Tumor-Infiltrating PD-L1+ Neutrophils Induced by GM-CSF Suppress T Cell Function in Laryngeal Squamous Cell Carcinoma and Predict Unfavorable Prognosis

References

• Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi:10.3322/caac.21492
   PubMed Web of Science ®Google Scholar
• Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–132. doi:10.3322/caac.21338
   PubMed Web of Science ®Google Scholar
• Sanmamed MF, Chen L, Paradigm A. Shift in Cancer Immunotherapy: from Enhancement to Normalization. Cell. 2018;175(2):313–326. doi:10.1016/j.cell.2018.09.035
   PubMed Web of Science ®Google Scholar
• Sun C, Mezzadra R, Schumacher TN. Regulation and Function of the PD-L1 Checkpoint. Immunity. 2018;48(3):434–452. doi:10.1016/j.immuni.2018.03.014
   PubMed Web of Science ®Google Scholar
• Teng MW, Ngiow SF, Ribas A, Smyth MJ. Classifying Cancers Based on T-cell Infiltration and PD-L1. Cancer Res. 2015;75(11):2139–2145. doi:10.1158/0008-5472.CAN-15-0255
   PubMed Web of Science ®Google Scholar
• Sionov RV, Fridlender ZG, Granot Z. The Multifaceted Roles Neutrophils Play in the Tumor Microenvironment. Cancer Microenviron. 2015;8(3):125–158. doi:10.1007/s12307-014-0147-5
   PubMed Web of Science ®Google Scholar
• Ilie M, Hofman V, Ortholan C, et al. Predictive clinical outcome of the intratumoral CD66b-positive neutrophil-to-CD8-positive T-cell ratio in patients with resectable nonsmall cell lung cancer. Cancer. 2012;118(6):1726–1737. doi:10.1002/cncr.26456
   PubMed Web of Science ®Google Scholar
• Wang TT, Zhao YL, Peng LS, et al. Tumour-activated neutrophils in gastric cancer foster immune suppression and disease progression through GM-CSF-PD-L1 pathway. Gut. 2017;66(11):1900–1911. doi:10.1136/gutjnl-2016-313075
   PubMed Web of Science ®Google Scholar
• He G, Zhang H, Zhou J, et al. Peritumoural neutrophils negatively regulate adaptive immunity via the PD-L1/PD-1 signalling pathway in hepatocellular carcinoma. J Exp Clin Cancer Res. 2015;34:141. doi:10.1186/s13046-015-0256-0
   PubMed Web of Science ®Google Scholar
• Wang Y, Fang T, Huang L, et al. Neutrophils infiltrating pancreatic ductal adenocarcinoma indicate higher malignancy and worse prognosis. Biochem Biophys Res Commun. 2018;501(1):313–319. doi:10.1016/j.bbrc.2018.05.024
   PubMed Web of Science ®Google Scholar
• Trellakis S, Bruderek K, Dumitru CA, et al. Polymorphonuclear granulocytes in human head and neck cancer: enhanced inflammatory activity, modulation by cancer cells and expansion in advanced disease. Int J Cancer. 2011;129(9):2183–2193. doi:10.1002/ijc.25892
   PubMed Web of Science ®Google Scholar
• Si Y, Merz SF, Jansen P, et al. Multidimensional imaging provides evidence for down-regulation of T cell effector function by MDSC in human cancer tissue. Sci Immunol. 2019;4(40). doi:10.1126/sciimmunol.aaw9159
   PubMed Web of Science ®Google Scholar
• Zhang D, Zhou J, Tang D, et al. Neutrophil infiltration mediated by CXCL5 accumulation in the laryngeal squamous cell carcinoma microenvironment: a mechanism by which tumour cells escape immune surveillance. Clin Immunol. 2017;175:34–40. doi:10.1016/j.clim.2016.11.009
   PubMed Web of Science ®Google Scholar
• Mascolo M, Ilardi G, Merolla F, et al. Tissue microarray-based evaluation of Chromatin Assembly Factor-1 (CAF-1)/p60 as tumour prognostic marker. Int J Mol Sci. 2012;13(9):11044–11062. doi:10.3390/ijms130911044
   PubMed Web of Science ®Google Scholar
• Kargl J, Busch SE, Yang GH, et al. Neutrophils dominate the immune cell composition in non-small cell lung cancer. Nat Commun. 2017;8:14381. doi:10.1038/ncomms14381
   PubMed Web of Science ®Google Scholar
• Becher B, Tugues S, Greter M. GM-CSF: from Growth Factor to Central Mediator of Tissue Inflammation. Immunity. 2016;45(5):963–973. doi:10.1016/j.immuni.2016.10.026
   PubMed Web of Science ®Google Scholar
• Du J, Liu J, Zhang X, et al. Pre-treatment neutrophil-to-lymphocyte ratio predicts survival in patients with laryngeal cancer. Oncol Lett. 2018;15(2):1664–1672. doi:10.3892/ol.2017.7501
   PubMed Web of Science ®Google Scholar
• Kano S, Homma A, Hatakeyama H, et al. Pretreatment lymphocyte-to-monocyte ratio as an independent prognostic factor for head and neck cancer. Head Neck. 2017;39(2):247–253. doi:10.1002/hed.24576
   PubMed Web of Science ®Google Scholar
• Kara M, Uysal S, Altinisik U, Cevizci S, Guclu O, Derekoy FS. The pre-treatment neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, and red cell distribution width predict prognosis in patients with laryngeal carcinoma. Eur Arch Otorhinolaryngol. 2017;274(1):535–542. doi:10.1007/s00405-016-4250-8
