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Journal of Immunology Research
Volume 2016 (2016), Article ID 4163094, 13 pages
http://dx.doi.org/10.1155/2016/4163094
Research Article

Analysis of the Expression and Function of Immunoglobulin-Like Transcript 4 (ILT4, LILRB2) in Dendritic Cells from Patients with Systemic Lupus Erythematosus

1Departamento de Inmunología, Facultad de Medicina, Universidad Autónoma de San Luis Potosí, Avenida Venustiano Carranza 2405, 78210 San Luis Potosí, SLP, Mexico
2Departamento de Reumatología, Hospital Central “Dr. Ignacio Morones Prieto”, Avenida Venustiano Carranza 2395, 78290 San Luis Potosí, SLP, Mexico

Received 10 November 2015; Revised 1 January 2016; Accepted 5 January 2016

Academic Editor: Ethan M. Shevach

Copyright © 2016 Paola del Carmen Guerra-de Blas 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. J. Banchereau and R. M. Steinman, “Dendritic cells and the control of immunity,” Nature, vol. 392, no. 6673, pp. 245–252, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. A. J. Kassianos, S. L. Jongbloed, D. N. J. Hart, and K. J. Radford, “Isolation of human blood DC subtypes,” in Dendritic Cell Protocols, vol. 595 of Methods in Molecular Biology, pp. 45–54, Humana Press, New York, NY, USA, 2010. View at Publisher · View at Google Scholar
  3. R. M. Steinman, D. Hawiger, and M. C. Nussenzweig, “Tolerogenic dendritic cells,” Annual Review of Immunology, vol. 21, pp. 685–711, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Pulendran, H. Tang, and S. Manicassamy, “Programming dendritic cells to induce T(H)2 and tolerogenic responses,” Nature Immunology, vol. 11, no. 8, pp. 647–655, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. R. M. Steinman and J. Banchereau, “Taking dendritic cells into medicine,” Nature, vol. 449, no. 7161, pp. 419–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Hubo, B. Trinschek, F. Kryczanowsky, A. Tuettenberg, K. Steinbrink, and H. Jonuleit, “Costimulatory molecules on immunogenic versus tolerogenic human dendritic cells,” Frontiers in Immunology, vol. 4, article 82, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Ito, M. Yang, Y.-H. Wang et al., “Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand,” The Journal of Experimental Medicine, vol. 204, no. 1, pp. 105–115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Vlad, C.-C. Chang, A. I. Colovai, E. R. Vasilescu, R. Cortesini, and N. Suciu-Foca, “Membrane and soluble ILT3 are critical to the generation of T suppressor cells and induction of immunological tolerance,” International Reviews of Immunology, vol. 29, no. 2, pp. 119–132, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Brown, J. Trowsdale, and R. Allen, “The LILR family: modulators of innate and adaptive immune pathways in health and disease,” Tissue Antigens, vol. 64, no. 3, pp. 215–225, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. K. J. Anderson and R. L. Allen, “Regulation of T-cell immunity by leucocyte immunoglobulin-like receptors: innate immune receptors for self on antigen-presenting cells,” Immunology, vol. 127, no. 1, pp. 8–17, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Colonna, J. Samaridis, M. Cella et al., “Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules,” The Journal of Immunology, vol. 160, no. 7, pp. 3096–3100, 1998. View at Google Scholar
  12. N. T. Young, E. C. P. Waller, R. Patel, A. Roghanian, J. M. Austyn, and J. Trowsdale, “The inhibitory receptor LILRB1 modulates the differentiation and regulatory potential of human dendritic cells,” Blood, vol. 111, no. 6, pp. 3090–3096, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. V. Ristich, W. Zhang, S. Liang, and A. Horuzsko, “Mechanisms of prolongation of allograft survival by HLA-G/ILT4-modified dendritic cells,” Human Immunology, vol. 68, no. 4, pp. 264–271, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. C. C. Chang, R. Ciubotariu, J. S. Manavalan et al., “Tolerization of dendritic cells by Ts cells: the crucial role of inhibitory receptors ILT3 and ILT4,” Nature Immunology, vol. 3, no. 3, pp. 