Heterogeneous Tumor-Immune Microenvironments among Differentially Growing Metastases in an Ovarian Cancer Patient

Cell

Volumn 170, Issue 5, 2017, Pages 927-938.e20

  Jiménez Sánchez, Alejandro ^a   Memon, Danish ^a,b   Pourpe, Stephane ^c   Veeraraghavan, Harini ^c   Li, Yanyun ^c   Vargas, Hebert Alberto ^c   Gill, Michael B ^a   Park, Kay J ^c   Zivanovic, Oliver ^c   Konner, Jason ^c   Ricca, Jacob ^c   Zamarin, Dmitriy ^c   Walther, Tyler ^c   Aghajanian, Carol ^c   Wolchok, Jedd D ^c,d,e   Sala, Evis ^c   Merghoub, Taha ^c   Snyder, Alexandra ^c,d   Miller, Martin L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e Weill Cornell Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; CARBOPLATIN; CISPLATIN; CYCLOPHOSPHAMIDE; DOXORUBICIN; EPITOPE; GEMCITABINE; NEOEPITOPE; PACLITAXEL; PEMETREXED; TOPOTECAN; UNCLASSIFIED DRUG; TRANSCRIPTOME; TUMOR ANTIGEN;

ADULT; ARTICLE; ASSAY; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CANCER STAGING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL ISOLATION; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE EXPRESSION; GENOMICS; HIGH GRADE SEROUS OVARIAN CANCER; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGENOMIC; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LYMPHOCYTIC INFILTRATION; METASTASIS; MIDDLE AGED; MRNA EXPRESSION ASSAY; OVARY CANCER; PRIORITY JOURNAL; T CELL NEOEPITOPE CHALLENGE ASSAY; T LYMPHOCYTE SUBPOPULATION; TRANSCRIPTOMICS; TUMOR GROWTH; TUMOR IMMUNE MICROENVIRONMENT; TUMOR IMMUNOGENICITY; TUMOR MICROENVIRONMENT; TUMOR REGRESSION; WHOLE EXOME SEQUENCING; CASE REPORT; CYSTADENOCARCINOMA, SEROUS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MUTATION; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; PATHOLOGY; T LYMPHOCYTE;

ANTIGENS, NEOPLASM; CYSTADENOCARCINOMA, SEROUS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTATION; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; T-LYMPHOCYTES; TRANSCRIPTOME; TUMOR MICROENVIRONMENT;

EID: 85028377618     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.07.025     Document Type: Article

References (100)

1. Ascierto, M.L., Makohon-Moore, A., Lipson, E.J., Taube, J.M., McMiller, T.L., Berger, A.E., Fan, J., Kaunitz, G., Cottrell, T., Kohutek, Z., et al. Transcriptional mechanisms of resistance to anti-PD-1 therapy. Clin. Cancer Res., 23, 2017 clincanres.0270.2016.
2. Bahram, S., Arnold, D., Bresnahan, M., Strominger, J.L., Spies, T., Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proc. Natl. Acad. Sci. USA 88 (1991), 10094–10098.
3. Barbie, D.A., Tamayo, P., Boehm, J.S., Kim, S.Y., Moody, S.E., Dunn, I.F., Schinzel, A.C., Sandy, P., Meylan, E., Scholl, C., et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 462 (2009), 108–112.
4. Bashashati, A., Ha, G., Tone, A., Ding, J., Prentice, L.M., Roth, A., Rosner, J., Shumansky, K., Kalloger, S., Senz, J., et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J. Pathol. 231 (2013), 21–34.
5. Bauer, S., Groh, V., Wu, J., Steinle, A., Phillips, J.H., Lanier, L.L., Spies, T., Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285 (1999), 727–729.
6. Benci, J.L., Xu, B., Qiu, Y., Wu, T.J., Dada, H., Twyman-Saint Victor, C., Cucolo, L., Lee, D.S.M., Pauken, K.E., Huang, A.C., et al. Tumor interferon signaling regulates a multigenic resistance program to immune checkpoint blockade. Cell 167 (2016), 1540–1554.e12.
7. Bernards, A., Settleman, J., GAP control: regulating the regulators of small GTPases. Trends Cell Biol. 14 (2004), 377–385.
8. Bhang, H.E., Ruddy, D.A., Krishnamurthy Radhakrishna, V., Caushi, J.X., Zhao, R., Hims, M.M., Singh, A.P., Kao, I., Rakiec, D., Shaw, P., et al. Studying clonal dynamics in response to cancer therapy using high-complexity barcoding. Nat. Med. 21 (2015), 440–448.
