Issue
Variations in the lipid peroxidation and antioxidant biomarkers in some tissues of anadromous cyprinid fish during migration
Corresponding Author(s) : Burak Kaptaner
Cellular and Molecular Biology,
Vol. 65 No. 3: Issue 3
Abstract
Alburnus tarichi is an endemic fish species inhabiting the Lake Van basin of Turkey. This anadromous cyprinid fish migrates for spawning to the freshwater inlets pouring into Lake Van, which has highly alkaline and brackish water. During the migration, the fish moves to a new habitat from a different habitat and encounters many challenges. The objective of the present study is to investigate whether antioxidant responses occur in the tissues of A. tarichi during its anadromous migration. To this end, fish were sampled at three different points and in two different periods from the migration route, including in Lake Van at prespawning, at the entrance of a freshwater stream (Karasu) at spawning and in the upstream of the freshwater stream at spawning. Malondialdehyde (MDA) content and antioxidant defenses including activities of the enzymes superoxide dismutase, glutathione peroxidase, glutathione-S-transferase and catalase and the level of glutathione were assayed in liver, gill, white muscle, trunk kidney and anterior intestine tissues. Our results showed increased MDA levels in liver, white muscle and anterior intestine and tissue-specific antioxidant responses in the freshwater environment. This study reports that alterations occurred in the antioxidant defense system indicators in the tissues of anadromous cyprinid fish during migration and that the antioxidant defenses might reflect an important role in spawning migration that ultimately leads to accomplishment of reproductive activity.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- Birnie"Gauvin K, Costantini D, Cooke SJ, Willmore WG. A comparative and evolutionary approach to oxidative stress in fish: a review. Fish Fish 2017a; 18:928–42.
- Benzie IF. Evolution of antioxidant defence mechanisms. Eur J Nutr 2000; 39:53–61.
- Lushchak VI. Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 2011; 101:13-30.
- Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J 2012; 5:9-19.
- Birnie-Gauvin K, Peiman KS, Larsen MH, Baktoft H, Aarestrup K, Willmore WG et al. Oxidative stress and partial migration in brown trout (Salmo trutta). Can J Zool 2017b; 95:829–35.
- Costantini D, Cardinale M, Carere C. Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp Biochem Physiol C Toxicol Pharmacol 2007; 144:363–71.
- Costantini D. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 2008; 11:1238–51.
- Alonso"Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G. Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 2004; 7:363–68.
- Wilson SM, Taylor JJ, Mackie TA, Patterson DA, Cooke SJ, Willmore WG. Oxidative stress in Pacific salmon (Oncorhynchus spp.) during spawning migration. Physiol Biochem Zool 2014; 87:346-52.
- Danulat E, Selcuk B. Life history and environmental conditions of the anadromous Chalcalburnus tarichi (Cyprinidae) in the highly alkaline lake Van, Eastern Anatolia, Turkey. Arch Hydrobiol 1992; 126:105-25.
- Danulat E. Biochemical-physiological adaptations of teleosts to highly alkaline, saline lakes. In: Biochemistry and Molecular Biology of Fishes, Elsevier, 1995, Vol. 5, pp. 229-249).
- Sari M. Threatened fishes of the world: Chalcalburnus tarichi (Pallas 1811) (Cyprinidae) living in the highly alkaline lake Van, Turkey. Environ Biol Fishes 2008; 81:21-23.
- íœnal G, í‡etinkaya O, Elp M. Histological investigation of gonad development of Chalcalburnus tarichi (P., 1811). Tr J Zool 1999; 23:329-38.
- Kaptaner B, Kankaya E. Analysis of germ cell proliferation, apoptosis, and androgenesis in the Lake Van fish (Chalcalburnus tarichi) during testicular development. Fish Physiol Biochem 2013; 39:1165-79.
- Jain SK, McVie R, Duett J, Herbst JJ. Erythrocyte membrane lipid peroxidation and glycolylated hemoglobin in diabetes. Diabetes 1989; 38:1539-43.
