Skip to main content
Top
Published in: Thyroid Research 1/2018

Open Access 01-12-2018 | Short report

Role of the T and B lymphocytes in pathogenesis of autoimmune thyroid diseases

Authors: Marta Rydzewska, Michał Jaromin, Izabela Elżbieta Pasierowska, Karlina Stożek, Artur Bossowski

Published in: Thyroid Research | Issue 1/2018

Login to get access

Abstract

Autoimmune thyroid disorders (AITD) broadly include Graves’ disease and Hashimoto’s thyroiditis which are the most common causes of thyroid gland dysfunctions. These disorders develop due to complex interactions between environmental and genetic factors and are characterized by reactivity to self-thyroid antigens due to autoreactive lymphocytes escaping tolerance. Both cell-mediated and humoral responses lead to tissue injury in autoimmune thyroid disease. The differentiation of CD4+ cells in the specific setting of immune mediators (for example cytokines, chemokines) results in differentiation of various T cell subsets. T cell identification has shown a mixed pattern of cytokine production indicating that both subtypes of T helper, Th1 and Th2, responses are involved in all types of AITD. Furthermore, recent studies described T cell subtypes Th17 and Treg which also play an essential role in pathogenesis of AITD. This review will focus on the role of the T regulatory (Treg) and T helper (Th) (especially Th17) lymphocytes, and also of B lymphocytes in AITD pathogenesis. However, we have much more to learn about cellular mechanisms and interactions in AITD before we can develop complete understanding of AITD pathophysiology.
Literature
1.
go back to reference Iwatani Y, Watanabe M. Normal mechanisms for self-tolerance. In: Volpe R, editor. Autoimmune Endocrinopathies. Totowa, NJ: Humana Press; 1999. p. 1–31. Iwatani Y, Watanabe M. Normal mechanisms for self-tolerance. In: Volpe R, editor. Autoimmune Endocrinopathies. Totowa, NJ: Humana Press; 1999. p. 1–31.
2.
go back to reference Hollowell JG, Staehling NW, Flanders WD, Hannon WH, Gunter EW, Spencer CA, Braverman LE, Serum TSH. T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and nutrition examination survey(NHANES III). J Clin Endocrinol Metab. 2002;87:489–99.PubMedCrossRef Hollowell JG, Staehling NW, Flanders WD, Hannon WH, Gunter EW, Spencer CA, Braverman LE, Serum TSH. T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and nutrition examination survey(NHANES III). J Clin Endocrinol Metab. 2002;87:489–99.PubMedCrossRef
4.
go back to reference Foley TP Jr, Abbassi V, Copeland KC, Draznin MB. Brief report: hypothyroidism caused by chronic autoimmune thyroiditis in very young infants. N Engl J Med. 1994;330:466–8.PubMedCrossRef Foley TP Jr, Abbassi V, Copeland KC, Draznin MB. Brief report: hypothyroidism caused by chronic autoimmune thyroiditis in very young infants. N Engl J Med. 1994;330:466–8.PubMedCrossRef
6.
go back to reference Jacobson DL, Gange SJ, Rose NR, Graham NM. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol. 1997;84:223–43.PubMedCrossRef Jacobson DL, Gange SJ, Rose NR, Graham NM. Epidemiology and estimated population burden of selected autoimmune diseases in the United States. Clin Immunol Immunopathol. 1997;84:223–43.PubMedCrossRef
7.
go back to reference Carle A, Pedersen IB, Knudsen N, Perrild H, Ovesen L, Rasmussen LB, Laurberg P. Epidemiology of subtypes of hyperthyroidism in Denmark: a population-based study. Eur J Endocrinol. 2011;164:801–9.PubMedCrossRef Carle A, Pedersen IB, Knudsen N, Perrild H, Ovesen L, Rasmussen LB, Laurberg P. Epidemiology of subtypes of hyperthyroidism in Denmark: a population-based study. Eur J Endocrinol. 2011;164:801–9.PubMedCrossRef
8.
go back to reference Antonelli A, Ferrari SM, Corrado A, Di Domenicantonio A, Fallahi P. Autoimmune thyroid disorders. Autoimmun Rev. 2015;14:174–80.PubMedCrossRef Antonelli A, Ferrari SM, Corrado A, Di Domenicantonio A, Fallahi P. Autoimmune thyroid disorders. Autoimmun Rev. 2015;14:174–80.PubMedCrossRef
10.
go back to reference Ramos-Leví AM, Marazuela M. Pathogenesis of thyroid auto- immune disease: the role of cellular mechanisms. Endocrinol Nutr. 2016;63:421–9.PubMedCrossRef Ramos-Leví AM, Marazuela M. Pathogenesis of thyroid auto- immune disease: the role of cellular mechanisms. Endocrinol Nutr. 2016;63:421–9.PubMedCrossRef
11.
go back to reference Nanba T, Watanabe M, Inoue N, Iwatani Y. Increases of the Th1/Th2 cell ratio in severe Hashimoto’s disease and in the proportion of Th17 cells in intractable graves’ disease. Thyroid. 2009;19:495–501.PubMedCrossRef Nanba T, Watanabe M, Inoue N, Iwatani Y. Increases of the Th1/Th2 cell ratio in severe Hashimoto’s disease and in the proportion of Th17 cells in intractable graves’ disease. Thyroid. 2009;19:495–501.PubMedCrossRef
14.
go back to reference Caturegli P, De Remigis A, Rose NR. Hashimoto thyroiditis: clinical and diagnostic criteria. Autoimmun Rev. 2014;13:391–7.PubMedCrossRef Caturegli P, De Remigis A, Rose NR. Hashimoto thyroiditis: clinical and diagnostic criteria. Autoimmun Rev. 2014;13:391–7.PubMedCrossRef
16.
go back to reference Evans C, Morgenthaler NG, Lee S, Llewellyn DH, Clifton-Bligh R, John R, Lazarus JH, Chatterjee VK, Ludgate M. Development of a luminescent bioassay for thyroid stimulating antibodies. J Clin Endocrinol Metab. 1999;84:374–7.PubMedCrossRef Evans C, Morgenthaler NG, Lee S, Llewellyn DH, Clifton-Bligh R, John R, Lazarus JH, Chatterjee VK, Ludgate M. Development of a luminescent bioassay for thyroid stimulating antibodies. J Clin Endocrinol Metab. 1999;84:374–7.PubMedCrossRef
17.
go back to reference Latif R, Morshed SA, Zaidi M, Davies TF. The thyroid-stimulating hormone receptor: impact of thyroid-stimulating hormone and thyroid-stimulating hormone receptor antibodies on multimerization, cleavage, and signaling. Endocrinol Metab Clin N Am. 2009;38:319–41.CrossRef Latif R, Morshed SA, Zaidi M, Davies TF. The thyroid-stimulating hormone receptor: impact of thyroid-stimulating hormone and thyroid-stimulating hormone receptor antibodies on multimerization, cleavage, and signaling. Endocrinol Metab Clin N Am. 2009;38:319–41.CrossRef
18.
go back to reference Menconi F, Marcocci C, Marinò M. Diagnosis and classification of graves’ disease. Autoimmun Rev. 2014;13:398–402.PubMedCrossRef Menconi F, Marcocci C, Marinò M. Diagnosis and classification of graves’ disease. Autoimmun Rev. 2014;13:398–402.PubMedCrossRef
19.
