Evaluation of IL-17 Producing Memory Regulatory and Effector T Cells Expressing CD26 Molecule in Patients with Psoriasis
Abstract
Memory regulatory T cells (Tregs) has been demonstrated to produce IL-17 in Psoriasis. Forkhead box P3 (Foxp3) has been demonstrated not to be reliable marker to evaluate Treg cells. Effector CD4+T cells also express Foxp3 after activation. Human T helper-17 cells (Th-17) express high level of surface CD26, while regulatory T cells are CD26 negative or low and this phenotype is stable even after activation of Treg cells. In this study, we aimed to analyze IL-17 producing Treg cells using CD26. Memory T cells were isolated from 10 patients with psoriasis and 10 controls. Ex vivo stimulated IL-17 producing regulatory (Forkhead Box P3 (Foxp3)+CD25+CD26-/low) and effector (Foxp3+CD25+CD26hi) memory T cells were analyzed by flow cytometry. IL-23, IL-6, TNFα, TGFβ and IL-17 cytokine levels were also evaluated. No significant difference in IL-17+memory regulatory T cells was seen between patients and controls (p=0.19). A significant decrease in the percentage of IL-17 producing CD26hi effector memory T cells was observed in patients (p=0.04). However, the percentage of these cells was not different between patients with mild or severe form of psoriasis compared to controls (p=0.13). We could not find any significant difference regarding IL-23, IL-6, TNFα, TGFβ and IL-17 cytokine levels in plasma and cell culture supernatant samples between patients and controls. Taken together, our results showed a reduced IL-17 producing effector memory CD26hi T cells in patients with psoriasis compared to controls. However, IL-17 producing memory regulatory CD4+T cells of patients showed no significant difference from that of controls.
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2. Liang Y, Sarkar MK, Tsoi LC, Gudjonsson JE. Psoriasis: a mixed autoimmune and autoinflammatory disease. Curr Opin Immunol 2017; 49:1-8.
3. Ryan C, Korman NJ, Gelfand JM, Lim HW, Elmets CA, Feldman SR, et al. Research gaps in psoriasis: opportunities for future studies. J Am Acad Dermatol. 2014;70(1):146-67.
4. Kagami S, Rizzo HL, Lee JJ, Koguchi Y, Blauvelt A. Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol 2010; 130(5):1373-83.
5. Lowes MA, Kikuchi T, Fuentes-Duculan J, Cardinale I, Zaba LC, Haider AS, et al. Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol 2008; 128(5):1207-11.
6. Kagen M, McCormick T, Cooper K. Regulatory T cells in psoriasis. Cytokines as Potential Therapeutic Targets for Inflammatory Skin Diseases. Springer 2005; 193-209.
7. Sugiyama H, Gyulai R, Toichi E, Garaczi E, Shimada S, Stevens SR, et al. Dysfunctional blood and target tissue CD4+ CD25high regulatory T cells in psoriasis: mechanism underlying unrestrained pathogenic effector T cell proliferation. J Immunol 2005; 174(1):164-73.
8. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004; 22:531-62.
9. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155(3):1151-64.
10. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat Immunol 2003; 4(4):330-6.
11. Haiqi H, Yong Z, Yi L. Transcriptional regulation of Foxp3 in regulatory T cells. Immunobiology 2011; 216(6):678-85.
12. Hori S. Lineage stability and phenotypic plasticity of Foxp3+ regulatory T cells. Immunol Rev 2014; 259(1):159-72.
13. Duarte JH, Zelenay S, Bergman ML, Martins AC, Demengeot J. Natural Treg cells spontaneously differentiate into pathogenic helper cells in lymphopenic conditions. Eur J Immunol 2009; 39(4):948-55.
14. Bovenschen HJ, van de Kerkhof PC, van Erp PE, Woestenenk R, Joosten I, Koenen HJ. Foxp3+ Regulatory T Cells of Psoriasis Patients Easily Differentiate into IL-17A-Producing Cells and Are Found in Lesional Skin. J Invest Dermatol 2011; 131(9):1853-60.
15. Hovhannisyan Z, Treatman J, Littman DR, Mayer L. Characterization of interleukin-17–producing regulatory T cells in inflamed intestinal mucosa from patients with inflammatory bowel diseases. Gastroenterology 2011; 140(3):957-65.
16. Zhou L, Lopes JE, Chong MM, Ivanov II, Min R, Victora GD, et al. TGF-&bgr;-induced Foxp3 inhibits TH17 cell differentiation by antagonizing ROR&ggr; t function. Nature 2008; 453(7192):236-40.
