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Oncology

High endothelial venules proportion in tertiary lymphoid structure is a prognostic marker and correlated with anti-tumor immune microenvironment in colorectal cancer

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Pages 114-126 | Received 08 Nov 2022, Accepted 27 Nov 2022, Published online: 12 Dec 2022

References

  • 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.
  • Zhong W, Yu Z, Zhan J, et al. Association of serum levels of CEA, CA199, CA125, CYFRA21-1 and CA72-4 and disease characteristics in colorectal cancer. Pathol Oncol Res. 2015;21(1):83–95.
  • Schrock AB, Ouyang C, Sandhu J, et al. Tumor mutational burden is predictive of response to immune checkpoint inhibitors in MSI-high metastatic colorectal cancer. Ann Oncol. 2019;30(7):1096–1103.
  • Wang F, Zhao Q, Wang YN, et al. Evaluation of POLE and POLD1 mutations as biomarkers for immunotherapy outcomes across multiple cancer types. JAMA Oncol. 2019;5(10):1504–1506.
  • Kroemer M, Turco C, Spehner L, et al. Investigation of the prognostic value of CD4 T cell subsets expanded from tumor-infiltrating lymphocytes of colorectal cancer liver metastases. J Immunother Cancer. 2020;8(2):e001478.
  • Rozek LS, Schmit SL, Greenson JK, et al. Tumor-infiltrating lymphocytes, Crohn’s-Like lymphoid reaction, and survival from colorectal cancer. J Natl Cancer Inst. 2016;108(8):djw027.
  • Li Y, Liang L, Dai W, et al. Prognostic impact of programed cell death-1 (PD-1) and PD-ligand 1 (PD-L1) expression in cancer cells and tumor infiltrating lymphocytes in colorectal cancer. Mol Cancer. 2016;15(1):55.
  • Guren MG. The global challenge of colorectal cancer. Lancet Gastroenterol Hepatol. 2019;4(12):894–895.
  • Yang Y. Cancer immunotherapy: harnessing the immune system to battle cancer. J Clin Invest. 2015;125(9):3335–3337.
  • Cabrita R, Lauss M, Sanna A, et al. Tertiary lymphoid structures improve immunotherapy and survival in melanoma. Nature. 2020;577(7791):561–565.
  • Bruno TC. New predictors for immunotherapy responses sharpen our view of the tumour microenvironment. Nature. 2020;577(7791):474–476.
  • Sautes-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.
  • Colbeck EJ, Ager A, Gallimore A, et al. Tertiary lymphoid structures in cancer: drivers of antitumor immunity, immunosuppression, or bystander sentinels in disease? Front Immunol. 2017;8(1830):1830.
  • Petitprez F, de Reynies A, Keung EZ, et al. B cells are associated with survival and immunotherapy response in sarcoma. Nature. 2020;577(7791):556–560.
  • Goc J, Fridman WH, Sautes-Fridman C, et al. Characteristics of tertiary lymphoid structures in primary cancers. Oncoimmunology. 2013;2(12):e26836.
  • Hiraoka N, Ino Y, Yamazaki-Itoh R, et al. Intratumoral tertiary lymphoid organ is a favourable prognosticator in patients with pancreatic cancer. Br J Cancer. 2015;112(11):1782–1790.
  • Girard JP, Moussion C, Forster R. HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat Rev Immunol. 2012;12(11):762–773.
  • Ivetic A, Hoskins Green HL, Hart SJ. L-selectin: a major regulator of leukocyte adhesion, migration and signaling. Front Immunol. 2019;10:1068.
  • Hong SA, Hwang HW, Kim MK, et al. High endothelial venule with concomitant high CD8+ tumor-infiltrating lymphocytes is associated with a favorable prognosis in resected gastric cancer. JCM. 2020;9(8):2628.
  • Zeng J, Eljalby M, Aryal RP, et al. Cosmc controls B cell homing. Nat Commun. 2020;11(1):3990.
  • Martinet L, Garrido I, Filleron T, et al. Human solid tumors contain high endothelial venules: association with T- and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res. 2011;71(17):5678–5687.
  • Bahmani B, Uehara M, Ordikhani F, et al. Ectopic high endothelial venules in pancreatic ductal adenocarcinoma: a unique site for targeted delivery. EBioMedicine. 2018;38:79–88.
  • He B, Jabouille A, Steri V, et al. Vascular targeting of LIGHT normalizes blood vessels in primary brain cancer and induces intratumoural high endothelial venules. J Pathol. 2018;245(2):209–221.
  • Wirsing AM, Ervik IK, Seppola M, et al. Presence of high-endothelial venules correlates with a favorable immune microenvironment in oral squamous cell carcinoma. Mod Pathol. 2018;31(6):910–922.
  • Okayama H, Kumamoto K, Saitou K, et al. Ectopic expression of MECA-79 as a novel prognostic indicator in gastric cancer. Cancer Sci. 2011;102(5):1088–1094.
  • 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 Clin Oncol. 2008;26(27):4410–4417.
  • Dieu-Nosjean MC, Goc J, Giraldo NA, et al. Tertiary lymphoid structures in cancer and beyond. Trends Immunol. 2014;35(11):571–580.
