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Potential use of bovine lactoferrin as adjuvant for the modulation of the specific immune response in rainbow trout (Oncorhynchus mykiss W.)

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Abstract

The present experiment was carried out in order to evaluate the potential adjuvant effect of bovine lactoferrin (bLF) in modulating the specific antibody (Ab) response to an exogenous protein, the human-γ-globulins (HγG), injected intraperitoneally in rainbow trout Oncorhynchus mykiss (Walbaum 1792). Moreover, serum natural antibody (NatAb) level, serum total immunoglobulin (IgM) level and specific Ab response to bLF were also analysed. Experimental data showed that HγG is able to stimulate a specific Ab response when not adjuvanted with Freund’s complete adjuvant (FCA), whereas bLF induces a specific Ab response only if adjuvanted with FCA. Statistical analyses revealed that neither bLF or FCA administered singly had significant effects on serum NatAb and IgM levels, whereas the specific immune response observed against HγG when adjuvanted with bLF was comparable to that achieved when FCA was used as the adjuvant. These results provide evidence of the potential for bLF to be used as an adjuvant for salmonids.

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References

  • Anderson DP (1992) Immunostimulants, adjuvants, and vaccine carriers in fish: applications to aquaculture. Annu Rev Fish Dis 2:281–307. doi:10.1016/0959-8030(92)90067-8

    Article  Google Scholar 

  • Berg A, Rødseth T, Tangerås A, Hansen TJ (2006) Time of fish vaccination influences development of adherences, growth and spinal deformities in Atlantic salmon (Salmo salar L.). Dis Aquat Org 69:239–248. doi:10.3354/dao069239

    Article  PubMed  Google Scholar 

  • Cecchini S, Caputo AR (2010) Seminal plasma of brown trout, Salmo trutta fario (L.) contains a factor able to retain iron at acid pH, typical feature of lactoferrin. Fish Shell Immunol 28:927–930. doi:10.1016/j.fsi.2010.02.013

    Article  CAS  Google Scholar 

  • Cecchini S, Saroglia M (2002) Antibody response in sea bass (Dicentrarchus labrax, L.) in relation to water temperature and oxygenation. Aquacult Res 33:607–613. doi:10.1046/j.1365-2109.2002.00698.x

    Article  Google Scholar 

  • Cecchini S, Caputo AR, Mecca F (2004) Enhancement of pH-resistant iron-binding activity in supernatants of rainbow trout blood leucocytes by in vitro treatment with phorbol-12-myristate-13-acetate. J Fish Biol 65:1653–1656. doi:10.1111/j.0022-1112.2004.00555.x

    Article  CAS  Google Scholar 

  • Cecchini S, Caputo AR, Mecca F (2005) Evaluation of in vitro endocytosis and antibody synthesis by rainbow trout head kidney cells treated with bovine lactoferrin. J Fish Biol 66:609–617. doi:10.1111/j.0022-1112.2005.00624.x

    Article  CAS  Google Scholar 

  • Chodaczek G, Zimecki M, Lukasiewicz J, Lugowski C (2006) A complex of lactoferrin with monophosphoryl lipid A is an efficient adjuvant of the humoral and cellular immune response in mice. Med Microbiol Immunol 195:207–216. doi:10.1007/s00430-006-0020-3

    Article  CAS  PubMed  Google Scholar 

  • Crowther JR (2001) The ELISA Guidebook. Humana Press, Totowa

    Google Scholar 

  • Cuesta A, Esteban MA, Meseguer J (2004) Total serum immunoglobulin M levels are affected by immunomodulators in seabream (Sparus aurata L.) specimens. Vet Immunol Immunopathol 101:203–210. doi:10.1016/j.vetimm.2004.04.021

    Article  CAS  PubMed  Google Scholar 

  • Drago-Serrano ME, Rivera-Aguilar V, Reséndiz-Albor AA, Campos-Rodríguez R (2010) Lactoferrin increases both resistance to Salmonella typhimurium infection and the production of antibodies in mice. Immunol Lett 134:35–46. doi:10.1016/j.imlet.2010.08.007

    Article  CAS  PubMed  Google Scholar 

  • Eslamloo K, Falahatkar B, Yokoyama S (2012) Effects of dietary bovine lactoferrin on growth, physiological performance, iron metabolism and non-specific immune responses of Siberian sturgeon Acipenser baeri. Fish Shell Immunol 32:976–985. doi:10.1016/j.fsi.2012.02.007

