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Fish Physiology and Biochemistry

, Volume 43, Issue 4, pp 1161–1174 | Cite as

Vitamin D3 affects innate immune status of European sea bass (Dicentrarchus labrax L.)

  • M. Dioguardi
  • F. A. Guardiola
  • M. Vazzana
  • A. Cuesta
  • M. A. Esteban
  • M. Cammarata
Article

Abstract

The effects of vitamin D3 dietary administration on certain innate immune parameters on the expression of immune-related genes in head-kidney (HK) and gut were investigated in European sea bass Dicentrarchus labrax. Vitamin D3 (vD3) was orally administered to fish in a commercial pellet food supplemented with 0 (control); 3750; 18,750; or 37,500 U kg−1. Furthermore, gut histology was considered. This study showed a modulation in the activities examined in fish fed with the addition of vD3. After just 2 weeks of administration, diet supplementation with the vitamin resulted in increased phagocytic ability, while serum peroxidase content was increased in fish fed with all experimental diets after 4 weeks, no significant differences were observed in protease, anti-protease, natural haemolytic complement activities and total IgM level. At gene level, fbl and rbl transcripts were up-regulated in HK in fish fed with the highest concentration of vD3-supplemented diets after 4 weeks, while in the gut, an up-regulation of hep gene was observed in fish fed with the different doses of vD3. These results suggest that vD3 may be of great interest for immunostimulatory purposes in fish farms.

Keywords

Cholecalciferol (vitamin D3Innate immunity European sea bass (Dicentrarchus labrax L.) Teleost 

Notes

Acknowledgements

This work was supported by grants from MC RITMARE project (CNR and CONISMA). The financial support of the Spanish Ministerio de Economía y Competitividad under grant no. AGL-2011-30381-C03-01 and of Fundación Séneca de la Región de Murcia (Spain) (grant no. 04538/GERM/06, Grupo de Excelencia de la Región de Murcia) is gratefully acknowledged. F.A. Guardiola benefited from grant by Fundação para a Ciência e Tecnologia, Portugal (SFRH/BPD/104497/2014).

Compliance with ethical standards

The experiments were performed in full compliance with the national rules (D. Lgs 116/92 and subsequent amendments) and the international European Commission Recommendation guidelines for the accommodation and care of animals used for experimental and other scientific purposes (2007/526/EC).