237–243, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. C. S. C. Chui and D. Li, “Role of immunolglobulin-like transcript family receptors and their ligands in suppressor T-cell-induced dendritic cell tolerization,” Human Immunology, vol. 70, no. 9, pp. 686–691, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Lichterfeld, D. G. Kavanagh, K. L. Williams et al., “A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomonocytic cells,” Journal of Experimental Medicine, vol. 204, no. 12, pp. 2813–2824, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Gregori, D. Tomasoni, V. Pacciani et al., “Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway,” Blood, vol. 118, no. 18, p. 5060, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. O. A. Huynh, T. Hampartzoumian, J. P. Arm et al., “Down-regulation of leucocyte immunoglobulin-like receptor expression in the synovium of rheumatoid arthritis patients after treatment with disease-modifying anti-rheumatic drugs,” Rheumatology, vol. 46, no. 5, pp. 742–751, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Kollnberger, L. Bird, M.-Y. Sun et al., “Cell-surface expression and immune receptor recognition of HLA-B27 homodimers,” Arthritis & Rheumatism, vol. 46, no. 11, pp. 2972–2982, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. L. Doníz-Padilla, A. E. Paniagua, P. Sandoval-Correa et al., “Analysis of expression and function of the inhibitory receptor ILT2 in lymphocytes from patients with autoimmune thyroid disease,” European Journal of Endocrinology, vol. 165, no. 1, pp. 129–136, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Bergamini, M. S. Chimenti, E. Baffari et al., “Downregulation of immunoglobulin-like transcript-4 (ILT4) in patients with psoriatic arthritis,” PLoS ONE, vol. 9, no. 3, Article ID e92018, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Monsiváis-Urenda, D. Gómez-Martin, K. Santana-de-Anda, J. Cruz-Martínez, J. Alcocer-Varela, and R. González-Amaro, “Defective expression and function of the ILT2/CD85j regulatory receptor in dendritic cells from patients with systemic lupus erythematosus,” Human Immunology, vol. 74, no. 9, pp. 1088–1096, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Monsiváis-Urenda, P. Niño-Moreno, C. Abud-Mendoza et al., “Analysis of expression and function of the inhibitory receptor ILT2 (CD85j/LILRB1/LIR-1) in peripheral blood mononuclear cells from patients with systemic lupus erythematosus (SLE),” Journal of Autoimmunity, vol. 29, no. 2-3, pp. 97–105, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. J. H. Fransen, J. V. D. Vlag, J. Ruben, G. J. Adema, J. H. Berden, and L. B. Hilbrands, “The role of dendritic cells in the pathogenesis of systemic lupus erythematosus,” Arthritis Research and Therapy, vol. 12, no. 2, article 207, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. J. M. Kim, S.-H. Park, H.-Y. Kim, and S.-K. Kwok, “A plasmacytoid dendritic cells-type i interferon axis is critically implicated in the pathogenesis of systemic lupus erythematosus,” International Journal of Molecular Sciences, vol. 16, no. 6, pp. 14158–14170, 2015. View at Publisher · View at Google Scholar
  26. J. P. Mackern-Oberti, C. Llanos, C. A. Riedel, S. M. Bueno, and A. M. Kalergis, “Contribution of dendritic cells to the autoimmune pathology of systemic lupus erythematosus,” Immunology, vol. 146, no. 4, pp. 497–507, 2015. View at Publisher · View at Google Scholar
  27. E. M. Tan, A. S. Cohen, J. F. Fries et al., “The 1982 revised criteria for the classification of systemic lupus erythematosus,” Arthritis & Rheumatism, vol. 25, no. 11, pp. 1271–1277, 1982. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Bombardier, D. D. Gladman, M. B. Urowitz et al., “Derivation of the sledai. A disease activity index for lupus patients,” Arthritis & Rheumatism, vol. 35, no. 6, pp. 630–640, 1992. View at Publisher · View at Google Scholar
