Transcriptional meta-analysis of regulatory B cells.
B cells
Bregs
gene expression
granzyme B
meta-analysis
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
26
11
2019
revised:
01
05
2020
accepted:
09
06
2020
pubmed:
13
6
2020
medline:
2
2
2021
entrez:
13
6
2020
Statut:
ppublish
Résumé
Regulatory B cells (Bregs) have the ability to regulate inflammation in various pathological situations, making them key players in immune regulation. Several mechanisms have been described and we recently identified a GZMB expressing Breg population in kidney transplanted patients who tolerate a kidney graft. To further investigate their biology and mechanisms, we conducted a transcriptomic analysis by RNAseq of these cells and we performed the first weighted meta-analysis of publicly available transcriptomic data from published Breg studies both in humans and mice. We identified two distinct and unique transcriptional signatures of 126 and 93 genes, respectively, associated with these Bregs. While we highlighted genes coding for proteins with potent involvement in regulatory functions, proliferation, and coding for transcription factors, the comparison between humans and mice did not allow identifying a common pattern. Thus, our results suggest distinct species-restricted Breg transcriptional signatures in humans and mice.
Identifiants
pubmed: 32529638
doi: 10.1002/eji.201948489
doi:
Substances chimiques
Granzymes
EC 3.4.21.-
Types de publication
Journal Article
Meta-Analysis
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1757-1769Subventions
Organisme : European Union's Horizon 2020 Research and Innovation Programme
ID : 706296
Pays : International
Organisme : Agence Nationale de la Recherche
ID : ANR-10-IBHU-005
Pays : International
Organisme : Agence Nationale de la Recherche
ID : ANR-11- LABX-0016-01
Pays : International
Organisme : Agence Nationale de la Recherche
ID : ANR-17-CE17-0008
Pays : International
Organisme : Agence Nationale de la Recherche
ID : ANR-17-RHUS-0010
Pays : International
Organisme : H2020 Marie Skłodowska-Curie Actions
ID : 706296
Pays : International
Informations de copyright
© 2020 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
Wasik, M., Nazimek, K. and Bryniarski, K., Regulatory B cell phenotype and mechanism of action: the impact of stimulating conditions. Microbiol. Immunol. 2018. 62: 485-496.
Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D. and Anderton, S. M., B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002. 3: 944-950.
Mauri, C., Gray, D., Mushtaq, N. and Londei, M., Prevention of arthritis by interleukin 10-producing B cells. J. Exp. Med. 2003. 197: 489-501.
Mizoguchi, A., Mizoguchi, E., Takedatsu, H., Blumberg, R. S. and Bhan, A. K., Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002. 16: 219-230.
Iwata, Y., Matsushita, T., Horikawa, M., Dilillo, D. J., Yanaba, K., Venturi, G. M., Szabolcs, P. 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.
Chesneau, M., Pallier, A., Braza, F., Lacombe, G., Le Gallou, S., Baron, D., Giral, M., et al., Unique B cell differentiation profile in tolerant kidney transplant patients. Am. J. Transplant. 2014. 14: 144-155.
Minagawa, R., Okano, S., Tomita, Y., Kishihara, K., Yamada, H., Nomoto, K., Shimada, M., et al., The Critical Role of Fas-Fas Ligand Interaction in Donor-Specific Transfusion-Induced Tolerance to H-Y Antigen. Transplantation 2004. 78: 799-806.
Jahrsdorfer, B., Blackwell, S. E., Wooldridge, J. E., Huang, J., Andreski, M. W., Jacobus, L. S., Taylor, C. M. and Weiner, G. J., B-chronic lymphocytic leukemia cells and other B cells can produce granzyme B and gain cytotoxic potential after interleukin-21-based activation. Blood 2006. 108: 2712-2719.
Lindner, S., Dahlke, K., Sontheimer, K., Hagn, M., Kaltenmeier, C., Barth, T. F., Beyer, T., et al., Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013. 73: 2468-2479.
Hagn, M., Ebel, V., Sontheimer, K., Schwesinger, E., Lunov, O., Beyer, T., Fabricius, D., et al., CD5+ B cells from individuals with systemic lupus erythematosus express granzyme B. Eur. J. Immunol. 2010. 40: 2060-2069.
Kaltenmeier, C., Gawanbacht, A., Beyer, T., Lindner, S., Trzaska, T., van der Merwe, J. A., Harter, G., et al., CD4+ T cell-derived IL-21 and deprivation of CD40 signaling favor the in vivo development of granzyme B-expressing regulatory B cells in HIV patients. J. Immunol. 2015. 194: 3768-3777.