References

  1. Adorini I, Penna G, Giarratana N, Uskokovic M (2003) Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting allograft rejection and immune and autoimmune diseases. J Cell Biochem 1:227–233CrossRefGoogle Scholar
  2. Ai Q, Mai K, Zhang L, Tan B, Zhang W, Xu W et al (2007) Effects of dietary beta-1, 3 glucan on innate immune response of large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol 22:394–402CrossRefPubMedGoogle Scholar
  3. Alappat L, Valerio M, Awad AB (2010) Effect of vitamin D and β-sitosterol on immune function of macrophages. Int Immunopharmacol 10:1390–1396CrossRefPubMedGoogle Scholar
  4. Arnson Y, Amital H, Shoenfeld Y (2007) Vitamin D and autoimmunity: new etiological and therapeutical considerations. Ann Rheum Dis 66:1137–1142CrossRefPubMedPubMedCentralGoogle Scholar
  5. Atalah E, Cruz CMH, Izquierdo MS, Rosenlund G, Caballero MJ, Valencia A, Robaina L (2007) Two microalgae Crypthecodinium cohnii and Phaeodactylum tricornutum as alternative source of essential fatty acids in starter feeds for seabream (Sparus aurata). Aquaculture 270:178–185CrossRefGoogle Scholar
  6. Austin B, Austin DA (2005) Bacterial fish pathogens: diseases of farmed and wild fish, 4th ed. Springer-Praxis 2007, Chichester, UK. Hernandez P. Responsible use of antibiotics in aquaculture in: FAO(Ed), FAO Fisheries technical Paper N°469. Rome pp 1–97Google Scholar
  7. Baeke F, Korf H, Overbergh L, Verstuyf A, Gysemans C et al (2010) Human T lymphocytes are direct targets of 1, 25-dihydroxyvitamin D3 in the immune system. J Steroid Biochem 121:221–227CrossRefGoogle Scholar
  8. Bar-Shavit Z, Noff D, Edelstein S, Meyer M, Shibolet S, Goldman R (1983) 1, 25 dihydroxyvitamin D3 and the regulation of macrophage function. Calcif Tissue Int 33:673–676CrossRefGoogle Scholar
  9. Bich Hang BT, Phuong NT, Kestemont P (2014) Can immunostimulants efficiently replace antibiotic in striped catfish (Pangasianodon hypophthalmus) against bacterial infection by Edwardsiella ictaluri? Fish Shellfish Immunol 40:556–562CrossRefPubMedGoogle Scholar
  10. Cammarata M, Vazzana M, Accardi D, Parrinello N (2012) Seabream (Sparus aurata L) long-term dominant-subordinate interplay affects phagocytosis by peritoneal cavity cells. Brain Behav Immun 26:580–587CrossRefPubMedGoogle Scholar
  11. Cammarata M, Parisi MG, Benenati G, Vasta GR, Parrinello N (2014) A rhamnose-binding lectin from sea bass (Dicentrarchus labrax) plasma agglutinates and opsonizes pathogenic bacteria. Dev Comp Immunol 44:332–340CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cerezuela R, Cuesta A, Meseguer J, Esteban MA (2008) Effects of dietary vitamin D3 administration on innate immune parameters of seabream (Sparus aurata L.) Fish Shellfish Immun 26:243–245CrossRefGoogle Scholar
  13. Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MA, Esteban MÁ (2012a) Histological alterations and microbial ecology of the intestine in gilthead seabream (Sparus aurata L.) fed dietary probiotics and microalgae. Cell Tissue Res 350:477–489CrossRefPubMedGoogle Scholar
  14. Cerezuela R, Guardiola FA, González P, Meseguer J, Esteban MÁ (2012b) Effects of dietary Bacillus subtilis, Tetraselmis chuii, and Phaeodactylum tricornutum, singularly or in combination, on the immune response and disease resistance of sea bream (Sparus aurata L.) Fish Shellfish Immunol 33:242–249CrossRefGoogle Scholar
  15. Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MA, Esteban MÁ (2013) Changes in intestinal morphology and microbiota caused by dietary administration of inulin and Bacillus subtilis in gilthead sea bream (Sparus aurata L.) specimens. Fish Shellfish Immunol 34:1063–1070CrossRefPubMedGoogle Scholar
  16. Chomczynski P (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. BioTechniques 15:532–537PubMedGoogle Scholar