go back to reference Bossowski A, Stasiak-Barmuta A, Urban M. Relationship between CTLA-4 and CD28 molecule expression on T lymphocytes and stimulating and blocking autoantibodies to the TSH-receptor in children with graves’ disease. Horm Res. 2005;64:189–97. https://doi.org/10.1159/000088875.PubMed Bossowski A, Stasiak-Barmuta A, Urban M. Relationship between CTLA-4 and CD28 molecule expression on T lymphocytes and stimulating and blocking autoantibodies to the TSH-receptor in children with graves’ disease. Horm Res. 2005;64:189–97. https://​doi.​org/​10.​1159/​000088875.PubMed
20.
go back to reference Bossowski A, Stasiak-Barmuta A, Urban M, Bossowska A. Analysis of costimulatory molecules OX40/4-1 BB (CD1 34/CD1 37) detection on chosen mononuclear cells in children and adolescents with graves’ disease during methimazole therapy. J Pediatr Endocrinol Metab. 2005;18:1365–72.PubMedCrossRef Bossowski A, Stasiak-Barmuta A, Urban M, Bossowska A. Analysis of costimulatory molecules OX40/4-1 BB (CD1 34/CD1 37) detection on chosen mononuclear cells in children and adolescents with graves’ disease during methimazole therapy. J Pediatr Endocrinol Metab. 2005;18:1365–72.PubMedCrossRef
21.
go back to reference Tanda ML, Piantanida E, Liparulo L, Veronesi G, Lai A, Sassi L, et al. Prevalence and natural history of graves’ orbitopathy in a large series of patients with newly diagnosed graves’ hyperthyroidism seen at a single center. J Clin Endocrinol Metab. 2013;98:1443–9.PubMedCrossRef Tanda ML, Piantanida E, Liparulo L, Veronesi G, Lai A, Sassi L, et al. Prevalence and natural history of graves’ orbitopathy in a large series of patients with newly diagnosed graves’ hyperthyroidism seen at a single center. J Clin Endocrinol Metab. 2013;98:1443–9.PubMedCrossRef
22.
go back to reference Shan SJ, Douglas RS. The pathophysiology of thyroid eye disease. J Neuroophthalmol. 2014;34:177–85.PubMedCrossRef Shan SJ, Douglas RS. The pathophysiology of thyroid eye disease. J Neuroophthalmol. 2014;34:177–85.PubMedCrossRef
23.
go back to reference Hadj-Kacem H, Rebuffat S, Mnif-Feki M, Belguith-Maalej S, Ayadi H, Peraldi-Roux S. Autoimmune thyroid dis- eases: genetic susceptibility of thyroid-specific genes and thyroid autoantigens contributions. Int J Immunogenet. 2009;36:85–96.PubMedCrossRef Hadj-Kacem H, Rebuffat S, Mnif-Feki M, Belguith-Maalej S, Ayadi H, Peraldi-Roux S. Autoimmune thyroid dis- eases: genetic susceptibility of thyroid-specific genes and thyroid autoantigens contributions. Int J Immunogenet. 2009;36:85–96.PubMedCrossRef
24.
go back to reference Duntas LH. Environmental factors and autoimmune thyroiditis. Nat Clin Pract Endocrinol Metab. 2008;4:454–60.PubMedCrossRef Duntas LH. Environmental factors and autoimmune thyroiditis. Nat Clin Pract Endocrinol Metab. 2008;4:454–60.PubMedCrossRef
25.
go back to reference Marino M, Latrofa F, Menconi F, Chiovato L, Vitti P. Role of genetic and non- genetic factors in the etiology of graves’ disease. J Endocrinol Investig. 2015;38:283–94.CrossRef Marino M, Latrofa F, Menconi F, Chiovato L, Vitti P. Role of genetic and non- genetic factors in the etiology of graves’ disease. J Endocrinol Investig. 2015;38:283–94.CrossRef
27.
go back to reference Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature. 1996;383:787–93.PubMedCrossRef Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature. 1996;383:787–93.PubMedCrossRef
29.
go back to reference Kronenberg M, Siu G, Hood LE, Shastri N. The molecular genetics of the T-cell antigen receptor and T- cell antigen recognition. Annu Rev Immunol. 1986;4:529–91.PubMedCrossRef Kronenberg M, Siu G, Hood LE, Shastri N. The molecular genetics of the T-cell antigen receptor and T- cell antigen recognition. Annu Rev Immunol. 1986;4:529–91.PubMedCrossRef
31.
33.
go back to reference Mosmann TR, Coffman RL. Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Ann Rev Immunol. 1989;7:145–73.CrossRef Mosmann TR, Coffman RL. Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Ann Rev Immunol. 1989;7:145–73.CrossRef
34.
go back to reference Hu C, Salgame P. Inability of interleukin-12 to modulate T-helper 0 effectors to T-helper 1 effectors: a possible distinct subset of T cells. Immunology. 1999;97:84–91.PubMedPubMedCentralCrossRef Hu C, Salgame P. Inability of interleukin-12 to modulate T-helper 0 effectors to T-helper 1 effectors: a possible distinct subset of T cells. Immunology. 1999;97:84–91.PubMedPubMedCentralCrossRef
35.
go back to reference Chaplin DD. Overview of the immune response. J Allergy Clin Immunol. 2010;125:3–23.CrossRef Chaplin DD. Overview of the immune response. J Allergy Clin Immunol. 2010;125:3–23.CrossRef
36.
go back to reference Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature. 2006;441:235–8.PubMedCrossRef Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector Th17 and regulatory T cells. Nature. 2006;441:235–8.PubMedCrossRef
37.
go back to reference Nossal GJ, Pike BL. Evidence for the clonal abortion theory of B-lymphocyte tolerance. J Exp Med. 1975;141:904–17.PubMed Nossal GJ, Pike BL. Evidence for the clonal abortion theory of B-lymphocyte tolerance. J Exp Med. 1975;141:904–17.PubMed
38.
go back to reference Volpe R, Iitaka M. Evidence for an antigen-specific defect in suppressor T- lymphocytes in autoimmune thyroid disease. Exp Clin Endocrinol. 1991;97:133–8.PubMedCrossRef Volpe R, Iitaka M. Evidence for an antigen-specific defect in suppressor T- lymphocytes in autoimmune thyroid disease. Exp Clin Endocrinol. 1991;97:133–8.PubMedCrossRef
39.
go back to reference Parijs LV, Abbas AK. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science. 1998;280:243–8.PubMedCrossRef Parijs LV, Abbas AK. Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science. 1998;280:243–8.PubMedCrossRef
40.
go back to reference Bartalena L, Tanda ML, Piantanida A, et al. Environment and thyroid autoimmunity. In: Wiersinga WM, Drexhage HA, Weetman AP, et al., editors. The thyroid and autoimmunity. Stuttgart: Verlag; 2007. p. 60–73. Bartalena L, Tanda ML, Piantanida A, et al. Environment and thyroid autoimmunity. In: Wiersinga WM, Drexhage HA, Weetman AP, et al., editors. The thyroid and autoimmunity. Stuttgart: Verlag; 2007. p. 60–73.