   PubMed Web of Science ®Google Scholar
• Greten FR, Grivennikov SI. Inflammation and Cancer: triggers, Mechanisms, and Consequences. Immunity. 2019;51(1):27–41. doi:10.1016/j.immuni.2019.06.025
   PubMed Web of Science ®Google Scholar
• Binnewies M, Roberts EW, Kersten K, et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 2018;24(5):541–550. doi:10.1038/s41591-018-0014-x
   PubMed Web of Science ®Google Scholar
• Shalapour S, Karin M. Pas de Deux: control of Anti-tumor Immunity by Cancer-Associated Inflammation. Immunity. 2019;51(1):15–26. doi:10.1016/j.immuni.2019.06.021
   PubMed Web of Science ®Google Scholar
• Zhang X, Shi M, Chen T, Zhang B. Characterization of the Immune Cell Infiltration Landscape in Head and Neck Squamous Cell Carcinoma to Aid Immunotherapy. Mol Ther Nucleic Acids. 2020;22:298–309. doi:10.1016/j.omtn.2020.08.030
   PubMedGoogle Scholar
• Xue Y, Du HD, Tang D, et al. Correlation Between the NLRP3 Inflammasome and the Prognosis of Patients With LSCC. Front Oncol. 2019;9:588. doi:10.3389/fonc.2019.00588
   PubMed Web of Science ®Google Scholar
• Zhang D, Tang D, Heng Y, et al. Prognostic Impact of Tumor-Infiltrating Lymphocytes in Laryngeal Squamous Cell Carcinoma Patients. Laryngoscope. 2021;131(4):E1249–E1255. doi:10.1002/lary.29196
   PubMed Web of Science ®Google Scholar
• Allen CT, Clavijo PE, Van Waes C, Chen Z. Anti-Tumor Immunity in Head and Neck Cancer: understanding the Evidence, How Tumors Escape and Immunotherapeutic Approaches. Cancers. 2015;7(4):2397–2414. doi:10.3390/cancers7040900
   PubMed Web of Science ®Google Scholar
• Eruslanov EB. Phenotype and function of tumor-associated neutrophils and their subsets in early-stage human lung cancer. Cancer Immunol Immunother. 2017;66(8):997–1006. doi:10.1007/s00262-017-1976-0
   PubMed Web of Science ®Google Scholar
• Catacchio I, Scattone A, Silvestris N, Mangia A. Immune Prophets of Lung Cancer: the Prognostic and Predictive Landscape of Cellular and Molecular Immune Markers. Transl Oncol. 2018;11(3):825–835. doi:10.1016/j.tranon.2018.04.006
   PubMed Web of Science ®Google Scholar
• Wang JF, Li JB, Zhao YJ, et al. Up-regulation of programmed cell death 1 ligand 1 on neutrophils may be involved in sepsis-induced immunosuppression: an animal study and a prospective case-control study. Anesthesiology. 2015;122(4):852–863. doi:10.1097/ALN.0000000000000525
   PubMed Web of Science ®Google Scholar
• Khanna S, Graef S, Mussai F, et al. Tumor-Derived GM-CSF Promotes Granulocyte Immunosuppression in Mesothelioma Patients. Clin Cancer Res. 2018;24(12):2859–2872. doi:10.1158/1078-0432.CCR-17-3757
   PubMed Web of Science ®Google Scholar
• Hock BD, Taylor KG, Cross NB, Kettle AJ, Hampton MB, McKenzie JL. Effect of activated human polymorphonuclear leucocytes on T lymphocyte proliferation and viability. Immunology. 2012;137(3):249–258. doi:10.1111/imm.12004
   PubMed Web of Science ®Google Scholar
• Buddhisa S, Rinchai D, Ato M, Bancroft GJ, Lertmemongkolchai G. Programmed death ligand 1 on Burkholderia pseudomallei-infected human polymorphonuclear neutrophils impairs T cell functions. J Immunol. 2015;194(9):4413–4421. doi:10.4049/jimmunol.1402417
   PubMed Web of Science ®Google Scholar
• De Santo C, Arscott R, Booth S, et al. Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat Immunol. 2010;11(11):1039–1046. doi:10.1038/ni.1942
   PubMed Web of Science ®Google Scholar
• Jablonska J, Leschner S, Westphal K, Lienenklaus S, Weiss S. Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J Clin Invest. 2010;120(4):1151–1164. doi:10.1172/JCI37223
   PubMed Web of Science ®Google Scholar
• Fridlender ZG, Sun J, Kim S, et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell. 2009;16(3):183–194. doi:10.1016/j.ccr.2009.06.017
   PubMed Web of Science ®Google Scholar
• Casbon AJ, Reynaud D, Park C, et al. Invasive breast cancer reprograms early myeloid differentiation in the bone marrow to generate immunosuppressive neutrophils. Proc Natl Acad Sci U S A. 2015;112(6):E566–75. doi:10.1073/pnas.1424927112
   PubMed Web of Science ®Google Scholar
• Mishalian I, Bayuh R, Levy L, Zolotarov L, Michaeli J, Fridlender ZG. Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol Immunother. 2013;62(11):1745–1756. doi:10.1007/s00262-013-1476-9
   PubMed Web of Science ®Google Scholar
• Coffelt SB, Wellenstein MD, de Visser KE. Neutrophils in cancer: neutral no more. Nat Rev Cancer. 2016;16(7):431–446. doi:10.1038/nrc.2016.52
   PubMed Web of Science ®Google Scholar
• Mach N, Gillessen S, Wilson SB, Sheehan C, Mihm M, Dranoff G. Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 2000;60(12):3239–3246.
