B Cell-mediated Immune Regulation and the Quest for Transplantation Tolerance.
Journal
Transplantation
ISSN: 1534-6080
Titre abrégé: Transplantation
Pays: United States
ID NLM: 0132144
Informations de publication
Date de publication:
23 Feb 2024
23 Feb 2024
Historique:
medline:
23
2
2024
pubmed:
23
2
2024
entrez:
23
2
2024
Statut:
aheadofprint
Résumé
Pathophysiologic function of B cells in graft rejection has been well recognized in transplantation. B cells promote alloantigen-specific T-cell response and secrete antibodies that can cause antibody-mediated graft failures and rejections. Therefore, strategies targeting B cells, for example, B-cell depletion, have been used for the prevention of both acute and chronic rejections. Interestingly, however, recent mounting evidence indicates that subsets of B cells yet to be further identified can display potent immune regulatory functions, and they contribute to transplantation tolerance and operational tolerance in both experimental and clinical settings, respectively. In this review, we integrate currently available information on B-cell subsets, including T-cell Ig domain and mucin domain 1-positive transitional and T-cell immunoreceptor with Ig and immunoreceptor tyrosine-based inhibitory motif domain-positive memory B cells, displaying immune regulatory functions, with a focus on transplantation tolerance, by analyzing their mechanisms of action. In addition, we will discuss potential T-cell Ig domain and mucin domain 1-positive and T-cell immunoreceptor with Ig and immunoreceptor tyrosine-based inhibitory motif domain-positive B cell-based strategies for the enhancement of operational tolerance in transplantation patients.
Identifiants
pubmed: 38389135
doi: 10.1097/TP.0000000000004948
pii: 00007890-990000000-00669
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
The authors declare no conflicts of interests.
Références
Salisbury EM, Game DS, Lechler RI. Transplantation tolerance. Pediatr Nephrol. 2014;29:2263–2272.
Feng S, Ekong UD, Lobritto SJ, et al. Complete immunosuppression withdrawal and subsequent allograft function among pediatric recipients of parental living donor liver transplants. JAMA. 2012;307:283–293.
Levitsky J. Operational tolerance: past lessons and future prospects. Liver Transpl. 2011;17:222–232.
Brouard S, Dupont A, Giral M, et al. Operationally tolerant and minimally immunosuppressed kidney recipients display strongly altered blood T-cell clonal regulation. Am J Transplant. 2005;5:330–340.
Brouard S, Mansfield E, Braud C, et al. Identification of a peripheral blood transcriptional biomarker panel associated with operational renal allograft tolerance. Proc Natl Acad Sci U S A. 2007;104:15448–15453.
Christensen LL, Grunnet N, Rudiger N, et al. Indications of immunological tolerance in kidney transplantation. Tissue Antigens. 1998;51:637–644.
Owens ML, Maxwell JG, Goodnight J, et al. Discontinuance of immunosuppression in renal transplant patients. Arch Surg. 1975;110:1450–1451.
Roussey-Kesler G, Giral M, Moreau A, et al. Clinical operational tolerance after kidney transplantation. Am J Transplant. 2006;6:736–746.
Uehling DT, Hussey JL, Weinstein AB, et al. Cessation of immunosuppression after renal transplantation. Surgery. 1976;79:278–282.
Strober S, Benike C, Krishnaswamy S, et al. Clinical transplantation tolerance twelve years after prospective withdrawal of immunosuppressive drugs: studies of chimerism and anti-donor reactivity. Transplantation. 2000;69:1549–1554.
Ramos HC, Reyes J, Abu-Elmagd K, et al. Weaning of immunosuppression in long-term liver transplant recipients. Transplantation. 1995;59:212–217.
Takatsuki M, Uemoto S, Inomata Y, et al. Weaning of immunosuppression in living donor liver transplant recipients. Transplantation. 2001;72:449–454.
Louis S, Braudeau C, Giral M, et al. Contrasting CD25hiCD4+T cells/FOXP3 patterns in chronic rejection and operational drug-free tolerance. Transplantation. 2006;81:398–407.
Iwase H, Kobayashi T, Kodera Y, et al. Clinical significance of regulatory T-cell-related gene expression in peripheral blood after renal transplantation. Transplantation. 2011;91:191–198.
