The 12-CK Score: Global Measurement of Tertiary Lymphoid Structures
Open accessAbstract
There is emerging evidence that the adaptive anti-tumor activity may be orchestrated by secondary lymphoid organ-like aggregates residing in the tumor microenvironment. Known as tertiary lymphoid structures, these lymphoid aggregates serve as key outposts for lymphocyte recruitment, priming and activation. They have been linked to favorable outcomes in many tumor types, and more recently, have been shown to be effective predictors of response to immune checkpoint blockade. We have previously described a 12-chemokine (12-CK) transcriptional score which recapitulates an overwhelming enrichment for immune-related and inflammation-related genes in colorectal carcinoma. Subsequently, the 12-CK score was found to prognosticate favorable survival in multiple tumors types including melanoma, breast cancer, and bladder cancer. In the current study, we summarize the discovery and validation of the 12-CK score in various tumor types, its relationship to TLSs found within the tumor microenvironment, and explore its potential role as both a prognostic and predictive marker in the treatment of various cancers.
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CXCL10 expression has been correlated with the presence of tumor-associated tertiary lymphoid structures.
“Also, as a member of the 12-chemokine gene signature classifier33, its expression has been correlated with the presence of tumor-associated tertiary lymphoid structures50–52 which are rapidly emerging as a powerful prognostic marker in melanoma and a number of other cancer types53–55.”
From Epigenetic state determines the in vivo efficacy of STING agonist therapy (2023) · cites this paper as [52]
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PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989 · see citing works
Signatures of mutational processes in human cancer
Initiative, A. P. C. G., Alexandrov, L. B., ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, PedBrain, I., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., et al. (2013) · Nature · doi:10.1038/nature12477 · Cited by 9,660 · see citing works
Genetic Basis for Clinical Response to CTLA-4 Blockade in Melanoma
Snyder, A., Makarov, V., Merghoub, T., Yuan, J., Zaretsky, J. M., Desrichard, A., Walsh, L. A., Postow, M. A., Wong, P., Ho, T. S., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1406498 · Cited by 4,286 · see citing works
Rosenberg, J. E., Hoffman-Censits, J., Powles, T., van der Heijden, M. S., Balar, A. V., Necchi, A., Dawson, N., O'Donnell, P. H., Balmanoukian, A., Loriot, Y., et al. (2016) · The Lancet · doi:10.1016/s0140-6736(16)00561-4 · Cited by 3,669 · see citing works
B cells and tertiary lymphoid structures promote immunotherapy response
Helmink, B. A., Reddy, S. M., Gao, J., Zhang, S., Basar, R., Thakur, R., Yizhak, K., Sade-Feldman, M., Blando, J., Han, G., et al. (2020) · Nature · doi:10.1038/s41586-019-1922-8 · Cited by 2,731 · cited 4× · see citing works
“Cabrita et al. constructed a signature using hallmark TLSrelated genes (CCL19, CCL21,CXCL13, CCR7, CXCR5, SELL and LAMP3) (14), while Helmink et al. resorted to B cell related genes (MZB1, JCHAIN, IGLL5, FCRL5, IDO1, IFNG and BTLA) (15).”
