Altered Phenotypes of Colonic and Peripheral Blood Follicular Helper and Follicular Cytotoxic T Cells in Mice with DSS-Induced Colitis

References

• Ungaro R, Colombel JF, Lissoos T, Peyrin-Biroulet L. A treat-to-target update in ulcerative colitis: a systematic review. Am J Gastroenterol. 2019;114(6):874–883. doi:10.14309/ajg.0000000000000183
   PubMed Web of Science ®Google Scholar
• Coward S, Clement F, Benchimol EI, et al. Past and future burden of inflammatory bowel diseases based on modeling of population-based data. Gastroenterology. 2019;156(5):1345–1353.e4. doi:10.1053/j.gastro.2019.01.002
   PubMed Web of Science ®Google Scholar
• Herszényi L, Barabás L, Miheller P, Tulassay Z. Colorectal cancer in patients with inflammatory bowel disease: the true impact of the risk. Digest Dis. 2015;33(1):52–57. doi:10.1159/000368447
   PubMed Web of Science ®Google Scholar
• Lee H, Schneider Y, Lichtenstein GR. Going third class: treatment of steroid-dependent ulcerative colitis. Dig Dis Sci. 2019;64(5):1138–1141. doi:10.1007/s10620-019-05610-w
   PubMed Web of Science ®Google Scholar
• Ebert EC, Geng X, Bajpai M, Pan Z, Tatar E, Das KM. Antibody to tropomyosin isoform 5 and complement induce the lysis of colonocytes in ulcerative colitis. Am J Gastroenterol. 2009;104(12):2996–3003. doi:10.1038/ajg.2009.455
   PubMed Web of Science ®Google Scholar
• Uo M, Hisamatsu T, Miyoshi J, et al. Mucosal CXCR4+ IgG plasma cells contribute to the pathogenesis of human ulcerative colitis through FcγR-mediated CD14 macrophage activation. Gut. 2013;62(12):1734–1744. doi:10.1136/gutjnl-2012-303063
   PubMed Web of Science ®Google Scholar
• Pararasa C, Zhang N, Tull TJ, et al. Reduced CD27(-)IgD(-) B cells in blood and raised CD27(-)IgD(-) B cells in gut-associated lymphoid tissue in inflammatory bowel disease. Front Immunol. 2019;10:361. doi:10.3389/fimmu.2019.00361
   PubMed Web of Science ®Google Scholar
• Onuma EK, Amenta PS, Ramaswamy K, Lin JJ, Das KM. Autoimmunity in ulcerative colitis (UC): a predominant colonic mucosal B cell response against human tropomyosin isoform 5. Clin Exp Immunol. 2000;121(3):466–471. doi:10.1046/j.1365-2249.2000.01330.x
   PubMed Web of Science ®Google Scholar
• Halstensen TS, Das KM, Brandtzaeg P. Epithelial deposits of immunoglobulin G1 and activated complement colocalise with the M(r) 40 kD putative autoantigen in ulcerative colitis. Gut. 1993;34(5):650–657. doi:10.1136/gut.34.5.650
   PubMed Web of Science ®Google Scholar
• Hibi T, Aiso S, Ishikawa M, et al. Circulating antibodies to the surface antigens on colon epithelial cells in ulcerative colitis. Clin Exp Immunol. 1983;54(1):163–168.