Bhorade SM, Chen H, Molinero L, et al. Decreased percentage of CD4+FoxP3+ cells in bronchoalveolar lavage from lung transplant recipients correlates with development of bronchiolitis obliterans syndrome. Transplantation. 2010;90:540–546.
Baan CC, Dijke IE, Weimar W. Regulatory T cells in alloreactivity after clinical heart transplantation. Curr Opin Organ Transplant. 2009;14:577–582.
Sagoo P, Perucha E, Sawitzki B, et al. Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J Clin Invest. 2010;120:1848–1861.
Newell KA, Asare A, Kirk AD, et al.; Immune Tolerance Network ST507 Study Group. Identification of a B cell signature associated with renal transplant tolerance in humans. J Clin Invest. 2010;120:1836–1847.
Pallier A, Hillion S, Danger R, et al. Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int. 2010;78:503–513.
Viklicky O, Krystufkova E, Brabcova I, et al. B-cell-related biomarkers of tolerance are up-regulated in rejection-free kidney transplant recipients. Transplantation. 2013;95:148–154.
Guinn MT, Szuter ES, Yokose T, et al. Intragraft B cell differentiation during the development of tolerance to kidney allografts is associated with a regulatory B cell signature revealed by single cell transcriptomics. Am J Transplant. 2023;23:1319–1330.
Martínez-Llordella M, Lozano JJ, Puig-Pey I, et al. Using transcriptional profiling to develop a diagnostic test of operational tolerance in liver transplant recipients. J Clin Invest. 2008;118:2845–2857.
Lozano JJ, Pallier A, Martinez-Llordella M, et al. Comparison of transcriptional and blood cell-phenotypic markers between operationally tolerant liver and kidney recipients. Am J Transplant. 2011;11:1916–1926.
Silva HM, Takenaka MC, Moraes-Vieira PM, et al. Preserving the B-cell compartment favors operational tolerance in human renal transplantation. Mol Med. 2012;18:733–743.
Ding Q, Yeung M, Camirand G, et al. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J Clin Invest. 2011;121:3645–3656.
Nouel A, Segalen I, Jamin C, et al. B cells display an abnormal distribution and an impaired suppressive function in patients with chronic antibody-mediated rejection. Kidney Int. 2014;85:590–599.
Chesneau M, Michel L, Dugast E, et al. Tolerant kidney transplant patients produce B cells with regulatory properties. J Am Soc Nephrol. 2015;26:2588–2598.
Lal G, Nakayama Y, Sethi A, et al. IL-10 from marginal zone precursor B cell subset is required for costimulatory blockade induced transplantation tolerance. Transplantation. 2015;99:1817–1828.
Mauri C, Gray D, Mushtaq N, et al. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med. 2003;197:489–501.
Blair PA, Noreña LY, Flores-Borja F, et al. CD19+ CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32:129–140.
Yoshizaki A, Miyagaki T, DiLillo DJ, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature. 2012;491:264–268.
Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10–competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117:530–541.
Carter NA, Rosser EC, Mauri C. Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther. 2012;14:R32.
Evans JG, Chavez-Rueda KA, Eddaoudi A, et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol. 2007;178:7868–7878.
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.
Cui D, Zhang L, Chen J, et al. Changes in regulatory B cells and their relationship with rheumatoid arthritis disease activity. Clin Exp Med. 2015;15:285–292.
Shen P, Roch T, Lampropoulou V, et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature. 2014;507:366–370.
Gong Y, Zhao C, Zhao P, et al. Role of IL-10-producing regulatory B cells in chronic hepatitis B virus infection. Dig Dis Sci. 2015;60:1308–1314.
Liu Y, Cheng LS, Wu SD, et al. IL-10-producing regulatory B-cells suppressed effector T-cells but enhanced regulatory T-cells in chronic HBV infection. Clin Sci (Lond). 2016;130:907–919.
Han X, Yang J, Zhang Y, et al. Potential role for regulatory B cells as a major source of interleukin-10 in spleen from Plasmodium chabaudi-infected mice. Infect Immun. 2018;86:e00016–e00018.
Liu Y, Chen Y, Li Z, et al. Role of IL-10-producing regulatory B cells in control of cerebral malaria in Plasmodium berghei infected mice. Eur J Immunol. 2013;43:2907–2918.
