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BioMed Research International
Volume 2018, Article ID 3419565, 8 pages
https://doi.org/10.1155/2018/3419565
Research Article

CD4+CD45RAFOXP3low Regulatory T Cells as Potential Biomarkers of Disease Activity in Systemic Lupus Erythematosus Brazilian Patients

1Laboratório de Imunomodulação e Novas Abordagens Terapêuticas (LINAT), Núcleo de Pesquisa em Inovação Terapêutica Suely Galdino (NUPIT-SG), Universidade Federal de Pernambuco (UFPE), 50670-901, Brazil
2Laboratório de Parasitologia, Centro Acadêmico de Vitória, Universidade Federal de Pernambuco (UFPE), 50670-901, Brazil
3Hospital das Clínicas, Universidade Federal de Pernambuco (UFPE), 50670-901, Brazil
4Faculdade Nova Roma, 50830-260, Brazil
5Centre for Immunology & Infection, Department of Biology and Hull York Medical School, University of York, YO10 5DD, UK

Correspondence should be addressed to Maira G. R. Pitta; moc.liamg@attiprgm

Received 18 March 2018; Revised 1 May 2018; Accepted 16 May 2018; Published 12 June 2018

Academic Editor: Michael Mahler

Copyright © 2018 Helena L. Silva-Neta 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. M. C. Carroll, “A protective role for innate immunity in systemic lupus erythematosus,” Nature Reviews Immunology, vol. 4, no. 10, pp. 825–831, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. G. C. Tsokos, “Systemic lupus erythematosus,” The New England Journal of Medicine, vol. 365, no. 22, pp. 2110–2121, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. F. W. A. Barros, T. G. Silva, M. G. Da Rocha Pitta et al., “Synthesis and cytotoxic activity of new acridine-thiazolidine derivatives,” Bioorganic & Medicinal Chemistry, vol. 20, no. 11, pp. 3533–3539, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Picchianti-Diamanti, M. M. Rosado, M. Scarsella, B. Laganà, and R. D'Amelio, “P-glycoprotein and drug resistance in systemic autoimmune diseases,” International Journal of Molecular Sciences, vol. 15, no. 3, pp. 4965–4976, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Miyara, Y. Ito, and S. Sakaguchi, “TREG-cell therapies for autoimmune rheumatic diseases,” Nature Reviews Rheumatology, vol. 10, no. 9, pp. 543–551, 2014. View at Publisher · View at Google Scholar
  6. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda, “Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases,” The Journal of Immunology, vol. 155, no. 3, pp. 1151–1164, 1995. View at Google Scholar · View at Scopus
  7. S. Sakaguchi, T. Yamaguchi, T. Nomura, and M. Ono, “Regulatory T cells and immune tolerance,” Cell, vol. 133, no. 5, pp. 775–787, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. K.-M. Chavele and M. R. Ehrenstein, “Regulatory T-cells in systemic lupus erythematosus and rheumatoid arthritis,” FEBS Letters, vol. 585, no. 23, pp. 3603–3610, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. J.-H. Tao, M. Cheng, J.-P. Tang, Q. Liu, F. Pan, and X.-P. Li, “Foxp3, Regulatory T Cell, and Autoimmune Diseases,” Inflammation, vol. 40, no. 1, pp. 328–339, 2017. View at Publisher · View at Google Scholar · View at Scopus
  10. R. M. Talaat, S. F. Mohamed, I. H. Bassyouni, and A. A. Raouf, “Th1/Th2/Th17/Treg cytokine imbalance in systemic lupus erythematosus (SLE) patients: correlation with disease activity,” Cytokine, vol. 72, no. 2, pp. 146–153, 2015 (Chinese). View at Publisher · View at Google Scholar · View at Scopus
  11. D. Klatzmann and A. K. Abbas, “The promise of low-dose interleukin-2 therapy for autoimmune and inflammatory diseases,” Nature Reviews Immunology, vol. 15, no. 5, pp. 283–294, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Miyara, Y. Yoshioka, A. Kitoh et al., “Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor,” Immunity, vol. 30, no. 6, pp. 899–911, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Miyara, G. Gorochov, M. Ehrenstein, L. Musset, S. Sakaguchi, and Z. Amoura, “Human FoxP3+ regulatory T cells in systemic autoimmune diseases,” Autoimmunity Reviews, vol. 10, no. 12, pp. 744–755, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Newton, B. Priyadharshini, and L. A. Turka, “Immunometabolism of regulatory T cells,” Nature Immunology, vol. 17, no. 6, pp. 618–625, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. B. Yan, S. Ye, G. Chen, M. Kuang, N. Shen, and S. Chen, “Dysfunctional CD4+,CD25+ regulatory T cells in untreated active systemic lupus erythematosus secondary to interferon-alpha-producing antigen-presenting cells,” Arthritis & Rheumatology, vol. 58, no. 3, pp. 801–812, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Zhang, X. Zhang, F. L. Tang, L. P. Zhu, Y. Liu, and P. E. Lipsky, “Clinical significance of increased CD4+CD25Foxp3+ T cells in patients with new-onset systemic lupus erythematosus,” Annals of the Rheumatic Diseases, vol. 67, no. 7, pp. 1037–1040, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Bonelli, A. Savitskaya, K. von Dalwigk et al., “Quantitative and qualitative deficiencies of regulatory T cells in patients with systemic lupus erythematosus (SLE),” International Immunology, vol. 20, no. 7, pp. 861–868, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Miyara, Z. Amoura, C. Parizot et al., “Global natural regulatory T cell depletion in active systemic lupus erythematosus,” The Journal of Immunology, vol. 175, no. 12, pp. 8392–8400, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Alvarado-Sánchez, B. Hernández-Castro, D. Portales-Pérez et al., “Regulatory T cells in patients with systemic lupus erythematosus,” Journal of Autoimmunity, vol. 27, no. 2, pp. 110–118, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. X. Pan, X. Yuan, Y. Zheng et al., “Increased CD45RA +FOXP3 low regulatory T cells with impaired suppressive function in patients with systemic lupus erythematosus,” PLoS ONE, vol. 7, no. 4, Article ID e34662, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Żabińska, M. Krajewska, K. Kościelska-Kasprzak et al., “CD4+CD25+CD127− and CD4+CD25+Foxp3+ Regulatory T Cell Subsets in Mediating Autoimmune Reactivity in Systemic Lupus Erythematosus Patients,” Archivum Immunologiae et Therapia Experimentalis, vol. 64, no. 5, pp. 399–407, 2016. View at Publisher · View at Google Scholar · View at Scopus
