Scalable whole-exome sequencing of cell-free DNA reveals high concordance with metastatic tumors

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Adalsteinsson, Viktor A ^a,b   Ha, Gavin ^a,c,d   Freeman, Samuel S ^a,d   Choudhury, Atish D ^c   Stover, Daniel G ^c,d   Parsons, Heather A ^c,d   Gydush, Gregory ^a   Reed, Sarah C ^a   Rotem, Denisse ^a   Rhoades, Justin ^a   Loginov, Denis ^a,b   Livitz, Dimitri ^a   Rosebrock, Daniel ^a,d   Leshchiner, Ignaty ^a   Kim, Jaegil ^a   Stewart, Chip ^a   Rosenberg, Mara ^a   Francis, Joshua M ^a,c   Zhang, Cheng Zhong ^a,c,d   Cohen, Ofir ^a,c   Oh, Coyin ^a   Ding, Huiming ^b   Polak, Paz ^a,d,e   Lloyd, Max ^c   Mahmud, Sairah ^c   Helvie, Karla ^c   Merrill, Margaret S ^c   Santiago, Rebecca A ^c   O'Connor, Edward P ^c   Jeong, Seong H ^c   Leeson, Rachel ^b   Barry, Rachel M ^b   Kramkowski, Joseph F ^c   Zhang, Zhenwei ^c   Polacek, Laura ^c   Lohr, Jens G ^a,c   Schleicher, Molly ^a   Lipscomb, Emily ^a   Saltzman, Andrea ^a   Oliver, Nelly M ^c   Marini, Lori ^c   Waks, Adrienne G ^c,f   Harshman, Lauren C ^c   Tolaney, Sara M ^c   Van Allen, Eliezer M ^a,c,d,f   Winer, Eric P ^c   Lin, Nancy U ^c   Nakabayashi, Mari ^c,d   Taplin, Mary Ellen ^c   Johannessen, Cory M ^a   Garraway, Levi A ^a,c,d,f,g   Golub, Todd R ^a,c,d,g   Boehm, Jesse S ^a   Wagle, Nikhil ^a,c,d   Getz, Gad ^a,d,e   Love, J Christopher ^a,b   Meyerson, Matthew ^a,c,d,f   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABIRATERONE; APALUTAMIDE; AROMATASE INHIBITOR; ATM PROTEIN; CCND1 PROTEIN; CELL FREE DNA; CRIZOTINIB; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; DNA; DUTASTERIDE; ENZALUTAMIDE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESR1 PROTEIN; ESTROGEN RECEPTOR; GLUCOCORTICOID; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN P53; RB1 PROTEIN; RETINOBLASTOMA BINDING PROTEIN 2; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG; CELL FREE NUCLEIC ACID; TUMOR ANTIGEN;

BIOINFORMATICS; BIOTECHNOLOGY; BLOOD; DISEASE TREATMENT; DNA; GENETIC ANALYSIS; GENOME; MUTATION; SOFTWARE; TUMOR;

ARTICLE; BLOOD SAMPLING; CASTRATION RESISTANT PROSTATE CANCER; CELL FREE SYSTEM; CIRCULATING TUMOR CELL; CLINICAL ASSESSMENT; COHORT ANALYSIS; CONTROLLED STUDY; COPY NUMBER VARIATION; FEMALE; GENE MUTATION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; METASTATIC BREAST CANCER; OUTCOME ASSESSMENT; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); SOFTWARE; SOMATIC MUTATION; TUMOR BIOPSY; TUMOR GENE; WHOLE EXOME SEQUENCING; BLOOD; BREAST TUMOR; DNA MUTATIONAL ANALYSIS; GENE DOSAGE; GENETICS; METASTASIS; PROCEDURES; PROSPECTIVE STUDY; PROSTATE TUMOR; SECONDARY; STATISTICS AND NUMERICAL DATA;

ANTIGENS, NEOPLASM; BREAST NEOPLASMS; CELL-FREE NUCLEIC ACIDS; DNA MUTATIONAL ANALYSIS; DNA, NEOPLASM; FEMALE; GENE DOSAGE; HUMANS; MALE; NEOPLASM METASTASIS; PROSPECTIVE STUDIES; PROSTATIC NEOPLASMS; SOFTWARE; WHOLE EXOME SEQUENCING;

EID: 85032954984     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00965-y     Document Type: Article

References (63)