Chesneau, M., Michel, L., Dugast, E., Chenouard, A., Baron, D., Pallier, A., Durand, J., et al., Tolerant kidney transplant patients produce B cells with regulatory properties. J. Am. Soc. Nephrol. 2015. 26: 2588-2598.
Rosser, E. C. and Mauri, C., Regulatory B cells: origin, phenotype, and function. Immunity 2015. 42: 607-612.
Oleinika, K., Mauri, C. and Salama, A. D., Effector and regulatory B cells in immune-mediated kidney disease. Nat. Rev. Nephrol. 2019. 15: 11-26.
Ray, A., Wang, L. and Dittel, B. N., IL-10-independent regulatory B-cell subsets and mechanisms of action. Int. Immunol. 2015. 27: 531-536.
Shen, P., Roch, T., Lampropoulou, V., O'Connor, R. A., Stervbo, U., Hilgenberg, E., Ries, S., et al., IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014. 507: 366-370.
Lin, W., Cerny, D., Chua, E., Duan, K., Yi, J. T., Shadan, N. B., Lum, J., et al., Human regulatory B cells combine phenotypic and genetic hallmarks with a distinct differentiation fate. J. Immunol. 2014. 193: 2258-2266.
van der Veen, W., Stanic, B., Yaman, G., Wawrzyniak, M., Sollner, S., Akdis, D. G., Ruckert, B., 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.
Bigot, J., Pilon, C., Matignon, M., Grondin, C., Leibler, C., Aissat, A., Pirenne, F., et al., Transcriptomic signature of the CD24(hi) CD38(hi) transitional B cells associated with an immunoregulatory phenotype in renal transplant recipients. Am. J. Transplant. 2016. 16: 3430-3442.
Khan, A. R., Amu, S., Saunders, S. P., Hams, E., Blackshields, G., Leonard, M. O., Weaver, C. T., et al., Ligation of TLR7 on CD19(+) CD1d(hi) B cells suppresses allergic lung inflammation via regulatory T cells. Eur. J. Immunol. 2015. 45: 1842-1854.
Braza, F., Chesne, J., Durand, M., Dirou, S., Brosseau, C., Mahay, G., Cheminant, M. A., et al., A regulatory CD9(+) B-cell subset inhibits HDM-induced allergic airway inflammation. Allergy 2015. 70: 1421-1431.
Lino, A. C., Dang, V. D., Lampropoulou, V., Welle, A., Joedicke, J., Pohar, J., Simon, Q., et al., LAG-3 inhibitory receptor expression identifies immunosuppressive natural regulatory plasma cells. Immunity 2018. 49: 120-133.
Ray, A., Khalil, M. I., Pulakanti, K. L., Burns, R. T., Gurski, C. J., Basu, S., Wang, D., et al., Mature IgD(low/-) B cells maintain tolerance by promoting regulatory T cell homeostasis. Nat. Commun. 2019. 10: 190.
Johnson, W. E., Li, C. and Rabinovic, A., Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007. 8: 118-127.
Schumacher, A., Ehrentraut, S., Scharm, M., Wang, H., Hartig, R., Morse, H. C., 3rd. and Zenclussen, A. C., Plasma cell alloantigen 1 and IL-10 secretion define two distinct peritoneal B1a B cell subsets with opposite functions, PC1(high) cells being protective and PC1(low) cells harmful for the growing fetus. Front. Immunol. 2018. 9: 1045.
Tran, D. Q., Andersson, J., Wang, R., Ramsey, H., Unutmaz, D. and Shevach, E. M., GARP (LRRC32) is essential for the surface expression of latent TGF-beta on platelets and activated FOXP3+ regulatory T cells. Proc. Natl. Acad. Sci. U. S. A. 2009. 106: 13445-13450.
Cuende, J., Lienart, S., Dedobbeleer, O., van der Woning, B., De Boeck, G., Stockis, J., Huygens, C., et al., Monoclonal antibodies against GARP/TGF-beta1 complexes inhibit the immunosuppressive activity of human regulatory T cells in vivo. Sci. Transl. Med. 2015. 7: 284ra256.
Grotsch, B., Brachs, S., Lang, C., Luther, J., Derer, A., Schlotzer-Schrehardt, U., Bozec, A., et al., The AP-1 transcription factor Fra1 inhibits follicular B cell differentiation into plasma cells. J. Exp. Med. 2014. 211: 2199-2212.