41.
go back to reference Tamai H, Ohsako N, Takeno K, et al. Changes in thyroid function in euthyroid subjects with family history of graves’ disease; a follow up study of 69 patients. J Clin Endocrinol Metab. 1980;51:1123–8.PubMedCrossRef Tamai H, Ohsako N, Takeno K, et al. Changes in thyroid function in euthyroid subjects with family history of graves’ disease; a follow up study of 69 patients. J Clin Endocrinol Metab. 1980;51:1123–8.PubMedCrossRef
42.
go back to reference Kraiem Z, Baron E, Kahana L, Sadeh O, Sheinfeld M. Changes in stimulating and blocking TSH receptor antibodies in a patient undergoing three cycles of transition from hypo to hyper-thyroidism and back to hypothyroidism. Clin Endocrinol. 1992;36:211.CrossRef Kraiem Z, Baron E, Kahana L, Sadeh O, Sheinfeld M. Changes in stimulating and blocking TSH receptor antibodies in a patient undergoing three cycles of transition from hypo to hyper-thyroidism and back to hypothyroidism. Clin Endocrinol. 1992;36:211.CrossRef
43.
go back to reference Ajjan RA, Watson PF, Weetman AP. Cytokines and thyroid function. Adv Neuroimmunol. 1996;6:359–86.PubMedCrossRef Ajjan RA, Watson PF, Weetman AP. Cytokines and thyroid function. Adv Neuroimmunol. 1996;6:359–86.PubMedCrossRef
44.
go back to reference Ben-Skowronek I, Szewczyk L, Kulik-Rechberger B, Korobowicz E. The differences in T and B cell subsets in thyroid of children with graves’ disease and Hashimoto’s thyroiditis. World J Pediatr. 2013;9:245–50.PubMedCrossRef Ben-Skowronek I, Szewczyk L, Kulik-Rechberger B, Korobowicz E. The differences in T and B cell subsets in thyroid of children with graves’ disease and Hashimoto’s thyroiditis. World J Pediatr. 2013;9:245–50.PubMedCrossRef
45.
go back to reference Giordano C, Stassi G, De Maria R, et al. Potential involvement of Fas and its ligand in the pathogenesis of Hashimoto’s thyroiditis. Science. 1997;275:960–3.PubMedCrossRef Giordano C, Stassi G, De Maria R, et al. Potential involvement of Fas and its ligand in the pathogenesis of Hashimoto’s thyroiditis. Science. 1997;275:960–3.PubMedCrossRef
46.
go back to reference Berghi NO. Immunological mechanisms implicated in the pathogenesis of chronic Urticaria and Hashimoto thyroiditis. Iran J Allergy Asthma Immunol. 2017;16(4):358–66.PubMed Berghi NO. Immunological mechanisms implicated in the pathogenesis of chronic Urticaria and Hashimoto thyroiditis. Iran J Allergy Asthma Immunol. 2017;16(4):358–66.PubMed
48.
go back to reference Chardes T, Chapal N, Bresson D, Bes C, Giudicelli V, Lefranc MP, Peraldi-Roux S. The human anti-thyroid peroxidase autoantibody repertoire in graves’ and Hashimoto’s autoimmune thyroid diseases. Immunogenetics. 2002;54:141–57.PubMedCrossRef Chardes T, Chapal N, Bresson D, Bes C, Giudicelli V, Lefranc MP, Peraldi-Roux S. The human anti-thyroid peroxidase autoantibody repertoire in graves’ and Hashimoto’s autoimmune thyroid diseases. Immunogenetics. 2002;54:141–57.PubMedCrossRef
49.
go back to reference Siebenkotten G, Radbruch A. Towards a molecular understanding of immunoglobulin class switching. Ther Immunol. 1995;3:141–6. Siebenkotten G, Radbruch A. Towards a molecular understanding of immunoglobulin class switching. Ther Immunol. 1995;3:141–6.
50.
go back to reference Rapoport B, McLachlan SM. Graves’ hyperthyroidism is antibody-mediated but is predominantly a Th1-type cytokine disease. J Clin Endocrinol Metab. 2014;99:4060–1.PubMedPubMedCentralCrossRef Rapoport B, McLachlan SM. Graves’ hyperthyroidism is antibody-mediated but is predominantly a Th1-type cytokine disease. J Clin Endocrinol Metab. 2014;99:4060–1.PubMedPubMedCentralCrossRef
52.
go back to reference Leovey A, Nagy E, Balazs G, Bako G. Lymphocytes resided in the thyroid are the main source of TSH-receptor antibodies in basedow’s-graves’ disease? Exp Clin Endocrinol. 1992;99:147–50.PubMedCrossRef Leovey A, Nagy E, Balazs G, Bako G. Lymphocytes resided in the thyroid are the main source of TSH-receptor antibodies in basedow’s-graves’ disease? Exp Clin Endocrinol. 1992;99:147–50.PubMedCrossRef
53.
go back to reference McLachlan SM, Rapoport B. Breaking tolerance to thyroid antigens: changing concepts in thyroid autoimmunity. Endocr Rev. 2014;35:59–105.PubMedCrossRef McLachlan SM, Rapoport B. Breaking tolerance to thyroid antigens: changing concepts in thyroid autoimmunity. Endocr Rev. 2014;35:59–105.PubMedCrossRef
54.
go back to reference Eshaghkhani Y, Sanati MH, Nakhjavani M, Safari R, Khajavi A, Ataei M, Jadali Z. Disturbed Th1 and Th2 balance in patients with graves’ disease. Minerva Endocrinol. 2016;41(1):28–36.PubMed Eshaghkhani Y, Sanati MH, Nakhjavani M, Safari R, Khajavi A, Ataei M, Jadali Z. Disturbed Th1 and Th2 balance in patients with graves’ disease. Minerva Endocrinol. 2016;41(1):28–36.PubMed
55.
go back to reference Zuniga LA, Jain R, Haines C, Cua DJ. Th17 cell development: from the cradle to the grave. Immunol Rev. 2013;252:78–88.PubMedCrossRef Zuniga LA, Jain R, Haines C, Cua DJ. Th17 cell development: from the cradle to the grave. Immunol Rev. 2013;252:78–88.PubMedCrossRef
56.
go back to reference Aggarwal S, Ghilardi N, Xie MH, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct Cd4 Tcell activation state characterized by the production of interleukin-17. J Biol Chem. 2003;278:1910–4.PubMedCrossRef Aggarwal S, Ghilardi N, Xie MH, de Sauvage FJ, Gurney AL. Interleukin-23 promotes a distinct Cd4 Tcell activation state characterized by the production of interleukin-17. J Biol Chem. 2003;278:1910–4.PubMedCrossRef
57.
go back to reference Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6:1133–41.PubMedPubMedCentralCrossRef Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6:1133–41.PubMedPubMedCentralCrossRef
58.
go back to reference Weaver CT, Hatton RD, Mangan PR, et al. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol. 2007;25:821–52.PubMedCrossRef Weaver CT, Hatton RD, Mangan PR, et al. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol. 2007;25:821–52.PubMedCrossRef
59.
go back to reference Liu Y, Tang X, Tian J, Zhu C, Peng H, Rui K, Wang Y, Mao C, Ma J, Lu L, Xu H, Wang S. Th17/Treg cells imbalance and GITRL profile in patients with Hashimoto’s thyroiditis. Int J Mol Sci. 2014;15:21674–86.PubMedPubMedCentralCrossRef Liu Y, Tang X, Tian J, Zhu C, Peng H, Rui K, Wang Y, Mao C, Ma J, Lu L, Xu H, Wang S. Th17/Treg cells imbalance and GITRL profile in patients with Hashimoto’s thyroiditis. Int J Mol Sci. 2014;15:21674–86.PubMedPubMedCentralCrossRef
60.
go back to reference Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Thl7 cells. Annu Rev Immunol. 2009;27:485–517.PubMedCrossRef Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Thl7 cells. Annu Rev Immunol. 2009;27:485–517.PubMedCrossRef
61.
go back to reference Crome SQ, Wang AY, Kang CY, Levings MK. The role of retinoic acid-related orphan receptor variant 2 and IL-17 in the development and function of human CD4+ T cells. Eur J Immunol. 2009;39:1480–93.PubMedCrossRef Crome SQ, Wang AY, Kang CY, Levings MK. The role of retinoic acid-related orphan receptor variant 2 and IL-17 in the development and function of human CD4+ T cells. Eur J Immunol. 2009;39:1480–93.PubMedCrossRef
62.
