Research progress of tertiary lymphoid structure in prognosis and immunotherapy of esophageal squamous cell carcinoma_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

NIU Zhenyi ¹ , JIN Runsen ¹ , YAN Kepeng ² , ZHANG Yan ² ,  LI Hecheng ¹

1. Department of Thoracic Surgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, P. R. China;
2. Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, P. R. China;

Corresponding author：

LI Hecheng, Email: lihecheng2000@hotmail.com

Keywords：

Esophageal squamous cell carcinoma; tertiary lymphoid structure; immunotherapy; review

DOI：

10.7507/1007-4848.202403018

Video：

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Abstract Full text Figures/Tables Video References Cited by

Esophageal squamous cell carcinoma is the main histological type of esophageal cancer in China, which seriously threatens the health of people. The application of immunotherapy, mainly immune checkpoint inhibitors, has greatly improved the prognosis of patients with esophageal squamous cell carcinoma, but the efficacy of treatment is still limited. Tertiary lymphoid structure (TLS) is an ectopic organized lymphoid structure that accumulates in non-lymphoid organs. Previous studies have found that TLS in esophageal squamous cell carcinoma is associated with better patient outcomes and enhanced immunotherapy efficacy. Based on current researches about TLS in esophageal squamous cell carcinoma, this paper reviews the relationship between TLS and the prognosis and immunotherapy of patients. We hope to provide reference for the precise immunotherapy of esophageal squamous cell carcinoma.

