Skip to main content
SpringerLink
Log in

Involution of the rat thymus in experimentally induced hypothyroidism

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

Abstract

The thymus, as part of the immune-neuroendocrine axis, is greatly influenced by factors from most endocrine glands, especially the thyroid. Antithyroid drugs (carbimazole and methimazole) were used to induce hypothyroidism in rats. Histological and ultrastructural examination of the thymus showed progressive thymic involution after 4 weeks of drug treatment to the end of observations (7 weeks). The involution was characterised by increased thymocyte apoptosis and thymocyte phagocytosis by macrophages. This resulted in thymocyte depopulation, increases in numbers of interdigitating cells, alterations to mainly subcapsular and medullary epithelial cells, an apparent increase of mast cells and collagen in the capsule and septa, and increased numbers of B cells and plasma cells. Lymphoid cells immuno-reactive with MRC OX12 (which detects B cells) were observed within blood vessel walls, suggesting that they may have been moving in and out of the thymus. The administration of drugs causing hypothyroidism, therefore, also caused marked involution of the thymus.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aronson M (1989) Reversible thymic collapse following acute stress is beneficial: a hypothesis. Thymus 14:61–63

    Google Scholar 

  • Baker BL, Ingle DJ, Li CH (1951) The histology of the lymphoid organs of rats treated with adrenocorticotropin. Am J Anat 88:313–49

    Google Scholar 

  • Baroni CD, FAbris N, Bertoli (1969) Effects of hormones on development and function of lymphoid tissues. Synergistic action of thyroxin and somatotropic hormones in pituitary dwarf mice. Immunology 17:303–314

    Google Scholar 

  • Berthier C, Lemarchand-Beraud T (1978) Importance of thyroid iodine and cyclic AMP, and TSH concentration on goitre formation in rats. Acta Endocrinol 89:567–580

    Google Scholar 

  • Besedovsky HO, Sorkin E (1981) Immuno-neuroendocrine circuits: Physiological approaches. In: Ader R (ed) Psychoneuroimmunology. Academic Press, New York, pp 545–574

    Google Scholar 

  • Blau JN (1967) The dynamic behaviour of Hassall's corpuscles and the transport of particulate matter in the thymus of the guinea-pig. Immunology 13:281–292

    Google Scholar 

  • Blau N, Veall N (1967) The uptake and localization of proteins, Evans Blue and carbon black in the normal and pathological thymus of the guinea-pig. Immunology 12:363–372

    Google Scholar 

  • Brelinska R, Kaczmarck E, Warchol JB, Jaroszewsji J (1985) Distribution of different cell types within the rat thymus in the neonatal period of life. Cell Tissue Res 240:473–478

    Google Scholar 

  • Clarke AG, Kendall MD (1989) Histological changes in the thymus during mouse pregnancy. Thymus 14:65–78

    Google Scholar 

  • Cowan WK, Sorenson GD (1964) Electron microscopic observations of acute thymic involution produced by hydrocortisone. Lab Invest 13:353–370

    Google Scholar 

  • Csaba G (1969) Mechanism of the formation of mast-cell granules. II. Cell-free model. Acta Biol Acad Sci Hung 20:205–210

    Google Scholar 

  • Dallman MJ, Thomas ML, Green JR (1984) MRC Ox-19: a monoclonal antibody that labels rat T lymphocytes and augments in vitro proliferative responses. Eur J Immunol 14:260–267

    Google Scholar 

  • Dougherty TF, White A (1945) Functional alterations in lymphoid tissue. Physiol Rev 32:479–401

    Google Scholar 

  • Dourov N (1974) Study of the cytoplasmic lipids in thymic involution. Pathol Eur 9:43–57

    Google Scholar 

  • Duijvestijn AM, Hoefsmit ECM (1981) Ultrastructure of the rat thymus: The microenvironment of T-lymphocytes maturation. Cell Tissue Res 218:279–292

    Google Scholar 

  • Dumont F, Habbersett RC, Barrois R, Gerard H (1982) Accumulation of mature T and B cells and abnormalities of lymphocytes traffic in the thymus of aged NZB × SIL F1 female mice. In: Nieuwenhuis P, Broek van der AA, Hanna MG (eds) In vivo immunology. Plenum Press, New York, pp 297–302

    Google Scholar 

  • Fabris N, Mocchegiani E, Mariotti S, Pacini F, Pinchera A (1986) Thyroid function modulates thymic endocrine activity. J Clin Endocrin Metab 62:474–478

    Google Scholar 

  • Ghossein NA, Azar und Williams J (1963) Local irradiation of the thymus. Histological changes with observations on circulating lymphocytes and serum protein fractions in adult mice. Am J Path 43:269–379

