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Journal of Environmental Science and Health, Part A
Toxic/Hazardous Substances and Environmental Engineering
Volume 56, 2021 - Issue 2
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Research Article

Dietary supplementation of garlic, propolis, and wakame improves recuperation in cadmium exposed Japanese medaka fish (Oryzias latipes)

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Pages 199-212 | Received 23 Sep 2020, Accepted 09 Dec 2020, Published online: 27 Dec 2020

References

  • Ali, H.; Khan, E.; Ilahi, I. Environmental and Ecotoxicology of Hazardous Heavy Metals: environmental Persistence, Toxicity, and Bioaccumulation. J. Chem. 2019, 2019, 1–14. DOI: 10.1155/2019/6730305.
  • Moulis, J. M. Cellular Mechanisms of Cadmium Toxicity Related to the Homeostasis of Essential Metals. Biometals. 2010, 23, 877–896. DOI: 10.1007/s10534-010-9336-y.
  • Ammendola, S.; Cerasi, M.; Battistoni, A. Deregulation of Transition Metals Homeostasis is a Key Feature of Cadmium Toxicity in Salmonella. Biometals. 2014, 27, 703–714. DOI: 10.1007/s10534-014-9763-2.
  • Ahad, R. I. A.; Syiem, M. B. Influence of Calcium on Cadmium Uptake and Toxicity to the Cyanobacterium Nostoc Muscorum Meg 1. Biotechnol. Res. Innov. 2019, 3, 231–241. DOI: 10.1016/j.biori.2019.06.002.
  • Choong, G.; Liu, Y.; Templeton, D. M. Interplay of Calcium and Cadmium in Mediating Cadmium Toxicity. Chem. Biol. Interact. 2014, 211, 54–65. DOI: 10.1016/j.cbi.2014.01.007.
  • Vesey, D. A. Transport Pathways for Cadmium in the Intestine and Kidney Proximal Tubule: Focus on the Interaction with Essential Metals. Toxicol. Lett. 2010, 198, 13–19. DOI: 10.1016/j.toxlet.2010.05.004.
  • Zhang, H.; Pang, Z.; Han, C. Undaria Pinnatifida (Wakame): a Seaweed with Pharmacological Properties. Sci. Int. 2014, 2, 32–36.
  • Scandalios, J. G. Oxidative Stress: Molecular Perception and Transduction of Signals Triggering Antioxidant Gene Defenses. Braz. J. Med. Biol. Res. 2005, 38, 995–1014. DOI: 10.1590/s0100-879x2005000700003.
  • Kumar, P.; Singh, A. Cadmium Toxicity in Fish: An Overview. GERF Bull. Biosci. 2010, 1, 41–47.
  • Mosbaha, A.; Guerbe, H.; Boussettaa, H.; Banni, M. Effects of Dietary Garlic against Cadmium Induced Immunotoxicity in Sea Bass Head, Kidney and Liver Tissues: A Transcriptomic Approach. J. Environ. Chem. Toxicol 2017, 1, 9–14.
  • Tandon, S. K.; Singh, S.; Prasad, S. Influence of Garlic on the Disposition and Toxicity of Lead and Cadmium in Rat. Pharmaceut. Biol 2001, 39, 450–454. DOI: 10.1076/phbi.39.6.450.5887.
  • Kamiya, T.; Izumi, M.; Hara, H.; Adachi, T. Propolis Suppresses CdCl2-Induced Cytotoxicity of COS7 Cells through the Prevention of Reactive Oxygen Species Accumulation. Biol. Pharm. Bull 2012, 35, 1126–1131.
  • El-Masry, T. A.; Emara, A. M.; El-Shitany, N. A. Possible Protective Effects of Propolis against Lead-Induced Neurotoxicity in Animal Model. J. Evolut. Biol. Res. 2011, 3, 4–11.
  • Talas, Z. S.; Gulhan, M. F.; Erdogan, K.; Orun, I. Antioxidant Effects of Propolis on Carp Cyprinus Carpio Exposed to Arsenic: Biochemical and Histopathologic Findings. Dis. Aquat. Organ. 2014, 108, 241–249. DOI: 10.3354/dao02714.
