B cells and tertiary lymphoid structures as determinants of tumour immune contexture and clinical outcome.
Journal
Nature reviews. Clinical oncology
ISSN: 1759-4782
Titre abrégé: Nat Rev Clin Oncol
Pays: England
ID NLM: 101500077
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
accepted:
04
03
2022
pubmed:
3
4
2022
medline:
28
6
2022
entrez:
2
4
2022
Statut:
ppublish
Résumé
B cells are a major component of the tumour microenvironment, where they are predominantly associated with tertiary lymphoid structures (TLS). In germinal centres within mature TLS, B cell clones are selectively activated and amplified, and undergo antibody class switching and somatic hypermutation. Subsequently, these B cell clones differentiate into plasma cells that can produce IgG or IgA antibodies targeting tumour-associated antigens. In tumours without mature TLS, B cells are either scarce or differentiate into regulatory cells that produce immunosuppressive cytokines. Indeed, different tumours vary considerably in their TLS and B cell content. Notably, tumours with mature TLS, a high density of B cells and plasma cells, as well as the presence of antibodies to tumour-associated antigens are typically associated with favourable clinical outcomes and responses to immunotherapy compared with those lacking these characteristics. However, polyclonal B cell activation can also result in the formation of immune complexes that trigger the production of pro-inflammatory cytokines by macrophages and neutrophils. In complement-rich tumours, IgG antibodies can also activate the complement cascade, resulting in the production of anaphylatoxins that sustain tumour-promoting inflammation and angiogenesis. Herein, we review the phenotypic heterogeneity of intratumoural B cells and the importance of TLS in their generation as well as the potential of B cells and TLS as prognostic and predictive biomarkers. We also discuss novel therapeutic approaches that are being explored with the aim of increasing mature TLS formation, B cell differentiation and anti-tumour antibody production within tumours.
Identifiants
pubmed: 35365796
doi: 10.1038/s41571-022-00619-z
pii: 10.1038/s41571-022-00619-z
doi:
Substances chimiques
Antigens, Neoplasm
0
Cytokines
0
Immunoglobulin G
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
441-457Informations de copyright
© 2022. Springer Nature Limited.
Références
Thomas, L. in Cellular and Humoral Aspects of Hypersensitivity 529–532 (Hoeber-Harper, 1959).
Burnet, F. M. Immunological aspects of malignant disease. Lancet 289, 1171–1174 (1967).
doi: 10.1016/S0140-6736(67)92837-1
Ribatti, D. The concept of immune surveillance against tumors. The first theories. Oncotarget 8, 7175–7180 (2017).
pubmed: 27764780
doi: 10.18632/oncotarget.12739
Shankaran, V. et al. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410, 1107–1111 (2001).
pubmed: 11323675
doi: 10.1038/35074122
Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J. & Schreiber, R. D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3, 991–998 (2002).
pubmed: 12407406
doi: 10.1038/ni1102-991
Dunn, G. P., Old, L. J. & Schreiber, R. D. The three Es of cancer immunoediting. Annu. Rev. Immunol. 22, 329–360 (2004).
pubmed: 15032581
doi: 10.1146/annurev.immunol.22.012703.104803
Fridman, W. H., Pagès, F., Sautès-Fridman, C. & Galon, J. The immune contexture in human tumours: impact on clinical outcome. Nat. Rev. Cancer 12, 298–306 (2012).
pubmed: 22419253
doi: 10.1038/nrc3245
Fridman, W. H., Zitvogel, L., Sautès–Fridman, C. & Kroemer, G. The immune contexture in cancer prognosis and treatment. Nat. Rev. Clin. Oncol. 14, 717–734 (2017).
pubmed: 28741618
doi: 10.1038/nrclinonc.2017.101
Becht, E. et al. Immune contexture, immunoscore, and malignant cell molecular subgroups for prognostic and theranostic classifications of cancers. Adv. Immunol. 130, 95–190 (2016).
pubmed: 26923001
doi: 10.1016/bs.ai.2015.12.002
Bindea, G. et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 39, 782–795 (2013).
pubmed: 24138885
doi: 10.1016/j.immuni.2013.10.003
Cassetta, L. et al. Human tumor-associated macrophage and monocyte transcriptional landscapes reveal cancer-specific reprogramming, biomarkers, and therapeutic targets. Cancer Cell 35, 588–602.e10 (2019).
pubmed: 30930117
pmcid: 6472943
doi: 10.1016/j.ccell.2019.02.009
Mantovani, A., Marchesi, F., Jaillon, S., Garlanda, C. & Allavena, P. Tumor-associated myeloid cells: diversity and therapeutic targeting. Cell Mol. Immunol. 18, 566–578 (2021).
pubmed: 33473192
pmcid: 8027665
doi: 10.1038/s41423-020-00613-4
Galon, J. et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313, 1960–1964 (2006).
pubmed: 17008531
doi: 10.1126/science.1129139
Galon, J. & Bruni, D. Tumor immunology and tumor evolution: intertwined histories. Immunity 52, 55–81 (2020).
pubmed: 31940273
doi: 10.1016/j.immuni.2019.12.018
Jass, J. R. Lymphocytic infiltration and survival in rectal cancer. J. Clin. Pathol. 39, 585–589 (1986).
pubmed: 3722412
pmcid: 499954
doi: 10.1136/jcp.39.6.585
Oliveira, G. et al. Phenotype, specificity and avidity of antitumour CD8
pubmed: 34290406
pmcid: 9187974
doi: 10.1038/s41586-021-03704-y
Remark, R. et al. The non-small cell lung cancer immune contexture. A major determinant of tumor characteristics and patient outcome. Am. J. Respir. Crit. Care Med. 191, 377–390 (2015).
pubmed: 25369536
pmcid: 5447326
doi: 10.1164/rccm.201409-1671PP
Scheper, W. et al. Low and variable tumor reactivity of the intratumoral TCR repertoire in human cancers. Nat. Med. 25, 89–94 (2019).
pubmed: 30510250
doi: 10.1038/s41591-018-0266-5
Pasetto, A. et al. Tumor- and neoantigen-reactive T-cell receptors can be identified based on their frequency in fresh tumor. Cancer Immunol. Res. 4, 734–743 (2016).
pubmed: 27354337
pmcid: 5010958
doi: 10.1158/2326-6066.CIR-16-0001
Schumacher, T. N. & Schreiber, R. D. Neoantigens in cancer immunotherapy. Science 348, 69–74 (2015).