Das A, Ellis G, Pallant C, et al. IL-10-producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J Immunol. 2012;189:3925–3935.
Horikawa M, Minard-Colin V, Matsushita T, et al. Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice. J Clin Invest. 2011;121:4268–4280.
Shao Y, Lo CM, Ling CC, et al. Regulatory B cells accelerate hepatocellular carcinoma progression via CD40/CD154 signaling pathway. Cancer Lett. 2014;355:264–272.
Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4(+) T cells to T-regulatory cells. Cancer Res. 2011;71:3505–3515.
Schioppa T, Moore R, Thompson RG, et al. B regulatory cells and the tumor-promoting actions of TNF-alpha during squamous carcinogenesis. Proc Natl Acad Sci U S A. 2011;108:10662–10667.
Wolf SD, Dittel BN, Hardardottir F, et al. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med. 1996;184:2271–2278.
Fillatreau S, Sweenie CH, McGeachy MJ, et al. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3:944–950.
Mizoguchi A, Mizoguchi E, Takedatsu H, et al. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity. 2002;16:219–230.
DiLillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci. 2010;1183:38–57.
Mohib K, Cherukuri A, Zhou Y, et al. Antigen-dependent interactions between regulatory B cells and T cells at the T:B border inhibit subsequent T cell interactions with DCs. Am J Transplant. 2020;20:52–63.
Mauri C. Novel frontiers in regulatory B cells. Immunol Rev. 2021;299:5–9.
Simon Q, Pers JO, Cornec D, et al. In-depth characterization of CD24(high)CD38(high) transitional human B cells reveals different regulatory profiles. J Allergy Clin Immunol. 2016;137:1577–1584.e10.
Carter NA, Vasconcellos R, Rosser EC, et al. Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol. 2011;186:5569–5579.
Schwarz C, Mayerhoffer S, Berlakovich GA, et al. Long-term outcome of belatacept therapy in de novo kidney transplant recipients—a case-match analysis. Transpl Int. 2015;28:820–827.
Stolp J, Turka LA, Wood KJ. B cells with immune-regulating function in transplantation. Nat Rev Nephrol. 2014;10:389–397.
Menon M, Blair PA, Isenberg DA, et al. A regulatory feedback between plasmacytoid dendritic cells and regulatory B cells is aberrant in systemic lupus erythematosus. Immunity. 2016;44:683–697.
Cherukuri A, Rothstein DM, Clark B, et al. Immunologic human renal allograft injury associates with an altered IL-10/TNF-alpha expression ratio in regulatory B cells. J Am Soc Nephrol. 2014;25:1575–1585.
Cherukuri A, Salama AD, Mehta R, et al. Transitional B cell cytokines predict renal allograft outcomes. Sci Transl Med. 2021;13:eabe4929.
Yanaba K, Bouaziz J-D, Haas KM, et al. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity. 2008;28:639–650.
Colgan SP, Hershberg RM, Furuta GT, et al. Ligation of intestinal epithelial CD1d induces bioactive IL-10: critical role of the cytoplasmic tail in autocrine signaling. Proc Natl Acad Sci U S A. 1999;96:13938–13943.
Hasan MM, Nair SS, O’Leary JG, et al. Implication of TIGIT(+) human memory B cells in immune regulation. Nat Commun. 2021;12:1534.
Hasan MM, Thompson-Snipes L, Klintmalm G, et al. CD24hiCD38hi and CD24hiCD27+ human regulatory B cells display common and distinct functional characteristics. J Immunol. 2019;203:2110–2120.
Glass MC, Glass DR, Oliveria JP, et al. Human IL-10-producing B cells have diverse states that are induced from multiple B cell subsets. Cell Rep. 2022;39:110728.
Matsushita T, Yanaba K, Bouaziz JD, et al. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008;118:3420–3430.
Le Huu D, Matsushita T, Jin G, et al. Donor-derived regulatory B cells are important for suppression of murine sclerodermatous chronic graft-versus-host disease. Blood. 2013;121:3274–3283.
Zhang M, Zheng X, Zhang J, et al. CD19+ CD1d+ CD5+ B cell frequencies are increased in patients with tuberculosis and suppress Th17 responses. Cell Immunol. 2012;274:89–97.