- Aebi H. Catalase. In: Methods of Enzymatic Analysis. Bergemeyer HU (Ed.), Academic Press, NewYork, 1974, pp.673–684.
- Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70:158–69.
- Beutler E. Red cell metabolism. In: A Manual of Biochemical Methods, Third ed. Grune and Startton, New York,1984, pp 105–106.
- Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974; 249:7130−39.
- Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–54.
- í‡etinkaya O, Sarı M, Åžen F, Arabacı M, Duyar HA. Limnological characteristics of Karasu river inflowing lake Van. YYU J Agr Sci 1994; 4:151–68.
- Kempe S, Khoo F, Gurleyik Y. Hydrograpy of lake Van and its drainage area. E.T. Degens and F. Kurtman, The geology of lake Van. M.T.A., No:169, 1978, Ankara, 158 pp.
- Tugrul S, Dumlu G, Baştürk í–, ć°lhal C, Balkas T. Van gölü özümleme kapasitesinin saptanması ve evsel nitelikli atıksu arıtımı ve deşarjı optimizasyonu. ć°ller Bank. Gen. Müd. ve TUBITAK Marmara Arş. Enst. Ortak Projesi, No.0730018301, Yayın No: 145, Gebze, 1984, 183 s.
- Arabacı M, Cağırgan H, Sarı M, Åžekeroğlu R. Serum ionic content of endemic Chalcalburnus tarichi during spawning, prespawning and postspawning terms, living in highly alkaline waters of Lake Van (pH 9.8), Turkey. Turk J Fish Aquat Sci 2001; 1:53–57.
- Kaptaner B. Relation between increased oxidative stress and histological abnormalities in the ovaries of Alburnus tarichi in Lake Van, Turkey. Environ Monit Assess 2015; 187:702.
- Kaptaner B, Kankaya E, Dogan A, Durmuş A. Histological alterations and oxidative stress in the testes of the pearl mullet (Alburnus tarichi) in Lake Van, Turkey. Environ Monit Assess 2016; 188:474.
- Atici AA, Elp M, Åžen F. The effects of sand pits and sand extractions region on Karasu stream (Van) to water quality criteria. Fresen Environ Bull 2018; 27:6583–90.
- Arihan O, Kaptaner B, Kankaya E. Erythrocyte fragility in pearl mullet (Alburnus tarichi Guldenstadt, 1814) during migration from highly alkaline water to freshwater. Fresen Environ Bull 2017; 26:2325–29.
- Welker TL, Congleton JL. Oxidative stress in migrating spring Chinook salmon smolts of hatchery origin: changes in vitamin E and lipid peroxidation. Trans Am Fish Soc 2005; 134(6):1499-1508.
- Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 1990; 9:515–40.
- Tocher DR. Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 2003; 11:107–84.
- Rí¸jbek MC, Jacobsen C, Tomkiewicz J, Stí¸ttrup JG. Linking lipid dynamics with the reproductive cycle in Baltic cod Gadus morhua. Mar Ecol Prog Ser 2012; 71:215–34.
- Penney ZL, Moffitt CM. Fatty"acid profiles of white muscle and liver in stream"maturing steelhead trout Oncorhynchus mykiss from early migration to kelt emigration. J Fish Biol 2015; 86:105–20.
- de Zwart LL, Meerman JH,. Commandeur JN, Vermeulen NP. Biomarkers of free radical damage: applications in experimental animals and in humans. Free Radic Biol Med 1999; 26(1–2):202–26.
- Hernández-Aguilar SB, Zenteno-Savin T, De-Anda-Montañez JA, Méndez-Rodríguez LC. Temporal variation in oxidative stress indicators in liver of totoaba (Totoaba macdonaldi) Perciformes: Sciaenidae. J Mar Biol Assoc UK 2018; 98:833–44.
- Miller KM, Schulze AD, Ginther N, Li S, Patterson DA, Farrell AP, Hinch SG. Salmon spawning migration: metabolic shifts and environmental triggers. Comp Biochem Physiol Part D 2009; 4:75-89.
