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Amoebicidal activity of Cassia angustifolia extract and its effect on Acanthamoeba triangularis autophagy-related gene expression at the transcriptional level

Published online by Cambridge University Press:  10 May 2021

Rachasak Boonhok ,
Suthinee Sangkanu ,
Roghayeh Norouzi ,
Abolghasem Siyadatpanah ,
Farzaneh Mirzaei ,
Watcharapong Mitsuwan ,
Nurdina Charong ,
Sueptrakool Wisessombat ,
Maria de Lourdes Pereira  and
Mohammed Rahmatullah
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Rachasak Boonhok
Affiliation:
Department of Medical Technology, School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat80160, Thailand
Suthinee Sangkanu
Affiliation:
School of Allied Health Sciences, Southeast Asia Water Team (SEA Water Team) and World Union for Herbal Drug Discovery (WUHeDD), and Research Excellence Center for Innovation and Health Products, Walailak University, Nakhon Si Thammarat80160, Thailand
Roghayeh Norouzi
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, University of Tabriz, Tabriz51664, Iran
Abolghasem Siyadatpanah
Affiliation:
Ferdows School of Paramedical and Health, Birjand University of Medical Sciences, Birjand9717853577, Iran
Farzaneh Mirzaei
Affiliation:
Department Parasitology and Mycology, School of Medicine, Shahid Sadoughi University of Medical Sciences, Yazd14188-15971, Iran
Watcharapong Mitsuwan
Affiliation:
School of Allied Health Sciences, Southeast Asia Water Team (SEA Water Team) and World Union for Herbal Drug Discovery (WUHeDD), and Research Excellence Center for Innovation and Health Products, Walailak University, Nakhon Si Thammarat80160, Thailand Akkhraratchakumari Veterinary College, and Research Center of Excellence in Innovation of Essential Oil, Walailak University, Nakhon Si Thammarat80160, Thailand
Nurdina Charong
Affiliation:
Department of Medical Technology, School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat80160, Thailand
Sueptrakool Wisessombat
Affiliation:
Department of Medical Technology, School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat80160, Thailand
Maria de Lourdes Pereira
Affiliation:
Department of Medical Sciences, CICECO-Aveiro Institute of Materials, University of Aveiro, Aveiro3810-193, Portugal
Mohammed Rahmatullah
Affiliation:
Department of Biotechnology and Genetic Engineering, University of Development Alternative Lalmatia, Dhaka1209, Bangladesh
Polrat Wilairatana*
Affiliation:
Department of Clinical Tropical Medicine, Faculty of Tropical Medicine, Mahidol University, Bangkok10400, Thailand
Christophe Wiart
Affiliation:
School of Pharmacy, University of Nottingham Malaysia Campus, Selangor43500, Malaysia
Hazel Anne Tabo
Affiliation:
Biological Sciences Department, College of Science and Computer Studies, De La Salle University-Dasmarinas, Cavite4115, Philippines
Karma G. Dolma
Affiliation:
Department of Microbiology, Sikkim Manipal Institute of Medical Sciences (SMIMS), Gangtok, Sikkim737102, India
Veeranoot Nissapatorn*
Affiliation:
Department of Medical Technology, School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat80160, Thailand School of Allied Health Sciences, Southeast Asia Water Team (SEA Water Team) and World Union for Herbal Drug Discovery (WUHeDD), and Research Excellence Center for Innovation and Health Products, Walailak University, Nakhon Si Thammarat80160, Thailand
*
Authors for correspondence: Polrat Wilairatana, E-mail: polrat.wil@mahidol.ac.th; Veeranoot Nissapatorn, E-mail: nissapat@gmail.com
