Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
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.
ADVANCED SEARCH
Log in
Top
Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2021

Open Access 01-12-2021 | Systemic Sclerosis | Research

TFH cells in systemic sclerosis

Authors: Pauline Beurier, Laure Ricard, Deborah Eshagh, Florent Malard, Lama Siblany, Olivier Fain, Mohamad Mohty, Béatrice Gaugler, Arsène Mekinian

Published in: Journal of Translational Medicine | Issue 1/2021

Login to get access

Abstract

Systemic sclerosis is an autoimmune disease characterized by excessive dermal fibrosis with progression to internal organs, vascular impairment and immune dysregulation evidenced by the infiltration of inflammatory cells in affected tissues and the production of auto antibodies. While the pathogenesis remains unclear, several data highlight that T and B cells deregulation is implicated in the disease pathogenesis. Over the last decade, aberrant responses of circulating T follicular helper cells, a subset of CD4 T cells which are able to localise predominantly in the B cell follicles through a high level of chemokine receptor CXCR5 expression are described in pathogenesis of several autoimmune diseases and chronic graft-versus-host-disease. In the present review, we summarized the observed alteration of number and frequency of circulating T follicular helper cells in systemic sclerosis. We described their role in aberrant B cell activation and differentiation though interleukine-21 secretion. We also clarified T follicular helper-like cells involvement in fibrogenesis in both human and mouse model. Finally, because T follicular helper cells are involved in both fibrosis and autoimmune abnormalities in systemic sclerosis patients, we presented the different strategies could be used to target T follicular helper cells in systemic sclerosis, the therapeutic trials currently being carried out and the future perspectives from other auto-immune diseases and graft-versus-host-disease models.
Literature
1.
Dumoitier N, Lofek S, Mouthon L. Pathophysiology of systemic sclerosis: state of the art in 2014. Presse Medicale Paris. 2014;43(102):e267-278.CrossRef
2.
Cutolo M, Soldano S, Smith V. Pathophysiology of systemic sclerosis: current understanding and new insights. Expert Rev Clin Immunol. 2019;15(7):753–64.PubMedCrossRef
3.
Forestier A, Guerrier T, Jouvray M, Giovannelli J, Lefèvre G, Sobanski V, et al. Altered B lymphocyte homeostasis and functions in systemic sclerosis. Autoimmun Rev mars. 2018;17(3):244–55.CrossRef
4.
Gasparini G, Cozzani E, Parodi A. Interleukin-4 and interleukin-13 as possible therapeutic targets in systemic sclerosis. Cytokine. 2020;125:154799.PubMedCrossRef
5.
Postlethwaite AE, Holness MA, Katai H, Raghow R. Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J Clin Invest. 1992;90(4):1479–85.PubMedPubMedCentralCrossRef
6.
Liu M, Yang J, Xing X, Cui X, Li M. Interleukin-17A promotes functional activation of systemic sclerosis patient-derived dermal vascular smooth muscle cells by extracellular-regulated protein kinases signalling pathway. Arthritis Res Ther. 2014;16(6):4223.PubMedPubMedCentralCrossRef
7.
Xing X, Li A, Tan H, Zhou Y. IFN-γ+ IL-17+ Th17 cells regulate fibrosis through secreting IL-21 in systemic scleroderma. J Cell Mol Med. 2020;24(23):13600–8.PubMedPubMedCentralCrossRef
8.
Xing X, Yang J, Yang X, Wei Y, Zhu L, Gao D, et al. IL-17A induces endothelial inflammation in systemic sclerosis via the ERK signaling pathway. PLoS ONE. 2013;8(12):e85032.PubMedPubMedCentralCrossRef
9.
Liu T, Li S, Ying S, Tang S, Ding Y, Li Y, et al. The IL-23/IL-17 pathway in inflammatory skin diseases: from bench to bedside. Front Immunol. 2020;11:594735.PubMedPubMedCentralCrossRef