BackgroundInfluentialTertiary lymphoid structures improve immunotherapy and survival in melanoma
Cabrita, R., Lauss, M., Sanna, A., Donia, M., Skaarup Larsen, M., Mitra, S., Johansson, I., Phung, B., Harbst, K., Vallon-Christersson, J., et al. (2020) · Nature · doi:10.1038/s41586-019-1914-8 · Cited by 2,374 · see citing works
Denkert, C., von Minckwitz, G., Darb-Esfahani, S., Lederer, B., Heppner, B. I., Weber, K. E., Budczies, J., Huober, J., Klauschen, F., Furlanetto, J., et al. (2018) · The Lancet Oncology · doi:10.1016/s1470-2045(17)30904-x · Cited by 2,157 · see citing works
Strimbu, K., & Tavel, J. A. (2010) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0b013e32833ed177 · Cited by 2,062 · see citing works
B cells are associated with survival and immunotherapy response in sarcoma
Petitprez, F., de Reyniès, A., Keung, E. Z., Chen, T. W.-W., Sun, C.-M., Calderaro, J., Jeng, Y.-M., Hsiao, L.-P., Lacroix, L., Bougoüin, A., et al. (2020) · Nature · doi:10.1038/s41586-019-1906-8 · Cited by 1,942 · see citing works
Tertiary lymphoid structures in the era of cancer immunotherapy
Sautès-Fridman, C., Petitprez, F., Calderaro, J., & Fridman, W. H. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0144-6 · Cited by 1,884 · see citing works
Sharma, P., Retz, M. M., Siefker-Radtke, A. O., Baron, A. D., Necchi, A., Bedke, J., Plimack, E. R., Vaena, D. A., Grimm, M., Sergio Bracarda, A., et al. (2017) · The Lancet Oncology · doi:10.1016/s1470-2045(17)30065-7 · Cited by 1,729 · see citing works
A chemokine-driven positive feedback loop organizes lymphoid follicles
Ansel, K. M., Ngo, V. N., Hyman, P. L., Luther, S. A., Förster, R., Sedgwick, J. D., Browning, J. L., Lipp, M., & Cyster, J. G. (2000) · Nature · doi:10.1038/35018581 · Cited by 1,282 · see citing works
Variants in ELL2 influencing immunoglobulin levels associate with multiple myeloma
Swaminathan, B., Þorleifsson, G., Jöud, M., Ali, M., Johnsson, E., Ajore, R., Sulem, P., Halvarsson, B.-M., Eyjolfsson, G. I., Haraldsdóttir, V., et al. (2015) · Nature Communications · doi:10.1038/ncomms8213 · Cited by 1,211 · see citing works
CD4+ follicular helper T cell infiltration predicts breast cancer survival
Gu‐Trantien, C., Loi, S., Garaud, S., Equeter, C., Libin, M., de Wind, A., Ravoet, M., Buanec, H. L., Sibille, C., Manfouo-Foutsop, G., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67428 · Cited by 1,075 · see citing works
Dieu‐Nosjean, M., Antoine, M., Danel, C. J., Heudes, D., Wislez, M., Poulot, V., Rabbe, N., Laurans, L., Tartour, É., de Chaisemartin, L., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.15.0284 · Cited by 1,033 · see citing works
Ectopic lymphoid-like structures in infection, cancer and autoimmunity
Pitzalis, C., Jones, G. W., Bombardieri, M., & Jones, S. A. (2014) · Nature reviews. Immunology · doi:10.1038/nri3700 · Cited by 700 · see citing works
Goc, J., Germain, C., Vo-Bourgais, T. K. D., Mansuet‐Lupo, A., Klein, C., Knockaert, S., de Chaisemartin, L., Ouakrim, H., Becht, É., Alifano, M., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-1342 · Cited by 675 · see citing works
OX40 Promotes Bcl-xL and Bcl-2 Expression and Is Essential for Long-Term Survival of CD4 T Cells
Rogers, P., Song, J. J., Gramaglia, I., Killeen, N. P., & Croft, M. (2001) · Immunity · doi:10.1016/s1074-7613(01)00191-1 · Cited by 645 · see citing works
