Immune cytolytic activity stratifies molecular subsets of human pancreatic cancer

Clinical Cancer Research

Volumn 23, Issue 12, 2017, Pages 3129-3138

  Balli, David ^a   Rech, Andrew J ^a   Stanger, Ben Z ^a,b   Vonderheide, Robert H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NOTCH2 RECEPTOR; PROGRAMMED DEATH 1 LIGAND 1; EPITOPE;

ARTICLE; CDKN 2A GENE; CDKN 2B GENE; CELL CYCLE CHECKPOINT; COPY NUMBER VARIATION; CYTOTOXIC T LYMPHOCYTE; GENE AMPLIFICATION; GENE DELETION; GENE EXPRESSION PROFILING; HUMAN; LYMPHOCYTE FUNCTION; MUTATIONAL ANALYSIS; NOTCH2 GENE; ONCOGENE MYC; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; T LYMPHOCYTE SUBPOPULATION; TUMOR IMMUNITY; TUMOR VOLUME; ADENOCARCINOMA; CD8+ T LYMPHOCYTE; CYTOTOXICITY; GENE; GENE EXPRESSION REGULATION; IMMUNOLOGY; IMMUNOTHERAPY; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; PROGNOSIS;

ADENOCARCINOMA; CARCINOMA, PANCREATIC DUCTAL; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, MHC CLASS I; HUMANS; IMMUNOTHERAPY; PANCREATIC NEOPLASMS; PROGNOSIS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 85020905525     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-16-2128     Document Type: Article

References (57)