63.
go back to reference Gonzalez-Amaro R, Marazuela M. T regulatory (Treg) and T helper 17 (Th17) lymphocytes in thyroid autoimmunity. Endocrine. 2016;52:30–8.PubMedCrossRef Gonzalez-Amaro R, Marazuela M. T regulatory (Treg) and T helper 17 (Th17) lymphocytes in thyroid autoimmunity. Endocrine. 2016;52:30–8.PubMedCrossRef
64.
go back to reference Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol. 2007;8:950–7.PubMedCrossRef Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol. 2007;8:950–7.PubMedCrossRef
66.
go back to reference Figueroa-Vega N, Alfonso-Perez M, Benedicto I, Sanchez-Madrid F, Gonzalez-Amaro R, Marazuela M. Increased circulating pro-inflammatory cytokines and Th17 lymphocytes in Hashimoto’s thyroiditis. J Clin Endocrinol Metab. 2010;95:953–62.PubMedCrossRef Figueroa-Vega N, Alfonso-Perez M, Benedicto I, Sanchez-Madrid F, Gonzalez-Amaro R, Marazuela M. Increased circulating pro-inflammatory cytokines and Th17 lymphocytes in Hashimoto’s thyroiditis. J Clin Endocrinol Metab. 2010;95:953–62.PubMedCrossRef
67.
go back to reference Ruggeri RM, Minciullo P, Saitta S, Giovinazzo S, Certo R, Campenni A, Trimarchi F, Gangemi S, Benvenga S. Serum interleukin-22 (IL-22) is increased in the early stage of. Hashimoto’s thyroiditis compared to non-autoimmune thyroid disease and healthy controls. Hormones (Athens). 2014;13(3):338–44. https://doi.org/10.14310/horm.2002.1483. Ruggeri RM, Minciullo P, Saitta S, Giovinazzo S, Certo R, Campenni A, Trimarchi F, Gangemi S, Benvenga S. Serum interleukin-22 (IL-22) is increased in the early stage of. Hashimoto’s thyroiditis compared to non-autoimmune thyroid disease and healthy controls. Hormones (Athens). 2014;13(3):338–44. https://​doi.​org/​10.​14310/​horm.​2002.​1483.
68.
go back to reference Song RH, Yu ZY, Qin Q, Wang X, Muhali FS, Shi LF, Jiang WJ, Xiao L, Li DF, Zhang JA. Different levels of circulating Th22 cell and its related molecules in graves’ disease and Hashimoto’s thyroiditis. Int J Clin Exp Pathol. 2014;7(7):4024–31.PubMedPubMedCentral Song RH, Yu ZY, Qin Q, Wang X, Muhali FS, Shi LF, Jiang WJ, Xiao L, Li DF, Zhang JA. Different levels of circulating Th22 cell and its related molecules in graves’ disease and Hashimoto’s thyroiditis. Int J Clin Exp Pathol. 2014;7(7):4024–31.PubMedPubMedCentral
69.
go back to reference Guan LJ, Wang X, Meng S, Shi LF, Jiang WJ, Xiao L, Shi XH, Xu J, Zhang JA. Increased IL-21/IL-21R expression and its proinflammatory effects in autoimmune thyroid disease. Cytokine. 2015;72:160–5.PubMedCrossRef Guan LJ, Wang X, Meng S, Shi LF, Jiang WJ, Xiao L, Shi XH, Xu J, Zhang JA. Increased IL-21/IL-21R expression and its proinflammatory effects in autoimmune thyroid disease. Cytokine. 2015;72:160–5.PubMedCrossRef
70.
go back to reference Ghoreschi K, Laurence A, Yang XP, Tato CM, McGeachy MJ, Konkel JE, et al. Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature. 2010;467:967–71.PubMedPubMedCentralCrossRef Ghoreschi K, Laurence A, Yang XP, Tato CM, McGeachy MJ, Konkel JE, et al. Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature. 2010;467:967–71.PubMedPubMedCentralCrossRef
71.
go back to reference Song X, Gao H, Qian Y. Th17 differentiation and their pro-inflammation function. Adv Exp Med Biol. 2014;841:99–151.PubMedCrossRef Song X, Gao H, Qian Y. Th17 differentiation and their pro-inflammation function. Adv Exp Med Biol. 2014;841:99–151.PubMedCrossRef
72.
go back to reference Basdeo SA, Moran B, Cluxton D, Canavan M, McCormick J, Connolly M, Orr C, Mills KH, Veale DJ, Fearon U, Fletcher JM. Polyfunctional, pathogenic CD161+ Th17. Lineage cells are resistant to regulatory T cell-mediated suppression in the context of autoimmunity. J Immunol. 2015;195:528–40.PubMedCrossRef Basdeo SA, Moran B, Cluxton D, Canavan M, McCormick J, Connolly M, Orr C, Mills KH, Veale DJ, Fearon U, Fletcher JM. Polyfunctional, pathogenic CD161+ Th17. Lineage cells are resistant to regulatory T cell-mediated suppression in the context of autoimmunity. J Immunol. 2015;195:528–40.PubMedCrossRef
74.
go back to reference Feng T, Cao AT, Weaver CT, Elson CO, Cong Y. Interleukin-12 converts Foxp3+regulatory T cells to interferon-gamma-producing Foxp3+ T cells that inhibit colitis. Gastroenterology. 2011;140:2031–43.PubMedPubMedCentralCrossRef Feng T, Cao AT, Weaver CT, Elson CO, Cong Y. Interleukin-12 converts Foxp3+regulatory T cells to interferon-gamma-producing Foxp3+ T cells that inhibit colitis. Gastroenterology. 2011;140:2031–43.PubMedPubMedCentralCrossRef
75.
go back to reference Wang S, Baidoo SE, Liu Y, Zhu C, Tian J, Ma J, Tong J, Chen J, Tang X, Xu H, Lu L. T cell-derived leptin contributes to increased frequency of T helper type 17 cells in female patients with Hashimoto’s thyroiditis. Clin Exp Immunol. 2013;171:63–8.PubMedCrossRef Wang S, Baidoo SE, Liu Y, Zhu C, Tian J, Ma J, Tong J, Chen J, Tang X, Xu H, Lu L. T cell-derived leptin contributes to increased frequency of T helper type 17 cells in female patients with Hashimoto’s thyroiditis. Clin Exp Immunol. 2013;171:63–8.PubMedCrossRef
76.
go back to reference Leskela S, Serrano A, de la Fuente H, Rodriguez-Munoz A, Ramos-Levi A, Sampedro-Nunez M, Sanchez-Madrid F, Gonzalez-Amaro R, Marazuela M. Graves’ disease is associated with a defective expression of the immune regulatory molecule galectin-9 in antigen-presenting dendritic cells. PLoS ONE. 2015; https://doi.org/10.1371/journal.pone.0123938. Leskela S, Serrano A, de la Fuente H, Rodriguez-Munoz A, Ramos-Levi A, Sampedro-Nunez M, Sanchez-Madrid F, Gonzalez-Amaro R, Marazuela M. Graves’ disease is associated with a defective expression of the immune regulatory molecule galectin-9 in antigen-presenting dendritic cells. PLoS ONE. 2015; https://​doi.​org/​10.​1371/​journal.​pone.​0123938.