Kroeger, D. R., Milne, K., & Nelson, B. H. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-2762 · Cited by 603 · see citing works
Becht, E., de Reyniès, A., Giraldo, N. A., Pilati, C., Buttard, B., Lacroix, L., Selves, J., Sautès-Fridman, C., Laurent-Puig, P., & Fridman, W. H. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-2879 · Cited by 590 · see citing works
Luther, S. A., Bidgol, A., Hargreaves, D. C., Schmidt, A., Xu, Y., Paniyadi, J., Matloubian, M., & Cyster, J. G. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.1.424 · Cited by 583 · see citing works
Martinet, L., Garrido, I., Filleron, T., Guellec, S. L., Bellard, E., Fournié, J., Rochaix, P., & Girard, J. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0431 · Cited by 523 · see citing works
Hollern, D. P., Xu, N., Thennavan, A., Glodowski, C. R., García‐Recio, S., Mott, K. R., He, X., Garay, J. P., Carey-Ewend, K., Marron, D. L., et al. (2019) · Cell · doi:10.1016/j.cell.2019.10.028 · Cited by 470 · see citing works
Luther, S. A., Lopez, T., Bai, W., Hanahan, D., & Cyster, J. G. (2000) · Immunity · doi:10.1016/s1074-7613(00)80199-5 · Cited by 468 · see citing works
Siliņa, K., Soltermann, A., Attar, F. M., Casanova, R., Uckeley, Z. M., Thut, H., Wandres, M., Isajevs, S., Cheng, P. F., Fontecedro, A. C., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-1987 · Cited by 451 · see citing works
Coppola, D., Nebozhyn, M., Khalil, F., Dai, H., Yeatman, T., Loboda, A., & Mulé, J. J. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2011.03.007 · Cited by 434 · see citing works
Self-citationMessina, J. L., Fenstermacher, D. A., Eschrich, S., Qu, X., Berglund, A. E., Lloyd, M. C., Schell, M. J., Sondak, V. K., Weber, J. S., & Mulé, J. J. (2012) · Scientific Reports · doi:10.1038/srep00765 · Cited by 426 · see citing works
Self-citationvan Dijk, N., Gil-Jimenez, A., Siliņa, K., Hendricksen, K., Smit, L. A., de Feijter, J. M., van Montfoort, M. L., van Rooijen, C. C. N., Peters, D. D. G. C., Broeks, A., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1085-z · Cited by 405 · see citing works
Maturation of tertiary lymphoid structures and recurrence of stage II and III colorectal cancer
Posch, F., Silina, K., Leibl, S., Mündlein, A., Moch, H., Siebenhüner, A., Samaras, P., Riedl, J., Stotz, M., Szkandera, J., et al. (2018) · OncoImmunology · doi:10.1080/2162402x.2017.1378844 · Cited by 380 · see citing works
Priming of naive T cells inside tumors leads to eradication of established tumors
Yu, P., Lee, Y., Liu, W., Chin, R., Wang, J. H., Wang, Y., Schietinger, A., Philip, M., Schreiber, H. W., & Fu, Y. (2004) · Nature Immunology · doi:10.1038/ni1029 · Cited by 356 · see citing works
CXCL13 is a plasma biomarker of germinal center activity
Havenar‐Daughton, C., Lindqvist, M., Heit, A., Wu, J. E., Reiss, S. M., Kendric, K. J., Bélanger, S., Kasturi, S. P., Landais, E., Akondy, R. S., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1520112113 · Cited by 343 · see citing works
Johansson, A., He, B., Li, Z.-J., Kjellén, A., Russell, K., Li, J., Larma, I., & Ganß, R. (2017) · Nature Immunology · doi:10.1038/ni.3836 · Cited by 335 · see citing works
Gao, J., Navai, N., Alhalabi, O., Siefker-Radtke, A., Campbell, M. T., Tidwell, R. S., Guo, C. C., Kamat, A. M., Matin, S. F., Araujo, J. C., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1086-y · Cited by 318 · see citing works
