Skip to main content

Advertisement

Log in

Early innate immune response and redistribution of inflammatory cells in the bony fish gilthead seabream experimentally infected with Vibrio anguillarum

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

An obvious difference between the immune system of fish and mammals is that fish lack both bone marrow and lymph nodes; in their place, the head-kidney acts as a major haematopoietic and lymphoid organ in adult fish, whereas the thymus, spleen and mucosa-associated lymphoid tissues are common to both fish and mammals. This suggests that differences exist in antigen presentation and naïve lymphocyte stimulation, a prerequisite for the initiation of adaptive immune responses. Intraperitoneal injection of the bony fish gilthead seabream (Sparus aurata L.) with intact Vibrio anguillarum, as a particulate bacterial antigen, results in the mobilisation of head-kidney leucocytes to the peritoneal cavity and priming of their respiratory burst activity. We have also observed the rapid infiltration of acidophilic granulocytes, which are leucocytes functionally equivalent to mammalian neutrophils, into the spleen. These cells may be involved in antigen capture and transport to the spleen, since an apparent association between mobilised acidophilic granulocytes, bacterial antigens and proliferating lymphocytes has been seen in this organ. Collectively, these results suggest that, in addition to being actively involved in bacterial clearance, fish phagocytic granulocytes play a role in the initiation and support of the adaptive immune response.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arnesen SM, Schrøder MB, Dalmo RA, Bøgwald J (2002) Antigen uptake and immunoglobulin production in Atlantic cod (Gadus morhua L.) after intraperitoneal injection of Vibrio anguillarum. Fish Shellfish Immunol 13:159–170

    Google Scholar 

  • Chaves-Pozo E, Pelegrín P, García-Castillo J, García-Ayala A, Mulero V, Meseguer J (2004) Acidophilic granulocytes of the marine fish gilthead seabream (Sparus aurata L.) produce interleukin-1β following infection with Vibrio anguillarum. Cell Tissue Res 316:189–195

    Article  Google Scholar 

  • Ellis TN, Beaman BL (2004) Interferon-γ activation of polymorphonuclear neutrophil function. Immunology 112:2–12

    Article  Google Scholar 

  • Espenes A, Press CM, Dannevig BH, Landsverk T (1995) Immune-complex trapping in the splenic ellipsoids of rainbow trout (Oncorhynchus mykiss). Cell Tissue Res 282:41–48

    Google Scholar 

  • Espenes A, Press CM, Rooijen NV, Landsverk T (1997) Apoptosis in phagocytotic cells of lymphoid tissues in rainbow trout (Oncorhynchus mykiss) following administration of clodronate liposomes. Cell Tissue Res 289:323–331

    Article  Google Scholar 

  • Fänge R (1986) Lymphoid organs in sturgeons (Acipenseridae). Vet Immunol Immunopathol 12:153–161

    Article  Google Scholar 

  • Ferguson HW, Claxton MJ, Moccia RD, Wilkie EJ (1982) The quantitative clearance of bacteria from the bloodstream of rainbow trout (Salmo gairdneri). Vet Pathol 19:687–699

    Google Scholar 

  • García-Castillo J, Chaves-Pozo E, Olivares P, Pelegrín P, Meseguer J, Mulero V (2004) The tumor necrosis factor α of the bony fish seabream exhibits the in vivo proinflammatory and proliferative activities of its mammalian counterparts, yet it functions in a species-specific manner. Cell Mol Life Sci 61:1331–1340

    Article  Google Scholar 

  • Grove S, Høie S, Evensen Ø (2003) Distribution and retention of antigens of Aeromonas salmonicida in Atlantic salmon (Salmo salar L.) vaccinated with a Δ aroA mutant or formalin-inactivated bacteria in oil-adjuvant. Fish Shellfish Immunol 15:349–358

    Google Scholar 

  • Herbomel P, Thisse B, Thisse C (2001) Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol 238:274–288

    Article  Google Scholar 

  • Kaattari SL, Irwin MJ (1985) Salmonid spleen and anterior kidney harbor populations of lymphocytes with different B cell repertoires. Dev Comp Immunol 9:433–444

    Google Scholar 

  • Kobayashi SD, Voyich JM, DeLeo FR (2003) Regulation of the neutrophil-mediated inflammatory response to infection. Microbes Infect 5:1337–1344

    Article  Google Scholar 

  • Meseguer J, López-Ruiz A, García-Ayala A (1995) Reticulo-endothelial stroma of the head-kidney from the seawater teleost gilthead seabream (Sparus aurata L.): an ultrastructural and cytochemical study. Anat Rec 241:303–309

    Google Scholar 

  • Mulero V, Pelegrín P, Sepulcre MP, Muñoz J, Meseguer J (2001) A fish cell surface receptor defined by a mAb mediates leukocyte aggregation and deactivation. Dev Comp Immunol 25:619–627

    Google Scholar 

  • Press CM, Evensen Ø (1999) The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 9:309–318

    Article  Google Scholar 

  • Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, Ostrowski MC, Himes SR, Hume DA (2003) A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101:1155–1163

    Article  Google Scholar 

  • Sepulcre MP, Pelegrín P, Mulero V, Meseguer J (2002) Characterisation of gilthead seabream acidophilic granulocytes by a monoclonal antibody unequivocally points to their involvement in fish phagocytic response. Cell Tissue Res 308:97–102

    Article  Google Scholar 

  • Stensvåg K, Bøgwald J, Smedsrød B, Jørgensen T (1999) Distribution of intravenously injected A-layer protein and lipopolysaccharide (LPS) from Aeromonas salmonicida in Atlantic salmon, Salmo salar L. Fish Shellfish Immunol 9:591–607

    Google Scholar 

  • Sternberger LA (1986) Immunocytochemistry. Wiley, New York

    Google Scholar 

  • Thisse C, Zon LI (2002) Organogenesis—heart and blood formation from the zebrafish point of view. Science 295:457–462

    Article  Google Scholar 

  • Toranzo AE, Barja JL (1990) A review of the taxonomy and seroepizootiology of Vibrio anguillarum, with special reference to aquaculture in the northwest of Spain. Dis Aquat Org 9:73–82

    Google Scholar 

Download references

Acknowledgements

We thank Drs. A.E. Toranzo and J.L. Barja (University of Santiago) for the bacterium and its specific antiserum.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Victoriano Mulero.

Additional information

This work was supported by the Spanish Ministry of Science and Technology (grants BIO2001-2324-C02-02, AGL2002-03529 and AGL2002-04306-C03-01 to V.M. and J.M. and Programa Ramón y Cajal’s contract to P.M.), Spanish Ministry of Education, Culture and Sport (fellowship to E.C.-P.) and the Fundación Séneca (grant PI-51/00782/FS/01 to J.M. and fellowship to P.P.).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chaves-Pozo, E., Muñoz, P., López-Muñoz, A. et al. Early innate immune response and redistribution of inflammatory cells in the bony fish gilthead seabream experimentally infected with Vibrio anguillarum. Cell Tissue Res 320, 61–68 (2005). https://doi.org/10.1007/s00441-004-1063-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-004-1063-7

Keywords

Navigation