17. Koenen HJ, Smeets RL, Vink PM, Van Rijssen E, Boots AM, Joosten I. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17–producing cells. Blood 2008; 112(6):2340-52.
18. Voo KS, Wang Y-H, Santori FR, Boggiano C, Wang Y-H, Arima K, et al. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc Natl Acad Sci U S A 2009; 106(12):4793-8.
19. Rubtsov YP, Niec RE, Josefowicz S, Li L, Darce J, Mathis D, et al. Stability of the regulatory T cell lineage in vivo. Science 2010; 329(5999):1667-71.
20. Miyao T, Floess S, Setoguchi R, Luche H, Fehling HJ, Waldmann H, et al. Plasticity of Foxp3+ T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 2012; 36(2):262-75.
21. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, et al. IL-17–producing human peripheral regulatory T cells retain suppressive function. Blood 2009; 113(18):4240-9.
22. Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-Hora M, Kodama T, et al. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med 2014; 20(1):62-8.
23. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+ FOXP3− T cells by T-cell receptor stimulation is transforming growth factor-β–dependent but does not confer a regulatory phenotype. Blood 2007; 110(8):2983-90.
24. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, Bacchetta R, et al. Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 2007; 19(4):345-54.
25. Rosenblum MD, Way SS, Abbas AK. Regulatory T cell memory. Nat Rev Immunol 2016; 16(2):90-101.
26. Klemann C, Wagner L, Stephan M, von Hörsten S. Cut to the chase: a review of CD26/dipeptidyl peptidase‐4's (DPP4) entanglement in the immune system. Clin Exp Immunol 2016; 185(1):1-21.
27. Pierson DM, Jones D, Muzzafar T, Kersh MJ, Challagundla P, Medeiros LJ, et al. Utility of CD26 in flow cytometric immunophenotyping of T‐cell lymphomas in tissue and body fluid specimens. Cytometry B Clin Cytom 2008; 74(6):341-8.
28. Bengsch B, Seigel B, Flecken T, Wolanski J, Blum HE, Thimme R. Human Th17 cells express high levels of enzymatically active dipeptidylpeptidase IV (CD26). J Immunol 2012; 188(11):5438-47.
29. Salgado FJ, Pérez‐Díaz A, Villanueva NM, Lamas O, Arias P, Nogueira M. CD26: a negative selection marker for human Treg cells. Cytometry A 2012; 81(10):843-55.
30. Garcia Santana CA, Tung JW, Gulnik S. Human treg cells are characterized by low/negative CD6 expression. Cytometry A 2014; 85(10):901-8.
31. Mandapathil M, Hilldorfer B, Szczepanski MJ, Czystowska M, Szajnik M, Ren J, et al. Generation and accumulation of immunosuppressive adenosine by human CD4+ CD25highFOXP3+ regulatory T cells. J Biol Chem 2010; 285(10):7176-86.
32. Schmitt J, Wozel G. The psoriasis area and severity index is the adequate criterion to define severity in chronic plaque-type psoriasis. Dermatology 2005; 210(3):194-9.
33. Girolomoni G, Mrowietz U, Paul C. Psoriasis: rationale for targeting interleukin‐17. Br J Dermatol 2012; 167(4):717-24.
34. Martin DA, Towne JE, Kricorian G, Klekotka P, Gudjonsson JE, Krueger JG, et al. The emerging role of IL-17 in the pathogenesis of psoriasis: preclinical and clinical findings. J Invest Dermatol 2013; 133(1):17-26.
35. Kryczek I, Wu K, Zhao E, Wei S, Vatan L, Szeliga W, et al. IL-17+ regulatory T cells in the microenvironments of chronic inflammation and cancer. J Immunol 2011; 186(7):4388-95.
36. Aerts NE, Dombrecht EJ, Ebo DG, Bridts CH, Stevens WJ, De Clerck LS. Activated T cells complicate the identification of regulatory T cells in rheumatoid arthritis. Cell Immunol 2008; 251(2):109-15.
37. Mandapathil M, Lang S, Gorelik E, Whiteside TL. Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. J Immunol Methods 2009; 346(1):55-63.
38. Mandapathil M, Szczepanski M, Harasymczuk M, Ren J, Cheng D, Jackson EK, et al. CD26 expression and adenosine deaminase activity in regulatory T cells (Treg) and CD4+ T effector cells in patients with head and neck squamous cell carcinoma. Oncoimmunology 2012; 1(5):659-69.
39. Bailey SR, Nelson MH, Majchrzak K, Bowers JS, Wyatt MM, Smith AS, et al. Human CD26 high T cells elicit tumor immunity against multiple malignancies via enhanced migration and persistence. Nature communications. 2017;8(1):1961.