Zha B, Wang L, Liu X, et al. Decrease in proportion of CD19+ CD24(hi) CD27+ B cells and impairment of their suppressive function in Graves’ disease. PLoS One. 2012;7:e49835.
van der Vlugt LE, Mlejnek E, Ozir-Fazalalikhan A, et al. CD 24hi CD 27+ B cells from patients with allergic asthma have impaired regulatory activity in response to lipopolysaccharide. Clin Exp Allergy. 2014;44:517–528.
Bankoti R, Gupta K, Levchenko A, et al. Marginal zone B cells regulate antigen-specific T cell responses during infection. J Immunol. 2012;188:3961–3971.
Lal G, Kulkarni N, Nakayama Y, et al. IL-10 from marginal zone precursor B cells controls the differentiation of Th17, Tfh and Tfr cells in transplantation tolerance. Immunol Lett. 2016;170:52–63.
van de Veen W, Stanic B, Yaman G, et al. IgG4 production is confined to human IL-10–producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immunol. 2013;131:1204–1212.
Kim AS, Doherty TA, Karta MR, et al. Regulatory B cells and T follicular helper cells are reduced in allergic rhinitis. J Allergy Clin Immunol. 2016;138:1192–1195.e5.
Braza F, Chesne J, Castagnet S, et al. Regulatory functions of B cells in allergic diseases. Allergy. 2014;69:1454–1463.
Guzel HG, Yilmaz VT, Koksoy S, et al. Regulatory B cells profile in kidney transplant recipients with chronic-active antibody-mediated rejection. Transplant Proc. 2023;55:1140–1146.
Lino AC, Lampropoulou V, Welle A, et al. LAG-3 inhibitory receptor expression identifies immunosuppressive natural regulatory plasma cells. Immunity. 2018;49:120–133.e9.
Matsumoto M, Baba A, Yokota T, et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity. 2014;41:1040–1051.
Charoentong P, Finotello F, Angelova M, et al. Pan-cancer immunogenomic analyses reveal genotype-immunophenotype relationships and predictors of response to checkpoint blockade. Cell Rep. 2017;18:248–262.
Iglesia MD, Parker JS, Hoadley KA, et al. Genomic analysis of immune cell infiltrates across 11 tumor types. J Natl Cancer Inst. 2016;108:djw144.
Mose LE, Selitsky SR, Bixby LM, et al. Assembly-based inference of B-cell receptor repertoires from short read RNA sequencing data with V’DJer. Bioinformatics. 2016;32:3729–3734.
Bolotin DA, Poslavsky S, Davydov AN, et al. Antigen receptor repertoire profiling from RNA-seq data. Nat Biotechnol. 2017;35:908–911.
Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348:69–74.
Al-Shibli KI, Donnem T, Al-Saad S, et al. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res. 2008;14:5220–5227.
Shalapour S, Lin XJ, Bastian IN, et al. Inflammation-induced IgA+ cells dismantle anti-liver cancer immunity. Nature. 2017;551:340–345.
Hagn M, Sontheimer K, Dahlke K, et al. Human B cells differentiate into granzyme B-secreting cytotoxic B lymphocytes upon incomplete T-cell help. Immunol Cell Biol. 2012;90:457–467.
Lindner S, Dahlke K, Sontheimer K, et al. Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013;73:2468–2479.
Zhu J, Zeng Y, Dolff S, et al. Granzyme B producing B-cells in renal transplant patients. Clin Immunol. 2017;184:48–53.
Xu W, Narayanan P, Kang N, et al. Human plasma cells express granzyme B. Eur J Immunol. 2014;44:275–284.
Sun J, Wang J, Pefanis E, et al. Transcriptomics identify CD9 as a marker of murine IL-10-competent regulatory B cells. Cell Rep. 2015;13:1110–1117.
Mohd Jaya FN, Garcia SG, Borras FE, et al. In vitro characterization of human CD24(hi)CD38(hi) regulatory B cells shows CD9 is not a stable Breg cell marker. Int J Mol Sci . 2021;22:4583.
Kuchroo VK, Dardalhon V, Xiao S, et al. New roles for TIM family members in immune regulation. Nat Rev Immunol. 2008;8:577–580.
