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Original Research

Regulatory B cells promote graft-versus-host disease prevention and maintain graft-versus-leukemia activity following allogeneic bone marrow transplantation

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Article: e1284721 | Received 28 Nov 2016, Accepted 16 Jan 2017, Published online: 15 Mar 2017

References

  • Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet 2009; 373:1550-61; PMID:19282026; http://dx.doi.org/10.1016/S0140-6736(09)60237-3
  • Chang YJ, Xu LP, Wang Y, Zhang XH, Chen H, Chen YH, Wang FR, Han W, Sun YQ, Yan CH et al. Controlled, randomized, open-label trial of risk-stratified corticosteroid prevention of acute graft-versus-host disease after haploidentical transplantation. J Clin Oncol 2016; 34:1855-63; PMID:27091717; http://dx.doi.org/10.1200/JCO.2015.63.8817
  • Negrin RS. Graft-versus-host disease versus graft-versus-leukemia. Hematology Am Soc Hematol Educ Program 2015; 2015:225-30; PMID:26637726; http://dx.doi.org/10.1182/asheducation-2015.1.225
  • Zhao XY, Xu LL, Lu SY, Huang XJ. IL-17-producing T cells contribute to acute graft-versus-host disease in patients undergoing unmanipulated blood and marrow transplantation. Eur J Immunol 2011; 41:514-26; PMID:21268020; http://dx.doi.org/10.1002/eji.201040793
  • Highfill SL, Rodriguez PC, Zhou Q, Goetz CA, Koehn BH, Veenstra R, Taylor PA, Panoskaltsis-Mortari A, Serody JS, Munn DH et al. Bone marrow myeloid-derived suppressor cells (MDSCs) inhibit graft-versus-host disease (GVHD) via an arginase-1-dependent mechanism that is up-regulated by interleukin-13. Blood 2010; 116:5738-47; PMID:20807889; http://dx.doi.org/10.1182/blood-2010-06-287839
  • Christensen ME, Turner BE, Sinfield LJ, Kollar K, Cullup H, Waterhouse NJ, Hart DN, Atkinson K, Rice AM. Mesenchymal stromal cells transiently alter the inflammatory milieu post-transplant to delay graft-versus-host disease. Haematologica 2010; 95:2102-10; PMID:20801899; http://dx.doi.org/10.3324/haematol.2010.028910
  • Sudres M, Norol F, Trenado A, Grégoire S, Charlotte F, Levacher B, Lataillade JJ, Bourin P, Holy X, Vernant JP et al. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol 2006; 176:7761-7; PMID:16751424; http://dx.doi.org/10.4049/jimmunol.176.12.7761
  • Auletta JJ, Eid SK, Wuttisarnwattana P, Human mese Silva I, Metheny L, Keller MD, Guardia-Wolff R, Liu C, Wang F, Bowen T et al. Human mesenchymal stromal cells attenuate graft-versus-host disease and maintain graft-versus-leukemia activity following experimental allogeneic bone marrow transplantation. Stem Cells 2015; 33:601-14; PMID:25336340; http://dx.doi.org/10.1002/stem.1867
  • Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, Strober S, Negrin RS. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003; 9:1144-50; PMID:12925844; http://dx.doi.org/10.1038/nm915
  • Ning H, Yang F, Jiang M, Hu L, Feng K, Zhang J, Yu Z, Li B, Xu C, Li Y et al. The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rate in hematologic malignancy patients: outcome of a pilot clinical study. Leukemia 2008; 22:593-9; PMID:18185520; http://dx.doi.org/10.1038/sj.leu.2405090
  • Gao L, Zhang Y, Hu B, Liu J, Kong P, Lou S, Su Y, Yang T, Li H, Liu Y et al. Phase II multicenter, randomized, double-blind controlled study of efficacy and safety of umbilical cord-derived mesenchymal stromal cells in the prophylaxis of chronic graft-versus-host disease after HLA-haploidentical stem-cell transplantation. J Clin Oncol 2016; 34:2843-50; PMID:27400949; http://dx.doi.org/10.1200/JCO.2015.65.3642
  • 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; PMID:25957264; http://dx.doi.org/10.1093/intimm/dxv026
  • Mauri C, Blair PA. The incognito journey of a regulatory B cell. Immunity 2014; 41:878-80; PMID:25526301; http://dx.doi.org/10.1016/j.immuni.2014.12.003
  • Matsumoto M, Baba A, Yokota T, Nishikawa H, Ohkawa Y, Kayama H, Kallies A, Nutt SL, Sakaguchi S, Takeda K et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity 2014; 41:1040-51; PMID:25484301; http://dx.doi.org/10.1016/j.immuni.2014.10.016
  • Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, Szabolcs PM, Bernstein SH, Magro CM, Williams AD et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011; 117:530-41; PMID:20962324; http://dx.doi.org/10.1182/blood-2010-07-294249
  • Blair PA, Norena LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, Mauri C. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010; 32:129-40; PMID:20079667; http://dx.doi.org/10.1016/j.immuni.2009.11.009
  • Weber M, Stein P, Prufer S, Rudolph B, Kreft A, Schmitt E, Bopp T, Roers A, Schild H, Fillatreau S et al. Donor and host B cell-derived IL-10 contributes to suppression of graft-versus-host disease. Eur J Immunol 2014; 44:1857-65; PMID:24643745; http://dx.doi.org/10.1002/eji.201344081
  • Rowe V, Banovic T, MacDonald KP, Kuns R, Don AL, Morris ES, Burman AC, Bofinger HM, Clouston AD, Hill GR. Host B cells produce IL-10 following TBI and attenuate acute GVHD after allogeneic bone marrow transplantation. Blood 2006; 108:2485-92; PMID:16788097; http://dx.doi.org/10.1182/blood-2006-04-016063
  • Le Huu D, Matsushita T, Jin G, Hamaguchi Y, Hasegawa M, Takehara K, Tedder TF, Fujimoto M. Donor-derived regulatory B cells are important for suppression of murine sclerodermatous chronic graft-versus-host disease. Blood 2013; 121:3274-83; PMID:23422748; http://dx.doi.org/10.1182/blood-2012-11-465658
  • Khoder A, Sarvaria A, Alsuliman A, Chew C, Sekine T, Cooper N, Mielke S, de Lavallade H, Muftuoglu M, Fernandez Curbelo I et al. Regulatory B cells are enriched within the IgM memory and transitional subsets in healthy donors but are deficient in chronic GVHD. Blood 2014; 124:2034-45; PMID:25051962; http://dx.doi.org/10.1182/blood-2014-04-571125
  • de Masson A, Bouaziz JD, Le Buanec H, Robin M, O'Meara A, Parquet N, Rybojad M, Hau E, Monfort JB, Branchtein M et al. CD24(hi)CD27(+) and plasmablast-like regulatory B cells in human chronic graft-versus-host disease. Blood 2015; 125:1830-9; PMID:25605369; http://dx.doi.org/10.1182/blood-2014-09-599159
  • Shlomchik WD. Graft-versus-host disease. Nat Rev Immunol 2007; 7:340-52; PMID:17438575; http://dx.doi.org/10.1038/nri2000
  • Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat Rev Immunol 2010; 10:236-47; PMID:20224569; http://dx.doi.org/10.1038/nri2729
  • Yoshizaki A, Miyagaki T, DiLillo DJ, Matsushita T, Horikawa M, Kountikov EI, Spolski R, Poe JC, Leonard WJ, Tedder TF. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012; 491:264-8; PMID:23064231; http://dx.doi.org/10.1038/nature11501
  • Yu Y, Wang D, Liu C, Kaosaard K, Semple K, Anasetti C, Yu XZ. Prevention of GVHD while sparing GVL effect by targeting Th1 and Th17 transcription factor T-bet and RORgammat in mice. Blood 2011; 118:5011-20; PMID:21856864; http://dx.doi.org/10.1182/blood-2011-03-340315
  • Yi T, Chen Y, Wang L, Du G, Huang D, Zhao D, Johnston H, Young J, Todorov I, Umetsu DT et al. Reciprocal differentiation and tissue-specific pathogenesis of Th1, Th2, and Th17 cells in graft-versus-host disease. Blood 2009; 114:3101-12; PMID:19602708; http://dx.doi.org/10.1182/blood-2009-05-219402
  • Krenger W, Snyder KM, Byon JC, Falzarano G, Ferrara JL. Polarized type 2 alloreactive CD4+ and CD8+ donor T cells fail to induce experimental acute graft-versus-host disease. J Immunol 1995; 155:585-93; PMID:7608537; http://www.jimmunol.org/content/155/2/585
  • Hashimoto D, Asakura S, Miyake S, Yamamura T, Van Kaer L, Liu C, Tanimoto M, Teshima T. Stimulation of host NKT cells by synthetic glycolipid regulates acute graft-versus-host disease by inducing Th2 polarization of donor T cells. J Immunol 2005; 174:551-6; PMID:15611282; http://dx.doi.org/10.4049/jimmunol.174.1.551
  • Flores-Borja F, Bosma A, Ng D, Reddy V, Ehrenstein MR, Isenberg DA, Mauri C. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med 2013; 5:173ra123; http://dx.doi.org/10.1126/scitranslmed.3005407
  • Long J, Chang L, Shen Y, Gao WH, Wu YN, Dou HB, Huang MM, Wang Y, Fang WY, Shan JH et al. Valproic Acid Ameliorates Graft-versus-Host Disease by Downregulating Th1 and Th17 Cells. J Immunol 2015; 195:1849-57; PMID:26179902; http://dx.doi.org/10.4049/jimmunol.1500578
