Development and clinical application of an integrative genomic approach to personalized cancer therapy

Genome Medicine

Volumn 8, Issue 1, 2016, Pages

  Uzilov, Andrew V ^a   Ding, Wei ^a   Fink, Marc Y ^a,b   Antipin, Yevgeniy ^a   Brohl, Andrew S ^a,c   Davis, Claire ^a   Lau, Chun Yee ^a   Pandya, Chetanya ^a   Shah, Hardik ^a   Kasai, Yumi ^a   Powell, James ^a   Micchelli, Mark ^a   Castellanos, Rafael ^a   Zhang, Zhongyang ^a   Linderman, Michael ^a   Kinoshita, Yayoi ^a   Zweig, Micol ^a   Raustad, Katie ^a   Cheung, Kakit ^a   Castillo, Diane ^a   Wooten, Melissa ^a   Bourzgui, Imane ^a   Newman, Leah C ^a   Deikus, Gintaras ^a   Mathew, Bino ^a   Zhu, Jun ^a   Glicksberg, Benjamin S ^a   Moe, Aye S ^a   Liao, Jun ^a   Edelmann, Lisa ^a   Dudley, Joel T ^a   Maki, Robert G ^a   Kasarskis, Andrew ^a   Holcombe, Randall F ^a   Mahajan, Milind ^a   Hao, Ke ^a   Reva, Boris ^a   Longtine, Janina ^a   Starcevic, Daniela ^a   Sebra, Robert ^a   Donovan, Michael J ^a   Li, Shuyu ^a   Schadt, Eric E ^a   Chen, Rong ^a   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b LONG ISLAND UNIVERSITY   (United States)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Cancer; Clinical application; Genomics; Personalized medicine

Indexed keywords

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER PROGNOSIS; CANCER THERAPY; CHILD; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA MICROARRAY; FEMALE; GENOME ANALYSIS; HUMAN; HUMAN TISSUE; MALE; PERSONALIZED MEDICINE; PRIORITY JOURNAL; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; THYROID MEDULLARY CARCINOMA; WHOLE EXOME SEQUENCING; ADOLESCENT; EXOME; GENETIC VARIATION; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; MIDDLE AGED; NEOPLASMS; PATHOLOGY; PROCEDURES; PROGNOSIS; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; CHILD; DNA COPY NUMBER VARIATIONS; EXOME; FEMALE; GENETIC VARIATION; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; MIDDLE AGED; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; PRECISION MEDICINE; PROGNOSIS; YOUNG ADULT;

EID: 85007605354     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/s13073-016-0313-0     Document Type: Article

References (63)