9. Bowtell, D.D., Böhm, S., Ahmed, A.A., Aspuria, P.-J., Bast, R.C. Jr., Beral, V., Berek, J.S., Birrer, M.J., Blagden, S., Bookman, M.A., et al. Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer. Nat. Rev. Cancer 15 (2015), 668–679.
10. Brabletz, T., Lyden, D., Steeg, P.S., Werb, Z., Roadblocks to translational advances on metastasis research. Nat. Med. 19 (2013), 1104–1109.
11. Bronger, H., Singer, J., Windmüller, C., Reuning, U., Zech, D., Delbridge, C., Dorn, J., Kiechle, M., Schmalfeldt, B., Schmitt, M., Avril, S., CXCL9 and CXCL10 predict survival and are regulated by cyclooxygenase inhibition in advanced serous ovarian cancer. Br. J. Cancer 115 (2016), 553–563.
12. Brown, S.D., Warren, R.L., Gibb, E.A., Martin, S.D., Spinelli, J.J., Nelson, B.H., Holt, R.A., Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 24 (2014), 743–750.
13. Calis, J.J.A., Maybeno, M., Greenbaum, J.A., Weiskopf, D., De Silva, A.D., Sette, A., Keşmir, C., Peters, B., Properties of MHC class I presented peptides that enhance immunogenicity. PLoS Comput. Biol., 9, 2013, e1003266.
14. Cannistra, S.A., Cancer of the ovary. N. Engl. J. Med. 351 (2004), 2519–2529.
15. Carson, W.E. 3rd, Shapiro, C.L., Crespin, T.R., Thornton, L.M., Andersen, B.L., Cellular immunity in breast cancer patients completing taxane treatment. Clin. Cancer Res. 10 (2004), 3401–3409.
16. Carter, S.L., Cibulskis, K., Helman, E., McKenna, A., Shen, H., Zack, T., Laird, P.W., Onofrio, R.C., Winckler, W., Weir, B.A., et al. Absolute quantification of somatic DNA alterations in human cancer. Nat. Biotechnol. 30 (2012), 413–421.
17. Challa-Malladi, M., Lieu, Y.K., Califano, O., Holmes, A.B., Bhagat, G., Murty, V.V., Dominguez-Sola, D., Pasqualucci, L., Dalla-Favera, R., Combined genetic inactivation of β2-Microglobulin and CD58 reveals frequent escape from immune recognition in diffuse large B cell lymphoma. Cancer Cell 20 (2011), 728–740.
18. Chen, P.L., Roh, W., Reuben, A., Cooper, Z.A., Spencer, C.N., Prieto, P.A., Miller, J.P., Bassett, R.L., Gopalakrishnan, V., Wani, K., et al. Analysis of immune signatures in longitudinal tumor samples yields insight into biomarkers of response and mechanisms of resistance to immune checkpoint blockade. Cancer Discov. 6 (2016), 827–837.
19. Cibulskis, K., Lawrence, M.S., Carter, S.L., Sivachenko, A., Jaffe, D., Sougnez, C., Gabriel, S., Meyerson, M., Lander, E.S., Getz, G., Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31 (2013), 213–219.
20. Davoli, T., Uno, H., Wooten, E.C., Elledge, S.J., Tumor aneuploidy correlates with markers of immune evasion and with reduced response to immunotherapy. Science, 355, 2017, eaaf8399.
21. De Mattos-Arruda, L., Bidard, F.C., Won, H.H., Cortes, J., Ng, C.K.Y., Peg, V., Nuciforo, P., Jungbluth, A.A., Weigelt, B., Berger, M.F., et al. Establishing the origin of metastatic deposits in the setting of multiple primary malignancies: the role of massively parallel sequencing. Mol. Oncol. 8 (2014), 150–158.
22. DuPage, M., Mazumdar, C., Schmidt, L.M., Cheung, A.F., Jacks, T., Expression of tumour-specific antigens underlies cancer immunoediting. Nature 482 (2012), 405–409.
23. Edgar, R., Domrachev, M., Lash, A.E., Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30 (2002), 207–210.
24. Fabregat, A., Sidiropoulos, K., Garapati, P., Gillespie, M., Hausmann, K., Haw, R., Jassal, B., Jupe, S., Korninger, F., McKay, S., et al. The reactome pathway knowledgebase. Nucleic Acids Res. 44:D1 (2016), D481–D487.