- Leary SC, Lyons CN, Rosenberger AG, Ballantyne JS, Stillman J, Moyes CD. Fiber-type differences in muscle mitochondrial profiles. Am J Physiol Regul Integr Comp Physiol 2003; 285:R817-R826.
- Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008; 88:1243–76.
- Weber JM. The physiology of long-distance migration: extending the limits of endurance metabolism. J Exp Biol 2009; 212:593-97.
- Taylor JR, Grosell M. Feeding and osmoregulation: dual function of the marine teleost intestine. J Exp Biol 2006; 209(15):2939–51.
- Takahashi H, Sakamoto T, Narita K. Cell proliferation and apoptosis in the anterior intestine of an amphibious, euryhaline mudskipper (Periophthalmus modestus). J Comp Physiol B 2006a; 176:463–68.
- Ferrando S, Ferrando T, Girosi L, Mauceri A, Fasulo S, Tagliafierro G. Apoptosis, cell proliferation and serotonin immunoreactivity in gut of Liza aurata from natural heavy metal polluted environments: preliminary observations. Eur J Histochem 2005; 49:331–40.
- Takahashi H, Takahashi A, Sakamoto T. In vivo effects of thyroid hormone, corticosteroids and prolactin on cell proliferation and apoptosis in the anterior intestine of the euryhaline mudskipper (Periophthalmus modestus). Life Sci 2006b; 79:1873–80.
- Wilhelm Filho D, Tribess T, Gaspari C, Claudio FD, Torres MA, Magalhaes AR. Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 2001; 203:149-58.
- Verlecar XN, Jena KB, Chainy GB. Seasonal variation of oxidative biomarkers in gills and digestive gland of green-lipped mussel Perna viridis from Arabian Sea. Estuar Coast Shelf Sci 2008; 76:745-52.
- Martinez-Alvarez RM, Hidalgo MC, Domezain A, Morales AE, García-Gallego M, Sanz A. Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 2002, 205:3699-706.
- Parihar MS, Dubey AK. Lipid peroxidation and ascorbic acid status in respiratory organs of male and female freshwater catfish Heteropneustes fossilis exposed to temperature increase. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1995; 112:309–13.
- Hermes-Lima M. Oxygen in biology and biochemistry: role of free radicals. In: Functional Metabolism: Regulation Adaptation, Storey KB (Ed), 2004, pp. 319–368.
- Pandey S, Parvez S, Sayeed I, Haque R, Hafeez BB, Raisuddin S. Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.). Sci Total Environ 2003; 309:105–15.
- Kaptaner B, Kankaya E, Doğan A, í‡elik ć°. Histopathology and oxidative stress in the liver of Chalcalburnus tarichi living in lake Van, Turkey. Life Sci J 2014, 11:66ï€77.
- Dimitrova MST, Tsinova V, Velcheva V. Combined effect of zinc and lead on the hepatic superoxide dismutase-catalase system in carp (Cyprinus carpio). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1994; 108:43–46.
- Bagnyukova TV, Chahrak OI, Lushchak VI. Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 2006; 78:325–31.
- Wilhelm Filho D, Giulivi C, Boveris A. Antioxidant defences in marine fish”I. Teleosts. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1993; 106:409ï€13.
- Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J. Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 2003; 145:191–99.
- Furné M, García"Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A, Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquac Nutr 2009; 15:587–95.
- Bayir A, Sirkecioglu AN, Bayir M, Haliloglu HI, Kocaman EM, Aras NM. Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defenses. Comp Biochem Physiol B Biochem Mol Biol 2011; 59:191–96.
- Rivera-Ingraham GA, Barri K, Boí«l M, Farcy E, Charles AL, Geny B, Lignot JH. Osmoregulation and salinity-induced oxidative stress: is oxidative adaptation determined by gill function?. J Exp Biol 2016; 219:80–89.
- Van der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 2003; 13:57-149.
- Grim JM, Hyndman KA, Kriska T, Girotti AW, Crockett EL. Relationship between oxidizable fatty acid content and level of antioxidant glutathione peroxidases in marine fish. J Exp Biol 2011, 214:3751–59.