  • Bento DC, Jones E, Junaid S, et al. High endothelial venules are rare in colorectal cancers but accumulate in extra-tumoral areas with disease progression. Oncoimmunology. 2015;4(3):e974374.
  • 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. Clin Cancer Res. 2014;20(8):2147–2158.
  • Chao X, Li L, Wu M, et al. Comparison of screening strategies for lynch syndrome in patients with newly diagnosed endometrial cancer: a prospective cohort study in China. Cancer Commun (Lond). 2019;39(1):42.
  • Bistrup A, Tsay D, Shenoy P, et al. Detection of a sulfotransferase (HEC-GlcNAc6ST) in high endothelial venules of lymph nodes and in high endothelial venule-like vessels within ectopic lymphoid aggregates: relationship to the MECA-79 epitope. Am J Pathol. 2004;164(5):1635–1644.
  • He W, Zhang D, Liu H, et al. The high level of tertiary lymphoid structure is correlated with superior survival in patients with advanced gastric cancer. Front Oncol. 2020;10:980.
  • Klintrup K, Mäkinen JM, Kauppila S, et al. Inflammation and prognosis in colorectal cancer. Eur J Cancer. 2005;41(17):2645–2654.
  • Väyrynen JP, Sajanti SA, Klintrup K, et al. Characteristics and significance of colorectal cancer associated lymphoid reaction. Int J Cancer. 2014;134(9):2126–2135.
  • Choe K, Hwang Y, Seo H, et al. In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes. J Biomed Opt. 2013;18(3):036005.
  • Kennel-De March A, Béné MC, Hurault de Ligny B, et al. Enhanced expression of CD31 and CD54 on tonsillar high endothelial venules in IgA nephropathy. Clin Immunol Immunopathol. 1997;84(2):158–165.
  • Milutinovic S, Abe J, Godkin A, et al. The dual role of high endothelial venules in cancer progression versus immunity. Trends Cancer. 2021;7(3):214–225.
  • Pagès F, Kirilovsky A, Mlecnik B, et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol. 2009;27(35):5944–5951.
  • Joshi Nikhil S, Akama-Garren Elliot H, 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.
  • Sofopoulos M, Fortis SP, Vaxevanis CK, et al. The prognostic significance of peritumoral tertiary lymphoid structures in breast cancer. Cancer Immunol Immunother. 2019;68(11):1733–1745.
  • Sakimura C, Tanaka H, Okuno T, et al. B cells in tertiary lymphoid structures are associated with favorable prognosis in gastric cancer. J Surg Res. 2017;215:74–82.
  • Liu X, Tsang JYS, Hlaing T, et al. Distinct tertiary lymphoid structure associations and their prognostic relevance in HER2 positive and negative breast cancers. Oncologist. 2017;22(11):1316–1324. Epub 07/12.
  • 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.
  • 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. https://www.nature.com/articles/ni.3290#supplementary-information.
  • Martinet L, Le Guellec S, Filleron T, et al. High endothelial venules (HEVs) in human melanoma lesions: major gateways for tumor-infiltrating lymphocytes. Oncoimmunology. 2012;1(6):829–839.
  • Qian CN, Berghuis B, Tsarfaty G, et al. Preparing the “soil”: the primary tumor induces vasculature reorganization in the sentinel lymph node before the arrival of metastatic cancer cells. Cancer Res. 2006;66(21):10365–10376.
  • He B, Johansson-Percival A, Backhouse J, et al. Remodeling of metastatic vasculature reduces lung colonization and sensitizes overt metastases to immunotherapy. Cell Rep. 2020;30(3):714–724.e5.
  • Baekkevold ES, Yamanaka T, Palframan RT, et al. The Ccr7 ligand ELC (Ccl19) is transcytosed in high endothelial venules and mediates T cell recruitment. J Exp Med. 2001;193(9):1105–1112.
  • Weinstein AM, Giraldo NA, Petitprez F, et al. Association of IL-36γ with tertiary lymphoid structures and inflammatory immune infiltrates in human colorectal cancer. Cancer Immunol Immunother. 2019;68(1):109–120.
  • Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313(5795):1960–1964.
  • Freeman MR, Schneck FX, Gagnon ML, et al. Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role for T cells in angiogenesis. Cancer Res. 1995;55(18):4140–4145.
  • Menzel L, Höpken UE, Rehm A. Angiogenesis in lymph nodes is a critical regulator of immune response and lymphoma growth. Front Immunol. 2020;11:591741.
  • Qin Z, Blankenstein T. CD4+ T cell–mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells. Immunity. 2000;12(6):677–686.
  • Allen E, Jabouille A, Rivera LB, et al. Combined antiangiogenic and anti-PD-L1 therapy stimulates tumor immunity through HEV formation. Sci Transl Med. 2017;9(385):eaak9679.
  • Zhu C, Kros JM, Cheng C, et al. The contribution of tumor-associated macrophages in glioma neo-angiogenesis and implications for anti-angiogenic strategies. Neuro Oncol. 2017;19(11):1435–1446.