Browning, J. L., Allaire, N., Ngam-ek, A., Notidis, E., Hunt, J., Perrin, S., & Fava, R. A. (2005) · Immunity · doi:10.1016/j.immuni.2005.10.002 · Cited by 265 · see citing works
Neogenesis of Lymphoid Structures and Antibody Responses Occur in Human Melanoma Metastases
Cipponi, A., Mercier, M., Seremet, T., Baurain, J., Théate, I., van den Oord, J., Stas, M., Boon, T., Coulie, P. G., & van Baren, N. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1377 · Cited by 259 · see citing works
Tumor masses support naive T cell infiltration, activation, and differentiation into effectors
Thompson, E. D., Enriquez, H. L., Fu, Y., & Engelhard, V. H. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20092454 · Cited by 250 · see citing works
Montfort, A., Pearce, O. M. T., Maniati, E., Vincent, B. G., Bixby, L. M., Böhm, S., Dowe, T., Wilkes, E. H., Chakravarty, P., Thompson, R. D., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0081 · Cited by 231 · see citing works
Immune Cell Infiltration and Tertiary Lymphoid Structures as Determinants of Antitumor Immunity
Engelhard, V. H., Rodriguez, A. B., Mauldin, I. S., Woods, A. N., Peske, J. D., & Slingluff, C. L. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701269 · Cited by 230 · see citing works
Hennequin, A., Dérangère, V., Boidot, R., Apétoh, L., Vincent, J., Orry, D., Fraisse, J., Causeret, S., Martin, F., Arnould, L., et al. (2015) · OncoImmunology · doi:10.1080/2162402x.2015.1054598 · Cited by 228 · see citing works
Peske, J. D., Thompson, E. D., Gemta, L. F., Baylis, R. A., Fu, Y., & Engelhard, V. H. (2015) · Nature Communications · doi:10.1038/ncomms8114 · Cited by 227 · see citing works
Regulation of TH2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells
León, B., Ballesteros‐Tato, A., Browning, J. L., Dunn, R., Randall, T. D., & Lund, F. E. (2012) · Nature Immunology · doi:10.1038/ni.2309 · Cited by 214 · see citing works
Pfannstiel, C., Strissel, P. L., Chiappinelli, K. B., Sikic, D., Wach, S., Wirtz, R. M., Wullweber, A., Taubert, H. W., Breyer, J., Otto, W., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0758 · Cited by 210 · see citing works
Fan, Z., Yu, P., Wang, Y., Wang, Y., Fu, M. L., Liu, W., Sun, Y., & Fu, Y. (2005) · Blood · doi:10.1182/blood-2005-08-3485 · Cited by 169 · see citing works
Prabhakaran, S., Rizk, V. T., Ma, Z., Cheng, C.-H., Berglund, A. E., Coppola, D., Khalil, F., Mulé, J. J., & Soliman, H. H. (2017) · Breast Cancer Research · doi:10.1186/s13058-017-0864-z · Cited by 150 · see citing works
Self-citationSong, I. H., Heo, S.-H., Bang, W. S., Park, H. S., Park, I. A., Kim, Y.-A., Park, S. Y., Roh, J., Gong, G., & Lee, H. J. (2017) · Cancer Research and Treatment · doi:10.4143/crt.2016.215 · Cited by 143 · see citing works
Self-citationLee, H. J., Kim, J. Y., Park, I. A., Song, I. H., Yu, J. H., Ahn, J., & Gong, G. (2015) · American Journal of Clinical Pathology · doi:10.1309/ajcpixuydvz0rz3g · Cited by 128 · see citing works
Specific Immune Cell and Cytokine Characteristics of Human Testicular Germ Cell Neoplasia
Klein, B., Haggeney, T., Fietz, D., Indumathy, S., Loveland, K. L., Hedger, M., Kliesch, S., Weidner, W., Bergmann, M., & Schuppe, H.-C. (2016) · Human Reproduction · doi:10.1093/humrep/dew211 · Cited by 114 · see citing works
