Advertisement

Cell and Tissue Research

, Volume 275, Issue 1, pp 51–62 | Cite as

Development and cell phenotypes in primary follicles of foetal sheep lymph nodes

  • Marit Halleraker
  • Charles McL. Press
  • Thor Landsverk
Article

Abstract

Lymph nodes from sheep foetuses and postnatal lambs were examined to determine the participation of different leucocyte populations in primary follicle formation, with special emphasis on the emergence and subsequent development of follicular dendritic cells during late gestation and early postnatal life. A series of immune and enzyme histochemical markers was used. The first 5′-nucleotidase-positive primary follicles were found at 80 days gestational age (gestation in sheep is 150 days) in superficial cervical lymph nodes. In the last month of gestation the primary follicles possessed follicular dendritic cells, macrophages, dendritic cells, and CD5-positive lymphocytes, in addition to IgM-positive cells. Follicular dendritic cells in primary follicles were found to be ultrastructurally immature. These follicular dendritic cells were characterised by a few, coarse surface projections and many ribosomes attached to the endoplasmic reticulum. A final differentiation to mature follicular dendritic cells was coincident with the postnatal germinal centre reaction. Computer-assisted morphometric analysis demonstrated that the size of 5′-nucleotidase-positive primary follicles in the distal jejunal lymph node, but not in the superficial cervical lymph node, increased significantly during late gestation. It was concluded that stromal cells in primary follicles of foetal sheep lymph nodes were a continuously developing population but that ultrastructural maturity was only achieved in the germinal centres of postnatal lambs.

