Skip to main content
Log in

Characterization of non-lymphoid cells in the white pulp of the mouse spleen: An in vivo and in vitro study

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

Summary

Non-lymphoid cells (marginal metallophils, follicular immunecomplex-retaining cells, interdigitating cells), which are present in certain areas of the white pulp in the mouse spleen were characterized by means of (immuno)enzyme histochemical techniques, carbon uptake and experiments with lethal X-irradiation. Marginal metallophils are clearly present at the inner border of the marginal zone and show a very strong, E-600 sensitive, non-specific esterase (NSE) activity. Follicular immune-complex-retaining cells show a weak and diffuse NSE activity and no carbon uptake as shown by the combined application of an immunohistoperoxidase technique (for the demonstration of immune complexes), enzyme histochemistry (for NSE activity) and carbon uptake (for phagocytosis). Interdigitating cells show a distinct focus of NSE activity in the cytoplasm, weak carbon uptake and high radiation sensitivity. Demonstration of NSE activity is useful for the identification of the different non-lymphoid cells in the white pulp of the mouse spleen. It is suggested that the in vitro observed dendritic cells of Steinman and Cohn (1973) belong to the mononuclear phagocyte system, as “transitional cells” are encountered with cytological features of both dendritic cells and macrophages. These in vitro dendritic cells (or a portion of them) are probably similar to the interdigitating cells.

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

Abbreviations

HRP:

horseradish peroxidase

IDC:

interdigitating cells

PALS:

periarteriolar lymphocytic sheath

NSE:

non-specific esterase

References

  • Ballantyne, B.: The reticuloendothelial localization of splenic esterases. J. Reticuloendothelial Soc. 5, 399–411 (1968)

    Google Scholar 

  • Brown, J.C., Harris, G., Papamichail, M., Sljivić, V.S., Holborow, E.J.: The localization of aggregated human γ-globulin in the spleens of normal mice. Immunology 24, 955–968 (1973)

    Google Scholar 

  • Catayee, G., Chalet, M.: Compartement des cellules réticulaires phosphatasiques dans le parenchyme splénique de la souris normale et porteuze de tumeur. C.R. Soc. Biol. (Paris) 170, 794–797 (1976)

    Google Scholar 

  • Chen, L.L., Adams, J.C., Steinman, R.M.: Anatomy of germinal centers in mouse spleen, with special reference to “follicular dendritic cells”. J. Cell Biol. 77, 148–164 (1978)

    Google Scholar 

  • Davis, B.J., Ornstein, L.: High resolution enzyme localization with a new diazo reagent “Hexazonium Pararosaline”. J. Histochem. Cytochem. 7, 297–298 (1959)

    Google Scholar 

  • Duque, O.: Histology of the reticuloendothelial system of the spleen in mice of inbred strains. J. Nat. Cancer Inst. 35, 15–27 (1965)

    Google Scholar 

  • Eikelenboom, P.: Dendritic cells in the rat spleen follicles: a combined immuno- and enzyme histochemical study. Cell Tiss. Res. 190, 79–87 (1978)

    Google Scholar 

  • Ewijk, W. van, Verzijden, J.H.M., Kwast, Th.M. van der, Luijcx-Meyer, S.W.M.: Reconstitution of the thymus-dependent area in the spleen of letally irradiated mice. A light and electron microscopic study of the T-cell microenvironment. Cell Tiss. Res. 149, 43–60 (1974)

    Google Scholar 

  • Furth, R. van, Cohn, Z.A., Hirsch, J.G., Humphrey, J.H., Spector, W.G., Langevoort, H.L.: The mononuclear phagocyte system: a new classification of macrophages, monocytes and their precursor cells. Bull. Wld. Hlth. Org. 46, 845–852 (1972)

    Google Scholar 

  • Hanna, M.G., Jr, Szakal, A.K.: Localization of 125I labeled antigen in germinal centers of mouse spleen: histological and ultrastructural autoradiographic studies of the secondary immune reaction. J. Immunol. 101, 949–962 (1968)

    Google Scholar 

  • Hoefsmit, E.Ch.M.: Mononuclear phagocytes, reticulum cells, and dendritic cells in lymphoid tissues. In: Mononuclear phagocytes (Furth, R. van, ed.), pp. 129–146. Oxford: Blackwell Scientific Publications 1975

    Google Scholar 

  • Jaroslov, B.N., Nossal, G.J.V.: Effects of X-irradiation on antigen localization in lymphoid follicles. Austr. J. Exp. Biol. Med. Sci. 44, 609–628 (1968)

    Google Scholar 

  • Kamperdijk, E.A.W., Raaymakers, E.M., Leeuw, J.H.S. de, Hoefsmit, E.Ch.M.: Lymph node macrophages and reticulum cells in the immune response. I. The primary response to paratyphoid vaccine. Cell Tiss. Res. 192, 1–23 (1978)

    Google Scholar 

  • Katsura, S., Satodate, R., Fukuda Y., Terui Y.: Morphological studies on the reticuloendothelial system in tumor bearing hosts. I. Silver impregnation for reticuloendothelial cells. J. Iwate Med. Ass. 16, 232–236 (1964)

    Google Scholar 

  • Keene, W.R.: Detoxification of bacterial endotoxin by soluble tissue extracts. J. Lab. Clin. Med. 60, 433–438 (1962)

    Google Scholar 

  • Langevoort, H.L., Cohn, Z.A., Hirsch, J.G., Humphrey, J.H., Spector, W.G., Furth, R. van: The nomenclature of mononuclear phagocyte cells: a proposal for new classification. In: Mononuclear phagocytes (Furth, R. van, ed.), pp. 1–6. Oxford: Blackwell Scientific Publication 1970

    Google Scholar 

  • Marshall, A.H.E.: An outline of the cytology and pathology of the reticular tissue. Edinburgh: Oliver and Boyd 1956

    Google Scholar 

  • Meyer, A.E.F.H.: Semipermeable membranes for improving the histochemical demonstration of enzyme activities in tissue sections. I. Acid phosphatase. Histochemie 30, 31–39 (1972)

    Google Scholar 

  • Meyer, A.E.F.H., Vliedman, A.H.T.: Semipermeable membranes for improving the histochemical demonstration of enzyme activities in tissue sections. II. Non-specific esterase and β-glucuronidase. Histochemie 34, 127–132 (1973)

    Google Scholar 

  • Müller-Hermelink, H.K., Heusermann, U., Stutte, H.J.: Enzyme histochemical observations on the localization and structure of the T cell and B cell regions in the human spleen. Cell Tiss. Res. 154, 167–179 (1974)

    Google Scholar 

  • Nossal, G.J.V., Abbot, A., Mitchell, J., Lummus, Z.: Antigens in immunity. XV. Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J. Exp. Med. 127, 277–290 (1968)

    Google Scholar 

  • Pearse, A.G.E.: Histochemistry. Theoretical and applied, Vol. I, 3rd ed. Edinburgh: Churchill Livingstone 1968

    Google Scholar 

  • Pearse, A.G.E.: Histochemistry. Theoretical and applied, Vol. II, 3rd ed. Edinburgh: Churchill Livingstone 1972

    Google Scholar 

  • Pettersen, J.C.: A comparison of the metalophilic reticulo-endothelial cells to cells containing acid phosphatase and non-specific esterase in the lymphoid nodules of normal and stimulated rat spleens. Anat. Rec. 149, 269–278 (1964)

    Google Scholar 

  • Rooijen, N. van: A method for the separate detection of tritium and iodine radioisotopes in the same cell smears using a double autoradiographic stripping technique. J. Immunol. Methods 3, 71–78 (1973)

