Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Quantitative light and electron microscopic changes in thymic reticular epithelial cells during moloney-virus-induced lymphoma development

  • 21 Accesses

  • 8 Citations


This report describes two types of reticular epithelial cell in the thymic cortex of the BALB/c mouse, an immature and a mature form. During early stages of lymphoma development, i.e., 2–6 weeks postinfection (p.i.) with Moloney leukemia virus (M-MuLV), activation of the epithelial cells is observed. Although the percentage of these cells in the total cell population of the thymic cortex remains constant during that time, the number of mature epithelial cells is significantly increased in infected animals. Subsequently, about 6 weeks p.i., the number of immature epithelial cells starts to increase, whereas the number of mature reticular epithelial cells declines and the appearance of the mature epithelial cells changes drastically. The results of light and electron microscopic studies indicate degeneration of the mature reticular epithelial cells at the onset of lymphoma development at a time when the first deficiencies in the immunologic competence of the reticular epithelial cells are apparent.

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


  1. Bevan M (1977a) In a radiation chimera, host H-2 antigens determine immune responsiveness of donor cytotoxic cells. Nature 269:417–418

  2. Bevan MJ (1977b) Cytotoxic T-cell response to histocompatibility antigens: the role of H-2. Cold Spring Harbor Symp Quant Biol 41:519–527

  3. Clark SL Jr (1963) The thymus in mice of strain 129/J, studied with the electron microscope. Am J Anat 112:1–33

  4. Dalton AJ, Law LW, Moloney JB, Manaker RA (1961) An electron microscopic study of a series of murine lymphoid neoplasms. J Natl Cancer Inst 27:747–791

  5. Dappen GE, Crouse DA, Anderson RW, Jordan RK Robinson JH, Sharp JG (1981) Morphological assessment of immunologically relevant cells in the thymus. Proc 7th Intl Conf on Lymphatic Tissues and Germinal Centers in Immune Reactions. Plenum Press, New York

  6. de Harven E (1964) Virus particles in the thymus of conventional and germ-free mice. J Exp Med 120:857–868

  7. Feldman DG, Dreyfuss Y, Gross L (1967) Electron microscopic study of the mouse leukemia virus (Gross) in organs of mouse embryos from virus-infected and normal C3HF parents. Cancer Res 27:1792–1804

  8. Gillette RW, Fox A (1977) Changes caused in the homing patterns of chromium 51-labeled lymphoid cells by Moloney sarcoma virus infection. J Natl Cancer Inst 58:121–1628

  9. Gregoire C, Duchateau G (1956) A study on lympho-epithelial symbiosis in thymus. Reactions on the lymphatic tissue to extracts and to implants of epithelial components of the thymus. Arch Biol (Liege) 67:269–296

  10. Haas M, Sher T, Smolinsky S (1977) Leukemogenesis in vitro induced by thymus epithelial reticulum cells transmitting murine leukemia viruses. Cancer Res 37:1800–1807

  11. Haas W, Deying T, Krueger GRF, Féaux de Lacroix W (1981) Autoradiographic and immunocytologic identification of atypical cell proliferation during Moloney virus induced lymphoma development. In: Yohn DS, Blakeslee JR (eds) Advances Comparative Leukemia Research. Elsevier North Holland (pp. 241–243)

  12. Hays EF (1968) The role of thymus reticular epithelial cells in virusleukemogenesis. Cancer Res 28:21–26

  13. Humble JG, Jayhe WHW, Pulvertaft RJV (1956) Biological interaction between lymphocytes and other cells. Br J Haematol 2:283–294

  14. Izard J, de Harven E (1968) Increased number of a characteristic type of reticular cell in the thymus and lymph nodes of leukemic mice: An electron microscope study. Cancer Res 28:421–433

  15. Jaerplid B (1974) Dark reticular cells in the thymus of mice. Acta Radiol [Ther] (Stockh) 13:319–328

  16. Jordan RK, Crouse DA (1980) Non-lymphoid cells and intrathymic T-cell differentiation. In: Holton JD (ed). Development and differentiation of vertebrate lymphocytes. Elsevier North Holland (pp. 47–61)

  17. Jordan RK, Crouse DA, Harper CM, Watkins EB, Sharp JG (1979) The thymic microenvironment. In: Baum SJ (ed) Experimental haematology today. Springer Verlag, New York (pp. 139–153)

  18. Jordan RK, Robinson JH, Bentley AL, Crouse DA (1982) Studies on the development of the murine thymic microenvironment. Behring Inst Mitt 70:3–8

  19. Kosmidis HV, Lusher GN, Shope TC, Ravindranath Y, Dajani A (1980) Infections in leukemic children: a prospective analysis. J Pediatr 96:814–819