- Choi CY, An KW, An MI. Molecular characterization and mRNA expression of glutathione peroxidase and glutathione S-transferase during osmotic stress in olive flounder (Paralichthys olivaceus). Comp Biochem Physiol A Mol Integr Physiol 2008, 149:330–37.
- Vaglio A, Landriscina C. Changes in liver enzyme activity in the teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 1999; 43:111-16.
- Liu Y, Wang WN, Wang AL, Wang JM, Sun RY. Effects of dietary vitamin E supplementation on antioxidant enzyme activities in Litopenaeus vannamei (Boone, 1931) exposed to acute salinity changes. Aquaculture 2007; 265:351-58.
- Sheehan D, Meade G, Foley VM, Dowd CA. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. The Biochem J 2001; 360:1ï€16 .
- Pavlović SZ, Borković-Miti S, Gavrilovi B, Despotovi SG, Gavri JP, Saii ZS. Seasonal changes of oxidative stress biomarkers in white muscle of longfin gurnard (Chelidonychthys obscurus) from the Adriatic Sea. Water Res Manag 2013; 23:19–25.
- Bebianno MJ, Lopes B, Guerra L, Hoarau P, Ferreira AM. Glutathione S-tranferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. Environ Int 2007; 33:550–58.
- Pavlović SZ, Borković SS, Kovacevic TB, Ognjanović BI, Zikić RV, Stajn AS, Saicić ZS. Antioxidant defense enzyme activities in the liver of red mullet (Mullus barbatus L.) from the Adriatic Sea: the effects of locality and season. Fresen Environ Bull 2008; 17:558–63.
- Aras NM, Bayir A, Sirkecioglu AN, Bayir M, Aksakal E, Haliloglu HI. Seasonal changes in antioxidant defence system of liver and gills of Salmo trutta caspius, Salmo trutta labrax and Salmo trutta macrostigma. J Fish Biol 2009; 74:842–56.
- Lushchak VI, Bagnyukova TV, Husak VV, Luzhna LI, Lushchak V, Storey KB. Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. Int J Biochem Cell Biol 2005; 37:1670-80.
- Stephensen E, Sturve J, Forlin L. Effects of redox cycling compounds on glutathione content and activity of glutathione-related enzymes in rainbow trout liver. Comp Biochem Physiol C Toxicol Pharmacol 2002; 133:435–42.
- Gorbi S, Baldini C, Regoli F. Seasonal variability of metallothioneins, cytochrome P450, bile metabolites and oxyradical metabolism in the European eel Anguilla anguilla L. (Anguillidae) and striped mullet Mugil cephalus L. (Mugilidae). Arch Environ Contam Toxicol 2005; 49:62–70.
References
Birnie"Gauvin K, Costantini D, Cooke SJ, Willmore WG. A comparative and evolutionary approach to oxidative stress in fish: a review. Fish Fish 2017a; 18:928–42.
Benzie IF. Evolution of antioxidant defence mechanisms. Eur J Nutr 2000; 39:53–61.
Lushchak VI. Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 2011; 101:13-30.
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J 2012; 5:9-19.
Birnie-Gauvin K, Peiman KS, Larsen MH, Baktoft H, Aarestrup K, Willmore WG et al. Oxidative stress and partial migration in brown trout (Salmo trutta). Can J Zool 2017b; 95:829–35.
Costantini D, Cardinale M, Carere C. Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp Biochem Physiol C Toxicol Pharmacol 2007; 144:363–71.
Costantini D. Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 2008; 11:1238–51.
Alonso"Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G. Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 2004; 7:363–68.
Wilson SM, Taylor JJ, Mackie TA, Patterson DA, Cooke SJ, Willmore WG. Oxidative stress in Pacific salmon (Oncorhynchus spp.) during spawning migration. Physiol Biochem Zool 2014; 87:346-52.