   PubMed Web of Science ®Google Scholar
• Jinno Y, Ohtani H, Nakamura S, et al. Infiltration of CD19+ plasma cells with frequent labeling of Ki-67 in corticosteroid-resistant active ulcerative colitis. Virchows Archiv. 2006;448(4):412–421. doi:10.1007/s00428-005-0136-7
   PubMed Web of Science ®Google Scholar
• Wang X, Jiang Y, Zhu Y, et al. Circulating memory B cells and plasmablasts are associated with the levels of serum immunoglobulin in patients with ulcerative colitis. J Cell Mol Med. 2016;20(5):804–814. doi:10.1111/jcmm.12728
   PubMed Web of Science ®Google Scholar
• Long Y, Xia C, Xu L, et al. The imbalance of circulating follicular helper T cells and follicular regulatory T cells is associated with disease activity in patients with ulcerative colitis. Front Immunol. 2020;11:104. doi:10.3389/fimmu.2020.00104
   PubMed Web of Science ®Google Scholar
• Bsat M, Chapuy L, Rubio M, et al. Differential pathogenic Th17 profile in mesenteric lymph nodes of crohn’s disease and ulcerative colitis patients. Front Immunol. 2019;10:1177. doi:10.3389/fimmu.2019.01177
   PubMed Web of Science ®Google Scholar
• Xue G, Zhong Y, Hua L, et al. Aberrant alteration of follicular T helper cells in ulcerative colitis patients and its correlations with interleukin-21 and B cell subsets. Medicine. 2019;98(10):e14757. doi:10.1097/md.0000000000014757
   PubMed Web of Science ®Google Scholar
• Kräutler NJ, Suan D, Butt D, et al. Differentiation of germinal center B cells into plasma cells is initiated by high-affinity antigen and completed by Tfh cells. J Exp Med. 2017;214(5):1259–1267. doi:10.1084/jem.20161533
   PubMed Web of Science ®Google Scholar
• Stebegg M, Kumar SD, Silva-Cayetano A, Fonseca VR, Linterman MA, Graca L. Regulation of the germinal center response. Front Immunol. 2018;9:2469. doi:10.3389/fimmu.2018.02469
   PubMed Web of Science ®Google Scholar
• Vinuesa CG, Linterman MA, Yu D, MacLennan IC. Follicular Helper T Cells. Annu Rev Immunol. 2016;34:335–368. doi:10.1146/annurev-immunol-041015-055605
   PubMed Web of Science ®Google Scholar
• Xie MM, Dent AL. Unexpected help: follicular regulatory T cells in the germinal center. Front Immunol. 2018;9:1536. doi:10.3389/fimmu.2018.01536
   PubMed Web of Science ®Google Scholar
• Liu C, Wang D, Song Y, Lu S, Zhao J, Wang H. Increased circulating CD4(+)CXCR5(+)FoxP3(+) follicular regulatory T cells correlated with severity of systemic lupus erythematosus patients. Int Immunopharmacol. 2018;56:261–268. doi:10.1016/j.intimp.2018.01.038
   PubMed Web of Science ®Google Scholar
• Liu C, Wang D, Lu S, et al. Increased circulating follicular treg cells are associated with lower levels of autoantibodies in patients with rheumatoid arthritis in stable remission. Arthritis Rheumatol. 2018;70(5):711–721. doi:10.1002/art.40430
   PubMed Web of Science ®Google Scholar
• Zhang H, Hu Q, Zhang M, et al. Bach2 deficiency leads to spontaneous expansion of IL-4-producing T follicular helper cells and autoimmunity. Front Immunol. 2019;10:2050. doi:10.3389/fimmu.2019.02050
   PubMed Web of Science ®Google Scholar
• Xu Y, Xu H, Zhen Y, et al. Imbalance of circulatory T follicular helper and T follicular regulatory cells in patients with ANCA-associated vasculitis. Mediators Inflamm. 2019;2019:8421479. doi:10.1155/2019/8421479
   PubMed Web of Science ®Google Scholar
• Leong YA, Chen Y, Ong HS, et al. CXCR5(+) follicular cytotoxic T cells control viral infection in B cell follicles. Nat Immunol. 2016;17(10):1187–1196. doi:10.1038/ni.3543
   PubMed Web of Science ®Google Scholar
• Oehen S, Brduscha-Riem K. Differentiation of naive CTL to effector and memory CTL: correlation of effector function with phenotype and cell division. J Immunol. 1998;161(10):5338–5346. doi:10.4049/jimmunol.161.10.5338
   PubMed Web of Science ®Google Scholar