Luo, S., Ding, S., Liao, J., Zhang, P., Liu, Y., Zhao, M. and Lu, Q. Excessive miR-152-3p results in increased BAFF expression in SLE B-Cells by inhibiting the KLF5 expression. Front. Immunol. 2019. 10: 1127.
Huang, G., Krig, S., Kowbel, D., Xu, H., Hyun, B., Volik, S., Feuerstein, B., et al., ZNF217 suppresses cell death associated with chemotherapy and telomere dysfunction. Hum. Mol. Genet. 2005. 14: 3219-3225.
Smith, S. B., Qu, H. Q., Taleb, N., Kishimoto, N. Y., Scheel, D. W., Lu, Y., Patch, A. M., et al., Rfx6 directs islet formation and insulin production in mice and humans. Nature 2010. 463: 775-780.
Nakashima, A., Kawamoto, T., Honda, K. K., Ueshima, T., Noshiro, M., Iwata, T., Fujimoto, K., et al., DEC1 modulates the circadian phase of clock gene expression. Mol. Cell. Biol. 2008. 28: 4080-4092.
Klinker, M. W., Reed, T. J., Fox, D. A. and Lundy, S. K., Interleukin-5 supports the expansion of fas ligand-expressing killer B cells that induce antigen-specific apoptosis of CD4(+) T cells and secrete interleukin-10. PLoS One 2013. 8: e70131.
Crotty, S., Johnston, R. J. and Schoenberger, S. P., Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 2010. 11: 114-120.
Mauri, C. and Menon, M., The expanding family of regulatory B cells. Int. Immunol. 2015. 27: 479-486.
Walsh, C. J., Hu, P., Batt, J. and Santos, C. C., Microarray meta-analysis and cross-platform normalization: integrative genomics for robust biomarker discovery. Microarrays (Basel) 2015. 4: 389-406.
Lin, D. Y. and Zeng, D., Proper analysis of secondary phenotype data in case-control association studies. Genet. Epidemiol. 2009. 33: 256-265.
Sun, J., Wang, J., Pefanis, E., Chao, J., Rothschild, G., Tachibana, I., Chen, J. K., et al., Transcriptomics identify CD9 as a marker of murine IL-10-competent regulatory B cells. Cell Rep. 2015. 13: 1110-1117.
Wang, H., Shin, D. M., Abbasi, S., Jain, S., Kovalchuk, A. L., Beaty, N., Chen, S., et al., Expression of plasma cell alloantigen 1 defines layered development of B-1a B-cell subsets with distinct innate-like functions. Proc. Natl. Acad. Sci. U. S. A. 2012. 109: 20077-20082.
Yoon, J., Wang, H., Kim, Y. C., Yoshimoto, M., Abbasi, S. and Morse Iii, H. C., Plasma cell alloantigen ENPP1 is expressed by a subset of human B cells with potential regulatory functions. Immunol. Cell Biol. 2016. 94: 719-728.
Rui, L., Healy, J. I., Blasioli, J. and Goodnow, C. C., ERK signaling is a molecular switch integrating opposing inputs from B cell receptor and T cell cytokines to control TLR4-driven plasma cell differentiation. J. Immunol. 2006. 177: 5337-5346.
Liang, B., Workman, C., Lee, J., Chew, C., Dale, B. M., Colonna, L., Flores, M., et al., Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II. J. Immunol. 2008. 180: 5916-5926.
Denoeud, J. and Moser, M., Role of CD27/CD70 pathway of activation in immunity and tolerance. J. Leukoc. Biol. 2011. 89: 195-203.
Tonon, S., Mion, F., Dong, J., Chang, H. D., Dalla, E., Scapini, P., Perruolo, G., et al., IL-10-producing B cells are characterized by a specific methylation signature. Eur. J. Immunol. 2019. 49: 1213-1225.
Huygens, C., Lienart, S., Dedobbeleer, O., Stockis, J., Gauthy, E., Coulie, P. G. and Lucas, S., Lysosomal-associated transmembrane protein 4B (LAPTM4B) decreases transforming growth factor beta1 (TGF-beta1) production in human regulatory T cells. J. Biol. Chem. 2015. 290: 20105-20116.
Allen, C. E., Mak, C. H. and Wu, L. C., The kappa B transcriptional enhancer motif and signal sequences of V(D)J recombination are targets for the zinc finger protein HIVEP3/KRC: a site selection amplification binding study. BMC Immunol. 2002. 3: 10.
