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Proteasomes on thyroid tissue allotransplantation under induction of donor-specific tolerance in rats

Russian Journal of Bioorganic Chemistry volume 40, pages 36–47 (2014)Cite this article

Abstract

Proteasomes in the liver of August rats (RT1c) were investigated 30 days after allotransplantation of Wistar rat (RT1u) thyroid tissue under renal capsule with/without induction of donor-specific tolerance by donor splenocyte intraportal administration. The levels of total proteasome pool, immune proteasomes containing subunits LMP2 and/or LMP7, and proteasome regulators 19S and 11S were defined. Intact and sham-operated August rats were used as control groups. The level of all immune proteasome forms and 11S regulator increased while the level of the total proteasome pool and 19S regulator decreased in the liver of experimental animals compared to the control groups, which indicated changes of liver functional state after transplantation. The 19S/11S ratio increased in the liver of nontolerant rats compared to tolerant animals. In the liver of tolerant rats with accepted grafts, the number of mononuclear cells expressing the immune subunit LMP2 greatly increased in comparison with control and nontolerant animals. Study of accepted grafts showed an increase in the ratio of LMP2/LMP7 immune subunits and 19S/11S regulators in them, compared to the tissue replacing the rejected grafts. Immune proteasomes were almost completely absent from the control intact thyroid tissue, while 19S/11S ratio was maximal in it. Thus, the development of the immune reaction or its suppression are accompanied by a change in the balance between different proteasome forms. Immune subunit LMP7 and 11S regulator are associated with the response against donor tissue. On the contrary, immune subunit LMP2 and 19S regulator are likely to be important for the development of immune tolerance and surviving tissue functioning. Immunofluorescence assay revealed a low content of the immune proteasomes in the follicle cells. Probably, formation of antigens for the major histocompatibility complex class I molecules was impaired by the low content of immune proteasomes, which led to immunological tolerance of hormone-producing follicle cells.

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Abbreviations

DST:

donor-specific tolerance

MHC:

major histocompatibility complex

IFN:

interferon

References

  1. Johnson, J.D., Ao, Z., Ao, P., Li, H., Dai, L.J., He, Z., Tee, M., Potter, K.J., Klimek, A.M., Meloche, R.M., Thompson, D.M., Verchere, C.B., and Warnock, G.L., Cell Transplant., 2009, vol. 18, pp. 833–845.

    PubMed  Article  Google Scholar 

  2. Shushan, A. and Schenker, J.G., Am. J. Reprod. Immunol., 1992, vol. 28, pp. 285–287.

    CAS  PubMed  Article  Google Scholar 

  3. Sato, Y., Ichida, T., Watanabe, H., Yamamoto, S., Oya, H., Nakatsuka, H., Kobayashi, T., Watanabe, T., Kameyama, H., and Hatakeyama, K., Hepatogastroenterology, 2003, vol. 50, pp. 601–606.

    PubMed  Google Scholar 

  4. Wong, W., Morris, P.J., and Wood, K.J., Transplantation, 1997, vol. 63, pp. 1490–1494.

    CAS  PubMed  Article  Google Scholar 

  5. Margenthaler, J.A., Landeros, K., Kataoka, M., and Flye, M.W., Transpl. Immunol., 2003, vol. 11, pp. 23–29.

    CAS  PubMed  Article  Google Scholar 

  6. Wang, F.S., Yamaguchi, Y., Furuhashi, T., Uchino, S., Kihara, S., Yamada, S., Mori, K., and Ogawa, M., J. Surg. Res., 2006, vol. 135, pp. 52–60.

    PubMed  Article  Google Scholar 

  7. Morita, H., Sugiura, K., Inaba, M., Jin, T., Ishikawa, J., Lian, Z., Adachi, Y., Sogo, S., Yamanishi, K., Taki, H., Adachi, M., Noumi, T., Kamiyama, Y., Good, R.A., and Ikehara, S., Proc. Natl. Acad. Sci. USA, 1998, vol. 95, pp. 6947–6952.

    CAS  PubMed  Article  Google Scholar 

  8. Diaz-Peromingo, J.A. and Gonzalez-Quintela, A., Eur. Surg. Res., 2005, vol. 37, pp. 45–49.

    CAS  PubMed  Article  Google Scholar 

  9. Bozhok, G.A., Kiroshka, V.V., Tishchenko, Yu.O., Lyupina, Yu.V., Karpova, Ya.D., Sharova, N.P., and Legach, E.I., Meditsina S’ogodi Zavtra, 2011, vols. 1–2, pp. 13–16.

    Google Scholar 

  10. Bozhok, G.A., Probl. Endokrin. Patal., 2011, pp. 60–66.

    Google Scholar 

  11. Bozhok, G.A., Legach, E.I., Ustichenko, V.D., Fedosova, S.N., and Bondarenko, T.P., Vestn. Neotlozh. Vosstanovit. Med., 2012, vol. 13, pp. 37–40.