  22. H.-Y. Lee, Y.-K. Hong, H.-J. Yun, Y.-M. Kim, J.-R. Kim, and W.-H. Yoo, “Altered frequency and migration capacity of CD4+ CD25+ regulatory T cells in systemic lupus erythematosus,” Rheumatology, vol. 47, no. 6, pp. 789–794, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Tselios, A. Sarantopoulos, I. Gkougkourelas, A. Papagianni, and P. Boura, “Increase of peripheral T regulatory cells during remission induction with cyclophosphamide in active systemic lupus erythematosus,” International Journal of Rheumatic Diseases, vol. 17, no. 7, pp. 790–795, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Ohl and K. Tenbrock, “Regulatory T cells in systemic lupus erythematosus,” European Journal of Immunology, vol. 45, no. 2, pp. 344–355, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. M. C. Hochberg, “Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus,” Arthritis & Rheumatology, vol. 40, no. 9, article 1725, 1997. View at Google Scholar · View at Scopus
  26. D. D. Gladman, D. Ibañez, and M. B. Urowitz, “Systemic lupus erythematosus disease activity index,” The Journal of Rheumatology, vol. 29, pp. 288–291, 2002. View at Google Scholar
  27. R. Njemini, O. O. Onyema, W. Renmans, I. Bautmans, M. De Waele, and T. Mets, “Shortcomings in the application of multicolour flow cytometry in lymphocyte subsets enumeration,” Scandinavian Journal of Immunology, vol. 79, no. 2, pp. 75–89, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Bonse, C. Santelli-Rouvier, J. Barbe, and R. L. Krauth-Siegel, “Inhibition of Trypanosoma cruzi trypanothione reductase by acridines: Kinetic studies and structure-activity relationships,” Journal of Medicinal Chemistry, vol. 42, no. 26, pp. 5448–5454, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. H. L. Buanec, M.-L. Gougeon, A. Mathian et al., “IFN-α and CD46 stimulation are associated with active lupus and skew natural T regulatory cell differentiation to type 1 regulatory T (Tr1) cells,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 108, no. 47, pp. 18995–19000, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. C. I. Cabeza-Alvarez, M. Gonzalez-Rubio, R. Garcia-Montero, and A. Alvarez-Tejerina, “Parkinsonian syndrome in relation to tacrine [3],” Neurología, vol. 14, no. 2, p. 96, 1999. View at Google Scholar · View at Scopus
  31. M. I. Vargas-Rojas, J. C. Crispín, Y. Richaud-Patin, and J. Alcocer-Varela, “Quantitative and qualitative normal regulatory T cells are not capable of inducing suppression in SLE patients due to T-cell resistance,” Lupus, vol. 17, no. 4, pp. 289–294, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Liu, A. L. Putnam, and Z. Xu-yu, “CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells,” The Journal of Experimental Medicine, vol. 203, no. 7, pp. 1701–1711, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Seddiki, B. Santner-Nanan, J. Martinson et al., “Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells,” The Journal of Experimental Medicine, vol. 203, no. 7, pp. 1693–1700, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Y. Lyssuk, A. V. Torgashina, S. K. Soloviev, E. L. Nassonov, and S. N. Bykovskaia, “Reduced number and function of CD4+CD25highFoxP3+ regulatory T cells in patients with systemic lupus erythematosus,” in Immune-Mediated Diseases: From Theory to Therapy, Advances in Experimental Medicine and Biology, pp. 601–113, Springer, Berlin, Germany, 2007. View at Publisher · View at Google Scholar
  35. R. K. Chowdary Venigalla, T. Tretter, S. Krienke et al., “Reduced CD4+,CD25- T cell sensitivity to the suppressive function of CD4+,CD25high,CD127-/low regulatory T cells in patients with active systemic lupus erythematosus,” Arthritis & Rheumatism, vol. 58, no. 7, pp. 2120–2130, 2008. View at Publisher · View at Google Scholar
  36. R. A. DeFronzo, R. M. Bergenstal, W. T. Cefalu et al., “Efficacy of inhaled insulin in patients with type 2 diabetes not controlled with diet and exercise: A 12-week, randomized, comparative trial,” Diabetes Care, vol. 28, no. 8, pp. 1922–1928, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. S. M. Callegari-Jacques, D. Grattapaglia, F. Salzano et al., “Historical genetics: Spatiotemporal analysis of the formation of the Brazilian population,” American Journal of Human Biology, vol. 15, no. 6, pp. 824–834, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. T. C. Lins, R. G. Vieira, B. S. Abreu, D. Grattapaglia, and R. W. Pereira, “Genetic composition of Brazilian population samples based on a set of twenty-eight ancestry informative SNPs,” American Journal of Human Biology, vol. 22, no. 2, pp. 187–192, 2010. View at Publisher · View at Google Scholar · View at Scopus