    Google Scholar 

  • Gilman AG, Murad F (1980) Thyroid and antithyroid drugs. In: Gilman AG, Goodman LS (eds) Goodman and Gilman's The pharmacological basis of therapeutic, 6th edn. Macmillan, New York, pp 1398–1422

    Google Scholar 

  • Goldstein G (1966) Plasma cells in the human thymus. Aust J Exp Biol Med Sci 44:695–699

    Google Scholar 

  • Gomori G (1941) Distribution of acid phosphatase in the tissues under normal and under pathologic conditions. Arch Pathol 32:189–199

    Google Scholar 

  • Gordon H, Sweets HH (1936) A simple method for the silver impregnation of reticulum. Am J Pathol 12:545–552

    Google Scholar 

  • Goth A (1981) Thyroid hormones and antithyroid drugs. In: Goth A (ed) Medical pharmacology: principles and concepts, 10th edn. Mosby, St. Louis, pp 494–502

    Google Scholar 

  • Gowans JL, Knight EJ (1964) The route of recirculation of lymphocytes in the rat. Proc Roy R Soc Lond [Biol] 159:257–282

    Google Scholar 

  • Haelst UJG von (1967) Light and electron microscopic study of the normal and pathological thymus of the rat. II. The acute thymic involution. Z Zellforsch Mikrosk Anat 80:142–189

    Google Scholar 

  • Höhn EO (1959) Action of certain hormones on the thymus of the domestic hen. J Endocrinol 19:282–287

    Google Scholar 

  • Ito T, Hoshino T (1962) Histological changes of the mouse thymus during involution and regeneration following administration of hydrocortisone. Z Zellforsch Mikrosk Anat 56:445–464

    Google Scholar 

  • Jefferis WA, Green JR, Williams AF (1985) Authentic T helper CD4 (W3/25) antigen on rat peritoneal macrophages. J Exp Med 162:117–127

    Google Scholar 

  • Johnson P, Gagnon J, Barclay AN, Williams AF (1985) Purification, chain separation and sequence of the MRC OX-8 antigen, a marker of rat cytoxic T lymphocytes. EMBO J 4:2539

    Google Scholar 

  • Kahri AI, Salmi A, Hannuksela M, Karaharju EO (1965) Histochemistry of rat thymus during involution induced by alkylating agents. Acta Pathol Microbiol Scand 64:441–449

    Google Scholar 

  • Kendall MD (1991) Functional anatomy of the thymic microenvironment. J Anat 177:1–29

    Google Scholar 

  • Kendall MD, Buckingham JC, Ritter M (1992) A rise in plasma thymulin alters thymocyte phenotype. Neuroimmunomodulation in pharmacology. 2nd Course of the Federation of Pharmacological Sciences, Paris, Feb 4–7 1992

  • Kendall MK (1986) The syncytial nature of epithelial cells in the thymic cortex. J Anat 147:95–106

    Google Scholar 

  • Kendall MK (1990) The cell biology of cell death in the thymus. Thymus Update 3. Harwood Academic Publishers, Chur, Switzerland, pp 47–70

    Google Scholar 

  • Kotani M, Ohmori J, Miyakawa K, Hayama T, Kawatsu R, Terso K (1988) Increased vascular permeability in the thymus of the autoimmune New Zealand mouse. J Anat 161:83–93

    Google Scholar 

  • Leene W, Waal Malefijt de R, Roholl PJM, Hoeben KA (1988) Lymphocyte depletion in thymic nurse cells: a tool to identify in situ lympho-epithelial complexes having thymic nurse cell characteristics. Cell Tissue Res 253:61–68

    Google Scholar 

  • Lewis UJ, Cheever EV, Vanderlan WP (1965) Alteration of the proteins of the pituitary gland of the rat by estradiol and cortisol. Endocrinology 76:362–368

    Google Scholar 

  • Lewis VM, Twomey JJ, Bealmear P, Goldstein G, Good RA (1978) Age, thymic involution and circulating thymic hormone activity. J Clin Endocrinol Metab 47:145–150

    Google Scholar 

  • Männistö PT, Ranta T, Leppäluoto J (1979) Effects of methylmercaptoimidazole (MMI), propylthioracil (PTU), potassium perchlorate (KCLO4) and potassium (K1) on the serum concentrations of thyotropin (TSH) and thyroid hormones in the rat. Acta Endocrinol 91:271–281

    Google Scholar 

  • Mason DY, Sammons RE (1978) Alkaline phosphatase and peroxidase for double immunoenzymatic labelling of cellular constitutents. J Clin Pathol 31:454–460