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3.	Zheng RS, Chen R, Han BF, et al. Cancer incidence and mortality in China, 2022. Zhonghua Zhong Liu Za Zhi, 2024, 46(3): 221-231.
4.	Yan Y, Feng X, Li C, et al. Treatments for resectable esophageal cancer: from traditional systemic therapy to immunotherapy. Chin Med J (Engl), 2022, 135(18): 2143-2156.
5.	Kraehenbuehl L, Weng CH, Eghbali S, et al. Enhancing immunotherapy in cancer by targeting emerging immunomodulatory pathways. Nat Rev Clin Oncol, 2022, 19(1): 37-50.
6.	Bejarano L, Jordāo MJC, Joyce JA. Therapeutic targeting of the tumor microenvironment. Cancer Discov, 2021, 11(4): 933-959.
7.	Lauss M, Donia M, Svane IM, et al. B cells and tertiary lymphoid structures: Friends or foes in cancer immunotherapy. Clin Cancer Res, 2022, 28(9): 1751-1758.
8.	Fukuhara M, Muto S, Inomata S, et al. The clinical significance of tertiary lymphoid structure and its relationship with peripheral blood characteristics in patients with surgically resected non-small cell lung cancer: A single-center, retrospective study. Cancer Immunol Immunother, 2022, 71(5): 1129-1137.
9.	Wang Q, Sun K, Liu R, et al. Single-cell transcriptome sequencing of B-cell heterogeneity and tertiary lymphoid structure predicts breast cancer prognosis and neoadjuvant therapy efficacy. Clin Transl Med, 2023, 13(8): e1346.
10.	Wang Q, Shen X, An R, et al. Peritumoral tertiary lymphoid structure and tumor stroma percentage predict the prognosis of patients with non-metastatic colorectal cancer. Front Immunol, 2022, 13: 962056.
11.	Horeweg N, Workel HH, Loiero D, et al. Tertiary lymphoid structures critical for prognosis in endometrial cancer patients. Nat Commun, 2022, 13(1): 1373.
12.	Cabrita R, Lauss M, Sanna A, et al. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature, 2020, 577(7791): 561-565.
13.	Helmink BA, Reddy SM, Gao J, et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature, 2020, 577(7791): 549-555.
14.	Petitprez F, de Reyniès A, Keung EZ, et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature, 2020, 577(7791): 556-560.
15.	Fridman WH, Meylan M, Pupier G, et al. Tertiary lymphoid structures and B cells: An intratumoral immunity cycle. Immunity, 2023, 56(10): 2254-2269.
16.	Gu-Trantien C, Loi S, Garaud S, et al. CD4⁺ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest, 2013, 123(7): 2873-2892.
17.	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. Cancer Res, 2014, 74(3): 705-715.
18.	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. Clin Cancer Res, 2016, 22(12): 3005-3015.
19.	Hennequin A, Derangère V, Boidot R, et al. Tumor infiltration by Tbet+ effector T cells and CD20+ B cells is associated with survival in gastric cancer patients. Oncoimmunology, 2015, 5(2): e1054598.
20.	Barone F, Gardner DH, Nayar S, et al. Stromal fibroblasts in tertiary lymphoid structures: A novel target in chronic inflammation. Front Immunol, 2016, 7: 477.
21.	Sato Y, Silina K, van den Broek M, et al. The roles of tertiary lymphoid structures in chronic diseases. Nat Rev Nephrol, 2023, 19(8): 525-537.
22.	Bressan D, Battistoni G, Hannon GJ. The dawn of spatial omics. Science, 2023, 381(6657): eabq4964.
23.	Li R, Huang X, Yang W, et al. Tertiary lymphoid structures favor outcome in resected esophageal squamous cell carcinoma. J Pathol Clin Res, 2022, 8(5): 422-435.
24.	Ling Y, Zhong J, Weng Z, et al. The prognostic value and molecular properties of tertiary lymphoid structures in oesophageal squamous cell carcinoma. Clin Transl Med, 2022, 12(10): e1074.
25.	Nakamura S, Ohuchida K, Hayashi M, et al. Tertiary lymphoid structures correlate with enhancement of antitumor immunity in esophageal squamous cell carcinoma. Br J Cancer, 2023, 129(8): 1314-1326.
26.	李梅, 王燕妮, 陈曦, 等. 食管鳞癌中三级淋巴结构的表达特征及临床意义. 肿瘤综合治疗电子杂志, 2023, 9(4): 27-33.
27.	Rakaee M, Kilvaer TK, Jamaly S, et al. Tertiary lymphoid structure score: A promising approach to refine the TNM staging in resected non-small cell lung cancer. Br J Cancer, 2021, 124(10): 1680-1689.
28.	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 Hepatol, 2019, 70(1): 58-65.
29.	Ukita M, Hamanishi J, Yoshitomi H, et al. CXCL13-producing CD4+ T cells accumulate in the early phase of tertiary lymphoid structures in ovarian cancer. JCI Insight, 2022, 7(12): e157215.
30.	Figenschau SL, Fismen S, Fenton KA, et al. Tertiary lymphoid structures are associated with higher tumor grade in primary operable breast cancer patients. BMC Cancer, 2015, 15: 101.
31.	Joshi NS, Akama-Garren EH, Lu Y, et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity, 2015, 43(3): 579-590.
32.	Finkin S, Yuan D, Stein I, et al. Ectopic lymphoid structures function as microniches for tumor progenitor cells in hepatocellular carcinoma. Nat Immunol, 2015, 16(12): 1235-1244.
33.	Sautès-Fridman C, Petitprez F, Calderaro J, et al. Tertiary lymphoid structures in the era of cancer immunotherapy. Nat Rev Cancer, 2019, 19(6): 307-325.
34.	Hayashi Y, Makino T, Sato E, et al. Density and maturity of peritumoral tertiary lymphoid structures in oesophageal squamous cell carcinoma predicts patient survival and response to immune checkpoint inhibitors. Br J Cancer, 2023, 128(12): 2175-2185.
35.	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. Oncoimmunology, 2015, 4(12): e1051922.
