PD-1/PD-L1-Associated Immunoarchitectural Patterns Stratify Pancreatic Cancer Patients into Prognostic/Predictive Subgroups.
Journal
Cancer immunology research
ISSN: 2326-6074
Titre abrégé: Cancer Immunol Res
Pays: United States
ID NLM: 101614637
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
22
02
2021
revised:
21
05
2021
accepted:
10
09
2021
pubmed:
17
9
2021
medline:
17
3
2022
entrez:
16
9
2021
Statut:
ppublish
Résumé
Immunotherapy, including PD-1/PD-L1 agonists, has shown limited efficacy in pancreatic ductal adenocarcinoma (PDAC). We examined the PD-1/PD-L1 expression and immunoarchitectural features by automated morphometric analysis using multiplex immunofluorescence and 118 microsatellite-stable, treatment-naïve, surgically resected PDACs (study cohort). Five microsatellite-instable cases were stained in parallel (MSI cohort). Molecular analysis was additionally performed. An independent PDAC cohort (
Identifiants
pubmed: 34526323
pii: 2326-6066.CIR-21-0144
doi: 10.1158/2326-6066.CIR-21-0144
doi:
Substances chimiques
Antibodies, Monoclonal
0
B7-H1 Antigen
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1439-1450Informations de copyright
©2021 American Association for Cancer Research.
Références
Beatty GL, Eghbali S, Kim R. Deploying immunotherapy in pancreatic cancer: defining mechanisms of response and resistance. Am Soc Clin Oncol Educ Book. 2017;37:267–78.
Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366:2455–65.
Aglietta M, Barone C, Sawyer MB, Moore MJ, Miller WH Jr, Bagalà C, et al. A phase I dose escalation trial of tremelimumab (CP-675,206) in combination with gemcitabine in chemotherapy-naive patients with metastatic pancreatic cancer. Ann Oncol. 2014;25:1750–5.
Balachandran VP, Beatty GL, Dougan SK. Broadening the impact of immunotherapy to pancreatic cancer: challenges and opportunities. Gastroenterology. 2019;156:2056–72.
Sahin IH, Askan G, Hu ZI, O'Reilly EM. Immunotherapy in pancreatic ductal adenocarcinoma: an emerging entity?. Ann Oncol. 2017;28:2950–61.
Lutz ER, Wu AA, Bigelow E, Sharma R, Mo G, Soares K, et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol Res. 2014;2:616–31.
Taube JM, Galon J, Sholl LM, Rodig SJ, Cottrell TR, Giraldo NA, et al. Implications of the tumor immune microenvironment for staging and therapeutics. Mod Pathol. 2018;31:214–34.
Gajewski TF, Schreiber H, Fu YX. Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol. 2013;14:1014–22.
Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol. 2011;29:235–71.
Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012;4:127–37.
Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest. 2014;94:107–16.
Cimino-Mathews A, Thompson E, Taube JM, Ye X, Lu Y, Meeker A, et al. PD-L1 (B7-H1) expression and the immune tumor microenvironment in primary and metastatic breast carcinomas. Hum Pathol. 2016;47:52–63.
Yanik EL, Kaunitz GJ, Cottrell TR, Succaria F, McMiller TL, Ascierto ML, et al. Association of HIV status with local immune response to anal squamous cell carcinoma: implications for immunotherapy. JAMA Oncol. 2017;3:974–8.
Topalian SL, Taube JM, Anders RA, Pardoll DM. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 2016;16:275–87.
Xu C, Fillmore CM, Koyama S, Wu H, Zhao Y, Chen Z, et al. Loss of Lkb1 and Pten leads to lung squamous cell carcinoma with elevated PD-L1 expression. Cancer Cell. 2014;25:590–604.
Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med. 2007;13:84–8.
Van Allen EM, Golay HG, Liu Y, Koyama S, Wong K, Taylor-Weiner A, et al. Long-term benefit of PD-L1 blockade in lung cancer associated with JAK3 activation. Cancer Immunol Res. 2015;3:855–63.
Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12:252–64.
Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint Blockade. N Engl J Med. 2018;378:158–68.
Vasaturo A, Galon J. Multiplexed immunohistochemistry for immune cell phenotyping, quantification and spatial distribution in situ. Methods Enzymol. 2020;635:51–66.
