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Analytical Cellular Pathology
Volume 2015, Article ID 324980, 10 pages
http://dx.doi.org/10.1155/2015/324980
Research Article

Immunosuppressive Drugs Affect High-Mannose/Hybrid N-Glycans on Human Allostimulated Leukocytes

1Department of Glycoconjugate Biochemistry, Institute of Zoology, Faculty of Biology and Earth Science, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland
2Department of Immunology, Institute of Zoology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
3Department of Clinical Immunology, Transplantation Institute, Medical University of Warsaw, Nowogrodzka 59, 02-006 Warsaw, Poland

Received 10 April 2015; Accepted 21 July 2015

Academic Editor: Consuelo Amantini

Copyright © 2015 Ewa Pocheć et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. M. Haslam, S. Julien, J. M. Burchell et al., “Characterizing the glycome of the mammalian immune system,” Immunology and Cell Biology, vol. 86, no. 7, pp. 564–573, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. J. L. Johnson, M. B. Jones, S. O. Ryan, and B. A. Cobb, “The regulatory power of glycans and their binding partners in immunity,” Trends in Immunology, vol. 34, no. 6, pp. 290–298, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. J. D. Marth and P. K. Grewal, “Mammalian glycosylation in immunity,” Nature Reviews Immunology, vol. 8, no. 11, pp. 874–887, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. P. M. Rudd, M. R. Wormald, and R. A. Dwek, “Sugar-mediated ligand-receptor interactions in the immune system,” Trends in Biotechnology, vol. 22, no. 10, pp. 524–530, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. G. A. Rabinovich, Y. van Kooyk, and B. A. Cobb, “Glycobiology of immune responses,” Annals of the New York Academy of Sciences, vol. 1253, no. 1, pp. 1–15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Kobata, “A journey to the world of glycobiology,” Glycoconjugate Journal, vol. 17, no. 7–9, pp. 443–464, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Boscher, J. W. Dennis, and I. R. Nabi, “Glycosylation, galectins and cellular signaling,” Current Opinion in Cell Biology, vol. 23, no. 4, pp. 383–392, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. S. O. Ryan and B. A. Cobb, “Roles for major histocompatibility complex glycosylation in immune function,” Seminars in Immunopathology, vol. 34, no. 3, pp. 425–441, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Ringeard, J. Harb, F. Gautier, J. Menanteau, and K. Meflah, “Altered glycosylation of α(s)β1 integrins from rat colon carcinoma cells decreases their interaction with fibronectin,” Journal of Cellular Biochemistry, vol. 62, no. 1, pp. 40–49, 1996. View at Google Scholar · View at Scopus
  10. Y. Zhang, J.-H. Zhao, X.-Y. Zhang, H.-B. Guo, F. Liu, and H.-L. Chen, “Relations of the type and branch of surface N-glycans to cell adhesion, migration and integrin expressions,” Molecular and Cellular Biochemistry, vol. 260, no. 1, pp. 137–146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Ehlers, “DC-SIGN and mannosylated surface structures of Mycobacterium tuberculosis: a deceptive liaison,” European Journal of Cell Biology, vol. 89, no. 1, pp. 95–101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. van Kooyk and G. A. Rabinovich, “Protein-glycan interactions in the control of innate and adaptive immune responses,” Nature Immunology, vol. 9, no. 6, pp. 593–601, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. A. V. Muchmore, N. Sathyamoorthy, J. Decker, and A. P. Sherblom, “Evidence that specific high-mannose oligosaccharides can directly inhibit antigen-driven T-cell responses,” Journal of Leukocyte Biology, vol. 48, no. 5, pp. 457–464, 1990. View at Google Scholar · View at Scopus
  14. S. K. Akiyama, S. S. Yamada, and K. M. Yamada, “Analysis of the role of glycosylation of the human fibronectin receptor,” The Journal of Biological Chemistry, vol. 264, no. 30, pp. 18011–18018, 1989. View at Google Scholar · View at Scopus