1. Meric-Bernstam F, Johnson A, Holla V, Bailey AM, Brusco L, Chen K, et al. A decision support framework for genomically informed investigational cancer therapy. J Natl Cancer Inst. 2015;107:djv098. doi:10.1093/jnci/djv098.
2. Chmielecki J, Meyerson M. DNA sequencing of cancer: what have we learned Annu Rev Med. 2014;65:63-79. doi:10.1146/annurev-med-060712- 200152.
3. Garraway LA, Lander ES. Lessons from the cancer genome. Cell. 2013;153: 17-37. doi:10.1016/j.cell.2013.03.002.
4. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz Jr LA, Kinzler KW. Cancer genome landscapes. Science (New York, NY). 2013;339:1546-58. doi:10.1126/science.1235122.
5. Garraway LA. Genomics-driven oncology: framework for an emerging paradigm. J Clin Oncol. 2013;31:1806-14. doi:10.1200/jco.2012.46.8934.
6. Chen K, Meric-Bernstam F, Zhao H, Zhang Q, Ezzeddine N, Tang LY, et al. Clinical actionability enhanced through deep targeted sequencing of solid tumors. Clin Chem. 2015;61:544-53. doi:10.1373/clinchem.2014.231100.
7. Frampton GM, Fichtenholtz A, Otto GA, Wang K, Downing SR, He J, et al. Development and validation of a clinical cancer genomic profiling test based on massively parallel DNA sequencing. Nat Biotechnol. 2013;31: 1023-31. doi:10.1038/nbt.2696.
8. 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. doi:10.1126/scitranslmed. aaa7161.
9. Schwaederle M, Daniels GA, Piccioni DE, Fanta PT, Schwab RB, Shimabukuro KA, et al. On the road to precision cancer medicine: analysis of genomic biomarker actionability in 439 patients. Mol Cancer Ther. 2015;14:1488-94. doi:10.1158/1535-7163.mct-14-1061.
10. Roychowdhury S, Iyer MK, Robinson DR, Lonigro RJ, Wu YM, Cao X, et al. Personalized oncology through integrative high-throughput sequencing: a pilot study. Sci Transl Med. 2011;3:111ra21. doi:10.1126/scitranslmed. 3003161.
11. Van Allen EM, Wagle N, Stojanov P, Perrin DL, Cibulskis K, Marlow S, et al. Whole-exome sequencing and clinical interpretation of formalin-fixed, paraffin-embedded tumor samples to guide precision cancer medicine. Nat Med. 2014;20:682-8. doi:10.1038/nm.3559.
12. Beltran H, Eng K, Mosquera JM, Sigaras A, Romanel A, Rennert H, et al. Whole-exome sequencing of metastatic cancer and biomarkers of treatment response. JAMA Oncol. 2015;1:466-74. doi:10.1001/ jamaoncol.2015.1313.
13. Robinson D, Van Allen EM, Wu YM, Schultz N, Lonigro RJ, Mosquera JM, et al. Integrative clinical genomics of advanced prostate cancer. Cell. 2015;161: 1215-28. doi:10.1016/j.cell.2015.05.001.
14. Mody RJ, Wu YM, Lonigro RJ, Cao X, Roychowdhury S, Vats P, et al. Integrative clinical sequencing in the management of refractory or relapsed cancer in youth. JAMA. 2015;314:913-25. doi:10.1001/jama.2015.10080.
15. 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. doi:10.1038/nature12477.
16. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, et al. Mutational heterogeneity in cancer and the search for new cancerassociated genes. Nature. 2013;499:214-8. doi:10.1038/nature12213.
17. Gnant M, Harbeck N, Thomssen C. St. Gallen 2011: Summary of the Consensus Discussion. Breast Care (Basel, Switzerland). 2011;6:136-41. doi:10.1159/000328054.
18. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27:1160-7. doi:10.1200/jco.2008.18.1370.
19. Tibshirani R, Hastie T, Narasimhan B, Chu G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci U S A. 2002;99:6567-72. doi:10.1073/pnas.082099299.
20. Glicksberg BS, Li L, Cheng WY, Shameer K, Hakenberg J, Castellanos R, et al. An integrative pipeline for multi-modal discovery of disease relationships. Pac Symp Biocomput. 2015;20:407-18. http://dx.doi.org/10.1142/ 9789814644730_0039.
21. Ma M, Ru Y, Chuang LS, Hsu NY, Shi LS, Hakenberg J, et al. Disease-associated variants in different categories of disease located in distinct regulatory elements. BMC Genomics. 2015;16 Suppl 8:S3. doi:10.1186/1471-2164-16-s8-s3.
22. Stenson PD, Mort M, Ball EV, Shaw K, Phillips A, Cooper DN. The Human Gene Mutation Database: building a comprehensive mutation repository for clinical and molecular genetics, diagnostic testing and personalized genomic medicine. Hum Genet. 2014;133:1-9. doi:10.1007/s00439-013-1358-4.
23. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27-30.
24. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2016;44:D457-62. doi:10.1093/nar/gkv1070.
25. Forbes SA, Beare D, Gunasekaran P, Leung K, Bindal N, Boutselakis H, et al. COSMIC: exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res. 2015;43(Database issue):D805-11. doi:10.1093/nar/ gku1075.
26. Integrated genomic characterization of papillary thyroid carcinoma. Cell. 2014;159:676-90. doi:10.1016/j.cell.2014.09.050.
27. Zack TI, Schumacher SE, Carter SL, Cherniack AD, Saksena G, Tabak B, et al. Pan-cancer patterns of somatic copy number alteration. Nat Genet. 2013;45: 1134-40. doi:10.1038/ng.2760.
28. Zheng J. Oncogenic chromosomal translocations and human cancer (review). Oncol Rep. 2013;30:2011-9. doi:10.3892/or.2013.2677.
29. Agrawal N, Jiao Y, Sausen M, Leary R, Bettegowda C, Roberts NJ, et al. Exomic sequencing of medullary thyroid cancer reveals dominant and mutually exclusive oncogenic mutations in RET and RAS. J Clin Endocrinol Metab. 2013;98:E364-9. doi:10.1210/jc.2012-2703.
30. Cerrato A, De Falco V, Santoro M. Molecular genetics of medullary thyroid carcinoma: the quest for novel therapeutic targets. J Mol Endocrinol. 2009; 43:143-55. doi:10.1677/JME-09-0024.
31. Perri F, Pezzullo L, Chiofalo MG, Lastoria S, Di Gennaro F, Scarpati GD, et al. Targeted therapy: a new hope for thyroid carcinomas. Crit Rev Oncol Hematol. 2015;94:55-63. doi:10.1016/j.critrevonc.2014.10.012
32. Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature. 2012;487:330-7. doi:10.1038/nature11252.
33. Powell E, Piwnica-Worms D, Piwnica-Worms H. Contribution of p53 to metastasis. Cancer Discov. 2014;4:405-14. doi:10.1158/2159-8290.cd-13-0136.
34. Jacobs B, De Roock W, Piessevaux H, Van Oirbeek R, Biesmans B, De Schutter J, et al. Amphiregulin and epiregulin mRNA expression in primary tumors predicts outcome in metastatic colorectal cancer treated with cetuximab. J Clin Oncol. 2009;27:5068-74. doi:10.1200/jco.2008.21.3744.
35. Khambata-Ford S, Garrett CR, Meropol NJ, Basik M, Harbison CT, Wu S, et al. Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol. 2007;25:3230-7. doi:10.1200/jco.2006.10.5437.
36. Peifer M, Fernandez-Cuesta L, Sos ML, George J, Seidel D, Kasper LH, et al. Integrative genome analyses identify key somatic driver mutations of smallcell lung cancer. Nat Genet. 2012;44:1104-10. doi:10.1038/ng.2396.
37. Turner NC, Reis-Filho JS. Tackling the diversity of triple-negative breast cancer. Clin Cancer Res. 2013;19:6380-8. doi:10.1158/1078-0432.CCR-13-0915.
38. Tilch E, Seidens T, Cocciardi S, Reid LE, Byrne D, Simpson PT, et al. Mutations in EGFR, BRAF and RAS are rare in triple-negative and basal-like breast cancers from Caucasian women. Breast Cancer Res Treat. 2014;143:385-92. doi:10.1007/s10549-013-2798-1.
39. Craig DW, O'Shaughnessy JA, Kiefer JA, Aldrich J, Sinari S, Moses TM, et al. Genome and transcriptome sequencing in prospective metastatic triplenegative breast cancer uncovers therapeutic vulnerabilities. Mol Cancer Ther. 2013;12:104-16. doi:10.1158/1535-7163.MCT-12-0781.
40. Eroles P, Bosch A, Perez-Fidalgo JA, Lluch A. Molecular biology in breast cancer: intrinsic subtypes and signaling pathways. Cancer Treat Rev. 2012;38: 698-707. doi:10.1016/j.ctrv.2011.11.005.
41. Kim HS, Park I, Cho HJ, Gwak G, Yang K, Bae BN, et al. Analysis of the potent prognostic factors in luminal-type breast cancer. J Breast Cancer. 2012;15: 401-6. doi:10.4048/jbc.2012.15.4.401.
42. Giordano A, Tagliabue E, Pupa SM. Promise and failure of targeted therapy in breast cancer. Front Biosci (Schol Ed). 2012;4:356-74.
43. Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol. 2010;28:2784-95. doi:10.1200/jco.2009.25.6529.
44. Kurosawa A, Adachi N. Functions and regulation of Artemis: a goddess in the maintenance of genome integrity. J Radiat Res. 2010;51:503-9.
45. Byrski T, Dent R, Blecharz P, Foszczynska-Kloda M, Gronwald J, Huzarski T, et al. Results of a phase II open-label, non-randomized trial of cisplatin chemotherapy in patients with BRCA1-positive metastatic breast cancer. Breast Cancer Res. 2012;14:R110. doi:10.1186/bcr3231.
46. Isakoff SJ, Mayer EL, He L, Traina TA, Carey LA, Krag KJ, et al. TBCRC009: A multicenter phase II clinical trial of platinum monotherapy with biomarker assessment in metastatic triple-negative breast cancer. J Clin Oncol. 2015;33: 1902-9. doi:10.1200/jco.2014.57.6660.
47. 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. doi:10.1056/NEJMoa1406498.
48. Robinson GW, Orr BA, Gajjar A. Complete clinical regression of a BRAF V600E-mutant pediatric glioblastoma multiforme after BRAF inhibitor therapy. BMC Cancer. 2014;14:258. doi:10.1186/1471-2407-14-258.
49. Ammoun S, Ristic N, Matthies C, Hilton DA, Hanemann CO. Targeting ERK1/activation and proliferation in human primary schwannoma cells with MEK1/2 inhibitor AZD6244. Neurobiol Dis. 2010;37:141-6. doi:10.1016/j.nbd. 2009.09.017.
50. Jessen WJ, Miller SJ, Jousma E, Wu J, Rizvi TA, Brundage ME, et al. MEK inhibition exhibits efficacy in human and mouse neurofibromatosis tumors. J Clin Invest. 2013;123:340-7. doi:10.1172/jci60578.
51. Johansson G, Mahller YY, Collins MH, Kim MO, Nobukuni T, Perentesis J, et al. Effective in vivo targeting of the mammalian target of rapamycin pathway in malignant peripheral nerve sheath tumors. Mol Cancer Ther. 2008;7:1237-45. doi:10.1158/1535-7163.mct-07-2335.
52. Dalgliesh GL, Furge K, Greenman C, Chen L, Bignell G, Butler A, et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature. 2010;463:360-3. doi:10.1038/nature08672.
53. Iyer G, Hanrahan AJ, Milowsky MI, Al-Ahmadie H, Scott SN, Janakiraman M, et al. Genome sequencing identifies a basis for everolimus sensitivity. Science (New York, NY). 2012;338:221. doi:10.1126/science.1226344.
54. Huynh H, Hao HX, Chan SL, Chen D, Ong R, Soo KC, et al. Loss of tuberous sclerosis complex 2 (TSC2) is frequent in hepatocellular carcinoma and predicts response to mTORC1 inhibitor everolimus. Mol Cancer Ther. 2015; 14:1224-35. doi:10.1158/1535-7163.mct-14-0768.
55. Franz DN. Everolimus in the treatment of subependymal giant cell astrocytomas, angiomyolipomas, and pulmonary and skin lesions associated with tuberous sclerosis complex. Biologics. 2013;7:211-21. doi:10.2147/btt.s25095.
56. Ferguson KM, Berger MB, Mendrola JM, Cho HS, Leahy DJ, Lemmon MA. EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol Cell. 2003;11:507-17.
57. Dahlman KB, Xia J, Hutchinson K, Ng C, Hucks D, Jia P, et al. BRAF(L597) mutations in melanoma are associated with sensitivity to MEK inhibitors. Cancer Discov. 2012;2:791-7. doi:10.1158/2159-8290.cd-12-0097.
58. Garraway LA, Baselga J. Whole-genome sequencing and cancer therapy: is too much ever enough Cancer Discov. 2012;2:766-8. doi:10.1158/2159- 8290.cd-12-0359.
59. Ooms LM, Horan KA, Rahman P, Seaton G, Gurung R, Kethesparan DS, et al. The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem J. 2009;419:29-49. doi:10.1042/bj20081673.
60. Tai D, Wells K, Arcaroli J, Vanderbilt C, Aisner DL, Messersmith WA, et al. Targeting the WNT signaling pathway in cancer therapeutics. Oncologist. 2015;20:1189-98. doi:10.1634/theoncologist.2015-0057.
61. Zhang Z, Hao K. SAAS-CNV: a joint segmentation approach on aggregated and allele specific signals for the identification of somatic copy number alterations with next-generation sequencing data. PLoS Comput Biol. 2015; 11:e1004618. doi:10.1371/journal.pcbi.1004618.
62. Meric-Bernstam F, Brusco L, Shaw K, Horombe C, Kopetz S, Davies MA, et al. feasibility of large-scale genomic testing to facilitate enrollment onto genomically matched clinical trials. J Clin Oncol. 2015;33:2753-62. doi:10.1200/jco.2014.60.4165.
63. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44:D279-85. doi:10.1093/nar/gkv1344.