Inflammatory Cytokine-Neutralizing Antibody Treatment Prevented Increases in Follicular Helper T Cells and Follicular Regulatory T Cells in a Mouse Model of Arthritis

References

• McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med. 2011;365(23):2205–2219. doi:10.1056/NEJMra1004965
   PubMed Web of Science ®Google Scholar
• Conigliaro P, Chimenti MS, Triggianese P, et al. Autoantibodies in inflammatory arthritis. Autoimmun Rev. 2016;15(7):673–683. doi:10.1016/j.autrev.2016.03.003
   PubMed Web of Science ®Google Scholar
• Li ZG. A new look at rheumatology in China–opportunities and challenges. Nat Rev Rheumatol. 2015;11(5):313–317. doi:10.1038/nrrheum.2014.218
   PubMed Web of Science ®Google Scholar
• Wang J, Shan Y, Jiang Z, et al. High frequencies of activated B cells and T follicular helper cells are correlated with disease activity in patients with new-onset rheumatoid arthritis. Clin Exp Immunol. 2013;174(2):212–220. doi:10.1111/cei.12162
   PubMed Web of Science ®Google Scholar
• Niu Q, Cai B, Huang ZC, Shi YY, Wang LL. Disturbed Th17/Treg balance in patients with rheumatoid arthritis. Rheumatol Int. 2012;32(9):2731–2736. doi:10.1007/s00296-011-1984-x
   PubMed Web of Science ®Google Scholar
• Wang W, Shao S, Jiao Z, et al. The Th17/Treg imbalance and cytokine environment in peripheral blood of patients with rheumatoid arthritis. Rheumatol Int. 2012;32(4):887–893. doi:10.1007/s00296-010-1710-0
   PubMed Web of Science ®Google Scholar
• Samson M, Audia S, Janikashvili N, et al. Brief report: inhibition of interleukin-6 function corrects Th17/Treg cell imbalance in patients with rheumatoid arthritis. Arthritis Rheum. 2012;64(8):2499–2503. doi:10.1002/art.34477
   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
• Lüthje K, Kallies A, Shimohakamada Y, et al. The development and fate of follicular helper T cells defined by an IL-21 reporter mouse. Nat Immunol. 2012;13(5):491–498. doi:10.1038/ni.2261
   PubMed Web of Science ®Google Scholar
• Shulman Z, Gitlin AD, Targ S, et al. T follicular helper cell dynamics in germinal centers. Science. 2013;341(6146):673–677. doi:10.1126/science.1241680
   PubMed Web of Science ®Google Scholar
• Szabo K, Papp G, Barath S, et al. Follicular helper T cells may play an important role in the severity of primary Sjögren’s syndrome. Clin Immunol. 2013;147(2):95–104. doi:10.1016/j.clim.2013.02.024
   PubMed Web of Science ®Google Scholar
• Morita R, Schmitt N, Bentebibel SE, et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity. 2011;34(1):108–121. doi:10.1016/j.immuni.2010.12.012
   PubMed Web of Science ®Google Scholar
• He J, Tsai LM, Leong YA, et al. Circulating precursor CCR7(lo)PD-1(hi) CXCR5+ CD4+ T cells indicate Tfh cell activity and promote antibody responses upon antigen reexposure. Immunity. 2013;39(4):770–781. doi:10.1016/j.immuni.2013.09.007
   PubMed Web of Science ®Google Scholar
• Ma J, Zhu C, Ma B, et al. Increased frequency of circulating follicular helper T cells in patients with rheumatoid arthritis. Clin Dev Immunol. 2012;2012:827480. doi:10.1155/2012/827480
   PubMedGoogle Scholar
• Rasmussen TK, Andersen T, Hvid M, et al. Increased interleukin 21 (IL-21) and IL-23 are associated with increased disease activity and with radiographic status in patients with early rheumatoid arthritis. J Rheumatol. 2010;37(10):2014–2020. doi:10.3899/jrheum.100259
   PubMed Web of Science ®Google Scholar