    Google Scholar 

  • Rooijen, N. van, Streefkerk, J.G.: Autoradiography and immunohistoperoxidase techniques applied to the same tissue sections. J. Immunol. Methods 10, 379–383 (1976)

    Google Scholar 

  • Satodate, R., Ogasawara, S., Sasou, S., Katsura, S.: Characteristic structure of the splenic white pulp of rats. J. Reticuloendothelial Soc. 10, 428–433 (1971)

    Google Scholar 

  • Smith, C., Wharton, T.J., Gerhardt, A.M.: Studies on the thymus of the mammal. XI. Histochemical studies of thymus, spleen and lymph node in normal and irradiated mice. Anat. Rec. 131, 369–386 (1958)

    Google Scholar 

  • Smith, E.E., Reitenburg, S.H., Reitenburg, A.M., Fine, J.: Detoxification of endotoxin by splenic extracts. Proc. Soc. Exp. Biol. Med. 113, 781–784 (1963)

    Google Scholar 

  • Snodgrass, M.J.: Cytochemical and functional aspects of the sinus-lining cells of the rabbit spleen. RES J. Reticuloendothelial Soc. 10, 184–199 (1971)

    Google Scholar 

  • Snodgrass, M.J., Snook, T.: A study of some histochemical and phagocytic reactions of the reticuloendothelial system of the rabbit spleen. Anat. Rec. 170, 243–254 (1971)

    Google Scholar 

  • Snook, T.: A comparative study of the vascular arrangement in mammalian spleens. Am. J. Anat. 87, 31–78 (1950)

    Google Scholar 

  • Snook, T.: Studies on the perifollicular region of the rat's spleen. Anat. Rec. 148, 149–160 (1964)

    Google Scholar 

  • Steinman, R.M., Cohn, Z.A.: Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation and tissue distribution. J. Exp. Med. 137, 1142–1162 (1973)

    Google Scholar 

  • Steinman, R.M., Cohn, Z.A.: Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J. Exp. Med. 139, 380–397 (1974)

    Google Scholar 

  • Steinman, R.M., Lustig, D.S., Cohn, Z.A.: Identification of a novel cell type in peripheral lymphoid organs of mice. III. Functional properties in vivo. J. Exp. Med. 139, 1431–1445 (1974)

    Google Scholar 

  • Steinman, R.M., Adams, J.C., Cohn, Z.A.: Identification of a novel cell type in peripheral lymphoid organs of mice. IV. Identification and distribution in mouse spleen. J. Exp. Med. 141, 804–820 (1975)

    Google Scholar 

  • Stevens, W.M., Snook, T.: The stimulatory effects of diethylstilbestrol and diethylstilbestrol diphosphate on the reticuloendothelial cells of the rat spleen. Am. J. Anat. 144, 339–360 (1975)

    Google Scholar 

  • Streefkerk, J.G., Veerman, A.J.P.: Histochemistry and electron microscopy of follicles lining reticular cells in the rat spleen. Z. Zellforsch. 115, 524–542 (1971)

    Google Scholar 

  • Veerman, A.J.P.: On the interdigitating cells in the thymus-dependent area of the rat spleen: a relation between the mononuclear phagocyte system and T lymphocytes. Cell Tiss. Res. 148, 247–257 (1974)

    Google Scholar 

  • Veerman, A.J.P., Ewijk, W. van: White pulp compartments in the spleen of rats and mice: a light and electron microscopic study of lymphoid and non-lymphoid cell types in T-and B-areas. Cell Tiss. Res. 156, 417–441 (1975)

    Google Scholar 

  • Veldman, J.E.: Histophysiology and electron microscopy of the immune response. Thesis, Groningen: N.V. Boekdrukkerij Dijkstra Niemeyer 1970

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eikelenboom, P. Characterization of non-lymphoid cells in the white pulp of the mouse spleen: An in vivo and in vitro study. Cell Tissue Res. 195, 445–460 (1978). https://doi.org/10.1007/BF00233888

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00233888

Key words

Navigation