Authors for correspondence: Polrat Wilairatana, E-mail: polrat.wil@mahidol.ac.th; Veeranoot Nissapatorn, E-mail: nissapat@gmail.com
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Abstract

Cassia angustifolia Vahl. plant is used for many therapeutic purposes, for example, in people with constipation, skin diseases, including helminthic and parasitic infections. In our study, we demonstrated an amoebicidal activity of C. angustifolia extract against Acanthamoeba triangularis trophozoite at a micromolar level. Scanning electron microscopy (SEM) images displayed morphological changes in the Acanthamoeba trophozoite, which included the formation of pores in cell membrane and the membrane rupture. In addition to the amoebicidal activity, effects of the extract on surviving trophozoites were observed, which included cyst formation and vacuolization by a microscope and transcriptional expression of Acanthamoeba autophagy in response to the stress by quantitative polymerase chain reaction. Our data showed that the surviving trophozoites were not transformed into cysts and the trophozoite number with enlarged vacuole was not significantly different from that of untreated control. Molecular analysis data demonstrated that the mRNA expression of AcATG genes was slightly changed. Interestingly, AcATG16 decreased significantly at 12 h post treatment, which may indicate a transcriptional regulation by the extract or a balance of intracellular signalling pathways in response to the stress, whereas AcATG3 and AcATG8b remained unchanged. Altogether, these data reveal the anti-Acanthamoeba activity of C. angustifolia extract and the autophagic response in the surviving trophozoites under the plant extract pressure, along with data on the formation of cysts. These represent a promising plant for future drug development. However, further isolation and purification of an active compound and cytotoxicity against human cells are needed, including a study on the autophagic response at the protein level.

Keywords

Acanthamoeba triangularisautophagyCassia angustifoliaencystation
Type
Research Article
Information
Parasitology , Volume 148 , Issue 9 , August 2021 , pp. 1074 - 1082
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Anwar, A, Khan, NA and Siddiqui, R (2018) Combating Acanthamoeba spp. cysts: what are the options? Parasites & Vectors 11, 26.CrossRefGoogle ScholarPubMed
Anwar, A, Ting, ELS, Anwar, A, ul Ain, N, Faizi, S, Shah, MR, Khan, NA and Siddiqui, R (2020) Antiamoebic activity of plant-based natural products and their conjugated silver nanoparticles against Acanthamoeba castellanii (ATCC 50492). AMB Express 10, 1–10.CrossRefGoogle Scholar
Aqeel, Y, Siddiqui, R, Iftikhar, H and Khan, NA (2013) The effect of different environmental conditions on the encystation of Acanthamoeba castellanii belonging to the T4 genotype. Experimental Parasitology 135, 30–35.CrossRefGoogle ScholarPubMed
Bellassoued, K, Hamed, H, Ghrab, F, Kallel, R, Van Pelt, J, Makni Ayadi, F and Elfeki, A (2019) Antioxidant and hepatopreventive effects of Cassia angustifolia extract against carbon tetrachloride-induced hepatotoxicity in rats. Archives of Physiology and Biochemistry 1–11. doi: 10.1080/13813455.2019.1650778CrossRefGoogle ScholarPubMed
Bouyer, S, Rodier, M-H, Guillot, A and Héchard, Y (2009) Acanthamoeba castellanii: proteins involved in actin dynamics, glycolysis, and proteolysis are regulated during encystation. Experimental Parasitology 123, 90–94.CrossRefGoogle ScholarPubMed
