Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells - PubMed (original) (raw)
. 2013 Apr 15;73(8):2468-79.
doi: 10.1158/0008-5472.CAN-12-3450. Epub 2013 Feb 5.
Karen Dahlke, Kai Sontheimer, Magdalena Hagn, Christof Kaltenmeier, Thomas F E Barth, Thamara Beyer, Frank Reister, Dorit Fabricius, Ramin Lotfi, Oleg Lunov, G Ulrich Nienhaus, Thomas Simmet, Rolf Kreienberg, Peter Möller, Hubert Schrezenmeier, Bernd Jahrsdörfer
Affiliations
- PMID: 23384943
- DOI: 10.1158/0008-5472.CAN-12-3450
Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells
Stefanie Lindner et al. Cancer Res. 2013.
Abstract
The pathogenic impact of tumor-infiltrating B cells is unresolved at present, however, some studies suggest that they may have immune regulatory potential. Here, we report that the microenvironment of various solid tumors includes B cells that express granzyme B (GrB, GZMB), where these B cells can be found adjacent to interleukin (IL)-21-secreting regulatory T cells (Treg) that contribute to immune tolerance of tumor antigens. Because Tregs and plasmacytoid dendritic cells are known to modulate T-effector cells by a GrB-dependent mechanism, we hypothesized that a similar process may operate to modulate regulatory B cells (Breg). IL-21 induced outgrowth of B cells expressing high levels of GrB, which thereby limited T-cell proliferation by a GrB-dependent degradation of the T-cell receptor ζ-chain. Mechanistic investigations into how IL-21 induced GrB expression in B cells to confer Breg function revealed a CD19(+)CD38(+)CD1d(+)IgM(+)CD147(+) expression signature, along with expression of additional key regulatory molecules including IL-10, CD25, and indoleamine-2,3-dioxygenase. Notably, induction of GrB by IL-21 integrated signals mediated by surface immunoglobulin M (B-cell receptor) and Toll-like receptors, each of which were enhanced with expression of the B-cell marker CD5. Our findings show for the first time that IL-21 induces GrB(+) human Bregs. They also establish the existence of human B cells with a regulatory phenotype in solid tumor infiltrates, where they may contribute to the suppression of antitumor immune responses. Together, these findings may stimulate novel diagnostic and cell therapeutic approaches to better manage human cancer as well as autoimmune and graft-versus-host pathologies.
©2013 AACR.
Similar articles
- Human CD19(+)CD25(high) B regulatory cells suppress proliferation of CD4(+) T cells and enhance Foxp3 and CTLA-4 expression in T-regulatory cells.
Kessel A, Haj T, Peri R, Snir A, Melamed D, Sabo E, Toubi E. Kessel A, et al. Autoimmun Rev. 2012 Jul;11(9):670-7. doi: 10.1016/j.autrev.2011.11.018. Epub 2011 Dec 2. Autoimmun Rev. 2012. PMID: 22155204 - Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1+ regulatory B cell expansion.
Ye L, Zhang Q, Cheng Y, Chen X, Wang G, Shi M, Zhang T, Cao Y, Pan H, Zhang L, Wang G, Deng Y, Yang Y, Chen G. Ye L, et al. J Immunother Cancer. 2018 Dec 10;6(1):145. doi: 10.1186/s40425-018-0451-6. J Immunother Cancer. 2018. PMID: 30526680 Free PMC article. - Reciprocal granzyme/perforin-mediated death of human regulatory and responder T cells is regulated by interleukin-2 (IL-2).
Czystowska M, Strauss L, Bergmann C, Szajnik M, Rabinowich H, Whiteside TL. Czystowska M, et al. J Mol Med (Berl). 2010 Jun;88(6):577-88. doi: 10.1007/s00109-010-0602-9. Epub 2010 Mar 12. J Mol Med (Berl). 2010. PMID: 20225066 Free PMC article. - Porcine T lymphocytes and NK cells--an update.
Gerner W, Käser T, Saalmüller A. Gerner W, et al. Dev Comp Immunol. 2009 Mar;33(3):310-20. doi: 10.1016/j.dci.2008.06.003. Epub 2008 Jul 2. Dev Comp Immunol. 2009. PMID: 18601948 Review. - Regulatory B cells in anti-tumor immunity.
Zhang Y, Gallastegui N, Rosenblatt JD. Zhang Y, et al. Int Immunol. 2015 Oct;27(10):521-30. doi: 10.1093/intimm/dxv034. Epub 2015 May 20. Int Immunol. 2015. PMID: 25999597 Review.
Cited by
- The Dual Role of B Cells in the Tumor Microenvironment: Implications for Cancer Immunology and Therapy.
Yang H, Zhang Z, Li J, Wang K, Zhu W, Zeng Y. Yang H, et al. Int J Mol Sci. 2024 Nov 4;25(21):11825. doi: 10.3390/ijms252111825. Int J Mol Sci. 2024. PMID: 39519376 Free PMC article. Review. - The current understanding of the phenotypic and functional properties of human regulatory B cells (Bregs).
Ahsan NF, Lourenço S, Psyllou D, Long A, Shankar S, Bashford-Rogers R. Ahsan NF, et al. Oxf Open Immunol. 2024 Sep 20;5(1):iqae012. doi: 10.1093/oxfimm/iqae012. eCollection 2024. Oxf Open Immunol. 2024. PMID: 39346706 Free PMC article. Review. - Regulatory B Cells Expressing Granzyme B from Tolerant Renal Transplant Patients: Highly Differentiated B Cells with a Unique Pathway with a Specific Regulatory Profile and Strong Interactions with Immune System Cells.
Sailliet N, Dupuy A, Brinas F, Renaudin K, Colas L, Kerleau C, Nguyen TV, Fourgeux C, Poschmann J, Gosset C, Giral M, Degauque N, Mai HL, Danger R, Brouard S; DIVAT Consortium. Sailliet N, et al. Cells. 2024 Jul 31;13(15):1287. doi: 10.3390/cells13151287. Cells. 2024. PMID: 39120317 Free PMC article. - Comprehensive analysis of single cell and bulk RNA sequencing reveals the heterogeneity of melanoma tumor microenvironment and predicts the response of immunotherapy.
Zhang Y, Zhang C, He J, Lai G, Li W, Zeng H, Zhong X, Xie B. Zhang Y, et al. Inflamm Res. 2024 Aug;73(8):1393-1409. doi: 10.1007/s00011-024-01905-5. Epub 2024 Jun 19. Inflamm Res. 2024. PMID: 38896289 - Reassessing granzyme B: unveiling perforin-independent versatility in immune responses and therapeutic potentials.
Thompson R, Cao X. Thompson R, et al. Front Immunol. 2024 May 23;15:1392535. doi: 10.3389/fimmu.2024.1392535. eCollection 2024. Front Immunol. 2024. PMID: 38846935 Free PMC article. Review.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Research Materials