• Sage PT, Francisco LM, Carman CV, Sharpe AH. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat Immunol. 2013;14(2):152–161. doi:10.1038/ni.2496
   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
• Fu W, Liu X, Lin X, et al. Deficiency in T follicular regulatory cells promotes autoimmunity. J Exp Med. 2018;215(3):815–825. doi:10.1084/jem.20170901
   PubMed Web of Science ®Google Scholar
• Shan Y, Qi C, Zhao J, et al. Higher frequency of peripheral blood follicular regulatory T cells in patients with new onset ankylosing spondylitis. Clin Exp Pharmacol Physiol. 2015;42(2):154–161. doi:10.1111/1440-1681.12330
   PubMed Web of Science ®Google Scholar
• Liu C, Wang D, Song Y, et al. 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
• 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
• 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
• 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
• Good-Jacobson KL, Szumilas CG, Chen L, et al. 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, et al. 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
• Brand DD, Latham KA, Rosloniec EF. Collagen-induced arthritis. Nat Protoc. 2007;2(5):1269–1275. doi:10.1038/nprot.2007.173
   PubMed Web of Science ®Google Scholar
• Haleagrahara N, Miranda-Hernandez S, Alim MA, et al. Therapeutic effect of quercetin in collagen-induced arthritis. Biomed Pharmacother. 2017;90:38–46. doi:10.1016/j.biopha.2017.03.026
   PubMed Web of Science ®Google Scholar
• Croft M, Benedict CA, Ware CF. Clinical targeting of the TNF and TNFR superfamilies. Nat Rev Drug Discov. 2013;12(2):147–168. doi:10.1038/nrd3930
   PubMed Web of Science ®Google Scholar
• Strand V, Kimberly R, Isaacs JD. Biologic therapies in rheumatology: lessons learned, future directions. Nat Rev Drug Discov. 2007;6(1):75–92. doi:10.1038/nrd2196
   PubMed Web of Science ®Google Scholar
• Dinarello CA, Simon A, van der Meer JW. Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov. 2012;11(8):633–652. doi:10.1038/nrd3800
   PubMed Web of Science ®Google Scholar
• Alten R, Gomez-Reino J, Durez P, et al. Efficacy and safety of the human anti-IL-1β monoclonal antibody canakinumab in rheumatoid arthritis: results of a 12-week, Phase II, dose-finding study. BMC Musculoskelet Disord. 2011;12:153. doi:10.1186/1471-2474-12-153
   PubMed Web of Science ®Google Scholar
• Joosten LA, Helsen MM, van de Loo FA, van den Berg WB. Anticytokine treatment of established type II collagen-induced arthritis in DBA/1 mice: a comparative study using anti-TNFalpha, anti-IL-1alpha/beta and IL-1Ra. Arthritis Rheum. 2008;58(2Suppl):S110–122. doi:10.1002/art.23363
   PubMedGoogle Scholar
• Dekkers JS, Schoones JW, Huizinga TW, Toes RE, van der Helm-van Mil AH. Possibilities for preventive treatment in rheumatoid arthritis? Lessons from experimental animal models of arthritis: a systematic literature review and meta-analysis. Ann Rheum Dis. 2017;76(2):458–467. doi:10.1136/annrheumdis-2016-209830
   PubMed Web of Science ®Google Scholar
• Jacques C, Floris I, Lejeune B. Ultra-Low Dose Cytokines in Rheumatoid Arthritis, Three Birds with One Stone as the Rationale of the 2LARTH(®) Micro-Immunotherapy Treatment. Int J Mol Sci. 2021;22(13):548. doi:10.3390/ijms22136717
   PubMed Web of Science ®Google 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
• 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