   PubMed Web of Science ®Google Scholar
• Salgia R, Lynch T, Skarin A, et al. Vaccination with irradiated autologous tumor cells engineered to secrete granulocyte-macrophage colony-stimulating factor augments antitumor immunity in some patients with metastatic non-small-cell lung carcinoma. J Clin Oncol. 2003;21(4):624–630. doi:10.1200/JCO.2003.03.091
   PubMed Web of Science ®Google Scholar
• Gillessen S, Naumov YN, Nieuwenhuis EE, et al. CD1d-restricted T cells regulate dendritic cell function and antitumor immunity in a granulocyte-macrophage colony-stimulating factor-dependent fashion. Proc Natl Acad Sci U S A. 2003;100(15):8874–8879. doi:10.1073/pnas.1033098100
   PubMed Web of Science ®Google Scholar
• Parmiani G, Castelli C, Pilla L, Santinami M, Colombo MP, Rivoltini L. Opposite immune functions of GM-CSF administered as vaccine adjuvant in cancer patients. Ann Oncol. 2007;18(2):226–232. doi:10.1093/annonc/mdl158
   PubMed Web of Science ®Google Scholar
• Reggiani F, Labanca V, Mancuso P, et al. Adipose Progenitor Cell Secretion of GM-CSF and MMP9 Promotes a Stromal and Immunological Microenvironment That Supports Breast Cancer Progression. Cancer Res. 2017;77(18):5169–5182. doi:10.1158/0008-5472.CAN-17-0914
   PubMed Web of Science ®Google Scholar
• Quail DF, Olson OC, Bhardwaj P, et al. Obesity alters the lung myeloid cell landscape to enhance breast cancer metastasis through IL5 and GM-CSF. Nat Cell Biol. 2017;19(8):974–987. doi:10.1038/ncb3578
   PubMed Web of Science ®Google Scholar
• Zhan Y, Lew AM, Chopin M. The Pleiotropic Effects of the GM-CSF Rheostat on Myeloid Cell Differentiation and Function: more Than a Numbers Game. Front Immunol. 2019;10:2679. doi:10.3389/fimmu.2019.02679
   PubMed Web of Science ®Google Scholar
• Eash KJ, Greenbaum AM, Gopalan PK, Link DC. CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J Clin Invest. 2010;120(7):2423–2431. doi:10.1172/JCI41649
   PubMed Web of Science ®Google Scholar
• Zhou SL, Dai Z, Zhou ZJ, et al. Overexpression of CXCL5 mediates neutrophil infiltration and indicates poor prognosis for hepatocellular carcinoma. Hepatology. 2012;56(6):2242–2254. doi:10.1002/hep.25907
   PubMed Web of Science ®Google Scholar
• Chao T, Furth EE, Vonderheide RH. CXCR2-Dependent Accumulation of Tumor-Associated Neutrophils Regulates T-cell Immunity in Pancreatic Ductal Adenocarcinoma. Cancer Immunol Res. 2016;4(11):968–982. doi:10.1158/2326-6066.CIR-16-0188
   PubMed Web of Science ®Google Scholar
• Nywening TM, Belt BA, Cullinan DR, et al. Targeting both tumour-associated CXCR2(+) neutrophils and CCR2(+) macrophages disrupts myeloid recruitment and improves chemotherapeutic responses in pancreatic ductal adenocarcinoma. Gut. 2018;67(6):1112–1123. doi:10.1136/gutjnl-2017-313738
   PubMed Web of Science ®Google Scholar