25. Fisher, S., Barry, A., Abreu, J., Minie, B., Nolan, J., Delorey, T.M., Young, G., Fennell, T.J., Allen, A., Ambrogio, L., et al. A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biol., 12, 2011, R1.
26. Galluzzi, L., Buqué, A., Kepp, O., Zitvogel, L., Kroemer, G., Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell 28 (2015), 690–714.
27. Gavalas, N.G., Karadimou, A., Dimopoulos, M.A., Bamias, A., Immune response in ovarian cancer: how is the immune system involved in prognosis and therapy: potential for treatment utilization. Clin. Dev. Immunol., 2010, 2010, 791603.
28. Gerlinger, M., Rowan, A.J., Horswell, S., Math, M., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366 (2012), 883–892.
29. Giannakis, M., Mu, X.J., Shukla, S.A., Qian, Z.R., Cohen, O., Nishihara, R., Bahl, S., Cao, Y., Amin-Mansour, A., Yamauchi, M., et al. Genomic correlates of immune-cell infiltrates in colorectal carcinoma. Cell Rep. 15 (2016), 857–865.
30. Gnirke, A., Melnikov, A., Maguire, J., Rogov, P., LeProust, E.M., Brockman, W., Fennell, T., Giannoukos, G., Fisher, S., Russ, C., et al. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat. Biotechnol. 27 (2009), 182–189.
31. Groh, V., Rhinehart, R., Secrist, H., Bauer, S., Grabstein, K.H., Spies, T., Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96 (1999), 6879–6884.
32. Hänzelmann, S., Castelo, R., Guinney, J., GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics, 14, 2013, 7.
33. Homicsko, K., Hospitalier, C., Vaudois, U., De, É.P.F., Targeting programmed cell death 1 in ovarian cancer. J. Clin. Oncol. 33 (2016), 3987–3989.
34. Joyce, J.A., Fearon, D.T., T cell exclusion, immune privilege, and the tumor microenvironment. Science 348 (2015), 74–80.
35. Kanehisa, M., Goto, S., KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28 (2000), 27–30.
36. Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., Tanabe, M., KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44:D1 (2016), D457–D462.
37. Kim, Y., Ponomarenko, J., Zhu, Z., Tamang, D., Wang, P., Greenbaum, J., Lundegaard, C., Sette, A., Lund, O., Bourne, P.E., et al. Immune epitope database analysis resource. Nucleic Acids Res. 40 (2012), W525–W530.
38. Kotturi, M.F., Peters, B., Buendia-Laysa, F. Jr., Sidney, J., Oseroff, C., Botten, J., Grey, H., Buchmeier, M.J., Sette, A., The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: uncovering new tricks for an old virus. J. Virol. 81 (2007), 4928–4940.
39. Kreiter, S., Vormehr, M., van de Roemer, N., Diken, M., Löwer, M., Diekmann, J., Boegel, S., Schrörs, B., Vascotto, F., Castle, J.C., et al. Mutant MHC class II epitopes drive therapeutic immune responses to cancer. Nature 520 (2015), 692–696.
40. Kuilman, T., Velds, A., Kemper, K., Ranzani, M., Bombardelli, L., Hoogstraat, M., Nevedomskaya, E., Xu, G., de Ruiter, J., Lolkema, M.P., et al. CopywriteR: DNA copy number detection from off-target sequence data. Genome Biol., 16, 2015, 49.
41. Lee, J.-Y., Yoon, J.-K., Kim, B., Kim, S., Kim, M.A., Lim, H., Bang, D., Song, Y.-S., Tumor evolution and intratumor heterogeneity of an epithelial ovarian cancer investigated using next-generation sequencing. BMC Cancer, 15, 2015, 85.
42. Li, H., Peyrollier, K., Kilic, G., Brakebusch, C., Rho GTPases and cancer. Biofactors 40 (2014), 226–235.
43. Liao, F., Rabin, R.L., Yannelli, J.R., Koniaris, L.G., Vanguri, P., Farber, J.M., Human Mig chemokine: biochemical and functional characterization. J. Exp. Med. 182 (1995), 1301–1314.
44. Liberzon, A., Subramanian, A., Pinchback, R., Thorvaldsdóttir, H., Tamayo, P., Mesirov, J.P., Molecular signatures database (MSigDB) 3.0. Bioinformatics 27 (2011), 1739–1740.
