Generic placeholder image

Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

Research Article

Tertiary Lymphoid Structures Gene Signature Predicts Prognosis and Immune Infiltration Analysis in Head and Neck Squamous Cell Carcinoma

Author(s): Aiyan Xing, Dongxiao Lv, Changshun Wu, Kai Zhou, Tianhui Zhao, Lihua Zhao*, Huaqing Wang* and Hong Feng*

Volume 25, Issue 2, 2024

Published on: 29 January, 2024

Page: [88 - 104] Pages: 17

DOI: 10.2174/0113892029278082240118053857

Price: $65

Open Access Journals Promotions 2
Abstract

Objectives: This study aims to assess the prognostic implications of gene signature of the tertiary lymphoid structures (TLSs) in head and neck squamous cell carcinoma (HNSCC) and scrutinize the influence of TLS on immune infiltration.

Methods: Patients with HNSCC from the Cancer Genome Atlas were categorized into high/low TLS signature groups based on the predetermined TLS signature threshold. The association of the TLS signature with the immune microenvironment, driver gene mutation status, and tumor mutational load was systematically analyzed. Validation was conducted using independent datasets (GSE41613 and GSE102349).

Results: Patients with a high TLS signature score exhibited better prognosis compared to those with a low TLS signature score. The group with a high TLS signature score had significantly higher immune cell subpopulations compared to the group with a low TLS signature score. Moreover, the major immune cell subpopulations and immune circulation characteristics in the tumor immune microenvironment were positively correlated with the TLS signature. Mutational differences in driver genes were observed between the TLS signature high/low groups, primarily in the cell cycle and NRF2 signaling pathways. Patients with TP53 mutations and high TLS signature scores demonstrated a better prognosis compared to those with TP53 wild-type. In the independent cohort, the relationship between TLS signatures and patient prognosis and immune infiltration was also confirmed. Additionally, immune-related biological processes and signaling pathways were activated with elevated TLS signature.

Conclusion: High TLS signature is a promising independent prognostic factor for HNSCC patients. Immunological analysis indicated a correlation between TLS and immune cell infiltration in HNSCC. These findings provide a theoretical basis for future applications of TLS signature in HNSCC prognosis and immunotherapy.

Keywords: Tertiary lymphoid structure signature, head and neck squamous cell carcinoma, immune microenvironment, driver mutations, prognosis, TP53 mutation.