Wartenberg M, Cibin S, Zlobec I, Vassella E, Eppenberger-Castori S, Terracciano L, et al. Integrated genomic and immunophenotypic classification of pancreatic cancer reveals three distinct subtypes with prognostic/predictive significance. Clin Cancer Res. 2018;24:4444–54.
Mahajan UM, Langhoff E, Goni E, Costello E, Greenhalf W, Halloran C, et al. Immune cell and stromal signature associated with progression-free survival of patients with resected pancreatic ductal adenocarcinoma. Gastroenterology. 2018;155:1625–39.
Carstens JL, Correa de Sampaio P, Yang D, Barua S, Wang H, Rao A, et al. Spatial computation of intratumoral T cells correlates with survival of patients with pancreatic cancer. Nat Commun. 2017;8:15095.
Stromnes IM, Hulbert A, Pierce RH, Greenberg PD, Hingorani SR. T-cell localization, activation, and clonal expansion in human pancreatic ductal adenocarcinoma. Cancer Immunol Res. 2017;5:978–1.
Bailey P, Chang DK, Nones K, Johns AL, Patch AM, Gingras MC, et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature. 2016;531:47–52.
Riquelme E, Zhang Y, Zhang L, Montiel M, Zoltan M, Dong W, et al. Tumor microbiome diversity and composition influence pancreatic cancer outcomes. Cell. 2019;178:795–806.
Puleo F, Nicolle R, Blum Y, Cros J, Marisa L, Demetter P, et al. Stratification of pancreatic ductal adenocarcinomas based on tumor and microenvironment features. Gastroenterology. 2018;155:1999–2013.
Balachandran VP, Łuksza M, Zhao JN, Makarov V, Moral JA, Remark R, et al. Identification of unique neoantigen qualities in long-term survivors of pancreatic cancer. Nature. 2017;551:512–6.
Cristescu R, Mogg R, Ayers M, Murphy E, Yearley J, Sher X, et al. Pan-tumor genomic biomarkers for PD-1 checkpoint blockade-based immunotherapy. Science. 2018;362:eaar3593.
Tumeh PC, Harview CL, Yearley JH, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515:568–71.
Ambler R, Edmunds GL, Tan SL, Cirillo S, Pernes JI, Ruan X, et al. PD-1 suppresses the maintenance of cell couples between cytotoxic T cells and target tumor cells within the tumor. Sci Signal. 2020;13:eaau4518.
Burrack AL, Spartz EJ, Raynor JF, Wang I, Olson M, Stromnes IM. Combination PD-1 and PD-L1 blockade promotes durable neoantigen-specific T cell-mediated immunity in pancreatic ductal adenocarcinoma. Cell Rep. 2019;28:2140–55.
Liudahl SM, Betts CB, Sivagnanam S, Morales-Oyarvide V, da Silva A, Yuan C, et al. Leukocyte heterogeneity in pancreatic ductal adenocarcinoma: phenotypic and spatial features associated with clinical outcome. Cancer Discov. 2021;11:2014–31.
Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, et al. PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors. J Clin Invest. 2014;124:2246–59.
Collier JL, Weiss SA, Pauken KE, Sen DR, Sharpe AH. Not-so-opposite ends of the spectrum: CD8+ T cell dysfunction across chronic infection, cancer and autoimmunity. Nat Immunol. 2021;22:809–19.
Kim HD, Song GW, Park S, Jung MK, Kim MH, Kang HJ, et al. Association between expression level of PD1 by tumor-infiltrating CD8+ T cells and features of hepatocellular carcinoma. Gastroenterology. 2018;155:1936–50.
Menard LC, Fischer P, Kakrecha B, Linsley PS, Wambre E, Liu MC, et al. Renal cell carcinoma (RCC) tumors display large expansion of double positive (DP) CD4+CD8+ T cells with expression of exhaustion markers. Front Immunol. 2018;9:2728.
Danilova L, Ho WJ, Zhu Q, Vithayathil T, De Jesus-Acosta A, Azad NS, et al. Programmed cell death ligand-1 (PD-L1) and CD8 expression profiling identify an immunologic subtype of pancreatic ductal adenocarcinomas with favorable survival. Cancer Immunol Res. 2019;7:886–95.
