DC-SIGN–expressing macrophages trigger activation of mannosylated IgM B-cell receptor in follicular lymphoma

Blood - Tập 126 - Trang 1911-1920 - 2015
Rada Amin1,2,3, Frédéric Mourcin1,2,3, Fabrice Uhel1,4, Céline Pangault1,2,3,5, Philippe Ruminy6, Loic Dupré7,8, Marion Guirriec1,2,3, Tony Marchand1,2,3,9, Thierry Fest1,2,3,5, Thierry Lamy1,2,3,9, Karin Tarte1,2,3,5
1Equipe Labellisée Ligue Contre le Cancer, Unité Mixte de Recherche U917, INSERM, Rennes, France;
2Université Rennes 1, Unité Mixte de Recherche U917, Rennes, France;
3Etablissement Français du Sang Bretagne, Rennes, France;
4Service de réanimation médicale, Centre Hospitalier Universitaire de Rennes, Rennes, France;
5Pôle Biologie, Centre Hospitalier Universitaire de Rennes, Rennes, France;
6Centre Henri Becquerel, Université de Rouen, Unité Mixte de Recherche U918, INSERM, Rouen, France;
7Université Toulouse III Paul Sabatier, Toulouse, France;
8Centre de Physiopathologie de Toulouse Purpan, Unité Mixte de Recherche 1043, INSERM, Toulouse, France; and
9Service d'Hématologie Clinique, Centre Hospitalier Universitaire de Rennes, Rennes, France

Tóm tắt

Key Points IgM+ FL B cells display a stronger BCR response than their GC B-cell counterpart despite significant BCR-related phosphatase activity. M2 macrophages trigger DC-SIGN–dependent cell adhesion and BCR activation in IgM+ FL B cells with a highly mannosylated BCR.