pubmed: 25838375
doi: 10.1126/science.aaa4971
Petitprez, F. et al. Transcriptomic analysis of the tumor microenvironment to guide prognosis and immunotherapies. Cancer Immunol. Immunother. 67, 981–988 (2018).
pubmed: 28884365
doi: 10.1007/s00262-017-2058-z
Caushi, J. X. et al. Transcriptional programs of neoantigen-specific TIL in anti-PD-1-treated lung cancers. Nature 596, 126–132 (2021).
pubmed: 34290408
pmcid: 8338555
doi: 10.1038/s41586-021-03752-4
Blackburn, S. D., Shin, H., Freeman, G. J. & Wherry, E. J. Selective expansion of a subset of exhausted CD8 T cells by αPD-L1 blockade. Proc. Natl Acad. Sci. USA 105, 15016–15021 (2008).
pubmed: 18809920
pmcid: 2567485
doi: 10.1073/pnas.0801497105
Rizvi, N. A. et al. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348, 124–128 (2015).
pubmed: 25765070
pmcid: 4993154
doi: 10.1126/science.aaa1348
Le, D. T. et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science 357, 409–413 (2017).
pubmed: 28596308
pmcid: 5576142
doi: 10.1126/science.aan6733
Yarchoan, M., Hopkins, A. & Jaffee, E. M. Tumor mutational burden and response rate to PD-1 inhibition. N. Engl. J. Med. 377, 2500–2501 (2017).
pubmed: 29262275
pmcid: 6549688
doi: 10.1056/NEJMc1713444
Tumeh, P. C. et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515, 568–571 (2014).
pubmed: 25428505
pmcid: 4246418
doi: 10.1038/nature13954
Cortese, N., Carriero, R., Laghi, L., Mantovani, A. & Marchesi, F. Prognostic significance of tumor-associated macrophages: past, present and future. Semin. Immunol. 48, 101408 (2020).
pubmed: 32943279
doi: 10.1016/j.smim.2020.101408
Petitprez, F., Meylan, M., de Reyniès, A., Sautès-Fridman, C. & Fridman, W. H. The tumor microenvironment in the response to immune checkpoint blockade therapies. Front. Immunol. 11, 784 (2020).
pubmed: 32457745
pmcid: 7221158
doi: 10.3389/fimmu.2020.00784
Bronte, V. et al. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat. Commun. 7, 12150 (2016).
pubmed: 27381735
pmcid: 4935811
doi: 10.1038/ncomms12150
Jaillon, S. et al. Neutrophil diversity and plasticity in tumour progression and therapy. Nat. Rev. Cancer 20, 485–503 (2020).
pubmed: 32694624
doi: 10.1038/s41568-020-0281-y
Platonova, S. et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res. 71, 5412–5422 (2011).
pubmed: 21708957
doi: 10.1158/0008-5472.CAN-10-4179
Mamessier, E. et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J. Clin. Invest. 121, 3609–3622 (2011).
pubmed: 21841316
pmcid: 3171102
doi: 10.1172/JCI45816
Russick, J. et al. Natural killer cells in the human lung tumor microenvironment display immune inhibitory functions. J. Immunother. Cancer 8, e001054 (2020).
pubmed: 33067317
pmcid: 7570244
doi: 10.1136/jitc-2020-001054
Curiel, T. J. et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 10, 942–949 (2004).
pubmed: 15322536
doi: 10.1038/nm1093
de Visser, K. E., Korets, L. V. & Coussens, L. M. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7, 411–423 (2005).
pubmed: 15894262
doi: 10.1016/j.ccr.2005.04.014
DeNardo, D. G., Andreu, P. & Coussens, L. M. Interactions between lymphocytes and myeloid cells regulate pro- versus anti-tumor immunity. Cancer Metastasis Rev. 29, 309–316 (2010).
pubmed: 20405169
pmcid: 2865635
doi: 10.1007/s10555-010-9223-6
DiLillo, D. J., Yanaba, K. & Tedder, T. F. B cells are required for optimal CD4
pubmed: 20194720
doi: 10.4049/jimmunol.0903009
Sautès-Fridman, C., Petitprez, F., Calderaro, J. & Fridman, W. H. Tertiary lymphoid structures in the era of cancer immunotherapy. Nat. Rev. Cancer 19, 307–325 (2019).
pubmed: 31092904
doi: 10.1038/s41568-019-0144-6
Fridman, W. H. et al. B cells and cancer: to B or not to B? J. Exp. Med. 218, e2000851 (2020).
Wouters, M. C. A. & Nelson, B. H. Prognostic significance of tumor-infiltrating B cells and plasma cells in human cancer. Clin. Cancer Res. 24, 6125–6135 (2018).
pubmed: 30049748
doi: 10.1158/1078-0432.CCR-18-1481
Germain, C. et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am. J. Respir. Crit. Care Med. 189, 832–844 (2014).
pubmed: 24484236
doi: 10.1164/rccm.201309-1611OC
Chen, J. et al. Single-cell transcriptome and antigen-immunoglobin analysis reveals the diversity of B cells in non-small cell lung cancer. Genome Biol. 21, 152 (2020).
pubmed: 32580738
pmcid: 7315523
doi: 10.1186/s13059-020-02064-6
Griss, J. et al. B cells sustain inflammation and predict response to immune checkpoint blockade in human melanoma. Nat. Commun. 10, 4186 (2019).
pubmed: 31519915
pmcid: 6744450
doi: 10.1038/s41467-019-12160-2
Hu, Q. et al. Atlas of breast cancer infiltrated B-lymphocytes revealed by paired single-cell RNA-sequencing and antigen receptor profiling. Nat. Commun. 12, 2186 (2021).
pubmed: 33846305
pmcid: 8042001
doi: 10.1038/s41467-021-22300-2
Zhang, Y. et al. Single-cell analyses reveal key immune cell subsets associated with response to PD-L1 blockade in triple-negative breast cancer. Cancer Cell 39, 1578–1593.e8 (2021).
pubmed: 34653365
doi: 10.1016/j.ccell.2021.09.010
Jiang, J. et al. Tumour-infiltrating immune cell-based subtyping and signature gene analysis in breast cancer based on gene expression profiles. J. Cancer 11, 1568–1583 (2020).
