Hostname: page-component-7bb8b95d7b-dvmhs Total loading time: 0 Render date: 2024-09-17T02:13:28.091Z Has data issue: false hasContentIssue false

Toxicities of the copper and zinc oxide nanoparticles on Marshallagia marshalli (Nematoda: Trichostrongylidae): evidence on oxidative/nitrosative stress biomarkers, DNA damage and egg hatchability

Published online by Cambridge University Press:  02 December 2021

T. Shafienejad Jalali
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
F. Malekifard*
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
B. Esmaeilnejad
Affiliation:
Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
S. Asri Rezaie
Affiliation:
Department of Internal Medicine and Clinical Pathology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
*
Author for correspondence: F. Malekifard, E-mail: f.malekifard@urmia.ac.ir

Abstract

This study investigated the in vitro anthelmintic activity of copper oxide (CuO) and zinc oxide (ZnO) nanoparticles (NPs) against Marshallagia marshalli. The in vitro study was based on an egg hatch assay, adult and larvae motility inhibition assays, DNA damage, intensity protein profile along with several oxidative/nitrosative stress biomarkers including superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px), protein carbonylation (PCO), malondialdehyde (MDA), total antioxidant status (TAS) and nitric oxide (NO) content. Different concentrations of CuO-NPs and ZnO-NPs (1, 4, 8, 12 and 16 ppm) were used to assess anthelmintic effects on three stages of M. marshalli life cycle – that is, eggs, larvae and adult parasites for 24 h. The results indicated that CuO-NPs and ZnO-NPs played a significant role as anthelminthics, and the effect was dependent on time and concentration. The concentrations of 12 and 16 ppm of CuO-NPs and 16 ppm of ZnO-NPs resulted in the induction of oxidative/nitrosative stress (decreased SOD, GSH-Px and CAT, and increased MDA, PCO and NO), increased DNA damage, inhibition of adult and larval motility, egg hatch and low intensity of protein bands following sodium dodecyl sulphate–polyacrylamide gel electrophoresis, compared to control. It was concluded that CuO-NPs and ZnO-NPs could be utilized as novel and potential agents for the control and treatment of M. marshalli infection, and they have the pharmacological potential to be studied in vivo for further utilization in treating parasitic infections.

Type
Research Paper
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

Adeyemi, OS and Faniyan, TO (2014) Antioxidant status of rats administered silver nanoparticles orally. Journal of Taibah University Medical Sciences 9(3), 182186.CrossRefGoogle Scholar
Adeyemi, OS and Whiteley, CG (2013) Interaction of nanoparticles with arginine kinase from Trypanosoma brucei: kinetic and mechanistic evaluation. International Journal of Biological Macromolecules 62, 450456.CrossRefGoogle ScholarPubMed
Aleuy, OA, Hoberg, EP, Paquette, C, Ruckstuhl, KE and Kutz, S (2019) Adaptations and phenotypic plasticity in developmental traits of Marshallagia marshalli. International Journal for Parasitology 49(10), 789796.CrossRefGoogle ScholarPubMed
Azqueta, A, Meier, S, Priestley, C and Collins, A (2011) The influence of scoring method on variability in results obtained with the comet assay. Mutagenesis 26(3), 393399.CrossRefGoogle ScholarPubMed
Baghbani, Z, Esmaeilnejad, B and Asri-Rezaei, S (2020) Assessment of oxidative/nitrosative stress biomarkers and DNA damage in Teladorsagia circumcincta following exposure to zinc oxide nanoparticles. Journal of Helminthology 94, e115.CrossRefGoogle ScholarPubMed
Bhardwaj, R, Saudagar, P and Dubey, VK (2012) Nanobiosciences: a contemporary approach in antiparasitic drugs. Molecular and Cellular Pharmacology 4(3), 97103.Google Scholar
Buege, JA and Aust, SD (1978) Microsomal lipid peroxidation. Methods in Enzymology 52, 302310.CrossRefGoogle ScholarPubMed
Burney, S, Caulfield, JL, Niles, JC, Wishnok, JS and Tannenbaum, SR (1999) The chemistry of DNA damage from nitric oxide and peroxynitrite. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 424(1–2), 3749.CrossRefGoogle ScholarPubMed
Butkus, MA, Labare, MP, Starke, JA, Moon, K and Talbot, M (2004) Use of aqueous silver to enhance inactivation of coliphage MS-2 by UV disinfection. Applied and Environmental Microbiology 70(5), 2848.CrossRefGoogle ScholarPubMed
Camurça-Vasconcelos, ALF, Bevilaqua, CML, Morais, SM and Vieira, LS (2007) Anthelmintic activity of Croton zehntneri and Lippia sidoides essential oils. Veterinary Parasitology 148(3–4), 288294.CrossRefGoogle ScholarPubMed
Chen, M, Ike, M and Fujita, M (2002) Acute toxicity, mutagenicity, and estrogenicity of bisphenol-A and other bisphenols. Environmental Toxicology: An International Journal 17(1), 8086.CrossRefGoogle ScholarPubMed
Chitra, K and Annadurai, G (2013) Antimicrobial activity of wet chemically engineered spherical shaped ZnO nanoparticles on food borne pathogen. International Food Research Journal 20(1), 5964.Google Scholar
Chiumiento, L and Bruschi, F (2009) Enzymatic antioxidant systems in helminth parasites. Parasitology Research 105(3), 593603.CrossRefGoogle ScholarPubMed
Costa, CTC, Morais, SM, Bevilaqua, CML, Souza, MMC and Leite, FKA (2002) Ovicidal effect of Mangifera indica L. seeds extracts on Haemonchus contortus. Brazilian Journal of Veterinary Parasitology 11, 5760.Google Scholar
Cruz, LM, Allanson, M, Kwa, B, Azizan, A and Izurieta, R (2012) Morphological changes of Ascaris spp. eggs during their development outside the host. Journal of Parasitology 98(1), 6368.CrossRefGoogle ScholarPubMed
de Souza Chagas, AC and da Silva Vieira, L (2007) Azadirachta indica (Neem) action in goats gastrointestinal nematodes. Brazilian Journal of Veterinary Research and Animal Science 44(1), 4955.CrossRefGoogle Scholar
Ding, AH, Nathan, CF and Stuehr, DJ (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. The Journal of Immunology 141(7), 24072412.Google ScholarPubMed
Dorostkar, R, Ghalavand, M, Nazarizadeh, A, Tat, M and Hashemzadeh, MS (2017) Anthelmintic effects of zinc oxide and iron oxide nanoparticles against Toxocara vitulorum. International Nano Letters 7(2), 157164.CrossRefGoogle Scholar
Eslami, A, Meydani, M, Maleki, SH and Zargarzadeh, A (1979) Gastrointestinal nematodes of wild sheep (Ovis orientalis) from Iran. Journal of Wildlife Diseases 15(2), 263265.CrossRefGoogle ScholarPubMed
Esmaeilnejad, B, Samiei, A, Mirzaei, Y and Farhang-Pajuh, F (2018) Assessment of oxidative/nitrosative stress biomarkers and DNA damage in Haemonchus contortus, following exposure to zinc oxide nanoparticles. Acta Parasitologica 63(3), 563571.CrossRefGoogle ScholarPubMed
Eyambe, GS, Goven, AJ, Fitzpatrick, LC, Venables, BJ and Cooper, EL (1991) A non-invasive technique for sequential collection of earthworm (Lumbricus terrestris) leukocytes during subchronic immunotoxicity studies. Laboratory Animals 25(1), 6167.CrossRefGoogle ScholarPubMed
Ferreira, LE, Castro, PMN, Chagas, ACS, França, SC and Beleboni, RO (2013) In vitro anthelmintic activity of aqueous leaf extract of Annona muricata L.(Annonaceae) against Haemonchus contortus from sheep. Experimental Parasitology 134(3), 327332.CrossRefGoogle ScholarPubMed
Franklin, NM, Rogers, NJ, Apte, SC, Batley, GE, Gadd, GE and Casey, PS (2007) Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environmental Science & Technology 41(24), 84848490.CrossRefGoogle ScholarPubMed
Gasser, RB, Bott, NJ, Chilton, NB, Hunt, P and Beveridge, I (2008) Toward practical, DNA-based diagnostic methods for parasitic nematodes of livestock—bionomic and biotechnological implications. Biotechnology Advances 26(4), 325334.CrossRefGoogle ScholarPubMed
Ghiselli, A, Serafini, M, Natella, F and Scaccini, C (2000) Total antioxidant capacity as a tool to assess redox status: critical view and experimental data. Free Radical Biology and Medicine 29(11), 11061114.CrossRefGoogle ScholarPubMed
Gopalakrishnan, K, Ramesh, C, Ragunathan, V and Thamilselvan, M (2012) Antibacterial activity of Cu2O nanoparticles on E. coli synthesized from Tridax procumbens leaf extract and surface coating with polyaniline. Dig J Nanomater Bios 7(2), 833839.Google Scholar
Green, LC, Wagner, DA, Glogowski, J, Skipper, PL, Wishnok, JS and Tannenbaum, SR (1982) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Analytical Biochemistry 126(1), 131138.CrossRefGoogle Scholar
Hadaś, E and Stankiewicz, M (1998) Superoxide dismutase and total antioxidant status of larvae and adults of Trichostrongylus colubriformis, Haemonchus contortus and Ostertagia circumcincta. Parasitology Research 84(8), 646650.CrossRefGoogle ScholarPubMed
Hoberg, EP, Abrams, A, Pilitt, PA and Jenkins, EJ (2012) Discovery and description of a new trichostrongyloid species (Nematoda: Ostertagiinae), abomasal parasites in mountain goat, Oreamnos americanus, from the Western Cordillera of North America. Journal of Parasitology 98(4), 817846.CrossRefGoogle Scholar
Hounzangbe-Adote, MS, Paolini, V, Fouraste, I, Moutairou, K and Hoste, H (2005) In vitro effects of four tropical plants on three life-cycle stages of the parasitic nematode, Haemonchus contortus. Research in Veterinary Science 78(2), 155160.CrossRefGoogle ScholarPubMed
Hu, CW, Li, M, Cui, YB, Li, DS, Chen, J and Yang, LY (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biology and Biochemistry 42(4), 586591.CrossRefGoogle Scholar
Kalpana, VN and Devi Rajeswari, V (2018) A review on green synthesis, biomedical applications, and toxicity studies of ZnO NPs. Bioinorganic Chemistry and Applications 2018, Article ID 3569758, 12.CrossRefGoogle ScholarPubMed
Khan, YA, Singh, BR, Ullah, R, Shoeb, M, Naqvi, AH and Abidi, SMA (2015) Anthelmintic effect of biocompatible zinc oxide nanoparticles (ZnO NPs) on Gigantocotyle explanatum, a neglected parasite of Indian water buffalo. PLoS One 10(7), e0133086.CrossRefGoogle ScholarPubMed
Kotze, AC and McClure, SJ (2001) Haemonchus contortus utilises catalase in defence against exogenous hydrogen peroxide in vitro. International Journal for Parasitology 31(14), 15631571.CrossRefGoogle ScholarPubMed
Levine, ND (1985) Veterinary protozoology. Iowa, Iowa State University Press Ames.Google Scholar
Lichtenfels, JR and Pilitt, PA (1989) Cuticular ridge patterns of Marshallagia marshalli and Ostertagia occidentalis (Nematoda: Trichostrongyloidea) parasitic in ruminants of North America. Proceedings of the Helminthological Society of Washington 56(2), 173182.Google Scholar
Liu, Y, He, L, Mustapha, A, Li, H, Hu, ZQ and Lin, M (2009) Antibacterial activities of zinc oxide nanoparticles against Escherichia coli O157: H7. Journal of Applied Microbiology 107(4), 11931201.CrossRefGoogle ScholarPubMed
Malekifard, F, Tavassoli, M and Vaziri, K (2020) In vitro assessment antiparasitic effect of selenium and copper nanoparticles on Giardia deodenalis cyst. Iranian Journal of Parasitology 15(3), 411.Google ScholarPubMed
Marnett, LJ (2000) Oxyradicals and DNA damage. Carcinogenesis 21(3), 361370.CrossRefGoogle ScholarPubMed
