Skip to main content
SpringerLink
Log in

Effects of dietary vitamin D3 on growth performance, antioxidant capacities and innate immune responses in juvenile black carp Mylopharyngodon piceus

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The aim of this experiment was used to investigate the effects of different contents of dietary vitamin D3 on the growth performance and antioxidant and innate immune responses in juvenile black carp Mylopharyngodon piceus. Black carp juveniles were fed six levels of dietary vitamin D3 (VD3) (96, 220, 412, 840, 1480, and 3008 IU/Kg) for 9 weeks. Results showed that highest weight gain (WG) and special growth ratio (SGR) were obtained at 534.2 IU/Kg dietary VD3 according to the second-order polynomial regression model. The protein efficiency ratio (PER) of black carp could be significantly increased by 412, 840, and 1480 IU/Kg dietary VD3 (p < 0.05), while the feed conversion ratio (FCR) were reduced by 412, 840, and 1480 IU/Kg dietary VD3 (p < 0.05). Adequate dietary VD3 content (412, 840, and 1480 IU/Kg) could significantly upregulate expression levels of lipoxygenase 5 (LPO 5); increase the activities of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), and glutathione reductase (GR); and improve GSH contents and total antioxidant capacities (T-AOC) in the liver of black carp. However, glutathione S-transferase (GST) activities and malondialdehyde (MDA) levels were significantly reduced by adequate dietary VD3 content (412, 840, and 1480 IU/Kg) in the fish liver. In addition, 412, 840, and 1480 IU/Kg dietary VD3 could significantly upregulate the mRNA expression levels of interferon-α (IFN-α), lysozyme (LYZ), hepcidin (HEPC), natural resistance-associated macrophage protein (NRAMP), and complement component 3 (C3) and C9 in the hemocytes and liver of black carp juveniles compared with the VD3-deficient diet (96 IU/Kg). Meanwhile, higher contents of dietary VD3 could increase serum LYZ and ACP activities and C3 and C4 contents in black carp juveniles compared with the groups fed VD3-deficient diet. In conclusion, these results suggest that adequate dietary VD3 could increase growth performances, improve antioxidant capacities, and then enhance innate immune parameters in black carp juveniles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrews JW, Murai T, Page JW (1980) Effects of dietary cholecalciferol and ergocalciferol on catfish. Aquaculture 19:49–54

    CAS  Google Scholar 

  • Attwood EM, Weich DJV, Oosthuizen JMC (1996) The influence of carbon particles on the concentration of acid phosphatase and lysozyme enzymes within alveolar macrophages during the killing and degradation of Mycobacterium bovis. Tuber Lung Dis 77:341–347

    CAS  PubMed  Google Scholar 

  • Baeke F, Takiishi T, Korf H, Gysemans C, Mathieu C (2010) Vitamin D: modulator of the immune system. Curr Opin Pharmacol 10:482–496

    CAS  PubMed  Google Scholar 

  • Bao BY, Ting HJ, Hsu JW, Lee YF (2008) Protective role of 1α, 25-dihydroxyvitamin D3 against oxidative stress in nonmalignant human prostate epithelial cells. Int J Cancer 122:2699–2706

    CAS  PubMed  Google Scholar 

  • Barnett BJ, Cho CY, Slinger SJ (1982) Relative biopotency of dietary ergocalciferol and cholecalciferol and the role of and requirement for vitamin D in rainbow trout (Salmo gairdneri). J Nutr 112:2011–2019

    CAS  PubMed  Google Scholar 

  • Bogdan C, Rollinghoff M, Diefenbach A (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12:64–76

    CAS  PubMed  Google Scholar 

  • Boshra H, Li J, Sunyer JO (2006) Recent advances on the complement system of teleost fish. Fish Shellfish Immunol 20:239–262

    CAS  PubMed  Google Scholar 

  • Brock K, Huang WY, Fraser DR, Ke L, Tseng M, Stolzenberg-Solomon R, Peters U, Ahn J, Purdue M, Mason RS, McCarty C, Ziegler RG, Graubard B (2010) Low vitamin D status is associated with physical inactivity, obesity and low vitamin D intake in a large US sample of healthy middle-aged men and women. J Steroid Biochem 121:462–466