  • Yang, H.; Xing, R.; Liu, S.; Li, P. Effect of Fucoxanthin Administration on Thyroid Gland Injury Induced by Cadmium in Mice. Biol. Trace Elem. Res. 2020, in press. doi:10.1007/s12011-020-02291-9.
  • Nishibori, N.; Sagara, T.; Hiroi, T.; Sawaguchi, M.; Itoh, M.; Her, S.; Morita, K. Protective Effect of Undaria Pinnatifida Sporophyll Extract on Iron Induced Cytotoxicity and Oxidative Stress in PC12 Neuronal Cells. Phytopharmacology. 2012, 2, 271–284.
  • Padilla, S.; Cowden, J.; Hinton, D. E.; Yuen, B.; Law, S.; Kullman, S. W.; Johnson, R.; Hardman, R. C.; Flynn, K.; Au, D. W. Use of Medaka in Toxicity Testing. Curr. Protoc. Toxicol. 2009, Chapter 1, Unit1.10
  • Sasado, T.; Tanaka, M.; Kobayashi, K.; Sato, T.; Sakaizumi, M.; Naruse, K. The National BioResource Project Medaka (NBRP Medaka): An Integrated Bioresource for Biological and Biomedical Sciences. Exp. Anim. 2010, 59, 13–23. DOI: 10.1538/expanim.59.13.
  • Ishikawa, Y. Medakafish as a Model System for Vertebrate Developmental Genetics. Bioessays. 2000, 22, 487–495. DOI: 10.1002/(SICI)1521-1878(200005)22:5<487::AID-BIES11>3.0.CO;2-8.
  • Wittbrodt, J.; Shima, A.; Schartl, M. Medaka – A Model Organism from the Far East. Nat. Rev. Genet. 2002, 3, 53–64. [Database] DOI: 10.1038/nrg704.
  • Furusawa, R.; Okinaka, Y.; Nakai, T. Betanodavirus Infection in the Freshwater Model Fish Medaka (Oryzias Latipes). J. General Virol. 2006, 87, 2333–2339. DOI: 10.1099/vir.0.81761-0.
  • Abdallah, M. A. M. Trace Metal Behaviour in Mediterranean-Climate Coastal Bay: El-Mex Bay, Egypt and Its Coastal Environment. Global J. Environ. Res. 2008, 2, 23–29.
  • Ohimain, E.; Jonathan, G.; Abah, S. O. Variations in Heavy Metal Concentrations following the Dredging of an Oil Well Access Canal in the Niger Delta. Adv. Biol. Res. 2008, 2, 97–103.
  • Fakayode, S. O.; Onianwa, P. C. Heavy Metal Contamination of Soil, and Bioaccumulation in guinea Grass (Panicum Maximum) around Ikeja Industrial Estate, Lagos, Nigeria. Environ. Geol. 2002, 43, 145–150.
  • Bradford, M. M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. DOI: 10.1006/abio.1976.9999.
  • Ellman, G. L. Tissue Sulfhydryl Groups. Arch. Biochem. Biophys. 1959, 82, 70–77. DOI: 10.1016/0003-9861(59)90090-6.
  • Ighodaro, O. M.; Akinloye, O. A. First Line Defence Antioxidants-Superoxide Dismutase (SOD), Catalase (CAT) and Glutathione Peroxidase (GPX): Their Fundamental Role in the Entire Antioxidant Defence Grid. Alex. J. Med 2018, 54, 287–293. DOI: 10.1016/j.ajme.2017.09.001.
  • Pavarino, E. C.; Russo, A.; Galbiatti, A. L.; Almeida, W. P.; Bertollo, E. M. Bosynthesis and Mechanism of Action. In Biochemistry and Mechanism of Action; Labrou, N.; Flemetakis, E, Eds.; Nova Science Publishers, Inc: New York, 2013; pp. 1–31.