• Tsai LM, Yu D. Follicular helper T-cell memory: establishing new frontiers during antibody response. Immunol Cell Biol. 2014;92(1):57–63. doi:10.1038/icb.2013.68
   PubMed Web of Science ®Google Scholar
• Fazilleau N, Eisenbraun MD, Malherbe L, et al. Lymphoid reservoirs of antigen-specific memory T helper cells. Nat Immunol. 2007;8(7):753–761. doi:10.1038/ni1472
   PubMed Web of Science ®Google Scholar
• Takatori H, Kawashima H, Matsuki A, et al. Helios enhances treg cell function in cooperation with FoxP3. Arthritis Rheumatol. 2015;67(6):1491–1502. doi:10.1002/art.39091
   PubMed Web of Science ®Google Scholar
• Kim HJ, Barnitz RA, Kreslavsky T, et al. Stable inhibitory activity of regulatory T cells requires the transcription factor Helios. Science. 2015;350(6258):334–339. doi:10.1126/science.aad0616
   PubMed Web of Science ®Google Scholar
• Sebastian M, Lopez-Ocasio M, Metidji A, Rieder SA, Shevach EM, Thornton AM. Helios controls a limited subset of regulatory T cell functions. J Immunol. 2016;196(1):144–155. doi:10.4049/jimmunol.1501704
   PubMed Web of Science ®Google Scholar
• Sage PT, Paterson AM, Lovitch SB, Sharpe AH. The coinhibitory receptor CTLA-4 controls B cell responses by modulating T follicular helper, T follicular regulatory, and T regulatory cells. Immunity. 2014;41(6):1026–1039. doi:10.1016/j.immuni.2014.12.005
   PubMed Web of Science ®Google Scholar
• Fuhrman CA, Yeh WI, Seay HR, et al. Divergent phenotypes of human regulatory T cells expressing the receptors TIGIT and CD226. J Immunol. 2015;195(1):145–155. doi:10.4049/jimmunol.1402381
   PubMed Web of Science ®Google Scholar
• Lozano E, Dominguez-Villar M, Kuchroo V, Hafler DA. The TIGIT/CD226 axis regulates human T cell function. J Immunol. 2012;188(8):3869–3875. doi:10.4049/jimmunol.1103627
   PubMed Web of Science ®Google Scholar
• Kurtulus S, Sakuishi K, Ngiow SF, et al. TIGIT predominantly regulates the immune response via regulatory T cells. J Clin Invest. 2015;125(11):4053–4062. doi:10.1172/jci81187
   PubMed Web of Science ®Google Scholar
• Shibuya A, Campbell D, Hannum C, et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity. 1996;4(6):573–581. doi:10.1016/s1074-7613(00)70060-4
   PubMed Web of Science ®Google Scholar
• Qiu ZX, Zhang K, Qiu XS, Zhou M, Li WM. CD226 Gly307Ser association with multiple autoimmune diseases: a meta-analysis. Hum Immunol. 2013;74(2):249–255. doi:10.1016/j.humimm.2012.10.009
   PubMed Web of Science ®Google Scholar
• Bottino C, Castriconi R, Pende D, et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med. 2003;198(4):557–567. doi:10.1084/jem.20030788
   PubMed Web of Science ®Google Scholar
• Yusuf I, Kageyama R, Monticelli L, et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J Immunol. 2010;185(1):190–202. doi:10.4049/jimmunol.0903505
   PubMed Web of Science ®Google Scholar
• Dorfman DM, Brown JA, Shahsafaei A, Freeman GJ. Programmed death-1 (PD-1) is a marker of germinal center-associated T cells and angioimmunoblastic T-cell lymphoma. Am J Surg Pathol. 2006;30(7):802–810. doi:10.1097/01.pas.0000209855.28282.ce
   PubMed Web of Science ®Google Scholar
• Good-Jacobson KL, Szumilas CG, Chen L, Sharpe AH, Tomayko MM, Shlomchik MJ. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat Immunol. 2010;11(6):535–542. doi:10.1038/ni.1877
   PubMed Web of Science ®Google Scholar
• Gigoux M, Lovato A, Leconte J, Leung J, Sonenberg N, Suh WK. Inducible costimulator facilitates T-dependent B cell activation by augmenting IL-4 translation. Mol Immunol. 2014;59(1):46–54. doi:10.1016/j.molimm.2014.01.008
   PubMed Web of Science ®Google Scholar
• Warnatz K, Bossaller L, Salzer U, et al. Human ICOS deficiency abrogates the germinal center reaction and provides a monogenic model for common variable immunodeficiency. Blood. 2006;107(8):3045–3052. doi:10.1182/blood-2005-07-2955