77.
go back to reference Qin Q, Liu P, Liu L, Wang R, Yan N, Yang J, Wang X, Pandey M, Zhang JA. The increased but non-predominant expression of Th17- and Th1-specific cytokines in Hashimoto’s thyroiditis but not in graves’ disease. Braz J Med Biol Res. 2012;45:1202–8.PubMedPubMedCentralCrossRef Qin Q, Liu P, Liu L, Wang R, Yan N, Yang J, Wang X, Pandey M, Zhang JA. The increased but non-predominant expression of Th17- and Th1-specific cytokines in Hashimoto’s thyroiditis but not in graves’ disease. Braz J Med Biol Res. 2012;45:1202–8.PubMedPubMedCentralCrossRef
78.
go back to reference Dieckmann D, Plottner H, Berchtold S, Berger T, Schuler G. Ex vivo isolation and characterization of CD4+ CD25+ T cells with regulatory properties from human blood. J Exp Med. 2001;193:1303–10.PubMedPubMedCentralCrossRef Dieckmann D, Plottner H, Berchtold S, Berger T, Schuler G. Ex vivo isolation and characterization of CD4+ CD25+ T cells with regulatory properties from human blood. J Exp Med. 2001;193:1303–10.PubMedPubMedCentralCrossRef
79.
go back to reference Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006;441:235–8.PubMedCrossRef Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006;441:235–8.PubMedCrossRef
80.
go back to reference Kristensen B, Hegedus L, Madsen HO, et al. Altered balance between self- reactive T helper (Th)17 cells and Th10 cells and between full-length forkhead box protein 3 (FoxP3) and FoxP3 splice variants in Hashimoto’s thyroiditis. Clin Exp Immunol. 2015;180:58–69.PubMedPubMedCentralCrossRef Kristensen B, Hegedus L, Madsen HO, et al. Altered balance between self- reactive T helper (Th)17 cells and Th10 cells and between full-length forkhead box protein 3 (FoxP3) and FoxP3 splice variants in Hashimoto’s thyroiditis. Clin Exp Immunol. 2015;180:58–69.PubMedPubMedCentralCrossRef
81.
go back to reference Li D, Cai W, Gu R, Zhang Y, Zhang H, Tang K, Xu P, Katirai F, Shi W, Wang L, Huang T, Huang B. Th17 cell plays a role in the pathogenesis of Hashimoto’s thyroiditis in patients. Clin Immunol. 2013;149:411–20.PubMedCrossRef Li D, Cai W, Gu R, Zhang Y, Zhang H, Tang K, Xu P, Katirai F, Shi W, Wang L, Huang T, Huang B. Th17 cell plays a role in the pathogenesis of Hashimoto’s thyroiditis in patients. Clin Immunol. 2013;149:411–20.PubMedCrossRef
83.
go back to reference Zheng L, Ye P, Liu C. The role of the IL-23/IL-17 axis in the pathogenesis of graves’ disease. Endocr J. 2013;60:591–7.PubMedCrossRef Zheng L, Ye P, Liu C. The role of the IL-23/IL-17 axis in the pathogenesis of graves’ disease. Endocr J. 2013;60:591–7.PubMedCrossRef
84.
go back to reference Gershon RK, Kondo K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology. 1970;18:723–37.PubMedPubMedCentral Gershon RK, Kondo K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology. 1970;18:723–37.PubMedPubMedCentral
85.
86.
88.
go back to reference Akdis M, Akdis AC. Immune tolerance. In: Adkinson Jr BSB, Busse BW, Holgate WW, Lemanske Jr ST, O Hehir RE, editors. Middleton’s allergy: principle and practice. Philaadelphia: Elsevier Saunders Press; 2014. p. 45–64. Akdis M, Akdis AC. Immune tolerance. In: Adkinson Jr BSB, Busse BW, Holgate WW, Lemanske Jr ST, O Hehir RE, editors. Middleton’s allergy: principle and practice. Philaadelphia: Elsevier Saunders Press; 2014. p. 45–64.
89.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
90.
go back to reference Klarquist J, Denman CJ, Hernandez C, Wainwright DA, Strickland FM, Overbeck A, et al. Reduced skin homing by functional Treg in vitiligo. Pigment Cell Melanoma Res. 2010;23:276–86.PubMedPubMedCentralCrossRef Klarquist J, Denman CJ, Hernandez C, Wainwright DA, Strickland FM, Overbeck A, et al. Reduced skin homing by functional Treg in vitiligo. Pigment Cell Melanoma Res. 2010;23:276–86.PubMedPubMedCentralCrossRef
91.
go back to reference Dwivedi M, Kumar P, Laddha NC, Kemp EH. Induction of regulatory T cells: a role for probiotics and prebiotics to suppress autoimmunity. Autoimmun Rev. 2016;15:379–92.PubMedCrossRef Dwivedi M, Kumar P, Laddha NC, Kemp EH. Induction of regulatory T cells: a role for probiotics and prebiotics to suppress autoimmunity. Autoimmun Rev. 2016;15:379–92.PubMedCrossRef
93.
go back to reference Sakaguchi S, Wing K, Yamaguchi T. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol. 2009;39:2331–6.PubMedCrossRef Sakaguchi S, Wing K, Yamaguchi T. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol. 2009;39:2331–6.PubMedCrossRef
94.
go back to reference Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875–86.PubMedPubMedCentralCrossRef Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875–86.PubMedPubMedCentralCrossRef
95.
go back to reference Kanamori M, Nakatsukasa H, Okada M, Lu Q, Yoshimura A. Induced regulatory T cells: their development, stability, and applications. Trends Immunol. 2016;37:803–11.PubMedCrossRef Kanamori M, Nakatsukasa H, Okada M, Lu Q, Yoshimura A. Induced regulatory T cells: their development, stability, and applications. Trends Immunol. 2016;37:803–11.PubMedCrossRef
96.
go back to reference Marazuela M, Garcıa-Lopez MA, Figueroa-Vega N, de la Fuente H, Alvarado-Sanchez B, Monsivais-Urenda A, Sanchez-Madrid FR, González-Amaro R. Regulatory T cells in human autoimmune thyroid disease. J Clin Endocrinol Metab. 2006;91:3639–46.PubMedCrossRef Marazuela M, Garcıa-Lopez MA, Figueroa-Vega N, de la Fuente H, Alvarado-Sanchez B, Monsivais-Urenda A, Sanchez-Madrid FR, González-Amaro R. Regulatory T cells in human autoimmune thyroid disease. J Clin Endocrinol Metab. 2006;91:3639–46.PubMedCrossRef
97.
go back to reference Roncarolo MG, Gregori S, Bacchetta R, Battaglia M. Tr1 cells and the counter- regulation of immunity: natural mechanisms and therapeutic applications. Curr Top Microbiol Immunol. 2014;380:39–68.PubMed Roncarolo MG, Gregori S, Bacchetta R, Battaglia M. Tr1 cells and the counter- regulation of immunity: natural mechanisms and therapeutic applications. Curr Top Microbiol Immunol. 2014;380:39–68.PubMed
98.
