Skip to main content
SpringerLink
Log in

Different intrathyroid expression of intercellular adhesion molecule-1 (ICAM-1) in Hashimoto’s thyroiditis and Graves’ disease: Analysis at mRNA level and association with B7.1 costimulatory molecule

  • Comment
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Cultured thyroid epithelial cells can be induced to express intercellular adhesion molecule-1 (ICAM-1, or CD54). However, constitutive follicular expression of ICAM-1 has been reported only in thyroid autoimmunity. We evaluated the expression of ICAM-1 mRNA and protein on thyroid tissue from different autoimmune thyroid diseases, and its relationship with other immunologically relevant surface markers, namely costimulatory molecules of B7 family. Thyroid tissue sections were obtained by surgically removed thyroid glands from 6 patients with Hashimoto’s thyroiditis (HT), 6 with Graves’ disease (GD) and 3 with multinodular nontoxic goiter. We used in situ hybridization to localize ICAM-1 mRNA, and immunohistochemical analysis by alkaline phosphatase anti-alkaline phosphatase (APAAP) method. We showed a clear hybridization pattern, localized in follicular cells, in sections of glands with HT. The hybridization pattern was far less pronounced in GD: no staining was apparent on follicular cells. These results were strictly consistent with those obtained by means of immunohistochemistry. Moreover, double-staining experiments demonstrated colocalization of ICAM-1 and B7.1 molecules in HT, whereas no B7.1 expression was observed in Graves’ or in non-autoimmune thyroid diseases. These data agree with the hypothesis of distinct immunoregulatory phenomena and effector mechanisms in the 2 main autoimmune thyroid diseases.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  1. Rothlein R., Dustin M.L., Marlin S.D., Springer T.A. A human intercellular adhesion molecule (ICAM1) distinct from LFA1. J. Immunol. 1986, 137: 1270–1275.

    CAS  PubMed  Google Scholar 

  2. Makgoba M.W., Sanders M.E., Luce G.E.G., et al. ICAM-1: a ligand for LFA-1 dependent adhesion of B, T and myeloid cells. Nature 1988, 331: 86–88.

    Article  CAS  PubMed  Google Scholar 

  3. Springer T.A. Adhesion receptors of the immune system. Nature 1990, 346: 425–434.

    Article  CAS  PubMed  Google Scholar 

  4. Dustin M.L., Springer T.A. Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. Annu. Rev. Immunol. 1991, 9: 27–66.

    Article  CAS  PubMed  Google Scholar 

  5. Volpes R., Van Den Oord J.J., Desmet V.J. Immunohistochemical study of adhesion molecules in liver inflammation. Hepatology 1990, 12: 59–64.

    Article  CAS  PubMed  Google Scholar 

  6. Wegner C.D., Gundel R.H., Reilly P., et al. Intercellular adhesion molecule-1 (ICAM-1) in the pathogenesis of asthma. Science 1990, 247: 456–459.

    Article  CAS  PubMed  Google Scholar 

  7. Bagnasco M., Pesce G., Fiorino N., et al. In situ hybridization analysis of ICAM-1 on mRNA on conjunctival epithelium during allergic inflammation. Clin. Exp. Allergy 1997, 27: 737–743.

    Article  CAS  PubMed  Google Scholar 

  8. Natali P., Nicotra M.R., Cavaliere R., et al. Differential expression of intercellular adhesion molecule-1 in primary and metastatic melanoma lesions. Cancer Res. 1990, 50: 1271–1273.

    CAS  PubMed  Google Scholar 

  9. Rothlein R., Mainolfi E.A., Czajkowski M., Marlin S.D. A form of circulating ICAM-1 in human serum. J. Immunol. 1991, 147: 3788–3793.

    CAS  PubMed  Google Scholar 

  10. Kvale D., Krajci P., Brandtzaeg P. Expression and regulation of adhesion molecules ICAM-1 (CD54) and LFA-3 (CD58) in human intestinal epithelial cell lines. J. Immunol. 1992, 35: 669–676.

    CAS  Google Scholar 

  11. Springer T.A., Dustin M.L., Kishimoto T.K., Marlin S.D. The lymphocyte function-associated LFA-1, CD2 and LFA-3 molecules: cell adhesion receptors of the immune system. Annu. Rev. Immunol. 1987, 5: 223–252.

    Article  CAS  PubMed  Google Scholar 

  12. Shaw S., Makgoba M.W., Shimizu Y. Antigen-independent adhesion: a critical process in human cytotoxic T cell recognition. In: Springer T.A., Anderson D.C., Rosenthal A.S., Rothlein R. (Eds.), Leukocyte Adhesion Molecules: Structure, Function and Regulation. Springer-Verlag, New York, 1990, pp. 236–243.