Umetsu SE, Lee WL, McIntire JJ, et al. TIM-1 induces T cell activation and inhibits the development of peripheral tolerance. Nat Immunol. 2005;6:447–454.
Degauque N, Mariat C, Kenny J, et al. Immunostimulatory Tim-1-specific antibody deprograms Tregs and prevents transplant tolerance in mice. J Clin Invest. 2008;118:735–741.
Xiao S, Najafian N, Reddy J, et al. Differential engagement of Tim-1 during activation can positively or negatively costimulate T cell expansion and effector function. J Exp Med. 2007;204:1691–1702.
Ueno T, Habicht A, Clarkson MR, et al. The emerging role of T cell Ig mucin 1 in alloimmune responses in an experimental mouse transplant model. J Clin Invest. 2008;118:742–751.
Meyers JH, Chakravarti S, Schlesinger D, et al. TIM-4 is the ligand for TIM-1, and the TIM-1-TIM-4 interaction regulates T cell proliferation. Nat Immunol. 2005;6:455–464.
Santiago C, Ballesteros A, Tami C, et al. Structures of T cell immunoglobulin mucin receptors 1 and 2 reveal mechanisms for regulation of immune responses by the TIM receptor family. Immunity. 2007;26:299–310.
Tami C, Silberstein E, Manangeeswaran M, et al. Immunoglobulin A (IgA) is a natural ligand of hepatitis A virus cellular receptor 1 (HAVCR1), and the association of IgA with HAVCR1 enhances virus-receptor interactions. J Virol. 2007;81:3437–3446.
Kobayashi N, Karisola P, Pena-Cruz V, et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity. 2007;27:927–940.
Santiago C, Ballesteros A, Martinez-Munoz L, et al. Structures of T cell immunoglobulin mucin protein 4 show a metal-Ion-dependent ligand binding site where phosphatidylserine binds. Immunity. 2007;27:941–951.
Nakae S, Iikura M, Suto H, et al. TIM-1 and TIM-3 enhancement of Th2 cytokine production by mast cells. Blood. 2007;110:2565–2568.
Xiao S, Zhu B, Jin H, et al. Tim-1 stimulation of dendritic cells regulates the balance between effector and regulatory T cells. Eur J Immunol. 2011;41:1539–1549.
Ichimura T, Asseldonk EJ, Humphreys BD, et al. Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest. 2008;118:1657–1668.
Yeung MY, Ding Q, Brooks CR, et al. TIM-1 signaling is required for maintenance and induction of regulatory B cells. Am J Transplant. 2015;15:942–953.
Audo R, Hua C, Hahne M, et al. Phosphatidylserine outer layer translocation is implicated in IL-10 secretion by human regulatory B cells. PLoS One. 2017;12:e0169755.
Xiao S, Bod L, Pochet N, et al. Checkpoint receptor TIGIT expressed on Tim-1(+) B cells regulates tissue inflammation. Cell Rep. 2020;32:107892.
Moreau A, Blair PA, Chai JG, et al. Transitional-2 B cells acquire regulatory function during tolerance induction and contribute to allograft survival. Eur J Immunol. 2015;45:843–853.
Xiao S, Brooks CR, Sobel RA, et al. Tim-1 is essential for induction and maintenance of IL-10 in regulatory B cells and their regulation of tissue inflammation. J Immunol. 2015;194:1602–1608.
Huo Y, Chu Y, Guo L, et al. Cortisol is associated with low frequency of interleukin 10-producing B cells in patients with atherosclerosis. Cell Biochem Funct. 2017;35:178–183.
Gu XL, He H, Lin L, et al. Tim-1(+) B cells suppress T cell interferon-gamma production and promote Foxp3 expression, but have impaired regulatory function in coronary artery disease. APMIS. 2017;125:872–879.
Lee KM, Stott RT, Zhao G, et al. TGF-β-producing regulatory B cells induce regulatory T cells and promote transplantation tolerance. Eur J Immunol. 2014;44:1728–1736.
Aravena O, Ferrier A, Menon M, et al. TIM-1 defines a human regulatory B cell population that is altered in frequency and function in systemic sclerosis patients. Arthritis Res Ther. 2017;19:8.