Danulat E, Selcuk B. Life history and environmental conditions of the anadromous Chalcalburnus tarichi (Cyprinidae) in the highly alkaline lake Van, Eastern Anatolia, Turkey. Arch Hydrobiol 1992; 126:105-25.
Danulat E. Biochemical-physiological adaptations of teleosts to highly alkaline, saline lakes. In: Biochemistry and Molecular Biology of Fishes, Elsevier, 1995, Vol. 5, pp. 229-249).
Sari M. Threatened fishes of the world: Chalcalburnus tarichi (Pallas 1811) (Cyprinidae) living in the highly alkaline lake Van, Turkey. Environ Biol Fishes 2008; 81:21-23.
íœnal G, í‡etinkaya O, Elp M. Histological investigation of gonad development of Chalcalburnus tarichi (P., 1811). Tr J Zool 1999; 23:329-38.
Kaptaner B, Kankaya E. Analysis of germ cell proliferation, apoptosis, and androgenesis in the Lake Van fish (Chalcalburnus tarichi) during testicular development. Fish Physiol Biochem 2013; 39:1165-79.
Jain SK, McVie R, Duett J, Herbst JJ. Erythrocyte membrane lipid peroxidation and glycolylated hemoglobin in diabetes. Diabetes 1989; 38:1539-43.
Aebi H. Catalase. In: Methods of Enzymatic Analysis. Bergemeyer HU (Ed.), Academic Press, NewYork, 1974, pp.673–684.
Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967; 70:158–69.
Beutler E. Red cell metabolism. In: A Manual of Biochemical Methods, Third ed. Grune and Startton, New York,1984, pp 105–106.
Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 1974; 249:7130−39.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–54.
í‡etinkaya O, Sarı M, Åžen F, Arabacı M, Duyar HA. Limnological characteristics of Karasu river inflowing lake Van. YYU J Agr Sci 1994; 4:151–68.
Kempe S, Khoo F, Gurleyik Y. Hydrograpy of lake Van and its drainage area. E.T. Degens and F. Kurtman, The geology of lake Van. M.T.A., No:169, 1978, Ankara, 158 pp.
Tugrul S, Dumlu G, Baştürk í–, ć°lhal C, Balkas T. Van gölü özümleme kapasitesinin saptanması ve evsel nitelikli atıksu arıtımı ve deşarjı optimizasyonu. ć°ller Bank. Gen. Müd. ve TUBITAK Marmara Arş. Enst. Ortak Projesi, No.0730018301, Yayın No: 145, Gebze, 1984, 183 s.
Arabacı M, Cağırgan H, Sarı M, Åžekeroğlu R. Serum ionic content of endemic Chalcalburnus tarichi during spawning, prespawning and postspawning terms, living in highly alkaline waters of Lake Van (pH 9.8), Turkey. Turk J Fish Aquat Sci 2001; 1:53–57.
Kaptaner B. Relation between increased oxidative stress and histological abnormalities in the ovaries of Alburnus tarichi in Lake Van, Turkey. Environ Monit Assess 2015; 187:702.
Kaptaner B, Kankaya E, Dogan A, Durmuş A. Histological alterations and oxidative stress in the testes of the pearl mullet (Alburnus tarichi) in Lake Van, Turkey. Environ Monit Assess 2016; 188:474.
Atici AA, Elp M, Åžen F. The effects of sand pits and sand extractions region on Karasu stream (Van) to water quality criteria. Fresen Environ Bull 2018; 27:6583–90.
Arihan O, Kaptaner B, Kankaya E. Erythrocyte fragility in pearl mullet (Alburnus tarichi Guldenstadt, 1814) during migration from highly alkaline water to freshwater. Fresen Environ Bull 2017; 26:2325–29.
Welker TL, Congleton JL. Oxidative stress in migrating spring Chinook salmon smolts of hatchery origin: changes in vitamin E and lipid peroxidation. Trans Am Fish Soc 2005; 134(6):1499-1508.
Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 1990; 9:515–40.
Tocher DR. Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 2003; 11:107–84.