    Google Scholar 

  • Milićević NM, Milićević ZJ, Piletić O, Mujović S, Ninkov V (1984) Patterns of thymic regeneration of rats after a single or divided doses of cyclophosphamide. J Comp Pathol 94:197–202

    Google Scholar 

  • Milićević NM, Milićević ZJ, Piletić O, Mujović S (1987) Ultrastructural study of macrophages in the thymus, with special references to the cortio-medullary zone. J Anat 150:89–98

    Google Scholar 

  • Millington G, Buckingham JC (1992) Thymic peptides and neuroendocrine-immune communication. J Endocrinol 133:163–168

    Google Scholar 

  • Moorhead JW, Kite JH Jr, McClusky RT, Werdelin Q, Wick G (1974) Migration patterns of thymus and bursa lymphocytes in normal chickens and obese strain chickens with spontaneous thyroiditis. Clin Immunol Immunopathol 2:160–177

    Google Scholar 

  • Pabst R, Binns RM, Westermann J (1989) What is the function of peripheral lymphocytes migrating to the thymus and of B-lymphocytes proliferating in the thymus? Thymus 13:149–156

    Google Scholar 

  • Pacini F, Nakamura H, Degroot LJ (1983) Effect of hypo- and hyperthyroidism on the balance between helper and suppressor T cells in rats. Acta Endocrinol 103:528–534

    Google Scholar 

  • Redmond O, Tuffery AR (1981) Thyroid proliferation, body weight thyrotropin and thyroid hormones in chronic antithyroid (carbimazole) treatment in rats. J Anat 133:37–47

    Google Scholar 

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

    Google Scholar 

  • Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultra-thin sectioning in electron microscopy. Stain Technology 35:313–323

    Google Scholar 

  • Saint-Marie G (1965) Plasmocytes in the thymus of the normal rat. J Immunol 94:172–176

    Google Scholar 

  • Schmitt D, Monier JC, Dardenne M, Pleau JM, Deschaux P, Bach JF (1980) Cytoplasmic localization of FTS (fateur thymique sérique) in thymic epithelial cells. An immuno-electron microscopical study. Thymus 2:177–186

    Google Scholar 

  • Siegler R (1964) The morphology of the thymuses and their relation to leukaemia. In: Good RA, Gabrielson AE (eds) The thymus in immuno-biology, structure, function and role in disease. Harper and Row, New York London, pp 623–655

    Google Scholar 

  • Spencer J, Choy M, Hussell T, Papadaki L, Kington JP, Isaacson PG (1992) Properties of human thymic B cells. Immunology 75:596–600

    Google Scholar 

  • Steinmann GG (1986) Changes in the human thymus during ageing. In: Müller-Hermelink HK (ed) The human thymus. Histophysiology and pathology. Current topics in pathology, vol 75. Springer, Berlin Heidelberg New York, pp 43–88

    Google Scholar 

  • Töro I, Olah I (1967) Penetration of thymocytes into the blood circulation. J Ultra Res 17:439–451

    Google Scholar 

  • Weaver JA (1955) Changes induced in the thymus and lymph nodes of the rat by administration of cortisone and sex hormones and by other procedures. J Pathol Bact 69:133–139

    Google Scholar 

  • Wijngaert van de FP, Kendall MD, Schuurman H-J, Rademakers LHMP, Kater L (1984) Heterogeneity of human thymus epithelial cells at the ultrastructural level. Cell Tissue Res 237:227–237

    Google Scholar 

  • Wyllie AH (1980) Glucocorticoid induces in thymocytes a nuclease-like activity associated with the chromatin condensation of apoptosis. Nature 284:555–556

    Google Scholar 

Download references

Author information

Author notes

  1. M. D. Kendall

    Present address: The Thymus Laboratory, Cellular Physiology, The AFRC Babraham Institute, Babraham, CB2 4AT, Cambridge, UK

Authors and Affiliations

  1. Cell Biology Unit, United Medical and Dental Schools of Guy's and St. Thomas's Hospitals, Lambeth Palace Road, SE1 7EH, London, UK

    M. D. Kendall

  2. Histology Department, Faculty of Medicine, Ain Shams University, Abbassia, Cairo, Egypt

    N. Abou-Rabia

Authors
  1. N. Abou-Rabia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. D. Kendall
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abou-Rabia, N., Kendall, M.D. Involution of the rat thymus in experimentally induced hypothyroidism. Cell Tissue Res 277, 447–455 (1994). https://doi.org/10.1007/BF00300217

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00300217

Key words

Search

Navigation