Prague Med. Rep. 2022, 123, 166-180

https://doi.org/10.14712/23362936.2022.15

Disturbance in Serum Levels of IL-17 and TGF-β1 and in Gene Expression of ROR-γt and FOX-P3 Is Associated with Pathogenicity of Systematic Lupus Erythematosus

Hanaa N. Ali1, Ghassaq T. Alubaidi2, Faiq I. Gorial3, Ilham A. Jasim2

1Microbiology Unit, Emam Ali Hospital, Baghdad, Iraq
2Medical Research Unit, College of Medicine, Al-Nahrain University, Baghdad, Iraq
3Rheumatology Unit, Department of Medicine, College of Medicine, University of Baghdad, Baghdad, Iraq

Received December 27, 2021
Accepted August 2, 2022

References

1. Adamidis, K. N., Kopaka, M. E., Petraki, C., Charitaki, E., Apostolou, T., Christodoulidou, C., Nikolopoulou, N., Giatromanolaki, A., Vargemesis, V., Passadakis, P. (2019) Glomerular expression of matrix metalloproteinases in systemic lupus erythematosus in association with activity index and renal function. Ren. Fail. 41(1), 229–237. <https://doi.org/10.1080/0886022X.2019.1591998>
2. Ala, Y., Pasha, M. K., Rao, R. N., Komaravalli, P. L., Jahan, P. (2015) Association of IFN-γ: IL-10 cytokine ratio with nonsegmental vitiligo pathogenesis. Autoimmune Dis. 2015, 8.
3. Al-Hattab, M. K., Al-Waiz, M. (2004) Discoid lupus erythematosus in Iraqi patients: A clinical and histopathological study. Ann. Saudi Med. 24(4), 289–292. <https://doi.org/10.5144/0256-4947.2004.289>
4. Álvarez-Rodríguez, L., Martínez-Taboada, V., Calvo-Alén, J., Beares, I., Villa, I., López-Hoyos, M. (2019) Altered Th17/Treg ratio in peripheral blood of systemic lupus erythematosus but not primary antiphospholipid syndrome. Front. Immunol. 10, 391. <https://doi.org/10.3389/fimmu.2019.00391>
5. Becker-Merok, A., Eilertsen, G. Ø., Nossent, J. C. (2010) Levels of transforming growth factor-β are low in systemic lupus erythematosus patients with active disease. J. Rheumatol. 37(10), 2039–2045. <https://doi.org/10.3899/jrheum.100180>
6. Bombardier, C., Gladman, D. D., Urowitz, M. B., Caron, D., Chang, C. H., Austin, A., Bell, A., Bloch, D. A., Corey, P. N., Decker, J. L., Esdaile, J., Fries, J. F., Ginzler, E. M., Goldsmith, C. H., Hochberg, M. C., Jones, J. V., Le Riche, N. G. H., Liang, M. H., Lockshin, M. D., Muenz, L. R., Sackett, D. L., Schur, P. H. (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum. 35(6), 630–640. <https://doi.org/10.1002/art.1780350606>
7. Capone, A., Volpe, E. (2020) Transcriptional regulators of T helper 17 cell differentiation in health and autoimmune diseases. Front. Immunol. 11, 348. <https://doi.org/10.3389/fimmu.2020.00348>
8. Carrier, Y., Yuan, J., Kuchroo, V. K., Weiner, H. L. (2007) Th3 cells in peripheral tolerance. I. Induction of Foxp3-positive regulatory T cells by Th3 cells derived from TGF-β T cell-transgenic mice. J. Immunol. 178(1), 179–185. <https://doi.org/10.4049/jimmunol.178.1.179>
9. Chen, X. Q., Yu, Y. C., Deng, H. H., Sun, J. Z., Dai, Z., Wu, Y. W., Yang, M. (2010) Plasma IL-17A is increased in new-onset SLE patients and associated with disease activity. J. Clin. Immunol. 30(2), 221–225. <https://doi.org/10.1007/s10875-009-9365-x>
10. Chinen, T., Kannan, A., Levine, A., Fan, X., Klein, U., Zheng, Y., Gasteiger, G., Feng, Y., Fontenot, J., Rudensky, A. (2016) An essential role for IL-2 receptor in regulatory T cell function. Nat. Immunol. 17(11), 1322–1333. <https://doi.org/10.1038/ni.3540>
11. El Menyawi, M., Fawzy, M., Habib, M., Shaker, O. (2018) Serum transforming growth factor-beta 1 level in Egyptian systemic lupus erythematosus patients. Arch. Rheumatol. 33(3), 358–366. <https://doi.org/10.5606/ArchRheumatol.2018.6405>