36.	Bruno TC. New predictors for immunotherapy responses sharpen our view of the tumour microenvironment. Nature, 2020, 577(7791): 474-476.
37.	Pan C, Wang Y, Liu Q, et al. Phenotypic profiling and prognostic significance of immune infiltrates in esophageal squamous cell carcinoma. Oncoimmunology, 2021, 10(1): 1883890.
38.	Meylan M, Petitprez F, Becht E, et al. Tertiary lymphoid structures generate and propagate anti-tumor antibody-producing plasma cells in renal cell cancer. Immunity, 2022, 55(3): 527-541.
39.	Sharonov GV, Serebrovskaya EO, Yuzhakova DV, et al. B cells, plasma cells and antibody repertoires in the tumour microenvironment. Nat Rev Immunol, 2020, 20(5): 294-307.
40.	Adler LN, Jiang W, Bhamidipati K, et al. The other function: ClassⅡ-restricted antigen presentation by B cells. Front Immunol, 2017, 8: 319.
41.	Bruno TC, Ebner PJ, Moore BL, et al. Antigen-presenting intratumoral B cells affect CD4+ TIL phenotypes in non-small cell lung cancer patients. Cancer Immunol Res, 2017, 5(10): 898-907.
42.	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. Nat Commun, 2021, 12(1): 3349.
43.	Wu HX, Pan YQ, He Y, et al. Clinical benefit of first-line programmed death-1 antibody plus chemotherapy in low programmed cell death ligand 1-expressing esophageal squamous cell carcinoma: A post hoc analysis of JUPITER-06 and meta-analysis. J Clin Oncol, 2023, 41(9): 1735-1746.
44.	Ng KW, Boumelha J, Enfield KSS, et al. Antibodies against endogenous retroviruses promote lung cancer immunotherapy. Nature, 2023, 616(7957): 563-573.
45.	Italiano A, Bessede A, Pulido M, et al. Pembrolizumab in soft-tissue sarcomas with tertiary lymphoid structures: A phase 2 PEMBROSARC trial cohort. Nat Med, 2022, 28(6): 1199-1206.
46.	Chow A, Perica K, Klebanoff CA, et al. Clinical implications of T cell exhaustion for cancer immunotherapy. Nat Rev Clin Oncol, 2022, 19(12): 775-790.
47.	Miller BC, Sen DR, Al Abosy R, et al. Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade. Nat Immunol, 2019, 20(3): 326-336.
48.	Siddiqui I, Schaeuble K, Chennupati V, et al. Intratumoral Tcf1+PD-1+CD8+ T cells with stem-like properties promote tumor control in response to vaccination and checkpoint blockade immunotherapy. Immunity, 2019, 50(1): 195-211.
49.	He R, Hou S, Liu C, et al. Follicular CXCR5- expressing CD8(+) T cells curtail chronic viral infection. Nature, 2016, 537(7620): 412-428.
50.	Im SJ, Hashimoto M, Gerner MY, et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature, 2016, 537(7620): 417-421.
51.	Wu T, Ji Y, Moseman EA, et al. The TCF1-Bcl6 axis counteracts type Ⅰ interferon to repress exhaustion and maintain T cell stemness. Sci Immunol, 2016, 1(6): eaai8593.
52.	Kallies A, Zehn D, Utzschneider DT. Precursor exhausted T cells: Key to successful immunotherapy? Nat Rev Immunol, 2020, 20(2): 128-136.
53.	Giles JR, Globig AM, Kaech SM, et al. CD8+ T cells in the cancer-immunity cycle. Immunity, 2023, 56(10): 2231-2253.
54.	Utzschneider DT, Charmoy M, Chennupati V, et al. T cell factor 1-expressing memory-like CD8(+) T cells sustain the immune response to chronic viral infections. Immunity, 2016, 45(2): 415-427.
55.	Sade-Feldman M, Yizhak K, Bjorgaard SL, et al. Defining T cell states associated with response to checkpoint immunotherapy in melanoma. Cell, 2019, 176(1-2): 404.
56.	Zheng L, Qin S, Si W, et al. Pan-cancer single-cell landscape of tumor-infiltrating T cells. Science, 2021, 374(6574): abe6474.
57.	Liu B, Hu X, Feng K, et al. Temporal single-cell tracing reveals clonal revival and expansion of precursor exhausted T cells during anti-PD-1 therapy in lung cancer. Nat Cancer, 2022, 3(1): 108-121.
58.	Thommen DS, Koelzer VH, Herzig P, et al. A transcriptionally and functionally distinct PD-1+ CD8+ T cell pool with predictive potential in non-small-cell lung cancer treated with PD-1 blockade. Nat Med, 2018, 24(7): 994-1004.
59.	Oliveira G, Stromhaug K, Klaeger S, et al. Phenotype, specificity and avidity of antitumour CD8+ T cells in melanoma. Nature, 2021, 596(7870): 119-125.
60.	Caushi JX, Zhang J, Ji Z, et al. Transcriptional programs of neoantigen-specific TIL in anti-PD-1-treated lung cancers. Nature, 2021, 596(7870): 126-132.
61.	Liu Z, Zhang Y, Ma N, et al. Progenitor-like exhausted SPRY1+CD8+ T cells potentiate responsiveness to neoadjuvant PD-1 blockade in esophageal squamous cell carcinoma. Cancer Cell, 2023, 41(11): 1852-1870.
62.	Remark R, Lupo A, Alifano M, et al. Immune contexture and histological response after neoadjuvant chemotherapy predict clinical outcome of lung cancer patients. Oncoimmunology, 2016, 5(12): e1255394.
63.	Siliņa 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. Cancer Res, 2018, 78(5): 1308-1320.
64.	Brunet M, Crombé A, Cousin S, et al. Mature tertiary lymphoid structure is a specific biomarker of cancer immunotherapy and does not predict outcome to chemotherapy in non-small-cell lung cancer. Ann Oncol, 2022, 33(10): 1084-1085.
65.	Fehrenbacher L, Spira A, Ballinger M, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): A multicentre, open-label, phase 2 randomised controlled trial. Lancet, 2016, 387(10030): 1837-1846.
66.	Patil NS, Nabet BY, Müller S, et al. Intratumoral plasma cells predict outcomes to PD-L1 blockade in non-small cell lung cancer. Cancer Cell, 2022, 40(3): 289-300.

