A caffeine-supplemented diet modulates oxidative stress markers and prevents oxidative damage in the livers of Nile tilapia (Oreochromis niloticus) exposed to hypoxia
Recent evidence has revealed the involvement of oxidative stress and oxidative damage with health impairment and mortality in fish exposed to hypoxia. Thus, natural compounds with antioxidant and free-radical-scavenging properties, such as caffeine, might help to prevent or reduce hepatic damage elicited by hypoxia. Thus, the aim of this study was to evaluate whether dietary supplementation with caffeine could prevent or reduce oxidative damage in the livers of Nile tilapia (Oreochromis niloticus) exposed to hypoxia. Hepatic reactive oxygen species, lipid peroxidation levels, and xanthine oxidase (XO) activity were higher in fish exposed to hypoxia compared with normoxia. Hepatic catalase, glutathione peroxidase, and glutathione S-transferase activities, as well as the antioxidant capacity against peroxyl radical levels, were lower in fish exposed to hypoxia compared with normoxia. No significant difference between groups was observed regarding hepatic superoxide dismutase activity. Dietary supplementation with 8% caffeine prevented all alterations elicited by hypoxia. Based on this evidence, the use of dietary supplementation with 8% caffeine can be an interesting approach to preventing hepatic lipid damage and impairment of the antioxidant defense system elicited by hypoxia, and this effect can be mediated by protective effects on XO activity.
Keywords1,3,5-Trimethylxanthine Antioxidant status Lipid damage Xanthine oxidase
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001 - PhD fellowships to C.F. Souza and M.D. Baldissera. A. S. Da Silva and B. Baldisserotto are funded by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) research fellowships and S.N. Descovi by a FAPERGS (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul) undergraduate fellowship.
Compliance with ethical standards
All procedures were approved by the Ethical and Animal Welfare Committee of the Universidade do Estado de Santa Catarina (protocol 9959260218).
Conflict of interest
The authors declare that they have no conflict of interest.
- Abdel-Tawwab M, Samir F, Abd El-Naby AS, Monier MN (2018) Antioxidative and immunostimulatory effect of dietary cinnamon nanoparticles on the performance of Nile tilapia, Oreochromis niloticus (L.) and its susceptibility to hypoxia stress and Aeromonas hydrophila infection. Fish Shellfish Immunol 74:19–25CrossRefGoogle Scholar
- Dolci GS, Rosa HZ, Vey LT, Pase CS, Barcelos RCS, Dias VT, Loebens L, Dalla Vecchia P, Bizzi CA, Baldisserotto B, Burger ME (2017) Could hypoxia acclimation cause morphological changes and protect against Mn-induced oxidative injuries in silver catfish (Rhamdia quelen) even after reoxygenation? Environ Pollut 224:466–475CrossRefGoogle Scholar
- Doleski PH, Leal DBR, Machado VS, Bottari NB, Casali EA, Moritz CEJ, Camillo G, Vogel FF, Stefani LM, da Silva AS (2017) Hepatic xanthine oxidase activity and purine nucleoside levels as physiological mediators to analyze a subcutaneous treatment with (PhSe)2 in mice infected by Toxoplasma gondii. Microb Pathog 104:180–183CrossRefGoogle Scholar
- Gibbs BF, Silva IG, Prokhorov A, Abooali M, Yasinska IM, Casely-Hayford MA, Berger SM, Fasler-Kan E (2015) Caffeine affects the biological responses of human hematopoietic cells of myeloid lineage via downregulation of the mTOR pathway and xanthine oxidase activity. Oncotarget 6:28678–28692CrossRefGoogle Scholar
- Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
- Johannsson OE, Giacomin M, Sadauskaus-Henrique H, Campos DF, Braz-Mota S, Heinrichs-Caldas WD, Baptista R, Wood CM, Almeida-Val VMF, Val AL (2018) Does hypoxia or different rates of re-oxygenation after hypoxia induce an oxidative stress response in Cyphocharax abramoides (Kner 1858), a Characidfish of the Rio Negro? Comp Biochem Physiol Part A 224:53–67CrossRefGoogle Scholar
- León-Carmona JR, Galano A (2011) Is caffeine a good scavenger of oxygenated free radicals? J Phys Chem B 115:4583–4546Google Scholar
- Magnoni LJ, Martos-Sitcha JA, Queiroz A, Calduch-Giner JA, Gonçalves JFM, Rocha CMR, Abreu HT, Schrama JW, Ozorio ROA, Perez-Sanchez J (2017) Dietary supplementation of heat-treated Gracilaria and Ulva seaweeds enhanced acute hypoxia tolerance in gilthead sea bream (Sparus aurata). Biol Open 6:897–908Google Scholar
- Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocytes glutathione peroxidase. J Lab Clin Med 70:158–169Google Scholar
- Ribeiro PAP, Miranda-Filho C, De Melo DC, Luz RK (2015) Efficiency of eugenol as anesthetic for the early life stages of Nile tilapia (Oreochromis niloticus). Annals Braz Acad Sci 87:529–535Google Scholar
- Roth E, Marczin N, Balatonyi GS, Kovacs V, Alotti N, Borsiczky B, Gasz B (2011) Effect of a glutathione S-transferase inhibitor on oxidative stress and ischemia-reperfusion-induced apoptotic signalling of cultured cardiomyocytes. Exp Clin Cardiol 16:92–96Google Scholar
- Souza CF, Baldissera MD, Bianchini AE, da Silva EG, Mourão RHV, da Silva LVF, Schmidt D, Heinzmann BM, Baldisserotto B (2018) Citral and linalool chemotypes of Lippia alba essential oil as anesthetics for fish: a detailed physiological analysis of side effects during anesthetic recovery in silver catfish (Rhamdia quelen). Fish Physiol Biochem 44:21–34CrossRefGoogle Scholar
- Vieira JM, Carvalho FB, Gutierres JM, Soares MSP, Oliveira PS, Rubin MA, Morsch VM, Schetinger MR, Spanevello RM (2017) Caffeine prevents high-intensity exercise-induced increase in enzymatic antioxidant and Na+-K+-ATPase activities and reduction of anxiolytic like-behaviour in rats. Redox Rep 22:493–500CrossRefGoogle Scholar
- Wang Y, Zhang J, Zeng L (2018) β-Glucan decreases intensity of hypoxia-induced oxidative stress in large yellow croaker (Larimichthys crocea) and its corresponding mechanisms. J Fish China 42:828–837Google Scholar
- Zhao Y, Di G, Kong X, Zhang J, Li L, Nie G, Li X (2016) Effect on antioxidant defense in hepatopancreas of Carassius auratus after poly I: C injection under hypoxia. J Fish China 40:1830–1841Google Scholar