  20. Krueger GRF, Fischer KM, Flesch HG (1978) Sequential changes of T-and B-cells, virus antigen expression and primary histologic tumor diagnosis in virus-induced lymphomagenesis of mice. Z Krebsforsch 92:41–54

  21. Krueger GRF, Karpinski A, Heine UI (to be published) Differentiation block of prethymic lymphocytes during Moloney virus-induced lymphoma development secondary to thymic epithelial defect. J Cancer Res Clin Oncol

  22. Mandel T (1968) Ultrastructure of epithelial cells in the cortex of guinea pig thymus. Z Zellforsch 92:159–168

  23. Mertens H, Krueger GRF (1976) Percent distribution of T-and B-lymphoid cells in spleen and lymph nodes of Moloney virus infected mice. Z Krebsforsch 85:169–175

  24. Metcalf D (1956) The thymic origin of the plasma lymphocytosis stimulating factor. Br J Cancer 10:442–457

  25. Metcalf D (1966) Histologic and transplantation studies on preleukemic thymus of the AKR mouse. J Natl Cancer Inst 37:425–442

  26. Miller G, Shope T, Heston L, O'Brian R, Swartz A, Pearson H (1972) Prospective study of Epstein-Barr virus infections in acute lymphoblastic leukemia of childhood. J Pediatr 80:932–937

  27. Miller JFPA (1962) Role of thymus in virus-induced leukemia. In: Wolstenholme GEW, O'Connor M (eds) Tumor viruses of murine origin. Ciba Foundation Symposium. J and A Churchill

  28. Moore MAS, Owen JJT (1967) Experimental studies on the development of the thymus (Chromosome markers for Ly Infiltration). J Exp Med 126:715–726

  29. Oláh I, Roehlich P, Törő I (1975) Ultrastructure of lymphoid organs. JB Lippincott, Philadelphia

  30. Owen JJT, Jordan RK, Robinson JH, Singh U, Willcox HNA (1977) In vitro studies on the generation of lymphocyte diversity. Cold Spring Harbor Symp Quant Biol 41:129–137

  31. Pack FD, Chapman WL (1980) Light and electron microscopic evaluation of thymuses from feline leukemia virus-infected kittens. Exp Pathol 18:96–110

  32. Reynolds ES (1963) The use of lead citrate at high pH as an electronopaque stain in electron microscopy. J Cell Biol 17:208–212

  33. Sabatini DD, Bensch K, Barnett RJ (1963) Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J Cell Biol 17:19–58

  34. Stephens DA, Levine PH, Lee SK, Sonley MJ, Waggoner D (1971) Concurrent infectious mononucleosis and acute leukemia. Case reports. Review of the literature and serologic studies with the Herpes-type virus (EB virus). Am J Med 50:208–217

  35. Trainin N, Small M, Kook AI (1977) The role of thymic hormones in regulation of the lymphoid system. In: Loor F, Roelants GE (eds) B-and T-cells in Immune Recognition. John Wiley, Chichester (p. 83)

  36. Trump BF, Smuckler EA, Bendiott EP (1961) A method of staining epoxy sections for light microscopy. J Ultrastruct Res 5:343–348

  37. v Gaudecker B, Mueller-Hermelink HK (1980) Ontogeny and organization of the stationary nonlymphoid cells in the human thymus. Cell Tissue Res 207:287–306

  38. Wekerle H, Ketelsen UP, Ernest M (1980) Thymic nurse cells. J Exp Med 151:925–944

  39. Yanigihara K, Hamada K, Seyama T, Imamura N, Yokoro K (1982) In vitro studies of the mechanism of leukemogenesis. II. Characterization of endogenous murine leukemia viruses isolated from AKR thymic epithelial cell lines. J Virol 41:360–366

  40. Zinkernagel RM (1978) Thymus and lympho-hemopoetic cells: Their role in T-cell maturation in selection of T-cell's H-2-restriction specificity and in H-2 linked Ir gene control. Immunol Rev 42:224–270

Download references

Author information

Correspondence to G. R. F. Krueger.

Additional information

Supported by grant Kr476/6-4 of the German Science Foundation

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Heine, U.I., Krueger, G.R.F., Karpinski, A. et al. Quantitative light and electron microscopic changes in thymic reticular epithelial cells during moloney-virus-induced lymphoma development. J Cancer Res Clin Oncol 106, 102–111 (1983). https://doi.org/10.1007/BF00395387

Download citation

Key words

  • Murine lymphoma development
  • Virus infection
  • Thymus
  • Reticular epithelial cells
  • Electron microscopy