1. Sung H, Ferlay J, Siegel RL, et al. 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.
2. GBD 2017 Oesophageal Cancer Collaborators. The global, regional, and national burden of oesophageal cancer and its attributable risk factors in 195 countries and territories, 1990-2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol, 2020, 5(6): 582-597.
3. Zheng RS, Chen R, Han BF, et al. Cancer incidence and mortality in China, 2022. Zhonghua Zhong Liu Za Zhi, 2024, 46(3): 221-231.
4. Yan Y, Feng X, Li C, et al. Treatments for resectable esophageal cancer: from traditional systemic therapy to immunotherapy. Chin Med J (Engl), 2022, 135(18): 2143-2156.
5. Kraehenbuehl L, Weng CH, Eghbali S, et al. Enhancing immunotherapy in cancer by targeting emerging immunomodulatory pathways. Nat Rev Clin Oncol, 2022, 19(1): 37-50.
6. Bejarano L, Jordāo MJC, Joyce JA. Therapeutic targeting of the tumor microenvironment. Cancer Discov, 2021, 11(4): 933-959.
7. Lauss M, Donia M, Svane IM, et al. B cells and tertiary lymphoid structures: Friends or foes in cancer immunotherapy. Clin Cancer Res, 2022, 28(9): 1751-1758.
8. Fukuhara M, Muto S, Inomata S, et al. The clinical significance of tertiary lymphoid structure and its relationship with peripheral blood characteristics in patients with surgically resected non-small cell lung cancer: A single-center, retrospective study. Cancer Immunol Immunother, 2022, 71(5): 1129-1137.
9. Wang Q, Sun K, Liu R, et al. Single-cell transcriptome sequencing of B-cell heterogeneity and tertiary lymphoid structure predicts breast cancer prognosis and neoadjuvant therapy efficacy. Clin Transl Med, 2023, 13(8): e1346.
10. Wang Q, Shen X, An R, et al. Peritumoral tertiary lymphoid structure and tumor stroma percentage predict the prognosis of patients with non-metastatic colorectal cancer. Front Immunol, 2022, 13: 962056.
11. Horeweg N, Workel HH, Loiero D, et al. Tertiary lymphoid structures critical for prognosis in endometrial cancer patients. Nat Commun, 2022, 13(1): 1373.
12. Cabrita R, Lauss M, Sanna A, et al. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature, 2020, 577(7791): 561-565.
13. Helmink BA, Reddy SM, Gao J, et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature, 2020, 577(7791): 549-555.
14. Petitprez F, de Reyniès A, Keung EZ, et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature, 2020, 577(7791): 556-560.
15. Fridman WH, Meylan M, Pupier G, et al. Tertiary lymphoid structures and B cells: An intratumoral immunity cycle. Immunity, 2023, 56(10): 2254-2269.
16. Gu-Trantien C, Loi S, Garaud S, et al. CD4⁺ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest, 2013, 123(7): 2873-2892.
17. 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. Cancer Res, 2014, 74(3): 705-715.
18. 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. Clin Cancer Res, 2016, 22(12): 3005-3015.
19. Hennequin A, Derangère V, Boidot R, et al. Tumor infiltration by Tbet+ effector T cells and CD20+ B cells is associated with survival in gastric cancer patients. Oncoimmunology, 2015, 5(2): e1054598.
20. Barone F, Gardner DH, Nayar S, et al. Stromal fibroblasts in tertiary lymphoid structures: A novel target in chronic inflammation. Front Immunol, 2016, 7: 477.
21. Sato Y, Silina K, van den Broek M, et al. The roles of tertiary lymphoid structures in chronic diseases. Nat Rev Nephrol, 2023, 19(8): 525-537.
22. Bressan D, Battistoni G, Hannon GJ. The dawn of spatial omics. Science, 2023, 381(6657): eabq4964.
23. Li R, Huang X, Yang W, et al. Tertiary lymphoid structures favor outcome in resected esophageal squamous cell carcinoma. J Pathol Clin Res, 2022, 8(5): 422-435.
