Skip to main content
SpringerLink
Log in

Immunomodulatory effect of prolactin on Atlantic salmon (Salmo salar) macrophage function

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

Abstract

The in vitro and in vivo effect of prolactin (PRL) on kidney macrophages from Atlantic salmon (Salmo salar) was investigated under the assumption that PRL stimulates immune innate response in mammals. Kidney macrophages were treated two ways: first, cultured in RPMI 1640 medium containing 10, 25, 50 and 100 ng/mL of PRL and second, isolated from a fish with a PRL-injected dose of 100 ng/Kg. Reduced nitro blue tetrazolium (formazan) was used to produce intracellular superoxide anion. Phagocytic activity of PRL was determined in treated cells by optical microscopy observation of phagocytized Congo red-stained yeast. Kidney lysozyme activity was measured in PRL-injected fish. In vitro and in vivo macrophages treated with PRL presented an enhanced superoxide anion production, elevated phagocytic index and increased phagocytic activity. Treated fish showed higher levels of lysozyme activity in the head kidney compared to the control. These results indicate that PRL-stimulated innate immune response in Atlantic salmon and future studies will allow us to assess the possibility of using PRL as an immunostimulant in the Chilean salmon industry.

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

  • Almeida A, Rehder J, Dalge S, Martins-Filho J, Newburger P, Condino-Neto P (2005) The effect of IFN-γ and TNF-α on the NADPH oxidase system of human colostrum macrophages, blood monocytes, and THP-1 Cells. J Interferon Cytokine Res 25:540–546

    Article  PubMed  CAS  Google Scholar 

  • Andersen Ø, Skibeli V, Gautvik K (1989) Purification and characterization of Atlantic salmon prolactin. Gen Comp Endocrinol 73(3):354–360

    Article  PubMed  CAS  Google Scholar 

  • Aquaculture, Fisheries and Aquaculture Department, FAO (2010). www.fao.org/fishery/aquaculture/en. Accessed 13 Apr 2010

  • Bagni M, Romano N, Finoia M, Abelli L, Scapigliati G (2005) Short- and long-term effects of a dietary yeast beta-glucan (Macrogard) and alginic acid (Ergosan) preparation on immune response in sea bass (Dicentrarchus labrax). Fish Shellfish Immunol 18:311–325

    Article  PubMed  CAS  Google Scholar 

  • Bai N, Zhang W, Mai K, Wang X, Xu W, Ma H (2010) Effects of discontinuous administration of β-glucan and glycyrrhizin on the growth and immunity of white shrimp Litopenaeus vannamei. Aquaculture 306:218–224

    Article  CAS  Google Scholar 

  • Bole-Feysot H, Goffin V, Edery M, Binart N, Kelly P (1998) Prolactin and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19(3):225–268

    Article  PubMed  CAS  Google Scholar 

  • Bonaldo A, Thompson K, Manfrin A, Adams A, Murano E, Mordenti A, Gatta P (2009) The influence of dietary β-glucans on the adaptive and innate immune responses of European sea bass (Dicentrarchus labrax) vaccinated against vibriosis. Italian J Animal Sci 6(2):151–164

    Google Scholar 

  • Boutet I, Lorin-Nebel J, Lorgeril De, Guinand B (2007) Molecular characterisation of prolactin and analysis of extrapituitary expression in the European sea bass Dicentrarchus labrax under various salinity conditions. Comp Biochem Physiol D: Genomics Proteomics 2(1):74–83

    Article  PubMed  CAS  Google Scholar 

  • Cabello F (2004) Antibióticos y acuicultura en Chile: consecuencias para la salud humana y animal. Revista Médica de Chile 132:1001–1006

    Article  PubMed  CAS  Google Scholar 

  • Cabello F (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Ainsworth A (1992) Glucan administration potentiates immune defence mechanisms of channel catfish, Ictalurus punctatus Rafinesque. J Fish Dis 15:295–304

    Article  CAS  Google Scholar 

  • Chen Y, Johnson A (1993) In vivo activation of macrophages by prolactin from young and aging mice. Int J Immunopharmacol 15:39–43

    Article  PubMed  Google Scholar 

  • Clevenger C, Freier D, Kline J (1998) Prolactin receptor signal transduction in cells of the immune system. J Endocrinol 157:187–197

    Article  PubMed  CAS  Google Scholar 

  • Cook M, Hayball P, Hutchinson W, Nowak B, Hayball J (2003) Administration of a commercial immunostimulant preparation, EcoActiva™, as a feed supplement enhances macrophage respiratory burst and the growth rate of snapper (Pagrus auratus) in winter. Fish Shellfish Immunol 14:333–345

    Article  PubMed  CAS  Google Scholar 

  • Dimitrov T, Lange H, Fehm L, Born J (2004) A regulatory role for prolactin, growth hormone and corticosteroids for human T cell production of cytokines. Brain Behav Immun 18:368–374

    Article  PubMed  CAS  Google Scholar 

  • Engstad R, Robertsen B, Frivold E (1992) Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish Shellfish Immunol 2(4):287–297

    Article  Google Scholar 

  • Giacomini E, Iona E, Ferroni L (2001) Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J Immunol 166:7033–7040

    PubMed  CAS  Google Scholar 

  • Hoffman O, Olson E, Limper A (1993) Fungal β-glucans modulate macrophage release of tumor necrosis factor-alpha in response to bacterial lipopolysaccharide. Immunol Lett 37:19–25

    Article  PubMed  CAS  Google Scholar 

  • Jeney G, Anderson D (1993) Glucan injection or bath exposure given alone or in combination with bacterin enhance the non-specific defence mechanism in rainbow trout (Oncorhynchus mykiss). Aquaculture 116:315–329