45. Lundegaard, C., Lund, O., Nielsen, M., Accurate approximation method for prediction of class I MHC affinities for peptides of length 8, 10 and 11 using prediction tools trained on 9mers. Bioinformatics 24 (2008), 1397–1398.
46. Matsushita, H., Vesely, M.D., Koboldt, D.C., Rickert, C.G., Uppaluri, R., Magrini, V.J., Arthur, C.D., White, J.M., Chen, Y.-S., Shea, L.K., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482 (2012), 400–404.
47. McGranahan, N., Furness, A.J.S., Rosenthal, R., Ramskov, S., Lyngaa, R., Saini, S.K., Jamal-Hanjani, M., Wilson, G.A., Birkbak, N.J., Hiley, C.T., et al. Immune checkpoint blockade. Science 351 (2016), 1463–1469.
48. Melero, I., Rouzaut, A., Motz, G.T., Coukos, G., T-cell and NK-cell infiltration into solid tumors: a key limiting factor for efficacious cancer immunotherapy. Cancer Discov. 4 (2014), 522–526.
49. Miao, D., Van Allen, E.M., Genomic determinants of cancer immunotherapy. Curr. Opin. Immunol. 41 (2016), 32–38.
50. Moutaftsi, M., Peters, B., Pasquetto, V., Tscharke, D.C., Sidney, J., Bui, H.-H., Grey, H., Sette, A., A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat. Biotechnol. 24 (2006), 817–819.
51. Murugaesu, N., Wilson, G.A., Birkbak, N.J., Watkins, T., McGranahan, N., Kumar, S., Abbassi-Ghadi, N., Salm, M., Mitter, R., Horswell, S., et al. Tracking the genomic evolution of esophageal adenocarcinoma through neoadjuvant chemotherapy. Cancer Discov. 5 (2015), 821–831.
52. Neefjes, J.J., Momburg, F., Hammerling, G.J., Selective and ATP dependent translocation of peptides by the MHC encoded transporter. Science 261 (1993), 769–771.
53. Newman, A.M., Liu, C.L., Green, M.R., Gentles, A.J., Feng, W., Xu, Y., Hoang, C.D., Diehn, M., Alizadeh, A.A., Robust enumeration of cell subsets from tissue expression profiles. Nat. Methods 12 (2015), 453–457.
54. Nielsen, M., Lund, O., NN-align. An artificial neural network-based alignment algorithm for MHC class II peptide binding prediction. BMC Bioinformatics, 10, 2009, 296.
55. Nielsen, M., Lundegaard, C., Worning, P., Lauemøller, S.L., Lamberth, K., Buus, S., Brunak, S., Lund, O., Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci. 12 (2003), 1007–1017.
56. Nixon, K.C., The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15 (1999), 407–414.
57. Patch, A.-M., Christie, E.L., Etemadmoghadam, D., Garsed, D.W., George, J., Fereday, S., Nones, K., Cowin, P., Alsop, K., Bailey, P.J., et al., Australian Ovarian Cancer Study Group. Whole-genome characterization of chemoresistant ovarian cancer. Nature 521 (2015), 489–494.
58. Paul, S., Weiskopf, D., Angelo, M.A., Sidney, J., Peters, B., Sette, A., HLA class I alleles are associated with peptide-binding repertoires of different size, affinity, and immunogenicity. J. Immunol. 191 (2013), 5831–5839.
59. Peters, B., Sette, A., Generating quantitative models describing the sequence specificity of biological processes with the stabilized matrix method. BMC Bioinformatics, 6, 2005, 132.
60. Pfirschke, C., Engblom, C., Rickelt, S., Cortez-Retamozo, V., Garris, C., Pucci, F., Yamazaki, T., Poirier-Colame, V., Newton, A., Redouane, Y., et al. Immunogenic chemotherapy sensitizes tumors to checkpoint blockade therapy. Immunity 44 (2016), 343–354.
61. Powis, S.J., Townsend, A.R., Deverson, E.V., Bastin, J., Butcher, G.W., Howard, J.C., Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354 (1991), 528–531.
62. Rainczuk, A., Rao, J., Gathercole, J., Stephens, A.N., The emerging role of CXC chemokines in epithelial ovarian cancer. Reproduction 144 (2012), 303–317.
63. Remark, R., Alifano, M., Cremer, I., Lupo, A., Dieu-Nosjean, M.C., Riquet, M., Crozet, L., Ouakrim, H., Goc, J., Cazes, A., et al. Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin. Clin. Cancer Res. 19 (2013), 4079–4091.
