Loss of the HVEM Tumor Suppressor in Lymphoma and Restoration by Modified CAR-T Cells

Aguzzi, 2014, Follicular dendritic cells: Origin, phenotype, and function in health and disease, Trends Immunol., 35, 105, 10.1016/j.it.2013.11.001 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 Amé-Thomas, 2007, Human mesenchymal stem cells isolated from bone marrow and lymphoid organs support tumor B-cell growth: Role of stromal cells in follicular lymphoma pathogenesis, Blood, 109, 693, 10.1182/blood-2006-05-020800 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 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 Amin, 2015, DC-SIGN-expressing macrophages trigger activation of mannosylated IgM B-cell receptor in follicular lymphoma, Blood, 126, 1911, 10.1182/blood-2015-04-640912 Batlevi, 2016, Novel immunotherapies in lymphoid malignancies, Nat. Rev. Clin. Oncol., 13, 25, 10.1038/nrclinonc.2015.187 Beroukhim, 2010, The landscape of somatic copy-number alteration across human cancers, Nature, 463, 899, 10.1038/nature08822 Bjordahl, 2013, Lymphotoxin network pathways shape the tumor microenvironment, Curr. Opin. Immunol., 25, 222, 10.1016/j.coi.2013.01.001 Bouska, 2014, Genome-wide copy-number analyses reveal genomic abnormalities involved in transformation of follicular lymphoma, Blood, 123, 1681, 10.1182/blood-2013-05-500595 Brentjens, 2003, Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15, Nat. Med., 9, 279, 10.1038/nm827 Brentjens, 2013, CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia, Sci. Transl. Med., 5, 177ra38, 10.1126/scitranslmed.3005930 Cai, 2009, The CD160, BTLA, LIGHT/HVEM pathway: A bidirectional switch regulating T-cell activation, Immunol. Rev., 229, 244, 10.1111/j.1600-065X.2009.00783.x Challa-Malladi, 2011, Combined genetic inactivation of β2-Microglobulin and CD58 reveals frequent escape from immune recognition in diffuse large B cell lymphoma, Cancer Cell, 20, 728, 10.1016/j.ccr.2011.11.006 Chang, 2015, Stromal infrastructure of the lymph node and coordination of immunity, Trends Immunol., 36, 30, 10.1016/j.it.2014.11.003 Cheung, 2005, Evolutionarily divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway, Proc. Natl. Acad. Sci. USA, 102, 13218, 10.1073/pnas.0506172102 Cheung, 2009, T cell intrinsic heterodimeric complexes between HVEM and BTLA determine receptivity to the surrounding microenvironment, J. Immunol., 183, 7286, 10.4049/jimmunol.0902490 Cheung, 2010, Acquired TNFRSF14 mutations in follicular lymphoma are associated with worse prognosis, Cancer Res., 70, 9166, 10.1158/0008-5472.CAN-10-2460 Costello, 2003, Stimulation of non-Hodgkin’s lymphoma via HVEM: An alternate and safe way to increase Fas-induced apoptosis and improve tumor immunogenicity, Leukemia, 17, 2500, 10.1038/sj.leu.2403175 Crotty, 2014, T follicular helper cell differentiation, function, and roles in disease, Immunity, 41, 529, 10.1016/j.immuni.2014.10.004 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 De Silva, 2015, Dynamics of B cells in germinal centres, Nat. Rev. Immunol., 15, 137, 10.1038/nri3804 del Rio, 2010, HVEM/LIGHT/BTLA/CD160 cosignaling pathways as targets for immune regulation, J. Leukoc. Biol., 87, 223, 10.1189/jlb.0809590 Egle, 2004, VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia, Blood, 103, 2276, 10.1182/blood-2003-07-2469 Festing, 2002, Guidelines for the design and statistical analysis of experiments using laboratory animals, ILAR J., 43, 244, 10.1093/ilar.43.4.244 Fitzgibbon, 2007, Genome-wide detection of recurring sites of uniparental disomy in follicular and transformed follicular lymphoma, Leukemia, 21, 1514, 10.1038/sj.leu.2404696 Fletcher, 2015, Lymph node fibroblastic reticular cells in health and disease, Nat. Rev. Immunol., 15, 350, 10.1038/nri3846 Gavrieli, 2003, Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of B and T lymphocyte attenuator required for association with protein tyrosine phosphatases SHP-1 and SHP-2, Biochem. Biophys. Res. Commun., 312, 1236, 10.1016/j.bbrc.2003.11.070 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 Kridel, 2015, Cell of origin of transformed follicular lymphoma, Blood, 126, 2118, 10.1182/blood-2015-06-649905 Lauenborg, 2015, Malignant T cells express lymphotoxin α and drive endothelial activation in cutaneous T cell lymphoma, Oncotarget, 6, 15235, 10.18632/oncotarget.3837 Launay, 2012, High rate of TNFRSF14 gene alterations related to 1p36 region in de novo follicular lymphoma and impact on