10.
Gensous N, Charrier M, Duluc D, Contin-Bordes C, Truchetet M-E, Lazaro E, et al. T follicular helper cells in autoimmune disorders. Front Immunol. 2018;9:1637.PubMedPubMedCentralCrossRef
11.
12.
Kurata I, Matsumoto I, Sumida T. T follicular helper cell subsets: a potential key player in autoimmunity. Immunol Med mars. 2021;44(1):1–9.CrossRef
13.
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):1553–62.PubMedPubMedCentralCrossRef
14.
Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M, et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med. 2000;192(11):1545–52.PubMedPubMedCentralCrossRef
15.
16.
17.
Yoshitomi H, Ueno H. Shared and distinct roles of T peripheral helper and T follicular helper cells in human diseases. Cell Mol Immunol. 2021;18(3):523–7.PubMedCrossRef
18.
Makiyama A, Chiba A, Noto D, Murayama G, Yamaji K, Tamura N, et al. Expanded circulating peripheral helper T cells in systemic lupus erythematosus: association with disease activity and B cell differentiation. Rheumatol Oxf Engl. 2019;58(10):1861–9.
19.
Flynn R, Du J, Veenstra RG, Reichenbach DK, Panoskaltsis-Mortari A, Taylor PA, et al. Increased T follicular helper cells and germinal center B cells are required for cGVHD and bronchiolitis obliterans. Blood. 2014;123(25):3988–98.PubMedPubMedCentralCrossRef
20.
Asai Y, Chiba H, Nishikiori H, Kamekura R, Yabe H, Kondo S, et al. Aberrant populations of circulating T follicular helper cells and regulatory B cells underlying idiopathic pulmonary fibrosis. Respir Res. 2019;20(1):244.PubMedPubMedCentralCrossRef
21.
Knorr DA, Wang H, Aurora M, MacMillan ML, Holtan SG, Bergerson R, et al. Loss of T follicular helper cells in the peripheral blood of patients with chronic graft-versus-host disease. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant. 2016;22(5):825–33.CrossRef
22.
Forcade E, Kim HT, Cutler C, Wang K, Alho AC, Nikiforow S, et al. Circulating T follicular helper cells with increased function during chronic graft-versus-host disease. Blood. 2016;127(20):2489–97.PubMedPubMedCentralCrossRef
23.
Jin H, Yang K, Zhang H, Chen Y, Qi H, Fan Z, et al. Expansion of circulating extrafollicular helper T-like cells in patients with chronic graft-versus-host disease. J Autoimmun juin. 2019;100:95–104.CrossRef
24.
Ricard L, Jachiet V, Malard F, Ye Y, Stocker N, Rivière S, et al. Circulating follicular helper T cells are increased in systemic sclerosis and promote plasmablast differentiation through the IL-21 pathway which can be inhibited by ruxolitinib. Ann Rheum Dis. 2019;78(4):539–50.CrossRefPubMed
25.
Ly NTM, Ueda-Hayakawa I, Nguyen CTH, Huynh TNM, Kishimoto I, Fujimoto M, et al. Imbalance toward TFH 1 cells playing a role in aberrant B cell differentiation in systemic sclerosis. Rheumatol Oxf Engl. 2021;60(3):1553–62.CrossRef
26.
Kubo S, Nakayamada S, Miyazaki Y, Yoshikawa M, Yoshinari H, Satoh Y, et al. Distinctive association of peripheral immune cell phenotypes with capillaroscopic microvascular patterns in systemic sclerosis. Rheumatol Oxf Engl. 2019;58(12):2273–83.CrossRef
27.
Sobanski V, Giovannelli J, Allanore Y, Riemekasten G, Airò P, Vettori S, et al. Phenotypes determined by cluster analysis and their survival in the prospective European scleroderma trials and research cohort of patients with systemic sclerosis. Arthritis Rheumatol Hoboken NJ. 2019;71(9):1553–70.CrossRef
28.
Sobanski V, Lescoat A, Launay D. Novel classifications for systemic sclerosis: challenging historical subsets to unlock new doors. Curr Opin Rheumatol. 2020;32(6):463–71.PubMedCrossRef
29.