1. Diehl, F. et al. Circulating mutant DNA to assess tumor dynamics. Nat. Med. 14, 985-990 (2008).
2. Dawson, S.-J. et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl. J. Med. 368, 1199-1209 (2013).
3. Newman, A. M. et al. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat. Med. 20, 548-554 (2014).
4. Bettegowda, C. et al. Detection of circulating tumor DNA in early- and latestage human malignancies. Sci. Transl. Med. 6, 224ra24 (2014).
5. Russo, M. et al. Tumor heterogeneity and lesion-specific response to targeted therapy in colorectal cancer. Cancer Discov. 6, 147-153 (2015).
6. Lanman, R. B. et al. Analytical and clinical validation of a digital sequencing panel for quantitative, highly accurate evaluation of cell-free circulating tumor DNA. PLoS ONE 10, e0140712 (2015).
7. Newman, A. M. et al. Integrated digital error suppression for improved detection of circulating tumor DNA. Nat. Biotechnol. 34, 547-555 (2016).
8. Murtaza, M. et al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 497, 108-112 (2013).
9. Murtaza, M. et al. Multifocal clonal evolution characterized using circulating tumour DNA in a case of metastatic breast cancer. Nat. Commun. 6, 8760 (2015).
10. Butler, T. M. et al. Exome sequencing of cell-free DNA from metastatic cancer patients identifies clinically actionable mutations distinct from primary disease. PLoS ONE 10, e0136407 (2015).
11. Cibulskis, K. et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31, 213-219 (2013).
12. Beroukhim, R. et al. The landscape of somatic copy-number alteration across human cancers. Nature 463, 899-905 (2010).
13. Heitzer, E. et al. Tumor-associated copy number changes in the circulation of patients with prostate cancer identified through whole-genome sequencing. Genome Med. 5, 30 (2013).
14. Leary, R. J. et al. Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci. Transl. Med. 4, 162ra154 (2012).
15. Chan, K. C. A. et al. Noninvasive detection of cancer-associated genome-wide hypomethylation and copy number aberrations by plasma DNA bisulfite sequencing. Proc. Natl Acad. Sci. USA 110, 18761-18768 (2013).
16. Carter, S. L. et al. Absolute quantification of somatic DNA alterations in human cancer. Nat. Biotechnol. 30, 413-421 (2012).
17. Ha, G. et al. TITAN: inference of copy number architectures in clonal cell populations from tumor whole-genome sequence data. Genome Res. 24, 1881-1893 (2014).
18. Snyder, M. W., Martin, K., Hill, A. J., Daza, R. M. & Shendure, J. Cell-free DNA comprises an in vivo nucleosome footprint that informs its tissues-of-origin. Cell 164, 57-68 (2016).
19. Szpechcinski, A. et al. Cell-free DNA levels in plasma of patients with nonsmall-cell lung cancer and inflammatory lung disease. Br. J. Cancer 113, 476-483 (2015).
20. Robinson, D. et al. Integrative clinical genomics of advanced prostate cancer. Cell 161, 1215-1228 (2015).
21. Grasso, C. S. et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 487, 239-243 (2012).
22. Van Allen, E. M. et al. Whole-exome sequencing and clinical interpretation of formalin-fixed, paraffin-embedded tumor samples to guide precision cancer medicine. Nat. Med. 20, 682-688 (2014).
23. Lawrence, M. S. et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499, 214-218 (2013).
24. Lawrence, M. S. et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 505, 495-501 (2014).
25. Ciriello, G. et al. Comprehensive molecular portraits of invasive lobular breast cancer. Cell 163, 506-519 (2015).
26. Cohen, O. et al. Whole Exome and Transcriptome Sequencing of Resistant ER+ Metastatic Breast Cancer. In Proc. 2016 San Antonio Breast Cancer Symposium Abstr. S1-01 (2016).
27. Alexandrov, L. B., Nik-Zainal, S., Siu, H. C., Leung, S. Y. & Stratton, M. R. A mutational signature in gastric cancer suggests therapeutic strategies. Nat. Commun. 6, 8683 (2015).
28. Kasar, S. et al. Whole-genome sequencing reveals activation-induced cytidine deaminase signatures during indolent chronic lymphocytic leukaemia evolution. Nat. Commun. 6, 8866 (2015).
29. Kim, J. et al. Somatic ERCC2 mutations are associated with a distinct genomic signature in urothelial tumors. Nat. Genet. 48, 600-606 (2016).
30. Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415-421 (2013).
31. Mateo, J. et al. DNA-repair defects and olaparib in metastatic prostate cancer. N. Engl. J. Med. 373, 1697-1708 (2015).
