Sensitive detection of mono- and polyclonal ESR1 mutations in primary tumors, metastatic lesions, and cell-free DNA of breast cancer patients

Clinical Cancer Research

Volumn 22, Issue 5, 2016, Pages 1130-1137

  Wang, Peilu ^a,b   Bahreini, Amir ^b,c   Gyanchandani, Rekha ^b,d   Lucas, Peter C ^d   Hartmaier, Ryan J ^b,d   Watters, Rebecca J ^b,d   Jonnalagadda, Amruth R ^b   Trejo Bittar, Humberto E ^d   Berg, Aaron ^d   Hamilton, Ronald L ^d   Kurland, Brenda F ^e   Weiss, Kurt R ^f   Mathew, Aju ^g   Leone, Jose Pablo ^g   Davidson, Nancy E ^b,g   Nikiforova, Marina N ^d   Brufsky, Adam M ^b,g   Ambros, Tadeu F ^g   Stern, Andrew M ^c   Puhalla, Shannon L ^b,g   Lee, Adrian V ^b,c,d   Oesterreich, Steffi ^b,d   more..

^a Tsinghua University   (China)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^f UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^g UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CA 27-29 ANTIGEN; CELL FREE DNA; DNA; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; GENOMIC DNA; UNCLASSIFIED DRUG; ESTROGEN RECEPTOR ALPHA, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; BONE METASTASIS; BRAIN METASTASIS; BREAST CANCER; CANCER HORMONE THERAPY; CANCER PATIENT; CLINICAL ARTICLE; CONTROLLED STUDY; DIGITAL DROPLET POLYMERASE CHAIN REACTION; ESR1 GENE; GENE; GENE FREQUENCY; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; INCIDENCE; LIMIT OF DETECTION; LIVER METASTASIS; MUTATION RATE; MUTATIONAL ANALYSIS; ONCOLOGICAL PARAMETERS; PIK3CA GENE; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE; PRIMARY TUMOR; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SENSITIVITY ANALYSIS; SENSITIVITY AND SPECIFICITY; SKIN BIOPSY; TREATMENT RESPONSE; TUMOR BIOPSY; TUMOR CELLULARITY; ADULT; AGED; BONE TUMOR; BRAIN TUMOR; BREAST TUMOR; CLONAL EVOLUTION; FEMALE; GENETICS; LYMPH NODE METASTASIS; MIDDLE AGED; MUTATION; PATHOLOGY; SECONDARY;

ADULT; AGED; BONE NEOPLASMS; BRAIN NEOPLASMS; BREAST NEOPLASMS; CLONAL EVOLUTION; DNA, NEOPLASM; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE FREQUENCY; HUMANS; LYMPHATIC METASTASIS; MIDDLE AGED; MUTATION;

EID: 84962285052     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1534     Document Type: Article

References (43)

1. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med 2006;354:270-82.
2. Tamoxifen for early breast cancer: an overview of the randomised trials. Early Breast Cancer Trialists' Collaborative Group. Lancet 1998;351:1451-67.
3. Jaiyesimi IA, Buzdar AU, Decker DA, Hortobagyi GN. Use of tamoxifen for breast cancer: twenty-eight years later. J Clin Oncol 1995;13:513-29.
4. Musgrove EA, Sutherland RL. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 2009;9:631-43.
5. Osborne CK, Bardou V, Hopp TA, Chamness GC, Hilsenbeck SG, Fuqua SA, et al. Role of the estrogen receptor coactivatorAIB1 (SRC-3) andHER-2/neu in tamoxifen resistance in breast cancer. JNatl Cancer Inst 2003;95:353-61.
6. deGraffenried LA, Friedrichs WE, Russell DH, Donzis EJ, Middleton AK, Silva JM, et al. Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt Activity. Clin Cancer Res 2004;10: 8059-67.
7. Hutcheson IR, Knowlden JM, Madden TA, Barrow D, Gee JM, Wakeling AE, et al. Oestrogen receptor-mediated modulation of the EGFR/MAPK pathway in tamoxifen-resistant MCF-7 cells. Breast Cancer Res Treat 2003;81:81-93.
8. Britton DJ, Hutcheson IR, Knowlden JM, Barrow D, Giles M, McClelland RA, et al. Bidirectional cross talk between ERalpha and EGFR signalling pathways regulates tamoxifen-resistant growth. Breast Cancer Res Treat 2006;96:131-46.
9. Drury SC, Detre S, Leary A, Salter J, Reis-Filho J, Barbashina V, et al. Changes in breast cancer biomarkers in the IGF1R/PI3K pathway in recurrent breast cancer after tamoxifen treatment. Endocr Relat Cancer 2011;18:565-77.
10. Parisot JP, Hu XF, DeLuise M, Zalcberg JR. Altered expression of the IGF-1 receptor in a tamoxifen-resistant human breast cancer cell line. Br J Cancer 1999;79:693-700.
11. Martz CA, Ottina KA, Singleton KR, Jasper JS, Wardell SE, Peraza-Penton A, et al. Systematic identification of signaling pathways with potential to confer anticancer drug resistance. Sci Signal 2014;7:ra121.
12. Garcia T, SanchezM, Cox JL, Shaw PA, Ross JB, Lehrer S, et al. Identification of a variant form of the human estrogen receptor with an amino acid replacement. Nucleic Acids Res 1989;17:8364.
13. Karnik PS, Kulkarni S, Liu XP, Budd GT, Bukowski RM. Estrogen receptor mutations in tamoxifen-resistant breast cancer. Cancer Res 1994;54: 349-53.
14. McGuire WL, Chamness GC, Fuqua SA. Abnormal estrogen receptor in clinical breast cancer. J Steroid Biochem Mol Biol 1992;43:243-7.
15. RoodiN, Bailey LR, Kao WY, Verrier CS, Yee CJ, Dupont WD, et al. Estrogen receptor gene analysis in estrogen receptor-positive and receptor-negative primary breast cancer. J Natl Cancer Inst 1995;87:446-51.
16. Zhang QX, Borg A, Wolf DM, Oesterreich S, Fuqua SA. An estrogen receptor mutantwith strong hormone-independent activity from a metastatic breast cancer. Cancer Res 1997;57:1244-9.
17. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 2013;6:pl1.
18. Li S, Shen D, Shao J, Crowder R, Liu W, Prat A, et al. Endocrine-therapyresistant ESR1 variants revealed by genomic characterization of breastcancer- derived xenografts. Cell Rep 2013;4:1116-30.
19. Jeselsohn R, Yelensky R, Buchwalter G, Frampton G, Meric-Bernstam F, Gonzalez-Angulo AM, et al. Emergence of constitutively active estrogen receptor-alpha mutations in pretreated advanced estrogen receptor-positive breast cancer. Clin Cancer Res 2014;20:1757-67.
20. Merenbakh-Lamin K, Ben-Baruch N, Yeheskel A, Dvir A, Soussan-Gutman L, Jeselsohn R, et al. D538G mutation in estrogen receptor-alpha: A novel mechanism for acquired endocrine resistance in breast cancer. Cancer Res 2013;73:6856-64.
21. Robinson DR,WuYM, Vats P, Su F, Lonigro RJ,Cao X, et al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat Genet 2013;45:1446-51.
22. Toy W, Shen Y,WonH,Green B, Sakr RA, WillM, et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat Genet 2013;45:1439-45.
23. Veeraraghavan J, Tan Y, Cao XX, Kim JA, Wang X, Chamness GC, et al. Recurrent ESR1-CCDC170 rearrangements in an aggressive subset of oestrogen receptor-positive breast cancers. Nat Commun 2014;5:4577.
24. Rothe F, Laes JF, Lambrechts D, Smeets D, Vincent D, Maetens M, et al. Plasma circulating tumor DNA as an alternative to metastatic biopsies for mutational analysis in breast cancer. Ann Oncol 2014;25: 1959-65.
25. DeMattos-Arruda L, Weigelt B, Cortes J, Won HH, Ng CK, Nuciforo P, et al. Capturing intra-tumor genetic heterogeneity by de novo mutation profiling of circulating cell-free tumor DNA: a proof-of-principle. Ann Oncol 2014;25:1729-35.
26. Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 2014;6:224ra24.
27. Dawson SJ, Tsui DW, Murtaza M, Biggs H, Rueda OM, Chin SF, et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med 2013;368:1199-209.
28. Yu M, Bardia A, Aceto N, Bersani F, Madden MW, Donaldson MC, et al. Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 2014;345: 216-20.
29. Beaver JA, Jelovac D, Balukrishna S, Cochran RL, Croessmann S, Zabransky DJ, et al. Detection of cancer DNA in plasma of patients with early-stage breast cancer. Clin Cancer Res 2014;20:2643-50.
30. Day E, Dear PH, McCaughan F. Digital PCR strategies in the development and analysis of molecular biomarkers for personalized medicine.Methods 2013;59:101-7.
31. Diaz LA Jr, Bardelli A. Liquid biopsies: genotyping circulating tumor DNA. J Clin Oncol 2014;32:579-86.
32. 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.
33. Conway K, Parrish E, Edmiston SN, Tolbert D, Tse CK, Geradts J, et al. The estrogen receptor-alpha A908G (K303R) mutation occurs at a low frequency in invasive breast tumors: results from a population-based study. Breast Cancer Res 2005;7:R871-80.
34. Fuqua SA, Wiltschke C, Zhang QX, Borg A, Castles CG, Friedrichs WE, et al. A hypersensitive estrogen receptor-alpha mutation in premalignant breast lesions. Cancer Res 2000;60:4026-9.
35. Davies MP, O'Neill PA, Innes H, Sibson DR. Hypersensitive K303R oestrogen receptor-alpha variant not found in invasive carcinomas. Breast Cancer Res 2005;7:R113-8.
36. Ghimenti C, Mello-Grand M, Regolo L, Zambelli A, Chiorino G. Absence of the K303R estrogen receptor alpha mutation in breast cancer patients exhibiting different responses to aromatase inhibitor anastrozole neoadjuvant treatment. Exp Ther Med 2010;1:939-42.
37. Tokunaga E, Kimura Y, Maehara Y. No hypersensitive estrogen receptoralpha mutation (K303R) in Japanese breast carcinomas. Breast Cancer Res Treat 2004;84:289-92.
38. Herynk MH, Parra I, Cui Y, Beyer A, Wu MF, Hilsenbeck SG, et al. Association between the estrogen receptor alpha A908G mutation and outcomes in invasive breast cancer. Clin Cancer Res 2007;13:3235-43.
39. Abbasi S, Rasouli M, Nouri M, Kalbasi S. Association of estrogen receptoralpha A908G (K303R) mutation with breast cancer risk. Int J Clin ExpMed 2013;6:39-49.
40. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature 2012;490:61-70.
41. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, et al. Intratumor heterogeneity and branched evolution revealed bymultiregion sequencing. N Engl J Med 2012;366:883-92.
42. Chu D, Paoletti C, Gersch C, VanDenBerg D, Zabransky D, Cochran R, et al. ESR1 mutations in circulating plasma tumor DNA from metastatic breast cancer patients. Clin Cancer Res 2015.
43. Garcia-Murillas I, Schiavon G, Weigelt B, Ng C, Hrebien S, Cutts RJ, et al. Mutation tracking in circulating tumor DNA predicts relapse in early breast cancer. Sci Transl Med 2015;7:302ra133.