Fox DA, Lundy SK, Whitfield ML, Berrocal V, Campbell P, Rasmussen S, et al. Lymphocyte subset abnormalities in early diffuse cutaneous systemic sclerosis. Arthritis Res Ther. 2021;23(1):10.PubMedPubMedCentralCrossRef
30.
Morita R, Schmitt N, Bentebibel S-E, Ranganathan R, Bourdery L, Zurawski G, 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):108–21.PubMedPubMedCentralCrossRef
31.
Chizzolini C, Brembilla NC, Montanari E, Truchetet M-E. Fibrosis and immune dysregulation in systemic sclerosis. Autoimmun Rev. 2011;10(5):276–81.PubMedCrossRef
32.
Le Coz C, Joublin A, Pasquali J-L, Korganow A-S, Dumortier H, Monneaux F. Circulating TFH subset distribution is strongly affected in lupus patients with an active disease. PLoS ONE. 2013;8(9):e75319.PubMedPubMedCentralCrossRef
33.
Arroyo-Villa I, Bautista-Caro M-B, Balsa A, Aguado-Acín P, Bonilla-Hernán M-G, Plasencia C, et al. Constitutively altered frequencies of circulating follicullar helper T cell counterparts and their subsets in rheumatoid arthritis. Arthritis Res Ther. 2014;16(6):500.PubMedPubMedCentralCrossRef
34.
Grados A, Ebbo M, Piperoglou C, Groh M, Regent A, Samson M, et al. T cell polarization toward TH2/TFH2 and TH17/TFH17 in patients with IgG4-related disease. Front Immunol. 2017;8:235.PubMedPubMedCentralCrossRef
35.
Ricard L, Malard F, Riviere S, Laurent C, Fain O, Mohty M, et al. Regulatory B cell imbalance correlates with Tfh expansion in systemic sclerosis. Clin Exp Rheumatol. 2021;131(4):20–4.CrossRef
36.
Huang E, Peng N, Xiao F, Hu D, Wang X, Lu L. The roles of immune cells in the pathogenesis of fibrosis. Int J Mol Sci. 2020;21(15):E5203.PubMedCrossRef
37.
Lei L, He Z-Y, Zhao C, Sun X-J, Zhong X-N. Elevated frequencies of CD4(+) IL-21(+) T, CD4(+) IL-21R(+) T and IL-21(+) Th17 cells, and increased levels of IL-21 in bleomycin-induced mice may be associated with dermal and pulmonary inflammation and fibrosis. Int J Rheum Dis avr. 2016;19(4):392–404.CrossRef
38.
Taylor DK, Mittereder N, Kuta E, Delaney T, Burwell T, Dacosta K, et al. T follicular helper-like cells contribute to skin fibrosis. Sci Transl Med. 2018;10(431):eaaf5307.PubMedCrossRef
39.
Maehara T, Kaneko N, Perugino CA, Mattoo H, Kers J, Allard-Chamard H, et al. Cytotoxic CD4+ T lymphocytes may induce endothelial cell apoptosis in systemic sclerosis. J Clin Invest. 2020;130(5):2451–64.PubMedPubMedCentralCrossRef
40.
Xing R, Jin Y, Sun L, Yang L, Li C, Li Z, et al. Interleukin-21 induces migration and invasion of fibroblast-like synoviocytes from patients with rheumatoid arthritis. Clin Exp Immunol. 2016;184(2):147–58.PubMedPubMedCentralCrossRef
41.
Monteleone G, Caruso R, Fina D, Peluso I, Gioia V, Stolfi C, et al. Control of matrix metalloproteinase production in human intestinal fibroblasts by interleukin 21. Gut. 2006;55(12):1774–80.PubMedPubMedCentralCrossRef
42.
Xing R, Yang L, Jin Y, Sun L, Li C, Li Z, et al. Interleukin-21 induces proliferation and proinflammatory cytokine profile of fibroblast-like synoviocytes of patients with rheumatoid arthritis. Scand J Immunol. 2016;83(1):64–71.PubMedCrossRef
43.
François A, Chatelus E, Wachsmann D, Sibilia J, Bahram S, Alsaleh G, et al. B lymphocytes and B-cell activating factor promote collagen and profibrotic markers expression by dermal fibroblasts in systemic sclerosis. Arthritis Res Ther. 2013;15(5):R168.PubMedPubMedCentralCrossRef
44.
Dumoitier N, Chaigne B, Régent A, Lofek S, Mhibik M, Dorfmüller P, et al. Scleroderma peripheral B lymphocytes secrete interleukin-6 and transforming growth factor β and activate fibroblasts. Arthritis Rheumatol. 2017;69(5):1078–89.PubMedCrossRef
45.
De Palma R, Del Galdo F, Lupoli S, Altucci P, Abbate G, Valentini G. Peripheral T lymphocytes from patients with early systemic sclerosis co-cultured with autologous fibroblasts undergo an oligoclonal expansion similar to that occurring in the skin. Clin Exp Immunol. 2006;144(1):169–76.PubMedPubMedCentralCrossRef
