Interfaces of Malignant and Immunologic Clonal Dynamics in Ovarian Cancer

Cell

Volumn 173, Issue 7, 2018, Pages 1755-1769.e22

  Zhang, Allen W ^a,b,g   McPherson, Andrew ^a   Milne, Katy ^a   Kroeger, David R ^a   Hamilton, Phineas T ^a   Miranda, Alex ^a   Funnell, Tyler ^a,g   Little, Nicole ^a   de Souza, Camila P E ^a,g   Laan, Sonya ^a   LeDoux, Stacey ^a   Cochrane, Dawn R ^a   Lim, Jamie L P ^a   Yang, Winnie ^a   Roth, Andrew ^d   Smith, Maia A ^a   Ho, Julie ^e   Tse, Kane ^a   Zeng, Thomas ^a   Shlafman, Inna ^a   Mayo, Michael R ^a   Moore, Richard ^a   Failmezger, Henrik ^f   Heindl, Andreas ^f   Wang, Yi Kan ^a   Bashashati, Ali ^a   Grewal, Diljot S ^a   Brown, Scott D ^a,g   Lai, Daniel ^a   Wan, Adrian N C ^a   Nielsen, Cydney B ^g   Huebner, Curtis ^a   Tessier Cloutier, Basile ^g   Anglesio, Michael S ^g   Bouchard Côté, Alexandre ^g   Yuan, Yinyin ^f   Wasserman, Wyeth W ^b   Gilks, C Blake ^g   Karnezis, Anthony N ^g   Aparicio, Samuel ^a,g   McAlpine, Jessica N ^g   Huntsman, David G ^a,g   Holt, Robert A ^a   Nelson, Brad H ^a,c,g   Shah, Sohrab P ^a,g   more..

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b BC CHILDREN S HOSPITAL   (Canada)

^c UNIVERSITY OF VICTORIA   (Canada)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e VANCOUVER GENERAL HOSPITAL   (Canada)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

clonal evolution; clone; foldback inversion; HGSC; high grade serous ovarian cancer; HLA; human leukocyte antigen; immunoediting; intratumoral heterogeneity; metastatic; mutation signature; tumor infiltrating lymphocyte

Indexed keywords

B LYMPHOCYTE RECEPTOR; HLA ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; BRCA1 PROTEIN; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN; BRCA2 PROTEIN, HUMAN; CD8 ANTIGEN; HLA ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; TUMOR ANTIGEN;

ADULT; AGED; ARTICLE; CANCER CELL; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMAGE ANALYSIS; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; OVARY CANCER; PRIORITY JOURNAL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; VERY ELDERLY; WHOLE GENOME SEQUENCING; CANCER GRADING; CLASSIFICATION; CLUSTER ANALYSIS; CYTOLOGY; GENETICS; HETEROZYGOSITY LOSS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; OVARY TUMOR; PATHOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, NEOPLASM; BRCA1 PROTEIN; BRCA2 PROTEIN; CD8 ANTIGENS; CLUSTER ANALYSIS; FEMALE; HLA ANTIGENS; HUMANS; LOSS OF HETEROZYGOSITY; LYMPHOCYTES, TUMOR-INFILTRATING; MIDDLE AGED; NEOPLASM GRADING; OVARIAN NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, ANTIGEN, T-CELL; WHOLE GENOME SEQUENCING; YOUNG ADULT;

EID: 85046665554     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2018.03.073     Document Type: Article

References (53)