Langenkamp, A., Casorati, G., Garavaglia, C., Dellabona, P., Lanzavecchia, A., & Sallusto, F. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200207)32:7 · Cited by 113 · see citing works
Tamada, K., Ni, J., Zhu, G., Fiscella, M., Teng, B., van Deursen, J. M. A., & Chen, L. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.10.4832 · Cited by 93 · see citing works
CCR7: Roles in cancer cell dissemination, migration and metastasis formation
Legler, D. F., Allmen, E. U.-V., & Hauser, M. A. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.07.002 · Cited by 85 · see citing works
Targeting the Primary Tumor to Generate CTL for the Effective Eradication of Spontaneous Metastases
Yü, P., Lee, Y., Wang, Y., Liu, X., Auh, S. L., Gajewski, T. F., Schreiber, H. W., You, Z., Kaynor, C., Wang, X., et al. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.3.1960 · Cited by 79 · see citing works
Licensed human natural killer cells aid dendritic cell maturation via TNFSF14/LIGHT
Holmes, T. D., Wilson, E., Black, E. V. I., Benest, A. V., Vaz, C., Tan, B., Tanavde, V., & Cook, G. P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411072112 · Cited by 77 · see citing works
Tumour‐associated B cells in urothelial urinary bladder cancer
Zirakzadeh, A. A., Sherif, A. M., Rosenblatt, R., Bergman, E. A., Winerdal, M., Yang, D., Cederwall, J., Jakobsson, V., Hyllienmark, M., Winqvist, O., et al. (2019) · Scandinavian Journal of Immunology · doi:10.1111/sji.12830 · Cited by 52 · see citing works
Therapeutic Lymphoid Organogenesis in the Tumor Microenvironment
Weinstein, A. M., & Storkus, W. J. (2015) · Advances in cancer research · doi:10.1016/bs.acr.2015.04.003 · Cited by 51 · see citing works
Kanodia, S., Silva, D. M. D., Karamanukyan, T., Bogaert, L., Fu, Y., & Kast, W. M. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-3773 · Cited by 44 · see citing works
Coelho, F. M., Natale, D., Soriano, S. F., Hons, M., Swoger, J., Mayer, J., Danuser, R., Scandella, E., Pieczyk, M., Zerwes, H., et al. (2013) · Blood · doi:10.1182/blood-2012-10-465336 · Cited by 39 · see citing works
Badr, G. (2005) · International Immunology · doi:10.1093/intimm/dxh227 · Cited by 39 · see citing works
Miyagaki, T., Sugaya, M., Suga, H., Morimura, S., Ohmatsu, H., Fujita, H., Asano, Y., Tada, Y., Kadono, T., & Sato, S. (2012) · Journal of Investigative Dermatology · doi:10.1038/jid.2011.470 · Cited by 34 · see citing works
Ectopic Lymph Nodes Within Human Solid Tumors
Coppola, D., & Mulé, J. J. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.17.6149 · Cited by 30 · see citing works
Self-citationDendritic Cell‐Based Vaccines for Pancreatic Cancer and Melanoma
Mulé, J. J. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04936.x · Cited by 28 · see citing works
Self-citationHu, G., Liu, Y., Li, H., Zhao, D., Yang, L., Shen, J., Hong, X., Cao, X., & Wang, Q. (2010) · Cellular and Molecular Immunology · doi:10.1038/cmi.2010.15 · Cited by 11 · see citing works
Zemp, L. W., Berglund, A., Dhillon, J., Putney, R. M., Kim, Y., Jain, R., Grass, G. D., Zhang, J., Poch, M. A., Pow‐Sang, J. M., et al. (2021) · Journal of Clinical Oncology · doi:10.1200/jco.2021.39.6_suppl.466 · Cited by 4 · see citing works
Self-citationLi, R., Zemp, L. W., Berglund, A., Dhillon, J., Putney, R. M., Kim, Y., Jain, R., Grass, D., Zhang, J., Poch, M. A., et al. (2020) · Regular and Young Investigator Award Abstracts · doi:10.1136/jitc-2020-sitc2020.0068 · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
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Sorted by citations
Wang, Q., Sun, K., Liu, R., Song, Y., Lv, Y., Bi, P., Yang, F., Li, S., Zhao, J., Li, X., et al. (2023) · Clinical and Translational Medicine · doi:10.1002/ctm2.1346 · Cited by 97 · see citing works
Epigenetic state determines the in vivo efficacy of STING agonist therapy
Falahat, R., Berglund, A., Perez-Villarroel, P., Putney, R. M., Hamaidi, I., Kim, S., Pilon-Thomas, S., Barber, G. N., & Mulé, J. J. (2023) · Nature Communications · doi:10.1038/s41467-023-37217-1 · Cited by 94 · see citing works
Self-citationXu, W., Wu, Y., Liu, W., Anwaier, A., Tian, X., Su, J., Huang, H., Wei, G., Qu, Y., Zhang, H., et al. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.74647 · Cited by 78 · see citing works
Nanovaccines Fostering Tertiary Lymphoid Structure to Attack Mimicry Nasopharyngeal Carcinoma
Wen, Z., Liu, H., Qiao, D., Chen, H., Li, L., Yang, Z., Zhu, C., Zeng, Z., Chen, Y., & Liu, L. (2023) · ACS Nano · doi:10.1021/acsnano.2c09619 · Cited by 69 · see citing works
Cui, X., Gu, X., Li, D., Wu, P., Sun, N., Zhang, C., & He, J. (2025) · Cancer Letters · doi:10.1016/j.canlet.2025.217491 · Cited by 47 · see citing works
Spatial determinants of CD8+ T cell differentiation in cancer
Tooley, K., Escobar, G., & Anderson, A. C. (2022) · Trends in cancer · doi:10.1016/j.trecan.2022.04.003 · Cited by 36 · see citing works
Wang, Q., Yu, Y.-S., Wang, C.-X., Jiang, Z., Li, J.-L., Li, X.-F., Huang, X.-W., Song, Y., Li, Z.-H., Tang, S., et al. (2024) · British Journal of Cancer · doi:10.1038/s41416-024-02917-y · Cited by 38 · see citing works
Neglected no more: B cell-mediated anti-tumor immunity
Conejo-Garcia, J. R., Biswas, S., Chaurio, R. A., & Rodrı́guez, P. C. (2022) · Seminars in Immunology · doi:10.1016/j.smim.2022.101707 · Cited by 34 · see citing works
Self-citationDetection and quantitative analysis of tumor-associated tertiary lymphoid structures
Yang, M., Che, Y., Li, K., Fang, Z., Li, S., Wang, M., Zhang, Y., Zhu, X., Luo, L., Wu, C. K., et al. (2023) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2200605 · Cited by 34 · see citing works
Ahmed, J., Das, B., Shin, S. J., & Chen, A. P. (2023) · Cancers · doi:10.3390/cancers15245841 · Cited by 32 · see citing works
Radandish, M., Mashhadi, N., Aghayan, A. H., Taghizadeh, M., Salehianfard, S., Yahyazadeh, S., Vakili, O., & Igder, S. (2025) · Experimental Hematology and Oncology · doi:10.1186/s40164-025-00695-8 · Cited by 27 · see citing works
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Narvaez, D. P., Nadal, J. C., Nervo, A., Costanzo, M. V., Paletta, C., Petracci, F. E., Rivero, S. G., Ostinelli, A., Freile, B., Enrico, D. H., et al. (2024) · Cancers · doi:10.3390/cancers16020396 · Cited by 23 · see citing works
Lacinski, R. A., Dziadowicz, S. A., Melemai, V. K., Fitzpatrick, B., Pisquiy, J. J., Heim, T. E., Lohse, I., Schoedel, K. E., Llosa, N. J., Weiss, K. R., et al. (2024) · Bone Research · doi:10.1038/s41413-024-00359-z · Cited by 22 · see citing works