prognosis, Leukemia, 26, 559, 10.1038/leu.2011.266 Lenz, 2008, Stromal gene signatures in large-B-cell lymphomas, N. Engl. J. Med., 359, 2313, 10.1056/NEJMoa0802885 Li, 2013, IMGT/HighV QUEST paradigm for T cell receptor IMGT clonotype diversity and next generation repertoire immunoprofiling, Nat. Commun., 4, 2333, 10.1038/ncomms3333 Li, 2014, Mutations in linker histone genes HIST1H1 B, C, D, and E; OCT2 (POU2F2); IRF8; and ARID1A underlying the pathogenesis of follicular lymphoma, Blood, 123, 1487, 10.1182/blood-2013-05-500264 Lohr, 2012, Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing, Proc. Natl. Acad. Sci. USA, 109, 3879, 10.1073/pnas.1121343109 M’Hidi, 2009, High expression of the inhibitory receptor BTLA in T-follicular helper cells and in B-cell small lymphocytic lymphoma/chronic lymphocytic leukemia, Am. J. Clin. Pathol., 132, 589, 10.1309/AJCPPHKGYYGGL39C Martin-Guerrero, 2013, Recurrent loss of heterozygosity in 1p36 associated with TNFRSF14 mutations in IRF4 translocation negative pediatric follicular lymphomas, Haematologica, 98, 1237, 10.3324/haematol.2012.073916 Mavrakis, 2008, Tumorigenic activity and therapeutic inhibition of Rheb GTPase, Genes Dev., 22, 2178, 10.1101/gad.1690808 Morin, 2011, Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma, Nature, 476, 298, 10.1038/nature10351 Mourcin, 2012, Stromal cell contribution to human follicular lymphoma pathogenesis, Front. Immunol., 3, 280, 10.3389/fimmu.2012.00280 Mueller, 2009, Stromal cell contributions to the homeostasis and functionality of the immune system, Nat. Rev. Immunol., 9, 618, 10.1038/nri2588 Murphy, 2006, Balancing co-stimulation and inhibition with BTLA and HVEM, Nat. Rev. Immunol., 6, 671, 10.1038/nri1917 Okosun, 2014, Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma, Nat. Genet., 46, 176, 10.1038/ng.2856 Olshen, 2004, Circular binary segmentation for the analysis of array-based DNA copy number data, Biostatistics, 5, 557, 10.1093/biostatistics/kxh008 Oricchio, 2011, The Eph-receptor A7 is a soluble tumor suppressor for follicular lymphoma, Cell, 147, 554, 10.1016/j.cell.2011.09.035 Oricchio, 2014, Frequent disruption of the RB pathway in indolent follicular lymphoma suggests a new combination therapy, J. Exp. Med., 211, 1379, 10.1084/jem.20132120 Ortega-Molina, 2015, The histone lysine methyltransferase KMT2D sustains a gene expression program that represses B cell lymphoma development, Nat. Med., 21, 1199, 10.1038/nm.3943 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 Pasero, 2012, The HVEM network: New directions in targeting novel costimulatory/co-inhibitory molecules for cancer therapy, Curr. Opin. Pharmacol., 12, 478, 10.1016/j.coph.2012.03.001 Pasqualucci, 2014, Genetics of follicular lymphoma transformation, Cell Rep., 6, 130, 10.1016/j.celrep.2013.12.027 Pegram, 2012, Tumor-targeted T cells modified to secrete IL-12 eradicate systemic tumors without need for prior conditioning, Blood, 119, 4133, 10.1182/blood-2011-12-400044 Rehm, 2011, Cooperative function of CCR7 and lymphotoxin in the formation of a lymphoma-permissive niche within murine secondary lymphoid organs, Blood, 118, 1020, 10.1182/blood-2010-11-321265 Roozendaal, 2011, Stromal cell-immune cell interactions, Annu. Rev. Immunol., 29, 23, 10.1146/annurev-immunol-031210-101357 Ross, 2007, Comprehensive analysis of copy number and allele status identifies multiple chromosome defects underlying follicular lymphoma pathogenesis, Clin. Cancer Res., 13, 4777, 10.1158/1078-0432.CCR-07-0456 Sadelain, 2015, CD19 CAR Therapy for Acute Lymphoblastic Leukemia, Am. Soc. Clin. Oncol. Educ. Book, 2015, e360, 10.14694/EdBook_AM.2015.35.e360 Schatz, 2011, Targeting cap-dependent translation blocks converging survival signals by AKT and PIM kinases in lymphoma, J. Exp. Med., 208, 1799, 10.1084/jem.20110846 Steinberg, 2011, The signaling networks of the herpesvirus entry mediator (TNFRSF14) in immune regulation, Immunol. Rev., 244, 169, 10.1111/j.1600-065X.2011.01064.x Vendel, 2009, B and T lymphocyte attenuator regulates B cell receptor signaling by targeting Syk and BLNK, J. Immunol., 182, 1509, 10.4049/jimmunol.182.3.1509 Watanabe, 2003, BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1, Nat. Immunol., 4, 670, 10.1038/ni944 Wendel, 2004, Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy, Nature, 428, 332, 10.1038/nature02369 Yildiz, 2015, Activating STAT6 mutations in follicular lymphoma, Blood, 125, 668, 10.1182/blood-2014-06-582650