64. Reuben, A., Spencer, C.N., Prieto, P.A., Gopalakrishnan, V., Reddy, S.M., Miller, J.P., Mao, X., De Macedo, M.P., Chen, J., Song, X., et al. Genomic and immune heterogeneity are associated with differential responses to therapy in melanoma. Npj Genomic Med., 2, 2017, 10.
65. Rizvi, N.A., Hellmann, M.D., Snyder, A., Kvistborg, P., Makarov, V., Havel, J.J., Lee, W., Yuan, J., Wong, P., Ho, T.S., et al. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348 (2015), 1–10.
66. Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer. Nat. Biotechnol. 29 (2011), 24–26.
67. Rooney, M.S., Shukla, S.A., Wu, C.J., Getz, G., Hacohen, N., Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell 160 (2015), 48–61.
68. Roth, A., Khattra, J., Yap, D., Wan, A., Laks, E., Biele, J., Ha, G., Aparicio, S., Bouchard-Côté, A., Shah, S.P., PyClone: statistical inference of clonal population structure in cancer. Nat. Methods 11 (2014), 396–398.
69. Sala, E., Kataoka, M.Y., Priest, A.N., Gill, A.B., McLean, M.A., Joubert, I., Graves, M.J., Crawford, R.A., Jimenez-Linan, M., Earl, H.M., et al. Advanced ovarian cancer: multiparametric MR imaging demonstrates response- and metastasis-specific effects. Radiology 263 (2012), 149–159.
70. Satoh, J., Tabunoki, H., A comprehensive profile of ChIP-Seq-based STAT1 target genes suggests the complexity of STAT1-mediated gene regulatory mechanisms. Gene Regul. Syst. Bio. 7 (2013), 41–56.
71. Schliep, K.P., phangorn: phylogenetic analysis in R. Bioinformatics 27 (2011), 592–593.
72. Şenbabaoğlu, Y., Gejman, R.S., Winer, A.G., Liu, M., Van Allen, E.M., de Velasco, G., Miao, D., Ostrovnaya, I., Drill, E., Luna, A., et al. Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures. Genome Biol., 17, 2016, 231.
73. Sharma, P., Hu-Lieskovan, S., Wargo, J.A., Ribas, A., Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell 168 (2017), 707–723.
74. Shukla, S.A., Rooney, M.S., Rajasagi, M., Tiao, G., Dixon, P.M., Lawrence, M.S., Stevens, J., Lane, W.J., Dellagatta, J.L., Steelman, S., et al. Comprehensive analysis of cancer-associated somatic mutations in class I HLA genes. Nat. Biotechnol. 33 (2015), 1152–1158.
75. Sidney, J., Assarsson, E., Moore, C., Ngo, S., Pinilla, C., Sette, A., Peters, B., Quantitative peptide binding motifs for 19 human and mouse MHC class I molecules derived using positional scanning combinatorial peptide libraries. Immunome Res. 4 (2008), 2–15.
76. Sivan, A., Corrales, L., Hubert, N., Williams, J.B., Aquino-Michaels, K., Earley, Z.M., Benyamin, F.W., Man Lei, Y., Jabri, B., Alegre, M.-L., et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350 (2015), 1084–1089.
77. Spranger, S., Bao, R., Gajewski, T.F., Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity. Nature 523 (2015), 231–235.
78. Spranger, S., Dai, D., Horton, B., Gajewski, T.F., Tumor-residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell 31 (2017), 711–723.e4.
79. Sridharan, V., Gjini, E., Liao, X., Chau, N.G., Haddad, R.I., Severgnini, M., Hammerman, P., El-Naggar, A., Freeman, G.J., Hodi, F.S., et al. Immune profiling of adenoid cystic carcinoma: PD-L2 expression and associations with tumor-infiltrating lymphocytes. Cancer Immunol. Res. 4 (2016), 679–687.
80. Sturniolo, T., Bono, E., Ding, J., Raddrizzani, L., Tuereci, O., Sahin, U., Braxenthaler, M., Gallazzi, F., Protti, M.P., Sinigaglia, F., Hammer, J., Generation of tissue-specific and promiscuous HLA ligand databases using DNA microarrays and virtual HLA class II matrices. Nat. Biotechnol. 17 (1999), 555–561.