40. Nikaein A, Phillips C, Gilbert SC, Savino D, Silverman A, Stone MJ, et al. Characterization of skin-infiltrating lymphocytes in patients with psoriasis. J Invest Dermatol 1991; 96(1):3-9.
41. Michalak-Stoma A, Pietrzak A, Szepietowski JC, Zalewska-Janowska A, Paszkowski T, Chodorowska G. Cytokine network in psoriasis revisited. Eur Cytokine Netw 2011; 22(4):160-8.
42 Arican O, Aral M, Sasmaz S, Ciragil P. Serum levels of TNF-α, IFN-γ, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm 2005; 2005(5):273-9.
43. Kyriakou A, Patsatsi A, Vyzantiadis T-A, Sotiriadis D. Serum levels of TNF-α, IL-12/23p40, and IL-17 in plaque psoriasis and their correlation with disease severity. J Immunol Res 2014; 2014:467541.
44 Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006; 24(2):179-89.
45. Aggarwal S, Ghilardi N, Xie M-H, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278(3):1910-4.
46 Grossman RM, Krueger J, Yourish D, Granelli-Piperno A, Murphy DP, May LT, et al. Interleukin 6 is expressed in high levels in psoriatic skin and stimulates proliferation of cultured human keratinocytes. Proc Natl Acad Sci U S A 1989; 86(16):6367-71.
47 Goodman WA, Levine AD, Massari JV, Sugiyama H, McCormick TS, Cooper KD. IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J Immunol 2009; 183(5):3170-6.
48. Di Meglio P, Nestle FO. The role of IL-23 in the immunopathogenesis of psoriasis. F1000 Biol Rep 2010; 2.
49 Nockowski P, Szepietowski J, Ziarkiewicz M, Baran E. Serum concentrations of transforming growth factor beta 1 in patients with psoriasis vulgaris. Acta Dermatovenerol Croat 2003; 12(1):2-6.
50. Zaher H, Shaker O, EL‐Komy M, El‐Tawdi A, Fawzi M, Kadry D. Serum and tissue expression of transforming growth factor beta 1 in psoriasis. Journal J Eur Acad Dermatol Venereol 2009; 23(4):406-9.
51. Zhang L, Yang X-Q, Cheng J, Hui R-S, Gao T-W. Increased Th17 cells are accompanied by FoxP3+ Treg cell accumulation and correlated with psoriasis disease severity. Clin Immunol 2010; 135(1):108-17.
52. Oliveira PSSd, Cardoso PRG, Lima EVdA, Pereira MC, Duarte ALBP, Pitta IdR, et al. IL-17A, IL-22, IL-6, and IL-21 serum levels in plaque-type psoriasis in Brazilian patients. Mediators Inflamm 2015; 2015:819149.
2. Liang Y, Sarkar MK, Tsoi LC, Gudjonsson JE. Psoriasis: a mixed autoimmune and autoinflammatory disease. Curr Opin Immunol 2017; 49:1-8.
3. Ryan C, Korman NJ, Gelfand JM, Lim HW, Elmets CA, Feldman SR, et al. Research gaps in psoriasis: opportunities for future studies. J Am Acad Dermatol. 2014;70(1):146-67.
4. Kagami S, Rizzo HL, Lee JJ, Koguchi Y, Blauvelt A. Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol 2010; 130(5):1373-83.
5. Lowes MA, Kikuchi T, Fuentes-Duculan J, Cardinale I, Zaba LC, Haider AS, et al. Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol 2008; 128(5):1207-11.
6. Kagen M, McCormick T, Cooper K. Regulatory T cells in psoriasis. Cytokines as Potential Therapeutic Targets for Inflammatory Skin Diseases. Springer 2005; 193-209.
7. Sugiyama H, Gyulai R, Toichi E, Garaczi E, Shimada S, Stevens SR, et al. Dysfunctional blood and target tissue CD4+ CD25high regulatory T cells in psoriasis: mechanism underlying unrestrained pathogenic effector T cell proliferation. J Immunol 2005; 174(1):164-73.
8. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004; 22:531-62.
9. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155(3):1151-64.
10. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+ CD25+ regulatory T cells. Nat Immunol 2003; 4(4):330-6.
11. Haiqi H, Yong Z, Yi L. Transcriptional regulation of Foxp3 in regulatory T cells. Immunobiology 2011; 216(6):678-85.
12. Hori S. Lineage stability and phenotypic plasticity of Foxp3+ regulatory T cells. Immunol Rev 2014; 259(1):159-72.
13. Duarte JH, Zelenay S, Bergman ML, Martins AC, Demengeot J. Natural Treg cells spontaneously differentiate into pathogenic helper cells in lymphopenic conditions. Eur J Immunol 2009; 39(4):948-55.