Graphical Abstract
[1]
Mandal, R.; Şenbabaoğlu, Y.; Desrichard, A.; Havel, J.J.; Dalin, M.G.; Riaz, N.; Lee, K.W.; Ganly, I.; Hakimi, A.A.; Chan, T.A.; Morris, L.G.T. The head and neck cancer immune landscape and its immunotherapeutic implications. JCI Insight, 2016, 1(17), e89829.
[http://dx.doi.org/10.1172/jci.insight.89829] [PMID: 27777979]
[2]
Chi, A.C.; Day, T.A.; Neville, B.W. Oral cavity and oropharyngeal squamous cell carcinoma—an update. CA Cancer J. Clin., 2015, 65(5), 401-421.
[http://dx.doi.org/10.3322/caac.21293] [PMID: 26215712]
[3]
Johnson, D.E.; Burtness, B.; Leemans, C.R.; Lui, V.W.Y.; Bauman, J.E.; Grandis, J.R. Head and neck squamous cell carcinoma. Nat. Rev. Dis. Primers, 2020, 6(1), 92.
[http://dx.doi.org/10.1038/s41572-020-00224-3] [PMID: 33243986]
[4]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[5]
Burtness, B.; Harrington, K.J.; Greil, R.; Soulières, D.; Tahara, M.; de Castro, G., Jr; Psyrri, A.; Basté, N.; Neupane, P.; Bratland, Å.; Fuereder, T.; Hughes, B.G.M.; Mesía, R.; Ngamphaiboon, N.; Rordorf, T.; Wan Ishak, W.Z.; Hong, R.L.; González Mendoza, R.; Roy, A.; Zhang, Y.; Gumuscu, B.; Cheng, J.D.; Jin, F.; Rischin, D.; Lerzo, G.; Tatangelo, M.; Varela, M.; Zarba, J.J.; Boyer, M.; Gan, H.; Gao, B.; Hughes, B.; Mallesara, G.; Rischin, D.; Taylor, A.; Burian, M.; Fuereder, T.; Greil, R.; Barrios, C.H.; de Castro Junior, D.O.; Castro, G.; Franke, F.A.; Girotto, G.; Lima, I.P.F.; Nicolau, U.R.; Pinto, G.D.J.; Santos, L.; Victorino, A-P.; Chua, N.; Couture, F.; Gregg, R.; Hansen, A.; Hilton, J.; McCarthy, J.; Soulieres, D.; Ascui, R.; Gonzalez, P.; Villanueva, L.; Torregroza, M.; Zambrano, A.; Holeckova, P.; Kral, Z.; Melichar, B.; Prausova, J.; Vosmik, M.; Andersen, M.; Gyldenkerne, N.; Jurgens, H.; Putnik, K.; Reinikainen, P.; Gruenwald, V.; Laban, S.; Aravantinos, G.; Boukovinas, I.; Georgoulias, V.; Psyrri, A.; Kwong, D.; Al-Farhat, Y.; Csoszi, T.; Erfan, J.; Horvai, G.; Landherr, L.; Remenar, E.; Ruzsa, A.; Szota, J.; Billan, S.; Gluck, I.; Gutfeld, O.; Popovtzer, A.; Benasso, M.; Bui, S.; Ferrari, V.; Licitra, L.; Nole, F.; Fujii, T.; Fujimoto, Y.; Hanai, N.; Hara, H.; Matsumoto, K.; Mitsugi, K.; Monden, N.; Nakayama, M.; Okami, K.; Oridate, N.; Shiga, K.; Shimizu, Y.; Sugasawa, M.; Tahara, M.; Takahashi, M.; Takahashi, S.; Tanaka, K.; Ueda, T.; Yamaguchi, H.; Yamazaki, T.; Yasumatsu, R.; Yokota, T.; Yoshizaki, T.; Kudaba, I.; Stara, Z.; Wan Ishak, W.Z.; Cheah, S.K.; Aguilar Ponce, J.; Gonzalez Mendoza, R.; Hernandez Hernandez, C.; Medina Soto, F.; Buter, J.; Hoeben, A.; Oosting, S.; Suijkerbuijk, K.; Bratland, A.; Brydoey, M.; Alvarez, R.; Mas, L.; Caguioa, P.; Querol, J.; Regala, E.E.; Tamayo, M.B.; Villegas, E.M.; Kawecki, A.; Karpenko, A.; Klochikhin, A.; Smolin, A.; Zarubenkov, O.; Goh, B.C.; Cohen, G.; du Toit, J.; Jordaan, C.; Landers, G.; Ruff, P.; Szpak, W.; Tabane, N.; Brana, I.; Iglesias Docampo, L.; Lavernia, J.; Mesia, R.; Abel, E.; Muratidu, V.; Nielsen, N.; Cristina, V.; Rordorf, T.; Rothschild, S.; Hong, R-L.; Wang, H-M.; Yang, M-H.; Yeh, S-P.; Yen, C-J.; Ngamphaiboon, N.; Soparattanapaisarn, N.; Sriuranpong, V.; Aksoy, S.; Cicin, I.; Ekenel, M.; Harputluoglu, H.; Ozyilkan, O.; Harrington, K.; Agarwala, S.; Ali, H.; Alter, R.; Anderson, D.; Bruce, J.; Burtness, B.; Campbell, N.; Conde, M.; Deeken, J.; Edenfield, W.; Feldman, L.; Gaughan, E.; Goueli, B.; Halmos, B.; Hegde, U.; Hunis, B.; Jotte, R.; Karnad, A.; Khan, S.; Laudi, N.; Laux, D.; Martincic, D.; McCune, S.; McGaughey, D.; Misiukiewicz, K.; Mulford, D.; Nadler, E.; Neupane, P.; Nunnink, J.; Ohr, J.; O’Malley, M.; Patson, B.; Paul, D.; Popa, E.; Powell, S.; Redman, R.; Rella, V.; Rocha Lima, C.; Sivapiragasam, A.; Su, Y.; Sukari, A.; Wong, S.; Yilmaz, E.; Yorio, J. Pembrolizumab alone or with chemotherapy versus cetuximab with chemotherapy for recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-048): A randomised, open-label, phase 3 study. Lancet, 2019, 394(10212), 1915-1928.
[http://dx.doi.org/10.1016/S0140-6736(19)32591-7] [PMID: 31679945]
[6]
Gomes-da-Silva, L.C.; Kepp, O.; Kroemer, G. Regulatory approval of photoimmunotherapy: Photodynamic therapy that induces immunogenic cell death. OncoImmunology, 2020, 9(1), 1841393.
[http://dx.doi.org/10.1080/2162402X.2020.1841393] [PMID: 33178498]
[7]