pubmed: 32047563
pmcid: 6995381
doi: 10.7150/jca.37637
Meylan, M. et al. Tertiary lymphoid structures generate and propagate anti-tumor antibody-producing plasma cells in renal cell cancer. Immunity 55, 527–541.e5 (2022).
pubmed: 35231421
doi: 10.1016/j.immuni.2022.02.001
Ruffin, A. T. et al. B cell signatures and tertiary lymphoid structures contribute to outcome in head and neck squamous cell carcinoma. Nat. Commun. 12, 3349 (2021).
pubmed: 34099645
pmcid: 8184766
doi: 10.1038/s41467-021-23355-x
Montfort, A. et al. A strong B-cell response is part of the immune landscape in human high-grade serous ovarian metastases. Clin. Cancer Res. 23, 250–262 (2017).
pubmed: 27354470
doi: 10.1158/1078-0432.CCR-16-0081
Weiner, A. B. et al. Plasma cells are enriched in localized prostate cancer in black men and are associated with improved outcomes. Nat. Commun. 12, 935 (2021).
pubmed: 33568675
pmcid: 7876147
doi: 10.1038/s41467-021-21245-w
Inoue, S., Leitner, W. W., Golding, B. & Scott, D. Inhibitory effects of B cells on antitumor immunity. Cancer Res. 66, 7741–7747 (2006).
pubmed: 16885377
doi: 10.1158/0008-5472.CAN-05-3766
Rosser, E. C. & Mauri, C. Regulatory B cells: origin, phenotype, and function. Immunity 42, 607–612 (2015).
pubmed: 25902480
doi: 10.1016/j.immuni.2015.04.005
Lee-Chang, C. et al. Inhibition of breast cancer metastasis by resveratrol-mediated inactivation of tumor-evoked regulatory B cells. J. Immunol. 191, 4141–4151 (2013).
pubmed: 24043896
doi: 10.4049/jimmunol.1300606
Shao, Y. et al. Regulatory B cells accelerate hepatocellular carcinoma progression via CD40/CD154 signaling pathway. Cancer Lett. 355, 264–272 (2014).
pubmed: 25301451
doi: 10.1016/j.canlet.2014.09.026
Zhou, X., Su, Y.-X., Lao, X.-M., Liang, Y.-J. & Liao, G.-Q. CD19
pubmed: 26631955
doi: 10.1016/j.oraloncology.2015.11.003
Wang, W. et al. CD19
pubmed: 26378021
pmcid: 4741780
doi: 10.18632/oncotarget.5588
Roya, N. et al. Frequency of IL-10
pubmed: 33402974
pmcid: 7751534
doi: 10.4314/ahs.v20i3.31
Petitprez, F. et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature 577, 556–560 (2020).
pubmed: 31942077
doi: 10.1038/s41586-019-1906-8
Siliņa, K. et al. Germinal centers determine the prognostic relevance of tertiary lymphoid structures and are impaired by corticosteroids in lung squamous cell carcinoma. Cancer Res. 78, 1308–1320 (2018).
pubmed: 29279354
doi: 10.1158/0008-5472.CAN-17-1987
Posch, F. et al. Maturation of tertiary lymphoid structures and recurrence of stage II and III colorectal cancer. Oncoimmunology 7, e1378844 (2017).
pubmed: 29416939
pmcid: 5798199
doi: 10.1080/2162402X.2017.1378844
Wishnie, A. J., Chwat-Edelstein, T., Attaway, M. & Vuong, B. Q. BCR affinity influences T-B interactions and B cell development in secondary lymphoid organs. Front. Immunol. 12, 703918 (2021).
pubmed: 34381455
pmcid: 8350505
doi: 10.3389/fimmu.2021.703918
Gu-Trantien, C. et al. CD4
pubmed: 23778140
pmcid: 3696556
doi: 10.1172/JCI67428
Qin, Z. et al. B cells inhibit induction of T cell-dependent tumor immunity. Nat. Med. 4, 627–630 (1998).
pubmed: 9585241
doi: 10.1038/nm0598-627
Shah, S. et al. Increased rejection of primary tumors in mice lacking B cells: inhibition of anti-tumor CTL and TH1 cytokine responses by B cells. Int. J. Cancer 117, 574–586 (2005).
pubmed: 15912532
doi: 10.1002/ijc.21177
Brodt, P. & Gordon, J. Anti-tumor immunity in B lymphocyte-deprived mice. I. Immunity to a chemically induced tumor. J. Immunol. 121, 359–362 (1978).
pubmed: 307580
Barbera-Guillem, E. et al. B lymphocyte pathology in human colorectal cancer. Experimental and clinical therapeutic effects of partial B cell depletion. Cancer Immunol. Immunother. 48, 541–549 (2000).
pubmed: 10630306
doi: 10.1007/PL00006672
Shen, P. & Fillatreau, S. Antibody-independent functions of B cells: a focus on cytokines. Nat. Rev. Immunol. 15, 441–451 (2015).
pubmed: 26065586
doi: 10.1038/nri3857
Schwartz, M., Zhang, Y. & Rosenblatt, J. D. B cell regulation of the anti-tumor response and role in carcinogenesis. J. Immunother. Cancer 4, 40 (2016).
pubmed: 27437104
pmcid: 4950763
doi: 10.1186/s40425-016-0145-x
Sarvaria, A., Madrigal, J. A. & Saudemont, A. B cell regulation in cancer and anti-tumor immunity. Cell Mol. Immunol. 14, 662–674 (2017).
pubmed: 28626234
pmcid: 5549607
doi: 10.1038/cmi.2017.35
Sharonov, G. V., Serebrovskaya, E. O., Yuzhakova, D. V., Britanova, O. V. & Chudakov, D. M. B cells, plasma cells and antibody repertoires in the tumour microenvironment. Nat. Rev. Immunol. https://doi.org/10.1038/s41577-019-0257-x (2020).
doi: 10.1038/s41577-019-0257-x
pubmed: 31988391
Kinker, G. S. et al. B cell orchestration of anti-tumor immune responses: a matter of cell localization and communication. Front. Cell Dev. Biol. 9, 678127 (2021).
pubmed: 34164398
pmcid: 8215448
doi: 10.3389/fcell.2021.678127
Yoshizaki, A. et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491, 264–268 (2012).