Bunsuwansakul, C, Mahboob, T, Hounkong, K, Laohaprapanon, S, Chitapornpan, S, Jawjit, S, Yasiri, A, Barusrux, S, Bunluepuech, K and Sawangjaroen, N (2019) Acanthamoeba in Southeast Asia – overview and challenges. The Korean Journal of Parasitology 57, 341.CrossRefGoogle ScholarPubMed
Chagla, A and Griffiths, A (1974) Growth and encystation of Acanthamoeba castellanii. Microbiology (Reading, England) 85, 139–145.Google ScholarPubMed
de Lacerda, AG and Lira, M (2021) Acanthamoeba keratitis: a review of biology, pathophysiology and epidemiology. Ophthalmic and Physiological Optics 41, 116–135.CrossRefGoogle ScholarPubMed
Elsheikha, HM, Siddiqui, R and Khan, NA (2020) Drug discovery against Acanthamoeba infections: present knowledge and unmet needs. Pathogens (Basel, Switzerland) 9, 405.Google ScholarPubMed
Feng, Y, He, D, Yao, Z and Klionsky, DJ (2014) The machinery of macroautophagy. Cell Research 24, 24–41.CrossRefGoogle ScholarPubMed
Fujita, N, Itoh, T, Omori, H, Fukuda, M, Noda, T and Yoshimori, T (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Molecular Biology of the Cell 19, 2092–2100.CrossRefGoogle ScholarPubMed
Gatica, D, Lahiri, V and Klionsky, DJ (2018) Cargo recognition and degradation by selective autophagy. Nature Cell Biology 20, 233–242.CrossRefGoogle ScholarPubMed
Hasni, I, Andréani, J, Colson, P and La Scola, B (2020) Description of virulent factors and horizontal gene transfers of keratitis-associated amoeba Acanthamoeba triangularis by genome analysis. Pathogens (Basel, Switzerland) 9, 217.Google ScholarPubMed
Heredero-Bermejo, I, Martín-Pérez, T, Copa-Patiño, JL, Gómez, R, de la Mata, FJ, Soliveri, J and Pérez-Serrano, J (2020) Ultrastructural study of Acanthamoeba polyphaga trophozoites and cysts treated in vitro with cationic carbosilane dendrimers. Pharmaceutics 12, 565.CrossRefGoogle ScholarPubMed
Huang, F-C, Shih, M-H, Chang, K-F, Huang, J-M, Shin, J-W and Lin, W-C (2017) Characterizing clinical isolates of Acanthamoeba castellanii with high resistance to polyhexamethylene biguanide in Taiwan. Journal of Microbiology, Immunology and Infection 50, 570–577.CrossRefGoogle ScholarPubMed
Ibrahim, YW, Boase, DL and Cree, IA (2009) How could contact lens wearers be at risk of Acanthamoeba infection? A review. Journal of Optometry 2, 60–66.CrossRefGoogle Scholar
Iovieno, A, Oechsler, RA, Ledee, DR, Miller, D and Alfonso, EC (2010) Drug-resistant severe Acanthamoeba keratitis caused by rare T5 Acanthamoeba genotype. Eye & Contact Lens 36, 183–184.CrossRefGoogle ScholarPubMed
Jani, DK and Goswami, S (2020) Antidiabetic activity of Cassia angustifolia Vahl. and Raphanus sativus Linn. leaf extracts. Journal of Traditional and Complementary Medicine 10, 124.CrossRefGoogle ScholarPubMed
Juarez, MM, Tártara, LI, Cid, AG, Real, JP, Bermúdez, JM, Rajal, VB and Palma, SD (2018) Acanthamoeba in the eye, can the parasite hide even more? Latest developments on the disease. Contact Lens and Anterior Eye 41, 245–251.CrossRefGoogle ScholarPubMed
Khan, NA (2006) Acanthamoeba: biology and increasing importance in human health. FEMS Microbiology Reviews 30, 564–595.CrossRefGoogle ScholarPubMed
Khan, NA, Anwar, A and Siddiqui, R (2019) Acanthamoeba keratitis: current status and urgent research priorities. Current Medicinal Chemistry 26, 5711–5726.CrossRefGoogle ScholarPubMed
