1404. doi: 10.1099/jmm.0.2008/003459-0CrossRefGoogle ScholarPubMed
Mcbride, J, Ingram, PR, Henriquez, FL, Roberts, CW and Icrobiol, JCLINM (2005) Development of colorimetric microtiter plate assay for assessment of antimicrobials against Acanthamoeba. Journal of Clinical Microbiology 43, 629–634.CrossRefGoogle ScholarPubMed
Nijveldt, RJ, Van Nood, E, Van Hoorn, DEC, Boelens, PG, Van Norren, K and Van Leeuwen, PAM (2001) Flavonoids: a review of probable mechanisms of action and potential applications. American Journal of Clinical Nutrition 74, 418–425.CrossRefGoogle ScholarPubMed
Niyyati, M, Dodangeh, S and Lorenzo-Morales, J (2016) A review of the current research trends in the application of medicinal plants as a source for novel therapeutic agents against Acanthamoeba infections. Iranian Journal of Pharmaceutical Research 15, 893–900.Google ScholarPubMed
Paper, O (2008) Cytotoxic activities of flavonoid glycoside acetates from Consolida oliveriana. Planta Medica 74, 171–174. doi: 10.1055/s-2008-1034278Google Scholar
Polat, ZA, Tepe, B and Vural, A (2007) In vitro effectiveness of Thymus sipyleus subsp. sipyleus var. sipyleus on Acanthamoeba castellanii and its cytotoxic potential on corneal cells. Parasitology Research 101, 1551–1555.CrossRefGoogle ScholarPubMed
Radford, CF, Minassian, DC and Dart, JKG (2002) Acanthamoeba keratitis in England and Wales: incidence, outcome, and risk factors. British Journal of Ophthalmology 86, 536–542.CrossRefGoogle Scholar
Ramírez-Macías, I, Marín, C, Díaz, JG, Rosales, MJ, Gutiérrez-Sánchez, R and Sánchez-Moreno, M (2012) Leishmanicidal activity of nine novel flavonoids from Delphinium staphisagria. The Scientific World Journal 2012, 203646. doi: 10.1100/2012/203646CrossRefGoogle ScholarPubMed
Ródio, C, Da Rocha Vianna, D, Kowalski, KP, Panatieri, LF, Von Poser, G and Rott, MB (2008) In vitro evaluation of the amebicidal activity of Pterocaulon polystachyum (Asteraceae) against trophozoites of Acanthamoeba castellanii. Parasitology Research 104, 191–194.CrossRefGoogle ScholarPubMed
Rusciano, G, Capriglione, P, Pesce, G, Del Prete, S, Cennamo, G, Di Cave, D, Cerulli, L and Sasso, A (2013) Raman microspectroscopy analysis in the treatment of Acanthamoeba keratitis. PLoS ONE 8, e72127. doi: 10.1371/journal.pone.0072127CrossRefGoogle ScholarPubMed
Saoudi, S, Sifaoui, I, Chammem, N, Reyes-Batlle, M, López-Arencibia, A, Pacheco-Fernández, I, Pino, V, Hamdi, M, Jiménez, IA, Bazzocchi, IL, Piñero, JE and Lorenzo-Morales, J (2017) Anti-acanthamoeba activity of Tunisian Thymus capitatus essential oil and organic extracts. Experimental Parasitology 183, 231–235.CrossRefGoogle ScholarPubMed
Sauter, IP, Dos Santos, JC, Apel, MA, Cibulski, SP, Roehe, PM, Von Poser, GL and Rott, MB (2011) Amoebicidal activity and chemical composition of Pterocaulon polystachyum (Asteraceae) essential oil. Parasitology Research 109, 1367–1371.CrossRefGoogle ScholarPubMed
Sauter, IP, Rossa, GE, Lucas, AM, Cibulski, SP, Roehe, PM, da Silva, LAA, Rott, MB, Vargas, RMF, Cassel, E and von Poser, GL (2012) Chemical composition and amoebicidal activity of Piper hispidinervum (Piperaceae) essential oil. Industrial Crops and Products 40, 292–295.CrossRefGoogle Scholar
Schmidt, TJ, Khalid, SA, Romanha, AJ, Alves, TMA, Biavatti, MW, Brun, R, Da Costa, FB, de Castro, SL, Ferreira, VF, de Lacerda, MVG, Lago, JHG, Leon, LL, Lopes, NP, das Neves Amorim, RC, Niehues, M and Ogungbe, IV (2012) The potential of secondary metabolites from plants as drugs or leads against protozoan neglected diseases – part I. Current Medicinal Chemistry 19, 2128–2175.CrossRefGoogle ScholarPubMed
Schuster, FL and Visvesvara, GS (2004) Opportunistic amoebae: challenges in prophylaxis and treatment. Drug Resistance Updates 7, 41–51.CrossRefGoogle ScholarPubMed
Sifaoui, I, López-Arencibia, A, Ticona, JC, Martín-Navarro, CM, Reyes-Batlle, M, Mejri, M, Lorenzo-Morales, J, Jiménez, AI, Valladares, B, Lopez-Bazzocchi, I, Abderabba, M and Piñero, JE (2014) Bioassay guided isolation and identification of anti-Acanthamoeba compounds from Tunisian olive leaf extracts. Experimental Parasitology 145, S111–S114.CrossRefGoogle ScholarPubMed
Visvesvara, GS, Moura, H and Schuster, FL (2007) Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunology and Medical Microbiology 50, 1–26.CrossRefGoogle ScholarPubMed
Willaert, E (1971) Isolement et culture in vitro des amibes du genre Naegleria. Annales de la Société Belge de Médecine Tropicale 51, 701–708.Google Scholar