Oukka, M., Kim, S. T., Lugo, G., Sun, J., Wu, L. C. and Glimcher, L. H., A mammalian homolog of Drosophila schnurri, KRC, regulates TNF receptor-driven responses and interacts with TRAF2. Mol. Cell 2002. 9: 121-131.
Matsumoto, M., Baba, A., Yokota, T., Nishikawa, H., Ohkawa, Y., Kayama, H., Kallies, A., et al., Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity 2014. 41: 1040-1051.
Maseda, D., Smith, S. H., DiLillo, D. J., Bryant, J. M., Candando, K. M., Weaver, C. T. and Tedder, T. F., Regulatory B10 cells differentiate into antibody-secreting cells after transient IL-10 production in vivo. J. Immunol. 2012. 188: 1036-1048.
Cossarizza, A., Chang, H. D., Radbruch, A., Acs, A., Adam, D., Adam-Klages, S., Agace, W. W., et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur. J. Immunol. 2019. 49: 1457-1973.
Hrvatin, S., Deng, F., O'Donnell, C. W., Gifford, D. K. and Melton, D. A., MARIS: method for analyzing RNA following intracellular sorting. PLoS One 2014. 9: e89459.
Picelli, S., Bjorklund, A. K., Faridani, O. R., Sagasser, S., Winberg, G. and Sandberg, R., Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 2013. 10: 1096-1098.
Picelli, S., Faridani, O. R., Bjorklund, A. K., Winberg, G., Sagasser, S. and Sandberg, R., Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 2014. 9: 171-181.
Trombetta, J. J., Gennert, D., Lu, D., Satija, R., Shalek, A. K. and Regev, A., Preparation of single-cell RNA-Seq libraries for next generation sequencing. Curr Protoc Mol Biol 2014. 107: 4 22 21-17.
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. and Kingsford, C., Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 2017. 14: 417-419.
Love, M. I., Soneson, C., Hickey, P. F., Johnson, L. K., Pierce, N. T., Shepherd, L., Morgan, M. and Patro, R., Tximeta: Reference sequence checksums for provenance identification in RNA-seq. PLoS Comput. Biol. 2020. 16: e1007664.
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W. and Smyth, G. K., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic. Acids. Res. 2015. 43.
Maglott, D., Ostell, J., Pruitt, K. D. and Tatusova, T., Entrez Gene: gene-centered information at NCBI. Nucleic. Acids. Res. 2011. 39: D52-57.
Durinck, S., Moreau, Y., Kasprzyk, A., Davis, S., De Moor, B., Brazma, A. and Huber, W., BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 2005. 21: 3439-3440.
MacDonald, J., Huex10sttranscriptcluster. db: Affymetrix huex10 annotation data (chip huex10sttranscriptcluster). R package 2017. version 8.7.0.
Gentleman, R., Annotate: Annotation for microarrays. R package 2019. version 1.62.0.
Law, C. W., Chen, Y., Shi, W. and Smyth, G. K., Voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 2014. 15: R29.
Benjamini, Y. and Hochberg, Y., Controlling The False Discovery Rate - A Practical And Powerful Approach To Multiple Testing. J. R. Statist. Soc., Series B 1995. 57: 289-300.
Willer, C. J., Li, Y. and Abecasis, G. R., METAL: fast and efficient meta-analysis of genomewide association scans. Bioinformatics 2010. 26: 2190-2191.
Dray, S. and Dufour, A.-B. E., The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 2007. 22.
Siberchicot, A., Julien-Laferrière, A., Dufour, A.-B., Thioulouse, J. and Dray, S., Adegraphics: an S4 lattice-based package for the representation of multivariate data. R J 2017. 9: 198-212.
Zhao, S., Guo, Y., Sheng, Q. and Shyr, Y., Heatmap3: An improved heatmap package with more powerful and convenient features. BMC Bioinformatics 2014. 15: 16.
Yu, G., Wang, L. G., Han, Y. and He, Q. Y., clusterprofiler: an R package for comparing biological themes among gene clusters. OMICS 2012. 16: 284-287.
Liberzon, A., Birger, C., Thorvaldsdottir, H., Ghandi, M., Mesirov, J. P. and Tamayo, P., The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 2015. 1: 417-425.
Szklarczyk, D., Gable, A. L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., et al., STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic. Acids. Res. 2019. 47: D607-D613.