    Google Scholar 

  12. Cong, Y., Konrad, A., Iqbal, N., Hatton, R.D., Weaver, C.T., and Elson, C.O., J. Immunol., 2005, vol. 174, pp. 2787–2795.

    CAS  PubMed  Google Scholar 

  13. Blanco, B., Perez-Simon, J.A., Sanchez-Abarca, L.I., Caballero-Velazquez, T., Gutierrez-Cossio, S., Hernandez-Campo, P., Diez-Campelo, M., Herrero-Sanchez, C., Rodriguez-Serrano, C., Santamaria, C., Sanchez-Guijo, F.M., Del Canizo, C., Del Canizo, C., and San, Miguel, J.F., Haematologica, 2009, vol. 94, pp. 975–983.

    CAS  PubMed  Article  Google Scholar 

  14. Blanco, B., Perez-Simon, J.A., Sanchez-Abarca, L.I., Carvajal-Vergara, X., Mateos, J., Vidriales, B., Lopez-Holgado, N., Maiso, P., Alberca, M., Villaron, E., Schenkein, D., Pandiella, and San Miguel, J.F., Blood, 2006, vol. 107, pp. 3575–3583.

    CAS  PubMed  Article  Google Scholar 

  15. Sharova, N.P. and Zakharova, L.A., Recent Pat. Endocr. Metab. Immune Drug Discov., 2008, vol. 2, pp. 152–161.

    CAS  Article  Google Scholar 

  16. Tanaka, K., Proc. Jpn. Acad., Ser. B, 2009, vol. 85, pp. 12–36.

    CAS  Article  Google Scholar 

  17. Rock, K.L. and Goldberg, A.L., Annu. Rev. Immunol., 1999, vol. 17, pp. 739–779.

    CAS  PubMed  Article  Google Scholar 

  18. Caudill, C., Jayarapu, K., Elenich, L., Monaco, J.J., Colbert, R.A., and Griffin, T.A., J. Immunol., 2006, vol. 176, pp. 4075–4082.

    CAS  PubMed  Google Scholar 

  19. Sijts, E.J. and Kloetzel, P.M., Cell Mol. Life Sci., 2011, vol. 68, pp. 1491–1502.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  20. Groettrup, M., Kirk, C.J., and Basler, M., Nat. Rev. Immunol., 2010, vol. 10, pp. 73–78.

    CAS  PubMed  Article  Google Scholar 

  21. Bertolino, P., Bowen, D.G., McCaughan, G.W., and Fazekas de St. Groth, B., J. Immunol., 2001, vol. 166, pp. 5430–5438.

    CAS  PubMed  Google Scholar 

  22. Parker, G.A. and Picut, C.A., Toxic. Pathol., 2005, vol. 33, pp. 52–62.

    CAS  Article  Google Scholar 

  23. Knolle, P.A. and Gerken, G., Immunol. Rev., 2000, vol. 174, pp. 21–34.

    CAS  PubMed  Article  Google Scholar 

  24. Tokita, D., Shishida, M., Ohdan, H., Onoe, T., Hara, H., Tanaka, Y., Ishiyama, K., Mitsuta, H., Ide, K., Arihiro, K., and Asahara, T., J. Immunol., 2006, vol. 15, pp. 3615–3624.

    Google Scholar 

  25. Onoe, T., Ohdan, H., Tokita, D., Shishida, M., Tanaka, Y., Hara, H., Zhou, W., Ishiyama, K., Mitsuta, H., Ide, K., and Asahara, T., J. Immunol., 2005, vol. 175, pp. 139–146.

    CAS  PubMed  Google Scholar 

  26. Crispe, I.N., Giannandrea, M., Klein, I., John, B., Sampson, B., and Wuensch, S., Immunol. Rev., 2006, vol. 213, pp. 101–118.

    PubMed  Article  Google Scholar 

  27. Erhardt, A., Biburger, M., Papadopoulos, T., and Tiegs, G., Hepatology, 2007, vol. 45, pp. 475–485.

    CAS  PubMed  Article  Google Scholar 

  28. Griffin, T.A., Nandi, D., Cruz, M., Fehling, H.J., Kaer, L.V., Monaco, J.J., and Colbert, R.A., J. Exp. Med., 1998, vol. 5, pp. 97–104.

    Article  Google Scholar 

  29. Kazanskii, D.B., Chernyshova, A.D., Sernova, N.V., Abronina, I.F., Anosova, N.G., Rodin, D.V., Pobezinskii, L.A., and Agafonova, E.L., Mol. Biol., 1998, vol. 32, pp. 875–881.

    CAS  Google Scholar 

  30. Kuehn, L. and Dahlmann, B., Mol. Biol. Rep., 1997, vol. 24, pp. 89–93.

    CAS  PubMed  Article  Google Scholar 

  31. Dick, T.P., Ruppert, T., Groettrup, M., Kloetzel, P.M., Kuehn, L., Koszinowski, U.H., Stevanovic, S., Schild, H., and Rammensee, H.G., Cell, 1996, vol. 26, pp. 253–262.

    Article  Google Scholar 

  32. Groettrup, M., Ruppert, T., Kuehn, L., Seeger, M., Standera, S., Koszinowski, U., and Kloetzel, P.M., J. Biol. Chem., 1995, vol. 6, pp. 23808–23815.

    Google Scholar 

  33. Rechsteiner, M., Realini, C., and Ustrell, V., Biochem. J., 2000, vol. 345, pp. 1–15.

    CAS  PubMed  Article  Google Scholar 

  34. Cascio, P., Call, M., Petre, B.M., Walz, T., and Goldberg, A.L., EMBO J., 2002, vol. 21, pp. 2636–2645.

    CAS  PubMed  Article  Google Scholar 

  35. Jung, T., Catalgol, B., and Grune, T., Mol. Aspects Med., 2009, vol. 30, pp. 191–296.

    CAS  PubMed  Article  Google Scholar 

  36. Davies, K.J.A. and Shringarpure, R., Neurology, 2011, vol. 66, pp. 93–96.

    Article  Google Scholar 

  37. Bertolino, P., McCaughan, G.W., and Bowen, D.G., Immunol. Cell Biol., 2002, vol. 80, pp. 84–92.

    PubMed  Article  Google Scholar 

  38. Karpova, Ya.D., Bozhok, G.A., Lyupina, Yu.V., Legach, E.I., Astakhova, T.M., Stepanova, A.A., Bondarenko, T.P., and Sharova, N.P., Biol. Bull. (Moscow), 2012, vol. 39, no. 3, pp. 244–249.

    Article  Google Scholar 

  39. Seifert, U., Bialy, L.P., Ebstein, F., Bech-Otschir, D., Voigt, A., Schröter, F., Prozorovski, T., Lange, N., Steffen, J., Rieger, M., Kuckelkorn, U., Aktas, O., Kloetzel, P.M., and Krüger, E., Cell, 2010, vol. 20, pp. 613–624.

    Article  Google Scholar 

  40. Davies, K.J. and Shringarpure, R., Neurology, 2006, vol. 66, pp. 93–96.

    Article  Google Scholar 

  41. Halling, K.B., Ellison, G.W., Armstrong, D., Aoyagi, K., Detrisac, C.J., Graham, J.P., Newell, S.P., Martin, F.G., and Van Gilder, J.M., Can. Vet. J., 2004, vol. 45, pp. 831–837.

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Buchholz, B.M., Kaczorowski, D.J., Sugimoto, R., Yang, R., Wang, Y., Billiar, T.R., McCurry, K.R., Bauer, A.J., and Nakao, A., Am. J. Transplant., 2008, vol. 8, pp. 2015–2024.

    CAS  PubMed  Article  Google Scholar 

  43. Toda, S., Koike, N., and Sugihara, H., Pathol. Int., 2001, vol. 51, pp. 403–417.

    CAS  PubMed  Article  Google Scholar 

  44. Laemmli, U.K., Nature, 1970, vol. 227, pp. 680–685.

    CAS  PubMed  Article  Google Scholar 

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Authors and Affiliations

  1. Koltsov Institute of Developmental Biology, Russian Academy of Sciences, ul. Vavilova 26, Moscow, 119334, Russia

    A. A. Stepanova, Ya. D. Karpova, Yu. V. Lyupina & N. P. Sharova

  2. Institute for Problems of Cryobiology and Cryomedicine, National Academy of Sciences of Ukraine, ul. Pereyaslavskaya 23, Kharkov, 61015, Ukraine

    G. A. Bozhok, V. D. Ustichenko, E. I. Legach & T. P. Bondarenko

  3. Blokhin Cancer Research Center, Russian Academy of Medical Sciences, Kashirskoe sh. 23, Moscow, 115478, Russia

    M. S. Vagida & D. B. Kazansky

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  1. A. A. Stepanova
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Correspondence to A. A. Stepanova.

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Original Russian Text © A.A. Stepanova, Ya.D. Karpova, G.A. Bozhok, V.D. Ustichenko, Yu.V. Lyupina, E.I. Legach, M.S. Vagida, D.B. Kazansky, T.P. Bondarenko, N.P. Sharova, 2014, published in Bioorganicheskaya Khimiya, 2014, Vol. 40, No. 1, pp. 42–54.

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Stepanova, A.A., Karpova, Y.D., Bozhok, G.A. et al. Proteasomes on thyroid tissue allotransplantation under induction of donor-specific tolerance in rats. Russ J Bioorg Chem 40, 36–47 (2014). https://doi.org/10.1134/S1068162014010105

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Keywords

  • proteasomes
  • immune proteasomes
  • portal tolerance
  • thyroid tissue transplantation
  • liver
  • immunological tolerance