Amaria, R.N.; Prieto, P.A.; Tetzlaff, M.T.; Reuben, A.; Andrews, M.C.; Ross, M.I.; Glitza, I.C.; Cormier, J.; Hwu, W.J.; Tawbi, H.A.; Patel, S.P.; Lee, J.E.; Gershenwald, J.E.; Spencer, C.N.; Gopalakrishnan, V.; Bassett, R.; Simpson, L.; Mouton, R.; Hudgens, C.W.; Zhao, L.; Zhu, H.; Cooper, Z.A.; Wani, K.; Lazar, A.; Hwu, P.; Diab, A.; Wong, M.K.; McQuade, J.L.; Royal, R.; Lucci, A.; Burton, E.M.; Reddy, S.; Sharma, P.; Allison, J.; Futreal, P.A.; Woodman, S.E.; Davies, M.A.; Wargo, J.A. Neoadjuvant plus adjuvant dabrafenib and trametinib versus standard of care in patients with high-risk, surgically resectable melanoma: A single-centre, open-label, randomised, phase 2 trial. Lancet Oncol., 2018, 19(2), 181-193.
[http://dx.doi.org/10.1016/S1470-2045(18)30015-9] [PMID: 29361468]
[8]
Wusiman, D.; Li, W.; Guo, L.; Huang, Z.; Zhang, Y.; Zhang, X.; Zhao, X.; Li, L.; An, Z.; Li, Z.; Ying, J.; An, C. Comprehensive analysis of single-cell and bulk RNA-sequencing data identifies B cell marker genes signature that predicts prognosis and analysis of immune checkpoints expression in head and neck squamous cell carcinoma. Heliyon, 2023, 9(12), e22656.
[http://dx.doi.org/10.1016/j.heliyon.2023.e22656] [PMID: 38125461]
[9]
Wu, X.; Gu, Z.; Chen, Y.; Chen, B.; Chen, W.; Weng, L.; Liu, X. Application of PD-1 blockade in cancer immunotherapy. Comput. Struct. Biotechnol. J., 2019, 17, 661-674.
[http://dx.doi.org/10.1016/j.csbj.2019.03.006] [PMID: 31205619]
[10]
Gavrielatou, N.; Fortis, E.; Spathis, A.; Anastasiou, M.; Economopoulou, P.; Foukas, G.R.P.; Lelegiannis, I.M.; Rusakiewicz, S.; Vathiotis, I.; Aung, T.N.; Tissot, S.; Kastrinou, A.; Kotsantis, I.; Vagia, E.M.; Panayiotides, I.; Rimm, D.L.; Coukos, G.; Homicsko, K.; Foukas, P.; Psyrri, A. B-cell infiltration is associated with survival outcomes following programmed cell death protein 1 inhibition in head and neck squamous cell carcinoma. Ann. Oncol., 2023, S0923-7534(23)05118-9.
[http://dx.doi.org/10.1016/j.annonc.2023.12.011] [PMID: 38159908]
[11]
Borel, C.; Jung, A.C.; Burgy, M. Immunotherapy breakthroughs in the treatment of recurrent or metastatic head and neck squamous cell carcinoma. Cancers, 2020, 12(9), 2691.
[http://dx.doi.org/10.3390/cancers12092691] [PMID: 32967162]
[12]
Ferris, R.L.; Blumenschein, G., Jr; Fayette, J.; Guigay, J.; Colevas, A.D.; Licitra, L.; Harrington, K.; Kasper, S.; Vokes, E.E.; Even, C.; Worden, F.; Saba, N.F.; Iglesias Docampo, L.C.; Haddad, R.; Rordorf, T.; Kiyota, N.; Tahara, M.; Monga, M.; Lynch, M.; Geese, W.J.; Kopit, J.; Shaw, J.W.; Gillison, M.L. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N. Engl. J. Med., 2016, 375(19), 1856-1867.
[http://dx.doi.org/10.1056/NEJMoa1602252] [PMID: 27718784]
[13]
Seiwert, T.Y.; Burtness, B.; Mehra, R.; Weiss, J.; Berger, R.; Eder, J.P.; Heath, K.; McClanahan, T.; Lunceford, J.; Gause, C.; Cheng, J.D.; Chow, L.Q. Safety and clinical activity of pembrolizumab for treatment of recurrent or metastatic squamous cell carcinoma of the head and neck (KEYNOTE-012): An open-label, multicentre, phase 1b trial. Lancet Oncol., 2016, 17(7), 956-965.
[http://dx.doi.org/10.1016/S1470-2045(16)30066-3] [PMID: 27247226]
[14]
Ruffin, A.T.; Cillo, A.R.; Tabib, T.; Liu, A.; Onkar, S.; Kunning, S.R.; Lampenfeld, C.; Atiya, H.I.; Abecassis, I.; Kürten, C.H.L.; Qi, Z.; Soose, R.; Duvvuri, U.; Kim, S.; Oesterrich, S.; Lafyatis, R.; Coffman, L.G.; Ferris, R.L.; Vignali, D.A.A.; Bruno, T.C. B cell signatures and tertiary lymphoid structures contribute to outcome in head and neck squamous cell carcinoma. Nat. Commun., 2021, 12(1), 3349.
[http://dx.doi.org/10.1038/s41467-021-23355-x] [PMID: 34099645]
[15]
Economopoulou, P.; Kotsantis, I.; Psyrri, A. B cells and their role in shaping the immune response in squamous cell carcinoma of the head and neck. Immunotherapy, 2021, 13(9), 723-726.
[http://dx.doi.org/10.2217/imt-2021-0070] [PMID: 33910385]
[16]
Cabrita, R.; Lauss, M.; Sanna, A.; Donia, M.; Skaarup Larsen, M.; Mitra, S.; Johansson, I.; Phung, B.; Harbst, K.; Vallon-Christersson, J.; van Schoiack, A.; Lövgren, K.; Warren, S.; Jirström, K.; Olsson, H.; Pietras, K.; Ingvar, C.; Isaksson, K.; Schadendorf, D.; Schmidt, H.; Bastholt, L.; Carneiro, A.; Wargo, J.A.; Svane, I.M.; Jönsson, G. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature, 2020, 577(7791), 561-565.
[http://dx.doi.org/10.1038/s41586-019-1914-8] [PMID: 31942071]
[17]
Helmink, B.A.; Reddy, S.M.; Gao, J.; Zhang, S.; Basar, R.; Thakur, R.; Yizhak, K.; Sade-Feldman, M.; Blando, J.; Han, G.; Gopalakrishnan, V.; Xi, Y.; Zhao, H.; Amaria, R.N.; Tawbi, H.A.; Cogdill, A.P.; Liu, W.; LeBleu, V.S.; Kugeratski, F.G.; Patel, S.; Davies, M.A.; Hwu, P.; Lee, J.E.; Gershenwald, J.E.; Lucci, A.; Arora, R.; Woodman, S.; Keung, E.Z.; Gaudreau, P.O.; Reuben, A.; Spencer, C.N.; Burton, E.M.; Haydu, L.E.; Lazar, A.J.; Zapassodi, R.; Hudgens, C.W.; Ledesma, D.A.; Ong, S.; Bailey, M.; Warren, S.; Rao, D.; Krijgsman, O.; Rozeman, E.A.; Peeper, D.; Blank, C.U.; Schumacher, T.N.; Butterfield, L.H.; Zelazowska, M.A.; McBride, K.M.; Kalluri, R.; Allison, J.; Petitprez, F.; Fridman, W.H.; Sautès-Fridman, C.; Hacohen, N.; Rezvani, K.; Sharma, P.; Tetzlaff, M.T.; Wang, L.; Wargo, J.A. B cells and tertiary lymphoid structures promote immunotherapy response. Nature, 2020, 577(7791), 549-555.
[http://dx.doi.org/10.1038/s41586-019-1922-8] [PMID: 31942075]
[18]
Wu, Z.; Zhou, J.; Xiao, Y.; Ming, J.; Zhou, J.; Dong, F.; Zhou, X.; Xu, Z.; Zhao, X.; Lei, P.; Huang, T. CD20+CD22+ADAM28+ B cells in tertiary lymphoid structures promote immunotherapy response. Front. Immunol., 2022, 13, 865596.
[http://dx.doi.org/10.3389/fimmu.2022.865596] [PMID: 35634306]
[19]
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.; Moreira, M.; Lacroix, G.; Natario, I.; Adam, J.; Lucchesi, C.; Laizet, Y.; Toulmonde, M.; Burgess, M.A.; Bolejack, V.; Reinke, D.; Wani, K.M.; Wang, W.L.; Lazar, A.J.; Roland, C.L.; Wargo, J.A.; Italiano, A.; Sautès-Fridman, C.; Tawbi, H.A.; Fridman, W.H. B cells are associated with survival and immunotherapy response in sarcoma. Nature, 2020, 577(7791), 556-560.
[http://dx.doi.org/10.1038/s41586-019-1906-8] [PMID: 31942077]
[20]
Dieu-Nosjean, M.C.; Giraldo, N.A.; Kaplon, H.; Germain, C.; Fridman, W.H.; Sautès-Fridman, C. Tertiary lymphoid structures, drivers of the anti‐tumor responses in human cancers. Immunol. Rev., 2016, 271(1), 260-275.
[http://dx.doi.org/10.1111/imr.12405] [PMID: 27088920]
[21]
Tertiary lymphoid structures validated as biomarker.. Cancer Discov., 2023, OF1
[http://dx.doi.org/10.1158/2159-8290.CD-NB2023-0090]
[22]
Wang, X.; Juncker-Jensen, A.; Huang, G.; Nagy, M.L.; Lu, X.; Cheng, L.; Lu, X. Spatial relationship of tertiary lymphoid structures and tumor‐associated neutrophils in bladder cancer and prognostic potential for anti‐PD‐L1 immunotherapy. Cancer Commun., 2023, cac2.12491.
[http://dx.doi.org/10.1002/cac2.12491] [PMID: 37864307]
[23]
Calderaro, J.; Petitprez, F.; Becht, E.; Laurent, A.; Hirsch, T.Z.; Rousseau, B.; Luciani, A.; Amaddeo, G.; Derman, J.; Charpy, C.; Zucman-Rossi, J.; Fridman, W.H.; Sautès-Fridman, C. Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma. J. Hepatol., 2019, 70(1), 58-65.
[http://dx.doi.org/10.1016/j.jhep.2018.09.003] [PMID: 30213589]
[24]
Zhou, L.; Xu, B.; Liu, Y.; Wang, Z. Tertiary lymphoid structure signatures are associated with survival and immunotherapy response in muscle-invasive bladder cancer. OncoImmunology, 2021, 10(1), 1915574.
[http://dx.doi.org/10.1080/2162402X.2021.1915574] [PMID: 34104539]
[25]
Wood, O.; Woo, J.; Seumois, G.; Savelyeva, N.; McCann, K.J.; Singh, D.; Jones, T.; Peel, L.; Breen, M.S.; Ward, M.; Garrido Martin, E.; Sanchez-Elsner, T.; Thomas, G.; Vijayanand, P.; Woelk, C.H.; King, E.; Ottensmeier, C.; Consortium, S. Gene expression analysis of TIL rich HPV-driven head and neck tumors reveals a distinct B-cell signature when compared to HPV independent tumors. Oncotarget, 2016, 7(35), 56781-56797.
[http://dx.doi.org/10.18632/oncotarget.10788] [PMID: 27462861]
[26]
Schinke, H.; Shi, E.; Lin, Z.; Quadt, T.; Kranz, G.; Zhou, J.; Wang, H.; Hess, J.; Heuer, S.; Belka, C.; Zitzelsberger, H.; Schumacher, U.; Genduso, S.; Riecken, K.; Gao, Y.; Wu, Z.; Reichel, C.A.; Walz, C.; Canis, M.; Unger, K.; Baumeister, P.; Pan, M.; Gires, O. A transcriptomic map of EGFR-induced epithelial-to-mesenchymal transition identifies prognostic and therapeutic targets for head and neck cancer. Mol. Cancer, 2022, 21(1), 178.
[http://dx.doi.org/10.1186/s12943-022-01646-1] [PMID: 36076232]
[27]
Li, H.; Zhu, S.W.; Zhou, J.J.; Chen, D.R.; Liu, J.; Wu, Z.Z.; Wang, W.Y.; Zhang, M.J.; Sun, Z.J. Tertiary lymphoid structure raises survival and immunotherapy in HPV HNSCC. J. Dent. Res., 2023, 102(6), 678-688.
[http://dx.doi.org/10.1177/00220345231151685] [PMID: 36883630]
[28]
Shen, A.; Ye, Y.; Chen, F.; Xu, Y.; Zhang, Z.; Zhao, Q.; Zeng, Z. Integrated multi-omics analysis identifies CD73 as a prognostic biomarker and immunotherapy response predictor in head and neck squamous cell carcinoma. Front. Immunol., 2022, 13, 969034.
[http://dx.doi.org/10.3389/fimmu.2022.969034] [PMID: 36466881]
[29]
Chen, Y.; Li, Z.Y.; Zhou, G.Q.; Sun, Y. An immune-related gene prognostic index for head and neck squamous cell carcinoma. Clin. Cancer Res., 2021, 27(1), 330-341.
[http://dx.doi.org/10.1158/1078-0432.CCR-20-2166] [PMID: 33097495]
[30]
Thorsson, V.; Gibbs, D.L.; Brown, S.D.; Wolf, D.; Bortone, D.S.; Ou Yang, T.H.; Porta-Pardo, E.; Gao, G.F.; Plaisier, C.L.; Eddy, J.A.; Ziv, E.; Culhane, A.C.; Paull, E.O.; Sivakumar, I.K.A.; Gentles, A.J.; Malhotra, R.; Farshidfar, F.; Colaprico, A.; Parker, J.S.; Mose, L.E.; Vo, N.S.; Liu, J.; Liu, Y.; Rader, J.; Dhankani, V.; Reynolds, S.M.; Bowlby, R.; Califano, A.; Cherniack, A.D.; Anastassiou, D.; Bedognetti, D.; Mokrab, Y.; Newman, A.M.; Rao, A.; Chen, K.; Krasnitz, A.; Hu, H.; Malta, T.M.; Noushmehr, H.; Pedamallu, C.S.; Bullman, S.; Ojesina, A.I.; Lamb, A.; Zhou, W.; Shen, H.; Choueiri, T.K.; Weinstein, J.N.; Guinney, J.; Saltz, J.; Holt, R.A.; Rabkin, C.S.; Lazar, A.J.; Serody, J.S.; Demicco, E.G.; Disis, M.L.; Vincent, B.G.; Shmulevich, I.; Caesar-Johnson, S.J.; Demchok, J.A.; Felau, I.; Kasapi, M.; Ferguson, M.L.; Hutter, C.M.; Sofia, H.J.; Tarnuzzer, R.; Wang, Z.; Yang, L.; Zenklusen, J.C.; Zhang, J.J.; Chudamani, S.; Liu, J.; Lolla, L.; Naresh, R.; Pihl, T.; Sun, Q.; Wan, Y.; Wu, Y.; Cho, J.; DeFreitas, T.; Frazer, S.; Gehlenborg, N.; Getz, G.; Heiman, D.I.; Kim, J.; Lawrence, M.S.; Lin, P.; Meier, S.; Noble, M.S.; Saksena, G.; Voet, D.; Zhang, H.; Bernard, B.; Chambwe, N.; Dhankani, V.; Knijnenburg, T.; Kramer, R.; Leinonen, K.; Liu, Y.; Miller, M.; Reynolds, S.; Shmulevich, I.; Thorsson, V.; Zhang, W.; Akbani, R.; Broom, B.M.; Hegde, A.M.; Ju, Z.; Kanchi, R.S.; Korkut, A.; Li, J.; Liang, H.; Ling, S.; Liu, W.; Lu, Y.; Mills, G.B.; Ng, K-S.; Rao, A.; Ryan, M.; Wang, J.; Weinstein, J.N.; Zhang, J.; Abeshouse, A.; Armenia, J.; Chakravarty, D.; Chatila, W.K.; de Bruijn, I.; Gao, J.; Gross, B.E.; Heins, Z.J.; Kundra, R.; La, K.; Ladanyi, M.; Luna, A.; Nissan, M.G.; Ochoa, A.; Phillips, S.M.; Reznik, E.; Sanchez-Vega, F.; Sander, C.; Schultz, N.; Sheridan, R.; Sumer, S.O.; Sun, Y.; Taylor, B.S.; Wang, J.; Zhang, H.; Anur, P.; Peto, M.; Spellman, P.; Benz, C.; Stuart, J.M.; Wong, C.K.; Yau, C.; Hayes, D.N.; Parker, J.S.; Wilkerson, M.D.; Ally, A.; Balasundaram, M.; Bowlby, R.; Brooks, D.; Carlsen, R.; Chuah, E.; Dhalla, N.; Holt, R.; Jones, S.J.M.; Kasaian, K.; Lee, D.; Ma, Y.; Marra, M.A.; Mayo, M.; Moore, R.A.; Mungall, A.J.; Mungall, K.; Robertson, A.G.; Sadeghi, S.; Schein, J.E.; Sipahimalani, P.; Tam, A.; Thiessen, N.; Tse, K.; Wong, T.; Berger, A.C.; Beroukhim, R.; Cherniack, A.D.; Cibulskis, C.; Gabriel, S.B.; Gao, G.F.; Ha, G.; Meyerson, M.; Schumacher, S.E.; Shih, J.; Kucherlapati, M.H.; Kucherlapati, R.S.; Baylin, S.; Cope, L.; Danilova, L.; Bootwalla, M.S.; Lai, P.H.; Maglinte, D.T.; Van Den Berg, D.J.; Weisenberger, D.J.; Auman, J.T.; Balu, S.; Bodenheimer, T.; Fan, C.; Hoadley, K.A.; Hoyle, A.P.; Jefferys, S.R.; Jones, C.D.; Meng, S.; Mieczkowski, P.A.; Mose, L.E.; Perou, A.H.; Perou, C.M.; Roach, J.; Shi, Y.; Simons, J.V.; Skelly, T.; Soloway, M.G.; Tan, D.; Veluvolu, U.; Fan, H.; Hinoue, T.; Laird, P.W.; Shen, H.; Zhou, W.; Bellair, M.; Chang, K.; Covington, K.; Creighton, C.J.; Dinh, H.; Doddapaneni, H.V.; Donehower, L.A.; Drummond, J.; Gibbs, R.A.; Glenn, R.; Hale, W.; Han, Y.; Hu, J.; Korchina, V.; Lee, S.; Lewis, L.; Li, W.; Liu, X.; Morgan, M.; Morton, D.; Muzny, D.; Santibanez, J.; Sheth, M.; Shinbrot, E.; Wang, L.; Wang, M.; Wheeler, D.A.; Xi, L.; Zhao, F.; Hess, J.; Appelbaum, E.L.; Bailey, M.; Cordes, M.G.; Ding, L.; Fronick, C.C.; Fulton, L.A.; Fulton, R.S.; Kandoth, C.; Mardis, E.R.; McLellan, M.D.; Miller, C.A.; Schmidt, H.K.; Wilson, R.K.; Crain, D.; Curley, E.; Gardner, J.; Lau, K.; Mallery, D.; Morris, S.; Paulauskis, J.; Penny, R.; Shelton, C.; Shelton, T.; Sherman, M.; Thompson, E.; Yena, P.; Bowen, J.; Gastier-Foster, J.M.; Gerken, M.; Leraas, K.M.; Lichtenberg, T.M.; Ramirez, N.C.; Wise, L.; Zmuda, E.; Corcoran, N.; Costello, T.; Hovens, C.; Carvalho, A.L.; de