Key words

Primary follicle Lymph node Foetus Development Follicular dendritic cell Ontogeny Sheep 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Al Salami M (1985) The ontogeny of the haemopoietic system in foetal sheep. PhD Thesis. The Australian National University, CanberraGoogle Scholar
  2. Al Salami M, Simpson-Morgan MW, Morris B (1985) Haemopoiesis and the development of immunological reactivity in the sheep foetus. In: Morris B, Miyasaka M (eds) Immunology of the sheep. Hoffman-La Roche, Basel, pp 19–36Google Scholar
  3. Barfoot R, Denham S, Gyure LA, Hall JG, Hobbs SM, Jackson LE, Robertson D (1989) Some properties of dendritic macrophages from peripheral lymph. Immunology 68:233–239Google Scholar
  4. Beya MF, Miyasaka M, Dudler L, Ezaki T, Trnka Z (1986) Studies on the differentiation of T lymphocytes in sheep. II. Two monoclonal antibodies that recognize all ovine T lymphocytes. Immunology 57:115–121Google Scholar
  5. Boyd RDH, Haworth C, Stacey TE, Ward RHT (1976) Permeability of the sheep placenta to unmetabolized polar non-electrolytes. J Physiol 256:617–634Google Scholar
  6. BrainPower Inc. (1986) StatView 512+manual. Abacus Concepts, CalabasasGoogle Scholar
  7. Brambell FWR (1970) The transmission of passive immunity from mother to young. In: Frontiers of biology. vol 18. North-Holland, Amsterdam, pp 201–233Google Scholar
  8. Cahill RNP, Poskitt DC, Frost H, Trnka Z (1977) Two distinct pools of recirculating T lymphocytes: migratory characteristics of nodal and intestinal T lymphocytes. J Exp Med 145:420–428Google Scholar
  9. Cahill RNP, Heron I, Poskitt DC, Trnka Z (1980) Lymphocyte recirculation in the sheep foetus. In: Blood cells and vessel walls: functional interactions. Ciba Foundation Symposium 71 (new series). Excerpta Medica, Amsterdam Oxford New York, pp 145–166Google Scholar
  10. Cerny A, Zinkernagel RM, Groscurth P (1988) Development of follicular dendritic cells in lymph nodes of B cell-depleted mice. Cell Tissue Res 254:449–454Google Scholar
  11. Cole GJ, Morris B (1973) The lymphoid apparatus in sheep: its growth, development and significance in immunological reactions. Adv Vet Sci Comp Med 17:225–263Google Scholar
  12. Dijkstra CD, Tilburg NJ van, Døpp EA (1982) Ontogenetic aspects of immune-complex trapping in the spleen and popliteal lymph nodes of the rat. Cell Tissue Res 223:545–552Google Scholar
  13. Dijkstra CD, Kamperdijk EAW, Døpp EA (1984) The ontogenetic development of the follicular dendritic cell. An ultrastructural study by means of intravenously injected horseradish peroxidase (HRP)-anti-HRP complexes as a marker. Cell Tissue Res 236:203–206Google Scholar
  14. Fahey, KJ, Morris B (1978) Humoral immune responses in foetal sheep. Immunology 35:651–661Google Scholar
  15. Halleraker M, Landsverk T, Nicander L (1990) Organization of ruminant Peyer's patches as seen with enzyme histochemical markers of stromal and accessory cells. Vet Immunol Immunopathol 26:93–104Google Scholar
  16. Hopkins J, Dutia BM, McConnell I (1986) Monoclonal antibodies to sheep lymphocytes. I. Identification of MHC II molecules on lymphoid tissue and changes in the level of class II expression on lymph-borne cells following antigen stimulation in vivo. Immunology 59:433–438Google Scholar
  17. Hopkins J, Dutia BM, Bujdoso R, McConnell I (1989) In vivo modulation of CD1 and MHC class II expression by sheep afferent lymph dendritic cells. Comparison of primary and secondary immune responses. J Exp Med 170:1303–1318Google Scholar
  18. Kroese FGM, Wubbena AS, Kuijpers KC, Nieuwenhuis P (1987) The ontogeny of germinal centre forming capacity of neonatal rat spleen. Immunology 60:597–602Google Scholar
  19. Luaces CP de, Peral JI, Tejeiro MG, Aguirre C (1988) Immunotypic characterization of primary and secondary lymphoid follicles. Histol Histopathol 3:69–80Google Scholar
  20. Maddox JF, Mackay CR, Brandon MR (1985) Surface antigens, SBU-T4 and SBU-T8, of sheep lymphocyte subsets defined by monoclonal antibodies. Immunology 55:739–748Google Scholar
  21. Markgraf R, Gaudecker B von, Müller-Hermelink HK (1982) The development of the human lymph node. Cell Tissue Res 225:387–413Google Scholar
  22. McClure SJ, Hein WR (1989) Functional characteristics of 197+ CD4- CD8-sheep T lymphocytes: expression and differentiation of peripheral T cells. Immunol Cell Biol 67:223–231Google Scholar
  23. Müller-Hermelink HK, Lennert K (1978) IV. Histomorphology of the B cell region. In: Müller-Hermelink HK, Lennert K (eds) Malignant lymphomas. Springer, Berlin Heidelberg New York, pp 33–45Google Scholar
  24. Myking AO (1988) Studies on the volumetric composition of lymph nodes: problems of efficient sampling and the use of point counting versus digitizer tablets. In: Reith A, Mayhew TM (eds) Stereology and morphometry in electron microscopy: problems and solutions. Hemisphere Publishing, New York Washington London, pp 47–62Google Scholar
  25. Nicander L, Halleraker M, Landsverk T (1991) Ontogeny of reticular cells in the ileal Peyer's patch of sheep and goats. Am J Anat 191:237–249Google Scholar
  26. Nickel R, Schummer A, Seiferle E (1981) The anatomy of the domestic animals, vol 3. Paul Parey, Berlin HamburgGoogle Scholar
  27. Pearson LD, Simpson-Morgan MW, Morris B (1976) Lymphopoiesis and lymphocyte recirculation in the sheep foetus. J Exp Med 143:167–186Google Scholar
  28. Press C, McClure S, Landsverk T (1991) Computer-assisted morphometric analysis of absorptive and follicle-associated epithelia of Peyer's patches in sheep foetuses and lambs indicates the presence of distinct T- and B-cell components. Immunology 72:386–392Google Scholar
  29. Press CMcL, Halleraker M, Landsverk T (1992) Ontogeny of leukocyte populations in the ileal Peyer's patch of sheep. Dev Comp Immunol 16:229–241Google Scholar
  30. Reynolds JD, Morris B (1983) The evolution and involution of Peyer's patches in foetal and postnatal sheep. Eur J Immunol 13:627–635Google Scholar
  31. Romeis B (1948) Mikroskopische Technik. Leibniz, MünchenGoogle Scholar
  32. Sainte-Marie G, Peng F-S (1985) Evidence for the existence of a subsinus layer of the peripheral cortex in the lymph node of the rat. Cell Tissue Res 239:37–42Google Scholar
  33. Sakuma H, Asano S, Kojima M (1981) An ultrastructural study of the primary follicle in the lymph node. Acta Pathol Jpn 31:473–493Google Scholar
  34. Silverstein AM, Uhr JW, Kraner KL, Lukes RJ (1963) Foetal response to antigenic stimulus. II. Antibody production by the foetal lamb. J Exp Med 117:799–812Google Scholar
  35. Snedecor GW, Cochran WG (1980) Statistical methods, 7th edn. Iowa State University Press, AmesGoogle Scholar
  36. Stein H, Bonk A, Tolksdorf G, Lennert K, Rodt H, Gerdes J (1980) Immunohistologic analysis of the organization of normal lymphoid tissue and non-Hodgkin's lymphomas. J Histochem Cytochem 28:746–760Google Scholar
  37. Timens W, Boes A, Rozeboom-Uiterwijk T, Poppema S (1988) Immunoarchitecture of human foetal lymphoid tissue. Virchows Arch [A] 413:563–571Google Scholar
  38. Weiss L (1988) Lymphatic vessels and lymph nodes. In: Weiss L (ed) Cell and tissue biology. A textbook of histology, 6th edn. Urban & Schwarzenberg, Baltimore Munich, pp 497–514Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Marit Halleraker
    • 1
  • Charles McL. Press
    • 1
  • Thor Landsverk
    • 1
  1. 1.Department of PathologyNorwegian College of Veterinary MedicineOslo 1Norway

Personalised recommendations