1. Auer, K., Bachmayr-Heyda, A., Sukhbaatar, N., Aust, S., Schmetterer, K.G., Meier, S.M., Gerner, C., Grimm, C., Horvat, R., Pils, D., Role of the immune system in the peritoneal tumor spread of high grade serous ovarian cancer. Oncotarget 7 (2016), 61336–61354.
2. 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.
3. Bell, D., Berchuck, A., Birrer, M., Chien, J., Cramer, D.W., Dao, F., Dhir, R., DiSaia, P., Gabra, H., Glenn, P., et al., Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 474 (2011), 609–615.
4. Bolotin, D.A., Poslavsky, S., Mitrophanov, I., Shugay, M., Mamedov, I.Z., Putintseva, E.V., Chudakov, D.M., MiXCR: software for comprehensive adaptive immunity profiling. Nat. Methods 12 (2015), 380–381.
5. Campbell, P.J., Yachida, S., Mudie, L.J., Stephens, P.J., Pleasance, E.D., Stebbings, L.A., Morsberger, L.A., Latimer, C., McLaren, S., Lin, M.-L., et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467 (2010), 1109–1113.
6. Cesano, A., nCounter(®) PanCancer Immune Profiling Panel (NanoString Technologies, Inc., Seattle, WA). J. Immunother. Cancer, 3, 2015, 42.
7. Ding, J., Bashashati, A., Roth, A., Oloumi, A., Tse, K., Zeng, T., Haffari, G., Hirst, M., Marra, M.A., Condon, A., et al. Feature-based classifiers for somatic mutation detection in tumour-normal paired sequencing data. Bioinformatics 28 (2012), 167–175.
8. Emerson, R., Sherwood, A., Desmarais, C., Malhotra, S., Phippard, D., Robins, H., Estimating the ratio of CD4+ to CD8+ T cells using high-throughput sequence data. J. Immunol. Methods 391 (2013), 14–21.
9. Funnell, T., Zhang, A., Shiah, Y.-J., Grewal, D., Lesurf, R., McKinney, S., Bashashati, A., Wang, Y.K., Boutros, P., Shah, S., Integrated single-nucleotide and structural variation signatures of DNA-repair deficient human cancers. bioRxiv, 2018, 10.1101/267500.
10. Gaillard, S.L., Secord, A.A., Monk, B., The role of immune checkpoint inhibition in the treatment of ovarian cancer. Gynecol. Oncol. Res. Pract., 3, 2016, 11.
11. Getis, A., Ord, J.K., The Analysis of Spatial Association by Use of Distance Statistics. Geogr. Anal. 24 (1992), 189–206.
12. Goode, E.L., Block, M.S., Kalli, K.R., Vierkant, R.A., Chen, W., Fogarty, Z.C., Gentry-Maharaj, A., Tołoczko, A., Hein, A., Bouligny, A.L., et al., Ovarian Tumor Tissue Analysis (OTTA) Consortium. Dose-Response Association of CD8+ Tumor-Infiltrating Lymphocytes and Survival Time in High-Grade Serous Ovarian Cancer. JAMA Oncol., 3, 2017, e173290.
13. Ha, G., Roth, A., Khattra, J., Ho, J., Yap, D., Prentice, L.M., Melnyk, N., McPherson, A., Bashashati, A., Laks, E., et al. TITAN: inference of copy number architectures in clonal cell populations from tumor whole-genome sequence data. Genome Res. 24 (2014), 1881–1893.
14. Heindl, A., Lan, C., Rodrigues, D.N., Koelble, K., Yuan, Y., Similarity and diversity of the tumor microenvironment in multiple metastases: critical implications for overall and progression-free survival of high-grade serous ovarian cancer. Oncotarget 7 (2016), 71123–71135.
15. Herbst, R.S., Soria, J.-C., Kowanetz, M., Fine, G.D., Hamid, O., Gordon, M.S., Sosman, J.A., McDermott, D.F., Powderly, J.D., Gettinger, S.N., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515 (2014), 563–567.
16. Homicsko, K., Coukos, G., Targeting Programmed Cell Death 1 in Ovarian Cancer. J. Clin. Oncol. 33 (2015), 3987–3989.
17. Hwang, W.-T., Adams, S.F., Tahirovic, E., Hagemann, I.S., Coukos, G., Prognostic significance of tumor-infiltrating T cells in ovarian cancer: a meta-analysis. Gynecol. Oncol. 124 (2012), 192–198.
18. Jiménez-Sánchez, A., Memon, D., Pourpe, S., Veeraraghavan, H., Li, Y., Vargas, H.A., Gill, M.B., Park, K.J., Zivanovic, O., Konner, J., et al. Heterogeneous Tumor-Immune Microenvironments among Differentially Growing Metastases in an Ovarian Cancer Patient. Cell 170 (2017), 927–938.
19. Joshi, P.M., Sutor, S.L., Huntoon, C.J., Karnitz, L.M., Ovarian cancer-associated mutations disable catalytic activity of CDK12, a kinase that promotes homologous recombination repair and resistance to cisplatin and poly(ADP-ribose) polymerase inhibitors. J. Biol. Chem. 289 (2014), 9247–9253.
20. Klarenbeek, P.L., Doorenspleet, M.E., Esveldt, R.E.E., van Schaik, B.D.C., Lardy, N., van Kampen, A.H.C., Tak, P.P., Plenge, R.M., Baas, F., de Bakker, P.I.W., de Vries, N., Somatic Variation of T-Cell Receptor Genes Strongly Associate with HLA Class Restriction. PLoS ONE, 10, 2015, e0140815.
21. Kroeger, D.R., Milne, K., Nelson, B.H., Tumor-Infiltrating Plasma Cells Are Associated with Tertiary Lymphoid Structures, Cytolytic T-Cell Responses, and Superior Prognosis in Ovarian Cancer. Clin. Cancer Res. 22 (2016), 3005–3015.
22. Le, D.T., Uram, J.N., Wang, H., Bartlett, B.R., Kemberling, H., Eyring, A.D., Skora, A.D., Luber, B.S., Azad, N.S., Laheru, D., et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency. N. Engl. J. Med. 372 (2015), 2509–2520.
23. Leong, H.S., Galletta, L., Etemadmoghadam, D., George, J., Köbel, M., Ramus, S.J., Bowtell, D., Australian Ovarian Cancer Study. Efficient molecular subtype classification of high-grade serous ovarian cancer. J. Pathol. 236 (2015), 272–277.
24. Li, H., Durbin, R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (2009), 1754–1760.
25. Li, H.M., Hiroi, T., Zhang, Y., Shi, A., Chen, G., De, S., Metter, E.J., Wood, W.H. 3rd, Sharov, A., Milner, J.D., et al. TCRβ repertoire of CD4+ and CD8+ T cells is distinct in richness, distribution, and CDR3 amino acid composition. J. Leukoc. Biol. 99 (2016), 505–513.
26. Lipinski, K.A., Barber, L.J., Davies, M.N., Ashenden, M., Sottoriva, A., Gerlinger, M., Cancer Evolution and the Limits of Predictability in Precision Cancer Medicine. Trends in cancer 2 (2016), 49–63.
27. Lo, C.S., Sanii, S., Kroeger, D.R., Milne, K., Talhouk, A., Chiu, D.S., Rahimi, K., Shaw, P.A., Clarke, B.A., Nelson, B.H., Neoadjuvant Chemotherapy of Ovarian Cancer Results in Three Patterns of Tumor-Infiltrating Lymphocyte Response with Distinct Implications for Immunotherapy. Clin. Cancer Res. 23 (2017), 925–934.
28. 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. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science (80-.) 351 (2016), 1463–1469.
29. McGranahan, N., Rosenthal, R., Hiley, C.T., Rowan, A.J., Watkins, T.B.K., Wilson, G.A., Birkbak, N.J., Veeriah, S., Van Loo, P., Herrero, J., Swanton, C., TRACERx Consortium. Allele-Specific HLA Loss and Immune Escape in Lung Cancer Evolution. Cell 171 (2017), 1259–1271.
30. McPherson, A., Roth, A., Laks, E., Masud, T., Bashashati, A., Zhang, A.W., Ha, G., Biele, J., Yap, D., Wan, A., et al. Divergent modes of clonal spread and intraperitoneal mixing in high-grade serous ovarian cancer. Nat. Genet. 48 (2016), 758–767.
31. McPherson, A., Shah, S.P., Sahinalp, S.C., deStruct: Accurate Rearrangement Detection using Breakpoint Specific Realignment. bioRxiv, 2017, 10.1101/117523.
32. McPherson, A.W., Roth, A., Ha, G., Chauve, C., Steif, A., de Souza, C.P.E., Eirew, P., Bouchard-Côté, A., Aparicio, S., Sahinalp, S.C., Shah, S.P., ReMixT: clone-specific genomic structure estimation in cancer. Genome Biol., 18, 2017, 140.
33. Mirza, M.R., Monk, B.J., Herrstedt, J., Oza, A.M., Mahner, S., Redondo, A., Fabbro, M., Ledermann, J.A., Lorusso, D., Vergote, I., et al., ENGOT-OV16/NOVA Investigators. Niraparib Maintenance Therapy in Platinum-Sensitive, Recurrent Ovarian Cancer. N. Engl. J. Med. 375 (2016), 2154–2164.
34. Nawaz, S., Heindl, A., Koelble, K., Yuan, Y., Beyond immune density: critical role of spatial heterogeneity in estrogen receptor-negative breast cancer. Mod. Pathol. 28 (2015), 766–777.