81. Su, K.Y., Chen, H.Y., Li, K.C., Kuo, M.L., Yang, J.C.H., Chan, W.K., Ho, B.C., Chang, G.C., Shih, J.Y., Yu, S.L., Yang, P.C., Pretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. J. Clin. Oncol. 30 (2012), 433–440.
82. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
83. Suh, W.-K., Cohen-Doyle, M.F., Fruh, K., Wang, K., Peterson, P.A., Williams, D.B., Interaction of MHC class I molecules with the transporter associated with antigen processing. Science 264 (1994), 1322–1326.
84. Suzuki, E., Kapoor, V., Jassar, A.S., Kaiser, L.R., Albelda, S.M., Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11 (2005), 6713–6721.
85. Szolek, A., Schubert, B., Mohr, C., Sturm, M., Feldhahn, M., Kohlbacher, O., OptiType: precision HLA typing from next-generation sequencing data. Bioinformatics 30 (2014), 3310–3316.
86. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 474 (2011), 609–615.
87. Teng, M.W.L., Galon, J., Fridman, W.H., Smyth, M.J., From mice to humans: developments in cancer immunoediting. J. Clin. Invest. 125 (2015), 3338–3346.
88. Thorvaldsdóttir, H., Robinson, J.T., Mesirov, J.P., Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14 (2013), 178–192.
89. Tran, E., Robbins, P.F., Lu, Y.-C., Prickett, T.D., Gartner, J.J., Jia, L., Pasetto, A., Zheng, Z., Ray, S., Groh, E.M., et al. T-cell transfer therapy targeting mutant KRAS in cancer. N. Engl. J. Med. 375 (2016), 2255–2262.
90. Turke, A.B., Zejnullahu, K., Wu, Y.L., Song, Y., Dias-Santagata, D., Lifshits, E., Toschi, L., Rogers, A., Mok, T., Sequist, L., et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17 (2010), 77–88.
91. Verdegaal, E.M.E., de Miranda, N.F.C.C., Visser, M., Harryvan, T., van Buuren, M.M., Andersen, R.S., Hadrup, S.R., van der Minne, C.E., Schotte, R., Spits, H., et al. Neoantigen landscape dynamics during human melanoma-T cell interactions. Nature 536 (2016), 91–95.
92. Vetizou, M., Pitt, J.M., Daillere, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M.P., Duong, C.P.M., et al. Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350 (2015), 1079–1084.
93. Vita, R., Overton, J.A., Greenbaum, J.A., Ponomarenko, J., Clark, J.D., Cantrell, J.R., Wheeler, D.K., Gabbard, J.L., Hix, D., Sette, A., Peters, B., The immune epitope database (IEDB) 3.0. Nucleic Acids Res. 43 (2015), D405–D412.
94. Wang, P., Sidney, J., Dow, C., Mothé, B., Sette, A., Peters, B., A systematic assessment of MHC class II peptide binding predictions and evaluation of a consensus approach. PLoS Comput. Biol., 4, 2008, e1000048.
95. Wang, P., Sidney, J., Kim, Y., Sette, A., Lund, O., Nielsen, M., Peters, B., Peptide binding predictions for HLA DR, DP and DQ molecules. BMC Bioinformatics, 11, 2010, 568.
96. Wang, W., Kryczek, I., Dostál, L., Lin, H., Tan, L., Zhao, L., Lu, F., Wei, S., Maj, T., Peng, D., et al. Effector T cells abrogate stroma-mediated chemoresistance in ovarian cancer. Cell 165 (2016), 1092–1105.
97. Yoshihara, K., Shahmoradgoli, M., Martínez, E., Vegesna, R., Kim, H., Torres-Garcia, W., Treviño, V., Shen, H., Laird, P.W., Levine, D.A., et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat. Commun., 4, 2013, 2612.
98. Zaretsky, J.M., Garcia-Diaz, A., Shin, D.S., Escuin-Ordinas, H., Hugo, W., Hu-Lieskovan, S., Torrejon, D.Y., Abril-Rodriguez, G., Sandoval, S., Barthly, L., et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N. Engl. J. Med. 375 (2016), 819–829.
99. Zhang, L., Conejo-Garcia, J.R., Katsaros, D., Gimotty, P.A., Massobrio, M., Regnani, G., Makrigiannakis, A., Gray, H., Schlienger, K., Liebman, M.N., et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N. Engl. J. Med. 348 (2003), 203–213.
100. Zitvogel, L., Apetoh, L., Ghiringhelli, F., Kroemer, G., Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 8 (2008), 59–73.