1. Hidalgo M. Pancreatic cancer. N Engl J Med 2010;362:1605-17.
2. Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res 2014;74:2913-21.
3. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin 2016;66:7-30.
4. Von Hoff DD, Ervin T, Arena FP, Chiorean EG, Infante J, Moore M, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med 2013;369:1691-703.
5. Conroy T, Desseigne F, Ychou M, Bouche O, Guimbaud R, Becouarn Y, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 2011;364:1817-25.
6. 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.
7. Collisson EA, Sadanandam A, Olson P, Gibb WJ, Truitt M, Gu S, et al. Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy. Nat Med 2011;17:500-3.
8. Moffitt RA, Marayati R, Flate EL, Volmar KE, Loeza SG, Hoadley KA, et al. Virtual microdissection identifies distinct tumor- and stroma-specific subtypes of pancreatic ductal adenocarcinoma. Nat Genet 2015;47:1168-78.
9. Waddell N, Pajic M, Patch AM, Chang DK, Kassahn KS, Bailey P, et al. Whole genomes redefine the mutational landscape of pancreatic cancer. Nature 2015;518:495-501.
10. Witkiewicz AK, McMillan EA, Balaji U, Baek G, Lin WC, Mansour J, et al. Whole-exome sequencing of pancreatic cancer defines genetic diversity and therapeutic targets. Nat Commun 2015;6:6744.
11. Foley K, Kim V, Jaffee E, Zheng L. Current progress in immunotherapy for pancreatic cancer. Cancer Lett 2015;381:244-51.
12. Vonderheide RH, Bayne LJ. Inflammatory networks and immune surveillance of pancreatic carcinoma. Curr Opin Immunol 2013;25:200-5.
13. Royal RE, Levy C, Turner K, Mathur A, Hughes M, Kammula US, et al. Phase 2 trial of single agent Ipilimumab (anti-CTLA-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother 2010;33:828-33.
14. 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.
15. Wormann SM, Diakopoulos KN, Lesina M, Algul H. The immune network in pancreatic cancer development and progression. Oncogene 2014;33:2956-67.
16. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011;331:1612-6.
17. Fukunaga A, Miyamoto M, Cho Y, Murakami S, Kawarada Y, Oshikiri T, et al. CD8+ tumor-infiltrating lymphocytes together with CD4+ tumor-infiltrating lymphocytes and dendritic cells improve the prognosis of patients with pancreatic adenocarcinoma. Pancreas 2004;28:e26-31.
18. Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y, et al. Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer 2013;108:914-23.
19. Hiraoka N, Ino Y, Yamazaki-Itoh R, Kanai Y, Kosuge T, Shimada K. Intratumoral tertiary lymphoid organ is a favourable prognosticator in patients with pancreatic cancer. Br J Cancer 2015;112:1782-90.
20. Mermel CH, Schumacher SE, Hill B, Meyerson ML, Beroukhim R, Getz G. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol 2011;12:R41.
21. Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell 2015;160:48-61.
22. Law CW, Chen Y, Shi W, Smyth GK. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol 2014;15:R29.
23. Wickham H. ggplot2: elegant graphics for data analysis. New York, NY: Springer-Verlag; 2009.
24. Dees ND, Zhang Q, Kandoth C, Wendl MC, Schierding W, Koboldt DC, et al. MuSiC: identifying mutational significance in cancer genomes. Genome Res 2012;22:1589-98.
25. Favero F, Joshi T, Marquard AM, Birkbak NJ, Krzystanek M, Li Q, et al. Sequenza: allele-specific copy number and mutation profiles from tumor sequencing data. Ann Oncol 2015;26:64-70.
26. Carter SL, Cibulskis K, Helman E, McKenna A, Shen H, Zack T, et al. Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol 2012;30:413-21.
27. Shukla SA, Rooney MS, Rajasagi M, Tiao G, Dixon PM, Lawrence MS, et al. Comprehensive analysis of cancer-associated somatic mutations in class I HLA genes. Nat Biotechnol 2015;33:1152-8.
28. Szolek A, Schubert B, Mohr C, Sturm M, Feldhahn M, Kohlbacher O. OptiType: precision HLA typing from next-generation sequencing data. Bioinformatics 2014;30:3310-6.
29. Weese D, Holtgrewe M, Reinert K. RazerS 3: faster, fully sensitive read mapping. Bioinformatics 2012;28:2592-9.
30. Huang Y, Yang J, Ying D, Zhang Y, Shotelersuk V, Hirankarn N, et al. HLAreporter: a tool for HLA typing from next generation sequencing data. Genome Med 2015;7:25.
31. Kim Y, Ponomarenko J, Zhu Z, Tamang D, Wang P, Greenbaum J, et al. Immune epitope database analysis resource. Nucleic Acids Res 2012;40:W525-30.
32. Chowdhury D, Lieberman J. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu Rev Immunol 2008;26:389-420.
33. Johnson BJ, Costelloe EO, Fitzpatrick DR, Haanen JB, Schumacher TN, Brown LE, et al. Single-cell perforin and granzyme expression reveals the anatomical localization of effector CD8+ T cells in influenza virus-infected mice. Proc Natl Acad Sci U S A 2003;100:2657-62.
34. Keefe D, Shi L, Feske S, Massol R, Navarro F, Kirchhausen T, et al. Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity 2005;23:249-62.
35. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014;515:563-7.
36. The Cancer Genome Atlas Research Network,Weinstein JN, Collisson EA, Mills GB, Shaw KR, Ozenberger BA, et al. The Cancer Genome Atlas Pan-Cancer analysis project. Nat Genet 2013;45:1113-20.
37. Duraiswamy J, Ibegbu CC, Masopust D, Miller JD, Araki K, Doho GH, et al. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J Immunol 2011;186:4200-12.
38. Parish IA, Rao S, Smyth GK, Juelich T, Denyer GS, Davey GM, et al. The molecular signature of CD8+ T cells undergoing deletional tolerance. Blood 2009;113:4575-85.
39. Baruah P, Propato A, Dumitriu IE, Rovere-Querini P, Russo V, Fontana R, et al. The pattern recognition receptor PTX3 is recruited at the synapse between dying and dendritic cells, and edits the cross-presentation of self, viral, and tumor antigens. Blood 2006;107:151-8.
40. Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013;39:782-95.
41. Hingorani SR, Wang L, Multani AS, Combs C, Deramaudt TB, Hruban RH, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005;7:469-83.
42. Aguirre AJ, Brennan C, Bailey G, Sinha R, Feng B, Leo C, et al. High-resolution characterization of the pancreatic adenocarcinoma genome. Proc Natl Acad Sci U S A 2004;101:9067-72.
43. Zeller KI, Jegga AG, Aronow BJ, O'Donnell KA, Dang CV. An integrated database of genes responsive to the Myc oncogenic transcription factor: identification of direct genomic targets. Genome Biol 2003;4:R69.
44. Linsley PS, Speake C, Whalen E, Chaussabel D. Copy number loss of the interferon gene cluster in melanomas is linked to reduced T cell infiltrate and poor patient prognosis. PLoS One 2014;9:e109760.
45. Casey SC, Tong L, Li Y, Do R, Walz S, Fitzgerald KN, et al. MYC regulates the antitumor immune response through CD47 and PD-L1. Science 2016;352:227-31.
46. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science 2015;348:69-74.
47. McGranahan N, Furness AJ, Rosenthal R, Ramskov S, Lyngaa R, Saini SK, et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science 2016;351:1463-9.
48. Delitto D, Black BS, Sorenson HL, Knowlton AE, Thomas RM, Sarosi GA, et al. The inflammatory milieu within the pancreatic cancer microenvironment correlates with clinicopathologic parameters, chemoresistance and survival. BMC Cancer 2015;15:783.
49. Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT, et al. Upregulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Sci Transl Med 2013;5:200ra116.
50. Vonderheide RH, Nathanson KL. Immunotherapy at large: the road to personalized cancer vaccines. Nat Med 2013;19:1098-100.
51. Van Allen EM, Miao D, Schilling B, Shukla SA, Blank C, Zimmer L, et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 2015;350:207-11.
52. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014;371:2189-99.
53. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348:124-8.
54. Vonderheide RH. Tumor-promoting inflammatory networks in pancreatic neoplasia: another reason to loathe Kras. Cancer Cell 2014;25:553-4.
55. Pylayeva-Gupta Y, Lee KE, Hajdu CH, Miller G, Bar-Sagi D. Oncogenic Kras-induced GM-CSF production promotes the development of pancreatic neoplasia. Cancer Cell 2012;21:836-47.
56. Soares KC, Rucki AA, Wu AA, Olino K, Xiao Q, Chai Y, et al. PD-1/PD-L1 blockade together with vaccine therapy facilitates effector T-cell infiltration into pancreatic tumors. J Immunother 2015;38:1-11.
57. Vonderheide RH, Bajor DL, Winograd R, Evans RA, Bayne LJ, Beatty GL. CD40 immunotherapy for pancreatic cancer. Cancer Immunol Immunother 2013;62:949-54.