46.
Kitanaga Y, Imamura E, Nakahara Y, Fukahori H, Fujii Y, Kubo S, et al. In vitro pharmacological effects of peficitinib on lymphocyte activation: a potential treatment for systemic sclerosis with JAK inhibitors. Rheumatol Oxf Engl. 2020;59(8):1957–68.CrossRef
47.
Kane A, Deenick EK, Ma CS, Cook MC, Uzel G, Tangye SG. STAT3 is a central regulator of lymphocyte differentiation and function. Curr Opin Immunol. 2014;28:49–57.PubMedCrossRef
48.
Read KA, Powell MD, Baker CE, Sreekumar BK, Ringel-Scaia VM, Bachus H, et al. Integrated STAT3 and Ikaros zinc finger transcription factor activities regulate Bcl-6 expression in CD4+ Th Cells. J Immunol. 2017;199(7):2377–87.PubMedCrossRef
49.
Chen W, Nyuydzefe MS, Weiss JM, Zhang J, Waksal SD, Zanin-Zhorov A. ROCK2, but not ROCK1 interacts with phosphorylated STAT3 and co-occupies TH17/TFH gene promoters in TH17-activated human T cells. Sci Rep. 2018;8(1):16636.PubMedPubMedCentralCrossRef
50.
Weiss JM, Chen W, Nyuydzefe MS, Trzeciak A, Flynn R, Tonra JR, et al. ROCK2 signaling is required to induce a subset of T follicular helper cells through opposing effects on STATs in autoimmune settings. Sci Signal. 2016;9(437):ra73.PubMedPubMedCentralCrossRef
51.
Zanin-Zhorov A, Weiss JM, Nyuydzefe MS, Chen W, Scher JU, Mo R, et al. Selective oral ROCK2 inhibitor down-regulates IL-21 and IL-17 secretion in human T cells via STAT3-dependent mechanism. Proc Natl Acad Sci U S A. 2014;111(47):16814–9.PubMedPubMedCentralCrossRef
52.
Rozo C, Chinenov Y, Maharaj RK, Gupta S, Leuenberger L, Kirou KA, et al. Targeting the RhoA-ROCK pathway to reverse T-cell dysfunction in SLE. Ann Rheum Dis avr. 2017;76(4):740–7.CrossRef
53.
Flynn R, Paz K, Du J, Reichenbach DK, Taylor PA, Panoskaltsis-Mortari A, et al. Targeted Rho-associated kinase 2 inhibition suppresses murine and human chronic GVHD through a Stat3-dependent mechanism. Blood. 2016;127(17):2144–54.PubMedPubMedCentralCrossRef
54.
55.
56.
57.
Damsky W, Peterson D, Ramseier J, Al-Bawardy B, Chun H, Proctor D, et al. The emerging role of Janus kinase inhibitors in the treatment of autoimmune and inflammatory diseases. J Allergy Clin Immunol. 2021;147(3):814–26.PubMedCrossRef
58.
59.
60.
Komura K, Fujimoto M, Matsushita T, Yanaba K, Kodera M, Kawasuji A, et al. Increased serum soluble CD40 levels in patients with systemic sclerosis. J Rheumatol. 2007;34(2):353–8.PubMed
61.
Yanaba K, Asano Y, Noda S, Akamata K, Aozasa N, Taniguchi T, et al. Increased production of soluble inducible costimulator in patients with diffuse cutaneous systemic sclerosis. Arch Dermatol Res. 2013;305(1):17–23.PubMedCrossRef
62.
Visvanathan S, Daniluk S, Ptaszyński R, Müller-Ladner U, Ramanujam M, Rosenstock B, et al. Effects of BI 655064, an antagonistic anti-CD40 antibody, on clinical and biomarker variables in patients with active rheumatoid arthritis: a randomised, double-blind, placebo-controlled, phase IIa study. Ann Rheum Dis. 2019;78(6):754–60.PubMedCrossRef
63.
Ponsoye M, Frantz C, Ruzehaji N, Nicco C, Elhai M, Ruiz B, et al. Treatment with abatacept prevents experimental dermal fibrosis and induces regression of established inflammation-driven fibrosis. Ann Rheum Dis. 2016;75(12):2142–9.PubMedCrossRef
64.
Boleto G, Guignabert C, Pezet S, Cauvet A, Sadoine J, Tu L, et al. T-cell costimulation blockade is effective in experimental digestive and lung tissue fibrosis. Arthritis Res Ther. 2018;20(1):197.PubMedPubMedCentralCrossRef
65.
Glatigny S, Höllbacher B, Motley SJ, Tan C, Hundhausen C, Buckner JH, et al. Abatacept targets T follicular helper and regulatory T cells, disrupting molecular pathways that regulate their proliferation and maintenance. J Immunol. 2019;202(5):1373–82.PubMedCrossRef