99.
go back to reference Nakahara M, Nagayama Y, Ichikawa T, Yu L, Eisenbarth GS, Abiru N. The effect of regulatory T-cell depletion on the spectrum of organ-specific autoimmune diseases in nonobese diabetic mice at different ages. Autoimmunity. 2011;44:504–10.PubMedCrossRef Nakahara M, Nagayama Y, Ichikawa T, Yu L, Eisenbarth GS, Abiru N. The effect of regulatory T-cell depletion on the spectrum of organ-specific autoimmune diseases in nonobese diabetic mice at different ages. Autoimmunity. 2011;44:504–10.PubMedCrossRef
100.
go back to reference Verginis P, Li HS, Carayanniotis G. Tolerogenic semimature dendritic cells suppress experimental autoimmune thyroiditis by activation of thyroglobulin- specific CD4+CD25+ T cells. J Immunol. 2005;174:7433–9.PubMedCrossRef Verginis P, Li HS, Carayanniotis G. Tolerogenic semimature dendritic cells suppress experimental autoimmune thyroiditis by activation of thyroglobulin- specific CD4+CD25+ T cells. J Immunol. 2005;174:7433–9.PubMedCrossRef
101.
go back to reference Mao C, Wang S, Xiao Y, Xu J, Jiang Q, Jin M, Jiang X, Guo H, Ning G, Zhang Y. Impairment of regulatory capacity of CD4+CD25+ regulatory T cells mediated by dendritic cell polarization and hyperthyroidism in graves’ disease. J Immunol. 2011;186:4734–43.PubMedCrossRef Mao C, Wang S, Xiao Y, Xu J, Jiang Q, Jin M, Jiang X, Guo H, Ning G, Zhang Y. Impairment of regulatory capacity of CD4+CD25+ regulatory T cells mediated by dendritic cell polarization and hyperthyroidism in graves’ disease. J Immunol. 2011;186:4734–43.PubMedCrossRef
102.
go back to reference Kasprowicz DJ, Smallwood PS, Tyznik AJ, Ziegler SF. Scurfin (FoxP3) controls T-dependent immune responses in vivo through regulation of CD4+ T cell effector function. J Immunol. 2003;171:1216–23.PubMedCrossRef Kasprowicz DJ, Smallwood PS, Tyznik AJ, Ziegler SF. Scurfin (FoxP3) controls T-dependent immune responses in vivo through regulation of CD4+ T cell effector function. J Immunol. 2003;171:1216–23.PubMedCrossRef
103.
go back to reference Gambineri E, Torgerson TR, Ochs HD. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol. 2003;15:430–5.PubMedCrossRef Gambineri E, Torgerson TR, Ochs HD. Immune dysregulation, polyendocrinopathy, enteropathy, and X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol. 2003;15:430–5.PubMedCrossRef
104.
go back to reference Munoz-Rodríguez A, Vitales-Noyola M, Ramos-Levi A, Serrano-Somavilla A, González-Amaro R, Marazuela M. Levels of regulatory T cells CD69+NKG2D+ IL-10+ are increased in patients with autoimmune thyroid disorders. Endocrine. 2016;51:478–89.CrossRef Munoz-Rodríguez A, Vitales-Noyola M, Ramos-Levi A, Serrano-Somavilla A, González-Amaro R, Marazuela M. Levels of regulatory T cells CD69+NKG2D+ IL-10+ are increased in patients with autoimmune thyroid disorders. Endocrine. 2016;51:478–89.CrossRef
105.
go back to reference Pan D, Shin YH, Gopalakrishnan G, Hennessey J, De Groot LJ. Regulatory T cells in graves’ disease. Clin Endocrinol. 2009;71:587–93.CrossRef Pan D, Shin YH, Gopalakrishnan G, Hennessey J, De Groot LJ. Regulatory T cells in graves’ disease. Clin Endocrinol. 2009;71:587–93.CrossRef
106.
go back to reference Bossowski A, Moniuszko M, Dabrowska M, Sawicka B, Rusak M, Jeznach M, Wójtowicz J, Bodzenta-Lukaszyk A, Bossowska A. Lower proportions of CD4+ CD25(high) and CD4+FoxP3, but not CD4+CD25+CD127(low) FoxP3+ T cell levels in children with autoimmune thyroid diseases. Autoimmunity. 2013;46:222–30.PubMedCrossRef Bossowski A, Moniuszko M, Dabrowska M, Sawicka B, Rusak M, Jeznach M, Wójtowicz J, Bodzenta-Lukaszyk A, Bossowska A. Lower proportions of CD4+ CD25(high) and CD4+FoxP3, but not CD4+CD25+CD127(low) FoxP3+ T cell levels in children with autoimmune thyroid diseases. Autoimmunity. 2013;46:222–30.PubMedCrossRef
107.
go back to reference Miyara M, Ito Y, Sakaguchi S. TREG-cell therapies for autoimmune rheumatic diseases. Nat Rev Rheumatol. 2014;10:543–51.PubMedCrossRef Miyara M, Ito Y, Sakaguchi S. TREG-cell therapies for autoimmune rheumatic diseases. Nat Rev Rheumatol. 2014;10:543–51.PubMedCrossRef
109.
go back to reference Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol. 2009;21:274–80.PubMedCrossRef Lee YK, Mukasa R, Hatton RD, Weaver CT. Developmental plasticity of Th17 and Treg cells. Curr Opin Immunol. 2009;21:274–80.PubMedCrossRef
110.
go back to reference Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, Hafler DA. IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood. 2009;113:4240–9.PubMedPubMedCentralCrossRef Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, Baecher-Allan C, Hafler DA. IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood. 2009;113:4240–9.PubMedPubMedCentralCrossRef
111.
go back to reference Bossowski A, Moniuszko M, Idźkowska E, Grubczak K, Singh P, Bossowska A, Diana T, Kahaly GJ. Decreased proportions of CD4 + IL17+/CD4 + CD25 + CD127- and CD4 + IL17+/CD4 + CD25 + CD127 - FoxP3+ T cells in children with autoimmune thyroid diseases (.). Autoimmunity. 2016;49(5):320–8. doi:https://doi.org/10.1080/08916934.2016.1183654. Bossowski A, Moniuszko M, Idźkowska E, Grubczak K, Singh P, Bossowska A, Diana T, Kahaly GJ. Decreased proportions of CD4 + IL17+/CD4 + CD25 + CD127- and CD4 + IL17+/CD4 + CD25 + CD127 - FoxP3+ T cells in children with autoimmune thyroid diseases (.). Autoimmunity. 2016;49(5):320–8. doi:https://​doi.​org/​10.​1080/​08916934.​2016.​1183654.
112.
113.
go back to reference Allan SE, Passerini L, Bacchetta R, Crellin N, Dai M, Orban PC, Ziegler SF, Roncarolo MG, Levings MK. The role of 2 FOXP3 isoforms in the generation of human CD4+ Tregs. J Clin Invest. 2005;115:3276–84.PubMedPubMedCentralCrossRef Allan SE, Passerini L, Bacchetta R, Crellin N, Dai M, Orban PC, Ziegler SF, Roncarolo MG, Levings MK. The role of 2 FOXP3 isoforms in the generation of human CD4+ Tregs. J Clin Invest. 2005;115:3276–84.PubMedPubMedCentralCrossRef
114.
go back to reference Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol. 2007;8:191–7.PubMedCrossRef Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol. 2007;8:191–7.PubMedCrossRef
115.
go back to reference Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for scurfin in CD4þCD25þ T regulatory cells. Nat Immunol. 2003;4:337–42.PubMedCrossRef Khattri R, Cox T, Yasayko SA, Ramsdell F. An essential role for scurfin in CD4þCD25þ T regulatory cells. Nat Immunol. 2003;4:337–42.PubMedCrossRef
116.
go back to reference Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330–6.PubMedCrossRef Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330–6.PubMedCrossRef
117.
go back to reference Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor FOXP3+. Science. 2003;299:1057–61.PubMedCrossRef Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor FOXP3+. Science. 2003;299:1057–61.PubMedCrossRef
118.
go back to reference Wildin RS, Ramsdell F, Peake J, Faravelli F, Casanova JL, Buist N, Levy-Lahad E, Mazzella M, Goulet O, Perroni L, et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet. 2001;27:18–20.PubMedCrossRef Wildin RS, Ramsdell F, Peake J, Faravelli F, Casanova JL, Buist N, Levy-Lahad E, Mazzella M, Goulet O, Perroni L, et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet. 2001;27:18–20.PubMedCrossRef
119.
go back to reference Chatila TA, Blaeser F, Ho N, Lederman HM, Voulgaropoulos C, Helms C, Bowcock AM. JM2, encoding a fork head-related protein, is mutated in X-linked autoimmunity-allergic disregulation syndrome. J Clin Invest. 2000;106:75–81.CrossRef Chatila TA, Blaeser F, Ho N, Lederman HM, Voulgaropoulos C, Helms C, Bowcock AM. JM2, encoding a fork head-related protein, is mutated in X-linked autoimmunity-allergic disregulation syndrome. J Clin Invest. 2000;106:75–81.CrossRef
120.
go back to reference Wildin RS, Freitas A. IPEX and FOXP3: clinical and research perspectives. J Autoimmun. 2005;25:56–62.PubMedCrossRef Wildin RS, Freitas A. IPEX and FOXP3: clinical and research perspectives. J Autoimmun. 2005;25:56–62.PubMedCrossRef
121.
go back to reference Ban Y, Tozaki T, Tobe T, Ban Y, Jacobson EM, Concepcion ES, Tomer Y. The regulatory T cell gene FOXP3 and genetic susceptibility to thyroid autoimmunity: an association analysis in Caucasian and Japanese cohorts. J Autoimmun. 2007;28:201–7.PubMedCrossRef Ban Y, Tozaki T, Tobe T, Ban Y, Jacobson EM, Concepcion ES, Tomer Y. The regulatory T cell gene FOXP3 and genetic susceptibility to thyroid autoimmunity: an association analysis in Caucasian and Japanese cohorts. J Autoimmun. 2007;28:201–7.PubMedCrossRef
122.
go back to reference Inoue N, Watanabe M, Morita M, Tomizawa R, Akamizu T, Tatsumi K, et al. Association of functional polymorphisms related to the transcriptional level of FOXP3 with prognosis of autoimmune thyroid diseases. Clin Exp Immunol. 2010;162:402–6.PubMedPubMedCentralCrossRef Inoue N, Watanabe M, Morita M, Tomizawa R, Akamizu T, Tatsumi K, et al. Association of functional polymorphisms related to the transcriptional level of FOXP3 with prognosis of autoimmune thyroid diseases. Clin Exp Immunol. 2010;162:402–6.PubMedPubMedCentralCrossRef
124.
go back to reference Sakaguchi S, Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T. Regulatory T cells: how do they suppress immune responses? Int Immunol. 2009;21:1105–11.PubMedCrossRef Sakaguchi S, Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T. Regulatory T cells: how do they suppress immune responses? Int Immunol. 2009;21:1105–11.PubMedCrossRef
125.
go back to reference Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, Falorni A, et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol. 2002;3:1097–101.PubMedCrossRef Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, Falorni A, et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol. 2002;3:1097–101.PubMedCrossRef
126.
go back to reference Suri-Payer E, Cantor H. Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4+CD25+ T cells. J Autoimmun. 2001;16:115–23.PubMedCrossRef Suri-Payer E, Cantor H. Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4+CD25+ T cells. J Autoimmun. 2001;16:115–23.PubMedCrossRef
127.
go back to reference Maloy KJ, Powrie JF. Regulatory T cells in the control of immune pathology. Nat Immunol. 2001;2:816–22.PubMedCrossRef Maloy KJ, Powrie JF. Regulatory T cells in the control of immune pathology. Nat Immunol. 2001;2:816–22.PubMedCrossRef
128.
go back to reference Marek-Trzonkowska N, Myśliwiec M, Dobyszuk A, Grabowska M, Derkowska I, Juścińska J, Owczuk R, Szadkowska A, Witkowski P, Młynarski W, Jarosz-Chobot P, Bossowski A, Siebert J, Trzonkowski P. Therapy of type 1 diabetes with CD4(+)CD25(high)CD127-regulatory T cells prolongs survival of pancreatic islets - results of one year follow-up. Clin Immunol. 2014;153(1):23–30. https://doi.org/10.1016/j.clim.2014.03.016. Marek-Trzonkowska N, Myśliwiec M, Dobyszuk A, Grabowska M, Derkowska I, Juścińska J, Owczuk R, Szadkowska A, Witkowski P, Młynarski W, Jarosz-Chobot P, Bossowski A, Siebert J, Trzonkowski P. Therapy of type 1 diabetes with CD4(+)CD25(high)CD127-regulatory T cells prolongs survival of pancreatic islets - results of one year follow-up. Clin Immunol. 2014;153(1):23–30. https://​doi.​org/​10.​1016/​j.​clim.​2014.​03.​016.
129.
go back to reference Taams LS, Vukmanovic-Stejic M, Smith J, Dunne PJ, Fletcher JM, Plunkett FJ, Ebeling SB, Lombardi G, Rustin MH, Bijlsma JW, et al. Antigen-specific T cell suppression by human CD4+CD25* regulatory T cells. Eur J Immunol. 2002;32:1621–30.PubMedCrossRef Taams LS, Vukmanovic-Stejic M, Smith J, Dunne PJ, Fletcher JM, Plunkett FJ, Ebeling SB, Lombardi G, Rustin MH, Bijlsma JW, et al. Antigen-specific T cell suppression by human CD4+CD25* regulatory T cells. Eur J Immunol. 2002;32:1621–30.PubMedCrossRef
130.
go back to reference Suri-Payer E, Amar AZ, Thornton AM, Shevach EM. CD4+CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J Immunol. 1998;160(3):1212–8.PubMed Suri-Payer E, Amar AZ, Thornton AM, Shevach EM. CD4+CD25+ T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J Immunol. 1998;160(3):1212–8.PubMed
131.
