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Original Research

Identification of an immunogenic neo-epitope encoded by mouse sarcoma using CXCR3 ligand mRNAs as sensors

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Article: e1306617 | Received 23 Dec 2016, Accepted 09 Mar 2017, Published online: 28 Apr 2017

References

  • Matthew MG, Xiuli Z, Heiko S, Etienne C, Jeffrey PW, Takuro N, Yulia I, Jasreet H, Cora DA, Willem-Jan K et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 2014; 515:577-81; PMID:25428507; https://doi.org/10.1038/nature13988
  • John CC, Sebastian K, Jan D, Martin L, Niels van de R, Jos de G, Abderraouf S, Mustafa D, Sebastian B, Claudia P et al. Exploiting the mutanome for tumor vaccination. Cancer Res 2012; 72:1081-91; PMID:22237626; https://doi.org/10.1158/0008-5472.CAN-11-3722
  • Brown SD, Warren RL, Gibb EA, Martin SD, Spinelli JJ, Nelson BH, Holt RA. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res 2014; 24:743-50; PMID:24782321; https://doi.org/10.1101/gr.165985.113
  • Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014; 371:2189-99; PMID:25409260; https://doi.org/10.1056/NEJMoa1406498
  • van Rooij N, van Buuren MM, Philips D, Velds A, Toebes M, Heemskerk B, van Dijk LJ, Behjati S, Hilkmann H, El Atmioui D et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J Clin Oncol 2013; 31:e439-42; PMID:24043743; https://doi.org/10.1200/JCO.2012.47.7521
  • Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23; PMID:20525992; https://doi.org/10.1056/NEJMoa1003466
  • Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015; 348:124-8; PMID:25765070; https://doi.org/10.1126/science.aaa1348
  • Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 2015; 372:2509-20; PMID:26028255; https://doi.org/10.1056/NEJMoa1500596
  • Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, Gartner J, Lin JC, Teer JK, Cliften P, Tycksen E et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat Med 2013; 19:747-52; PMID:23644516; https://doi.org/DOI:10.1038/nm.3161
  • Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, Wunderlich JR, Somerville RP, Hogan K, Hinrichs CS et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science 2014; 344:641-5; PMID:24812403; https://doi.org/10.1126/science
  • Gros A, Parkhurst MR, Tran E, Pasetto A, Robbins PF, Ilyas S, Prickett TD, Gartner JJ, Crystal JS, Roberts IM et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med 2016; 22:433-8; PMID:26901407; https://doi.org/10.1038/nm.4051
  • Yadav M, Jhunjhunwala S, Phung QT, Lupardus P, Tanguay J, Bumbaca S, Franci C, Cheung TK, Fritsche J, Weinschenk T et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 2014; 515:572-6; PMID:25428506; https://doi.org/10.1038/nature14001
  • Bakker AH, Hoppes R, Linnemann C, Toebes M, Rodenko B, Berkers CR, Hadrup SR, van Esch WJ, Heemskerk MH, Ovaa H et al. Conditional MHC class I ligands and peptide exchange technology for the human MHC gene products HLA-A1, -A3, -A11, and -B7. Proc Natl Acad Sci USA 2008; 105:3825-30; PMID:18308940; https://doi.org/10.1073/pnas.0709717105
  • Chakera A, Bennett SC, Cornall RJ. A whole blood monokine-based reporter assay provides a sensitive and robust measurement of the antigen-specific T cell response. J Transl Med 2011; 9:143; PMID:21871084; https://doi.org/10.1186/1479-5876-9-143
  • Chen YT, Scanlan MJ, Sahin U, Türeci O, Gure AO, Tsang S, Williamson B, Stockert E, Pfreundschuh M, Old LJ. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc Natl Acad Sci USA 1997; 94:1914-8; PMID:9050879
  • Chen JL, Dunbar PR, Gileadi U, Jäger E, Gnjatic S, Nagata Y, Stockert E, Panicali DL, Chen YT, Knuth A et al. Identification of NY-ESO-1 peptide analogues capable of improved stimulation of tumor-reactive CTL. J Immunol 2000; 165:948-55; PMID:10878370; https://doi.org/10.4049/jimmunol.165.2.948
  • Burrows SR, Gardner J, Khanna R, Steward T, Moss DJ, Rodda S, Suhrbier A. Five new cytotoxic T cell epitopes identified within Epstein-Barr virus nuclear antigen 3. J Gen Virol 1994; 75:2489-93; PMID:7521394; https://doi.org/10.1099/0022-1317-75-9-2489
  • Ikeda H, Ohta N, Furukawa K, Miyazaki H, Wang L, Kuribayashi K, Old LJ, Shiku H. Mutated mitogen-activated protein kinase: a tumor rejection antigen of mouse sarcoma. Proc Natl Acad Sci USA 1997; 941:6375-9; PMID:9177225; https://doi.org/10.1073/pnas.94.12.6375
  • Hanson HL, Donermeyer DL, Ikeda H, White JM, Shankaran V, Old LJ, Shiku H, Schreiber RD, Allen PM. Eradication of established tumors by CD8+ T cell adoptive immunotherapy. Immunity 2000; 13:265-76; PMID:10981969; https://doi.org/10.1016/S1074-7613(00)00026-1