66.
Chakravarty EF, Martyanov V, Fiorentino D, Wood TA, Haddon DJ, Jarrell JA, et al. Gene expression changes reflect clinical response in a placebo-controlled randomized trial of abatacept in patients with diffuse cutaneous systemic sclerosis. Arthritis Res Ther. 2015;17:159.PubMedPubMedCentralCrossRef
67.
Khanna D, Spino C, Johnson S, Chung L, Whitfield ML, Denton CP, et al. Abatacept in early diffuse cutaneous systemic sclerosis: results of a phase II investigator-initiated, multicenter, double-blind, randomized, placebo-controlled trial. Arthritis Rheumatol. 2020;72(1):125–36.PubMedCrossRef
68.
Dong L, He Y, Cao Y, Wang Y, Jia A, Wang Y, et al. Functional differentiation and regulation of follicular T helper cells in inflammation and autoimmunity. Immunology mai. 2021;163(1):19–32.CrossRef
69.
Malard F, Labopin M, Yakoub-Agha I, Chantepie S, Guillaume T, Blaise D, et al. Rituximab-based first-line treatment of cGVHD after allogeneic SCT: results of a phase 2 study. Blood. 2017;130(20):2186–95.PubMedCrossRef
70.
Audia S, Rossato M, Trad M, Samson M, Santegoets K, Gautheron A, et al. B cell depleting therapy regulates splenic and circulating T follicular helper cells in immune thrombocytopenia. J Autoimmun. 2017;77:89–95.PubMedCrossRef
71.
Antonopoulos I, Daoussis D, Lalioti M-E, Markatseli TE, Drosos AA, Taraviras S, et al. B cell depletion treatment decreases CD4+IL4+ and CD4+CD40L+ T cells in patients with systemic sclerosis. Rheumatol Int. 2019;39(11):1889–98.PubMedCrossRef
72.
Tang R, Yu J, Shi Y, Zou P, Zeng Z, Tang B, et al. Safety and efficacy of Rituximab in systemic sclerosis: a systematic review and meta-analysis. Int Immunopharmacol. 2020;83:106389.PubMedCrossRef
73.
Matsushita T, Hasegawa M, Yanaba K, Kodera M, Takehara K, Sato S. Elevated serum BAFF levels in patients with systemic sclerosis: enhanced BAFF signaling in systemic sclerosis B lymphocytes. Arthritis Rheum. 2006;54(1):192–201.PubMedCrossRef
74.
Matsushita T, Kobayashi T, Mizumaki K, Kano M, Sawada T, Tennichi M, et al. BAFF inhibition attenuates fibrosis in scleroderma by modulating the regulatory and effector B cell balance. Sci Adv. 2018;4(7):e9944.CrossRef
75.
76.
Paz K, Flynn R, Du J, Qi J, Luznik L, Maillard I, et al. Small-molecule BCL6 inhibitor effectively treats mice with nonsclerodermatous chronic graft-versus-host disease. Blood. 2019;133(1):94–9.PubMedPubMedCentralCrossRef
77.
Affandi AJ, Carvalheiro T, Radstake TRDJ, Marut W. Dendritic cells in systemic sclerosis: advances from human and mice studies. Immunol Lett. 2018;195:18–29.PubMedCrossRef
78.
Carvalheiro T, Zimmermann M, Radstake TRDJ, Marut W. Novel insights into dendritic cells in the pathogenesis of systemic sclerosis. Clin Exp Immunol. 2020;201(1):25–33.PubMedPubMedCentralCrossRef
79.
Krishnaswamy JK, Alsén S, Yrlid U, Eisenbarth SC, Williams A. Determination of T follicular helper cell fate by dendritic cells. Front Immunol. 2018;9:2169.PubMedPubMedCentralCrossRef
80.
81.
Globig A-M, Sommer NP, Wild K, Schardey J, Zoldan K, Thomann AK, et al. Ustekinumab inhibits T follicular helper cell differentiation in patients with Crohn’s disease. Cell Mol Gastroenterol Hepatol. 2021;11(1):1–12.PubMedCrossRef
82.
Wu R, Li N, Zhao X, Ding T, Xue H, Gao C, et al. Low-dose Interleukin-2: biology and therapeutic prospects in rheumatoid arthritis. Autoimmun Rev. 2020;19(10):102645.PubMedCrossRef
83.
He J, Zhang R, Shao M, Zhao X, Miao M, Chen J, et al. Efficacy and safety of low-dose IL-2 in the treatment of systemic lupus erythematosus: a randomised, double-blind, placebo-controlled trial. Ann Rheum Dis. 2020;79(1):141–9.PubMedCrossRef
