Neratinib efficacy and circulating tumor DNA detection of HER2 mutations in HER2 nonamplified metastatic breast cancer

Clinical Cancer Research

Volumn 23, Issue 19, 2017, Pages 5687-5695

  Ma, Cynthia X ^a   Bose, Ron ^a   Gao, Feng ^a   Freedman, Rachel A ^b   Telli, Melinda L ^c   Kimmick, Gretchen ^d   Winer, Eric ^b   Naughton, Michael ^a   Goetz, Matthew P ^e   Russell, Christy ^f   Tripathy, Debu ^f   Cobleigh, Melody ^g   Forero, Andres ^h   Pluard, Timothy J ⁱ   Anders, Carey ^j   Niravath, Polly Ann ^k   Thomas, Shana ^a   Anderson, Jill ^a   Bumb, Caroline ^a   Banks, Kimberly C ^l   Lanman, Richard B ^l   Bryce, Richard ^m   Lalani, Alshad S ^m   Pfeifer, John ^a   Hayes, Daniel F ⁿ   Pegram, Mark ^o   Blackwell, Kimberly ^d   Bedard, Philippe L ^p   Al Kateb, Hussam ^a   Ellis, Matthew J C ^k   more..

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d DUKE CANCER INSTITUTE   (United States)

^e MAYO CLINIC   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g RUSH UNIVERSITY MEDICAL CENTER   (United States)

^h University of Alabama at Birmingham   (United States)

ⁱ Division of Gynecologic Oncology   (United States)

^j UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^k BAYLOR COLLEGE OF MEDICINE   (United States)

^l Guardant Health   (United States)

^m Puma Biotechnology Inc   (United States)

ⁿ UNIVERSITY OF MICHIGAN   (United States)

^o STANFORD CANCER INSTITUTE   (United States)

^p PRINCESS MARGARET HOSPITAL   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CRCULATING TUMOR DNA; DNA; ESTROGEN RECEPTOR; LOPERAMIDE; NERATINIB; RIBOCICLIB; UNCLASSIFIED DRUG; CIRCULATING TUMOR DNA; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; N-(4-(3-CHLORO-4-(2-PYRIDINYLMETHOXY)ANILINO)-3-CYANO-7-ETHOXY-6-QUINOLYL)-4-(DIMETHYLAMINO)-2-BUTENAMIDE; QUINOLINE DERIVATIVE;

ADULT; AGED; ANEMIA; ANOREXIA; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER GRADING; CANCER GROWTH; CANCER SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DEHYDRATION; DIARRHEA; DNA SEQUENCE; DRUG EFFICACY; DRUG RESPONSE; DYSPEPSIA; FAINTNESS; FATIGUE; GENE AMPLIFICATION; GENE FREQUENCY; GENE MUTATION; HER2 GENE; HUMAN; HUMAN CELL; HYPOPHOSPHATEMIA; METASTATIC BREAST CANCER; NAUSEA; ONCOGENE; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RECURRENCE FREE SURVIVAL; SENSITIVITY AND SPECIFICITY; SOMATIC MUTATION; SURVIVAL RATE; TREATMENT OUTCOME; VERY ELDERLY; VOMITING; BREAST TUMOR; CLINICAL TRIAL; DISEASE FREE SURVIVAL; FEMALE; GENETICS; METASTASIS; MIDDLE AGED; MUTATION; PATHOLOGY; PHASE 2 CLINICAL TRIAL;

ADULT; AGED; BREAST NEOPLASMS; CIRCULATING TUMOR DNA; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; MIDDLE AGED; MUTATION; NEOPLASM METASTASIS; QUINOLINES; RECEPTOR, ERBB-2; TREATMENT OUTCOME;

EID: 85029886742     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-17-0900     Document Type: Article

References (44)

1. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989;244:707–12.
2. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001;344:783–92.
3. Desmedt C, Zoppoli G, Gundem G, Pruneri G, Larsimont D, Fornili M, et al. Genomic characterization of primary invasive lobular breast cancer. J Clin Oncol 2016;34:1872–81.
4. Burstein HJ. The distinctive nature of HER2-positive breast cancers. N Engl J Med 2005;353:1652–4.
5. Abramson V, Arteaga CL. New strategies in HER2-overexpressing breast cancer: many combinations of targeted drugs available. Clin Cancer Res 2011;17:952–8.
6. Perez EA, Romond EH, Suman VJ, Jeong JH, Davidson NE, Geyer CE Jr., et al. Four-year follow-up of trastuzumab plus adjuvant chemotherapy for operable human epidermal growth factor receptor 2-positive breast cancer: joint analysis of data from NCCTG N9831 and NSABP B-31. J Clin Oncol 2011;29:3366–73.
7. Romond EH, Perez EA, Bryant J, Suman VJ, Geyer CE Jr., Davidson NE, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 2005;353:1673–84.
8. Smith I, Procter M, Gelber RD, Guillaume Sb, Feyereislova A, Dowsett M, et al. 2-year follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer: a randomised controlled trial. Lancet 2007; 369:29–36.
9. Robert N, Leyland-Jones B, Asmar L, Belt R, Ilegbodu D, Loesch D, et al. Randomized phase III study of trastuzumab, paclitaxel, and carboplatin compared with trastuzumab and paclitaxel in women with HER-2–overexpressing metastatic breast cancer. J Clin Oncol 2006;24:2786–92.
10. Wolff AC, Hammond MEH, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists Clinical Practice Guideline Update. J Clin Oncol 2013;31:3997–4013.
11. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235:177–82.
12. Andrulis IL, Bull SB, Blackstein ME, Sutherland D, Mak C, Sidlofsky S, et al. neu/erbB-2 amplification identifies a poor-prognosis group of women with node-negative breast cancer. Toronto Breast Cancer Study Group. J Clin Oncol 1998;16:1340–9.
13. Sjogren S, Inganas M, Lindgren A, Holmberg L, Bergh J. Prognostic and predictive value of c-erbB-2 overexpression in primary breast cancer, alone and in combination with other prognostic markers. J Clin Oncol 1998;16:462–9.
14. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 2002;20:719–26.
15. Network TCGA.Comprehensive molecular portraits of human breast tumours. Nature 2012;490:61–70.
16. Bose R, Kavuri SM, Searleman AC, Shen W, Shen D, Koboldt DC, et al. Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov 2013;3:224–37.
17. Ross JS, Wang K, Sheehan CE, Boguniewicz AB, Otto G, Downing SR, et al. Relapsed classic E-cadherin (CDH1)-mutated invasive lobular breast cancer shows a high frequency of HER2 (ERBB2) gene mutations. Clin Cancer Res 2013;19:2668–76.
18. Grellety T, Soubeyran I, Robert J, Bonnefoi H, Italiano A. A clinical case of invasive lobular breast carcinoma with ERBB2 and CDH1 mutations presenting a dramatic response to anti-HER2-directed therapy. Ann Oncol 2016;27:199–200.
19. Ross JS, Ali SM, Wang K, Khaira D, Palma NA, Chmielecki J, et al. Comprehensive genomic profiling of inflammatory breast cancer cases reveals a high frequency of clinically relevant genomic alterations. Breast Cancer Res Treat 2015;154:155–62.
20. Ross JS, Gay LM, Nozad S, Wang K, Ali SM, Boguniewicz A, et al. Clinically advanced and metastatic pure mucinous carcinoma of the breast: a comprehensive genomic profiling study. Breast Cancer Res Treat 2016;155: 405–13.
21. Wen W, Chen WS, Xiao N, Bender R, Ghazalpour A, Tan Z, et al. Mutations in the kinase domain of the HER2/ERBB2 gene identified in a wide variety of human cancers. J Mol Diagn 2015;17:487–95.
22. Ben-Baruch NE, Bose R, Kavuri SM, Ma CX, Ellis MJ. HER2-mutated breast cancer responds to treatment with single-agent neratinib, a second-generation HER2/EGFR tyrosine kinase inhibitor. J Natl Compr Canc Netw 2015;13:1061–4.
23. Boulbes DR, Arold ST, Chauhan GB, Blachno KV, Deng N, Chang WC, et al. HER family kinase domain mutations promote tumor progression and can predict response to treatment in human breast cancer. Mol Oncol 2015; 9:586–600.