    Article  CAS  Google Scholar 

  • Miranda C, Zemelman R (2002) Antimicrobial multiresistance in bacteria isolated from freshwater Chilean salmon farms. Sci Total Environ 293:207–218

    Article  CAS  Google Scholar 

  • Murtaugh P, Foss D (2002) Inflammatory cytokines and antigen presenting cell activation. Vet Immunol Immunopathol 87:109–114

    Article  PubMed  CAS  Google Scholar 

  • Narnaware Y, Kelly S, Woo Y (1998) Stimulation of macrophage phagocytosis and lymphocyte count by exogenous prolactin administration in silver sea bream (Sparus sarba) adapted to hyper- and hypo-osmotic salinities. Vet Immunol Immunopathol 61:387–391

    Article  PubMed  CAS  Google Scholar 

  • Olavarria V, Sepulcre M, Figueroa J, Mulero V (2010) Prolactin-induced production of reactive oxygen species and IL-1β in leukocytes from the bony fish gilthead seabream involves Jak/Stat and NF-κB signaling pathways. J Immunol 185:3873–3883

    Article  PubMed  CAS  Google Scholar 

  • Olavarria V, Figueroa F, Mulero V (2012) Prolactin-induced activation of phagocyte NADPH oxidase in the teleost fish gilthead seabream involves the phosphorylation of p47phox by protein kinase C. Dev Comp Immunol 36:216–221

    Article  PubMed  CAS  Google Scholar 

  • Ortega E, Forner A, Barriga C (1996) Effect of prolactin on the in vitro phagocytic capacity of macrophages. Comp Immunol Microbiol Infect Dis 19:139–146

    Article  PubMed  CAS  Google Scholar 

  • Pal D, Joardar S, Roy B (2007) Immunostimulatory effects of a yeast (Saccharomyces cerevisiae) cell wall feed supplement on rohu (Labeo rohita), an Indian major carp. Israeli J Aquacu–Bamidgeh 59:175–181

    Google Scholar 

  • Parry R Jr, Camden R, Shahani K (1965) A rapid and sensitive assay of muramidase. Proc Soc Exp Biol Med 119:384–386

    Google Scholar 

  • Paulsen S, Engstad E, Robertsen B (2000) Enhanced lysozyme production in Atlantic salmon (Salmo salar L.) macrophages treated with yeast β-glucan and bacterial lipopolysaccharide. Fish Shellfish Immunol 11:23–37

    Article  Google Scholar 

  • Peeva E, Venkatesh J, Michael D, Diamond B (2004) Prolactin as a modulator of B cell function: implications for SLE. Biomedecine Pharmacother 58:310–319

    Article  CAS  Google Scholar 

  • Sakai M, Kobayashi M, Kawauchi H (1996a) Mitogenic effect of growth hormone and prolactin on chum salmon (Oncorhynchus keta) leukocytes in vitro. Veterinay. Immunol Immunopathol 53:185–189

    Article  CAS  Google Scholar 

  • Sakai M, Kobayashi M, Kawauchi H (1996b) In vitro activation of fish phagocytic cells by GH, prolactin and somatolactin. J Endocrinol 151:113–118

    Article  PubMed  CAS  Google Scholar 

  • Szekanecz Z, Koch A (2007) Macrophages and their products in rheumatoid arthritis. Curr Opin Rheumatol 19:289–295

    Article  PubMed  Google Scholar 

  • Taylor P, Martinez-Pomares L, Stacey M, Lin H, Brown G, Gordon S (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23:901–944

    Article  PubMed  CAS  Google Scholar 

  • Tripathi A, Sodhi A (2008) Prolactin induced production of cytokines involves Jak/Stat and JNK MAP kinase pathways. Int Immunol 20:326–327

    Article  Google Scholar 

  • Wandurska-Nowak E (2004) The role of nitric oxide (NO) in parasitic infections. Wiad Parasytol 50:665–678

    Google Scholar 

  • Yada T, Nagae M, Moriyama S, Azuma T (1999) Effects of prolactin and growth hormone on plasma immunoglobulin M levels of hypophysectomized rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 115:46–52

    Article  PubMed  CAS  Google Scholar 

  • Yada T, Uchida K, Kajimura S, Azuma T, Hirano T, Grau E (2002) Immunomodulatory effects of prolactin and growth hormone in the tilapia, Oreochromis mossambicus. J Endocrinol 173:483–492

    Article  PubMed  CAS  Google Scholar 

  • Yada T, Misumi I, Muto K, Azuma T, Schreck C (2004) Effects of prolactin and growth hormone on proliferation and survival of cultured trout leucocytes. Gen Comp Endocrinol 136:298–306

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work is supported by FONDECYT grant 1040073 and DID-Doctorado grant 2005–07 from the Universidad Austral de Chile.

Author information

Authors and Affiliations

  1. Departamento de Ciencias Básicas, Facultad de Medicina, Universidad de La Frontera, Temuco, Chile

    Marco Paredes

  2. Escuela de Acuicultura, Universidad Católica de Temuco, Temuco, Chile

    Katerina Gonzalez

  3. Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile

    Jaime Figueroa

  4. Centro de Biotecnología en Reproducción (CEBIOR-BIOREN), Universidad de La Frontera, Temuco, Chile

    Enrique Montiel-Eulefi

Authors
  1. Marco Paredes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katerina Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaime Figueroa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Enrique Montiel-Eulefi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marco Paredes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paredes, M., Gonzalez, K., Figueroa, J. et al. Immunomodulatory effect of prolactin on Atlantic salmon (Salmo salar) macrophage function. Fish Physiol Biochem 39, 1215–1221 (2013). https://doi.org/10.1007/s10695-013-9777-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-013-9777-7

Keywords

Search

Navigation