  • Pizzorno, J. E.; Katzinger, J. J. Glutathione: Physiological and Clinical Relevance. j. Restorat. Med. 2012, 1, 24–37. DOI: 10.14200/jrm.2012.1.1002.
  • Mozsár, A.; Boros, G.; Saly, P.; Antal, L.; Nagy, S. A. Relationship between Fulton’s Condition Factor and Proximate Body Composition in Three Freshwater Fish Species. J. Appl. Ichthyol. 2015, 31, 315–320. DOI: 10.1111/jai.12658.
  • Hopkins, K. D. Reporting Fish Growth: A Review of the Basics. J. World Aquaculture Soc. 1992, 23, 173–179. DOI: 10.1111/j.1749-7345.1992.tb00766.x.
  • Li, Z. H.; Zlabek, V.; Grabic, R.; Li, P.; Machova, J.; Velisek, J.; Randak, T. Effects of Exposure to Sublethal Propiconazole on the Antioxidant Defense System and Na+-K+-ATPase Activity in Brain of Rainbow Trout, Oncorhynchus mykiss. Aquat. Toxicol. 2010, 98, 297–303. DOI: 10.1016/j.aquatox.2010.02.017.
  • Le Cren, E. D. The Length-Weight Relationships and Seasonal Cycle in Gonad Weight and Condition in the Perch (Perca Fluviatilis). J. Anim. Ecol. 1951, 20, 201–219. DOI: 10.2307/1540.
  • Sutton, S. G.; Bult, T. P.; Haedrich, R. L. Relationships among Fat Weight, Body Weight, Water Weight and Condition Factors in Wild Atlantic Salmon Parr. Transactions Am. Fish Soc. 2000, 129, 527–538. DOI: 10.1577/1548-8659(2000)129<0527:RAFWBW>2.0.CO;2.
  • National Research Council (US) Institute for Laboratory Animal Research. Guidance for the Description of Animal Research in Scientific Publications. National Academies Press (US): Washington (DC), 2011. Available from: https://www.ncbi.nlm.nih.gov/books/NBK84210/.
  • Li, H.; Mai, K.; Ai, Q.; Zhang, C.; Zhang, L. Effects of Dietary Squid Viscera Meal on Growth and Cadmium Accumulation in Tissues of Large Yellow Croaker. Front. Agric. China. 2009, 3, 78–83. DOI: 10.1007/s11703-009-0012-3.
  • Miranda, T.; Vieira, L. R.; Guilhermino, L. Neurotoxicity, Behavior, and Lethal Effects of Cadmium, Microplastics, and Their Mixtures on Pomatoschistus Microps Juveniles from Two Wild Populations Exposed under Laboratory Conditions―Implications to Environmental and Human Risk Assessment. Ijerph. 2019, 16, 2857. DOI: 10.3390/ijerph16162857.
  • Abdeltawwab, M.; Wafeek, M.; Elghobashy, H.; Fitzsimmons, K.; Diab, A. S. Response of Nile Tilapia, Oreochromis Niloticus (L.) to Environmental Cadmium Toxicity during Organic Selenium Supplementation. J. World Aquac. Soc. 2010, 41, 106–114. DOI: 10.1111/j.1749-7345.2009.00317.x.
  • Giari, L.; Manera, M.; Simoni, E.; Dezfuli, S. Cellular Alterations in Different Organs of European Sea Bass Dicentrarchus Labrax (L.) Exposed to Cadmium. Chemosphere. 2007, 67, 1171–1181. DOI: 10.1016/j.chemosphere.2006.10.061.
  • Xiong, X.; Li, H.; Qiu, N.; Su, L.; Huang, Z.; Song, L.; Wang, J. Bioconcentration and Depuration of Cadmium in the Selected Tissues of Rare Minnow (Gobiocypris Rarus) and the Effect of Dietary Mulberry Leaf Supplementation on Depuration. Environ. Toxicol. Pharmacol. 2020, 73, 103278. DOI: 10.1016/j.etap.2019.103278.