14. Bovenschen HJ, van de Kerkhof PC, van Erp PE, Woestenenk R, Joosten I, Koenen HJ. Foxp3+ Regulatory T Cells of Psoriasis Patients Easily Differentiate into IL-17A-Producing Cells and Are Found in Lesional Skin. J Invest Dermatol 2011; 131(9):1853-60.
15. Hovhannisyan Z, Treatman J, Littman DR, Mayer L. Characterization of interleukin-17–producing regulatory T cells in inflamed intestinal mucosa from patients with inflammatory bowel diseases. Gastroenterology 2011; 140(3):957-65.
16. Zhou L, Lopes JE, Chong MM, Ivanov II, Min R, Victora GD, et al. TGF-&bgr;-induced Foxp3 inhibits TH17 cell differentiation by antagonizing ROR&ggr; t function. Nature 2008; 453(7192):236-40.
17. Koenen HJ, Smeets RL, Vink PM, Van Rijssen E, Boots AM, Joosten I. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17–producing cells. Blood 2008; 112(6):2340-52.
18. Voo KS, Wang Y-H, Santori FR, Boggiano C, Wang Y-H, Arima K, et al. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc Natl Acad Sci U S A 2009; 106(12):4793-8.
19. Rubtsov YP, Niec RE, Josefowicz S, Li L, Darce J, Mathis D, et al. Stability of the regulatory T cell lineage in vivo. Science 2010; 329(5999):1667-71.
20. Miyao T, Floess S, Setoguchi R, Luche H, Fehling HJ, Waldmann H, et al. Plasticity of Foxp3+ T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 2012; 36(2):262-75.
21. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, et al. IL-17–producing human peripheral regulatory T cells retain suppressive function. Blood 2009; 113(18):4240-9.
22. Komatsu N, Okamoto K, Sawa S, Nakashima T, Oh-Hora M, Kodama T, et al. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat Med 2014; 20(1):62-8.
23. Tran DQ, Ramsey H, Shevach EM. Induction of FOXP3 expression in naive human CD4+ FOXP3− T cells by T-cell receptor stimulation is transforming growth factor-β–dependent but does not confer a regulatory phenotype. Blood 2007; 110(8):2983-90.
24. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, Bacchetta R, et al. Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 2007; 19(4):345-54.
25. Rosenblum MD, Way SS, Abbas AK. Regulatory T cell memory. Nat Rev Immunol 2016; 16(2):90-101.
26. Klemann C, Wagner L, Stephan M, von Hörsten S. Cut to the chase: a review of CD26/dipeptidyl peptidase‐4's (DPP4) entanglement in the immune system. Clin Exp Immunol 2016; 185(1):1-21.
27. Pierson DM, Jones D, Muzzafar T, Kersh MJ, Challagundla P, Medeiros LJ, et al. Utility of CD26 in flow cytometric immunophenotyping of T‐cell lymphomas in tissue and body fluid specimens. Cytometry B Clin Cytom 2008; 74(6):341-8.
28. Bengsch B, Seigel B, Flecken T, Wolanski J, Blum HE, Thimme R. Human Th17 cells express high levels of enzymatically active dipeptidylpeptidase IV (CD26). J Immunol 2012; 188(11):5438-47.
29. Salgado FJ, Pérez‐Díaz A, Villanueva NM, Lamas O, Arias P, Nogueira M. CD26: a negative selection marker for human Treg cells. Cytometry A 2012; 81(10):843-55.
30. Garcia Santana CA, Tung JW, Gulnik S. Human treg cells are characterized by low/negative CD6 expression. Cytometry A 2014; 85(10):901-8.
31. Mandapathil M, Hilldorfer B, Szczepanski MJ, Czystowska M, Szajnik M, Ren J, et al. Generation and accumulation of immunosuppressive adenosine by human CD4+ CD25highFOXP3+ regulatory T cells. J Biol Chem 2010; 285(10):7176-86.
32. Schmitt J, Wozel G. The psoriasis area and severity index is the adequate criterion to define severity in chronic plaque-type psoriasis. Dermatology 2005; 210(3):194-9.
33. Girolomoni G, Mrowietz U, Paul C. Psoriasis: rationale for targeting interleukin‐17. Br J Dermatol 2012; 167(4):717-24.
34. Martin DA, Towne JE, Kricorian G, Klekotka P, Gudjonsson JE, Krueger JG, et al. The emerging role of IL-17 in the pathogenesis of psoriasis: preclinical and clinical findings. J Invest Dermatol 2013; 133(1):17-26.
