Genome and transcriptome sequencing in prospective metastatic triple-negative breast cancer uncovers therapeutic vulnerabilities

Molecular Cancer Therapeutics

Volumn 12, Issue 1, 2013, Pages 104-116

  Craig, David W ^a   O'Shaughnessy, Joyce A ^b   Kiefer, Jeffrey A ^a   Aldrich, Jessica ^a   Sinari, Shripad ^a   Moses, Tracy M ^a   Wong, Shukmei ^a   Dinh, Jennifer ^a   Christoforides, Alexis ^a   Blum, Joanne L ^b   Aitelli, Cristi L ^c   Osborne, Cynthia R ^b   Izatt, Tyler ^a   Kurdoglu, Ahmet ^a   Baker, Angela ^a   Koeman, Julie ^e   Barbacioru, Catalin ^f   Sakarya, Onur ^f   De La Vega, Francisco M ^f   Siddiqui, Asim ^f   Hoang, Linh ^f   Billings, Paul R ^f   Salhia, Bodour ^a   Tolcher, Anthony W ^d   Trent, Jeffrey M ^a   Mousses, Spyro ^a   Von Hoff, Daniel ^a   Carpten, John D ^a   more..

^a TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^b BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^c TEXAS ONCOLOGY   (United States)

^d START Center for Cancer Care   (United States)

^e VAN ANDEL RESEARCH INSTITUTE   (United States)

^f Life Technologies   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P53; RAF PROTEIN; RAS PROTEIN;

AFRICAN AMERICAN; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE SEQUENCE; HUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; TRIPLE NEGATIVE BREAST CANCER;

ADULT; ALPHA CATENIN; BREAST NEOPLASMS; CHROMOSOMES, HUMAN, PAIR 7; DNA MUTATIONAL ANALYSIS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; GENES, NEOPLASM; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MIDDLE AGED; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; PROSPECTIVE STUDIES; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SEQUENCE ANALYSIS, RNA; SEQUENCE DELETION; SIGNAL TRANSDUCTION; TRANSCRIPTOME; TREATMENT OUTCOME; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84872585155     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0781     Document Type: Article

References (57)

1. Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med 2010;363:1938-48.
2. Rastelli F, Biancanelli S, Falzetta A, Martignetti A, Casi C, Bascioni R, et al. Triple-negative breast cancer: current state of the art. Tumori 2010;96:875-88.
3. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the socalled triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 2007;109:1721-8.
4. Huo D, Ikpatt F, Khramtsov A, Dangou JM, Nanda R, Dignam J, et al. Population differences in breast cancer: survey in indigenous African women reveals over-representation of triple-negative breast cancer. J Clin Oncol 2009;27:4515-21.
5. Agurs-Collins T, Dunn BK, Browne D, Johnson KA, Lubet R. Epidemiology of health disparities in relation to the biology of estrogen receptor-negative breast cancer. Semin Oncol 2010;37:384-401.
6. Stark A, Kleer CG, Martin I, Awuah B, Nsiah-Asare A, Takyi V, et al. African ancestry and higher prevalence of triple-negative breast cancer: findings from an international study. Cancer 2010;116:4926-32.
7. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001;98:10869-74.
8. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006;295:2492-502.
9. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005;434:917-21.
10. Perou CM. Molecular stratification of triple-negative breast cancers. Oncologist 2010;15(Suppl 5):39-48.
11. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010;12:R68.
12. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011;121:2750-67.
13. Reddy KB. Triple-negative breast cancers: an updated review on treatment options. Curr Oncol 2011;18:e173-179.
14. Chin K, DeVries S, Fridlyand J, Spellman PT, Roydasgupta R, Kuo WL, et al. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 2006;10:529-41.
15. Fridlyand J, Snijders AM, Ylstra B, Li H, Olshen A, Segraves R, et al. Breast tumor copy number aberration phenotypes and genomic instability. BMC Cancer 2006;6:96.
16. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006;10:515-27.
17. Loo LW, Wang Y, Flynn EM, Lund MJ, Bowles EJ, Buist DS, et al. Genome-wide copy number alterations in subtypes of invasive breast cancers in young white and African American women. Breast Cancer Res Treat 2011;127:297-308.
18. Weigman VJ, Chao HH, Shabalin AA, He X, Parker JS, Nordgard SH, et al. Basal-like Breast cancer DNA copy number losses identify genes involved in genomic instability, response to therapy, and patient survival. Breast Cancer Res Treat 2012;133:865-80.
19. Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW, et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010;464:999-1005.
20. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 2012;486:395-9.
21. Koboldt DC, Fulton RS, McLellan MD, Schmidt H, Kalicki-Veizer J, McMichael JF, et al. Comprehensive molecular portraits of human breast tumours. Nature 2012;490:61-70.
22. Tuch BB, Laborde RR, Xu X, Gu J, Chung CB, Monighetti CK, et al. Tumor transcriptome sequencing reveals allelic expression imbalances associated with copy number alterations. PloS ONE 2010;5: e9317.
23. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence Alignment/Map format and SAMtools. Bioinformatics 2009;25:2078-9.
24. Robbins CM, Tembe WA, Baker A, Sinari S, Moses TY, Beckstrom- Sternberg S, et al. Copy number and targeted mutational analysis reveals novel somatic events in metastatic prostate tumors. Genome Res 2011;21:47-55.
25. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010;20:1297-303.
26. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, et al. The Bioperl toolkit: Perl modules for the life sciences. Genome Res 2002;12:1611-8.
27. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010;26:139-40.
28. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010;11: R25.
29. Huusko P, Ponciano-Jackson D, Wolf M, Kiefer JA, Azorsa DO, Tuzmen S, et al. Nonsense-mediated decay microarray analysis identifies mutations of EPHB2 in human prostate cancer. Nat Genet 2004;36: 979-83.
30. Basu TN, Gutmann DH, Fletcher JA, Glover TW, Collins FS, Downward J. Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature 1992;356:713-5.
31. Banerjee S, Byrd JN, Gianino SM, Harpstrite SE, Rodriguez FJ, Tuskan RG, et al. The neurofibromatosis type 1 tumor suppressor controls cell growth by regulating signal transducer and activator of transcription-3 activity in vitro and in vivo. Cancer Res 2010;70:1356-66.