35. Nelson, B.H., New insights into tumor immunity revealed by the unique genetic and genomic aspects of ovarian cancer. Curr. Opin. Immunol. 33 (2015), 93–100.
36. Nielsen, J.S., Sahota, R.A., Milne, K., Kost, S.E., Nesslinger, N.J., Watson, P.H., Nelson, B.H., CD20+ tumor-infiltrating lymphocytes have an atypical CD27- memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin. Cancer Res. 18 (2012), 3281–3292.
37. Nik-Zainal, S., Davies, H., Staaf, J., Ramakrishna, M., Glodzik, D., Zou, X., Martincorena, I., Alexandrov, L.B., Martin, S., Wedge, D.C., et al. Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature 534 (2016), 47–54.
38. 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.
39. Popova, T., Manié, E., Boeva, V., Battistella, A., Goundiam, O., Smith, N.K., Mueller, C.R., Raynal, V., Mariani, O., Sastre-Garau, X., Stern, M.H., Ovarian Cancers Harboring Inactivating Mutations in CDK12 Display a Distinct Genomic Instability Pattern Characterized by Large Tandem Duplications. Cancer Res. 76 (2016), 1882–1891.
40. 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.
41. 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.
42. Saunders, C.T., Wong, W.S.W., Swamy, S., Becq, J., Murray, L.J., Cheetham, R.K., Strelka: accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics 28 (2012), 1811–1817.
43. Schwarz, R.F., Ng, C.K.Y., Cooke, S.L., Newman, S., Temple, J., Piskorz, A.M., Gale, D., Sayal, K., Murtaza, M., Baldwin, P.J., et al. Spatial and temporal heterogeneity in high-grade serous ovarian cancer: a phylogenetic analysis. PLoS Med., 12, 2015, e1001789.
44. Smid, M., Rodríguez-González, F.G., Sieuwerts, A.M., Salgado, R., Prager-Van der Smissen, W.J.C., Vlugt-Daane, M.V., van Galen, A., Nik-Zainal, S., Staaf, J., Brinkman, A.B., et al. Breast cancer genome and transcriptome integration implicates specific mutational signatures with immune cell infiltration. Nat. Commun., 7, 2016, 12910.
45. Spranger, S., Spaapen, R.M., Zha, Y., Williams, J., Meng, Y., Ha, T.T., Gajewski, T.F., Up-Regulation of PD-L1, IDO, and Tregs in the Melanoma Tumor Microenvironment Is Driven by CD8+ T Cells. Sci. Transl. Med., 5, 2013 200ra116.
46. 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.
47. Ternette, N., Yang, H., Partridge, T., Llano, A., Cedeño, S., Fischer, R., Charles, P.D., Dudek, N.L., Mothe, B., Crespo, M., et al. Defining the HLA class I-associated viral antigen repertoire from HIV-1-infected human cells. Eur. J. Immunol. 46 (2016), 60–69.
48. Tothill, R.W., Tinker, A.V., George, J., Brown, R., Fox, S.B., Lade, S., Johnson, D.S., Trivett, M.K., Etemadmoghadam, D., Locandro, B., et al., Australian Ovarian Cancer Study Group. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin. Cancer Res. 14 (2008), 5198–5208.
49. 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.
50. Wang, Y.K., Bashashati, A., Anglesio, M.S., Cochrane, D.R., Grewal, D.S., Ha, G., McPherson, A., Horlings, H.M., Senz, J., Prentice, L.M., et al. Genomic consequences of aberrant DNA repair mechanisms stratify ovarian cancer histotypes. Nat. Genet. 49 (2017), 856–865.
51. Wick, D.A., Webb, J.R., Nielsen, J.S., Martin, S.D., Kroeger, D.R., Milne, K., Castellarin, M., Twumasi-Boateng, K., Watson, P.H., Holt, R.A., Nelson, B.H., Surveillance of the tumor mutanome by T cells during progression from primary to recurrent ovarian cancer. Clin. Cancer Res. 20 (2014), 1125–1134.
52. Yoshihama, S., Roszik, J., Downs, I., Meissner, T.B., Vijayan, S., Chapuy, B., Sidiq, T., Shipp, M.A., Lizee, G.A., Kobayashi, K.S., NLRC5/MHC class I transactivator is a target for immune evasion in cancer. Proc. Natl. Acad. Sci. USA 113 (2016), 5999–6004.
53. 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.