32. Rizvi, N. A. et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348, 124-128 (2015).
33. Hoof, I. et al. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics 61, 1-13 (2009).
34. Shukla, S. A. et al. Comprehensive analysis of cancer-associated somatic mutations in class I HLA genes. Nat. Biotechnol. 33, 1152-1158 (2015).
35. Nielsen, M. et al. NetMHCpan, a method for quantitative predictions of peptide binding to any HLA-A and -B locus protein of known sequence. PLoS ONE 2, e796 (2007).
36. Curtis, C. et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486, 346-352 (2012).
37. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70 (2012).
38. Gundem, G. et al. The evolutionary history of lethal metastatic prostate cancer. Nature 520, 353-357 (2015).
39. Brastianos, P. K. et al. Genomic characterization of brain metastases reveals branched evolution and potential therapeutic targets. Cancer Discov. 5, 1164-1177 (2015).
40. Sun, K. et al. Plasma DNA tissue mapping by genome-wide methylation sequencing for noninvasive prenatal, cancer, and transplantation assessments. Proc. Natl Acad. Sci. USA 112, E5503-E5512 (2015).
41. Lohr, J. G. et al. Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer. Nat. Biotechnol. 32, 479-484 (2014).
42. Oh, W. K. et al. Development of an integrated prostate cancer research information system. Clin. Genitourin. Cancer 5, 61-66 (2006).
43. Ha, G. et al. Integrative analysis of genome-wide loss of heterozygosity and monoallelic expression at nucleotide resolution reveals disrupted pathways in triple-negative breast cancer. Genome Res. 22, 1995-2007 (2012).
44. Van Loo, P. et al. Allele-specific copy number analysis of tumors. Proc. Natl Acad. Sci. USA 107, 1-6 (2010).
45. Yau, C. et al. A statistical approach for detecting genomic aberrations in heterogeneous tumor samples from single nucleotide polymorphism genotyping data. Genome Biol. 11, R92 (2010).
46. Chapman, M. A. et al. Initial genome sequencing and analysis of multiple myeloma. Nature 471, 467-472 (2011).
47. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
48. Berger, M. F. et al. The genomic complexity of primary human prostate cancer. Nature 470, 214-220 (2012).
49. Cibulskis, K. et al. ContEst: estimating cross-contamination of human samples in next-generation sequencing data. Bioinformatics 27, 2601-2602 (2011).
50. Costello, M. et al. Discovery and characterization of artifactual mutations in deep coverage targeted capture sequencing data due to oxidative dna damage during sample preparation. Nucleic Acids Res. 41, e67 (2013).
51. Ramos, A. H. et al. Oncotator: cancer variant annotation tool. Hum. Mutat. 36, E2423-E2429 (2015).
52. Saunders, C. T. et al. Strelka: accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics 28, 1811-1817 (2012).
53. Olshen, A. B., Venkatraman, E. S., Lucito, R. & Wigler, M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 5, 557-572 (2004).
54. Venkatraman, E. S. & Olshen, A. B. A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23, 657-663 (2007).
55. McKenna, A. et al. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
56. Landau, D. A. et al. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 152, 714-726 (2013).
57. Harrow, J. et al. GENCODE: the reference human genome annotation for the ENCODE project. Genome Res. 22, 1760-1774 (2012).
58. Stachler, M. D. et al. Paired exome analysis of Barrett's esophagus and adenocarcinoma. Nat. Genet. 47, 1047-1055 (2015).
59. Kasar, S. et al. Whole-genome sequencing reveals activation-induced cytidine deaminase signatures during indolent chronic lymphocytic leukaemia evolution. Nat. Commun. 6, 8866 (2015).
60. Tan, V. Y. F. & Fevotte, C. Automatic relevance determination in nonnegative matrix factorization with the beta-divergence. IEEE Trans. Pattern Anal. Mach. Intell. 35, 1592-1605 (2013).
61. Alexandrov, L. B., Nik-Zainal, S., Wedge, D. C., Campbell, P. J. & Stratton, M. R. Deciphering signatures of mutational processes operative in human cancer. Cell Rep. 3, 246-259 (2013).
62. Shukla, S. A. et al. Comprehensive analysis of cancer-associated somatic mutations in class I HLA genes. Nat. Biotechnol. 33, 1152-1158 (2015).
63. Hoof, I. et al. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics 61, 1-13 (2009).