Zhu G, Liu Y, Zhang W, et al. CD27+ TIM-1+ memory B cells promoted the development of Foxp3+ Tregs and were associated with better survival in acute respiratory distress syndrome. Immunol Res. 2018;66:281–287.
Manieri NA, Chiang EY, Grogan JL. TIGIT: a key inhibitor of the cancer immunity cycle. Trends Immunol. 2017;38:20–28.
Lozano E, Dominguez-Villar M, Kuchroo V, et al. The TIGIT/CD226 axis regulates human T cell function. J Immunol. 2012;188:3869–3875.
Levin SD, Taft DW, Brandt CS, et al. Vstm3 is a member of the CD28 family and an important modulator of T-cell function. Eur J Immunol. 2011;41:902–915.
Yu X, Harden K, Gonzalez LC, et al. The surface protein TIGIT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat Immunol. 2009;10:48–57.
Joller N, Hafler JP, Brynedal B, et al. Cutting edge: TIGIT has T cell-intrinsic inhibitory functions. J Immunol. 2011;186:1338–1342.
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;40:569–581.
Stanietsky N, Simic H, Arapovic J, et al. The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc Natl Acad Sci U S A. 2009;106:17858–17863.
Boles KS, Vermi W, Facchetti F, et al. A novel molecular interaction for the adhesion of follicular CD4 T cells to follicular DC. Eur J Immunol. 2009;39:695–703.
Mendelsohn CL, Wimmer E, Racaniello VR. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989;56:855–865.
Masson D, Jarry A, Baury B, et al. Overexpression of the CD155 gene in human colorectal carcinoma. Gut. 2001;49:236–240.
Casado JG, Pawelec G, Morgado S, et al. Expression of adhesion molecules and ligands for activating and costimulatory receptors involved in cell-mediated cytotoxicity in a large panel of human melanoma cell lines. Cancer Immunol Immunother. 2009;58:1517–1526.
Bevelacqua V, Bevelacqua Y, Candido S, et al. Nectin like-5 overexpression correlates with the malignant phenotype in cutaneous melanoma. Oncotarget. 2012;3:882–892.
Oshima T, Sato S, Kato J, et al. Nectin-2 is a potential target for antibody therapy of breast and ovarian cancers. Mol Cancer. 2013;12:1–13.
Eberle F, Dubreuil P, Mattei MG, et al. The human PRR2 gene, related to the human poliovirus receptor gene (PVR), is the true homolog of the murine MPH gene. Gene. 1995;159:267–272.
Lopez M, Aoubala M, Jordier F, et al. The human poliovirus receptor related 2 protein is a new hematopoietic/endothelial homophilic adhesion molecule. Blood. 1998;92:4602–4611.
Satoh-Horikawa K, Nakanishi H, Takahashi K, et al. Nectin-3, a new member of immunoglobulin-like cell adhesion molecules that shows homophilic and heterophilic cell-cell adhesion activities. J Biol Chem. 2000;275:10291–10299.
Reymond N, Borg JP, Lecocq E, et al. Human nectin3/PRR3: a novel member of the PVR/PRR/nectin family that interacts with afadin. Gene. 2000;255:347–355.
Chen W, Xu Y, Zhong J, et al. MFHAS1 promotes colorectal cancer progress by regulating polarization of tumor-associated macrophages via STAT6 signaling pathway. Oncotarget. 2016;7:78726–78735.
Johnston RJ, Comps-Agrar L, Hackney J, et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function. Cancer Cell. 2014;26:923–937.
Anderson AC, Joller N, Kuchroo VK. Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity. 2016;44:989–1004.
Li M, Xia P, Du Y, et al. T-cell immunoglobulin and ITIM domain (TIGIT) receptor/poliovirus receptor (PVR) ligand engagement suppresses interferon-gamma production of natural killer cells via beta-arrestin 2-mediated negative signaling. J Biol Chem. 2014;289:17647–17657.
Liu S, Zhang H, Li M, et al. Recruitment of Grb2 and SHIP1 by the ITT-like motif of TIGIT suppresses granule polarization and cytotoxicity of NK cells. Cell Death Differ. 2013;20:456–464.