    Article  CAS  Google Scholar 

  • Esteban MA, Rodriguez A, Cuesta A, Meseguer J (2005) Effects of lactoferrin on non-specific immune responses of gilthead seabream (Sparus auratus L.). Fish Shell Immunol 18:109–124. doi:10.1016/j.fsi.2004.06.003

    Article  CAS  Google Scholar 

  • Gudmundsdóttir S, Magnadóttir B, Björnsdóttir B, Árnadóttir H, Gudmundsdóttir BK (2009) Specific and natural antibody response of cod juveniles vaccinated against Vibrio anguillarum. Fish Shell Immunol 26:619–624. doi:10.1016/j.fsi.2008.09.017

    Article  Google Scholar 

  • Guy B (2007) The perfect mix: recent progress in adjuvant research. Nat Rev Microbiol 5:505–517. doi:10.1038/nrmicro1681

    Article  CAS  PubMed  Google Scholar 

  • Hung C-M, Wu S-C, Yen C-C, Lin M-F, Lai Y-W, Tung Y-T, Chen H-L, Chen C-M (2010) Porcine lactoferrin as feedstuff additive elevates avian immunity and potentiates vaccination. Biometals 23:579–587. doi:10.1007/s10534-010-9321-5

    Article  CAS  PubMed  Google Scholar 

  • Hwang S-A, Wilk KM, Budnicka M, Olsen M, Bangale YA, Hunter RL, Kruzel ML, Actor JK (2007) Lactoferrin enhanced efficacy of the BCG vaccine to generate host protective responses against challenge with virulent Mycobacterium tuberculosis. Vaccine 25:6730–6743. doi:10.1016/j.vaccine.2007.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kakuta I (1997) Suppression of stress reactions of rainbow trout, Oncorhynchus mykiss, reared at high density by oral administration of bovine lactoferrin. Suisan Zoshoku 45:345–350

    CAS  Google Scholar 

  • Kakuta I (1998) Reduction of stress response in carp, Cyprinus carpio L., held under deteriorating environmental conditions, by oral administration of bovine lactoferrin. J Fish Dis 21:161–167. doi:10.1046/j.1365-2761.1998.00087.x

    Article  CAS  PubMed  Google Scholar 

  • Kamilya D, Maiti TK, Joardar SN, Mal BC (2006) Adjuvant effect of mushroom glucan and bovine lactoferrin upon Aeromonas hydrophila vaccination in catla, Catla catla (Hamilton). J Fish Dis 29:331–337. doi:10.1111/j.1365-2761.2006.00722.x

    Article  CAS  PubMed  Google Scholar 

  • Köllner B, Kotterba G (2002) Temperature dependent activation of leukocyte populations of rainbow trout, Oncorhynchus mykiss, after intraperitoneal immunisation with Aeromonas salmonicida. Fish Shellfish Immunol 12:35–48. doi:10.1006/fsim.2001.0352

    Article  PubMed  Google Scholar 

  • Kumari J, Sahoo PK (2006) Dietary immunostimulants influence specific immune response and resistance of healthy and immunocompromised Asian catfish Clarias batrachus to Aeromonas hydrophila infection. Dis Aquat Org 70:63–70. doi:10.3354/dao070063

    Article  CAS  PubMed  Google Scholar 

  • Kumari J, Swain T, Sahoo PK (2003) Dietary bovine lactoferrin changes in immunity level and disease resistance in Asian catfish Clarias batrachus. Vet Immunol Immunopathol 94:1–9. doi:10.1016/S0165-2427(03)00065-5

    Article  CAS  PubMed  Google Scholar 

  • Langston AL, Bricknell IR, Ellis AE (1998) Iron binding capacity of peripheral blood leucocyte lysates from Atlantic salmon (Salmo salar L.). In: Barnes AC, Davidson GA, Hiney MP, McIntosh D (eds) Methodology in fish disease research. Fisheries Research Services, Aberdeen, pp 111–116

    Google Scholar 

  • Legrand D, Mazurier J (2010) A critical review of the roles of host lactoferrin in immunity. Biometals 23:365–376. doi:10.1007/s10534-010-9297-1

    Article  CAS  PubMed  Google Scholar 

  • Lönnerdal B, Iyer S (1995) Lactoferrin: molecular structure and biological function. Annu Rev Nutr 15:93–110. doi:10.1146/annurev.nu.15.070195.000521

    Article  PubMed  Google Scholar 

  • Magnadottir B, Jónsdóttir H, Helgason S, Björnsson B, Solem ST, Pilstrom L (2001) Immune parameters of immunized cod (Gadus morhua L.). Fish Shell Immunol 11:75–89. doi:10.1006/fsim.2000.0296