  • Li J, Heinrichs J, Haarberg K, Semple K, Veerapathran A, Liu C, Anasetti C, Yu XZ. HY-Specific Induced Regulatory T Cells Display High Specificity and Efficacy in the Prevention of Acute Graft-versus-Host Disease. J Immunol 2015; 195:717-25; PMID:26048147; http://dx.doi.org/10.4049/jimmunol.1401250
  • Heinrichs J, Li J, Nguyen H, Wu Y, Bastian D, Daethanasanmak A, Sofi MH, Schutt S, Liu C, Jin J et al. CD8(+) Tregs promote GVHD prevention and overcome the impaired GVL effect mediated by CD4(+) Tregs in mice. Oncoimmunology 2016; 5:e1146842; PMID:27471614; http://dx.doi.org/10.1080/2162402X.2016.1146842
  • Nouel A, Pochard P, Simon Q, Ségalen I, Le Meur Y, Pers JO, Hillion S. B-Cells induce regulatory T cells through TGF-beta/IDO production in A CTLA-4 dependent manner. J Autoimmun 2015; 59:53-60; PMID:25753821; http://dx.doi.org/10.1016/j.jaut.2015.02.004
  • Sarvaria A, Basar R, Mehta RS, Shaim H, Muftuoglu M, Khoder A, Sekine T, Gokdemir E, Kondo K, Marin D et al. IL-10+ regulatory B cells are enriched in cord blood and may protect against cGVHD after cord blood transplantation. Blood 2016; 128:1346-61; PMID:27439912; http://dx.doi.org/10.1182/blood-2016-01-695122
  • Chakupurakal G, Garcia-Marquez MA, Shimabukuro-Vornhagen A, Kluth S, Schlosser H, Theurich S, Scheid C, Hallek M, Holtick U, von Bergwelt-Baildon M. Regulatory B10-cells display an altered homeostasis in acute Graft versus Host disease. Eur J Haematol 2016; 98:128-133; PMID:27717015; http://dx.doi.org/10.1111/ejh.12810
  • Taki S, Sato T, Ogasawara K, Fukuda T, Sato M, Hida S, Suzuki G, Mitsuyama M, Shin EH, Kojima S et al. Multistage regulation of Th1-type immune responses by the transcription factor IRF-1. Immunity 1997; 6:673-9; PMID:9208840; http://dx.doi.org/10.1016/S1074-7613(00)80443-4
  • Wang YY, Zhao LJ, Wu CF, Liu P, Shi L, Liang Y, Xiong SM, Mi JQ, Chen Z, Ren R et al. C-KIT mutation cooperates with full-length AML1-ETO to induce acute myeloid leukemia in mice. Proc Natl Acad Sci U S A 2011; 108:2450-5; PMID:21262832; http://dx.doi.org/10.1073/pnas.1019625108
  • Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte J Jr, Crawford JM, Ferrara JL. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 1996; 88:3230-9; PMID:8963063; http://www.bloodjournal.org/content/88/8/3230.full.html
  • Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, Ferrara JL. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood 1997; 90:3204-13; PMID:9376604; http://www.bloodjournal.org/content/90/8/3204.full.html
  • Wang Y, Liu QF, Xu LP, Liu KY, Zhang XH, Ma X, Fan ZP, Wu DP, Huang XJ. Haploidentical vs identical-sibling transplant for AML in remission: a multicenter, prospective study. Blood 2015; 125:3956-62; PMID:25940714; http://dx.doi.org/10.1182/blood-2015-02-627786
  • Wang Y, Liu QF, Xu LP, Liu KY, Zhang XH, Ma X, Wu MQ, Wu DP, Huang XJ. Haploidentical versus matched-sibling transplant in adults with Philadelphia-negative high-risk acute lymphoblastic leukemia: A biologically phase III randomized study. Clin Cancer Res 2016;22:3467-76; PMID:26927664; http://dx.doi.org/10.1158/1078-0432.CCR-15-2335
  • Maecker HT, McCoy JP, Nussenblatt R. Standardizing immunophenotyping for the Human Immunology Project. Nat Rev Immunol 2012; 12:191-200; PMID:22343568; http://dx.doi.org/10.1038/nri3158
  • Chang YJ, Zhao XY, Huo MR, Xu LP, Liu DH, Liu KY, Huang XJ. Immune reconstitution following unmanipulated HLA-mismatched/haploidentical transplantation compared with HLA-identical sibling transplantation. J Clin Immunol 2012; 32:268-80; PMID:22173879; http://dx.doi.org/10.1007/s10875-011-9630-7
  • Chang YJ, Zhao XS, Lv M, Zhao XY, Han TT, Wang HT, Huang XJ. CD19+CD24highCD38high B cells exhibit higher ability in TGF-{beta} and IL-10 secretion and suppressing of CD4+ T cell proliferation but are quantitatively decreased in G-BM of healthy donors (P2146). J Immunol 2013; 190:69.11

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