• Wang X, Yang C, Xu F, et al. Imbalance of circulating Tfr/Tfh ratio in patients with rheumatoid arthritis. Clin Exp Med. 2019;19(1):55–64. doi:10.1007/s10238-018-0530-5
   PubMed Web of Science ®Google Scholar
• Cao G, Wang P, Cui Z, et al. An imbalance between blood CD4(+)CXCR5(+)Foxp3(+) Tfr cells and CD4(+)CXCR5(+)Tfh cells may contribute to the immunopathogenesis of rheumatoid arthritis. Mol Immunol. 2020;125:1–8. doi:10.1016/j.molimm.2020.06.003
   PubMed Web of Science ®Google Scholar
• Anderson AC, Joller N, Kuchroo VK. Lag-3, Tim-3, and TIGIT: co-inhibitory Receptors with Specialized Functions in Immune Regulation. Immunity. 2016;44(5):989–1004. doi:10.1016/j.immuni.2016.05.001
   PubMed Web of Science ®Google Scholar
• Hutloff A, Dittrich AM, Beier KC, et al. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature. 1999;397(6716):263–266. doi:10.1038/16717
   PubMed Web of Science ®Google Scholar
• Locci M, Havenar-Daughton C, Landais E, et al. Human circulating PD-1+CXCR3-CXCR5+ memory Tfh cells are highly functional and correlate with broadly neutralizing HIV antibody responses. Immunity. 2013;39(4):758–769. doi:10.1016/j.immuni.2013.08.031
   PubMed Web of Science ®Google Scholar
• Sefer AP, Charbonnier LM, Kasap N, et al. A Patient with Novel ICOS Mutation Presented with Progressive Loss of B Cells. J Clin Immunol. 2021;41(1):251–255. doi:10.1007/s10875-020-00889-1
   PubMed Web of Science ®Google Scholar
• Long Y, Zhao X, Liu C, Xia C, Liu C. Activated inducible co-stimulator-positive programmed cell death 1-positive follicular helper T cells indicate disease activity and severity in ulcerative colitis patients. Clin Exp Immunol. 2020;202(1):106–118. doi:10.1111/cei.13485
   PubMed Web of Science ®Google Scholar
• Danger R, Chesneau M, Delbos F, et al. CXCR5(+)PD1(+)ICOS(+) Circulating T Follicular Helpers Are Associated With de novo Donor-Specific Antibodies After Renal Transplantation. Front Immunol. 2019;10:2071. doi:10.3389/fimmu.2019.02071
   PubMed Web of Science ®Google Scholar
• Linterman MA, Beaton L, Yu D, et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J Exp Med. 2010;207(2):353–363. doi:10.1084/jem.20091738
   PubMed Web of Science ®Google Scholar
• Spolski R, Leonard WJ. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu Rev Immunol. 2008;26:57–79. doi:10.1146/annurev.immunol.26.021607.090316
   PubMed Web of Science ®Google Scholar
• Gharibi T, Majidi J, Kazemi T, et al. Biological effects of IL-21 on different immune cells and its role in autoimmune diseases. Immunobiology. 2016;221(2):357–367. doi:10.1016/j.imbio.2015.09.021
   PubMed Web of Science ®Google Scholar
• Laidlaw BJ, Lu Y, Amezquita RA, et al. Interleukin-10 from CD4(+) follicular regulatory T cells promotes the germinal center response. Sci Immunol. 2017;2(16):547. doi:10.1126/sciimmunol.aan4767
   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
• Williams RO, Marinova-Mutafchieva L, Feldmann M, Maini RN. Evaluation of TNF-alpha and IL-1 blockade in collagen-induced arthritis and comparison with combined anti-TNF-alpha/anti-CD4 therapy. J Immunol. 2000;165(12):7240–7245. doi:10.4049/jimmunol.165.12.7240
   PubMed Web of Science ®Google Scholar
• van den Berg WB, Joosten LA, Kollias G, van De Loo FA. Role of tumour necrosis factor alpha in experimental arthritis: separate activity of interleukin 1beta in chronicity and cartilage destruction. Ann Rheum Dis. 1999;58(Suppl1):I40–48. doi:10.1136/ard.58.2008.i40
   PubMedGoogle Scholar