   PubMed Web of Science ®Google Scholar
• Kassiotis G, O’Garra A. Establishing the follicular helper identity. Immunity. 2009;31(3):450–452. doi:10.1016/j.immuni.2009.08.017
   PubMed Web of Science ®Google Scholar
• Chung Y, Tanaka S, Chu F, et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat Med. 2011;17(8):983–988. doi:10.1038/nm.2426
   PubMed Web of Science ®Google Scholar
• Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr Protocols Immunol. 2014;104:15.25.1–15.25.14. doi:10.1002/0471142735.im1525s104
   PubMedGoogle Scholar
• Couto M, Cates C. Laboratory guidelines for animal care. Methods Mol Biol. 2019;1920:407–430. doi:10.1007/978-1-4939-9009-2_25
   PubMedGoogle Scholar
• Zhang R, Qi CF, Hu Y, et al. T follicular helper cells restricted by IRF8 contribute to T cell-mediated inflammation. J Autoimmun. 2019;96:113–122. doi:10.1016/j.jaut.2018.09.001
   PubMed Web of Science ®Google Scholar
• Schaerli P, Willimann K, Lang AB, Lipp M, Loetscher P, Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J Exp Med. 2000;192(11):1553–1562. doi:10.1084/jem.192.11.1553
   PubMed Web of Science ®Google Scholar
• Valentine KM, Davini D, Lawrence TJ, et al. CD8 follicular T cells promote B cell antibody class switch in autoimmune disease. J Immunol. 2018;201(1):31–40. doi:10.4049/jimmunol.1701079
   PubMed Web of Science ®Google Scholar
• Godefroy E, Zhong H, Pham P, Friedman D, Yazdanbakhsh K. TIGIT-positive circulating follicular helper T cells display robust B-cell help functions: potential role in sickle cell alloimmunization. Haematologica. 2015;100(11):1415–1425. doi:10.3324/haematol.2015.132738
   PubMed Web of Science ®Google Scholar
• Joller N, Lozano E, Burkett PR, et al. Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity. 2014;40(4):569–581. doi:10.1016/j.immuni.2014.02.012
   PubMed Web of Science ®Google Scholar
• Yasutomi M, Christiaansen AF, Imai N, et al. CD226 and TIGIT cooperate in the differentiation and maturation of human Tfh cells. Front Immunol. 2022;13:840457. doi:10.3389/fimmu.2022.840457
   PubMed Web of Science ®Google Scholar
• Wang N, Liang S, Jin J, et al. CD226 attenuates Treg suppressive capacity via CTLA-4 and TIGIT during EAE. Immunol Res. 2019;67(6):486–496. doi:10.1007/s12026-019-09112-9
   PubMed Web of Science ®Google Scholar
• Liu C, Xu L, Xia C, et al. Increased proportion of functional subpopulations in circulating regulatory T cells in patients with chronic hepatitis B. Hepatol Res. 2020;50(4):439–452. doi:10.1111/hepr.13472
   PubMed Web of Science ®Google Scholar
• Long Y, Feng J, Ma Y, et al. Altered follicular regulatory T (Tfr)- and helper T (Tfh)-cell subsets are associated with autoantibody levels in microscopic polyangiitis patients. Eur J Immunol. 2021;51(7):1809–1823. doi:10.1002/eji.202049093
   PubMed Web of Science ®Google Scholar
• Long Y, Li W, Feng J, et al. Follicular helper and follicular regulatory T cell subset imbalance is associated with higher activated B cells and abnormal autoantibody production in primary anti-phospholipid syndrome patients. Clin Exp Immunol. 2021;206(2):141–152. doi:10.1111/cei.13647
   PubMed Web of Science ®Google Scholar
• Zeng X, Lu S, Li M, et al. Inflammatory cytokine-neutralizing antibody treatment prevented increases in follicular helper T cells and follicular regulatory T cells in a mouse model of arthritis. J Inflamm Res. 2022;15:3997–4011. doi:10.2147/jir.S355720
   PubMed Web of Science ®Google Scholar
• Yang Y, Lv X, Zhan L, et al. Case report: IL-21 and Bcl-6 regulate the proliferation and secretion of Tfh and Tfr cells in the intestinal germinal center of patients with inflammatory bowel disease. Front Pharmacol. 2020;11:587445. doi:10.3389/fphar.2020.587445
   PubMed Web of Science ®Google Scholar