Rí¸jbek MC, Jacobsen C, Tomkiewicz J, Stí¸ttrup JG. Linking lipid dynamics with the reproductive cycle in Baltic cod Gadus morhua. Mar Ecol Prog Ser 2012; 71:215–34.
Penney ZL, Moffitt CM. Fatty"acid profiles of white muscle and liver in stream"maturing steelhead trout Oncorhynchus mykiss from early migration to kelt emigration. J Fish Biol 2015; 86:105–20.
de Zwart LL, Meerman JH,. Commandeur JN, Vermeulen NP. Biomarkers of free radical damage: applications in experimental animals and in humans. Free Radic Biol Med 1999; 26(1–2):202–26.
Hernández-Aguilar SB, Zenteno-Savin T, De-Anda-Montañez JA, Méndez-Rodríguez LC. Temporal variation in oxidative stress indicators in liver of totoaba (Totoaba macdonaldi) Perciformes: Sciaenidae. J Mar Biol Assoc UK 2018; 98:833–44.
Miller KM, Schulze AD, Ginther N, Li S, Patterson DA, Farrell AP, Hinch SG. Salmon spawning migration: metabolic shifts and environmental triggers. Comp Biochem Physiol Part D 2009; 4:75-89.
Leary SC, Lyons CN, Rosenberger AG, Ballantyne JS, Stillman J, Moyes CD. Fiber-type differences in muscle mitochondrial profiles. Am J Physiol Regul Integr Comp Physiol 2003; 285:R817-R826.
Powers SK, Jackson MJ. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008; 88:1243–76.
Weber JM. The physiology of long-distance migration: extending the limits of endurance metabolism. J Exp Biol 2009; 212:593-97.
Taylor JR, Grosell M. Feeding and osmoregulation: dual function of the marine teleost intestine. J Exp Biol 2006; 209(15):2939–51.
Takahashi H, Sakamoto T, Narita K. Cell proliferation and apoptosis in the anterior intestine of an amphibious, euryhaline mudskipper (Periophthalmus modestus). J Comp Physiol B 2006a; 176:463–68.
Ferrando S, Ferrando T, Girosi L, Mauceri A, Fasulo S, Tagliafierro G. Apoptosis, cell proliferation and serotonin immunoreactivity in gut of Liza aurata from natural heavy metal polluted environments: preliminary observations. Eur J Histochem 2005; 49:331–40.
Takahashi H, Takahashi A, Sakamoto T. In vivo effects of thyroid hormone, corticosteroids and prolactin on cell proliferation and apoptosis in the anterior intestine of the euryhaline mudskipper (Periophthalmus modestus). Life Sci 2006b; 79:1873–80.
Wilhelm Filho D, Tribess T, Gaspari C, Claudio FD, Torres MA, Magalhaes AR. Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 2001; 203:149-58.
Verlecar XN, Jena KB, Chainy GB. Seasonal variation of oxidative biomarkers in gills and digestive gland of green-lipped mussel Perna viridis from Arabian Sea. Estuar Coast Shelf Sci 2008; 76:745-52.
Martinez-Alvarez RM, Hidalgo MC, Domezain A, Morales AE, García-Gallego M, Sanz A. Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 2002, 205:3699-706.
Parihar MS, Dubey AK. Lipid peroxidation and ascorbic acid status in respiratory organs of male and female freshwater catfish Heteropneustes fossilis exposed to temperature increase. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1995; 112:309–13.
Hermes-Lima M. Oxygen in biology and biochemistry: role of free radicals. In: Functional Metabolism: Regulation Adaptation, Storey KB (Ed), 2004, pp. 319–368.
Pandey S, Parvez S, Sayeed I, Haque R, Hafeez BB, Raisuddin S. Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl. & Schn.). Sci Total Environ 2003; 309:105–15.
Kaptaner B, Kankaya E, Doğan A, í‡elik ć°. Histopathology and oxidative stress in the liver of Chalcalburnus tarichi living in lake Van, Turkey. Life Sci J 2014, 11:66ï€77.
Dimitrova MST, Tsinova V, Velcheva V. Combined effect of zinc and lead on the hepatic superoxide dismutase-catalase system in carp (Cyprinus carpio). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1994; 108:43–46.
Bagnyukova TV, Chahrak OI, Lushchak VI. Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 2006; 78:325–31.
Wilhelm Filho D, Giulivi C, Boveris A. Antioxidant defences in marine fish”I. Teleosts. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1993; 106:409ï€13.
Pascual P, Pedrajas JR, Toribio F, López-Barea J, Peinado J. Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact 2003; 145:191–99.
Furné M, García"Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A, Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquac Nutr 2009; 15:587–95.
Bayir A, Sirkecioglu AN, Bayir M, Haliloglu HI, Kocaman EM, Aras NM. Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defenses. Comp Biochem Physiol B Biochem Mol Biol 2011; 59:191–96.
Rivera-Ingraham GA, Barri K, Boí«l M, Farcy E, Charles AL, Geny B, Lignot JH. Osmoregulation and salinity-induced oxidative stress: is oxidative adaptation determined by gill function?. J Exp Biol 2016; 219:80–89.
Van der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 2003; 13:57-149.
Grim JM, Hyndman KA, Kriska T, Girotti AW, Crockett EL. Relationship between oxidizable fatty acid content and level of antioxidant glutathione peroxidases in marine fish. J Exp Biol 2011, 214:3751–59.
Choi CY, An KW, An MI. Molecular characterization and mRNA expression of glutathione peroxidase and glutathione S-transferase during osmotic stress in olive flounder (Paralichthys olivaceus). Comp Biochem Physiol A Mol Integr Physiol 2008, 149:330–37.
Vaglio A, Landriscina C. Changes in liver enzyme activity in the teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 1999; 43:111-16.
Liu Y, Wang WN, Wang AL, Wang JM, Sun RY. Effects of dietary vitamin E supplementation on antioxidant enzyme activities in Litopenaeus vannamei (Boone, 1931) exposed to acute salinity changes. Aquaculture 2007; 265:351-58.
Sheehan D, Meade G, Foley VM, Dowd CA. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. The Biochem J 2001; 360:1ï€16 .
Pavlović SZ, Borković-Miti S, Gavrilovi B, Despotovi SG, Gavri JP, Saii ZS. Seasonal changes of oxidative stress biomarkers in white muscle of longfin gurnard (Chelidonychthys obscurus) from the Adriatic Sea. Water Res Manag 2013; 23:19–25.
Bebianno MJ, Lopes B, Guerra L, Hoarau P, Ferreira AM. Glutathione S-tranferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. Environ Int 2007; 33:550–58.
Pavlović SZ, Borković SS, Kovacevic TB, Ognjanović BI, Zikić RV, Stajn AS, Saicić ZS. Antioxidant defense enzyme activities in the liver of red mullet (Mullus barbatus L.) from the Adriatic Sea: the effects of locality and season. Fresen Environ Bull 2008; 17:558–63.
Aras NM, Bayir A, Sirkecioglu AN, Bayir M, Aksakal E, Haliloglu HI. Seasonal changes in antioxidant defence system of liver and gills of Salmo trutta caspius, Salmo trutta labrax and Salmo trutta macrostigma. J Fish Biol 2009; 74:842–56.
Lushchak VI, Bagnyukova TV, Husak VV, Luzhna LI, Lushchak V, Storey KB. Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. Int J Biochem Cell Biol 2005; 37:1670-80.
Stephensen E, Sturve J, Forlin L. Effects of redox cycling compounds on glutathione content and activity of glutathione-related enzymes in rainbow trout liver. Comp Biochem Physiol C Toxicol Pharmacol 2002; 133:435–42.
Gorbi S, Baldini C, Regoli F. Seasonal variability of metallothioneins, cytochrome P450, bile metabolites and oxyradical metabolism in the European eel Anguilla anguilla L. (Anguillidae) and striped mullet Mugil cephalus L. (Mugilidae). Arch Environ Contam Toxicol 2005; 49:62–70.