  17. Clem LW, Sizemore RC, Ellsaesser CF, Miller NW (1985) Monocytes as accessory cells in fish immune responses. Dev Comp Immunol 9:803–809CrossRefPubMedGoogle Scholar
  18. Cruz-Garcia L, Sánchez-Gurmaches J, Bouraoui L, Saera-Vila A, Pérez-Sánchez J, Gutiérrez J, Navarro I (2011) Changes in adipocyte cell size, gene expression of lipid metabolism markers, and lipolytic responses induced by dietary fish oil replacement in gilthead sea bream (Sparus aurata L.). Comp. Biochem Physiol 158:391–399Google Scholar
  19. Cuesta A, Meseguer J, Esteban MA (2004) Total serum immunoglobulin M levels are affected by immunomodulators in seabream (Sparus aurata L.) Vet Immunol Immunopathol 101:203–210CrossRefPubMedGoogle Scholar
  20. DeLuca HF (1988) The vitamin D story: a collaborative effort of basic science and clinical medicine. FASEB J 2:224–236PubMedGoogle Scholar
  21. Ellis T, Yildiz HY, Lopez-Olmeda J, Spedicato MT, Tort L, Øverli Ø, Martins CIM (2012) Cortisol and finfish welfare. Fish Physiol Biochem 38:163–188CrossRefPubMedGoogle Scholar
  22. Fujimoto RY, Santos RFB, Carneiro DJ (2013) Morphological deformities in the osseous structure in spotted sorubim Pseudoplatystoma coruscans (Agassiz & Spix, 1829) with vitamin c deficiency. An Acad Bras Cienc 85:379–384CrossRefPubMedGoogle Scholar
  23. Gannam AL, Schrock RM (2008) Immunostimulants in fish diets. J App Aquac 9:53–89CrossRefGoogle Scholar
  24. Guardiola FA, Cuesta A, Arizcun M, Meseguer J, Esteban MA (2014) Comparative skin mucus and serum humoral defence mechanisms in the teleost gilthead seabream (Sparus aurata). Fish Shellfish Immunol 36:545–551CrossRefPubMedGoogle Scholar
  25. Hanif A, Bakopoulos V, Dimitriadis GJ (2004) Maternal transfer of humoral specific and non-specific immune parameters to sea bream (Sparus aurata) larvae. Fish Shellfish Immunol 17:411–435CrossRefPubMedGoogle Scholar
  26. Hed J (1986) Methods for distinguishing ingested from adhering particles. Methods Enzymol 132:198–204CrossRefPubMedGoogle Scholar
  27. Hsieh JC, Pan CY, Chen JY (2010) Tilapia hepcidin (TH) 2-3 as a transgene in transgenic fish enhances resistance to Vibrio vulnificus infection and causes variations in immune-related genes after infection by different bacterial species. Fish Shellfish Immunol 30:1–10Google Scholar
  28. Kajita Y, Sakai M, Atsuta S, Kobayashi M (1990) The immunomodulatory effects of levamisole on rainbow trout Oncorhynchus mykiss. Fish Pathol 25:93–98CrossRefGoogle Scholar
  29. Karalazos V, Bendiksen EA, Dick JR, Tocher DR, Bell JG (2011) Influence of the dietary protein: lipid ratio and fish oil substitution on fatty acid composition and metabolism of Atlantic salmon (Salmo salar) reared at high water temperatures. Brit J Nutr 105:1012–1025CrossRefPubMedGoogle Scholar
  30. Keles O, Candan A, Bakırel T, Karatas S (2002) The investigation of the anabolic efficiency and effect on the non-specific immune system of zeranol in rainbow trout (Oncorhynchus mykiss, Walbaum). Turk J Vet Anim Sci 26:925–931Google Scholar
  31. Kiron V (2012) Fish immune system and its nutritional modulation for preventive health care. Anim Feed Sci Tech 173:111–133CrossRefGoogle Scholar
  32. Kitao T, Yoshida T, Anderson DP, Dixon OW, Blanch A (1987) Immunostimulation of antibody producing cells and humoral antibody to fish bacterins by a biological response modifier. J Fish Biol 31:87–91CrossRefGoogle Scholar
  33. Kumar V, Akinleye AO, Makkar HPS, Angulo-Escalante MA, Becker K (2011) Growth performance and metabolic efficiency in Nile tilapia (Oreochromis niloticus L.) fed on a diet containing Jatropha platyphylla kernel meal as a protein source. J Ani Physiol Ani Nutr 96:37–46CrossRefGoogle Scholar