  • - Fernandes, A.; Rontainhas-Fernandes, A.; Rocha, E.; Reis-Henriques, M. A. The Effect of Paraquat on Hepatic EROD Activity, Liver and Gonadal Histology in Males and Females of Nile Tilapia, Oreochromis Niloticus, Exposed at Different Temperatures. Arch. Environ. Contam. Toxicol. 2006, 51, 626–632.
  • Dang, Z. C.; Berntssen, M. H. G.; Lundebye, A. K.; Flik, G.; Bonga, S. E. W.; Lock, R. A. C. Metallothionein and Cortisol Receptor Expression in Gills of Atlantic Salmon, Salmo Salar, Exposed to Dietary Cadmium. Aquat. Toxicol. 2001, 53, 91–101. DOI: 10.1016/s0166-445x(00)00168-5.
  • Playle, R. C. Modelling Metal Interactions at Fish Gills. Sci. Total Environ. 1998, 219, 147–163. DOI: 10.1016/S0048-9697(98)00232-0.
  • Kim, S. G.; Jee, J. H.; Kang, J. C. Cadmium Accumulation and Elimination in Tissues of Juvenile Olive Flounder, Paralichthys Olivaceus after Sub-Chronic Cadmium Exposure. Environ. Pollut. 2004, 127, 117–123. DOI: 10.1016/s0269-7491(03)00254-9.
  • Boonpeng, S.; Siripongvutikorn, S.; Sae-Wong, C.; Sutthirak, P. The Antioxidant and anti-Cadmium Toxicity Properties of Garlic Extracts. Food Sci Nutr. 2014, 2, 792–801. DOI: 10.1002/fsn3.164.
  • Kay, Y. H.; Yang, W. J.; Kim, H. T.; Lee, Y. D.; Kang, B.; Ryu, J. H.; Jeon, R.; Kim, S. G. Ajoene, a Stable Garlic by-Product, Has an Antioxidant Effect through Nrf2-Mediated Glutamate-Cysteine Ligase Induction in HepG2 Cells and Primary Hepatocytes. J. Nutr. 2010, 140, 1211–1219. DOI: 10.3945/jn.110.121277.
  • Amagase, H. Clarifying the Real Bioactive Constituents of Garlic. J. Nutr. 2006, 136, 716S–725S. DOI: 10.1093/jn/136.3.716S.
  • Robert, V.; Mouillé, B.; Mayeur, C.; Michaud, M.; Blachier, F. Effects of the Garlic Compound Diallyl Disulfide on the Metabolism, Adherence and Cell Cycle of HT-29 Colon Carcinoma Cells: evidence of Sensitive and Resistant Sub-Populations. Carcinogenesis. 2001, 22, 1155–1161. DOI: 10.1093/carcin/22.8.1155.
  • José, P.; Ana, E. G.; Perla, D. M.; Diana, B.; Omar, N. M.; Rogelio, H. P. Diallyl Disulfide Ameliorates Gentamicin-Induced Oxidative Stress and Nephropathy in Rat. Eur. J. Pharmacol. 2003, 473, 71–78.
  • Lawal, O. A.; Elizabeth, M. E. The Chemopreventive Effects of Aged Garlic Extract against Cadmium-Induced Toxicity. Environ. Toxicol. Pharmacol. 2011, 32, 266–274. DOI: 10.1016/j.etap.2011.05.012.
  • Bankova, V.; Christov, R.; Kujumgiev, A.; Marcucci, M. C.; Popov, S. Chemical Composition and Antibacterial Activity of Brazilian Propolis. Z. Naturforsch. C. J. Biosci. 1995, 50, 167–172. DOI: 10.1515/znc-1995-3-402.
  • Ahn, M. R.; Kunimasa, K.; Kumazawa, S.; Nakayama, T.; Kaji, K.; Uto, Y.; Hori, H.; Nagasawa, H.; Ohta, T. Correlation between Antiangiogenic Activity and Antioxidant Activity of Various Components from Propolis. Mol. Nutr. Food Res. 2009, 53, 643–651. DOI: 10.1002/mnfr.200800021.