Li, R., Nocera, L., Rose, K. M., Raggi, D., Naidu, S. U., Mercinelli, C., Cigliola, A., Tateo, V., Patanè, D. A., Grass, G. D., et al. (2024) · European Urology Oncology · doi:10.1016/j.euo.2023.12.008 · Cited by 21 · see citing works
Self-citationBertucci, F., de Nonneville, A. T., Finetti, P., & Mamessier, É. (2023) · 癌症:英文版 · doi:10.1002/cac2.12447 · Cited by 21 · see citing works
Exploring the impact of tertiary lymphoid structures maturity in NSCLC: insights from TLS scoring
Berthe, J., Poudel, P., Segerer, F. J., Jennings, E. C., Ng, F., Surace, M. J., Andoni, A., Testori, M., Saraiya, M., Vuko, M., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1422206 · Cited by 18 · see citing works
Tertiary lymphoid structures in ovarian cancer
Sun, G., & Liu, Y. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1465516 · Cited by 18 · see citing works
Adaptive Immunity in Genitourinary Cancers
Koti, M., Bivalacqua, T. J., Black, P. C., Cathomen, T., Galsky, M. D., Gulley, J. L., Ingersoll, M. A., Kamat, A. M., Kassouf, W., Siemens, D. R., et al. (2023) · European Urology Oncology · doi:10.1016/j.euo.2023.03.002 · Cited by 17 · see citing works
Tertiary lymphoid structures: exploring opportunities to improve immunotherapy in ovarian cancer
Varghese, A., Hess, S. M., Chilakapati, S. R., Conejo-Garcia, J. R., McGray, A. R., & Zsíros, E. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1473969 · Cited by 14 · see citing works
Self-citationThe pivotal role of tertiary lymphoid structures in the tumor immune microenvironment
Liu, C., & Cao, J. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1616904 · Cited by 14 · see citing works
Gao, Z., Azar, J. H., Zhu, H., Williams-Perez, S. M., Kang, S. W., Marginean, C. E., Rubinstein, M. P., Makawita, S., Lee, H., & Camp, E. R. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1324093 · Cited by 7 · see citing works
Davidi, A. F., Shirenova, S. D., Michaelovich, D., Benedetti, G., Shtrasberg, H., Shoval, I., Hauschner, H., Oz, G., Vardy, K., Hirsh, T., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2425081122 · Cited by 7 · see citing works
Hassan, N., Michaud, E., Mansure, J. J., Farag, M. S., Kool, R., Alessa, M., Sadri, E., Cury, F., Brimo, F., Koti, M., et al. (2025) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2025.09.056 · Cited by 6 · see citing works
Monabbati, S., Fu, P., Asa, S. L., Pathak, T. B., Willis, J. E., Shi, Q., & Madabhushi, A. (2024) · Laboratory Investigation · doi:10.1016/j.labinv.2024.102168 · Cited by 6 · see citing works
Li, J.-R., Pan, L.-X., Su, J., Tian, W., Lin, L.-P., Huang, Z.-H., Luo, C., Li, Z.-Z., Ma, L., Guo, P., et al. (2026) · Hepatology Communications · doi:10.1097/hc9.0000000000000925 · Cited by 3 · see citing works
Lacinski, R. A., Dziadowicz, S. A., Roth, C., Ma, L., Melemai, V. K., Fitzpatrick, B., Chaharbakhshi, E. O., Heim, T. E., Lohse, I., Schoedel, K. E., et al. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1417459 · Cited by 3 · see citing works
Berglund, A., Puskas, J., Yoder, S., Smith, A. T., Marchion, D. C., Qin, D., Mulé, J. J., Torres–Roca, J. F., & Eschrich, S. A. (2025) · Cancer Research Communications · doi:10.1158/2767-9764.crc-24-0534 · Cited by 3 · see citing works
Self-citationThe formation and function of tertiary lymphoid structures
Zhang, C., Lv, P., Hou, Y., Yao, Z., Jiang, S., Chen, K., Liu, Z., & Liu, L. (2026) · Biomarker Research · doi:10.1186/s40364-026-00939-7 · Cited by 2 · see citing works