12. Gladman, D. D., Urowitz, M. B., Kagal, A., Hallett, D. (2000) Accurately describing changes in disease activity in systemic lupus erythematosus. J. Rheumatol. 27(2), 377–379.
13. Hristova, M., Kamenarska, Z., Dzhebir, G., Nikolova, S., Hristova, R., Mihova, K., Vinkov, A., Georgiev, T., Pozharashka, J., Kaneva, R., Savov, A., Koundurdjiev, A., Dourmishev, L. (2021) The role of IL-17 rs2275913, IL-17RC rs708567 and TGFB1 rs1800469 SNPs and IL-17A serum levels in patients with lupus nephritis. Rheumatol. Int. 41(12), 2205–2213. <https://doi.org/10.1007/s00296-021-04996-z>
14. Joshi, N., Minz, R. W., Anand, S., Parmar, N. V., Kanwar, A. J. (2014) Vitamin D deficiency and lower TGF-β/IL-17 ratio in a North Indian cohort of pemphigus vulgaris. BMC Res. Notes 7(1), 1–6. <https://doi.org/10.1186/1756-0500-7-536>
15. Kleczynska, W., Jakiela, B., Plutecka, H., Milewski, M., Sanak, M., Musial, J. (2011) Imbalance between Th17 and regulatory T-cells in systemic lupus erythematosus. Folia Histochem. Cytobiol. 49(4), 646–653. <https://doi.org/10.5603/FHC.2011.0088>
16. Komai, T., Inoue, M., Okamura, T., Morita, K., Iwasaki, Y., Sumitomo, S., Shoda, H., Yamamoto, K., Fujio, K. (2018) Transforming growth factor-β and interleukin-10 synergistically regulate humoral immunity via modulating metabolic signals. Front. Immunol. 9, 1364. <https://doi.org/10.3389/fimmu.2018.01364>
17. Lamb, D., De Sousa, D., Quast, K., Fundel-Clemens, K., Erjefält, J. S., Sandén, C., Hoffmann, H. J., Kästle, M., Schmid, R., Menden, K., Delic, D. (2021) RORγt inhibitors block both IL-17 and IL-22 conferring a potential advantage over anti-IL-17 alone to treat severe asthma. Respir. Res. 22(1), 1–14. <https://doi.org/10.1186/s12931-021-01743-7>
18. Lee, H. T., Wu, T. H., Lin, C. S., Lee, C. S., Wei, Y. H., Tsai, C. Y., Chang, D. M. (2016) The pathogenesis of systemic lupus erythematosus – From the viewpoint of oxidative stress and mitochondrial dysfunction. Mitochondrion 30, 1–7. <https://doi.org/10.1016/j.mito.2016.05.007>
19. Lee, H. Y., Hong, Y. K., Yun, H. J., Kim, Y. M., Kim, J. R., Yoo, W. H. (2008) Altered frequency and migration capacity of CD4+ CD25+ regulatory T cells in systemic lupus erythematosus. Rheumatology 47(6), 789–794. <https://doi.org/10.1093/rheumatology/ken108>
20. Liu, R., Lauridsen, H. M., Amezquita, R. A., Pierce, R. W., Jane-Wit, D., Fang, C., Pellowe, A. S., Kirkiles-Smith, N. C., Gonzalez, A. L., Pober, J. S. (2016) IL-17 promotes neutrophil-mediated immunity by activating microvascular pericytes and not endothelium. J. Immunol. 197(6), 2400–2408. <https://doi.org/10.4049/jimmunol.1600138>
21. Liu, S. M., King, C. (2013) IL-21-producing Th cells in immunity and autoimmunity. J. Immunol. 191(7), 3501–3506. <https://doi.org/10.4049/jimmunol.1301454>
22. Metawie, S. A., ElRefai, R. M., ElAdle, S. S., Shahin, R. M. H. (2015) Transforming growth factor-β1 in systemic lupus erythematosus patients and its relation to organ damage and disease activity. Egyptian Rheumatologist 37(4), S49–S54. <https://doi.org/10.1016/j.ejr.2015.02.001>
23. Mitra, S., Anand, S., Das, A., Thapa, B., Chawla, Y. K., Minz, R. W. (2015) A molecular marker of disease activity in autoimmune liver diseases with histopathological correlation; FoXp3/RORγt ratio. APMIS 123(11), 935–944. <https://doi.org/10.1111/apm.12457>
24. Miyara, M., Amoura, Z., Parizot, C., Badoual, C., Dorgham, K., Trad, S., Nochy, D., Debré, P., Piette, J. C., Gorochov, G. (2005) Global natural regulatory T cell depletion in active systemic lupus erythematosus. J. Immunol. 175(12), 8392–8400. <https://doi.org/10.4049/jimmunol.175.12.8392>