24. Ling Y, Zhong J, Weng Z, et al. The prognostic value and molecular properties of tertiary lymphoid structures in oesophageal squamous cell carcinoma. Clin Transl Med, 2022, 12(10): e1074.
25. Nakamura S, Ohuchida K, Hayashi M, et al. Tertiary lymphoid structures correlate with enhancement of antitumor immunity in esophageal squamous cell carcinoma. Br J Cancer, 2023, 129(8): 1314-1326.
26. 李梅, 王燕妮, 陈曦, 等. 食管鳞癌中三级淋巴结构的表达特征及临床意义. 肿瘤综合治疗电子杂志, 2023, 9(4): 27-33.
27. Rakaee M, Kilvaer TK, Jamaly S, et al. Tertiary lymphoid structure score: A promising approach to refine the TNM staging in resected non-small cell lung cancer. Br J Cancer, 2021, 124(10): 1680-1689.
28. 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 Hepatol, 2019, 70(1): 58-65.
29. Ukita M, Hamanishi J, Yoshitomi H, et al. CXCL13-producing CD4+ T cells accumulate in the early phase of tertiary lymphoid structures in ovarian cancer. JCI Insight, 2022, 7(12): e157215.
30. Figenschau SL, Fismen S, Fenton KA, et al. Tertiary lymphoid structures are associated with higher tumor grade in primary operable breast cancer patients. BMC Cancer, 2015, 15: 101.
31. Joshi NS, Akama-Garren EH, Lu Y, et al. Regulatory T cells in tumor-associated tertiary lymphoid structures suppress anti-tumor T cell responses. Immunity, 2015, 43(3): 579-590.
32. Finkin S, Yuan D, Stein I, et al. Ectopic lymphoid structures function as microniches for tumor progenitor cells in hepatocellular carcinoma. Nat Immunol, 2015, 16(12): 1235-1244.
33. Sautès-Fridman C, Petitprez F, Calderaro J, et al. Tertiary lymphoid structures in the era of cancer immunotherapy. Nat Rev Cancer, 2019, 19(6): 307-325.
34. Hayashi Y, Makino T, Sato E, et al. Density and maturity of peritumoral tertiary lymphoid structures in oesophageal squamous cell carcinoma predicts patient survival and response to immune checkpoint inhibitors. Br J Cancer, 2023, 128(12): 2175-2185.
35. 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. Oncoimmunology, 2015, 4(12): e1051922.
36. Bruno TC. New predictors for immunotherapy responses sharpen our view of the tumour microenvironment. Nature, 2020, 577(7791): 474-476.
37. Pan C, Wang Y, Liu Q, et al. Phenotypic profiling and prognostic significance of immune infiltrates in esophageal squamous cell carcinoma. Oncoimmunology, 2021, 10(1): 1883890.
38. Meylan M, Petitprez F, Becht E, et al. Tertiary lymphoid structures generate and propagate anti-tumor antibody-producing plasma cells in renal cell cancer. Immunity, 2022, 55(3): 527-541.
39. Sharonov GV, Serebrovskaya EO, Yuzhakova DV, et al. B cells, plasma cells and antibody repertoires in the tumour microenvironment. Nat Rev Immunol, 2020, 20(5): 294-307.
40. Adler LN, Jiang W, Bhamidipati K, et al. The other function: ClassⅡ-restricted antigen presentation by B cells. Front Immunol, 2017, 8: 319.
41. Bruno TC, Ebner PJ, Moore BL, et al. Antigen-presenting intratumoral B cells affect CD4+ TIL phenotypes in non-small cell lung cancer patients. Cancer Immunol Res, 2017, 5(10): 898-907.
42. 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. Nat Commun, 2021, 12(1): 3349.
43. Wu HX, Pan YQ, He Y, et al. Clinical benefit of first-line programmed death-1 antibody plus chemotherapy in low programmed cell death ligand 1-expressing esophageal squamous cell carcinoma: A post hoc analysis of JUPITER-06 and meta-analysis. J Clin Oncol, 2023, 41(9): 1735-1746.
44. Ng KW, Boumelha J, Enfield KSS, et al. Antibodies against endogenous retroviruses promote lung cancer immunotherapy. Nature, 2023, 616(7957): 563-573.
45. Italiano A, Bessede A, Pulido M, et al. Pembrolizumab in soft-tissue sarcomas with tertiary lymphoid structures: A phase 2 PEMBROSARC trial cohort. Nat Med, 2022, 28(6): 1199-1206.