  • Jung, W. K.; Choi, I.; Lee, D. Y.; Yea, S. S.; Choi, Y. H.; Kim, M. M.; Park, S. G.; Seo, S. K.; Lee, S. W.; Lee, C. M.; et al. Caffeic Acid Phenethyl Ester Protects Mice from Lethal Endotoxin Shock and Inhibits lipopolysaccharide-induced cyclooxygenase-2 and inducible nitric oxide synthase expression in RAW 264.7 macrophages via the p38/ERK and NF-kappaB pathways. Int. J. Biochem. Cell Biol.. 2008, 40, 2572–2582. DOI: 10.1016/j.biocel.2008.05.005.
  • Kujumgiev, A.; Tsvetkova, I.; Serkedjieva, Y.; Bankova, V.; Christov, R.; Popov, S. Antibacterial, Antifungal and Antiviral Activity of Propolis of Different Geographic Origin. J. Ethnopharmacol. 1999, 64, 235–240. DOI: 10.1016/s0378-8741(98)00131-7.
  • Watabe, M.; Hishikawa, K.; Takayanagi, A.; Shimizu, N.; Nakaki, T. Caffeic Acid Phenethyl Ester Induces Apoptosis by Inhibition of NFkappaB and Activation of Fas in Human Breast Cancer MCF-7 Cells. J. Biol. Chem. 2004, 279, 6017–6026. DOI: 10.1074/jbc.M306040200.
  • Sato, M.; Hosokawa, T.; Yamaguchi, T.; Nakano, T.; Muramoto, K.; Kahara, T.; Funayama, K.; Kobayashi, A.; Nakano, T. Angiotensin I-Converting Enzyme Inhibitory Peptides Derived from Wakame (Undaria Pinnatifida) and Their Antihypertensive Effect in Spontaneously Hypertensive Rats. J. Agric. Food Chem.. 2002, 50, 6245–6252. DOI: 10.1021/jf020482t.
  • Hu, T.; Liu, D.; Chen, Y.; Wu, J.; Wang, S. Antioxidant Activity of Sulfated Polysaccharide Fractions Extracted from Undaria Pinnitafida in Vitro. Int. J. Biol. Macromol. 2010, 46, 193–198. DOI: 10.1016/j.ijbiomac.2009.12.004.
  • Cakmak, I.; Strbac, D.; Marschner, H. Activities of Hydrogen Peroxide Scavenging Enzymes in Germinated Wheat Seeds. J. Exp. Bot. 1993, 44, 127–132. DOI: 10.1093/jxb/44.1.127.
  • EL-Gazzar, A. M.; Astry, K. E.; El-Sayed, Y. S. Physiological and Oxidative Stress Biomarkers in the Freshwater Nile Tilapia, Oreochromis Niloticus L., Exposed to Sublethal Doses of Cadmium. Alex. J. Vet. Sci. 2014, 40, 29–43.
  • Mehrpak, M.; Banaee, M.; Haghi, B. N.; Noori, A. Protective Effects of Vitamin C and Chitosan against Cadmium-Induced Oxidative Stress in the Liver of Common Carp (Cyprinus Carpio). Iranian J. Toxicol. 2015, 9, 1360–1367.
  • Banaee, M.; Mehrpak, M.; Haghi, B. N.; Noori, A. Amelioration of Cadmium-Induced Changes in Biochemical Parameters of the Muscle of Common Carp (Cyprinus Carpio) by Vitamin C and Chitosan. Int. J. Aquat. Biol. 2015, 2, 362–371.
  • Silvagno, F.; Vernone, A.; Pescarmona, P. The Role of Glutathione in Protecting against the Severe Inflammatory Response Triggered by COVID-19. Antioxidants. 2020, 9, 624. DOI: 10.3390/antiox9070624.
  • Forman, H. J.; Zhang, H.; Rinna, A. Glutathione: Overview of Its Protective Roles, Measurement, and Biosynthesis. Mol. Aspects Med. 2009, 30, 1–12.