Kim, SY, Syms, MJ, Holtel, MR and Nauschuetz, KK (2000) Acanthamoeba sinusitis with subsequent dissemination in an AIDS patient. Ear, Nose & Throat Journal 79, 168–174.CrossRefGoogle Scholar
Kim, S-H, Moon, E-K, Hong, Y, Chung, D-I and Kong, H-H (2015) Autophagy protein 12 plays an essential role in Acanthamoeba encystation. Experimental Parasitology 159, 46–52.CrossRefGoogle ScholarPubMed
Kolören, O, Kolören, Z, Şekeroğlu, ZA, Colayvaz, M and Karanis, P (2019) Amoebicidal and amoebistatic effects of Artemisia argyi methanolic extracts on Acanthamoeba castellanii trophozoites and cysts. Acta Parasitologica 64, 63–70.CrossRefGoogle ScholarPubMed
Kundu, S, Roy, S and Lyndem, LM (2014) Broad spectrum anthelmintic potential of Cassia plants. Asian Pacific Journal of Tropical Biomedicine 4, S436–S441.CrossRefGoogle ScholarPubMed
Lorenzo-Morales, J, Martín-Navarro, CM, López-Arencibia, A, Arnalich-Montiel, F, Piñero, JE and Valladares, B (2013) Acanthamoeba keratitis: an emerging disease gathering importance worldwide? Trends in Parasitology 29, 181–187.CrossRefGoogle ScholarPubMed
Lorenzo-Morales, J, Khan, NA and Walochnik, J (2015) An update on Acanthamoeba keratitis: diagnosis, pathogenesis and treatment. Parasite 22. doi: 10.1051/parasite/2015010CrossRefGoogle Scholar
Mahboob, T, Nawaz, M, Tian-Chye, T, Samudi, C, Wiart, C and Nissapatorn, V (2018) Preparation of poly (dl-lactide-co-glycolide) nanoparticles encapsulated with periglaucine A and betulinic acid for in vitro anti-Acanthamoeba and cytotoxicity activities. Pathogens (Basel, Switzerland) 7, 62.Google ScholarPubMed
Martínez-Sagasti, F, Gonzalez-Gallego, MA and Moneo-Gonzalez, A (2016) Monotherapy vs combined therapy in the treatment of multi-drug resistance Gram-negative bacteria. Revista Española de Quimioterapia 29, 43–46.Google Scholar
Matson, DO, Rouah, E, Lee, RT, Armstrong, D, Parke, JT and Baker, CJ (1988) Acanthameba meningoencephalitis masquerading as neurocysticercosis. The Pediatric Infectious Disease Journal 7, 121–124.CrossRefGoogle ScholarPubMed
Mitsuwan, W, Bunsuwansakul, C, Leonard, TE, Laohaprapanon, S, Hounkong, K, Bunluepuech, K, Chalermpol, K, Mahboob, T, Sumudi Raju, C and Dhobi, M (2020) Curcuma longa ethanol extract and curcumin inhibit the growth of Acanthamoeba triangularis trophozoites and cysts isolated from water reservoirs at Walailak University, Thailand. Pathogens and Global Health 114, 1–11.CrossRefGoogle ScholarPubMed
Moon, E-K, Chung, D-I, Hong, Y-C and Kong, H-H (2009) Autophagy protein 8 mediating autophagosome in encysting Acanthamoeba. Molecular and Biochemical Parasitology 168, 43–48.CrossRefGoogle ScholarPubMed
Moon, E-K, Chung, D-I, Hong, Y and Kong, H-H (2011) Atg3-mediated lipidation of Atg8 is involved in encystation of Acanthamoeba. The Korean Journal of Parasitology 49, 103.CrossRefGoogle ScholarPubMed
Moon, E-K, Hong, Y, Chung, D-I and Kong, H-H (2012) Cysteine protease involving in autophagosomal degradation of mitochondria during encystation of Acanthamoeba. Molecular and Biochemical Parasitology 185, 121–126.CrossRefGoogle ScholarPubMed
Moon, E-K, Hong, Y, Chung, D-I and Kong, H-H (2013) Identification of atg8 isoform in encysting Acanthamoeba. The Korean Journal of Parasitology 51, 497.CrossRefGoogle ScholarPubMed
Moon, E-K, Kim, S-H, Hong, Y, Chung, D-I, Goo, Y-K and Kong, H-H (2015) Autophagy inhibitors as a potential antiamoebic treatment for Acanthamoeba keratitis. Antimicrobial Agents and Chemotherapy 59, 4020–4025.CrossRefGoogle ScholarPubMed