35. Kryczek I, Wu K, Zhao E, Wei S, Vatan L, Szeliga W, et al. IL-17+ regulatory T cells in the microenvironments of chronic inflammation and cancer. J Immunol 2011; 186(7):4388-95.
36. Aerts NE, Dombrecht EJ, Ebo DG, Bridts CH, Stevens WJ, De Clerck LS. Activated T cells complicate the identification of regulatory T cells in rheumatoid arthritis. Cell Immunol 2008; 251(2):109-15.
37. Mandapathil M, Lang S, Gorelik E, Whiteside TL. Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. J Immunol Methods 2009; 346(1):55-63.
38. Mandapathil M, Szczepanski M, Harasymczuk M, Ren J, Cheng D, Jackson EK, et al. CD26 expression and adenosine deaminase activity in regulatory T cells (Treg) and CD4+ T effector cells in patients with head and neck squamous cell carcinoma. Oncoimmunology 2012; 1(5):659-69.
39. Bailey SR, Nelson MH, Majchrzak K, Bowers JS, Wyatt MM, Smith AS, et al. Human CD26 high T cells elicit tumor immunity against multiple malignancies via enhanced migration and persistence. Nature communications. 2017;8(1):1961.
40. Nikaein A, Phillips C, Gilbert SC, Savino D, Silverman A, Stone MJ, et al. Characterization of skin-infiltrating lymphocytes in patients with psoriasis. J Invest Dermatol 1991; 96(1):3-9.
41. Michalak-Stoma A, Pietrzak A, Szepietowski JC, Zalewska-Janowska A, Paszkowski T, Chodorowska G. Cytokine network in psoriasis revisited. Eur Cytokine Netw 2011; 22(4):160-8.
42 Arican O, Aral M, Sasmaz S, Ciragil P. Serum levels of TNF-α, IFN-γ, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm 2005; 2005(5):273-9.
43. Kyriakou A, Patsatsi A, Vyzantiadis T-A, Sotiriadis D. Serum levels of TNF-α, IL-12/23p40, and IL-17 in plaque psoriasis and their correlation with disease severity. J Immunol Res 2014; 2014:467541.
44 Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006; 24(2):179-89.
45. Aggarwal S, Ghilardi N, Xie M-H, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 2003; 278(3):1910-4.
46 Grossman RM, Krueger J, Yourish D, Granelli-Piperno A, Murphy DP, May LT, et al. Interleukin 6 is expressed in high levels in psoriatic skin and stimulates proliferation of cultured human keratinocytes. Proc Natl Acad Sci U S A 1989; 86(16):6367-71.
47 Goodman WA, Levine AD, Massari JV, Sugiyama H, McCormick TS, Cooper KD. IL-6 signaling in psoriasis prevents immune suppression by regulatory T cells. J Immunol 2009; 183(5):3170-6.
48. Di Meglio P, Nestle FO. The role of IL-23 in the immunopathogenesis of psoriasis. F1000 Biol Rep 2010; 2.
49 Nockowski P, Szepietowski J, Ziarkiewicz M, Baran E. Serum concentrations of transforming growth factor beta 1 in patients with psoriasis vulgaris. Acta Dermatovenerol Croat 2003; 12(1):2-6.
50. Zaher H, Shaker O, EL‐Komy M, El‐Tawdi A, Fawzi M, Kadry D. Serum and tissue expression of transforming growth factor beta 1 in psoriasis. Journal J Eur Acad Dermatol Venereol 2009; 23(4):406-9.
51. Zhang L, Yang X-Q, Cheng J, Hui R-S, Gao T-W. Increased Th17 cells are accompanied by FoxP3+ Treg cell accumulation and correlated with psoriasis disease severity. Clin Immunol 2010; 135(1):108-17.
52. Oliveira PSSd, Cardoso PRG, Lima EVdA, Pereira MC, Duarte ALBP, Pitta IdR, et al. IL-17A, IL-22, IL-6, and IL-21 serum levels in plaque-type psoriasis in Brazilian patients. Mediators Inflamm 2015; 2015:819149.
| Files | ||
| Issue | Vol 17, No 5 (2018) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v17i5.303 | |
| Keywords | ||
| CD26 Foxp3 Interleukin-17 Psoriasis Regulatory T–lymphocytes | ||
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How to Cite
1.
Esmaeili B, Mansouri P, Meysamie A, Izad M. Evaluation of IL-17 Producing Memory Regulatory and Effector T Cells Expressing CD26 Molecule in Patients with Psoriasis. Iran J Allergy Asthma Immunol. 2018;17(5):453-463.