32. Shimizu T, Tolcher AW, Papadopoulos KP, Beeram M, Rasco DW, Smith LS, et al. The clinical effect of the dual-targeting strategy involving PI3K/AKT/mTOR and RAS/MEK/ERK pathways in first-inhuman phase I study: the START Center experience. J Clin Oncol 29: 2011 (suppl; abstr 2502).
33. Nik-Zainal S, Alexandrov LB, Wedge DC, Van Loo P, Greenman CD, Raine K, et al. Mutational processes molding the genomes of 21 breast cancers. Cell 2012;149:979-93.
34. Nik-Zainal S, Van Loo P,WedgeDC, Alexandrov LB, GreenmanCD, Lau KW, et al. The life history of 21 breast cancers. Cell 2012;149:994-1007.
35. Laoukili J, Kooistra MR, Bras A, Kauw J, Kerkhoven RM, Morrison A, et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 2005;7:126-36.
36. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 2011;474:609-15.
37. Lok GT, Chan DW, Liu VW, Hui WW, Leung TH, Yao KM, et al. Aberrant activation of ERK/FOXM1 signaling cascade triggers the cell migration/ invasion in ovarian cancer cells. PloS ONE 2011;6:e23790.
38. Kristensen VN, Vaske CJ, Ursini-Siegel J, Van Loo P, Nordgard SH, Sachidanandam R, et al. Integrated molecular profiles of invasive breast tumors and ductal carcinoma in situ (DCIS) reveal differential vascular and interleukin signaling. Proc Natl Acad Sci U S A 2012;109:2802-7.
39. Bar J, Feniger-Barish R, Lukashchuk N, Shaham H, Moskovits N, Goldfinger N, et al. Cancer cells suppress p53 in adjacent fibroblasts. Oncogene 2009;28:933-6.
40. Walker EJ, Zhang C, Castelo-Branco P, Hawkins C, Wilson W, Zhukova N, et al. Monoallelic expression determines oncogenic progression and outcome in benign and malignant brain tumors. Cancer Res 2012;72:636-44.
41. Fujita T, Igarashi J, Okawa ER, Gotoh T, Manne J, Kolla V, et al. CHD5, a tumor suppressor gene deleted from 1p36.31 in neuroblastomas. J Natl Cancer Inst 2008;100:940-9.
42. Chong-Kopera H, Inoki K, Li Y, Zhu T, Garcia-Gonzalo FR, Rosa JL, et al. TSC1 stabilizes TSC2 by inhibiting the interaction between TSC2 and the HERC1 ubiquitin ligase. J Biol Chem 2006;281:8313-6.
43. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008;455:1069-75.
44. Cowin PA, George J, Fereday S, Loehrer E, Van Loo P, Cullinane C, et al. lrp1b deletion in high-grade serous ovarian cancers is associated with acquired chemotherapy resistance to liposomal doxorubicin. Cancer Res 2012;72:4060-73.
45. Heck MM, Hittelman WN, Earnshaw WC. Differential expression of DNA topoisomerases I and II during the eukaryotic cell cycle. Proc Natl Acad Sci U S A 1988;85:1086-90.
46. Glynn RW, Mahon S, Curran C, Callagy G, Miller N, Kerin MJ. TOP2A amplification in the absence of that of HER-2/neu: toward individualization of chemotherapeutic practice in breast cancer. Oncologist 2011;16:949-55.
47. Nelson WJ. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem Soc Trans 2008;36:149-55.
48. Yoshida R, Kimura N, Harada Y, Ohuchi N. The loss of E-cadherin, alpha- and beta-catenin expression is associated with metastasis and poor prognosis in invasive breast cancer. Int J Oncol 2001;18: 513-20.
49. Lien WH, Klezovitch O, Fernandez TE, Delrow J, Vasioukhin V. AlphaEcatenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science 2006;311:1609-12.
50. Chuu CP, Chen RY, Barkinge JL, Ciaccio MF, Jones RB. Systems-level analysis of ErbB4 signaling in breast cancer: a laboratory to clinical perspective. Mol Cancer Res 2008;6:885-91.
51. Prickett TD, Agrawal NS, Wei X, Yates KE, Lin JC, Wunderlich JR, et al. Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat Genet 2009;41:1127-32.
52. Das PM, Thor AD, Edgerton SM, Barry SK, Chen DF, Jones FE. Reactivation of epigenetically silenced HER4/ERBB4 results in apoptosis of breast tumor cells. Oncogene 2010;29:5214-9.
53. Rexer BN, Ghosh R, Arteaga CL. Inhibition of PI3K and MEK: it is all about combinations and biomarkers. Clin Cancer Res 2009;15: 4518-20.
54. Mirzoeva OK, Das D, Heiser LM, Bhattacharya S, Siwak D, Gendelman R, et al. Basal subtype andMAPK/ERK kinase (MEK)-phosphoinositide 3-kinase feedback signaling determine susceptibility of breast cancer cells to MEK inhibition. Cancer Res 2009;69:565-72.
55. Hoeflich KP, O'Brien C, Boyd Z, Cavet G, Guerrero S, Jung K, et al. In vivo antitumor activity of MEK and phosphatidylinositol 3-kinase inhibitors in basal-like breast cancer models. Clin Cancer Res 2009;15:4649-64.
56. Agoulnik IU, Hodgson MC, Bowden WA, Ittmann MM. INPP4B: the new kid on the PI3K block. Oncotarget 2011;2:321-8.
57. Trivedi CM, Luo Y, Yin Z, Zhang M, Zhu W, Wang T, et al. Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat Med 2007;13:324-31.