25. Narani, A. (2019) Systemic lupus erythematosus (SLE) – A review of clinical approach for diagnosis and current treatment strategies. Jaffna Medical Journal 31(2), 9–13. <https://doi.org/10.4038/jmj.v31i2.73>
26. Oh, S. A., Li, M. O. (2013) TGF-β: Guardian of T cell function. J Immunol. 191(8), 3973–3979. <https://doi.org/10.4049/jimmunol.1301843>
27. Ouyang, W., Kolls, J. K., Zheng, Y. (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28(4), 454–467. <https://doi.org/10.1016/j.immuni.2008.03.004>
28. Petri, M., Orbai, A. M., Alarcon, G. S., Gordon, C., Merrill, J. T., Fortin, P. R., Bruce, I. N., Isenberg, D., Wallace, D. J., Nived, O., Sturfelt, G., Ramsey-Goldman, R., Bae, S. C., Hanly, J. G., Sánchez-Guerrero, J., Clarke, A., Aranow, C., Manzi, S., Urowitz, M., Gladman, D., Kalunian, K., Costner, M., Werth, V. P., Zoma, A., Bernatsky, S., Ruiz-Irastorza, G., Khamashta, M. A., Jacobsen, S., Buyon, J. P., Maddison, P., Dooley, M. A., van Vollenhoven, R. F., Ginzler, E., Stoll, T., Peschken, C., Jorizzo, J. L., Callen, J. P., Lim, S. S., Fessler, B. J., Inance, M., Kamen, D. L., Rahman, A., Steinsson, K., Franks, A. G. Jr., Sigler, L., Hameed, S., Fang, H., Pham, N., Brey, R., Weisman, M. H., McGwin, G. Jr., Magder, L. S. (2012) Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 64(8), 2677–2686. <https://doi.org/10.1002/art.34473>
29. Poeranto, S. (2019) Escalating dose antigen specific therapy with dsDNA injection regulate inflammatory cells in pristane-induced lupus mice model. Journal of Stem Cell Research and Tissue Engineering 3(1), 22–33. <https://doi.org/10.20473/jscrte.v3i1.16329>
30. Rafael-Vidal, C., Perez, N., Altabas, I., Garcia, S., Pego-Reigosa, J. (2020) Blocking IL-17: A promising strategy in the treatment of systemic rheumatic diseases. Int. J. Mol. Sci. 21, 7100. <https://doi.org/10.3390/ijms21197100>
31. Robert, M., Miossec, P. (2020) Interleukin-17 and lupus: Enough to be a target? For which patients? Lupus 29(1), 6–14. <https://doi.org/10.1177/0961203319891243>
32. Rowshanravan, B., Halliday, N., Sansom, D. M. (2018) CTLA-4: A moving target in immunotherapy. Blood 131(1), 58–67. <https://doi.org/10.1182/blood-2017-06-741033>
33. Schinocca, C., Rizzo, C., Fasano, S., Grasso, G., La Barbera, L., Ciccia, F., Guggino, G. (2021) Role of the IL-23/IL-17 pathway in rheumatic diseases: an overview. Front. Immunol. 12, 637829. <https://doi.org/10.3389/fimmu.2021.637829>
34. Vincent, F. B., Northcott, M., Hoi, A., Mackay, F., Morand, E. (2013) Clinical association of serum interleukin-17 in systemic lupus erythematosus. Arthritis Res. Ther. 15, R97. <https://doi.org/10.1186/ar4277>
35. Xing, Q., Wang, B., Su, H., Cui, J., Li, J. (2012) Elevated Th17 cells are accompanied by FoxP3+ Treg cells decrease in patients with lupus nephritis. Rheumatol. Int. 32(4), 949–958. <https://doi.org/10.1007/s00296-010-1771-0>
36. Yang, X. O., Nurieva, R., Martinez, G. J., Kang, H. S., Chung, Y., Pappu, B. P., Shah, B., Chang, S. H., Schluns, K. S., Watowich, S. S., Feng, X. H., Jetten, A. M., Dong, C. (2008) Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29(1), 44–56. <https://doi.org/10.1016/j.immuni.2008.05.007>
37. Yuliasih, Y., Rahmawati, L. D., Putri, R. M. (2019) Th17/Treg ratio and disease activity in systemic lupus erythematosus. Caspian J. Intern. Med. 10(1), 65–72.
38. Zhao, X. F., Pan, H. F., Yuan, H., Zhang, W. H., Li, X. P., Wang, G. H., Wu, G. C., Su, H., Pan, F. M., Li, W. X., Li, L. H., Chen, G. P., Ye, D. Q. (2010) Increased serum interleukin 17 in patients with systemic lupus erythematosus. Mol. Biol. Rep. 37(1), 81–85. <https://doi.org/10.1007/s11033-009-9533-3>
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