Evolution of neoantigen landscape during immune checkpoint blockade in non-small cell lung cancer

Cancer Discovery

Volumn 7, Issue 3, 2017, Pages 264-276

  Anagnostou, Valsamo ^a   Smith, Kellie N ^a   Forde, Patrick M ^a   Niknafs, Noushin ^b   Bhattacharya, Rohit ^b   White, James ^a   Zhang, Theresa ^c   Adleff, Vilmos ^a   Phallen, Jillian ^a   Wali, Neha ^a   Hruban, Carolyn ^a   Guthrie, Violeta B ^b   Rodgers, Kristen ^d   Naidoo, Jarushka ^a   Kang, Hyunseok ^a   Sharfman, William ^a   Georgiades, Christos ^d   Verde, Franco ^d   Illei, Peter ^a,d   Li, Qing Kay ^d   Gabrielson, Edward ^a,d   Brock, Malcolm V ^a,d   Zahnow, Cynthia A ^a   Baylin, Stephen B ^a   Scharpf, Robert B ^a   Brahmer, Julie R ^a   Karchin, Rachel ^b   Pardoll, Drew M ^a   Velculescu, Victor E ^a,b,d   more..

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Johns Hopkins University   (United States)

^c Personal Genome Diagnostics   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CHECKPOINT KINASE INHIBITOR; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; IPILIMUMAB; MAJOR HISTOCOMPATIBILITY ANTIGEN; NEOANTIGEN; NIVOLUMAB; PROGRAMMED DEATH 1 RECEPTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOLOGICAL ANTINEOPLASTIC AGENT; JAK1 PROTEIN, HUMAN; JAK2 PROTEIN, HUMAN; JANUS KINASE 1; JANUS KINASE 2; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; PDCD1 PROTEIN, HUMAN;

ADULT; ALLELIC IMBALANCE; ANTIGEN RECOGNITION; ARTICLE; CANCER GROWTH; CASE REPORT; CELL CYCLE CHECKPOINT; CELL EXPANSION; CELL GROWTH; CELL HETEROGENEITY; CLONAL VARIATION; CONTROLLED STUDY; COPY NUMBER VARIATION; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; NEXT GENERATION SEQUENCING; NON SMALL CELL LUNG CANCER; PROTEIN BINDING; PROTEIN EXPRESSION; SOMATIC MUTATION; TREATMENT RESPONSE; WHOLE EXOME SEQUENCING; ANTAGONISTS AND INHIBITORS; COHORT ANALYSIS; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LUNG TUMOR; METABOLISM; MUTATION; PATHOLOGY;

ADULT; ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS, IMMUNOLOGICAL; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE CHECKPOINTS; COHORT STUDIES; CTLA-4 ANTIGEN; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; IMMUNOTHERAPY; IPILIMUMAB; JANUS KINASE 1; JANUS KINASE 2; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTORS, ANTIGEN, T-CELL;

EID: 85014747024     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-16-0828     Document Type: Article

References (51)

1. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW. Cancer genome landscapes. Science 2013; 339: 1546-58.
2. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science 2015; 348: 69-74.
3. Segal NH, Parsons DW, Peggs KS, Velculescu V, Kinzler KW, Vogelstein B, et al. Epitope landscape in breast and colorectal cancer. Cancer Res 2008; 68: 889-92.
4. 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.
5. 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.
6. 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.
7. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515: 568-71.
8. 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.
9. Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 2015; 372: 2018-28.
10. Topalian SL, Taube JM, Anders RA, Pardoll DM. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev 2016; 16: 275-87.
11. Gettinger SN, Horn L, Gandhi L, Spigel DR, Antonia SJ, Rizvi NA, et al. Overall survival and long-term safety of nivolumab (Anti- Programmed Death 1 Antibody, BMS-936558, ONO-4538) in patients with previously treated advanced non-small-cell lung cancer. J Clin Oncol 2015; 33: 2004-12.
12. Koyama S, Akbay EA, Li YY, Herter-Sprie GS, Buczkowski KA, Richards WG, et al. Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints. Nat Commun 2016; 7: 10501.
13. Maeurer MJ, Gollin SM, Storkus WJ, Swaney W, Karbach J, Martin D, et al. Tumor escape from immune recognition: Loss of HLA-A2 melanoma cell surface expression is associated with a complex rearrangement of the short arm of chromosome 6. Clin Cancer Res 1996; 2: 641-52.
14. 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.
15. Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, et al. Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med 2016; 375: 819-29.
16. Jones S, Anagnostou V, Lytle K, Parpart-Li S, Nesselbush M, Riley DR, et al. Personalized genomic analyses for cancer mutation discovery and interpretation. Sci Transl Med 2015; 7: 283ra53.
17. Cann KL, Dellaire G. Heterochromatin and the DNA damage response: The need to relax. Biochem Cell Biol 2011; 89: 45-60.
18. Cancer Genome Atlas Research N. C omprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489: 519-25.
19. Peng W, Chen JQ, Liu C, Malu S, Creasy C, Tetzlaff MT, et al. Loss of PTEN promotes resistance to T cell-mediated immunotherapy. Cancer Discov 2016; 6: 202-16.
20. Rudolph MG, Stanfield RL, Wilson IA. How TCRs bind MHCs, peptides, and coreceptors. Annu Rev Immunol 2006; 24: 419-66.
21. Yadav M, Jhunjhunwala S, Phung QT, Lupardus P, Tanguay J, Bumbaca S, et al. Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 2014; 515: 572-6.
22. Niknafs N, Beleva-Guthrie V, Naiman DQ, Karchin R. SubClonal hierarchy inference from somatic mutations: Automatic reconstruction of cancer evolutionary trees from multi-region next generation sequencing. PLoS Comput Biol 2015; 11: e1004416.
23. Bertotti A, Papp E, Jones S, Adleff V, Anagnostou V, Lupo B, et al. The genomic landscape of response to EGFR blockade in colorectal cancer. Nature 2015; 526: 263-7.
24. Jones S, Chen WD, Parmigiani G, Diehl F, Beerenwinkel N, Antal T, et al. Comparative lesion sequencing provides insights into tumor evolution. Proc Natl Acad Sci U S A 2008; 105: 4283-8.
25. Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010; 467: 1114-7.
26. C ampbell PJ, Yachida S, Mudie LJ, Stephens PJ, Pleasance ED, Stebbings LA, et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010; 467: 1109-13.
27. Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ, et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012; 482: 400-4.
28. Verdegaal EM, de Miranda NF, Visser M, Harryvan T, van Buuren MM, Andersen RS, et al. Neoantigen landscape dynamics during human melanoma-T cell interactions. Nature 2016; 536: 91-5.
29. D udley ME, Roopenian DC. Loss of a unique tumor antigen by cytotoxic T lymphocyte immunoselection from a 3-methylcholanthreneinduced mouse sarcoma reveals secondary unique and shared antigens. J Exp Med 1996; 184: 441-7.
30. Ribas A. Adaptive immune resistance: How cancer protects from immune attack. Cancer Discov 2015; 5: 915-9.
31. Hugo W, Zaretsky JM, Sun L, Song C, Moreno BH, Hu-Lieskovan S, et al. Genomic and transcriptomic features of response to anti-PD-1 therapy in metastatic melanoma. Cell 2016; 165: 35-44.
32. Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 2015; 373: 123-35.
33. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature 2013; 500: 415-21.
34. 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.
35. Sausen M, Leary RJ, Jones S, Wu J, Reynolds CP, Liu X, et al. Integrated genomic analyses identify ARID1A and ARID1B alterations in the childhood cancer neuroblastoma. Nat Genet 2013; 45: 12-7.
36. Needleman SB, Wunsch CD. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 1970; 48: 443-53.
37. Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 2013; 31: 213-9.
38. 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.
39. Nielsen M, Andreatta M. NetMHCpan-3.0; improved prediction of binding to MHC class I molecules integrating information from multiple receptor and peptide length datasets. Genome Med 2016; 8: 33.
40. Lundegaard C, Lamberth K, Harndahl M, Buus S, Lund O, Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res 2008; 36 (Web Server issue): W509-12.
41. 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 2008; 24: 1397-8.
42. Stranzl T, Larsen MV, Lundegaard C, Nielsen M. NetCTLpan: panspecific MHC class I pathway epitope predictions. Immunogenetics 2010; 62: 357-68.
43. Kim Y, Sidney J, Pinilla C, Sette A, Peters B. Derivation of an amino acid similarity matrix for peptide: MHC binding and its application as a Bayesian prior. BMC Bioinformatics 2009; 10: 394.
44. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: Database for MHC ligands and peptide motifs. Immunogenetics 1999; 50: 213-9.
45. Talevich E, Shain AH, Botton T, Bastian BC. CNVkit: Copy number detection and visualization for targeted sequencing using off-target reads. PLoS Comput Biol 2016 12:e1004873.
46. Aran D, Sirota M, Butte AJ. Systematic pan-cancer analysis of tumour purity. Nat Commun 2015; 6: 8971.
47. Li Y, Xie X. Deconvolving tumor purity and ploidy by integrating copy number alterations and loss of heterozygosity. Bioinformatics 2014; 30: 2121-9.
48. 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.
49. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B (methodological) 1995; 57: 289-300.
50. Carlson CS, Emerson RO, Sherwood AM, Desmarais C, Chung MW, Parsons JM, et al. Using synthetic templates to design an unbiased multiplex PCR assay. Nat Commun 2013; 4: 2680.
51. Robins HS, Campregher PV, Srivastava SK, Wacher A, Turtle CJ, Kahsai O, et al. Comprehensive assessment of T-cell receptor betachain diversity in alphabeta T cells. Blood 2009; 114: 4099-107.