    Article  CAS  Google Scholar 

  • Małaczewska J, Wójcik M, Wójcik R, Siwicki AK (2010) The in vitro effect of bovine lactoferrin on the activity of organ leukocytes in rainbow trout (Oncorhynchus mykiss), European eel (Anguilla anguilla) and wels catfish (Silurus glanis). Pol J Vet Sci 13:83–88

    PubMed  Google Scholar 

  • Miyauchi H, Kaino A, Shinoda I, Fukuwatari Y, Hayasawa H (1997) Immunomodulatory effect of bovine lactoferrin pepsin hydrolysate on murine splenocytes and Peyer’s patch cells. J Dairy Sci 80:2330–2339

    Article  CAS  PubMed  Google Scholar 

  • Rahimnejad S, Agh N, Kalbassi MR, Khosravi S (2012) Effect of dietary bovine lactoferrin on growth, haematology and non-specific immune response in rainbow trout (Oncorhynchus mykiss). Aquacult Res 43:1451–1459. doi:10.1111/j.1365-2109.2011.02947.x

    Article  CAS  Google Scholar 

  • 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 16:239–247. doi:10.1111/j.1365-2761.1993.tb01253.x

    Article  CAS  Google Scholar 

  • Wang Y-D, Chang H-Y, Chen J-Y, Chen J-C (2013) Oral administration of bovine lactoferrin inhibits bacterial infection in tilapia and elevates survival after bacterial infection: an examination of its immune-modulating properties. Aquacult Int 21:75–96. doi:10.1007/s10499-012-9537-1

    Article  Google Scholar 

  • Welker TL, Lim C, Yildirim-Aksoy M, Klesius PH (2007) Growth, immune function, and disease and stress resistance of juvenile Nile tilapia (Oreochromis niloticus) fed graded levels of bovine lactoferrin. Aquaculture 262:156–162. doi:10.1016/j.aquaculture.2006.09.036

    Article  CAS  Google Scholar 

  • Welker TL, Lim C, Yildirim-Aksoy M, Klesius PH (2010) Dietary bovine lactoferrin increases resistance of juvenile channel catfish, Ictalurus punctatus, to enteric septicaemia. J World Aquacult Soc 41(S1):28–39. doi:10.1111/j.1749-7345.2009.00330.x

    Article  Google Scholar 

  • Yokoyama S, Koshio S, Takakura N, Oshida K, Ishikawa M, Gallardo-Cigarroa FJ, S-i Teshima (2005) Dietary bovine lactoferrin enhance tolerance to high temperature stress in Japanese flouder Paralichthys olivaceus. Aquaculture 249:367–373. doi:10.1016/j.aquaculture.2005.03.024

    Article  CAS  Google Scholar 

  • Zimecki M, Kruzel ML (2000) Systemic or local co-administration of lactoferrin with sensitizing dose of antigen enhances delayed type hypersensitivity in mice. Immunol Let 74:183–188. doi:10.1016/S0165-2478(00)00260-1

    Article  CAS  Google Scholar 

  • Zimecki M, Mazurier J, Machnicki M, Wieczorek Z, Montreuil J, Spik G (1991) Immunostimulatory activity of lactotransferrin and maturation of CD4–CD8-murine thymocyte. Immunol Lett 30:119–124. doi:10.1016/0165-2478(91)90099-V

    Article  CAS  PubMed  Google Scholar 

  • Zimecki M, Mazurier J, Spik G, Kapp JA (1995) Human lactoferrin induces phenotypic and functional changes in splenic mouse B cells. Immunology 86:112–127

    Google Scholar 

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Acknowledgments

This study has been financially supported by University of Basilicata, Italy.

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Authors and Affiliations

  1. Dipartimento di Scienze, Università degli Studi della Basilicata, Viale dell’Ateneo Lucano 10, 85100, Potenza, Italy

    Stefano Cecchini

  2. Indipendent Agronomist, Baragiano, PZ, Italy

    Anna Rocchina Caputo

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  1. Stefano Cecchini
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  2. Anna Rocchina Caputo
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Correspondence to Stefano Cecchini.

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Cecchini, S., Caputo, A.R. Potential use of bovine lactoferrin as adjuvant for the modulation of the specific immune response in rainbow trout (Oncorhynchus mykiss W.). Aquacult Int 25, 223–232 (2017). https://doi.org/10.1007/s10499-016-0024-y

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  • DOI: https://doi.org/10.1007/s10499-016-0024-y

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