Vonderheide RH. The immune revolution: a case for priming, not checkpoint. Cancer Cell. 2018;33:563–9.
Morrison AH, Diamond MS, Hay CA, Byrne KT, Vonderheide RH. Sufficiency of CD40 activation and immune checkpoint blockade for T cell priming and tumor immunity. Proc Natl Acad Sci U S A. 2020;117:8022–31.
Long X, Cheng Q, Liang H, Zhao J, Wang J, Wang W, et al. Memory CD4+ T cells are suppressed by CD8+regulatory T cells in vitro and in vivo. Am J Transl Res. 2017;9:63–78.
Flippe L, Bézie S, Anegon I, Guillonneau C. Future prospects for CD8+regulatory T cells in immune tolerance. Immunol Rev. 2019;292:209–24.
Arias DAA, Kim HJ, Zhou P, Holderried TA, Wang X, Dranoff G, et al. Disruption of CD8+ Treg activity results in expansion of T follicular helper cells and enhanced antitumor immunity. Cancer Immunol Res. 2014;2:207–16.
Lau J, Cheung J, Navarro A, Lianoglou S, Haley B, Totpal K, et al. Tumour and host cell PD-L1 is required to mediate suppression of antitumour immunity in mice. Nat Commun. 2017;8:14572.
Zhang Y, Velez-Delgado A, Mathew E, Li D, Mendez FM, Flannagan K, et al. Myeloid cells are required for PD-1/PD-L1 checkpoint activation and the establishment of an immunosuppressive environment in pancreatic cancer. Gut. 2017;66:124–36.
Diskin B, Adam S, Cassini MF, Sanchez G, Liria M, Aykut B, et al. PD-L1 engagement on T cells promotes self-tolerance and suppression of neighboring macrophages and effector T cells in cancer. Nat Immunol. 2020;21:442–54.
Candido JB, Morton JP, Bailey P, Campbell AD, Karim SA, Jamieson T, et al. CSF1R+macrophages sustain pancreatic tumor growth through T cell suppression and maintenance of key gene programs that define the squamous subtype. Cell Rep. 2018;23:1448–60.
Peranzoni E, Lemoine J, Vimeux L, Feuillet V, Barrin S, Kantari-Mimoun C, et al. Macrophages impede CD8 T cells from reaching tumor cells and limit the efficacy of anti–PD-1 treatment. Proc Natl Acad Sci U S A. 2018;115:E4041–50.
Kim W, Chu TH, Nienhüser H, Jiang Z, Del Portillo A, Remotti HE, et al. PD-1 signaling promotes tumor-infiltrating myeloid-derived suppressor cells and gastric tumorigenesis in mice. Gastroenterology. 2021;160:781–96.
Nywening TM, Belt BA, Cullinan DR, Panni RZ, Han BJ, Sanford DE, et al. Targeting both tumour-associated CXCR2(+) neutrophils and CCR2(+) macrophages disrupts myeloid recruitment and improves chemotherapeutic responses in pancreatic ductal adenocarcinoma. Gut. 2018;67:1112–23.
Dougan SK, Dougan M. Regulation of innate and adaptive antitumor immunity by IAP antagonists. Immunotherapy. 2018;10:787–96.
Winograd R, Byrne KT, Evans RA, Odorizzi PM, Meyer AR, Bajor DL, et al. Induction of T-cell immunity overcomes complete resistance to PD-1 and CTLA-4 blockade and improves survival in pancreatic carcinoma. Cancer Immunol Res. 2015;3:399–411.
Sun H, Liu SY, Zhou JY, Xu JT, Zhang HK, Yan HH, et al. Specific TP53 subtype as biomarker for immune checkpoint inhibitors in lung adenocarcinoma. EBioMedicine. 2020;60:102990.
Biton J, Mansuet-Lupo A, Pécuchet N, Alifano M, Ouakrim H, Arrondeau J, et al. TP53, STK11, and EGFR mutations predict tumor immune profile and the response to anti-PD-1 in lung adenocarcinoma. Clin Cancer Res. 2018;24:5710–23.
Barrett MT, Lenkiewicz E, Malasi S, Basu A, Yearley JH, Annamalai L, et al. The association of genomic lesions and PD-1/PD-L1 expression in resected triple-negative breast cancers. Breast Cancer Res. 2018;20:71.