    CAS  Google Scholar 

  • Broeg K (2003) Acid phosphatase activity in liver macrophage aggregates as a marker for pollution-induced immunomodulation of the non-specific immune response in fish. Helgol Mar Res 57:166–175

    Google Scholar 

  • Brown PB, Robinson EH (1992) Vitamin-D studies with channel catfish (Ictalurus Punctatus) reared in calcium-free water. Comp Biochem Phys A 103:213–219

    Google Scholar 

  • Colston KW, Berger U, Coombes RC (1989) Possible role for vitamin D in controlling breast cancer cell proliferation. Lancet 1:188–191

    CAS  PubMed  Google Scholar 

  • Darias MJ, Mazurais D, Koumoundouros G, Cahu CL, Zambonino-Infante JL (2011) Overview of vitamin D and C requirements in fish and their influence on the skeletal system. Aquaculture 315:49–60

    CAS  Google Scholar 

  • Decker T, Stockinger S, Karaghiosoff M, Muller M, Kovarik P (2002) IFNs and STATs in innate immunity to microorganisms. J Clin Invest 109:1271–1277

    CAS  PubMed  PubMed Central  Google Scholar 

  • DeLuca HF (2004) Overview of general physiologic features and functions of vitamin D. Am J Clin Nutr 80:1689S–1696S

    CAS  PubMed  Google Scholar 

  • Ehrengruber MU, Geiser T, Deranleau DA (1994) Activation of human neutrophils by C3a and C5A. Comparison of the effects on shape changes, chemotaxis, secretion, and respiratory burst. FEBS Lett 346:181–184

    CAS  PubMed  Google Scholar 

  • Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18:872–879

    CAS  PubMed  Google Scholar 

  • Farhat MAK (2014) Response of fingerling stinging catfish, Heteropneustes fossilis (Bloch) to varying levels of dietary L-leucine in relation to growth, feed conversion, protein utilization, leucine retention and blood parameters. Aquac Nutr 20:291–302

    CAS  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247

    CAS  PubMed  Google Scholar 

  • Gasque P (2004) Complement: a unique innate immune sensor for danger signals. Mol Immunol 41:1089–1098

    CAS  PubMed  Google Scholar 

  • Halver JE (2002) The vitamins. In: Halver JE (ed) Fish nutrition. Academic Press, New York, p 119

    Google Scholar 

  • Heaney RP (2005) The Vitamin D requirement in health and disease. J Steroid Biochem Mol Biol 97:13–19

    CAS  PubMed  Google Scholar 

  • Hewison M (2012) An update on vitamin D and human immunity. Clin Endocrinol 76:315–325

    CAS  Google Scholar 

  • Holick MF (2007) Vitamin D deficiency. N Engl J Med 357:266–281

    CAS  PubMed  Google Scholar 

  • Hu Y, Huang Y, Wen H, Huan ZL, Zhong L, Mao XW (2013) Effect of vitamin C on growth, immunity and anti-ammonia-nitrite stress ability in juvenile black carp (Mylopharyngodon piceus). J Fish China 37:565–573

    CAS  Google Scholar 

  • Kadowaki N, Antonenko S, Lau JYN, Liu YJ (2000) Natural interferon α/β–producing cells link innate and adaptive immunity. J Exp Med 192:219–226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karges K, Brooks JC, Gill DR, Breazile JE, Owens FN, Morgan JB (2001) Effects of supplemental vitamin D3 on feed intake, carcass characteristics, tenderness, and muscle properties of beef steers. J Anim Sci 79:2844–2850

    CAS  PubMed  Google Scholar 

  • Kiron V, Puangkaew J, Ishizaka K, Satoh S, Watanabe T (2004) Antioxidant status and nonspecific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of vitamin E along with three lipid sources. Aquaculture 234:361–379

    CAS  Google Scholar 

  • Knight JA (2000) Review: Free radicals, antioxidants, and the immune system. Ann Clin Lab Sci 30:145–158

    CAS  PubMed  Google Scholar 

  • Lee J, Koo N, Min DB (2004) Reactive oxygen species, aging, and antioxidative nutraceuticals. Compr Rev Food Sci F 3:21–33