Stanietsky N, Rovis TL, Glasner A, et al. Mouse TIGIT inhibits NK-cell cytotoxicity upon interaction with PVR. Eur J Immunol. 2013;43:2138–2150.
Lucca LE, Axisa PP, Singer ER, et al. TIGIT signaling restores suppressor function of Th1 Tregs. JCI Insight. 2019;4:e124427.
Ouyang W, Liao W, Luo CT, et al. Novel Foxo1-dependent transcriptional programs control Treg cell function. Nature. 2012;491:554–559.
Urbanellis P, Shyu W, Khattar R, et al. The regulatory T cell effector molecule fibrinogen-like protein 2 is necessary for the development of rapamycin-induced tolerance to fully MHC-mismatched murine cardiac allografts. Immunology. 2015;144:91–106.
Piper CJM, Rosser EC, Oleinika K, et al. Aryl hydrocarbon receptor contributes to the transcriptional program of IL-10-producing regulatory B cells. Cell Rep. 2019;29:1878–1892.e7.
Godfrey J, Chen X, Sunseri N, et al. TIGIT is a key inhibitory checkpoint receptor in lymphoma. J ImmunoTher Cancer. 2023;11:e006582.
Bod L, Kye YC, Shi J, et al. B-cell-specific checkpoint molecules that regulate anti-tumour immunity. Nature. 2023;619:348–356.
Crotty S. T follicular helper cell differentiation, function, and roles in disease. Immunity. 2014;41:529–542.
Ma CS, Deenick EK, Batten M, et al. The origins, function, and regulation of T follicular helper cells. J Exp Med. 2012;209:1241–1253.
Vinuesa CG, Linterman MA, Yu D, et al. Follicular helper T cells. Annu Rev Immunol. 2016;34:335–368.
Nurieva RI, Chung Y. Understanding the development and function of T follicular helper cells. Cell Mol Immunol. 2010;7:190–197.
Halloran PF, Reeve JP, Pereira AB, et al. Antibody-mediated rejection, T cell-mediated rejection, and the injury-repair response: new insights from the Genome Canada studies of kidney transplant biopsies. Kidney Int. 2014;85:258–264.
Thaunat O, Koenig A, Leibler C, et al. Effect of immunosuppressive drugs on humoral allosensitization after kidney transplant. J Am Soc Nephrol. 2016;27:1890–1900.
Sellares J, de Freitas DG, Mengel M, et al. Understanding the causes of kidney transplant failure: the dominant role of antibody-mediated rejection and nonadherence. Am J Transplant. 2012;12:388–399.
Djamali A, Kaufman DB, Ellis TM, et al. Diagnosis and management of antibody-mediated rejection: current status and novel approaches. Am J Transplant. 2014;14:255–271.
Mohammed MT, Cai S, Hanson BL, et al. Follicular T cells mediate donor-specific antibody and rejection after solid organ transplantation. Am J Transplant. 2021;21:1893–1901.
Xie MM, Dent AL. Unexpected help: follicular regulatory T cells in the germinal center. Front Immunol. 2018;9:1536.
Liu H, Wu J, Xu X, et al. Peritumoral TIGIT+ CD20+ B cell infiltration indicates poor prognosis but favorable adjuvant chemotherapeutic response in gastric cancer. Int Immunopharmacol. 2022;108:108735.
Asashima H, Axisa PP, Pham THG, et al. Impaired TIGIT expression on B cells drives circulating follicular helper T cell expansion in multiple sclerosis. J Clin Invest. 2022;132:e156254.
Blair PA, Chavez-Rueda KA, Evans JG, et al. Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol. 2009;182:3492–3502.
Arnon TI, Xu Y, Lo C, et al. GRK2-dependent S1PR1 desensitization is required for lymphocytes to overcome their attraction to blood. Science. 2011;333:1898–1903.
Lee KM, Fu Q, Huai G, et al. Suppression of allograft rejection by regulatory B cells induced via TLR signaling. JCI Insight. 2022;7:e152213.
Shankar S, Stolp J, Juvet SC, et al. Ex vivo-expanded human CD19(+)TIM-1(+) regulatory B cells suppress immune responses in vivo and are dependent upon the TIM-1/STAT3 axis. Nat Commun. 2022;13:3121.
