Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of astaxanthin on antioxidant capacity of golden pompano (Trachinotus ovatus) in vivo and in vitro

  • Xie, Jia-jun (South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences) ;
  • Chen, Xu (South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences) ;
  • Niu, Jin (Institute of Aquatic Economic Animals, School of Life Science, Sun Yat-sen University) ;
  • Wang, Jun (South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences) ;
  • Wang, Yun (South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences) ;
  • Liu, Qiang-qiang (South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences)
  • Received : 2017.01.25
  • Accepted : 2017.04.18
  • Published : 2017.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

The objective of this research was to study the effect of astaxanthin (AST) on growth performance and antioxidant capacity in golden pompano (Trachinotus ovatus) both in vivo and in vitro. In the in vivo study, two diets were formulated with or without astaxanthin supplementation (D1 and D2; 0 and 200 mg/kg) to feed fish for 6 weeks. In the in vitro study, cells from hepatopancreas of golden pompano were isolated and four treatments with or without astaxanthin and $H_2O_2$ supplementation were applied (control group: without both astaxanthin and $H_2O_2$ treated; $H_2O_2$ group: just with $H_2O_2$ treated; $H_2O_2$ + AST group: with both astaxanthin and $H_2O_2$treated; AST group: just with AST treated). Results of the in vivo study showed that weight gain (WG) and special growth rate (SGR) significantly increased with astaxanthin supplemented (P < 0.05). Feed conversion ratio (FCR) of fish fed D2 diet was significantly lower than that of fish fed D1 diet (P < 0.05). Hepatic total antioxidant capacity (T-AOC) and the reduced glutathione (GSH) of golden pompano fed D2 diet were significant higher than those of fish fed D1 diet (P < 0.05). Superoxide dismutase (SOD) was significantly declined as astaxanthin was supplemented (P < 0.05). Results of the in vitro study showed that the cell viability of $H_2O_2$ group was 52.37% compared to the control group, and it was significantly elevated to 84.18% by astaxanthin supplementation ($H_2O_2$ + AST group) (P < 0.05). The total antioxidant capacity (T-AOC) and the reduced glutathione (GSH) of cell were significant decreased by oxidative stress from $H_2O_2$ (P < 0.05), but it could be raised by astaxanthin supplementation ($H_2O_2$ vs $H_2O_2$ + AST), and the malondialdehyde (MDA) was significant higher in $H_2O_2$ group (P < 0.05) and astaxanthin supplementation could alleviate the cells from lipid peroxidation injury. In conclusion, dietary astaxanthin supplementation can improve the growth performance of golden pompano. Moreover, astaxanthin can improve the golden pompano hepatic antioxidant capacity both in vivo and in vitro study by eliminating the reactive oxygen species.

Keywords

References

  1. Alishahi M, Karamifar M, Mesbah M. Effects of astaxanthin and Dunaliella salina on skin carotenoids, growth performance and immune response of Astronotus ocellatus. Aquac Int. 2015;23(5):1239-48. https://doi.org/10.1007/s10499-015-9880-0
  2. Amar E, Kiron V, Satoh S, Watanabe T. Influence of various dietary synthetic carotenoids on bio-defence mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult Res. 2001;32(s1):162-73. https://doi.org/10.1046/j.1355-557x.2001.00051.x
  3. Baker R, Pfeiffer A-M, Schoner F-J, Smith-Lemmon L. Pigmenting efficacy of astaxanthin and canthaxanthin in fresh-water reared Atlantic salmon, Salmo salar. Anim Feed Sci Technol. 2002;99(1):97-106. https://doi.org/10.1016/S0377-8401(02)00116-5
  4. Britton G. Structure and properties of carotenoids in relation to function. FASEB J. 1995;9(15):1551-8. https://doi.org/10.1096/fasebj.9.15.8529834
  5. Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol. 1978;52:302-10.
  6. Chen YY, Lee PC, Wu YL, Liu LY. In vivo effects of free form astaxanthin powder on anti-oxidation and lipid metabolism with high-cholesterol diet. PLoS One. 2015;10(8):e0134733. https://doi.org/10.1371/journal.pone.0134733
  7. Chew BP. Antioxidant vitamins affect food animal immunity and health. J Nutr. 1995;125(6 Suppl):1804S-8S.
  8. Chew BP, Park JS. Carotenoid action on the immune response. J Nutr. 2004;134(1):257S-61S. https://doi.org/10.1093/jn/134.1.257S
  9. Chien Y-H, Pan C-H, Hunter B. The resistance to physical stresses by Penaeus monodon juveniles fed diets supplemented with astaxanthin. Aquaculture. 2003;216(1):177-91. https://doi.org/10.1016/S0044-8486(02)00056-X
  10. Christiansen R, Torrissen OJ. Growth and survival of Atlantic salmon, Salmo salar L. fed different dietary levels of astaxanthin. Juveniles. Aquacult Nutr. 1996;2(1):55-62. https://doi.org/10.1111/j.1365-2095.1996.tb00008.x
  11. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol. 2003;15(2):247-54. https://doi.org/10.1016/S0955-0674(03)00002-4
  12. Huo-sheng Y. Studies on the culture of pompano, Trachinotus ovatus [J]. J Fujian Fish. 2006;1:009.
  13. James R., Sampath K., Thangarathinam R. and Vasudevan I. Effect of dietary spirulina level on growth, fertility, coloration and leucocyte count in red swordtail, Xiphophorus helleri. 2006;58(2):97-104.
  14. Kalinowski CT, Robaina LE, Izquierdo MS. Effect of dietary astaxanthin on the growth performance, lipid composition and post-mortem skin colouration of red porgy Pagrus pagrus. Aquac Int. 2011;19(5):811-23. https://doi.org/10.1007/s10499-010-9401-0
  15. Kop A, Durmaz Y. The effect of synthetic and natural pigments on the colour of the cichlids (Cichlasoma severum sp., Heckel 1840). Aquac Int. 2008;16(2):117-22. https://doi.org/10.1007/s10499-007-9130-1
  16. Latimer GW. Official methods of analysis of AOAC International. Maryland: AOAC International; 2012.
  17. Leite M, De Lima A, Massuyama M, Otton R. In vivo astaxanthin treatment partially prevents antioxidant alterations in dental pulp from alloxan-induced diabetic rats. Int Endod J. 2010;43(11):959-67. https://doi.org/10.1111/j.1365-2591.2010.01707.x
  18. Li M, Wu W, Zhou P, Xie F, Zhou Q, Mai K. Comparison effect of dietary astaxanthin and Haematococcus pluvialis on growth performance, antioxidant status and immune response of large yellow croaker Pseudosciaena crocea. Aquaculture. 2014;434:227-32. https://doi.org/10.1016/j.aquaculture.2014.08.022
  19. Lin HZ, Tan XH, Zhou CP, Niu J, Xia DM, Huang Z, Wang J, Wang Y. Effect of dietary arginine levels on the growth performance, feed utilization, nonspecific immune response and disease resistance of juvenile golden pompano Trachinotus ovatus. Aquaculture. 2015;437:382-9. https://doi.org/10.1016/j.aquaculture.2014.12.025
  20. Liu C, Chen C. The biology and cultured technology of Pompano (Trachinotus ovatus). Shandong Fisheries. 2009;26:32-3.
  21. Liu B, Xie J, Ge X, Xu P, Wang A, He Y, Zhou Q, Pan L, Chen R. Effects of anthraquinone extract from Rheum officinale Bail on the growth performance and physiological responses of Macrobrachium rosenbergii under high temperature stress. Fish Shellfish Immunol. 2010;29(1):49-57. https://doi.org/10.1016/j.fsi.2010.02.018
  22. Lygren B, Hamre K, Waagbo R. Effects of dietary pro-and antioxidants on some protective mechanisms and health parameters in Atlantic salmon. J Aquat Anim Health. 1999;11(3):211-21. https://doi.org/10.1577/1548-8667(1999)011<0211:EODPAA>2.0.CO;2
  23. Mallikarjuna K, Nishanth K, Hou CW, Kuo CH, Sathyavelu RK. Effect of exercise training on ethanol-induced oxidative damage in aged rats. Alcohol. 2009;43(1):59-64. https://doi.org/10.1016/j.alcohol.2008.09.003
  24. Mansour N, McNiven MA, Richardson GF. The effect of dietary supplementation with blueberry, ${\alpha}$-tocopherol or astaxanthin on oxidative stability of Arctic char (Salvelinus alpinus) semen. Theriogenology. 2006;66(2):373-82. https://doi.org/10.1016/j.theriogenology.2005.12.002
  25. Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974;47(3):469-74. https://doi.org/10.1111/j.1432-1033.1974.tb03714.x
  26. Martinez-Alvarez RM, Morales AE, Sanz A. Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fish. 2005;15(1-2):75-88. https://doi.org/10.1007/s11160-005-7846-4
  27. Misra S, Niyogi S. Selenite causes cytotoxicity in rainbow trout (Oncorhynchus mykiss) hepatocytes by inducing oxidative stress. Toxicol In Vitro. 2009;23(7):1249-58. https://doi.org/10.1016/j.tiv.2009.07.031
  28. Niu J, Du Q, Lin HZ, Cheng YQ, Huang Z, Wang Y, Wang J, Chen YF. Quantitative dietary methionine requirement of juvenile golden pompano Trachinotus ovatus at a constant dietary cystine level. Aquacult Nutr. 2013;19(5):677-86. https://doi.org/10.1111/anu.12015
  29. Niu J, Figueiredo-Silva C, Dong Y, Yue Y, Lin H, Wang J, Wang Y, Huang Z, Xia D, Lu X. Effect of replacing fish meal with soybean meal and of DL-methionine or lysine supplementation in pelleted diets on growth and nutrient utilization of juvenile golden pompano (Trachinotus ovatus). Aquacult Nutr. 2016;22:606-14. https://doi.org/10.1111/anu.12284
  30. Olmedilla B, Granado F, Southon S, Wright AJA, Blanco I, Gil-Martinez E, Berg H v d, Corridan B, Roussel A-M, Chopra M, Thurnham DI. Serum concentrations of carotenoids and vitamins A, E, and C in control subjects from five European countries. Br J Nutr. 2007;85(02):227.
  31. Pham MA, Byun HG, Kim KD, Lee SM. Effects of dietary carotenoid source and level on growth, skin pigmentation, antioxidant activity and chemical composition of juvenile olive flounder Paralichthys olivaceus. Aquaculture. 2014;431:65-72. https://doi.org/10.1016/j.aquaculture.2014.04.019
  32. Qi C-L, Lin H-Z, Huang Z, Zhou C-P, Wang Y, Wang J, Niu J, Zhao S-Y. Effects of dietary arachidonic acid levels on growth performance, whole-body proximate composition, digestive enzyme activities and gut morphology of juvenile golden pompano trachinotus. Isr J Aquacult Bamidgeh. 2016;68:1275-84.
  33. Qingming Y, Xianhui P, Weibao K, Hong Y, Yidan S, Li Z, Yanan Z, Yuling Y, Lan D, Guoan L. Antioxidant activities of malt extract from barley (Hordeum vulgare L.) toward various oxidative stress in vitro and in vivo. Food Chem. 2010;118(1):84-9. https://doi.org/10.1016/j.foodchem.2009.04.094
  34. Robinson EH, Wilson RP, Poe WE. Arginine requirement and apparent absence of a lysine-arginine antagonist in fingerling channel catfish. J Nutr. 1981;111(1):46-52. https://doi.org/10.1093/jn/111.1.46
  35. Segner H, Arend P, Von Poeppinghausen K, Schmidt H. The effect of feeding astaxanthin to Oreochromis niloticus and Colisa labiosa on the histology of the liver. Aquaculture. 1989;79(1-4):381-90. https://doi.org/10.1016/0044-8486(89)90480-8
  36. Shaw S. Lipid peroxidation, iron mobilization and radical generation induced by alcohol. Free Radic Biol Med. 1989;7(5):541-7. https://doi.org/10.1016/0891-5849(89)90030-0
  37. Shimidzu N, Goto M, Miki W. Carotenoids as singlet oxygen quenchers in marine organisms. Fish Sci. 1996;62(1):134-7.
  38. Tejera N, Cejas JR, Rodriguez C, Bjerkeng B, Jerez S, Bolanos A, Lorenzo A. Pigmentation, carotenoids, lipid peroxides and lipid composition of skin of red porgy (Pagrus pagrus) fed diets supplemented with different astaxanthin sources. Aquaculture. 2007;270(1):218-30. https://doi.org/10.1016/j.aquaculture.2007.01.019
  39. Tutman P, Glavic N, Kozul V, Skaramuca B, Glamuzina B. Preliminary information on feeding and growth of pompano, Trachinotus ovatus (Linnaeus, 1758)(Pisces; Carangidae) in captivity. Aquac Int. 2004;12(4-5):387-93. https://doi.org/10.1023/B:AQUI.0000042135.88381.f4
  40. Vardi N, Parlakpinar H, Ozturk F, Ates B, Gul M, Cetin A, Erdogan A, Otlu A. Potent protective effect of apricot and beta-carotene on methotrexate-induced intestinal oxidative damage in rats. Food Chem Toxicol. 2008;46(9):3015-22. https://doi.org/10.1016/j.fct.2008.05.039
  41. Vogt BL, Richie Jr JP. Glutathione depletion and recovery after acute ethanol administration in the aging mouse. Biochem Pharmacol. 2007;73(10):1613-21. https://doi.org/10.1016/j.bcp.2007.01.033
  42. Wan X, Ma T, Wu W, Wang Z. EROD activities in a primary cell culture of grass carp (Ctenopharyngodon idellus) hepatocytes exposed to polychlorinated aromatic hydrocarbonas. Ecotoxicol Environ Saf. 2004;58(1):84-9. https://doi.org/10.1016/j.ecoenv.2004.01.005
  43. Wang F, Han H, Wang Y, Ma X. Growth, feed utilization and body composition of juvenile golden pompano Trachinotus ovatus fed at different dietary protein and lipid levels. Aquacult Nutr. 2013;19(3):360-7. https://doi.org/10.1111/j.1365-2095.2012.00964.x
  44. Winston GW, Di Giulio RT. Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol. 1991;19(2):137-61. https://doi.org/10.1016/0166-445X(91)90033-6
  45. Xiao N, Wang XC, Diao YF, Liu R, Tian KL. Effect of initial fluid resuscitation on subsequent treatment in uncontrolled hemorrhagic shock in rats. Shock. 2004;21(3):276-80. https://doi.org/10.1097/01.shk.0000110622.42625.cb
  46. Yi XW, Xu W, Zhou HH, Zhang YJ, Luo YW, Zhang WB, Mai KS. Effects of dietary astaxanthin and xanthophylls on the growth and skin pigmentation of large yellow croaker Larimichthys croceus. Aquaculture. 2014;433:377-83. https://doi.org/10.1016/j.aquaculture.2014.06.038
  47. Zhang J, Li X, Leng X, Zhang C, Han Z, Zhang F. Effects of dietary astaxanthins on pigmentation of flesh and tissue antioxidation of rainbow trout (Oncorhynchus mykiss). Aquac Int. 2012;21(3):579-89. https://doi.org/10.1007/s10499-012-9590-9
  48. Zhou CP, Ge XP, Niu J, Lin HZ, Huang Z, Tan XH. Effect of dietary carbohydrate levels on growth performance, body composition, intestinal and hepatic enzyme activities, and growth hormone gene expression of juvenile golden pompano. Trachinotus ovatus Aquaculture. 2015;437:390-7.

Cited by

  1. Effects of astaxanthin and canthaxanthin on oxidative stress biomarkers in rainbow trout vol.82, pp.13, 2017, https://doi.org/10.1080/15287394.2019.1648346
  2. Dietary β‐carotene improves growth performance and antioxidant status of juvenile Piaractus mesopotamicus vol.25, pp.4, 2019, https://doi.org/10.1111/anu.12893
  3. Dietary administration of astaxanthin improves feed utilization, growth performance and survival of Asian seabass, Lates calcarifer (Bloch, 1790) vol.25, pp.6, 2017, https://doi.org/10.1111/anu.12961
  4. Identification of heme oxygenase-1 from golden pompano (Trachinotus ovatus) and response of Nrf2/HO-1 signaling pathway to copper-induced oxidative stress vol.253, pp.None, 2020, https://doi.org/10.1016/j.chemosphere.2020.126654
  5. Effects of dietary astaxanthin on the growth, innate immunity and antioxidant defence system of Paramisgurnus dabryanus vol.26, pp.5, 2017, https://doi.org/10.1111/anu.13093