  29. J. C. Crispín, M. I. Vargas-Rojas, A. Monsiváis-Urenda, and J. Alcocer-Varela, “Phenotype and function of dendritic cells of patients with systemic lupus erythematosus,” Clinical Immunology, vol. 143, no. 1, pp. 45–50, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Fedoric and R. Krishnan, “Rapamycin downregulates the inhibitory receptors ILT2, ILT3, ILT4 on human dendritic cells and yet induces T cell hyporesponsiveness independent of FoxP3 induction,” Immunology Letters, vol. 120, no. 1-2, pp. 49–56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Manicassamy and B. Pulendran, “Dendritic cell control of tolerogenic responses,” Immunological Reviews, vol. 241, no. 1, pp. 206–227, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. V. Ristich, S. Liang, W. Zhang, J. Wu, and A. Horuzsko, “Tolerization of dendritic cells by HLA-G,” European Journal of Immunology, vol. 35, no. 4, pp. 1133–1142, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. L. J. Carreño, R. Pacheco, M. A. Gutierrez, S. Jacobelli, and A. M. Kalergis, “Disease activity in systemic lupus erythematosus is associated with an altered expression of low-affinity Fcγ receptors and costimulatory molecules on dendritic cells,” Immunology, vol. 128, no. 3, pp. 334–341, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Ding, H. Mehta, W. J. McCune, and M. J. Kaplan, “Aberrant phenotype and function of myeloid dendritic cells in systemic lupus erythematosus,” The Journal of Immunology, vol. 177, no. 9, pp. 5878–5889, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Carvalheiro, A. Rodrigues, A. Lopes et al., “Tolerogenic versus inflammatory activity of peripheral blood monocytes and dendritic cells subpopulations in systemic lupus erythematosus,” Clinical and Developmental Immunology, vol. 2012, Article ID 934161, 14 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. N. Mozaffarian, A. E. Wiedeman, and A. M. Stevens, “Active systemic lupus erythematosus is associated with failure of antigen-presenting cells to express programmed death ligand-1,” Rheumatology, vol. 47, no. 9, pp. 1335–1341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. O. Jin, S. Kavikondala, M.-Y. Mok et al., “Abnormalities in circulating plasmacytoid dendritic cells in patients with systemic lupus erythematosus,” Arthritis Research and Therapy, vol. 12, no. 4, article R137, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Brenk, M. Scheler, S. Koch et al., “Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4+CD25+ Foxp3+ T regulatory cells,” The Journal of Immunology, vol. 183, no. 1, pp. 145–154, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. C.-C. Chang, Z. Liu, G. Vlad et al., “Ig-like transcript 3 regulates expression of proinflammatory cytokines and migration of activated T cells,” Journal of Immunology, vol. 182, no. 9, pp. 5208–5216, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Liang, V. Ristich, H. Arase, J. Dausset, E. D. Carosella, and A. Horuzsko, “Modulation of dendritic cell differentiation by HLA-G and ILT4 requires the IL-6—STAT3 signaling pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 24, pp. 8357–8362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Wozniacka, A. Lesiak, J. Narbutt, D. P. McCauliffe, and A. Sysa-Jedrzejowska, “Chloroquine treatment influences proinflammatory cytokine levels in systemic lupus erythematosus patients,” Lupus, vol. 15, no. 5, pp. 268–275, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. C.-H. Jang, J.-H. Choi, M.-S. Byun, and D.-M. Jue, “Chloroquine inhibits production of TNF-α, IL-1β and IL-6 from lipopolysaccharide-stimulated human monocytes/macrophages by different modes,” Rheumatology, vol. 45, no. 6, pp. 703–710, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. J. R. M. Carneiro, H. T. Fuzii, C. Kayser et al., “IL-2, IL-5, TNF-α and IFN-γ mRNA expression in epidermal keratinocytes of systemic lupus erythematosus skin lesions,” Clinics, vol. 66, no. 1, pp. 77–82, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. A.-M. Cepika, D. Soldo Jureša, J. Morović Vergles et al., “Decrease in circulating DNA, IL-10 and BAFF levels in newly-diagnosed SLE patients after corticosteroid and chloroquine treatment,” Cellular Immunology, vol. 276, no. 1-2, pp. 196–203, 2012. View at Publisher · View at Google Scholar · View at Scopus