McCord, JM and Fridovich, I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). Journal of Biological Chemistry 244(22), 60496055.CrossRefGoogle Scholar
Morphew, RM, Wright, HA, LaCourse, EJ and Brophy, PM (2011) Towards delineating functions within the Fasciola secreted cathepsin l protease family by integrating in vivo based sub-proteomics and phylogenetics. PLoS Neglected Tropical Diseases 5(1), e937.CrossRefGoogle ScholarPubMed
Morsy, K, Fahmy, S, Mohamed, A, Ali, S, El-Garhy, M and Shazly, M (2019) Optimizing and evaluating the antihelminthic activity of the biocompatible zinc oxide nanoparticles against the ascaridid nematode, Parascaris equorum in vitro. Acta Parasitologica 64(4), 873886.CrossRefGoogle ScholarPubMed
Nair, S, Sasidharan, A, Rani, VVD and Raina, S (2009) Role of size scale of ZnO nanoparticles and microparticles on toxicity toward bacteria and osteoblast cancer cells. Journal of Materials Science: Materials in Medicine 20(1), 235.Google ScholarPubMed
Nazarizadeh, A and Asri-Rezaie, S (2016) Comparative study of antidiabetic activity and oxidative stress induced by zinc oxide nanoparticles and zinc sulfate in diabetic rats. AAPS PharmSciTech 17(4), 834843.CrossRefGoogle ScholarPubMed
Preet, S and Tomar, RS (2017) Anthelmintic effect of biofabricated silver nanoparticles using Ziziphus jujuba leaf extract on nutritional status of Haemonchus contortus. Small Ruminant Research 154, 4551.CrossRefGoogle Scholar
Rajan, TV, Porte, P, Yates, JA, Keefer, L and Shultz, LD (1996) Role of nitric oxide in host defense against an extracellular, metazoan parasite, Brugia malayi. Infection and Immunity 64(8), 33513353.CrossRefGoogle ScholarPubMed
Ramyadevi, J, Jeyasubramanian, K, Marikani, A and Marimuthu, S (2011) Copper nanoparticles synthesized by polyol process used to control hematophagous parasites. Parasitology Research 109(5), 14031415.CrossRefGoogle ScholarPubMed
Rashid, MMO, Ferdous, J, Banik, S, Islam, MR, Uddin, AHMM and Robel, FN (2016) Anthelmintic activity of silver-extract nanoparticles synthesized from the combination of silver nanoparticles and M. charantia fruit extract. BMC Complementary and Alternative Medicine 16(1), 16.CrossRefGoogle ScholarPubMed
Reinecke, SA and Reinecke, AJ (2004) The comet assay as biomarker of heavy metal genotoxicity in earthworms. Archives of Environmental Contamination and Toxicology 46(2), 208215.CrossRefGoogle ScholarPubMed
Shirvan, SP, Movassaghi, A, Khakzad, MR and Abd El Hameed, AM (2016) A preliminary study on the protein profile of Marshallagia marshalli. Scientia Parasitologica 17(3/4), 6368.Google Scholar
Singh, NP, McCoy, MT, Tice, RR and Schneider, EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research 175(1), 184191.CrossRefGoogle ScholarPubMed
Soneja, A, Drews, M and Malinski, T (2005) Role of nitric oxide, nitroxidative and oxidative stress in wound healing. Pharmacological Reports 57, 108.Google ScholarPubMed
Spector, T (1978) Refinement of the Coomassie blue method of protein quantitation: a simple and linear spectrophotometric assay for ≤0.5 to 50 μg of protein. Analytical Biochemistry 86(1), 142146.CrossRefGoogle Scholar
Stadtman, ER and Levine, RL (2000) Protein oxidation. Annals of the New York Academy of Sciences 899(1), 191208.CrossRefGoogle ScholarPubMed
Taíse, P, Luciana Ferreira, D, Almeida, GNd and Batatinha, MJM (2009) Anthelmintic activity of aqueous extract of Zanthoxylum rhoifolium Lam. leaves (Rutaceae). Revista Brasileira de Parasitologia Veterinária 18, 4348.Google Scholar
Tariq, KA, Chishti, MZ, Ahmad, F and Shawl, AS (2008) Anthelmintic efficacy of Achillea millifolium against gastrointestinal nematodes of sheep: in vitro and in vivo studies. Journal of Helminthology 82(3), 227.CrossRefGoogle ScholarPubMed
Tiwari, R, Chakraborty, S, Dhama, K, Wani, MY, Kumar, A and Kapoor, S (2014) Wonder world of phages: potential biocontrol agents safeguarding biosphere and health of animals and humans-current scenario and perspectives. Pakistan Journal of Biological Sciences: PJBS 17(3), 316328.CrossRefGoogle Scholar
Tomar, RS and Preet, S (2017) Evaluation of anthelmintic activity of biologically synthesized silver nanoparticles against the gastrointestinal nematode, Haemonchus contortus. Journal of Helminthology 91(4), 454.CrossRefGoogle ScholarPubMed