Inaba A, Tuong ZK, Zhao TX, et al. Low-dose IL-2 enhances the generation of IL-10-producing immunoregulatory B cells. Nat Commun. 2023;14:2071.
Steinman RM. Lasker Basic Medical Research Award. Dendritic cells: versatile controllers of the immune system. Nat Med. 2007;13:1155–1159.
Rehman Z, Umar S, Meng C, et al. Dendritic cell harmonised immunity to poultry pathogens: a review. World’s Poult Sci J. 2017;73:581–590.
Ganguly D, Haak S, Sisirak V, et al. The role of dendritic cells in autoimmunity. Nat Rev Immunol. 2013;13:566–577.
Wollenberg I, Agua-Doce A, Hernandez A, et al. Regulation of the germinal center reaction by Foxp3+ follicular regulatory T cells. J Immunol. 2011;187:4553–4560.
Bottomley MJ, Chen M, Fuggle S, et al. Application of operational tolerance signatures are limited by variability and type of immunosuppression in renal transplant recipients: a cross-sectional study. Transplant Direct. 2017;3:e125.
Rebollo-Mesa I, Nova-Lamperti E, Mobillo P, et al.; Indices of Tolerance EU Consortium. Biomarkers of tolerance in kidney transplantation: are we predicting tolerance or response to immunosuppressive treatment? Am J Transplant. 2016;16:3443–3457.
Latorre I, Esteve-Sole A, Redondo D, et al. Calcineurin and mTOR inhibitors have opposing effects on regulatory T cells while reducing regulatory B cell populations in kidney transplant recipients. Transpl Immunol. 2016;35:1–6.
Tebbe B, Wilde B, Ye Z, et al. Renal transplant recipients treated with calcineurin-inhibitors lack circulating immature transitional CD19+CD24hiCD38hi regulatory B-lymphocytes. PLoS One. 2016;11:e0153170.
Song J, Du G, Chen W, et al. The advantage of sirolimus in amplifying regulatory B cells and regulatory T cells in liver transplant patients. Eur J Pharmacol. 2020;869:172872.
Pittenger MF, Discher DE, Péault BM, et al. Mesenchymal stem cell perspective: cell biology to clinical progress. NPJ Regen Med. 2019;4:22.
Comoli P, Ginevri F, Maccario R, et al. Human mesenchymal stem cells inhibit antibody production induced in vitro by allostimulation. Nephrol Dial Transplant. 2008;23:1196–1202.
Asari S, Itakura S, Ferreri K, et al. Mesenchymal stem cells suppress B-cell terminal differentiation. Exp Hematol. 2009;37:604–615.
Franquesa M, Mensah FK, Huizinga R, et al. Human adipose tissue-derived mesenchymal stem cells abrogate plasmablast formation and induce regulatory B cells independently of T helper cells. Stem Cells. 2015;33:880–891.
Gupte KS, Vanikar AV, Trivedi HL, et al. In-vitro generation of interleukin-10 secreting B-regulatory cells from donor adipose tissue derived mesenchymal stem cells and recipient peripheral blood mononuclear cells for potential cell therapy. Biomed J. 2017;40:49–54.
Perico N, Casiraghi F, Todeschini M, et al. Long-term clinical and immunological profile of kidney transplant patients given mesenchymal stromal cell immunotherapy. Front Immunol. 2018;9:1359.
Chen Y-B, Shah NN, Renteria AS, et al. Vedolizumab for prevention of graft-versus-host disease after allogeneic hematopoietic stem cell transplantation. Blood Adv. 2019;3:4136–4146.
Liu J, Liu Q, Chen X. The immunomodulatory effects of mesenchymal stem cells on regulatory B cells. Front Immunol. 2020;11:1843.
Xiao S, Brooks CR, Zhu C, et al. Defect in regulatory B-cell function and development of systemic autoimmunity in T-cell Ig mucin 1 (Tim-1) mucin domain-mutant mice. Proc Natl Acad Sci U S A. 2012;109:12105–12110.
Cherukuri A, Mohib K, Rothstein DM. Regulatory B cells: TIM-1, transplant tolerance, and rejection. Immunol Rev. 2021;299:31–44.
Fillatreau S. Regulatory plasma cells. Curr Opin Pharmacol. 2015;23:1–5.