    CAS  Google Scholar 

  • Lin MF, Shiau SY (2004) Requirements of vitamin C (L-ascorbyl-2-monophosphate-Mg and L-ascorbyl-2-monophosphate-Na) and its effects on immune responses of grouper, Epinephelus malabaricus. Aquac Nutr 10:327–333

    CAS  Google Scholar 

  • Lin AM, Chen KB, Chao PL (2005) Antioxidative effect of vitamin D3 on zinc-induced oxidative stress in CNS. Ann N Y Acad Sci 1053:319–329

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. methods 25, 402-408

  • Lock EJ, Waagbo R, Bonga SW, Flik G (2010) The significance of vitamin D for fish: a review. Aquac Nutr 16:100–116

    CAS  Google Scholar 

  • Lovell RT, Li YP (1978) Essentiality of vitamin-D in diets of channel catfish (Ictalurus Punctatus). T Am Fish Soc 107:809–811

    CAS  Google Scholar 

  • Miao LH, Ge XP, Xie J, Liu B, Wang KB, Zhu J, Ren MC, Zhou QL, Pan LK, Chen RL (2015) Dietary vitamin D-3 requirement of Wuchang bream (Megalobrama amblycephala). Aquaculture 436:104–109

    CAS  Google Scholar 

  • Ministry of Agriculture of the People’s Republic of China (2019) Chinese Fisheries Yearbook. Chinese Agricultural Press, Beijing

    Google Scholar 

  • Möller AM, Korytář T, Köllner B, Schmidt-Posthaus H, Segner H (2014) The teleostean liver as an immunological organ: intrahepatic immune cells (IHICs) in healthy and benzo [a] pyrene challenged rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 46:518–529

    PubMed  Google Scholar 

  • Nakao M, Tsujikura M, Ichiki S, Vo TK, Somamoto T (2011) The complement system in teleost fish: progress of post-homolog-hunting researches. Dev Comp Immunol 35:1296–1308

    CAS  PubMed  Google Scholar 

  • Narnaware YK, Peter RE (2002) Influence of diet composition on food intake and neuropeptide Y (NPY) gene expression in goldfish brain. Regul Pept 103:75–83

    CAS  PubMed  Google Scholar 

  • Narnaware YK, Peyon PP, Lin X, Peter RE (2000) Regulation of food intake by neuropeptide Y in goldfish. Am J Phys Regul Integr Comp Phys 279:R1025–R1034

    CAS  Google Scholar 

  • Nejatian N, Hafner AK, Shoghi F, Badenhoop K, Penna-Martinez M (2019) 5-Lipoxygenase (ALOX5): Genetic susceptibility to type 2 diabetes and vitamin D effects on monocytes. J Steroid Biochem Mol Biol 187:52–57

    CAS  PubMed  Google Scholar 

  • Nonaka M, Yamaguchi N, Natsuume-Sakai S, Takahashi M (1981) The complement system of rainbow trout (Salmo gairdneri). I. Identification of the serum lytic system homologous to mammalian complement. J Immunol 126:1489–1494

    CAS  PubMed  Google Scholar 

  • Oconnell JP, Gatlin DM (1994) Effects of dietary calcium and vitamin-D3 on weight gain and mineral composition of the blue tilapia (Oreochromis Aureus) in low calcium water. Aquaculture 125:107–117

    CAS  Google Scholar 

  • Ortuno J, Esteban MA, Meseguer J (2000) High dietary intake of alpha-tocopherol acetate enhances the non-specific immune response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 10:293–307

    CAS  PubMed  Google Scholar 

  • Park CH, Valore EV, Waring AJ, Ganz T (2001) Hepcidin, a urinary antimicrobial peptide synthesized in the liver. J Biol Chem 276:7806–7810

    CAS  PubMed  Google Scholar 

  • Pearce J, Harris JE, Davies SJ (2003) The effect of vitamin E on the serum complement activity of the rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Nutr 9:337–340

    CAS  Google Scholar 

  • Phieler J, Garcia-Martin R, Lambris JD, Chavakis T (2013) The role of the complement system in metabolic organs and metabolic diseases. Semin Immunol 25:47–53

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puangkaew J, Kiron V, Somamoto T, Okamoto N, Satoh S, Takeuchi T, Watanabe T (2004) Nonspecific immune response of rainbow trout (Oncorhynchus mykiss Walbaum) in relation to different status of vitamin E and highly unsaturated fatty acids. Fish Shellfish Immunol 16:25–39

    CAS  PubMed  Google Scholar 

  • Reichling JJ, Kaplan MM (1988) Clinical use of serum enzymes in liver-disease. Dig Dis Sci 33:1601–1614

    CAS  PubMed  Google Scholar 

  • Samuel S, Sitrin MD (2008) Vitamin D’s role in cell proliferation and differentiation. Nutr Rev 66:S116–S124

    PubMed  Google Scholar 

  • Sareneva T, Julkunen I, Matikainen S (2000) IFN-alpha and IL-12 induce IL-18 receptor gene expression in human NK and T cells. J Immunol 165:1933–1938

    CAS  PubMed  Google Scholar 

  • Sharifi N, Amani R, Hajiani E, Cheraghian B (2014) Does vitamin D improve liver enzymes, oxidative stress, and inflammatory biomarkers in adults with non-alcoholic fatty liver disease? A randomized clinical trial. Endocrine 47:70–80

    CAS  PubMed  Google Scholar 

  • Shiau SY, Hwang JY (1993) Vitamin D requirements of juvenile hybrid tilapia Oreochromis niloticus×O. aureus. Nipp Suican Gakkaishi 59:553–558

    CAS  Google Scholar 

  • Sies H (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27:916–921

    CAS  PubMed  Google Scholar 

  • Somjen D, Katzburg S, Knoll E, Sharon O, Posner GH, Stern N (2010) Vitamin D analogs induce lipoxygenase mRNA expression and activity as well as reactive oxygen species (ROS) production in human bone cells. J Steroid Biochem 121:265–267

    CAS  Google Scholar 

  • Somjen D, Katzburg S, Grafi-Cohen M, Knoll E, Sharon O, Posner GH (2011) Vitamin D metabolites and analogs induce lipoxygenase mRNA expression and activity as well as reactive oxygen species (ROS) production in human bone cell line. J Steroid Biochem 123:85–89

    CAS  Google Scholar 

  • Spiteller G (2001) Lipid peroxidation in aging and age-dependent diseases. Exp Gerontol 36:1425–1457

    CAS  PubMed  Google Scholar 

  • Sunyer JO, Zarkadis IK, Lambris JD (1998) Complement diversity: a mechanism for generating immune diversity? Immunol Today 19:519–523

    CAS  PubMed  Google Scholar 

  • Tan Q, He R, Xie S, Xie C, Zhang S (2007) Effect of dietary supplementation of vitamins A, D3, E and C on yearling rice field eel, Monopterus albus: serum indices, gonad development, and metabolism of calcium and phosphorus. J World Aquacult Soc 38:146–153

    Google Scholar 

  • Tan XH, Lin HZ, Huang Z, Zhou CP, Wang AL, Qi CL, Zhao SY (2016) Effects of dietary leucine on growth performance, feed utilization, non-specific immune responses and gut morphology of juvenile golden pompano Trachinotus ovatus. Aquaculture 465:100–107

    CAS  Google Scholar 

  • Thomas MJ (1995) The role of free radicals and antioxidants: how do we know that they are working? Crit Rev Food Sci Nutr 35:21–39

    CAS  PubMed  Google Scholar 

  • Thorpe GW, Fong CS, Alic N, Higgins VJ, Dawes IW (2004) Cells have distinct mechanisms to maintain protection against different reactive oxygen species: Oxidative-stress-response genes. Proc Natl Acad Sci U S A 101:6564–6569

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tipton NC, King DA, Paschal JC, Hale DS, Savell JW (2007) Effects of oral vitamin D(3) supplementation and supplement withdrawal on the accumulation of magnesium, calcium, and vitamin D in the serum, liver, and muscle tissue and subsequent carcass and meat quality of Bos indicus influenced cattle. Meat Sci 75:150–158

    CAS  PubMed  Google Scholar 

  • Watanuki H, Chakraborty G, Korenaga H, Kono T, Shivappa RB, Sakai M (2009) Immunostimulatory effects of natural human interferon-alpha (huIFN-alpha) on carps Cyprinus carpio L. Vet Immunol Immunopathol 131:273–277

    CAS  PubMed  Google Scholar 

  • Wiseman H (1993) Vitamin-D is a membrane antioxidant - ability to inhibit iron-dependent lipid-peroxidation in liposomes compared to cholesterol, ergosterol and tamoxifen and relevance to anticancer action. FEBS Lett 326:285–288

    CAS  PubMed  Google Scholar 

  • Woodward B (1994) Dietary vitamin requirements of cultured young fish, with emphasis on quantitative estimates for salmonids. Aquaculture 124:133–168

    CAS  Google Scholar 

  • Wren AM, Seal LJ, Cohen MA, Brynes AE, Frost GS, Murphy KG, Dhillo WS, Ghatei MA, Bloom SR (2001) Ghrelin enhances appetite and increases fd intake in humans. J Clin Endocrinol Metab 86:5992

    CAS  PubMed  Google Scholar 

  • Wu G, Fang YZ, Yang S, Lupton JR, Turner ND (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492

    CAS  PubMed  Google Scholar 

  • Wu C, Ye J, Gao J, Chen L, Lu Z (2016a) The effects of dietary carbohydrate on the growth, antioxidant capacities, innate immune responses and pathogen resistance of juvenile Black carp Mylopharyngodon piceus. Fish Shellfish Immunol 49:132–142

    CAS  PubMed  Google Scholar 

  • Wu CL, Ye JY, Gao JE, Yang X, Zhang YX (2016b) Effect of varying carbohydrate fractions on growth, body composition, metabolic, and hormonal indices in juvenile black carp, Mylopharyngodon piceus. J World Aquacult Soc 47:435–449

    CAS  Google Scholar 

  • Yu BP (1994) Cellular defenses against damage from reactive oxygen species. Physiol Rev 74:139–162

    CAS  PubMed  Google Scholar 

  • Zapata A, Diez B, Cejalvo T, Gutierrez-de Frias C, Cortes A (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136

    CAS  PubMed  Google Scholar 

  • Zhang L (2006) Nutritional physiology of several vitamins and protein sources development for Japanese seabass, Lateolabrax japonicus C. and large yellow croaker, Pseudosciaena crocea R. Ocean University of China, Qingdao, China

  • Zhang L, Li J, K M, Ai Q, Zhang C, Li H, Yuan Y (2016) Effects of different dietary vitamin D contents on growth performance, calcium and phosphrus metabolism of juvenile Japanese Seabass (Lateolabrax japonicas). Chin J Animal Nutr 28:1402–1411

    CAS  Google Scholar 

  • Zhu LY, Nie L, Zhu G, Xiang LX, Shao JZ (2013) Advances in research of fish immune-relevant genes: a comparative overview of innate and adaptive immunity in teleosts. Dev Comp Immunol 39:39–62

    CAS  PubMed  Google Scholar 

Download references

Funding

This research was financially supported by the National Key R&D Program of China (2018YFD0900400), the National Natural Science Foundation of China (31672669, 31202008), the Earmarked Fund for China Agriculture Research System (CARS-45), Zhejiang provincial Science Foundation of China (LY12C19002), and the Program for Zhejiang Leading Team of S & T Innovation (2010R10026-08).

Author information

Authors and Affiliations

  1. School of Life Science, Huzhou University, 759 East 2nd Road, Huzhou, 313000, People’s Republic of China

    Chenglong Wu, Bin Lu, Yunlong Wang, Chuanmin Jin, Yixiang Zhang & Jinyun Ye

Authors
  1. Chenglong Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunlong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chuanmin Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yixiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinyun Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chenglong Wu.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, C., Lu, B., Wang, Y. et al. Effects of dietary vitamin D3 on growth performance, antioxidant capacities and innate immune responses in juvenile black carp Mylopharyngodon piceus. Fish Physiol Biochem 46, 2243–2256 (2020). https://doi.org/10.1007/s10695-020-00876-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00876-8

Keywords

Search

Navigation