  • Feoli, A. M.; Siqueira, I.; Almeida, L. M.; Tramontina, A. C.; Battu, C.; Wofchuk, S. T.; Gottfried, C.; Perry, M. L.; Gonçalves, C. A. Brain Glutathione Content and Glutamate Uptake Are Reduced in Rats Exposed to Pre- and Postnatal Protein Malnutrition. J. Nutr. 2006, 136, 2357–2361. DOI: 10.1093/jn/136.9.2357.
  • López-López, A. L.; Jaime, H. B.; Escobar-Villanueva, M. D. C.; Padilla, M. B.; Palacios, G. V.; Aguilar, F. J. A. Chronic Unpredictable Mild Stress Generates Oxidative Stress and Systemic Inflammation in Rats. Physiol. Behav. 2016, 161, 15–23. DOI: 10.1016/j.physbeh.2016.03.017.
  • Babula, P.; Masarik, M.; Adam, V.; Eckschlager, T.; Stiborova, M.; Trnkova, L.; Skutkova, H.; Provaznik, I.; Hubalek, J.; Kizek, R. Mammalian Metallothioneins: properties and Functions. Metallomics. 2012, 4, 739–750. DOI: 10.1039/c2mt20081c.
  • Carginale, V.; Scudiero, R.; Capasso, C.; Capasso, A.; Kille, P.; di Prisco, G.; Parisi, E. Cadmium-Induced Differential Accumulation of Metallothionein Isoforms in the Antarctic Icefish, Which Exhibits No Basal Metallothionein Protein but High Endogenous mRNA Levels. Biochem. J. 1998, 332, 475–481. DOI: 10.1042/bj3320475.
  • Gaschler, M. M.; Stockwell, B. R. Lipid Peroxidation in Cell Death. Biochem. Biophys. Res. Commun. 2017, 482, 419–425. DOI: 10.1016/j.bbrc.2016.10.086.
  • Bhadauria, M.; Shukla, S.; Mathur, R.; Agrawal, O. P.; Shrivastava, S.; Johri, S.; Joshi, D.; Singh, V.; Mittal, D.; Nirala, K. S. Hepatic Endogenous Defense Potential of Propolis after Mercury Intoxication. Integr. Zool. 2008, 3, 311–321. DOI: 10.1111/j.1749-4877.2008.00103.x.
  • Bechard, K. M.; Gillis, P. L.; Wood, C. M. Trophic Transfer of Cd from Larval Chironomids (Chironomus Riparius) Exposed via sediment or waterborne routes, to zebrafish (Danio rerio): tissue-specific and subcellular comparisons. Aquat. Toxicol. 2008, 90, 310–321. DOI: 10.1016/j.aquatox.2008.07.014.
  • Yagi, K. Lipid Peroxides, Free Radicals, and Diseases. In Active Oxygen, Lipid Peroxides, and Antioxidants; Yagi, K, Ed.; Japan Scientific Press: Tokyo, 1993; pp. 39–67.
  • Halliwell, B.; Gutterridge, J. M. C. Free Radicals in Biology and Medicine; Clarendon (Oxford) Press: Oxford, 1989; pp.188–276.
  • Cross, C. E.; Halliwell, B.; Borish, E. T.; Pryor, W. A.; Ames, B. N.; Saul, R. L.; McCord, J. M.; Harman, D. Oxygen Radicals and Human Diseases. Ann. Intern. Med. 1987, 107, 526–545. DOI: 10.7326/0003-4819-107-4-526.
  • Pérez-Torres, I.; Torres-Narváez, J.; Pedraza-Chaverri, J.; Rubio-Ruiz, M.; Díaz-Díaz, E.; del Valle-Mondragón, L.; Martínez-Memije, R.; Varela López, E.; Guarner-Lans, V. Guarner-Lans, V. Effect of the Aged Garlic Extract on Cardiovascular Function in Metabolic Syndrome Rats. Molecules. 2016, 21, 1425. DOI: 10.3390/molecules21111425.

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