  34. Labudzyns’kyĭ DO, Shymans’kyĭ IO, Riasnyĭ VM, Velykyĭ MM (2014) Vitamin D3 availability and functional activity of peripheral blood phagocytes in experimental type 1 diabetes. Ukr Biokhim Zh 86:107–118Google Scholar
  35. Mathieu C, Adorini L (2002) The coming of age of 1, 25- dihydroxyvitamin D(3) analogs as immunomodulatory agents. Trends Mol Med 8:174–179CrossRefPubMedGoogle Scholar
  36. Matsushita M, Endo Y, Taira S, Sato Y, Fujita T, Ichikawa N, Nakata M, Mizuochi TA (1996) Novel human serum lectin with collagen-and fibrinogen like domains that functions as an opsonin. J Biol Chem 271:2448–2454CrossRefPubMedGoogle Scholar
  37. Meena DK, Das P, Kumar S, Mandal SC, Prusty AK, Singh SK (2013) Beta-glucan: an ideal immunostimulant in aquaculture (a review). Fish Physiol Biochem 39:431–457CrossRefPubMedGoogle Scholar
  38. Neves JV, Caldas C, Vieira I, Ramos MF, Rodrigues PNS (2015) Multiple hepcidins in a teleost fish, Dicentrarchus labrax: different hepcidins for different roles. J Immunol 195:2696–2709CrossRefPubMedGoogle Scholar
  39. Oliva-Teles A (2012) Nutrition and health of aquaculture fish. J Fish Dis 35:83–108CrossRefPubMedGoogle Scholar
  40. Ortuno J, Esteban MA, Mulero V, Meseguer J (1998) Methods for studying the haemolytic, chemoattractant and opsonic activities of seabream (Sparus aurata L.). In: Barnes AC, Davidson GA, Hiney M, McInthos D (ed) Methodology in fish diseases research Albion Press, pp. 97–100Google Scholar
  41. Provvedini DM, Tsoukas CD, Deftos LJ, Manolagas SC (1983) 1,25-Dihydroxyvitamin D3 receptors in human leukocytes. Science 221:1181–1183CrossRefPubMedGoogle Scholar
  42. Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248CrossRefPubMedGoogle Scholar
  43. Quin C, Zhang Y, Liu W, Xu L, Yang Y, Zhou Z (2014) Effects of chito-oligosaccharides supplementation on growth performance, intestinal cytokine expression, autochthonous gut bacteria and disease resistance in hybrid tilapia Oreochromis niloticus, Oreochromis aureus. Fish Shellfish Immunol 40:267–274CrossRefGoogle Scholar
  44. Rao YV, Chakrabarti R (2004) Enhanced anti-proteases in Labeo rohita fed with diet containing herbal ingredients. Indian J Chem B 19:132–134Google Scholar
  45. Rao DS, Raghuramulu N (1999) Is vitamin D redundant in an aquatic habitat? J Nutr Sci Vitaminol 45:1–8CrossRefPubMedGoogle Scholar
  46. Reichrath J, Lehmann B, Carlberg C, Varani J, Zouboulis CC (2007) Vitamins as hormones. Horm Metab Res 39:71–84CrossRefPubMedGoogle Scholar
  47. Reschly EJ, Bainy AC, Mattos JJ, Hagey LR, Bahary N, Mado SR et al (2007) Functional evolution of the vitamin D and pregnane X receptors. BMC Evol Biol 7:222CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ringø E, Myklebust R, Mayhew T, Olsen R (2007) Bacterial translocation and pathogenesis in the digestive tract of larvae and fry. Aquaculture 268:251–264CrossRefGoogle Scholar
  49. Rodrigues PNS, Vazquez-dorado S, Neves JV, Wilson JM (2006) Dual function of fish hepcidin: response to experimental iron overload and bacterial infection in sea bass (Dicentrarchus labrax). Dev Comp Immunol 30:1156–1167CrossRefPubMedGoogle Scholar
  50. Ross NW, Firth KJ, Wang A, Burka JF, Johson SC (2000) Changes in hydrolytic enzyme activities of naïve Atlantic salmon Salmo salar skin mucus due to infection with the Salmon louse Lepeophtheirus salmonis and cortisol implantation. Dis Aquat Org 41:43–51CrossRefPubMedGoogle Scholar
  51. Sado RY, Bicudo AJA, Cyrino JEP (2013) Growth and hematology of juvenile pacu Piaractus mesopotamicus (Holmberg 1887) fed with increasing levels of vitamin E (DL-α-tocopheryl acetate). An Acad Bras Cienc 85:385–393PubMedGoogle Scholar