pubmed: 23064231
pmcid: 3493692
doi: 10.1038/nature11501
Rosser, E. C. et al. Regulatory B cells are induced by gut microbiota-driven interleukin-1β and interleukin-6 production. Nat. Med. 20, 1334–1339 (2014).
pubmed: 25326801
doi: 10.1038/nm.3680
Wang, R.-X. et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat. Med. 20, 633–641 (2014).
pubmed: 24743305
pmcid: 4048323
doi: 10.1038/nm.3554
Dambuza, I. M. et al. IL-12p35 induces expansion of IL-10 and IL-35-expressing regulatory B cells and ameliorates autoimmune disease. Nat. Commun. 8, 719 (2017).
pubmed: 28959012
pmcid: 5620058
doi: 10.1038/s41467-017-00838-4
Fillatreau, S., Sweenie, C. H., McGeachy, M. J., Gray, D. & Anderton, S. M. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 3, 944–950 (2002).
pubmed: 12244307
doi: 10.1038/ni833
Menon, M., Blair, P. A., Isenberg, D. A. & Mauri, C. A regulatory feedback between plasmacytoid dendritic cells and regulatory B cells is aberrant in systemic lupus erythematosus. Immunity 44, 683–697 (2016).
pubmed: 26968426
pmcid: 4803914
doi: 10.1016/j.immuni.2016.02.012
Ran, Z., Yue-Bei, L., Qiu-Ming, Z. & Huan, Y. Regulatory B cells and its role in central nervous system inflammatory demyelinating diseases. Front. Immunol. 11, 1884 (2020).
pubmed: 32973780
pmcid: 7468432
doi: 10.3389/fimmu.2020.01884
Ishigami, E. et al. Coexistence of regulatory B cells and regulatory T cells in tumor-infiltrating lymphocyte aggregates is a prognostic factor in patients with breast cancer. Breast Cancer 26, 180–189 (2019).
pubmed: 30244409
doi: 10.1007/s12282-018-0910-4
Wei, X. et al. Regulatory B cells contribute to the impaired antitumor immunity in ovarian cancer patients. Tumor Biol. 37, 6581–6588 (2016).
doi: 10.1007/s13277-015-4538-0
Olkhanud, P. B. et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4
pubmed: 21444674
pmcid: 3096701
doi: 10.1158/0008-5472.CAN-10-4316
Mantovani, A., Sozzani, S., Locati, M., Allavena, P. & Sica, A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549–555 (2002).
pubmed: 12401408
doi: 10.1016/S1471-4906(02)02302-5
Wu, H. et al. PD-L1
pubmed: 32001420
doi: 10.1016/j.molimm.2020.01.008
Yang, C. et al. B cells promote tumor progression via STAT3 regulated-angiogenesis. PLoS ONE 8, e64159 (2013).
pubmed: 23734190
pmcid: 3667024
doi: 10.1371/journal.pone.0064159
Meylan, M. et al. Early hepatic lesions display immature tertiary lymphoid structures and show elevated expression of immune inhibitory and immunosuppressive molecules. Clin. Cancer Res. https://doi.org/10.1158/1078-0432.CCR-19-2929 (2020).
doi: 10.1158/1078-0432.CCR-19-2929
pubmed: 32269054
de Jonge, K. et al. Inflammatory B cells correlate with failure to checkpoint blockade in melanoma patients. OncoImmunology 10, 1873585 (2021).
pubmed: 33643691
pmcid: 7872097
doi: 10.1080/2162402X.2021.1873585
Kwak, J. W. et al. Complement activation via a C3a receptor pathway alters CD4
pubmed: 29118090
doi: 10.1158/0008-5472.CAN-17-0240
Roumenina, L. T., Daugan, M. V., Petitprez, F., Sautès-Fridman, C. & Fridman, W. H. Context-dependent roles of complement in cancer. Nat. Rev. Cancer 19, 698–715 (2019).
pubmed: 31666715
doi: 10.1038/s41568-019-0210-0
Tan, T.-T. & Coussens, L. M. Humoral immunity, inflammation and cancer. Curr. Opin. Immunol. 19, 209–216 (2007).
pubmed: 17276050
doi: 10.1016/j.coi.2007.01.001
Murphy, T. L. & Murphy, K. M. Dendritic cells in cancer immunology. Cell Mol. Immunol. https://doi.org/10.1038/s41423-021-00741-5 (2021).
doi: 10.1038/s41423-021-00741-5
pubmed: 34480145
pmcid: 8752832
Bruno, T. C. et al. Antigen-presenting intratumoral B cells affect CD4
pubmed: 28848053
pmcid: 5788174
doi: 10.1158/2326-6066.CIR-17-0075
Wennhold, K. et al. CD86
pubmed: 34155067
doi: 10.1158/2326-6066.CIR-20-0949
Nielsen, J. S. et al. CD20
pubmed: 22553348
doi: 10.1158/1078-0432.CCR-12-0234
Kroeger, D. R., Milne, K. & Nelson, B. H. Tumor-infiltrating plasma cells are associated with tertiary lymphoid structures, cytolytic T-cell responses, and superior prognosis in ovarian cancer. Clin. Cancer Res. 22, 3005–3015 (2016).
pubmed: 26763251
doi: 10.1158/1078-0432.CCR-15-2762
Nielsen, J. S. & Nelson, B. H. Tumor-infiltrating B cells and T cells: working together to promote patient survival. Oncoimmunology 1, 1623–1625 (2012).
pubmed: 23264915
pmcid: 3525624
doi: 10.4161/onci.21650
von Bergwelt-Baildon, M. S. et al. Human primary and memory cytotoxic T lymphocyte responses are efficiently induced by means of CD40-activated B cells as antigen-presenting cells: potential for clinical application. Blood 99, 3319–3325 (2002).
pubmed: 11964299
doi: 10.1182/blood.V99.9.3319
Gnjatic, S. et al. Cross-presentation of HLA class I epitopes from exogenous NY-ESO-1 polypeptides by nonprofessional APCs. J. Immunol. 170, 1191–1196 (2003).
pubmed: 12538675
doi: 10.4049/jimmunol.170.3.1191
Thommen, D. S. et al. A transcriptionally and functionally distinct PD-1
pubmed: 29892065
pmcid: 6110381
doi: 10.1038/s41591-018-0057-z
Willsmore, Z. N. et al. B cells in patients with melanoma: implications for treatment with checkpoint inhibitor antibodies. Front. Immunol. 11, 622442 (2020).