46. Chow A, Perica K, Klebanoff CA, et al. Clinical implications of T cell exhaustion for cancer immunotherapy. Nat Rev Clin Oncol, 2022, 19(12): 775-790.
47. Miller BC, Sen DR, Al Abosy R, et al. Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade. Nat Immunol, 2019, 20(3): 326-336.
48. Siddiqui I, Schaeuble K, Chennupati V, et al. Intratumoral Tcf1+PD-1+CD8+ T cells with stem-like properties promote tumor control in response to vaccination and checkpoint blockade immunotherapy. Immunity, 2019, 50(1): 195-211.
49. He R, Hou S, Liu C, et al. Follicular CXCR5- expressing CD8(+) T cells curtail chronic viral infection. Nature, 2016, 537(7620): 412-428.
50. Im SJ, Hashimoto M, Gerner MY, et al. Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy. Nature, 2016, 537(7620): 417-421.
51. Wu T, Ji Y, Moseman EA, et al. The TCF1-Bcl6 axis counteracts type Ⅰ interferon to repress exhaustion and maintain T cell stemness. Sci Immunol, 2016, 1(6): eaai8593.
52. Kallies A, Zehn D, Utzschneider DT. Precursor exhausted T cells: Key to successful immunotherapy? Nat Rev Immunol, 2020, 20(2): 128-136.
53. Giles JR, Globig AM, Kaech SM, et al. CD8+ T cells in the cancer-immunity cycle. Immunity, 2023, 56(10): 2231-2253.
54. Utzschneider DT, Charmoy M, Chennupati V, et al. T cell factor 1-expressing memory-like CD8(+) T cells sustain the immune response to chronic viral infections. Immunity, 2016, 45(2): 415-427.
55. Sade-Feldman M, Yizhak K, Bjorgaard SL, et al. Defining T cell states associated with response to checkpoint immunotherapy in melanoma. Cell, 2019, 176(1-2): 404.
56. Zheng L, Qin S, Si W, et al. Pan-cancer single-cell landscape of tumor-infiltrating T cells. Science, 2021, 374(6574): abe6474.
57. Liu B, Hu X, Feng K, et al. Temporal single-cell tracing reveals clonal revival and expansion of precursor exhausted T cells during anti-PD-1 therapy in lung cancer. Nat Cancer, 2022, 3(1): 108-121.
58. Thommen DS, Koelzer VH, Herzig P, et al. A transcriptionally and functionally distinct PD-1+ CD8+ T cell pool with predictive potential in non-small-cell lung cancer treated with PD-1 blockade. Nat Med, 2018, 24(7): 994-1004.
59. Oliveira G, Stromhaug K, Klaeger S, et al. Phenotype, specificity and avidity of antitumour CD8+ T cells in melanoma. Nature, 2021, 596(7870): 119-125.
60. Caushi JX, Zhang J, Ji Z, et al. Transcriptional programs of neoantigen-specific TIL in anti-PD-1-treated lung cancers. Nature, 2021, 596(7870): 126-132.
61. Liu Z, Zhang Y, Ma N, et al. Progenitor-like exhausted SPRY1+CD8+ T cells potentiate responsiveness to neoadjuvant PD-1 blockade in esophageal squamous cell carcinoma. Cancer Cell, 2023, 41(11): 1852-1870.
62. Remark R, Lupo A, Alifano M, et al. Immune contexture and histological response after neoadjuvant chemotherapy predict clinical outcome of lung cancer patients. Oncoimmunology, 2016, 5(12): e1255394.
63. Siliņa 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. Cancer Res, 2018, 78(5): 1308-1320.
64. Brunet M, Crombé A, Cousin S, et al. Mature tertiary lymphoid structure is a specific biomarker of cancer immunotherapy and does not predict outcome to chemotherapy in non-small-cell lung cancer. Ann Oncol, 2022, 33(10): 1084-1085.
65. Fehrenbacher L, Spira A, Ballinger M, et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): A multicentre, open-label, phase 2 randomised controlled trial. Lancet, 2016, 387(10030): 1837-1846.
66. Patil NS, Nabet BY, Müller S, et al. Intratumoral plasma cells predict outcomes to PD-L1 blockade in non-small cell lung cancer. Cancer Cell, 2022, 40(3): 289-300.

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