  52. Sahoo PK, Mukherjee SC (2002) Influence of high dietary α-tocopherol intakes on specific immune response, nonspecific resistance factors and disease resistance of healthy and aflatoxin B1-induced immunocompromised Indian major carp, Labeo rohita (Hamilton). Aquac Nutr 8:159–167CrossRefGoogle Scholar
  53. Sahoo PK, Mukherjee SC (2003) Immunomodulation by vitamin C in healthy and aflatoxin B1 induced immunocompromised rohu (Labeo rohita). Comp Immunol Microbiol Infs Dis 26:65–76CrossRefGoogle Scholar
  54. Sakai M (1999) Current research status of fish immunostimulant. Aquaculture 172:63–92CrossRefGoogle Scholar
  55. Sakai M, Kamiya H, Ishii S, Atsuta S, Kobayashi M (1992) The immunostimulating effects of chitin in rainbow trout, Oncorhynchus mykiss. In: Shariff M, Subasighe RP, Arthur JR (eds) Diseases in Asian aquaculture. Vol. 1. Fish Health Section, Asian Fisheries Society, Manila, pp 413–417Google Scholar
  56. Sakai M, Otubo T, Atsuta S, Kobayashi M (1993) Enhancement of resistance to bacterial infection in rainbow trout, Oncorhynchus mykiss Walbaum by oral administration of bovine lactoferrin. J Fish Dis 16:239–247CrossRefGoogle Scholar
  57. Shved N, Berishvili G, Mazel P, Baroiller JF, Eppler E (2011) Growth hormone (GH) treatment acts on the endocrine and autocrine/paracrine GH/IGF-axis and on TNF-α expression in bony fish pituitary and immune organs. Fish Shellfish Immunol 31:944–952CrossRefPubMedGoogle Scholar
  58. Subasinghe RP (2007) Epidemiological approach to aquatic animal health management: opportunities and challenges for developing countries to increase aquatic production through aquaculture. Prev Vet Med 67:117–124CrossRefGoogle Scholar
  59. Sundell K, Bishop JE, Björnsson BT, Norman AW (1992) 1,25-Dihydroxyvitamin D3 in the Atlantic cod: plasma levels, a plasma binding component, and organ distribution of a high affinity receptor. Endocrinol 131:2279–2286CrossRefGoogle Scholar
  60. Sutton AL, MacDonald PN (2003) Vitamin D: more than a “bone-a-fide” hormone. Mol Endocrinol 17:777–791CrossRefPubMedGoogle Scholar
  61. Vasta GR (2009) Roles of galectins in infection. Nat Rev Microbiol 7:424–438CrossRefPubMedPubMedCentralGoogle Scholar
  62. Verlhac V, Gabaudan J, Obach A, Schuep W, Hole R (1996) Influence of dietary glucan and vitamin Con non-specific and specific immune responses of rainbow trout Oncorhynchus mykiss. Aquaculture 143:123–133CrossRefGoogle Scholar
  63. Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotic bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wang KJ, Cai JJ, Cai L, Qu HD, Yang M, Zhang M (2009) Cloning and expression of a hepcidin gene from a marine fish (Pseudosciaena crocea) and the antimicrobial activity of its synthetic peptide. Peptides 30:638–646CrossRefPubMedGoogle Scholar
  65. Yamamoto N (2004) Vitamin D and the immune system. In: Roitt IM, Delves PJ (eds) Encyclopedia of immunology. Academic Press, London, pp 2494–2499Google Scholar
  66. Yoshida T, Sakai M, Kitao T, Khlil SM, Araki S, Saitoh R, Ineno T, Inglis V (1993) Immunomodulatory effects of the fermented products of chicken egg, EF203, on rainbow trout, Oncorhynchus mykiss. Aquaculture 109:207–214CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • M. Dioguardi
    • 1
  • F. A. Guardiola
    • 2
  • M. Vazzana
    • 1
  • A. Cuesta
    • 3
  • M. A. Esteban
    • 3
  • M. Cammarata
    • 1
  1. 1.Biological Chemical Pharmaceutical Sciences and TechnologiesUniversity of PalermoPalermoItaly
  2. 2.Fish Nutrition & Immunobiology Group, Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR)PortoPortugal
  3. 3.Fish Innate Immune System Group, Department of Cell Biology and Histology, Faculty of Biology, Campus Regional de Excelencia Internacional “Campus Mare Nostrum”University of MurciaMurciaSpain

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