  • Kageyama S, Wada H, Muro K, Niwa Y, Ueda S, Miyata H, Takiguchi S, Sugino SH, Miyahara Y, Ikeda H et al. Dose-dependent effects of NY-ESO-1 protein vaccine complexed with cholesteryl pullulan (CHP-NY-ESO-1) on immune responses and survival benefits of esophageal cancer patients. J Transl Med 2013; 11:246; PMID:24093426; https://doi.org/10.1186/1479-5876-11-246
  • Muraoka D, Nishikawa H, Noguchi T, Wang L, Harada N, Sato E, Luescher I, Nakayama E, Kato T, Shiku H. Establishment of animal models to analyze the kinetics and distribution of human tumor antigen-specific CD8+ T cells. Vaccine 2013; 31:2110-8; PMID:23499606; https://doi.org/10.1016/j.vaccine.2013.02.056
  • Dengel LT, Norrod AG, Gregory BL, Clancy-TE, Burdick MD, Strieter RM, Slingluff CL Jr, Mullins DW. Interferons induce CXCR3-cognate chemokine production by human metastatic melanoma. J Immunother 2010; 33:965-74; PMID:20948440; https://doi.org/10.1097/CJI.0b013e3181fb045d
  • Huang AY, Gulden PH, Woods AS, Thomas MC, Tong CD, Wang W, Engelhard VH, Pasternack G, Cotter R, Hunt D, Pardoll DM, Jaffee EM. The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc Natl Acad Sci USA 1996; 93:9730-5; PMID:8790399; https://doi.org/10.1073/pnas.93.18.9730
  • Lacotte S, Brun S, Muller S, Dumortier H. CXCR3, inflammation, and autoimmune diseases. Ann NY Acad Sci 2009; 1173:310-7; PMID:19758167; https://doi.org/10.1111/j.1749-6632.2009.04813.x
  • Wendel M, Galani IE, Suri-PE, Cerwenka A. Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res 2008; 68:8437-45; PMID:18922917; https://doi.org/10.1158/0008-5472.CAN-08-1440
  • Ohtani H, Jin Z, Takegawa S, Nakayama T, Yoshie O. Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3+ T cells in lymphocyte-rich gastric carcinoma. J Pathol 2009; 217:21-31; PMID:18980207; https://doi.org/10.1002/path.2448
  • Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, Slingluff C, McKee M, Gajewski TF. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res 2009; 69:3077-85; PMID:19293190; https://doi.org/10.1158/0008-5472.CAN-08-2281
  • Kondo T, Nakazawa H, Ito F, Hashimoto Y, Osaka Y, Futatsuyama K, Toma H, Tanabe K. Favorable prognosis of renal cell carcinoma with increased expression of chemokines associated with a Th1-type immune response. Cancer Sci 2006; 97:780-6; PMID:16863511; https://doi.org/10.1111/j.1349-7006.2006.00231.x
  • Kunz M, Toksoy A, Goebeler M, Engelhardt E, Bröcker E, Gillitzer R. Strong expression of the lymphoattractant C-X-C chemokine Mig is associated with heavy infiltration of T cells in human malignant melanoma. J Pathol 1999; 189:552-8; PMID:10629557; https://doi.org/10.1002/(SICI)1096-9896(199912)189:4%3c552::AID-PATH469%3e3.0.CO;2-I
  • Ulloa-Montoya F, Louahed J, Dizier B, Gruselle O, Spiessens B, Lehmann FF, Suciu S, Kruit WH, Eggermont AM, Vansteenkiste J et al. Predictive gene signature in MAGE-A3 antigen-specific cancer immunotherapy. J Clin Oncol 2013; 31:2388-95; PMID:23715562; https://doi.org/10.1200/JCO.2012.44.3762
  • Ji RR, Chasalow SD, Wang L, Hamid O, Schmidt H, Cogswell J, Alaparthy S, Berman D, Jure-Kunkel M, Siemers NO, Jackson JR, Shahabi V. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother 2012; 61:1019-31; PMID:22146893; https://doi.org/10.1007/s00262-011-1172-6
  • Duan F, Duitama J, Al Seesi S, Ayres CM, Corcelli SA, Pawashe AP, Blanchard T, McMahon D, Sidney J, Sette A et al. Genomic and bioinformatic profiling of mutational neoepitopes reveals new rules to predict anticancer immunogenicity. J Exp Med 2014; 11:2231-48; https://doi.org/10.1084/jem.20141308
  • Griswold DP, Corbett TH. A colon tumor model for anticancer agent evaluation. Cancer 1975; 36:2441-4; PMID:1212662; https://doi.org/10.1002/1097-0142(197512)36:6%3c2441::AID-CNCR2820360627%3e3.0.CO;2-P
  • DeLeo AB, Shiku H, Takahashi T, John M, Old LJ. Cell surface antigens of chemically induced sarcomas of the mouse. I. Murine leukemia virus-related antigens and alloantigens on cultured fibroblasts and sarcoma cells: description of a unique antigen on BALB/c Meth A sarcoma. J Exp Med 1977; 146:720-34; PMID:197192
  • Power CA, Grand CL, Ismail N, Peters NC, Yurkowski DP, Bretscher PA. A valid ELISPOT assay for enumeration of ex vivo, antigen-specific, IFNgamma-producing T cells. J Immunol Methods 1999; 227:99-107; PMID:10485258; https://doi.org/10.1016/S0022-1759(99)00074-5
  • Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25:1754-60; PMID:19451168; https://doi.org/10.1093/bioinformatics/btp324
  • Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009; 25:1105-11; PMID:19289445; https://doi.org/10.1093/bioinformatics/btp120
  • Moutaftsi M, Peters B, Pasquetto V, Tscharke DC, Sidney J, Bui HH, Grey H, Sette A. A consensus epitope prediction approach identifies the breadth of murine T (CD8+)-cell responses to vaccinia virus. Nat Biotechnol 2006; 24:817-9; PMID:16767078; https://doi.org/10.1038/nbt1215