    Chapter  Google Scholar 

  13. Matsui K., Boniface J.J., Ready P.A., et al. Low affinity interaction of peptide-MHC complexes with cell receptors. Science 1991, 254: 1788–1790.

    Article  CAS  PubMed  Google Scholar 

  14. Weetman A.P., Cohen S., Magkoba M.W., Borysiewicz L.K. Expression of an intercellular adhesion molecule, ICAM-1, by human thyroid cells. J. Endocrinol. 1989, 122: 185–191.

    Article  CAS  PubMed  Google Scholar 

  15. Zheng R.Q.H., Abney E.R., Grubeck-Loebenstein B., et al. Expression of intercellular adhesion molecule-1 and lymphocyte function-associated antigen-3 on human thyroid epithelial cells in Graves’ and Hashimoto’s diseases. J. Autoimmun. 1990, 3: 727–736.

    Article  CAS  PubMed  Google Scholar 

  16. Bagnasco M., Caretto A., Olive D., et al. Expression of intercellular adhesion molecule-1 (ICAM-1) on thyroid epithelial cells in Hashimoto’s thyroiditis but not in Graves’ disease or papillary thyroid cancer. Clin. Exp. Immunol. 1991, 83: 309–313.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Bagnasco M., Pesce G.P., Caretto A., et al. Follicular thyroid cells of autoimmune thyroiditis may coexpress ICAM-1 (CD54) and its natural ligand LFA-1 (CD11a/CD18). J. Allergy Clin. Immunol. 1995, 95: 1036–1043.

    Article  CAS  PubMed  Google Scholar 

  18. Tolosa E., Roura C., Catalfamo M., et al. Expression of intercellular adhesion molecule-1 in thyroid follicular cells in autoimmune, nonautoimmune and neoplastic diseases of the thyroid gland: discordance with HLA. J. Autoimmun 1992, 5: 107–118.

    Article  CAS  PubMed  Google Scholar 

  19. Ciampolillo A., Napolitano G., Mirakian R., et al. Intercellular adhesion molecule (ICAM-1) in Graves’ disease: contrast between in vivo and in vitro results. Clin. Exp. Immunol. 1993, 94: 478–482.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Marazuela M., Postigo A.A., Acevedo A., et al. Adhesion molecules from the LFA-1/ICAM-1,2,3 and VLA-4/VCAM-1 pathways on T lymphocytes and vascular endothelium in Graves’ and Hashimoto’s thyroid glands. Eur. J. Immunol. 1994, 24: 2483–2486.

    Article  CAS  PubMed  Google Scholar 

  21. Arao T., Morimoto I., Kakinuma A., et al. Thyrocyte proliferation by cellular adhesion to infiltrating lymphocytes through the intercellular adhesion molecule-1/lymphocyte function-associated antigen-1 pathway in Graves’ disease. J.Clin. Endocrinol. Metab. 2000, 85: 382–9.

    CAS  PubMed  Google Scholar 

  22. Battifora M., Pesce G., Paolieri F., et al. B7.1 costimulatory molecule is expressed on thyroid follicular cells in Hashimoto’s thyroiditis but not in Graves’ disease. J. Clin. Endocrinol. Metab. 1998, 83: 4130–4139.

    CAS  PubMed  Google Scholar 

  23. Zocchi M.R., Ferrero E., Leone B.E., et al. CD31/PECAM-1-driven chemokine-independent transmigration of human T lymphocytes. Immunology 1996, 26: 759–767.

    CAS  Google Scholar 

  24. Nunes J.A., Battifora M., Wodgett J.R., et al. CD28 signal trasduction pathways. A comparison of B7.1 and B7.2 regulation of the MAP kinases: Erk 2 and Jun kinases. Mol. Immunol. 1996, 33: 63–70.

    Article  CAS  PubMed  Google Scholar 

  25. Scott Young W.: In situ hybridization with oligodeoxyribonucleotide probes. In: Wilkinson D.G. (Ed.), In situ Hybridization. A practical approach, Oxford University Press, New York, 1992, p. 33.

    Google Scholar 

  26. Sanderberg M., Vuorio E. Localization of types I,II, and III collagen mRNAs in developing human skeletal tissue by in situ hybridization. J. Cell Biol. 1987, 104: 1077–1084.

    Article  Google Scholar 

  27. Tanaka K., Hiromatsu Y., Sato M., Inoue Y., Nonoka K. Localization of heat shock protein in orbital tissue from patients with Graves’ ophthalmopathy using in situ hybridization. Life Sci. 1993, 54: 355–359.

    Article  Google Scholar 

  28. Weetman A.P., Freeman M., Borysiewicz L.K., Makgoba M.W. Functional analysis of intercellular adhesion molecule-1-expressing human thyroid cells. Eur. J. Immunol. 1990, 20: 271–275.

    Article  CAS  PubMed  Google Scholar 

  29. Schuppert F., Reiser M., Heldin N.E., et al. Thyrotropin receptor and leukocyte adhesion molecules in autoimmunethyroid disease: a study of their gene expression by northern blot analysis and in situ hybridization. Eur. J. Endocrinol. 1994, 131: 480–488.

    Article  CAS  PubMed  Google Scholar 

  30. Del Prete G.F., Tiri A., Mariotti S., et al. Enhanced production of Γ-interferon by thyroid-derived T cell clones from patients with Hashimoto’s thyroiditis. Clin. Exp. Immunol. 1987, 69: 323–331.

    PubMed Central  PubMed  Google Scholar 

  31. Bagnasco M., Venuti D., Prigione I., et al. Graves’ disease: phenotypic and functional analysis at the clonal level of the T cell repertoire in peripheral blood and in thyroid. Clin. Immunol. Immunopathol. 1988, 47: 230–234.

    Article  CAS  PubMed  Google Scholar 

  32. Stassi G., Di Liberto D., Todaro M., et al. Control of target cell survival in thyroid autoimmunity by T helper cytokines via regulation of apoptotic proteins. Nat. Immunol. 2000, 1: 483–488.

    Article  CAS  PubMed  Google Scholar 

  33. Roura-Mir C., Catalfamo M., Sospedra M., Alcalde L., Pujol-Borrell R., Jaraquemada D. Single-cell analysis of intrathyroidal lymphocytes shows differential cytokine expression in Hashimoto’s and Graves’ disease. Eur. J. Immunol. 1997, 27: 3290–3302.

    Article  CAS  PubMed  Google Scholar 

  34. Paschke R., Kist A., Janicke R., et al. Lack of intrathyroidal tumor necrosis factor a in Graves’ disease. J. Clin. Endocrinol. Metab. 1993, 76: 97–101.

    CAS  PubMed  Google Scholar 

  35. Del Prete G.F., Tiri A., De Carli M., et al. High potential to tumor necrosis factor alpha (TNF-αlpha) production of thyroid infiltrating T lymphocytes in Hashimoto’s thyroiditis: a peculiar feature of destructive thyroid autoimmunity. Autoimmunity 1989, 4: 267–270.

    Article  PubMed  Google Scholar 

  36. Giordano C., Stassi G., De Maria R., et al. Potential involvement of Fas and its ligand in the pathogenesis of Hashimoto’s Thyroiditis. Science 1997, 275: 960–963.

    CAS  PubMed  Google Scholar 

  37. Giordano C., Richiusa P., Bagnasco M., et al. Differential regulation of Fas-mediated apoptosis in both thyrocyte and lymphocyte cellular compartments correlates with opposite phenotypic manifestations of autoimmune thyroid disease. Thyroid 2001, 11: 233–244.

    Article  CAS  PubMed  Google Scholar 

  38. Yan X.M., Guo J., Pichurin P., et al. Cytokines, IgG subclasses and costimulation in a mouse model of thyroid autoimmunity induced by injection of fibroblasts coexpressing MCH class II and thyroid autoantigens. Clin. Exp. Immunol. 2000, 122: 170–179.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Allergy and Clinical Immunology Unit, Ist. di Medicina Interna, V.le Benedetto XV 6, 16132, Genova, Italy

    G. Pesce, P. Montagna, C. Salmaso, V. Altrinetti &  M. Bagnasco

  2. Allergy and Respiratory Disease Unit, Department of Internal Medicine-D.I.M.I., University of Genoa, Genoa, Italy

    N. Fiorino & A. M. Riccio

  3. Endocrine Surgery Unit, Department of Surgery, University of Genoa, Genoa, Italy

    G. Torre

Authors
  1. G. Pesce
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Fiorino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. M. Riccio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Montagna
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Torre
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Salmaso
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. V. Altrinetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M. Bagnasco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Bagnasco.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pesce, G., Fiorino, N., Riccio, A.M. et al. Different intrathyroid expression of intercellular adhesion molecule-1 (ICAM-1) in Hashimoto’s thyroiditis and Graves’ disease: Analysis at mRNA level and association with B7.1 costimulatory molecule. J Endocrinol Invest 25, 289–295 (2002). https://doi.org/10.1007/BF03344004

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03344004

Key-words

Search

Navigation