84.
Whangbo JS, Kim HT, Mirkovic N, Leonard L, Poryanda S, Silverstein S, et al. Dose-escalated interleukin-2 therapy for refractory chronic graft-versus-host disease in adults and children. Blood Adv. 2019;3(17):2550–61.PubMedPubMedCentralCrossRef
85.
Ballesteros-Tato A, Papillion A. Mechanisms of action of low-dose IL-2 restoration therapies in SLE. Curr Opin Immunol déc. 2019;61:39–45.CrossRef
86.
He J, Zhang X, Wei Y, Sun X, Chen Y, Deng J, et al. Low-dose interleukin-2 treatment selectively modulates CD4(+) T cell subsets in patients with systemic lupus erythematosus. Nat Med sept. 2016;22(9):991–3.CrossRef
87.
Nurieva RI, Podd A, Chen Y, Alekseev AM, Yu M, Qi X, et al. STAT5 protein negatively regulates T follicular helper (Tfh) cell generation and function. J Biol Chem. 2012;287(14):11234–9.PubMedPubMedCentralCrossRef
88.
Jones DM, Read KA, Oestreich KJ. Dynamic roles for IL-2-STAT5 signaling in effector and regulatory CD4+ T cell populations. J Immunol. 2020;205(7):1721–30.PubMedCrossRef
89.
Hao H, Nakayamada S, Yamagata K, Ohkubo N, Iwata S, Inoue Y, et al. Conversion of T follicular helper cells to T follicular regulatory cells by interleukin-2 through transcriptional regulation in systemic lupus erythematosus. Arthritis Rheumatol. 2021;73(1):132–42.PubMedCrossRef
90.
91.
Reighard SD, Cranert SA, Rangel KM, Ali A, Gyurova IE, de la Cruz-Lynch AT, et al. Therapeutic targeting of follicular T cells with chimeric antigen receptor-expressing natural killer cells. Cell Rep Med. 2020;1(1):100003.PubMedPubMedCentralCrossRef
92.
Servaas NH, Zaaraoui-Boutahar F, Wichers CGK, Ottria A, Chouri E, Affandi AJ, et al. Longitudinal analysis of T-cell receptor repertoires reveals persistence of antigen-driven CD4+ and CD8+ T-cell clusters in systemic sclerosis. J Autoimmun. 2021;117:102574.PubMedCrossRef
Metadata
Title
TFH cells in systemic sclerosis
Authors
Pauline Beurier
Laure Ricard
Deborah Eshagh
Florent Malard
Lama Siblany
Olivier Fain
Mohamad Mohty
Béatrice Gaugler
Arsène Mekinian
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2021
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-021-03049-0

Other articles of this Issue 1/2021

Journal of Translational Medicine 1/2021 Go to the issue

Methodology

Qualitative and quantitative comparison of cell-free DNA and cell-free fetal DNA isolation by four (semi-)automated extraction methods: impact in two clinical applications: chimerism quantification and noninvasive prenatal diagnosis

Research

Immune landscape and prognostic immune-related genes in KRAS-mutant colorectal cancer patients

Correction

Correction to: Automatic identification of myopic maculopathy related imaging features in optic disc region via machine learning methods

Research

Cerebrospinal fluid cells immune landscape in multiple sclerosis

Research

What can the neurological manifestations of COVID-19 tell us: a meta-analysis

Research

Metabolic analysis of early nonalcoholic fatty liver disease in humans using liquid chromatography-mass spectrometry
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

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

Read more

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

Pediatric Cardiology Video

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

Cardiopulmonary Comorbidity Video

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

Valvular Heart Disease Video

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

Heart Failure Video

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

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

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

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits