Nutritional status as the key modulator of antioxidant responses induced by high environmental ammonia and salinity stress in European sea bass (Dicentrarchus labrax)

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Sinha, Amit Kumar ^a   AbdElgawad, Hamada ^a,b   Zinta, Gaurav ^a   Dasan, Antony Franklin ^a   Rasoloniriana, Rindra ^a   Asard, Han ^a   Blust, Ronny ^a   De Boeck, Gudrun ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b Beni Suef University   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 METHYLENEDIOXYAMPHETAMINE; AMMONIA; ASCORBATE PEROXIDASE; ASCORBIC ACID; CATALASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; MALONALDEHYDE; SUPEROXIDE DISMUTASE; XANTHINE OXIDASE; ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; SEA WATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; ECOTOXICITY; ENZYME ACTIVITY; EUROPEAN SEA BASS; FOOD INTAKE; HYPOOSMOTIC STRESS; LC50; LIPID PEROXIDATION; LIVER; NONHUMAN; NUTRITIONAL STATUS; OXIDATIVE STRESS; REGULATORY MECHANISM; SALINITY; SALT STRESS; STARVATION; ADAPTATION; ANIMAL; ATLANTIC OCEAN; BASS; CATERING SERVICE; CHEMISTRY; ECOSYSTEM; FOOD DEPRIVATION; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; AMMONIA; ANIMALS; ANTIOXIDANTS; ATLANTIC OCEAN; BASS; CATALASE; ECOSYSTEM; FOOD DEPRIVATION; FOOD SUPPLY; GLUTATHIONE; NUTRITIONAL STATUS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SALINITY; SEAWATER; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE;

EID: 84942342555     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135091     Document Type: Article

References (76)

1. IPCC. Summary for policymakers. In:Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, et al. (Eds.) Climate Change 2013. The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change: Cambridge University Press; 1993.
2. Freeland H, Whitney F. Climatic changes: Gulf of Alaska. In:Sheppard, C. (ed.), Global Issues and Processes, III. Pergamon, Amsterdam, Netherlands; 2000. pp. 179-186.
3. Pierce DW, Gleckler PJ, Barnett TP, Santer BD, Durack PJ. The fingerprint of human-induced changes in the ocean's salinity and temperature fields. Geophys Res Lett. 2012; 39(21): L21704.
4. Wong APS, Bindoff NL,Church JA. Large-scale freshening of intermediate waters in the Pacific and Indian oceans. Nature. 1999; 400 (6743): 440-443.
5. Kelly SP, Woo NYS. The response of sea bream following abrupt hyposmotic exposure. J Fish Biol. 1999; 55(4): 732-750.
6. Roessig JM, Woodley CM, Cech JJ, Hansen LJ. Effects of global climate change on marine and estuarine fishes and fisheries. Rev Fish Biol Fisher. 2004; 14(2): 251-275.
7. Sinha AK, Dasan AF, Rasoloniriana R, Pipralia N, Blust R, De Boeck G. Hypoosmotic stress induced physiological and ion-osmoregulatory responses in European sea bass (Dicentrarchus labrax) are modulated differentially by nutritional status. Comp Biochem Physiol A Mol Integr Physiol. 2015; 181: 87-99. doi: 10.1016/j.cbpa.2014.11.024 PMID: 25483239
8. Yan M, Li Z, Xiong B, Zhu J. Effects of salinity on food intake, growth, and survival of pufferfish (Fugu obscurus). J Appl Ichthyol. 2004; 20(2): 146-149.
9. 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(3): 330-337. doi: 10.1016/j.cbpa.2008.01.013 PMID: 18302988
10. 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(1): 351-358.
11. Livingstone DR. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull. 2001; 42(8): 656-666. PMID: 11525283
12. Yin F, Peng S, Sun P, Shi Z. Effects of low salinity on antioxidant enzymes activities in kidney and muscle of juvenile silver pomfret Pampus argenteus. Acta Ecologica Sinica. 2011; 31(1): 55-60.
13. Dosdat A, Ruyet JP, Coves D, Dutto G, Gasset E, Le Roux A, et al. Effect of chronic exposure to ammonia on growth, food utilization and metabolism of the European sea bass (Dicentrarchus labrax). Aquat Living Resour. 2003; 16(06): 509-520.
14. Sinha AK, Liew HJ, Diricx M, Blust R, De Boeck G. The interactive effects of ammonia exposure, nutritional status and exercise on metabolic and physiological responses in goldfish (Carassius auratus L.). Aquat Toxicol. 2012; 109: 33-46. doi: 10.1016/j.aquatox.2011.11.002 PMID: 22204987
15. Sinha AK, Rasoloniriana R, Dasan AF, Pipralia N, Blust R, De Boeck G. Interactive effect of high environmental ammonia and nutritional status on ecophysiological performance of European sea bass (Dicentrarchus labrax) acclimated to reduced seawater salinities. Aquat Toxicol. 2015; 160: 39-56. doi: 10.1016/j.aquatox.2015.01.005 PMID: 25625520
16. Sinha AK, Liew HJ, Diricx M, Kumar V, Darras VM, Blust R, et al. Combined effects of high environmental ammonia, starvation and exercise on hormonal and ion-regulatory response in goldfish (Carassius auratus L.). Aquat Toxicol. 2012; 114-115: 153-164. doi: 10.1016/j.aquatox.2012.02.027 PMID: 22446827
17. Sinha AK, Matey V, Giblen T, Blust R, De Boeck G. Gill remodeling in three freshwater teleosts in response to high environmental ammonia. Aquat Toxicol. 2014; 155: 166-180. doi: 10.1016/j.aquatox.2014.06.018 PMID: 25033244
18. Bianchini A, Wasielesky W Jr, Miranda Filho KC. Toxicity of nitrogenous compounds to juveniles of flat-fish Paralichthys orbignyanus. Bull Environ Contam Tox. 1996; 56(3): 453-459.
19. Sampaio LA, Wasielesky W, Miranda Filho KC. Effect of salinity on acute toxicity of ammonia and nitrite to juvenile Mugil platanus. Bull Environ Contam Toxicol. 2002; 68(5): 668-674. PMID: 12068932
20. Weirich CR, Tomasso JR, Smith TIJ. Toxicity of ammonia and nitrite to sunshine bass in selected environments. J Aquat Anim Health. 1993; 5(1): 64-72.
21. Weirich CR, Riche MA. Tolerance of juvenile black sea bass Centropristis striata to acute ammonia and nitrite exposure at various salinities. Fish Sci. 2006; 72(5): 915-921.
22. Wise DJ, Tomasso JR. Acute toxicity of nitrite to red drum Sciaenops ocellatus: effect of salinity. J World Aquacult Soc. 1989; 20(4): 193-198.
23. Ching B, Chew SF, Wong WP, Ip YK. Environmental ammonia exposure induces oxidative stress in gills and brain of Boleophthalmus boddarti (mudskipper). Aquat Toxicol. 2009; 95(3): 203-212. doi: 10.1016/j.aquatox.2009.09.004 PMID: 19819034
24. Hegazi MM, Attia ZI, Ashour OA. Oxidative stress and antioxidant enzymes in liver and white muscle of Nile tilapia juveniles in chronic ammonia exposure. Aquat Toxicol. 2010; 99(2): 118-125. doi: 10.1016/j.aquatox.2010.04.007 PMID: 20434782
25. Sun H, Lü K, Minter EJ, Chen Y, Yang Z, Montagnes DJ. Combined effects of ammonia and microcystin on survival, growth, antioxidant responses, and lipid peroxidation of bighead carp Hypophthalmythys nobilis larvae. J Hazard Mater. 2012; 221-222: 213-219. doi: 10.1016/j.jhazmat.2012.04.036 PMID: 22560242
26. Sinha AK, AbdElgawad H, Giblen T, Zinta G, De Rop M, Asard H, et al. Anti-oxidative defences are modulated differentially in three freshwater teleosts in response to ammonia-induced oxidative stress. PLoS One. 2014; 9(4): e95319. doi: 10.1371/journal.pone.0095319 PMID: 24740135
27. Gomi F, Matsuo M. Effects of aging and food restriction on the antioxidant enzymes activity of rat livers. J Gerontol A Biol Sci Med Sci. 1998; 53(3): B161-B167. PMID: 9597038
28. Johnson P. Antioxidant enzyme expression in health and disease: effects of exercise and hypertension. Comp Biochem Physiol C Toxicol Pharmacol. 2002; 133(4): 493-505. PMID: 12458178
29. Robinson MK, Rustum RR, Chambers EA, Rounds JD, Wilmore DW, Jacobs DO. Starvation enhances hepatic free radical release following endotoxemia. J Surg Res. 1997; 69(2): 325-330. PMID: 9224401
30. Vogt BL, Richie JP. Fasting-induced depletion of glutathione in the aging mouse. Biochem Pharmacol. 1993; 46(2): 257-263. PMID: 8347148
31. Guderley H, Lapointe D, Bedard M, Dutil JD. Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp Biochem Physiol A Mol Integr Physiol. 2003; 135(2): 347-356. PMID: 12781835
32. Pascual P, Pedrajas JR, Toribio F, Lopez-Barea J, Peinado J. Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chem Biol Interact. 2003; 145(2): 191-199. PMID: 12686495
33. Lushchak VI. Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol. 2011; 101(1): 13-30. doi: 10.1016/j.aquatox.2010.10.006 PMID: 21074869
34. Kelley EE, Khoo NK, Hundley NJ, Malik UZ, Freeman BA, Tarpey MM. Hydrogen peroxide is the major oxidant product of xanthine oxidase. Free Radic Biol Med. 2010; 48(4): 493-498. doi: 10.1016/j.freeradbiomed.2009.11.012 PMID: 19941951
35. Crain CM, Kroeker K, Halpern BS. Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett. 2008; 11(12): 1304-1315. doi: 10.1111/j.1461-0248.2008.01253.x PMID: 19046359
36. Darling ES, Cote IM. Quantifying the evidence for ecological synergies. Ecol Letters. 2008; 11(12): 1278-1286.
37. Holmstrup M, Bindesbøl AM, Oostingh GJ, Duschl A, Scheil V, Köhler H-R, et al. Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ. 2010; 408(18): 3746-3762. doi: 10.1016/j.scitotenv.2009.10.067 PMID: 19922980
38. Furné M, García-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, et al. Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquacult Nutr. 2009; 15(6): 587-595.
39. Sampaio FG, de Lima Boijink C, Oba ET, dos Santos LRB, Kalinin AL, Rantin FT. Antioxidant defenses and biochemical changes in pacu (Piaractus mesopotamicus) in response to single and combined copper and hypoxia exposure. Comp Biochem Physiol C Toxicol Pharmacol. 2008; 147(1): 43-51. PMID: 17728190
40. Sampaio FG, de Lima Boijink C, dos Santos LRB, Oba ET, Kalinin AL, Luiz AJB, et al. Antioxidant defenses and biochemical changes in the neotropical fish pacu, Piaractus mesopotamicus: Responses to single and combined copper and hypercarbia exposure. Comp Biochem Physiol C Toxicol Pharmacol. 2012; 156 (3): 178-186.
41. Wilhelm Filho D, Giulivi C, Boveris A. Antioxidant defenses in marine fish-I. Teleosts. Comp Biochem Physiol C Toxicol Pharmacol. 1993; 106(2): 409-413.
42. Person-Le Ruyet J, Chartois H, Quemener L. Comparative acute ammonia toxicity in marine fish and plasma ammonia response. Aquaculture. 1995; 136(1): 181-194.
43. Verdouw H, Van Echteld CJA, Dekkers EMJ. Ammonia determination based on indophenol formation with sodium salicylate. Water Res. 1978; 12(6): 399-402.
44. Wright P, Felskie A, Anderson P. Induction of ornithine-urea cycle enzymes and nitrogen metabolism and excretion in rainbow trout (Oncorhynchus mykiss) during early life stages. J Exp Biol. 1995; 198(1): 127-135.
45. Hodges DM, DeLong JM, Forney CF, Prange RK. Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta. 1999; 207(4): 604-611.
46. Jiang ZY, Woollard ACS, Wolff SP. Hydrogen peroxide production during experimental protein glycation. FEBS Lett. 1990; 268(1): 69-71. PMID: 2384174
47. Dhindsa RS, Plumb-Dhindsa P, Thorpe TA. Leaf Senescence: Correlated with Increased Levels of Membrane Permeability and Lipid Peroxidation, and Decreased Levels of Superoxide Dismutase and Catalase. J Exp Bot. 1981; 32(1): 93-101.
48. Aebi H. Catalase in vitro. Method Enzymol. 1984; 105: 121-126.
49. Ozer N, Oglu MM, Ogus IH. A simple and sensitive method for the activity staining of xanthine oxidase. J Biochem Biophys Methods. 1998; 36(2): 95-100.
50. Murshed R, Lopez-Lauri F, Sallanon H. Microplate quantification of enzymes of the plant ascorbate-glutathione cycle. Anal Biochem. 2008; 383(2): 320-322. doi: 10.1016/j.ab.2008.07.020 PMID: 18682244
51. Habig WH, Pabst MJ, Jacoby WB. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem. 1974; 249(22): 7130-7139. PMID: 4436300
52. Drotar A, Phelps P, Fall R. Evidence for glutathione peroxidase activities in cultured plant cells. Plant Sci. 1985; 42(1): 35-40.
53. Lowry OH, Rosebrough N J, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1): 265-275. PMID: 14907713
54. Martínez-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(23): 3699-3706.
55. Hidalgo MC, Exposito A, Palma JM, de la Higuera M. Oxidative stress generated by dietary Zn-deficiency; studies in rainbow trout (Oncorhynchus mykiss). Int J Biochem Cell Biol. 2002; 34(2): 183-193. PMID: 11809421
56. Morales AE, Perez-Jimenez A, Carmen Hidalgo M, Abellán E, Cardenete G. Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp Biochem Physiol C Toxicol Pharmacol. 2004; 139(1): 153-161.
57. Murthy CRK, Rama Rao KV, Bai G, Norenberg MD. Ammonia induced production of free radicals in primary cultures of rat astrocytes. J Neurosci Res. 2001; 66(2): 282-288. PMID: 11592125
58. Freeman BA, Crapo JD. Biology of disease. Free radicals and tissue injury. Lab Invest. 1982; 47(5): 412-426. PMID: 6290784
59. Halliwell B, Gutteridge JMC. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol. 1990; 186: 1-85.
60. Wang XJ, Zhang XM, Li WT. Effects of salinity on the non-specific immuno-enzymatic activity of Sebastes schlegeli. Mar Fish Res. 2005; 26: 17-21.
61. Antonopoulou E, Kentepozidou E, Feidantsis K, Roufidou C, Despoti S, Chatzifotis S. Starvation and re-feeding affect Hsp expression, MAPK activation and antioxidant enzymes activity of European Sea Bass (Dicentrarchus labrax). Comp Biochem Physiol A Mol Integr Physiol. 2013; 165 (1): 79-88. doi: 10.1016/j.cbpa.2013.02.019 PMID: 23462223
62. 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; 159(4): 191-196. doi: 10.1016/j.cbpb.2011.04.008 PMID: 21571088
63. Yu BP. Cellular defenses against damage from reactive oxygen species. Physiol Rev. 1994; 74(1): 139-162. PMID: 8295932
64. Aceto A, Amicarelli F, Sacchetta P, Dragani B, Bucciarelli T, Masciocco L, et al. Developmental aspects of detoxifying enzymes in fish (Salmo iridaeus). Free Radical Res. 1994; 21(5): 285-294.
65. Wang WN, Wu J, Su SJ. Effects of salinity stress on antioxidant enzymes of Penaeus monodon of two different life stages. Comp Biochem Physiol C Toxicol Pharmacol. 2008; 148(4): 466.
66. Fei Y, Shiming P, Peng S, Zhaohong S. Effects of low salinity on antioxidant enzymes activities in kidney and muscle of juvenile silver pomfret Pampus argenteus. Acta Ecologica Sinica. 2011; 31(1): 55-60.
67. Vigano L, Arillo A, Bagnasco M, Bennicelli C, Melodia F. Xenobiotic metabolizing enzymes in uninduced and induced rainbow trout (Oncorhynchus mykiss): effects of diets and food deprivation. Comp Biochem Physiol C Toxicol Pharmacol. 1993; 104(1): 51-55.
68. Barroso JB, Peragon J, Contreras-Jurado C, Garcia-Salguero L, Corpas FJ, Esteban FJ, et al. Impact of starvation-refeeding on kinetics and protein expression of trout liver NADPH-production systems. Am J Physiol. 1998; 274(6): R1578-R1587. PMID: 9608011
69. Meton I, Fernandez F, Baanante IV. Short- and long-term effects of refeeding on key enzyme activities in glycolysis-gluconeogenesis in the liver of gilthead seabream (Sparus aurata). Aquaculture. 2003; 225(1): 99-107.
70. Blom S, Andersson TB, Forlin L. Effects of food deprivation and handling stress on head kidney 17α-hydroxyprogesterone 21-hydroxylase activity, plasma cortisol and the activities of liver detoxification enzymes in rainbow trout. Aquat Toxicol. 2000; 48(2): 265-274.
71. Papadopoulos MC, Koumenis IL, Dugan LL, Giffard RG. Vulnerability to glucose deprivation injury correlates with glutathione levels in astrocytes. Brain Res. 1997; 748(1): 151-156.
72. Vendemiale G, Grattagliano I, Caraceni P, Caraccio G, Domenicali M, Dall'Agata M, et al. Mitochondrial oxidative injury and energy metabolism alteration in rat fatty liver: effect of the nutritional status. Hepatology. 2001; 33(4): 808-815. PMID: 11283843
73. Hunter EA, Grimble RF. Dietary sulphur amino acid adequacy influences glutathione synthesis and glutathione-dependent enzymes during the inflammatory response to endotoxin and tumour necrosis factor-alpha in rats. Clin Sci. 1997; 92(3): 297-305. PMID: 9093011
74. Paterson PG, Lyon AW, Kamencic H, Andersen LB, Juurlink BH. Sulfur amino acid deficiency depresses brain glutathione concentration. Nutr Neurosci. 2001; 4(3): 213-222. PMID: 11842890
75. Eyckmans M, Celis N, Horemans N, Blust R, De Boeck G. Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquat Toxicol. 2011; 103(1): 112-120.
76. Jena SD, Behera M, Dandapat J, Mohanty N. Non-enzymatic antioxidant status and modulation of lipid peroxidation in the muscles of Labeo rohita by sub lethal exposure of CuSO4. Vet Res Commun. 2009; 33(5): 421-429. doi: 10.1007/s11259-008-9188-x PMID: 19034682