pubmed: 33569063
doi: 10.3389/fimmu.2020.622442
Iglesia, M. D. et al. Prognostic B-cell signatures using mRNA-seq in patients with subtype-specific breast and ovarian cancer. Clin. Cancer Res. 20, 3818–3829 (2014).
pubmed: 24916698
pmcid: 4102637
doi: 10.1158/1078-0432.CCR-13-3368
Iglesia, M. D. et al. Genomic analysis of immune cell infiltrates across 11 tumor types. J. Natl Cancer Inst. 108, djw144 (2016).
pmcid: 5241901
doi: 10.1093/jnci/djw144
Selitsky, S. R. et al. Prognostic value of B cells in cutaneous melanoma. Genome Med. 11, 36 (2019).
pubmed: 31138334
pmcid: 6540526
doi: 10.1186/s13073-019-0647-5
Garaud, S. et al. Tumor infiltrating B-cells signal functional humoral immune responses in breast cancer. JCI Insight 5, e129641 (2019).
doi: 10.1172/jci.insight.129641
Biswas, S. et al. IgA transcytosis and antigen recognition govern ovarian cancer immunity. Nature https://doi.org/10.1038/s41586-020-03144-0 (2021).
doi: 10.1038/s41586-020-03144-0
pubmed: 34819672
pmcid: 8742224
Shalapour, S. & Karin, M. The neglected brothers come of age: B cells and cancer. Semin. Immunol. https://doi.org/10.1016/j.smim.2021.101479 (2021).
doi: 10.1016/j.smim.2021.101479
pubmed: 34215491
Ito, T. et al. Class distribution of immunoglobulin-containing plasma cells in the stroma of medullary carcinoma of breast. Breast Cancer Res. Treat. 7, 97–103 (1986).
pubmed: 3013350
doi: 10.1007/BF01806794
Bolotin, D. A. et al. Antigen receptor repertoire profiling from RNA-seq data. Nat. Biotechnol. 35, 908–911 (2017).
pubmed: 29020005
pmcid: 6169298
doi: 10.1038/nbt.3979
Saul, L. et al. IgG subclass switching and clonal expansion in cutaneous melanoma and normal skin. Sci. Rep. 6, 29736 (2016).
pubmed: 27411958
pmcid: 4944184
doi: 10.1038/srep29736
Goc, J. et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8
pubmed: 24366885
doi: 10.1158/0008-5472.CAN-13-1342
de Chaisemartin, L. et al. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res. 71, 6391–6399 (2011).
pubmed: 21900403
doi: 10.1158/0008-5472.CAN-11-0952
Cipponi, A. et al. Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res. 72, 3997–4007 (2012).
pubmed: 22850419
doi: 10.1158/0008-5472.CAN-12-1377
Wieland, A. et al. Defining HPV-specific B cell responses in patients with head and neck cancer. Nature https://doi.org/10.1038/s41586-020-2931-3 (2020).
doi: 10.1038/s41586-020-2931-3
pubmed: 33208941
Shalapour, S. et al. Immunosuppressive plasma cells impede T-cell-dependent immunogenic chemotherapy. Nature 521, 94–98 (2015).
pubmed: 25924065
pmcid: 4501632
doi: 10.1038/nature14395
Shalapour, S. et al. Inflammation-induced IgA
pubmed: 29144460
pmcid: 5884449
doi: 10.1038/nature24302
Pilette, C., Detry, B., Guisset, A., Gabriels, J. & Sibille, Y. Induction of interleukin-10 expression through Fcalpha receptor in human monocytes and monocyte-derived dendritic cells: role of p38 MAPKinase. Immunol. Cell Biol. 88, 486–493 (2010).
pubmed: 20084080
doi: 10.1038/icb.2009.120
Saha, C. et al. Monomeric immunoglobulin A from plasma inhibits human Th17 responses in vitro independent of FcαRI and DC-SIGN. Front. Immunol. 8, 275 (2017).
pubmed: 28352269
pmcid: 5349300
doi: 10.3389/fimmu.2017.00275
Peppas, I. et al. Association of serum immunoglobulin levels with solid cancer: a systematic review and meta-analysis. Cancer Epidemiol. Biomark. Prev. 29, 527–538 (2020).
doi: 10.1158/1055-9965.EPI-19-0953
Kalergis, A. M. & Ravetch, J. V. Inducing tumor immunity through the selective engagement of activating Fcgamma receptors on dendritic cells. J. Exp. Med. 195, 1653–1659 (2002).
pubmed: 12070293
pmcid: 2193555
doi: 10.1084/jem.20020338
Roumenina, L. T. et al. Tumor cells hijack macrophage-produced complement C1q to promote tumor growth. Cancer Immunol. Res. 7, 1091–1105 (2019).
pubmed: 31164356
doi: 10.1158/2326-6066.CIR-18-0891
Bulla, R. et al. C1q acts in the tumour microenvironment as a cancer-promoting factor independently of complement activation. Nat. Commun. 7, 10346 (2016).
pubmed: 26831747
pmcid: 4740357
doi: 10.1038/ncomms10346
Karagiannis, P. et al. IgG4 subclass antibodies impair antitumor immunity in melanoma. J. Clin. Invest. 123, 1457–1474 (2013).
pubmed: 23454746
pmcid: 3613918
doi: 10.1172/JCI65579
Fujimoto, M. et al. Stromal plasma cells expressing immunoglobulin G4 subclass in non-small cell lung cancer. Hum. Pathol. 44, 1569–1576 (2013).
pubmed: 23465276
doi: 10.1016/j.humpath.2013.01.002
Sahin, U. et al. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc. Natl Acad. Sci. USA 92, 11810–11813 (1995).
pubmed: 8524854
pmcid: 40492
doi: 10.1073/pnas.92.25.11810
Stockert, E. et al. A survey of the humoral immune response of cancer patients to a panel of human tumor antigens. J. Exp. Med. 187, 1349–1354 (1998).
pubmed: 9547346
pmcid: 2212223
doi: 10.1084/jem.187.8.1349
Brichory, F. M. et al. An immune response manifested by the common occurrence of annexins I and II autoantibodies and high circulating levels of IL-6 in lung cancer. Proc. Natl Acad. Sci. USA 98, 9824–9829 (2001).