Carvalho, A.C.; Fregnani, J.H.; Longatto-Filho, A.; Reis, R.M.; Scapulatempo-Neto, C.; Silveira, H.C.S.; Vidal, D.O.; Burnette, A.; Eschbacher, J.; Hermes, B.; Noss, A.; Singh, R.; Anderson, M.L.; Castro, P.D.; Ittmann, M.; Huntsman, D.; Kohl, B.; Le, X.; Thorp, R.; Andry, C.; Duffy, E.R.; Lyadov, V.; Paklina, O.; Setdikova, G.; Shabunin, A.; Tavobilov, M.; McPherson, C.; Warnick, R.; Berkowitz, R.; Cramer, D.; Feltmate, C.; Horowitz, N.; Kibel, A.; Muto, M.; Raut, C.P.; Malykh, A.; Barnholtz-Sloan, J.S.; Barrett, W.; Devine, K.; Fulop, J.; Ostrom, Q.T.; Shimmel, K.; Wolinsky, Y.; Sloan, A.E.; De Rose, A.; Giuliante, F.; Goodman, M.; Karlan, B.Y.; Hagedorn, C.H.; Eckman, J.; Harr, J.; Myers, J.; Tucker, K.; Zach, L.A.; Deyarmin, B.; Hu, H.; Kvecher, L.; Larson, C.; Mural, R.J.; Somiari, S.; Vicha, A.; Zelinka, T.; Bennett, J.; Iacocca, M.; Rabeno, B.; Swanson, P.; Latour, M.; Lacombe, L.; Têtu, B.; Bergeron, A.; McGraw, M.; Staugaitis, S.M.; Chabot, J.; Hibshoosh, H.; Sepulveda, A.; Su, T.; Wang, T.; Potapova, O.; Voronina, O.; Desjardins, L.; Mariani, O.; Roman-Roman, S.; Sastre, X.; Stern, M-H.; Cheng, F.; Signoretti, S.; Berchuck, A.; Bigner, D.; Lipp, E.; Marks, J.; McCall, S.; McLendon, R.; Secord, A.; Sharp, A.; Behera, M.; Brat, D.J.; Chen, A.; Delman, K.; Force, S.; Khuri, F.; Magliocca, K.; Maithel, S.; Olson, J.J.; Owonikoko, T.; Pickens, A.; Ramalingam, S.; Shin, D.M.; Sica, G.; Van Meir, E.G.; Zhang, H.; Eijckenboom, W.; Gillis, A.; Korpershoek, E.; Looijenga, L.; Oosterhuis, W.; Stoop, H.; van Kessel, K.E.; Zwarthoff, E.C.; Calatozzolo, C.; Cuppini, L.; Cuzzubbo, S.; DiMeco, F.; Finocchiaro, G.; Mattei, L.; Perin, A.; Pollo, B.; Chen, C.; Houck, J.; Lohavanichbutr, P.; Hartmann, A.; Stoehr, C.; Stoehr, R.; Taubert, H.; Wach, S.; Wullich, B.; Kycler, W.; Murawa, D.; Wiznerowicz, M.; Chung, K.; Edenfield, W.J.; Martin, J.; Baudin, E.; Bubley, G.; Bueno, R.; De Rienzo, A.; Richards, W.G.; Kalkanis, S.; Mikkelsen, T.; Noushmehr, H.; Scarpace, L.; Girard, N.; Aymerich, M.; Campo, E.; Giné, E.; Guillermo, A.L.; Van Bang, N.; Hanh, P.T.; Phu, B.D.; Tang, Y.; Colman, H.; Evason, K.; Dottino, P.R.; Martignetti, J.A.; Gabra, H.; Juhl, H.; Akeredolu, T.; Stepa, S.; Hoon, D.; Ahn, K.; Kang, K.J.; Beuschlein, F.; Breggia, A.; Birrer, M.; Bell, D.; Borad, M.; Bryce, A.H.; Castle, E.; Chandan, V.; Cheville, J.; Copland, J.A.; Farnell, M.; Flotte, T.; Giama, N.; Ho, T.; Kendrick, M.; Kocher, J-P.; Kopp, K.; Moser, C.; Nagorney, D.; O’Brien, D.; O’Neill, B.P.; Patel, T.; Petersen, G.; Que, F.; Rivera, M.; Roberts, L.; Smallridge, R.; Smyrk, T.; Stanton, M.; Thompson, R.H.; Torbenson, M.; Yang, J.D.; Zhang, L.; Brimo, F.; Ajani, J.A.; Gonzalez, A.M.A.; Behrens, C.; Bondaruk, J.; Broaddus, R.; Czerniak, B.; Esmaeli, B.; Fujimoto, J.; Gershenwald, J.; Guo, C.; Lazar, A.J.; Logothetis, C.; Meric-Bernstam, F.; Moran, C.; Ramondetta, L.; Rice, D.; Sood, A.; Tamboli, P.; Thompson, T.; Troncoso, P.; Tsao, A.; Wistuba, I.; Carter, C.; Haydu, L.; Hersey, P.; Jakrot, V.; Kakavand, H.; Kefford, R.; Lee, K.; Long, G.; Mann, G.; Quinn, M.; Saw, R.; Scolyer, R.; Shannon, K.; Spillane, A.; Stretch; Synott, M.; Thompson, J.; Wilmott, J.; Al-Ahmadie, H.; Chan, T.A.; Ghossein, R.; Gopalan, A.; Levine, D.A.; Reuter, V.; Singer, S.; Singh, B.; Tien, N.V.; Broudy, T.; Mirsaidi, C.; Nair, P.; Drwiega, P.; Miller, J.; Smith, J.; Zaren, H.; Park, J-W.; Hung, N.P.; Kebebew, E.; Linehan, W.M.; Metwalli, A.R.; Pacak, K.; Pinto, P.A.; Schiffman, M.; Schmidt, L.S.; Vocke, C.D.; Wentzensen, N.; Worrell, R.; Yang, H.; Moncrieff, M.; Goparaju, C.; Melamed, J.; Pass, H.; Botnariuc, N.; Caraman, I.; Cernat, M.; Chemencedji, I.; Clipca, A.; Doruc, S.; Gorincioi, G.; Mura, S.; Pirtac, M.; Stancul, I.; Tcaciuc, D.; Albert, M.; Alexopoulou, I.; Arnaout, A.; Bartlett, J.; Engel, J.; Gilbert, S.; Parfitt, J.; Sekhon, H.; Thomas, G.; Rassl, D.M.; Rintoul, R.C.; Bifulco, C.; Tamakawa, R.; Urba, W.; Hayward, N.; Timmers, H.; Antenucci, A.; Facciolo, F.; Grazi, G.; Marino, M.; Merola, R.; de Krijger, R.; Gimenez-Roqueplo, A-P.; Piché, A.; Chevalier, S.; McKercher, G.; Birsoy, K.; Barnett, G.; Brewer, C.; Farver, C.; Naska, T.; Pennell, N.A.; Raymond, D.; Schilero, C.; Smolenski, K.; Williams, F.; Morrison, C.; Borgia, J.A.; Liptay, M.J.; Pool, M.; Seder, C.W.; Junker, K.; Omberg, L.; Dinkin, M.; Manikhas, G.; Alvaro, D.; Bragazzi, M.C.; Cardinale, V.; Carpino, G.; Gaudio, E.; Chesla, D.; Cottingham, S.; Dubina, M.; Moiseenko, F.; Dhanasekaran, R.; Becker, K-F.; Janssen, K-P.; Slotta-Huspenina, J.; Abdel-Rahman, M.H.; Aziz, D.; Bell, S.; Cebulla, C.M.; Davis, A.; Duell, R.; Elder, J.B.; Hilty, J.; Kumar, B.; Lang, J.; Lehman, N.L.; Mandt, R.; Nguyen, P.; Pilarski, R.; Rai, K.; Schoenfield, L.; Senecal, K.; Wakely, P.; Hansen, P.; Lechan, R.; Powers, J.; Tischler, A.; Grizzle, W.E.; Sexton, K.C.; Kastl, A.; Henderson, J.; Porten, S.; Waldmann, J.; Fassnacht, M.; Asa, S.L.; Schadendorf, D.; Couce, M.; Graefen, M.; Huland, H.; Sauter, G.; Schlomm, T.; Simon, R.; Tennstedt, P.; Olabode, O.; Nelson, M.; Bathe, O.; Carroll, P.R.; Chan, J.M.; Disaia, P.; Glenn, P.; Kelley, R.K.; Landen, C.N.; Phillips, J.; Prados, M.; Simko, J.; Smith-McCune, K.; VandenBerg, S.; Roggin, K.; Fehrenbach, A.; Kendler, A.; Sifri, S.; Steele, R.; Jimeno, A.; Carey, F.; Forgie, I.; Mannelli, M.; Carney, M.; Hernandez, B.; Campos, B.; Herold-Mende, C.; Jungk, C.; Unterberg, A.; von Deimling, A.; Bossler, A.; Galbraith, J.; Jacobus, L.; Knudson, M.; Knutson, T.; Ma, D.; Milhem, M.; Sigmund, R.; Godwin, A.K.; Madan, R.; Rosenthal, H.G.; Adebamowo, C.; Adebamowo, S.N.; Boussioutas, A.; Beer, D.; Giordano, T.; Mes-Masson, A-M.; Saad, F.; Bocklage, T.; Landrum, L.; Mannel, R.; Moore, K.; Moxley, K.; Postier, R.; Walker, J.; Zuna, R.; Feldman, M.; Valdivieso, F.; Dhir, R.; Luketich, J.; Pinero, E.M.M.; Quintero-Aguilo, M.; Carlotti, C.G., Jr; Dos Santos, J.S.; Kemp, R.; Sankarankuty, A.; Tirapelli, D.; Catto, J.; Agnew, K.; Swisher, E.; Creaney, J.; Robinson, B.; Shelley, C.S.; Godwin, E.M.; Kendall, S.; Shipman, C.; Bradford, C.; Carey, T.; Haddad, A.; Moyer, J.; Peterson, L.; Prince, M.; Rozek, L.; Wolf, G.; Bowman, R.; Fong, K.M.; Yang, I.; Korst, R.; Rathmell, W.K.; Fantacone-Campbell, J.L.; Hooke, J.A.; Kovatich, A.J.; Shriver, C.D.; DiPersio, J.; Drake, B.; Govindan, R.; Heath, S.; Ley, T.; Van Tine, B.; Westervelt, P.; Rubin, M.A.; Lee, J.I.; Aredes, N.D.; Mariamidze, A. The immune landscape of cancer. Immunity, 2018, 48(4), 812-830.e14.
[http://dx.doi.org/10.1016/j.immuni.2018.03.023] [PMID: 29628290]
[31]
Wang, Q.; Zhao, Y.; Wang, F.; Tan, G. A novel immune signature predicts immunotherapy responsiveness and reveals the landscape of the tumor immune microenvironment in head and neck squamous cell carcinoma. Front. Genet., 2022, 13, 1051051.
[http://dx.doi.org/10.3389/fgene.2022.1051051] [PMID: 36437964]
[32]
Charoentong, P.; Finotello, F.; Angelova, M.; Mayer, C.; Efremova, M.; Rieder, D.; Hackl, H.; Trajanoski, Z. Pan-cancer immunogenomic analyses reveal genotype-immunophenotype relationships and predictors of response to checkpoint blockade. Cell Rep., 2017, 18(1), 248-262.
[http://dx.doi.org/10.1016/j.celrep.2016.12.019] [PMID: 28052254]
[33]
Angelova, M.; Charoentong, P.; Hackl, H.; Fischer, M.L.; Snajder, R.; Krogsdam, A.M.; Waldner, M.J.; Bindea, G.; Mlecnik, B.; Galon, J.; Trajanoski, Z. Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy. Genome Biol., 2015, 16(1), 64.
[http://dx.doi.org/10.1186/s13059-015-0620-6] [PMID: 25853550]
[34]
Karasaki, T.; Nagayama, K.; Kuwano, H.; Nitadori, J.; Sato, M.; Anraku, M.; Hosoi, A.; Matsushita, H.; Morishita, Y.; Kashiwabara, K.; Takazawa, M.; Ohara, O.; Kakimi, K.; Nakajima, J. An immunogram for the cancer-immunity cycle: Towards personalized immunotherapy of lung cancer. J. Thorac. Oncol., 2017, 12(5), 791-803.
[http://dx.doi.org/10.1016/j.jtho.2017.01.005] [PMID: 28088513]
[35]
Sautès-Fridman, C.; Petitprez, F.; Calderaro, J.; Fridman, W.H. Tertiary lymphoid structures in the era of cancer immunotherapy. Nat. Rev. Cancer, 2019, 19(6), 307-325.
[http://dx.doi.org/10.1038/s41568-019-0144-6] [PMID: 31092904]
[36]
Teillaud, J.L.; Dieu-Nosjean, M.C. Tertiary lymphoid structures: An anti-tumor school for adaptive immune cells and an antibody factory to fight cancer? Front. Immunol., 2017, 8, 830.
[http://dx.doi.org/10.3389/fimmu.2017.00830] [PMID: 28785261]
[37]
Le, X.; Ferrarotto, R.; Wise-Draper, T.; Gillison, M. Evolving role of immunotherapy in recurrent metastatic head and neck cancer. J. Natl. Compr. Canc. Netw., 2020, 18(7), 899-906.
[http://dx.doi.org/10.6004/jnccn.2020.7590] [PMID: 32634775]
[38]
