A pilot study of durvalumab and tremelimumab and immunogenomic dynamics in metastatic breast cancer

Oncotarget

Volumn 9, Issue 27, 2018, Pages 18985-18996

  Santa Maria, Cesar August ^c   Kato, Taigo ^b   Park, Jae Hyun ^b   Kiyotani, Kazuma ^b   Rademaker, Alfred ^a   Shah, Ami N ^a   Gross, Leeaht ^a   Blanco, Luis Z ^a   Jain, Sarika ^a   Flaum, Lisa ^a   Tellez, Claudia ^a   Stein, Regina ^a   Uthe, Regina ^a   Gradishar, William J ^a   Cristofanilli, Massimo ^a   Nakamura, Yusuke ^b   Giles, Francis J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Immune checkpoint; Immunogenomics; Metastatic breast cancer; T cell receptor sequencing

Indexed keywords

ANTIGEN; CD8 ANTIGEN; DURVALUMAB; GRANZYME A; NEOANTIGEN; OLIGOCLONAL BAND; PERFORIN; PERFORIN 1; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; TICILIMUMAB; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CD8 GENE; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; ELECTROLYTE DISTURBANCE; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; GENE EXPRESSION PROFILING; GENE MUTATION; GENE SEQUENCE; GRANZYME A GENE; HEPATITIS; HUMAN; HUMAN CELL; IMMUNOGENOMIC DYNAMICS; IMMUNOTHERAPY; METASTATIC BREAST CANCER; MUTATIONAL BURDEN; OVERALL RESPONSE RATE; PERFORIN 1 GENE; PHENOTYPE; PILOT STUDY; PLASMA CELL; RASH; TCR GENE; TREATMENT RESPONSE; TRIPLE NEGATIVE BREAST CANCER; TUMOR IMMUNOGENICITY; UPREGULATION; WHOLE EXOME SEQUENCING;

EID: 85045192932     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.24867     Document Type: Article

References (30)

1. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol. 2002; 3:991-8. https://doi.org/10.1038/ ni1102-991ni1102-991
2. Nanda R, Chow LQ, Dees EC, Berger R, Gupta S, Geva R, Pusztai L, Pathiraja K, Aktan G, Cheng JD, Karantza V, Buisseret L. Pembrolizumab in Patients With Advanced Triple-Negative Breast Cancer: Phase Ib KEYNOTE-012 Study. J Clin Oncol. 2016; 34:2460-7. https://doi. org/10.1200/jco.2015.64.8931
3. Emens LA, Braiteh FS, Cassier P, Delord JP, Eder JP, Fasso M, Xiao Y, Wang Y, Molinero L, Chen DS, Krop I. Abstract 2859: Inhibition of PD-L1 by MPDL3280A leads to clinical activity in patients with metastatic triple-negative breast cancer (TNBC). Cancer Research. 2015; 75:2859. https:// doi.org/10.1158/1538-7445.am2015-2859
4. Dirix LY, Takacs I, Nikolinakos P, Jerusalem G, Arkenau HT, Hamilton EP, von Heydebreck A, Grote HJ, Chin K, Lippman ME. Abstract S1-04: Avelumab (MSB0010718C), an anti-PD-L1 antibody, in patients with locally advanced or metastatic breast cancer: A phase Ib JAVELIN solid tumor trial. Cancer Research. 2016; 76:S1-04
5. Finn RS, Martin M, Rugo HS, Jones S, Im SA, Gelmon K, Harbeck N, Lipatov ON, Walshe JM, Moulder S, Gauthier E, Lu DR, Randolph S, et al. Palbociclib and Letrozole in Advanced Breast Cancer. New England Journal of Medicine. 2016; 375:1925-36. https://doi.org/doi:10.1056/ NEJMoa1607303
6. Curran MA, Montalvo W, Yagita H, Allison JP. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci U S A. 2010; 107:4275-80. https://doi.org/10.1073/pnas.0915174107
7. Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, Ferrucci PF, Hill A, Wagstaff J, et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med. 2015; 373:23-34. https://doi.org/10.1056/NEJMoa1504030
8. Nakamura Y. Immunopharmacogenomics. Springer. 2015
9. Choudhury N, Nakamura Y. Importance of immunopharmacogenomics in cancer treatment: Patient selection and monitoring for immune checkpoint antibodies. Cancer Sci. 2016; 107:107-15. https://doi.org/10.1111/ cas.12862
10. Liu X, Venkataraman G, Lin J, Kiyotani K, Smith S, Montoya M, Nakamura Y, Kline J. Highly clonal regulatory T-cell population in follicular lymphoma-inverse correlation with the diversity of CD8 T cells. Oncoimmunology. 2015; 4:e1002728. https://doi.org/10.1 080/2162402X.2014.1002728
11. Park JH, Jang M, Tarhan YE, Katagiri T, Sasa M, Miyoshi Y, Kalari KR, Suman VJ, Weinshilboum R, Wang L, Boughey JC, Goetz MP, Nakamura Y. Clonal expansion of antitumor T cells in breast cancer correlates with response to neoadjuvant chemotherapy. Int J Oncol. 2016; 49:471-8. https://doi.org/10.3892/ijo.2016.3540
12. Tamura K, Hazama S, Yamaguchi R, Imoto S, Takenouchi H, Inoue Y, Kanekiyo S, Shindo Y, Miyano S, Nakamura Y, Kiyotani K. Characterization of the T cell repertoire by deep T cell receptor sequencing in tissues and blood from patients with advanced colorectal cancer. Oncol Lett. 2016; 11:3643-9. https://doi.org/10.3892/ ol.2016.4465
13. Inoue H, Park JH, Kiyotani K, Zewde M, Miyashita A, Jinnin M, Kiniwa Y, Okuyama R, Tanaka R, Fujisawa Y, Kato H, Morita A, Asai J, et al. Intratumoral expression levels of PD-L1, GZMA, and HLA-A along with oligoclonal T cell expansion associate with response to nivolumab in metastatic melanoma. Oncoimmunology. 2016; 5:e1204507. https://doi.org/10.1080/2162402X.2016.1204507
14. Jang M, Yew PY, Hasegawa K, Ikeda Y, Fujiwara K, Fleming GF, Nakamura Y, Park JH. Characterization of T cell repertoire of blood, tumor, and ascites in ovarian cancer patients using next generation sequencing. Oncoimmunology. 2015; 4:e1030561. https://doi.org/10.1080/2162402X.2015.1030561
15. Adams S, Loi S, Toppmeyer D, Cescon DW, Laurentiis MD, Nanda R, Winer EP, Mukai H, Tamura K, Armstrong A, Liu MC, Iwata H, Ryvo L, et al. Phase 2 study of pembrolizumab as first-line therapy for PD-L1-positive metastatic triple-negative breast cancer (mTNBC): Preliminary data from KEYNOTE-086 cohort B. Journal of Clinical Oncology. 2017; 35:1088. https://doi.org/10.1200/ JCO.2017.35.15_suppl.1088
16. Adams S, Schmid P, Rugo HS, Winer EP, Loirat D, Awada A, Cescon DW, Iwata H, Campone M, Nanda R, Hui R, Curigliano G, Toppmeyer D, et al. Phase 2 study of pembrolizumab (pembro) monotherapy for previously treated metastatic triple-negative breast cancer (mTNBC): KEYNOTE-086 cohort A. Journal of Clinical Oncology. 2017; 35:1008. https://doi.org/10.1200/JCO.2017.35.15_suppl.1008
17. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, West AN, Carmona M, Kivork C, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014; 515:568-71. https://doi. org/10.1038/nature13954
18. Le DT, Durham JN, Smith KN, Wang H, Bartlett BR, Aulakh LK, Lu S, Kemberling H, Wilt C, Luber BS, Wong F, Azad NS, Rucki AA, et al. Mismatch-repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017; 357:409-413. https://doi.org/10.1126/science.aan6733
19. Santa-Maria CA, Park SJ, Jain S, Gradishar WJ. Breast cancer and immunology: biomarker and therapeutic developments. Expert Rev Anticancer Ther. 2015; 15:1215-22. https://doi.org/10.1586/14737140.2015.1086270
20. Dieu-Nosjean MC, Goc J, Giraldo NA, Sautes-Fridman C, Fridman WH. Tertiary lymphoid structures in cancer and beyond. Trends Immunol. 2014; 35:571-80. https://doi. org/10.1016/j.it.2014.09.006
21. Leisegang M, Engels B, Schreiber K, Yew PY, Kiyotani K, Idel C, Arina A, Duraiswamy J, Weichselbaum RR, Uckert W, Nakamura Y, Schreiber H. Eradication of Large Solid Tumors by Gene Therapy with a T-Cell Receptor Targeting a Single Cancer-Specific Point Mutation. Clin Cancer Res. 2016; 22:2734-43. https://doi.org/10.1158/1078-0432. CCR-15-2361
22. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25:1754-60. https://doi.org/10.1093/bioinformatics/btp324
23. 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. https://doi.org/10.1093/bioinformatics/btu548
24. Choudhury NJ, Kiyotani K, Yap KL, Campanile A, Antic T, Yew PY, Steinberg G, Park JH, Nakamura Y, O'Donnell PH. Low T-cell Receptor Diversity, High Somatic Mutation Burden and High Neoantigen Load as Predictors of Clinical Outcome in Muscle-invasive Bladder Cancer. European Urology Focus. 2016; 2:445-452. https://doi.org/http:// dx.doi.org/10.1016/j.euf.2015.09.007
25. Hoof I, Peters B, Sidney J, Pedersen LE, Sette A, Lund O, Buus S, Nielsen M. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics. 2009; 61:1-13. https://doi.org/10.1007/s00251-008-0341-z
26. Nielsen M, Lundegaard C, Blicher T, Lamberth K, Harndahl M, Justesen S, Roder G, Peters B, Sette A, Lund O, Buus S. NetMHCpan, a method for quantitative predictions of peptide binding to any HLA-A and-B locus protein of known sequence. PLoS One. 2007; 2:e796. https://doi. org/10.1371/journal.pone.0000796
27. Fang H, Yamaguchi R, Liu X, Daigo Y, Yew PY, Tanikawa C, Matsuda K, Imoto S, Miyano S, Nakamura Y. Quantitative T cell repertoire analysis by deep cDNA sequencing of T cell receptor alpha and beta chains using next-generation sequencing (NGS). Oncoimmunology. 2014; 3:e968467. https://doi.org/10.4161/21624011.2014.968467
28. Giudicelli V, Chaume D, Lefranc MP. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res. 2005; 33:D256-61. https://doi.org/10.1093/nar/gki010
29. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9:357-9. https://doi. org/10.1038/nmeth.1923
30. Lefranc MP, Giudicelli V, Kaas Q, Duprat E, Jabado-Michaloud J, Scaviner D, Ginestoux C, Clement O, Chaume D, Lefranc G. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 2005; 33:D593-7. https://doi.org/10.1093/nar/gki065