pubmed: 11504947
pmcid: 55537
doi: 10.1073/pnas.171320598
Reuschenbach, M., von Knebel Doeberitz, M. & Wentzensen, N. A systematic review of humoral immune responses against tumor antigens. Cancer Immunol. Immunother. 58, 1535–1544 (2009).
pubmed: 19562338
pmcid: 2782676
doi: 10.1007/s00262-009-0733-4
Amornsiripanitch, N. et al. Complement factor H autoantibodies are associated with early stage NSCLC. Clin. Cancer Res. 16, 3226–3231 (2010).
pubmed: 20515868
pmcid: 2891404
doi: 10.1158/1078-0432.CCR-10-0321
Garaud, S. et al. Antigen specificity and clinical significance of IgG and IgA autoantibodies produced in situ by tumor-infiltrating B cells in breast cancer. Front. Immunol. 9, 2660 (2018).
pubmed: 30515157
pmcid: 6255822
doi: 10.3389/fimmu.2018.02660
Gnjatic, S. et al. Seromic profiling of ovarian and pancreatic cancer. Proc. Natl Acad. Sci. USA 107, 5088–5093 (2010).
pubmed: 20194765
pmcid: 2841879
doi: 10.1073/pnas.0914213107
Mazor, R. D. et al. Tumor-reactive antibodies evolve from non-binding and autoreactive precursors. Cell, https://doi.org/10.1016/j.cell.2022.02.012 (2022).
Schmidt, M. et al. A comprehensive analysis of human gene expression profiles identifies stromal immunoglobulin κ C as a compatible prognostic marker in human solid tumors. Clin. Cancer Res. 18, 2695–2703 (2012).
pubmed: 22351685
doi: 10.1158/1078-0432.CCR-11-2210
Horeweg, N. et al. Tertiary lymphoid structures critical for prognosis in endometrial cancer patients. Nat. Commun. 13, 1373 (2022).
pubmed: 35296668
pmcid: 8927106
doi: 10.1038/s41467-022-29040-x
Kim, S. S. et al. B cells improve overall survival in HPV-associated squamous cell carcinomas and are activated by radiation and PD-1 blockade. Clin. Cancer Res. 26, 3345–3359 (2020).
pubmed: 32193227
pmcid: 7334097
doi: 10.1158/1078-0432.CCR-19-3211
Lundgren, S., Berntsson, J., Nodin, B., Micke, P. & Jirström, K. Prognostic impact of tumour-associated B cells and plasma cells in epithelial ovarian cancer. J. Ovarian Res. 9, 21 (2016).
pubmed: 27048364
pmcid: 4822228
doi: 10.1186/s13048-016-0232-0
Zirakzadeh, A. A. et al. Tumour-associated B cells in urothelial urinary bladder cancer. Scand. J. Immunol. 91, e12830 (2020).
pubmed: 31823416
doi: 10.1111/sji.12830
Murakami, Y. et al. Increased regulatory B cells are involved in immune evasion in patients with gastric cancer. Sci. Rep. 9, 13083 (2019).
pubmed: 31511630
pmcid: 6739478
doi: 10.1038/s41598-019-49581-4
Calderaro, J. et al. Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma. J. Hepatol. 70, 58–65 (2019).
pubmed: 30213589
doi: 10.1016/j.jhep.2018.09.003
Li, H. et al. Existence of intratumoral tertiary lymphoid structures is associated with immune cells infiltration and predicts better prognosis in early-stage hepatocellular carcinoma. Aging 12, 3451–3472 (2020).
pubmed: 32087064
pmcid: 7066901
doi: 10.18632/aging.102821
Nault, J. C. et al. Telomerase reverse transcriptase promoter mutation is an early somatic genetic alteration in the transformation of premalignant nodules in hepatocellular carcinoma on cirrhosis. Hepatology 60, 1983–1992 (2014).
pubmed: 25123086
doi: 10.1002/hep.27372
Finkin, S. et al. Ectopic lymphoid structures function as microniches for tumor progenitor cells in hepatocellular carcinoma. Nat. Immunol. 16, 1235–1244 (2015).
pubmed: 26502405
pmcid: 4653079
doi: 10.1038/ni.3290
Di Caro, G. et al. Occurrence of tertiary lymphoid tissue is associated with T-cell infiltration and predicts better prognosis in early-stage colorectal cancers. Clin. Cancer Res. 20, 2147–2158 (2014).
pubmed: 24523438
doi: 10.1158/1078-0432.CCR-13-2590
Helmink, B. A. et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature 577, 549–555 (2020).
pubmed: 31942075
pmcid: 8762581
doi: 10.1038/s41586-019-1922-8
Cabrita, R. et al. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature 577, 561–565 (2020).
pubmed: 31942071
doi: 10.1038/s41586-019-1914-8
Patil, N. S. et al. Intratumoral plasma cells predict outcomes to PD-L1 blockade in non-small cell lung cancer. Cancer Cell https://doi.org/10.1016/j.ccell.2022.02.002 (2022).
doi: 10.1016/j.ccell.2022.02.002
pubmed: 35216676
Vanhersecke, L. et al. Mature tertiary lymphoid structures predict immune checkpoint inhibitor efficacy in solid tumors independently of PD-L1 expression. Nat. Cancer 2, 794–802 (2021).
pubmed: 35118423
pmcid: 8809887
doi: 10.1038/s43018-021-00232-6
Gao, J. et al. Neoadjuvant PD-L1 plus CTLA-4 blockade in patients with cisplatin-ineligible operable high-risk urothelial carcinoma. Nat. Med. 26, 1845–1851 (2020).
pubmed: 33046869
doi: 10.1038/s41591-020-1086-y
Italiano, A. et al. PD1 inhibition in soft-tissue sarcomas with tertiary lymphoid structures: a multicentre phase II trial. J. Clin. Oncol. 39 (Suppl. 15), 11507 (2021).
doi: 10.1200/JCO.2021.39.15_suppl.11507
Affara, N. I. et al. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell 25, 809–821 (2014).
pubmed: 24909985
pmcid: 4063283
doi: 10.1016/j.ccr.2014.04.026
Lu, Y. et al. Complement signals determine opposite effects of B cells in chemotherapy-induced immunity. Cell https://doi.org/10.1016/j.cell.2020.02.015 (2020).