  15. B. A. Nacev, P. Grassi, A. Dell, S. M. Haslam, and J. O. Liu, “The antifungal drug itraconazole inhibits vascular endothelial growth factor receptor 2 (VEGFR2) glycosylation, trafficking, and signaling in endothelial cells,” The Journal of Biological Chemistry, vol. 286, no. 51, pp. 44045–44056, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Evans, I. Patzak, L. Svensson et al., “Integrins in immunity,” Journal of Cell Science, vol. 122, no. 2, pp. 215–225, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. N. Hogg, M. Laschinger, K. Giles, and A. McDowall, “T-cell integrins: more than just sticking points,” Journal of Cell Science, vol. 116, no. 23, pp. 4695–4705, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. J. T. Pribila, A. C. Quale, K. L. Mueller, and Y. Shimizu, “Integrins and T cell-mediated immunity,” Annual Review of Immunology, vol. 22, pp. 157–180, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Zhang and H. Wang, “Integrin signalling and function in immune cells,” Immunology, vol. 135, no. 4, pp. 268–275, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. E. S. Harris, T. M. McIntyre, S. M. Prescott, and G. A. Zimmerman, “The leukocyte integrins,” The Journal of Biological Chemistry, vol. 275, no. 31, pp. 23409–23412, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. T. N. Sims and M. L. Dustin, “The immunological synapse: integrins take the stage,” Immunological Reviews, vol. 186, pp. 100–117, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. M. L. Dustin and J. A. Cooper, “The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling,” Nature Immunology, vol. 1, no. 1, pp. 23–29, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. G. M. Griffiths, A. Tsun, and J. C. Stinchcombe, “The immunological synapse: a focal point for endocytosis and exocytosis,” Journal of Cell Biology, vol. 189, no. 3, pp. 399–406, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. D. M. Rose, R. Alon, and M. H. Ginsberg, “Integrin modulation and signaling in leukocyte adhesion and migration,” Immunological Reviews, vol. 218, no. 1, pp. 126–134, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Lacy-Hulbert, T. Ueno, T. Ito et al., “β3 integrins regulate lymphocyte migration and cytokine responses in heart transplant rejection,” American Journal of Transplantation, vol. 7, no. 5, pp. 1080–1090, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. D. Luster, R. Alon, and U. H. von Andrian, “Immune cell migration in inflammation: present and future therapeutic targets,” Nature Immunology, vol. 6, no. 12, pp. 1182–1190, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Sarnacki, Y. Révillon, A. Fischer et al., “Blockade of the integrin αLβ2 but not of integrins α4 and/or β7 significantly prolongs intestinal allograft survival in mice,” Gut, vol. 47, no. 1, pp. 97–104, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Gu and N. Taniguchi, “Potential of N-glycan in cell adhesion and migration as either a positive or negative regulator,” Cell Adhesion & Migration, vol. 2, no. 4, pp. 243–245, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. M. A. Daniels, K. A. Hogquist, and S. C. Jameson, “Sweet ‘n’ sour: the impact of differential glycosylation on T cell responses,” Nature Immunology, vol. 3, no. 10, pp. 903–910, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. M. C. Clark and L. G. Baum, “T cells modulate glycans on CD43 and CD45 during development and activation, signal regulation, and survival,” Annals of the New York Academy of Sciences, vol. 1253, no. 1, pp. 58–67, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. P. M. Rudd, M. R. Wormald, R. L. Stanfield et al., “Roles for glycosylation of cell surface receptors involved in cellular immune recognition,” Journal of Molecular Biology, vol. 293, no. 2, pp. 351–366, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. D. H. Dube and C. R. Bertozzi, “Glycans in cancer and inflammation—potential for therapeutics and diagnostics,” Nature Reviews Drug Discovery, vol. 4, no. 6, pp. 477–488, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Ohtsubo and J. D. Marth, “Glycosylation in cellular mechanisms of health and disease,” Cell, vol. 126, no. 5, pp. 855–867, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Chinen and R. H. Buckley, “Transplantation immunology: solid organ and bone marrow,” Journal of Allergy and Clinical Immunology, vol. 125, no. 2, pp. S324–S335, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. E. T. Long, S. Baker, V. Oliveira, B. Sawitzkib, and K. J. Wood, “Alpha-1,2-mannosidase and hence N-glycosylation are required for regulatory T cell migration and allograft tolerance in mice,” PLoS ONE, vol. 5, no. 1, Article ID e8894, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Bocian, J. Borysowski, P. Wierzbicki et al., “Rapamycin, unlike cyclosporine A, enhances suppressive functions of in vitro-induced CD4+CD25+ Tregs,” Nephrology Dialysis Transplantation, vol. 25, no. 3, pp. 710–717, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. R. N. Saunders, M. S. Metcalfe, and M. L. Nicholson, “Rapamycin in transplantation: a review of the evidence,” Kidney International, vol. 59, no. 1, pp. 3–16, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. C.-L. Lee, P.-P. Jiang, W.-H. Sit, and J. M.