Morrison, AO, Morris, R, Shannon, A, Lauer, SR, Guarner, J and Kraft, CS (2016) Disseminated Acanthamoeba infection presenting with cutaneous lesions in an immunocompromised patient: a case report, review of histomorphologic findings, and potential diagnostic pitfalls. American Journal of Clinical Pathology 145, 266–270.CrossRefGoogle Scholar
Neelam, S and Niederkorn, JY (2017) Focus: infectious diseases: pathobiology and immunobiology of Acanthamoeba keratitis: insights from animal models. The Yale Journal of Biology and Medicine 90, 261.Google Scholar
Nielsen, SE, Ivarsen, A and Hjortdal, J (2020) Increasing incidence of Acanthamoeba keratitis in a large tertiary ophthalmology department from year 1994 to 2018. Acta Ophthalmologica 98, 445–448.CrossRefGoogle Scholar
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.Google ScholarPubMed
Picazarri, K, Nakada-Tsukui, K and Nozaki, T (2008) Autophagy during proliferation and encystation in the protozoan parasite Entamoeba invadens. Infection and Immunity 76, 278–288.CrossRefGoogle ScholarPubMed
Sanguan, S, Wannasan, A, Junkum, A, Jitpakdi, A, Riyong, D, Champakaew, D and Pitasawat, B (2018) Screening for in vitro amoebicidal activity of plant essential oils against Acanthamoeba sp. Chiang Mai Medical Journal 57, 89–98.Google Scholar
Song, S-M, Han, B-I, Moon, E-K, Lee, Y-R, Yu, HS, Jha, BK, Danne, D-BS, Kong, H-H, Chung, D-I and Hong, Y (2012) Autophagy protein 16-mediated autophagy is required for the encystation of Acanthamoeba castellanii. Molecular and Biochemical Parasitology 183, 158–165.CrossRefGoogle ScholarPubMed
Szentmáry, N, Daas, L, Shi, L, Laurik, KL, Lepper, S, Milioti, G and Seitz, B (2019) Acanthamoeba keratitis – clinical signs, differential diagnosis and treatment. Journal of Current Ophthalmology 31, 16–23.CrossRefGoogle ScholarPubMed
Taravaud, A, Loiseau, PM and Pomel, S (2017) In vitro evaluation of antimicrobial agents on Acanthamoeba sp. and evidence of a natural resilience to amphotericin B. The International Journal for Parasitology: Drugs and Drug Resistance 7, 328–336.Google ScholarPubMed
Tepekule, B, Uecker, H, Derungs, I, Frenoy, A and Bonhoeffer, S (2017) Modeling antibiotic treatment in hospitals: a systematic approach shows benefits of combination therapy over cycling, mixing, and mono-drug therapies. PLoS Computational Biology 13, e1005745.CrossRefGoogle ScholarPubMed
Tripathi, Y (1999) Cassia angustifolia, a versatile medicinal crop. International Tree Crops Journal 10, 121–129.CrossRefGoogle Scholar
Tyers, M and Wright, GD (2019) Drug combinations: a strategy to extend the life of antibiotics in the 21st century. Nature Reviews Microbiology 17, 141–155.CrossRefGoogle ScholarPubMed
Ukil, B, Roy, S, Nandi, S and Lyndem, LM (2018) Senna plant induces disruption on the mitochondria of Hymenolepis diminuta. International Journal of Pharmacy and Pharmaceutical Sciences 10, 136–138.CrossRefGoogle Scholar
Xuan, Y-H, Chung, B-S, Hong, Y-C, Kong, H-H, Hahn, T-W and Chung, D-I (2008) Keratitis by Acanthamoeba triangularis: report of cases and characterization of isolates. The Korean Journal of Parasitology 46, 157.CrossRefGoogle ScholarPubMed
Yorimitsu, T and Klionsky, DJ (2005) Autophagy: molecular machinery for self-eating. Cell Death and Differentiation 12, 1542–1552.CrossRefGoogle ScholarPubMed
Zhang, Y, Chen, X, Gueydan, C and Han, J (2018) Plasma membrane changes during programmed cell deaths. Cell Research 28, 9–21.CrossRefGoogle ScholarPubMed
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