doi: 10.1016/j.cell.2020.02.015
pubmed: 33248023
pmcid: 7584921
DuPage, M., Mazumdar, C., Schmidt, L. M., Cheung, A. F. & Jacks, T. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 482, 405–409 (2012).
pubmed: 22318517
pmcid: 3288744
doi: 10.1038/nature10803
Joshi, N. S. et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity 43, 579–590 (2015).
pubmed: 26341400
pmcid: 4826619
doi: 10.1016/j.immuni.2015.08.006
Delvecchio, F. R. et al. Pancreatic cancer chemotherapy is potentiated by induction of tertiary lymphoid structures in mice. Cell Mol. Gastroenterol. Hepatol. https://doi.org/10.1016/j.jcmgh.2021.06.023 (2021).
doi: 10.1016/j.jcmgh.2021.06.023
pubmed: 34252585
pmcid: 8529396
Peske, J. D., Woods, A. B. & Engelhard, V. H. Control of CD8 T-cell infiltration into tumors by vasculature and microenvironment. Adv. Cancer Res. 128, 263–307 (2015).
pubmed: 26216636
pmcid: 4638417
doi: 10.1016/bs.acr.2015.05.001
Rodriguez, A. B. et al. Immune mechanisms orchestrate tertiary lymphoid structures in tumors via cancer-associated fibroblasts. Cell Rep. 36, 109422 (2021).
pubmed: 34289373
pmcid: 8362934
doi: 10.1016/j.celrep.2021.109422
Onder, L. & Ludewig, B. Redefining the nature of lymphoid tissue organizer cells: response to ‘Complexity of Lymphoid Tissue Organizers’ by Koning and Mebius. Trends Immunol. 39, 952–953 (2018).
pubmed: 30396803
doi: 10.1016/j.it.2018.10.007
Drayton, D. L., Ying, X., Lee, J., Lesslauer, W. & Ruddle, N. H. Ectopic LTαβ directs lymphoid organ neogenesis with concomitant expression of peripheral node addressin and a HEV-restricted sulfotransferase. J. Exp. Med. 197, 1153–1163 (2003).
pubmed: 12732657
pmcid: 2193975
doi: 10.1084/jem.20021761
Luther, S. A., Lopez, T., Bai, W., Hanahan, D. & Cyster, J. G. BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 12, 471–481 (2000).
pubmed: 10843380
doi: 10.1016/S1074-7613(00)80199-5
Shields, J. D., Kourtis, I. C., Tomei, A. A., Roberts, J. M. & Swartz, M. A. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 328, 749–752 (2010).
pubmed: 20339029
doi: 10.1126/science.1185837
Lu, T. T. & Browning, J. L. Role of the lymphotoxin/LIGHT system in the development and maintenance of reticular networks and vasculature in lymphoid tissues. Front. Immunol. 5, 47 (2014).
pubmed: 24575096
pmcid: 3920476
Johansson-Percival, A. et al. De novo induction of intratumoral lymphoid structures and vessel normalization enhances immunotherapy in resistant tumors. Nat. Immunol. 18, 1207–1217 (2017).
pubmed: 28892469
doi: 10.1038/ni.3836
GeurtsvanKessel, C. H. et al. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus-infected mice. J. Exp. Med. 206, 2339–2349 (2009).
pubmed: 19808255
pmcid: 2768850
doi: 10.1084/jem.20090410
Chelvanambi, M., Fecek, R. J., Taylor, J. L. & Storkus, W. J. STING agonist-based treatment promotes vascular normalization and tertiary lymphoid structure formation in the therapeutic melanoma microenvironment. J. Immunother. Cancer 9, e001906 (2021).
pubmed: 33526609
pmcid: 7852948
doi: 10.1136/jitc-2020-001906
Rangel-Moreno, J. et al. The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat. Immunol. 12, 639–646 (2011).
pubmed: 21666689
pmcid: 3520063
doi: 10.1038/ni.2053
Teillaud, J.-L., Regard, L., Martin, C., Sibéril, S. & Burgel, P.-R. Exploring the role of tertiary lymphoid structures using a mouse model of bacteria-infected lungs. Methods Mol. Biol. 1845, 223–239 (2018).
pubmed: 30141016
doi: 10.1007/978-1-4939-8709-2_13
Chen, L. et al. Extranodal induction of therapeutic immunity in the tumor microenvironment after intratumoral delivery of Tbet gene-modified dendritic cells. Cancer Gene Ther. 20, 469–477 (2013).
pubmed: 23846252
pmcid: 3775601
doi: 10.1038/cgt.2013.42
van Hooren, L. et al. Agonistic CD40 therapy induces tertiary lymphoid structures but impairs responses to checkpoint blockade in glioma. Nat. Commun. 12, 4127 (2021).
pubmed: 34226552
pmcid: 8257767
doi: 10.1038/s41467-021-24347-7
Boivin, G. et al. Cellular composition and contribution of tertiary lymphoid structures to tumor immune infiltration and modulation by radiation therapy. Front. Oncol. https://doi.org/10.3389/fonc.2018.00256 (2018).
doi: 10.3389/fonc.2018.00256
pubmed: 30038899
pmcid: 6046619
Sánchez-Alonso, S. et al. A new role for circulating T follicular helper cells in humoral response to anti-PD-1 therapy. J. Immunother. Cancer 8, e001187 (2020).
pubmed: 32900863
pmcid: 7478024
doi: 10.1136/jitc-2020-001187
Hollern, D. P. et al. B cells and T follicular helper cells mediate response to checkpoint inhibitors in high mutation burden mouse models of breast cancer. Cell 179, 1191–1206.e21 (2019).
pubmed: 31730857
pmcid: 6911685
doi: 10.1016/j.cell.2019.10.028
Galluzzi, L., Humeau, J., Buqué, A., Zitvogel, L. & Kroemer, G. Immunostimulation with chemotherapy in the era of immune checkpoint inhibitors. Nat. Rev. Clin. Oncol. 17, 725–741 (2020).
pubmed: 32760014
doi: 10.1038/s41571-020-0413-z
Kuwabara, S. et al. Prognostic relevance of tertiary lymphoid organs following neoadjuvant chemoradiotherapy in pancreatic ductal adenocarcinoma. Cancer Sci. 110, 1853–1862 (2019).