Lin, W.; Chen, M.; Hong, L.; Zhao, H.; Chen, Q. Crosstalk between PD-1/PD-L1 blockade and its combinatorial therapies in tumor immune microenvironment: A focus on HNSCC. Front. Oncol., 2018, 8, 532.
[http://dx.doi.org/10.3389/fonc.2018.00532] [PMID: 30519541]
[39]
Lechner, A.; Schlößer, H.; Rothschild, S.I.; Thelen, M.; Reuter, S.; Zentis, P.; Shimabukuro-Vornhagen, A.; Theurich, S.; Wennhold, K.; Garcia-Marquez, M.; Tharun, L.; Quaas, A.; Schauss, A.; Isensee, J.; Hucho, T.; Huebbers, C.; von Bergwelt-Baildon, M.; Beutner, D. Characterization of tumor-associated T-lymphocyte subsets and immune checkpoint molecules in head and neck squamous cell carcinoma. Oncotarget, 2017, 8(27), 44418-44433.
[http://dx.doi.org/10.18632/oncotarget.17901] [PMID: 28574843]
[40]
Chen, D.S.; Mellman, I. Oncology meets immunology: The cancer-immunity cycle. Immunity, 2013, 39(1), 1-10.
[http://dx.doi.org/10.1016/j.immuni.2013.07.012] [PMID: 23890059]
[41]
Pio, R.; Ajona, D.; Ortiz-Espinosa, S.; Mantovani, A.; Lambris, J.D. Complementing the cancer-immunity cycle. Front. Immunol., 2019, 10, 774.
[http://dx.doi.org/10.3389/fimmu.2019.00774] [PMID: 31031765]
[42]
Brown, A.L.; Li, M.; Goncearenco, A.; Panchenko, A.R. Finding driver mutations in cancer: Elucidating the role of background mutational processes. PLOS Comput. Biol., 2019, 15(4), e1006981.
[http://dx.doi.org/10.1371/journal.pcbi.1006981] [PMID: 31034466]
[43]
Li, J.; Wang, W.; Zhang, Y.; Cieślik, M.; Guo, J.; Tan, M.; Green, M.D.; Wang, W.; Lin, H.; Li, W.; Wei, S.; Zhou, J.; Li, G.; Jing, X.; Vatan, L.; Zhao, L.; Bitler, B.; Zhang, R.; Cho, K.R.; Dou, Y.; Kryczek, I.; Chan, T.A.; Huntsman, D.; Chinnaiyan, A.M.; Zou, W. Epigenetic driver mutations in ARID1A shape cancer immune phenotype and immunotherapy. J. Clin. Invest., 2020, 130(5), 2712-2726.
[http://dx.doi.org/10.1172/JCI134402] [PMID: 32027624]
[44]
Leroy, B.; Anderson, M.; Soussi, T. TP53 mutations in human cancer: Database reassessment and prospects for the next decade. Hum. Mutat., 2014, 35(6), 672-688.
[http://dx.doi.org/10.1002/humu.22552] [PMID: 24665023]
[45]
Zhou, G.; Liu, Z.; Myers, J.N. TP53 mutations in head and neck squamous cell carcinoma and their impact on disease progression and treatment response. J. Cell. Biochem., 2016, 117(12), 2682-2692.
[http://dx.doi.org/10.1002/jcb.25592] [PMID: 27166782]
[46]
Feng, H.; Yang, F.; Qiao, L.; Zhou, K.; Wang, J.; Zhang, J.; Tian, T.; Du, Y.; Shangguan, H. Prognostic significance of gene signature of tertiary lymphoid structures in patients with lung adenocarcinoma. Front. Oncol., 2021, 11, 693234.
[http://dx.doi.org/10.3389/fonc.2021.693234] [PMID: 34381716]
[47]
Outh-Gauer, S.; Morini, A.; Tartour, E.; Lépine, C.; Jung, A.C.; Badoual, C. The microenvironment of head and neck cancers: Papillomavirus involvement and potential impact of immunomodulatory treatments. Head Neck Pathol., 2020, 14(2), 330-340.
[http://dx.doi.org/10.1007/s12105-020-01147-x] [PMID: 32124416]
[48]
de Ruiter, E.J.; Mulder, F.J.; Koomen, B.M.; Speel, E.J.; van den Hout, M.F.C.M.; de Roest, R.H.; Bloemena, E.; Devriese, L.A.; Willems, S.M. Comparison of three PD-L1 immunohistochemical assays in head and neck squamous cell carcinoma (HNSCC). Mod. Pathol., 2021, 34(6), 1125-1132.
[http://dx.doi.org/10.1038/s41379-020-0644-7] [PMID: 32759978]
[49]
Marletta, S.; Fusco, N.; Munari, E.; Luchini, C.; Cimadamore, A.; Brunelli, M.; Querzoli, G.; Martini, M.; Vigliar, E.; Colombari, R.; Girolami, I.; Pagni, F.; Eccher, A. Atlas of PD-L1 for pathologists: Indications, scores, diagnostic platforms and reporting systems. J. Pers. Med., 2022, 12(7), 1073.
[http://dx.doi.org/10.3390/jpm12071073] [PMID: 35887569]
[50]
Anastasiou, M.; Kyriazoglou, A.; Kotsantis, I.; Economopoulou, P.; Kyrkasiadou, M.; Giannopoulou, A.; Kosmidou, A.; Smerdi, D.; Moutafi, M.; Gavrielatou, N.; Psyrri, A. Immune checkpoint inhibitors in sarcomas: A systematic review. Immuno-Oncology and Technology, 2023, 20, 100407.
[http://dx.doi.org/10.1016/j.iotech.2023.100407] [PMID: 38192615]
[51]
Lin, Z.; Huang, L.; Li, S.; Gu, J.; Cui, X.; Zhou, Y. Pan-cancer analysis of genomic properties and clinical outcome associated with tumor tertiary lymphoid structure. Sci. Rep., 2020, 10(1), 21530.
[http://dx.doi.org/10.1038/s41598-020-78560-3] [PMID: 33299035]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy