|Table of Contents|

Research progress on the role of tertiary lymphoid structure in the prognosis and immunotherapy of patients with malignant solid tumors

Journal Of Modern Oncology[ISSN:1672-4992/CN:61-1415/R]

Issue:
2024 10
Page:
1907-1912
Research Field:
Publishing date:

Info

Title:
Research progress on the role of tertiary lymphoid structure in the prognosis and immunotherapy of patients with malignant solid tumors
Author(s):
ZHANG JinjinCHEN LinRONG Chao
Department of Pathology and Pathophysiology,School of Biology and Basic Medical Sciences,Suzhou Medical College of Soochow University,Jiangsu Suzhou 215123,China.
Keywords:
tertiary lymphoid structuresolid tumortumor immune microenvironmentimmunotherapy
PACS:
R730
DOI:
10.3969/j.issn.1672-4992.2024.10.026
Abstract:
Tertiary lymphoid structure (TLS) is a cluster of lymphocytes generated in non-lymphoid tissues such as tumor immune microenvironment due to chronic inflammation or cancer stimulation.TLS has different manifestations in different cancers and is often associated with good prognosis in most solid tumors.At present,the composition of TLS has been identified in a variety of cancers,but the selection of its markers is quite different,resulting in the lack of a unified scoring standard for judging its maturity.This article summarizes the methods and markers of related research on the basis of introducing TLS,and finds that TLS is associated with a good prognosis in most patients with malignant solid tumors,which provides a theoretical basis for us to explore prognostic markers related to immunotherapy.

References:

[1] JIANG D,ZHANG L,LIU W,et al.Trends in cancer mortality in China from 2004 to 2018:A nationwide longitudinal study [J].Cancer Commun (Lond),2021,41(10):1024-1036.
[2] DIEU-NOSJEAN MC,GOC J,GIRALDO NA,et al.Tertiary lymphoid structures in cancer and beyond [J].Trends Immunol,2014,35(11):571-580.
[3] SILINA K,SOLTERMANN A,ATTAR FM,et al.Germinal centers determine the prognostic relevance of tertiary lymphoid structures and are impaired by corticosteroids in lung squamous cell carcinoma [J].Cancer Res,2018,78(5):1308-1320.
[4] SATO Y,SILINA K,VAN DEN BROEK M,et al.The roles of tertiary lymphoid structures in chronic diseases [J].Nat Rev Nephrol,2023,19(8):525-537.
[5] WU YH,WU F,YAN GR,et al.Features and clinical significance of tertiary lymphoid structure in cutaneous squamous cell carcinoma [J].J Eur Acad Dermatol Venereol,2022,36(11):2043-2050.
[6] LIANG H,ZHANG Z,GUAN Z,et al.Follicle-like tertiary lymphoid structures:A potential biomarker for prognosis and immunotherapy response in patients with laryngeal squamous cell carcinoma [J].Front Immunol,2023,14:1096220.
[7] LI Q,LIU X,WANG D,et al.Prognostic value of tertiary lymphoid structure and tumour infiltrating lymphocytes in oral squamous cell carcinoma [J].Int J Oral Sci,2020,12(1):24.
[8] YAMAGUCHI K,ITO M,OHMURA H,et al.Helper T cell-dominant tertiary lymphoid structures are associated with disease relapse of advanced colorectal cancer [J].Oncoimmunology,2020,9(1):1724763.
[9] SEOW DYB,YEONG JPS,LIM JX,et al.Tertiary lymphoid structures and associated plasma cells play an important role in the biology of triple-negative breast cancers [J].Breast Cancer Res Treat,2020,180(2):369-377.
[10] DIEU-NOSJEAN MC,GIRALDO NA,KAPLON H,et al.Tertiary lymphoid structures,drivers of the anti-tumor responses in human cancers [J].Immunol Rev,2016,271(1):260-275.
[11] HIRAOKA N,INO Y,YAMAZAKI-ITOH R.Tertiary lymphoid organs in cancer tissues [J].Front Immunol,2016,7:244.
[12] SAUTES-FRIDMAN C,PETITPREZ F,CALDERARO J,et al.Tertiary lymphoid structures in the era of cancer immunotherapy [J].Nat Rev Cancer,2019,19(6):307-325.
[13] SCHUMACHER TN,THOMMEN DS.Tertiary lymphoid structures in cancer [J].Science,2022,375(6576):eabf9419.
[14] ZHAO H,WU L,YAN G,et al.Inflammation and tumor progression:signaling pathways and targeted intervention [J].Signal Transduct Target Ther,2021,6(1):263.
[15] DIEU-NOSJEAN MC,ANTOINE M,DANEL C,et al.Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures [J].J Clin Oncol,2008,26(27):4410-4417.
[16] GOC J,GERMAIN C,VO-BOURGAIS TK,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+ T cells [J].Cancer Res,2014,74(3):705-715.
[17] COSGROVE J,NOVKOVIC M,ALBRECHT S,et al.B cell zone reticular cell microenvironments shape CXCL13 gradient formation [J].Nat Commun,2020,11(1):3677.
[18] BLANCHARD L,GIRARD JP.High endothelial venules (HEVs) in immunity,inflammation and cancer [J].Angiogenesis,2021,24(4):719-753.
[19] RUDDLE NH.High endothelial venules and lymphatic vessels in tertiary lymphoid organs:characteristics,functions,and regulation [J].Front Immunol,2016,7:491.
[20] KRAUTLER NJ,KANA V,KRANICH J,et al.Follicular dendritic cells emerge from ubiquitous perivascular precursors [J].Cell,2012,150(1):194-206.
[21] DE CHAISEMARTIN L,GOC J,DAMOTTE D,et al.Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer [J].Cancer Res,2011,71(20):6391-6399.
[22] GERMAIN C,GNJATIC S,TAMZALIT F,et al.Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer [J].Am J Respir Crit Care Med,2014,189(7):832-844.
[23] NZULA S,GOING JJ,STOTT DI.Antigen-driven clonal proliferation,somatic hypermutation,and selection of B lymphocytes infiltrating human ductal breast carcinomas [J].Cancer Res,2003,63(12):3275-3280.
[24] ZHU W,GERMAIN C,LIU Z,et al.A high density of tertiary lymphoid structure B cells in lung tumors is associated with increased CD4(+) T cell receptor repertoire clonality [J].Oncoimmunology,2015,4(12):e1051922.
[25] JOHANSSON-PERCIVAL A,HE B,LI ZJ,et al.De novo induction of intratumoral lymphoid structures and vessel normalization enhances immunotherapy in resistant tumors [J].Nat Immunol,2017,18(11):1207-1217.
[26] GERMAIN C,GNJATIC S,DIEU-NOSJEAN MC.Tertiary lymphoid structure-associated B cells are key players in anti-tumor immunity [J].Front Immunol,2015,6:67.
[27] BANNARD O,HORTON RM,ALLEN CD,et al.Germinal center centroblasts transition to a centrocyte phenotype according to a timed program and depend on the dark zone for effective selection [J].Immunity,2013,39(5):912-924.
[28] ALLEN CD,OKADA T,CYSTER JG.Germinal-center organization and cellular dynamics [J].Immunity,2007,27(2):190-202.
[29] LING Y,ZHONG J,WENG Z,et al.The prognostic value and molecular properties of tertiary lymphoid structures in oesophageal squamous cell carcinoma [J].Clin Transl Med,2022,12(10):e1074.
[30] HOREWEG N,WORKEL HH,LOIERO D,et al.Tertiary lymphoid structures critical for prognosis in endometrial cancer patients [J].Nat Commun,2022,13(1):1373.
[31] POWELL SF,VU L,SPANOS WC,et al.The key differences between human papillomavirus-positive and-negative head and neck cancers:biological and clinical implications [J].Cancers,2021,13(20):5206.
[32] RUFFIN AT,CILLO AR,TABIB T,et al.B cell signatures and tertiary lymphoid structures contribute to outcome in head and neck squamous cell carcinoma [J].Nat Commun,2021,12(1):3349.
[33] J GUNDERSON A,RAJAMANICKAM V,BUI C,et al.Germinal center reactions in tertiary lymphoid structures associate with neoantigen burden,humoral immunity and long-term survivorship in pancreatic cancer [J].Oncoimmunology,2021,10(1):1900635.
[34] POSCH F,SILINA K,LEIBL S,et al.Maturation of tertiary lymphoid structures and recurrence of stage II and III colorectal cancer [J].Oncoimmunology,2018,7(2):e1378844.
[35] DING GY,MA JQ,YUN JP,et al.Distribution and density of tertiary lymphoid structures predict clinical outcome in intrahepatic cholangiocarcinoma [J].J Hepatol,2022,76(3):608-618.
[36] MASUDA T,TANAKA N,TAKAMATSU K,et al.Unique characteristics of tertiary lymphoid structures in kidney clear cell carcinoma:prognostic outcome and comparison with bladder cancer [J].J Immunother Cancer,2022,10(3):e003883.
[37] LIU X,TSANG JYS,HLAING T,et al.Distinct tertiary lymphoid structure associations and their prognostic relevance in HER2 positive and negative breast cancers [J].Oncologist,2017,22(11):1316-1324.
[38] DI CARO G,BERGOMAS F,GRIZZI F,et al.Occurrence of tertiary lymphoid tissue is associated with T-cell infiltration and predicts better prognosis in early-stage colorectal cancers [J].Clin Cancer Res,2014,20(8):2147-2158.
[39] MORCRETTE G,HIRSCH TZ,BADOUR E,et al.APC germline hepatoblastomas demonstrate cisplatin-induced intratumor tertiary lymphoid structures [J].Oncoimmunology,2019,8(6):e1583547.
[40] CALDERARO J,PETITPREZ F,BECHT E,et al.Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma [J].J Hepatol,2019,70(1):58-65.
[41] CABRITA R,LAUSS M,SANNA A,et al.Tertiary lymphoid structures improve immunotherapy and survival in melanoma [J].Nature,2020,577(7791):561-565.
[42] KROEGER DR,MILNE K,NELSON BH.Tumor-infiltrating plasma cells are associated with tertiary lymphoid structures,cytolytic T-cell responses,and superior prognosis in ovarian cancer [J].Clin Cancer Res,2016,22(12):3005-3015.
[43] KUWABARA S,TSUCHIKAWA T,NAKAMURA T,et al.Prognostic relevance of tertiary lymphoid organs following neoadjuvant chemoradiotherapy in pancreatic ductal adenocarcinoma [J].Cancer Sci,2019,110(6):1853-1862.
[44] PETITPREZ F,DE REYNIES A,KEUNG EZ,et al.B cells are associated with survival and immunotherapy response in sarcoma [J].Nature,2020,577(7791):556-560.
[45] FRIDMAN WH,PETITPREZ F,MEYLAN M,et al.B cells and cancer:To B or not to B[J].J Exp Med,2021,218(1):e20200851.
[46] RIBAS A,WOLCHOK JD.Cancer immunotherapy using checkpoint blockade [J].Science,2018,359(6382):1350-1355.
[47] HELMINK BA,REDDY SM,GAO J,et al.B cells and tertiary lymphoid structures promote immunotherapy response [J].Nature,2020,577(7791):549-555.
[48] MOUNZER RH,SVENDSEN OS,BALUK P,et al.Lymphotoxin-alpha contributes to lymphangiogenesis [J].Blood,2010,116(12):2173-2182.
[49] ZHANG Q,LU Y,PROULX ST,et al.Increased lymphangiogenesis in joints of mice with inflammatory arthritis [J].Arthritis Res Ther,2007,9(6):R118.
[50] LEE Y,CHIN RK,CHRISTIANSEN P,et al.Recruitment and activation of naive T cells in the islets by lymphotoxin beta receptor-dependent tertiary lymphoid structure [J].Immunity,2006,25(3):499-509.
[51] LUTHER SA,LOPEZ T,BAI W,et al.BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis [J].Immunity,2000,12(5):471-481.
[52] LUTHER SA,BIDGOL A,HARGREAVES DC,et al.Differing activities of homeostatic chemokines CCL19,CCL21,and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis [J].J Immunol,2002,169(1):424-433.
[53] STOWMAN AM,HICKMAN AW,MAULDIN IS,et al.Lymphoid aggregates in desmoplastic melanoma have features of tertiary lymphoid structures [J].Melanoma Res,2018,28(3):237-245.
[54] 章杭,沈晓燕,杨杨,等.三级淋巴结构在非小细胞肺癌中的研究进展[J].现代肿瘤医学,2017,25(13):2183-2186. ZHANG Hang,SHEN Xiaoyan,YANG Yang,et al.Advances of tertiary lymphoid structures in non-small cell lung cancer[J].Modern Oncology,2017,25(13):2183-2186.
[55] KABASHIMA K,HONDA T,GINHOUX F,et al.The immunological anatomy of the skin [J].Nat Rev Immunol,2019,19(1):19-30.
[56] JACOBSON A,YANG D,VELLA M,et al.The intestinal neuro-immune axis:crosstalk between neurons,immune cells,and microbes [J].Mucosal Immunol,2021,14(3):555-565.
[57] FRIDMAN WH,SIBERIL S,PUPIER G,et al.Activation of B cells in tertiary lymphoid structures in cancer:Anti-tumor or anti-self [J].Semin Immunol,2023,65:101703.

Memo

Memo:
National Natural Science Foundation of China(No.82103121);国家自然科学基金项目(编号:82103121);江苏省自然科学基金项目(编号:BK20200878);苏州大学大学生课外学术科研基金重点项目(编号:KY2023093A)
Last Update: 1900-01-01