pubmed: 30997706
pmcid: 6549910
doi: 10.1111/cas.14023
Morcrette, G. et al. APC germline hepatoblastomas demonstrate cisplatin-induced intratumor tertiary lymphoid structures. Oncoimmunology 8, e1583547 (2019).
pubmed: 31069152
pmcid: 6492969
doi: 10.1080/2162402X.2019.1583547
Benzerdjeb, N. et al. Tertiary lymphoid structures in epithelioid malignant peritoneal mesothelioma are associated with neoadjuvant chemotherapy, but not with prognosis. Virchows Arch. https://doi.org/10.1007/s00428-021-03099-1 (2021).
doi: 10.1007/s00428-021-03099-1
pubmed: 34169365
Rückert, M., Flohr, A.-S., Hecht, M. & Gaipl, U. S. Radiotherapy and the immune system: more than just immune suppression. Stem Cell 39, 1155–1165 (2021).
doi: 10.1002/stem.3391
Di Giacomo, A. M. et al. Guadecitabine plus ipilimumab in unresectable melanoma: the NIBIT-M4 clinical trial. Clin. Cancer Res. 25, 7351–7362 (2019).
pubmed: 31530631
doi: 10.1158/1078-0432.CCR-19-1335
Chen, P.-L. et al. Analysis of immune signatures in longitudinal tumor samples yields insight into biomarkers of response and mechanisms of resistance to immune checkpoint blockade. Cancer Discov. 6, 827–837 (2016).
pubmed: 27301722
pmcid: 5082984
doi: 10.1158/2159-8290.CD-15-1545
Cindy Yang, S. Y. et al. Pan-cancer analysis of longitudinal metastatic tumors reveals genomic alterations and immune landscape dynamics associated with pembrolizumab sensitivity. Nat. Commun. 12, 5137 (2021).
pubmed: 34446728
pmcid: 8390680
doi: 10.1038/s41467-021-25432-7
Lutz, E. R. et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol. Res. 2, 616–631 (2014).
pubmed: 24942756
pmcid: 4082460
doi: 10.1158/2326-6066.CIR-14-0027
Zheng, L. et al. Vaccine-induced intratumoral lymphoid aggregates correlate with survival following treatment with a neoadjuvant and adjuvant vaccine in patients with resectable pancreatic adenocarcinoma. Clin. Cancer Res. 27, 1278–1286 (2021).
pubmed: 33277370
doi: 10.1158/1078-0432.CCR-20-2974
Maldonado, L. et al. Intramuscular therapeutic vaccination targeting HPV16 induces T cell responses that localize in mucosal lesions. Sci. Transl. Med. 6, 221ra13 (2014).
pubmed: 24477000
pmcid: 4086631
doi: 10.1126/scitranslmed.3007323
Coppola, D. et al. Unique ectopic lymph node-like structures present in human primary colorectal carcinoma are identified by immune gene array profiling. Am. J. Pathol. 179, 37–45 (2011).
pubmed: 21703392
pmcid: 3123872
doi: 10.1016/j.ajpath.2011.03.007
Mahmoud, S. M. A. et al. The prognostic significance of B lymphocytes in invasive carcinoma of the breast. Breast Cancer Res. Treat. 132, 545–553 (2012).
pubmed: 21671016
doi: 10.1007/s10549-011-1620-1
Yeong, J. et al. High densities of tumor-associated plasma cells predict improved prognosis in triple negative breast cancer. Front. Immunol. 9, 1209 (2018).
pubmed: 29899747
pmcid: 5988856
doi: 10.3389/fimmu.2018.01209
Garg, K. et al. Tumor-associated B cells in cutaneous primary melanoma and improved clinical outcome. Hum. Pathol. 54, 157–164 (2016).
pubmed: 27107457
doi: 10.1016/j.humpath.2016.03.022
Sorbye, S. W. et al. High expression of CD20
pubmed: 22720216
pmcid: 3376973
doi: 10.4161/onci.1.1.17825
Yamakoshi, Y. et al. Immunological potential of tertiary lymphoid structures surrounding the primary tumor in gastric cancer. Int. J. Oncol. 57, 171–182 (2020).
pubmed: 32319601
pmcid: 7252463
Goeppert, B. et al. Prognostic impact of tumour-infiltrating immune cells on biliary tract cancer. Br. J. Cancer 109, 2665–2674 (2013).
pubmed: 24136146
pmcid: 3833207
doi: 10.1038/bjc.2013.610
Shi, J.-Y. et al. Margin-infiltrating CD20
pubmed: 24056784
doi: 10.1158/1078-0432.CCR-12-3497
Garnelo, M. et al. Interaction between tumour-infiltrating B cells and T cells controls the progression of hepatocellular carcinoma. Gut 66, 342–351 (2017).
pubmed: 26669617
doi: 10.1136/gutjnl-2015-310814
van Herpen, C. M. L. et al. Intratumoral rhIL-12 administration in head and neck squamous cell carcinoma patients induces B cell activation. Int. J. Cancer 123, 2354–2361 (2008).
pubmed: 18729197
doi: 10.1002/ijc.23756
Milne, K. et al. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS ONE 4, e6412 (2009).
pubmed: 19641607
pmcid: 2712762
doi: 10.1371/journal.pone.0006412
Santoiemma, P. P. et al. Systematic evaluation of multiple immune markers reveals prognostic factors in ovarian cancer. Gynecol. Oncol. 143, 120–127 (2016).
pubmed: 27470997
doi: 10.1016/j.ygyno.2016.07.105
Berntsson, J., Nodin, B., Eberhard, J., Micke, P. & Jirström, K. Prognostic impact of tumour-infiltrating B cells and plasma cells in colorectal cancer. Int. J. Cancer 139, 1129–1139 (2016).
pubmed: 27074317
doi: 10.1002/ijc.30138
Edin, S. et al. The prognostic importance of CD20
pubmed: 31882709
pmcid: 6934737
doi: 10.1038/s41598-019-56441-8
Hiraoka, N. et al. Intratumoral tertiary lymphoid organ is a favourable prognosticator in patients with pancreatic cancer. Br. J. Cancer 112, 1782–1790 (2015).
pubmed: 25942397
pmcid: 4647237
doi: 10.1038/bjc.2015.145
Gu-Trantien, C. et al. CXCL13-producing TFH cells link immune suppression and adaptive memory in human breast cancer. JCI Insight 2, e91487 (2017).
pmcid: 5453706
doi: 10.1172/jci.insight.91487