-F. Wan, “Proteome of human T lymphocytes with treatment of cyclosporine and polysaccharopeptide: analysis of significant proteins that manipulate T cells proliferation and immunosuppression,” International Immunopharmacology, vol. 7, no. 10, pp. 1311–1324, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Kędzierska, K. Sporniak-Tutak, K. Sindrewicz et al., “Effects of immunosuppressive treatment on protein expression in rat kidney,” Drug Design, Development and Therapy, vol. 8, pp. 1695–1708, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. D. F. Martin, L. R. DeBarge, R. B. Nussenblatt, C.-C. Chan, and F. G. Roberge, “Synergistic effect of rapamycin and cyclosporin A in the treatment of experimental autoimmune uveoretinitis,” Journal of Immunology, vol. 154, no. 2, pp. 922–927, 1995. View at Google Scholar · View at Scopus
  41. T. Engl, J. Makarević, B. Relja et al., “Mycophenolate mofetil modulates adhesion receptors of the beta1 integrin family on tumor cells: impact on tumor recurrence and malignancy,” BMC Cancer, vol. 5, article 4, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. J. A. Faralli, D. Gagen, M. S. Filla, T. N. Crotti, and D. M. Peters, “Dexamethasone increases αvβ3 integrin expression and affinity through a calcineurin/NFAT pathway,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1833, no. 12, pp. 3306–3313, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. Y.-H. Huang, Y.-L. Ma, L. Ma et al., “Cyclosporine A improves adhesion and invasion of mouse preimplantation embryos via upregulating integrin β3 and matrix metalloproteinase-9,” International Journal of Clinical and Experimental Pathology, vol. 7, no. 4, pp. 1379–1388, 2014. View at Google Scholar · View at Scopus
  44. F. Zal, Z. Mostafavi-Pour, A. Moattari, A. Sardarian, and M. Vessal, “Altered expression of alpha2beta1 integrin in kidney fibroblasts: a potential mechanism for CsA-induced nephrotoxicity,” Archives of Iranian Medicine, vol. 17, no. 8, pp. 556–562, 2014. View at Google Scholar
  45. T. Isaji, S. Im, W. Gu et al., “An oncogenic protein Golgi phosphoprotein 3 up-regulates cell migration via sialylation,” The Journal of Biological Chemistry, vol. 289, no. 30, pp. 20694–20705, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. L. C. Paul, J.-F. Valentin, J. A. Bruijn, and S. Zhang, “Donor treatment with mycophenolate mofetil protects against ischemia-reperfusion injury,” Transplantation Proceedings, vol. 31, no. 1-2, p. 1026, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. M. M. Aw, “Transplant immunology,” Journal of Pediatric Surgery, vol. 38, no. 9, pp. 1275–1280, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. M.-A. Doucey, D. F. Legler, M. Faroudi et al., “The beta1 and beta3 integrins promote T cell receptor-mediated cytotoxic T lymphocyte activation,” The Journal of Biological Chemistry, vol. 278, no. 29, pp. 26983–26991, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. M. L. Dustin and A. R. de Fougerolles, “Reprograming T cells: the role of extracellular matrix in coordination of T cell activation and migration,” Current Opinion in Immunology, vol. 13, no. 3, pp. 286–290, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. A. C. Allison and E. M. Eugui, “Mycophenolate mofetil and its mechanisms of action,” Immunopharmacology, vol. 47, no. 2-3, pp. 85–118, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Frey and A. De Maio, “The antifungal agent itraconazole induces the accumulation of high mannose glycoproteins in macrophages,” Journal of Biological Chemistry, vol. 284, no. 25, pp. 16882–16890, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. Y. Lavie, H.-T. Cao, A. Volner et al., “Agents that reverse multidrug resistance, tamoxifen, verapamil, and cyclosporin A, block glycosphingolipid metabolism by inhibiting ceramide glycosylation in human cancer cells,” The Journal of Biological Chemistry, vol. 272, no. 3, pp. 1682–1687, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Renkonen and J. Ustinov, “Carbohydrate synthesis inhibitors decrease interleukin 1-stimulated lymphocyte binding to endothelial cells,” European Journal of Immunology, vol. 21, no. 3, pp. 777–781, 1991. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Tulp, M. Barnhoorn, E. Bause, and H. Ploegh, “Inhibition of N-linked oligosaccharide trimming mannosidases blocks human B cell development,” The EMBO Journal, vol. 5, no. 8, pp. 1783–1790, 1986. View at Google Scholar · View at Scopus
  55. M. Sperandio, C. A. Gleissner, and K. Ley, “Glycosylation in immune cell trafficking,” Immunological Reviews, vol. 230, no. 1, pp. 97–113, 2009. View at Publisher · View at Google Scholar · View at Scopus