Tertiary lymphoid structures in breast cancer: formation, immune functions and clinical implications
Dong, W., Ai, S., Shen, X., & Yao, Y. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1827875 · Cited by 2 · see citing works
Tertiary Lymphoid Structure Formation and Function in the Tumor Microenvironment
MacFawn, I., & Bruno, T. C. (2024) · Springer eBooks · doi:10.1007/978-3-030-80962-1_83-1 · Cited by 2 · see citing works
Marwedel, B. R., Medina, L. Y., May, H. D., Adogla, J. E., Kennedy, E., Flores, E. B., Lim, E., Adams, S. F., Bartee, E., & Serda, R. E. (2024) · OncoImmunology · doi:10.1080/2162402x.2024.2421029 · Cited by 2 · see citing works
Prognostic Value of Lymphoid Infiltration and Aggregation in Cervical Cancer
Gorecki, G., Hale, M. M., Taylor, S. E., Garcia, G. L., MacFawn, I., Soong, T. R., Bruno, T. C., & Coffman, L. G. (2025) · Cancers · doi:10.3390/cancers18010129 · Cited by 1 · see citing works
cheng, C., Chen, G. P., Zhang, J., Qiu, L., Li, Z., Dong, X., Lu, C., Wu, Q., Peng, X., Cai, Z., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1818138 · Cited by 1 · see citing works
Chen, Y., Xiao, Y., Zhang, T., & Wang, X. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1784463 · Cited by 1 · see citing works
Tertiary Lymphoid Structure Formation and Function in the Tumor Microenvironment
MacFawn, I., & Bruno, T. C. (2025) · Springer eBooks · doi:10.1007/978-3-032-00761-2_83
Zheng, J., Huang, H., Li, W., Li, S., Liu, J., Lu, Z., Yan, C., & Zhang, W. (2026) · The Innovation Oncology · doi:10.59717/j.xinn-oncol.2026.100011
Li, X. B., Qin, H.-Z., Wei, J.-Y., Wei, K., & Huang, Z. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1773927
Le, S., Fang, W., Le, Y., & Zhang, L. (2026) · Cancer Medicine · doi:10.1002/cam4.72181
Yu, Y., Wang, Q., Lin, Y., Huang, K., Wang, R., Wang, J., Huang, X., Zhang, J., Chen, W., Chen, R., et al. (2026) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2026-015224
- Authors
- Li, R., Berglund, A., Zemp, L., Dhillon, J., Putney, R., Kim, Y., Jain, R. K., Grass, G. D., Conejo-Garcia, J., & Mulé, J. J.
- Affiliations
- Moffitt Cancer Center (US)
- Corresponding author
- Li, Roger
- ORCID
- Venue
- Frontiers in Immunology
- Publisher
- Frontiers Media SA
- Published
- 2021-06-29
- Volume
- 12
- Pages
- 694079-694079
- ISSN
- 1664-3224 (ISSN-L)
- PMC
- PMC8276102
- OpenAlex
- W3174070279
- Cited by
- 39
- References
- 63
- Citations by year
- 2026: 9 · 2025: 9 · 2024: 11 · 2023: 7 · 2022: 3
- FWCI
- 0.64
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Immunology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Cancer Institute
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene expression and cancer classification
- Keywords
- tertiary lymphoid structures, tumor microenvironment, chemokine expression, prognostic factors, predictive biomarkers, immune checkpoint blockade response, colorectal cancer, melanoma, breast cancer, bladder cancer
- MeSH terms
- Clinical Decision-Making, Tertiary Lymphoid Structures, Female, Humans, Immunotherapy, Male, Neoplasms, Predictive Value of Tests, Prognosis, Biomarkers, Tumor, Chemokines, Gene Expression Profiling, Tumor Microenvironment, Transcriptome
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