go back to reference Levings MK, Sangregorio R, Roncarolo MG. Human cd25(+)cd4(+) t regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J Exp Med. 2001;193:1295–302.PubMedPubMedCentralCrossRef Levings MK, Sangregorio R, Roncarolo MG. Human cd25(+)cd4(+) t regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J Exp Med. 2001;193:1295–302.PubMedPubMedCentralCrossRef
132.
go back to reference Kotsa K, Watson PF, Weetman AP. A CTLA-4 gene polymorphism is associated with both graves disease and autoimmune hypothyroidism. Clin Endocrinol. 1997;46:551–4.CrossRef Kotsa K, Watson PF, Weetman AP. A CTLA-4 gene polymorphism is associated with both graves disease and autoimmune hypothyroidism. Clin Endocrinol. 1997;46:551–4.CrossRef
134.
go back to reference Yanagawa T, Taniyama M, Enomoto S, Gomi K, Maruyama H, Ban Y, et al. CTLA4 gene polymorphism confers susceptibility to graves’ disease in Japanese. Thyroid. 1997;7:843–6.PubMedCrossRef Yanagawa T, Taniyama M, Enomoto S, Gomi K, Maruyama H, Ban Y, et al. CTLA4 gene polymorphism confers susceptibility to graves’ disease in Japanese. Thyroid. 1997;7:843–6.PubMedCrossRef
135.
go back to reference Villanueva RB, Inzerillo AM, Tomer Y, Barbesino G, Meltzer M, Concepcion ES, et al. Limited genetic susceptibility to severe graves’ ophthalmopathy: no role for ctla-4 and evidence for an environmental etiology. Thyroid. 2000;10:791–8.PubMedCrossRef Villanueva RB, Inzerillo AM, Tomer Y, Barbesino G, Meltzer M, Concepcion ES, et al. Limited genetic susceptibility to severe graves’ ophthalmopathy: no role for ctla-4 and evidence for an environmental etiology. Thyroid. 2000;10:791–8.PubMedCrossRef
136.
go back to reference Koenecke C, Czeloth N, Bubke A, Schmitz S, Kissenpfennig A, Malissen B, et al. Alloantigenspecific de novo-induced Foxp3+ Treg revert in vivo and do not protect from experimental GVHD. Eur J Immunol. 2009;39:3091–6.PubMedCrossRef Koenecke C, Czeloth N, Bubke A, Schmitz S, Kissenpfennig A, Malissen B, et al. Alloantigenspecific de novo-induced Foxp3+ Treg revert in vivo and do not protect from experimental GVHD. Eur J Immunol. 2009;39:3091–6.PubMedCrossRef
139.
go back to reference Kambayashi T, Laufer TM. Atypical MHC class II-expressing antigen-presenting cells: can anything replace a dendritic cell? Nat Rev Immunol. 2014;14:719–30.PubMedCrossRef Kambayashi T, Laufer TM. Atypical MHC class II-expressing antigen-presenting cells: can anything replace a dendritic cell? Nat Rev Immunol. 2014;14:719–30.PubMedCrossRef
140.
go back to reference Kristensen B. Regulatory B and T cell responses in patients with autoimmune thyroid disease and healthy controls. Dan Med J. 2016;63(2):B5177.PubMed Kristensen B. Regulatory B and T cell responses in patients with autoimmune thyroid disease and healthy controls. Dan Med J. 2016;63(2):B5177.PubMed
141.
142.
go back to reference Kuklina EM, Smirnova EN, Nekrasova IV, Balashova TS. Role of B cells in presentation of autoantigens to CD4(+) T cells in patients with autoimmune thyroiditis. Dokl Biol Sci. 2015;464:263–6.PubMedCrossRef Kuklina EM, Smirnova EN, Nekrasova IV, Balashova TS. Role of B cells in presentation of autoantigens to CD4(+) T cells in patients with autoimmune thyroiditis. Dokl Biol Sci. 2015;464:263–6.PubMedCrossRef
143.
go back to reference Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42:607–12.PubMedCrossRef Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42:607–12.PubMedCrossRef
144.
go back to reference Hong SH, Braley-Mullen H. Follicular B cells in thyroids of mice with spontaneous autoimmune thyroiditis contribute to disease pathogenesis and are targets of anti-CD20 antibody therapy. J Immunol. 2014;192:897–905.PubMedCrossRef Hong SH, Braley-Mullen H. Follicular B cells in thyroids of mice with spontaneous autoimmune thyroiditis contribute to disease pathogenesis and are targets of anti-CD20 antibody therapy. J Immunol. 2014;192:897–905.PubMedCrossRef
145.
go back to reference Salvi M. Immunotherapy for graves’ ophthalmopathy. Curr Opin Endocrinol Diabetes Obes. 2014;21:409–14.PubMedCrossRef Salvi M. Immunotherapy for graves’ ophthalmopathy. Curr Opin Endocrinol Diabetes Obes. 2014;21:409–14.PubMedCrossRef
146.
go back to reference Maravillas-Montero JL, Acevedo-Ochoa E. Human B regulatory cells: the new players in autoimmune disease. Rev Investig Clin. 2017;69:243–6. Maravillas-Montero JL, Acevedo-Ochoa E. Human B regulatory cells: the new players in autoimmune disease. Rev Investig Clin. 2017;69:243–6.
147.
go back to reference Miyagaki T, Fujimoto M, Sato S. Regulatory B cells in human inflammatory and autoimmune diseases: from mouse models to clinical research. Int Immunol. 2015;27:495–504.PubMedCrossRef Miyagaki T, Fujimoto M, Sato S. Regulatory B cells in human inflammatory and autoimmune diseases: from mouse models to clinical research. Int Immunol. 2015;27:495–504.PubMedCrossRef
148.
go back to reference Ray A, Dittel BN. Mechanisms of regulatory B cell function in autoimmune and inflammatory diseases beyond IL-10. J Clin Med. 2017;6:12.PubMedCentralCrossRef Ray A, Dittel BN. Mechanisms of regulatory B cell function in autoimmune and inflammatory diseases beyond IL-10. J Clin Med. 2017;6:12.PubMedCentralCrossRef
149.
go back to reference Bossowski A, Grubczak K, Singh P, Radzikowska U, Dabrowska M, Sawicka B, Bossowska A, Moniuszko M. Analysis of B regulatory cells with phenotype CD19+CD24hiCD27+IL-10+ and CD19+IL-10+ in the peripheral blood of children with graves’ disease and Hashimoto’s thyroiditis. Pediatr Endocrinol. 2015;14(Suppl 1):40. https://doi.org/10.18544/EP-02.14.01.1552. Bossowski A, Grubczak K, Singh P, Radzikowska U, Dabrowska M, Sawicka B, Bossowska A, Moniuszko M. Analysis of B regulatory cells with phenotype CD19+CD24hiCD27+IL-10+ and CD19+IL-10+ in the peripheral blood of children with graves’ disease and Hashimoto’s thyroiditis. Pediatr Endocrinol. 2015;14(Suppl 1):40. https://​doi.​org/​10.​18544/​EP-02.​14.​01.​1552.
Metadata
Title
Role of the T and B lymphocytes in pathogenesis of autoimmune thyroid diseases
Authors
Marta Rydzewska
Michał Jaromin
Izabela Elżbieta Pasierowska
Karlina Stożek
Artur Bossowski
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Thyroid Research / Issue 1/2018
Electronic ISSN: 1756-6614
DOI
https://doi.org/10.1186/s13044-018-0046-9

Other articles of this Issue 1/2018

Thyroid Research 1/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.