Tài liệu tham khảo

Amé-Thomas, 2014, The yin and the yang of follicular lymphoma cell niches: role of microenvironment heterogeneity and plasticity., Semin Cancer Biol, 24, 23, 10.1016/j.semcancer.2013.08.001 Scott, 2014, The tumour microenvironment in B cell lymphomas., Nat Rev Cancer, 14, 517, 10.1038/nrc3774 Zuckerman, 2010, Ig gene diversification and selection in follicular lymphoma, diffuse large B cell lymphoma and primary central nervous system lymphoma revealed by lineage tree and mutation analyses., Int Immunol, 22, 875, 10.1093/intimm/dxq441 Loeffler, 2015, Genomic and epigenomic co-evolution in follicular lymphomas., Leukemia, 29, 456, 10.1038/leu.2014.209 Meeker, 1985, Emergence of idiotype variants during treatment of B-cell lymphoma with anti-idiotype antibodies., N Engl J Med, 312, 1658, 10.1056/NEJM198506273122602 Raffeld, 1985, Spontaneous alteration of idiotype in a monoclonal B-cell lymphoma. Escape from detection by anti-idiotype., N Engl J Med, 312, 1653, 10.1056/NEJM198506273122601 Irish, 2006, Altered B-cell receptor signaling kinetics distinguish human follicular lymphoma B cells from tumor-infiltrating nonmalignant B cells., Blood, 108, 3135, 10.1182/blood-2006-02-003921 Irish, 2010, B-cell signaling networks reveal a negative prognostic human lymphoma cell subset that emerges during tumor progression., Proc Natl Acad Sci USA, 107, 12747, 10.1073/pnas.1002057107 Khalil, 2012, B cell receptor signal transduction in the GC is short-circuited by high phosphatase activity., Science, 336, 1178, 10.1126/science.1213368 Mueller, 2015, Cutting edge: an in vivo reporter reveals active B cell receptor signaling in the germinal center., J Immunol, 194, 2993, 10.4049/jimmunol.1403086 Cha, 2013, Nonstereotyped lymphoma B cell receptors recognize vimentin as a shared autoantigen., J Immunol, 190, 4887, 10.4049/jimmunol.1300179 Sachen, 2012, Self-antigen recognition by follicular lymphoma B-cell receptors., Blood, 120, 4182, 10.1182/blood-2012-05-427534 Zhu, 2002, Acquisition of potential N-glycosylation sites in the immunoglobulin variable region by somatic mutation is a distinctive feature of follicular lymphoma., Blood, 99, 2562, 10.1182/blood.V99.7.2562 Radcliffe, 2007, Human follicular lymphoma cells contain oligomannose glycans in the antigen-binding site of the B-cell receptor., J Biol Chem, 282, 7405, 10.1074/jbc.M602690200 Mamessier, 2015, Contiguous follicular lymphoma and follicular lymphoma in situ harboring N-glycosylated sites., Haematologica, 100, e155, 10.3324/haematol.2014.115782 Coelho, 2010, Glycosylation of surface Ig creates a functional bridge between human follicular lymphoma and microenvironmental lectins., Proc Natl Acad Sci USA, 107, 18587, 10.1073/pnas.1009388107 Schneider, 2015, Lectins from opportunistic bacteria interact with acquired variable-region glycans of surface immunoglobulin in follicular lymphoma., Blood, 125, 3287, 10.1182/blood-2014-11-609404 Vaandrager, 1998, DNA fiber fluorescence in situ hybridization analysis of immunoglobulin class switching in B-cell neoplasia: aberrant CH gene rearrangements in follicle center-cell lymphoma., Blood, 92, 2871, 10.1182/blood.V92.8.2871 Ruminy, 2007, Recurrent disruption of the Imu splice donor site in t(14;18) positive lymphomas: a potential molecular basis for aberrant downstream class switch recombination., Genes Chromosomes Cancer, 46, 735, 10.1002/gcc.20453 Garcia-Vallejo, 2013, The physiological role of DC-SIGN: a tale of mice and men., Trends Immunol, 34, 482, 10.1016/j.it.2013.03.001 Martinez-Pomares, 2012, The mannose receptor., J Leukoc Biol, 92, 1177, 10.1189/jlb.0512231 Dave, 2004, Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells., N Engl J Med, 351, 2159, 10.1056/NEJMoa041869 Farinha, 2005, Analysis of multiple biomarkers shows that lymphoma-associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL)., Blood, 106, 2169, 10.1182/blood-2005-04-1565 Byers, 2008, Clinical quantitation of immune signature in follicular lymphoma by RT-PCR-based gene expression profiling., Blood, 111, 4764, 10.1182/blood-2007-10-115915 Segura, 2013, Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells., J Exp Med, 210, 1035, 10.1084/jem.20121103 Clear, 2010, Increased angiogenic sprouting in poor prognosis FL is associated with elevated numbers of CD163+ macrophages within the immediate sprouting microenvironment., Blood, 115, 5053, 10.1182/blood-2009-11-253260 Calvo, 2008, IL-4 protein expression and basal activation of Erk in vivo in follicular lymphoma., Blood, 112, 3818, 10.1182/blood-2008-02-138933 Pangault, 2010, Follicular lymphoma cell niche: identification of a preeminent IL-4-dependent T(FH)-B cell axis., Leukemia, 24, 2080, 10.1038/leu.2010.223 Domínguez-Soto, 2011, Dendritic cell-specific ICAM-3-grabbing nonintegrin expression on M2-polarized and tumor-associated macrophages is macrophage-CSF dependent and enhanced by tumor-derived IL-6 and IL-10., J Immunol, 186, 2192, 10.4049/jimmunol.1000475 Guilloton, 2012, Mesenchymal stromal cells orchestrate follicular lymphoma cell niche through the CCL2-dependent recruitment and polarization of monocytes., Blood, 119, 2556, 10.1182/blood-2011-08-370908 Young, 2013, Targeting pathological B cell receptor signalling in lymphoid malignancies., Nat Rev Drug Discov, 12, 229, 10.1038/nrd3937 Guo, 2013, IL-4 upregulates Igα and Igβ protein, resulting in augmented IgM maturation and B cell receptor-triggered B cell activation., J Immunol, 191, 670, 10.4049/jimmunol.1203211 Amé-Thomas, 2015, CD10 delineates a subset of human IL-4 producing follicular helper T cells involved in the survival of follicular lymphoma B cells., Blood, 125, 2381, 10.1182/blood-2015-02-625152 Horikawa, 2007, Enhancement and suppression of signaling by the conserved tail of IgG memory-type B cell antigen receptors., J Exp Med, 204, 759, 10.1084/jem.20061923 Laffleur, 2014, AID-induced remodeling of immunoglobulin genes and B cell fate., Oncotarget, 5, 1118, 10.18632/oncotarget.1546 Dogan, 2009, Multiple layers of B cell memory with different effector functions., Nat Immunol, 10, 1292, 10.1038/ni.1814 Pape, 2011, Different B cell populations mediate early and late memory during an endogenous immune response., Science, 331, 1203, 10.1126/science.1201730 Sungalee, 2014, Germinal center reentries of BCL2-overexpressing B cells drive follicular lymphoma progression., J Clin Invest, 124, 5337, 10.1172/JCI72415 Tellier, 2014, Human t(14;18)positive germinal center B cells: a new step in follicular lymphoma pathogenesis?, Blood, 123, 3462, 10.1182/blood-2013-12-545954 Linley, Lectin binding to surface Ig variable regions provides a universal persistent activating signal for follicular lymphoma cells [published online ahead of print July 20, 2015]. Blood. Park, 2014, Mapping the distinctive populations of lymphatic endothelial cells in different zones of human lymph nodes [published correction appears in PLoS One. 2014;9(8):e106814]., PLoS One, 9, e94781, 10.1371/journal.pone.0094781 Wartenberg, 2013, Somatic hypermutation analysis in follicular lymphoma provides evidence suggesting bidirectional cell migration between lymph node and bone marrow during disease progression and relapse., Haematologica, 98, 1433, 10.3324/haematol.2012.074252 Mourcin, 2012, Stromal cell contribution to human follicular lymphoma pathogenesis., Front Immunol, 3, 280, 10.3389/fimmu.2012.00280 Gazi, 2009, Influence of the mannose receptor in host immune responses., Immunobiology, 214, 554, 10.1016/j.imbio.2008.11.004 Amé-Thomas, 2012, Characterization of intratumoral follicular helper T cells in follicular lymphoma: role in the survival of malignant B cells., Leukemia, 26, 1053, 10.1038/leu.2011.301 Epron, 2012, Monocytes and T cells cooperate to favor normal and follicular lymphoma B-cell growth: role of IL-15 and CD40L signaling., Leukemia, 26, 139, 10.1038/leu.2011.179 Mueller, 2007, Critical role of monocytes to support normal B cell and diffuse large B cell lymphoma survival and proliferation., J Leukoc Biol, 82, 567, 10.1189/jlb.0706481 Novak, 2009, Genetic variation in B-cell-activating factor is associated with an increased risk of developing B-cell non-Hodgkin lymphoma., Cancer Res, 69, 4217, 10.1158/0008-5472.CAN-08-4915 Carbonnelle-Puscian, 2009, The novel immunosuppressive enzyme IL4I1 is expressed by neoplastic cells of several B-cell lymphomas and by tumor-associated macrophages., Leukemia, 23, 952, 10.1038/leu.2008.380 Shain, 2014, The B-cell receptor orchestrates environment-mediated lymphoma survival and drug resistance in B-cell malignancies., Oncogene, 33, 4107, 10.1038/onc.2013.379