Skip to main content
Log in

Immune-complex trapping in the splenic ellipsoids of rainbow trout (Oncorhynchus mykiss)

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

Abstract

Rainbow trout (Oncorhynchus mykiss), immunised with horseradish peroxidase, were given horseradish peroxidase intravenously, and the trapping of antigen in the spleen was followed 1, 24, and 48 h after injection. After 1 h, the localisation of horseradish peroxidase indicated that the antigen had been extensively trapped in the walls of the splenic ellipsoids. The colocalisation of horseradish peroxidase with rainbow trout immunoglobulin M and complement factor 3 was shown with a double immunofluorescence technique and suggested that horseradish peroxidase was trapped in the form of immune complexes. After 24 and 48 h, very little horseradish peroxidase was detected in the ellipsoids, and horseradish peroxidase was mainly found in association with large cells with prominent cytoplasmic extensions. In nonimmunised fish given horseradish peroxidase intravenously, antigen was not detected in ellipsoids. Thus, the observed difference between immunised and nonimmunised trout suggests a specific role for the splenic ellipsoids in rapid immune-complex trapping and invites speculation on its significance in a secondary 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.

Similar content being viewed by others

References

  • Arkoosh MR, Kaattari SL (1991) Development of immunological memory in rainbow trout (Oncorhynchus mykiss). I. An immunochemical and cellular analysis of the B cell response. Dev Comp Immunol 15:279–293

    Google Scholar 

  • Bjerring Jensen L, Koch C (1992) Use of monoclonal and polyclonal antibodies to analyse the degradation of rainbow trout C3 in inulin-activated serum. Fish Shellfish Immunol 2:241–249

    Google Scholar 

  • Blue J, Weiss L (1981) Periaterial macrophage sheaths (ellipsoids) in cat spleen — an electron microscope study. Am J Anat 161:115–134

    Google Scholar 

  • Brattgjerd S (1994) Nonspecific immunity of Atlantic salmon-with special emphasis on macrophages and the complement system. Thesis, Norwegian College of Veterinary Medicine, Oslo, Norway

  • Brown EM, Dellmann H-D, Nicander L, Landsverk T (1993) Lymphatic organs. In: Dellmann H-D (ed) Textbook of veterinary histology, 4th edn. Lea & Febiger, Philadelphia, pp 120–135

    Google Scholar 

  • Buyssens N, Paulus G, Bourgeois N (1984) Ellipsoids in the human spleen. Virchows Arch [A] 403:27–40

    Google Scholar 

  • Chen LL, Frank AM, Adams JC, Steinman RM (1978) Distribution of horseradish peroxidase (HRP)-anti-HRP immune complexes in mouse spleen with special reference to follicular dendritic cells. J Cell Biol 79:184–199

    Google Scholar 

  • Dannevig BH, Berg T (1978) Uptake and proteolysis of denatured human serum albumin by kidneys in chars (Salmo alpinus L.). Comp Biochem Physiol 59:299–303

    Google Scholar 

  • Davies KA, Erlendsson K, Beynon HLC, Peters AM, Steinsson K, Valdimarsson H, Walport MJ (1993) Splenic uptake of immune complexes in man is complement-dependent. J Immunol 151:3866–3873

    Google Scholar 

  • Dustin P (1975) Ultrastructure and function of the ellipsoids of the spleen. Their relationship with fat metabolism and red blood cells. Haematologica 60:136–155

    Google Scholar 

  • Eikelenboom P, Kroese FGM, Van Rooijen N (1983) Immune complex-trapping cells in the spleen of the chicken. Cell Tissue Res 231:377–386

    Google Scholar 

  • Ellis AE (1980) Antigen-trapping in the spleen and kidney of the plaice Pleuronectes platessa L. J Fish Dis 3:413–426

    Google Scholar 

  • Espenes A, Press CM, Dannevig BH, Landsverk T (1995) Investigation of the structural and functional features of splenic ellipsoids in rainbow trout (Oncorhynchus mykiss). Cell Tissue Res 279:469–474

    Google Scholar 

  • Glick B, Oláh I (1984) A continuum of cells leading to an in-vivo humoral response. Immunol Today 5:162–165

    Google Scholar 

  • Graf R, Schlüns J (1979) Ultrastructural and histochemical investigation of the terminal capillaries in the spleen of the carp (Cyprinus carpio L.). Cell Tissue Res 196:289–306

    Google Scholar 

  • Irwin MJ, Kaattari SL (1986) Salmonid B lymphocytes demonstrate organ dependent functional heterogeneity. Vet Immunol Immunopathol 12:39–45

    Google Scholar 

  • Jeurissen SHM, Janse EM, De Boer GF (1991) Antigen handling by nonlymphoid cells in the chicken spleen. In: Imhof B, Ezine S (eds) Lymphatic tissues and in vivo immune responses. Marcel Dekker, New York, pp 771–775

    Google Scholar 

  • Klaus GGB, Humphrey JM (1977) The generation of memory cells I. The role of C3 in the generation of B memory cells. Immunology 33:31–40

    Google Scholar 

  • Kroese FGM, Van Rooijen N (1982) The architecture of the spleen of the red-eared slider, Chrysemys scripta elegans (Reptilia, Testudines). J Morphol 173:279–284

    Google Scholar 

  • Maas MG, Bootsma R (1982) Uptake of bacterial antigens in the spleen of carp (Cyprinus carpio L.). Dev Comp Immunol 2 [Suppl]:47–52

    Google Scholar 

  • Miller GW, Nussenzweig V (1975) A new complement function: solubilization of antigen-antibody aggregates. Proc Natl Acad Sci USA 72:418–422

    Google Scholar 

  • Mills ES (1926) The vascular arrangements of the mammalian spleen. Quart J Exp Physiol 16:301–319

    Google Scholar 

  • Nossal GJV, Ada GL (1971) Antigens, lymphoid cells and the immune response. Academic Press, New York

    Google Scholar 

  • Oláh I, Glick B (1982) Splenic white pulp and associated vascular channels in chicken spleen. Am J Anat 165:445–480

    Google Scholar 

  • Press CM, Dannevig BH, Landsverk T (1994) Immune and enzyme histochemical phenotypes of lymphoid and nonlymphoid cells within the spleen and head kidney of Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 4:79–93

    Google Scholar 

  • Pulsford A, Fänge R, Morrow WJW (1982) Cell types and interactions in the spleen of the dogfish Scyliorhinus canicula L.: an electron microscopic study. J Fish Biol 21:649–662

    Google Scholar 

  • Quesada J, Villena MI, Agullerio B (1990) Structure of the spleen of the sea bass (Dicentrarchus labrax): a light and electron microscopic study. J Morphol 206:273–281

    Google Scholar 

  • Sakai DK (1992) Repertoire of complement in immunological defence mechanisms of fish. Annu Rev Fish Dis 2:223–247

    Google Scholar 

  • Schweigger-Seidel F (1863) Untersuchungen über die Milz. Virchows Arch [A] 27:460–504

    Google Scholar 

  • Secombes CJ, Manning MJ (1980) Comparative studies on the immune system of fishes and amphibians: antigen localization in the carp Cyprinus carpio L. J Fish Dis 3:399–412

    Google Scholar 

  • Secombes CJ, Manning MJ, Ellis AE (1982) Localization of immune complexes and heat-aggregated immunoglobulin in the carp Cyprinus carpio L. Immunology 47:101–105

    Google Scholar 

  • Tatner MF, Findlay C (1991) Lymphocyte migration and localisation patterns in rainbow trout Oncorhynchus mykiss, studied using the tracer sample method. Fish Shellfish Immunol 1: 107–117

    Google Scholar 

  • Tew JG, Phipps RP, Mandel TE (1980) The maintenance and regulation of the humoral immune response: persisting antigen and the role of follicular antigen-binding dendritic cells as accessory cells. Immunol Rev 53:175–201

    Google Scholar 

  • Tew JG, Kosco MH, Szakal AK (1989) The alternative antigen pathway. Immunol Today 10:229–232

    Google Scholar 

  • Thuvander A, Fossum C, Lorenzen N (1990) Monoclonal antibodies to salmonid immunoglobulin: characterization and applicability in immunoassays. Dev Comp Immunol 14:415–423

    Google Scholar 

  • Van Rooijen N (1990) Antigen processing and presentation in vivo: the microenvironment as a crucial factor. Immunol Today 11:436–439

    Google Scholar 

  • Weiss L (1988) The spleen. In: Weiss L (ed) Cell and tissue biology. A textbook of histology, 6th edn. Urban & Schwarzenberg, Baltimore München, pp 515–538

    Google Scholar 

  • White RG (1981) Antigen transport in the spleen. Immunol Today 2:150–151

    Google Scholar 

  • White RG, Gordon J (1970) Macrophage reception and recognition mechanisms in the chicken spleen. In: van Furth R (ed) Mononuclear phagocytes. Blackwell, Oxford, pp 510–523

    Google Scholar 

  • White RG, Henderson DC, Eslami MB, Nielsen KH (1975) Localization of a protein antigen in the chicken spleen. Effect of various manipulative procedures on the morphogenesis of the germinal centre. Immunology 28:1–21

    Google Scholar 

  • Wilson MR, Warr GW (1992) Fish immunoglobulins and the genes that encode them. Annu Rev Fish Dis 2:201–221

    Google Scholar 

  • Yoffey JM (1929) A contribution to the study of the comparative histology and physiology of the spleen, with reference chiefly to its cellular constituents. J Anat 63/64:314–344

    Google Scholar 

  • Zapata A (1982) Lymphoid organs of teleost fish. III. Splenic lymphoid tissue of Rutilus rutilus and Gobio gobio. Dev Comp Immunol 6:87–94

    Google Scholar 

  • Zapata AG, Cooper EL (1990) The immune system: Comparative histophysiology. Wiley, Chichester

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Espenes, A., Press, C.M., Dannevig, B.H. et al. Immune-complex trapping in the splenic ellipsoids of rainbow trout (Oncorhynchus mykiss). Cell Tissue Res 282, 41–48 (1995). https://doi.org/10.1007/BF00319131

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00319131

Key words

Navigation