24. Chumsri S, Weidler J, Ali S, Balasubramanian S, Wallweber G, DeFazio-Eli L, et al. Prolonged response to trastuzumab in a patient with HER2-nonamplified breast cancer with elevated HER2 dimerization harboring an ERBB2 S310F mutation. J Natl Compr Canc Netw 2015;13:1066–70.
25. Ali SM, Alpaugh RK, Downing SR, Stephens PJ, Yu JQ, Wu H, et al. Response of an ERBB2-mutated inflammatory breast carcinoma to human epidermal growth factor receptor 2-targeted therapy. J Clin Oncol 2014;32:e88–91.
26. Greulich H, Kaplan B, Mertins P, Chen TH, Tanaka KE, Yun CH, et al. Functional analysis of receptor tyrosine kinase mutations in lung cancer identifies oncogenic extracellular domain mutations of ERBB2. Proc Natl Acad Sci U S A 2012;109:14476–81.
27. Wang SE, Narasanna A, Perez-Torres M, Xiang B, Wu FY, Yang S, et al. HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 2006;10:25–38.
28. Rabindran SK, Discafani CM, Rosfjord EC, Baxter M, Floyd MB, Golas J, et al. Antitumor activity of HKI-272, an orally active, irreversible inhibitor of the HER-2 tyrosine kinase. Cancer Res 2004;64:3958–65.
29. Tsou H-R, Overbeek-Klumpers EG, Hallett WA, Reich MF, Floyd MB, Johnson BD, et al. Optimization of 6,7-disubstituted-4-(arylamino)quin-oline-3-carbonitriles as orally active, irreversible inhibitors of human epidermal growth factor receptor-2 kinase activity. J Med Chem 2005;48: 1107–31.
30. Wong KK, Fracasso PM, Bukowski RM, Lynch TJ, Munster PN, Shapiro GI, et al. A phase I study with neratinib (HKI-272), an irreversible pan ErbB receptor tyrosine kinase inhibitor, in patients with solid tumors. Clin Cancer Res 2009;15:2552–8.
31. Burstein HJ, Sun Y, Dirix LY, Jiang Z, Paridaens R, Tan AR, et al. Neratinib, an irreversible ErbB receptor tyrosine kinase inhibitor, in patients with advanced ErbB2-positive breast cancer. J Clin Oncol 2010;28:1301–7.
32. Martin M, Bonneterre J, Geyer CE Jr., Ito Y, Ro J, Lang I, et al. A phase two randomised trial of neratinib monotherapy versus lapatinib plus capeci-tabine combination therapy in patients with HER2þ advanced breast cancer. Eur J Cancer 2013;49:3763–72.
33. Chan A, Delaloge S, Holmes FA, Moy B, Iwata H, Harvey VJ, et al. Neratinib after trastuzumab-based adjuvant therapy in patients with HER2-positive breast cancer (ExteNET): a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol 2016;17:367–77.
34. Feldinger K, Kong A. Profile of neratinib and its potential in the treatment of breast cancer. Breast Cancer: Targets and Therapy 2015;7:147–62.
35. Lanman RB, Mortimer SA, Zill OA, Sebisanovic D, Lopez R, Blau S, et al. Analytical and clinical validation of a digital sequencing panel for quantitative, highly accurate evaluation of cell-free circulating tumor DNA. PloS one 2015;10:e0140712.
36. Kancha RK, von Bubnoff N, Bartosch N, Peschel C, Engh RA, Duyster J. Differential sensitivity of ERBB2 kinase domain mutations towards lapatinib. PloS one 2011;6:e26760.
37. Rexer BN, Ghosh R, Narasanna A, Estrada MV, Chakrabarty A, Song Y, et al. Human breast cancer cells harboring a gatekeeper T798M mutation in HER2 overexpress EGFR ligands and are sensitive to dual inhibition of EGFR and HER2. Clin Cancer Res 2013;19:5390–401.
38. Hanker AB, Red Brewer M, Sheehan JH, Koch JP, Sliwoski GR, Nagy R, et al. An Acquired HER2 T798I gatekeeper mutation induces resistance to neratinib in a patient with HER2 mutant-driven breast cancer. Cancer Discov 2017;7:575–85.
39. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA: A Cancer J Clin 2016;66:7–30.
40. O'Shaughnessy J. Extending survival with chemotherapy in metastatic breast cancer. Oncologist 2005;10:20–9.
41. DeMichele A, Clark AS, Tan KS, Heitjan DF, Gramlich K, Gallagher M, et al. CDK 4/6 inhibitor palbociclib (PD0332991) in Rbþ advanced breast cancer: phase II activity, safety, and predictive biomarker assessment. Clin Cancer Res 2015;21:995–1001.
42. Schwartzberg LS, Franco SX, Florance A, O'Rourke L, Maltzman J, Johnston S. Lapatinib plus letrozole as first-line therapy for HER-2þ hormone receptor-positive metastatic breast cancer. Oncologist 2010;15:122–9.
43. Marcom PK, Isaacs C, Harris L, Wong ZW, Kommarreddy A, Novielli N, et al. The combination of letrozole and trastuzumab as first or second-line biological therapy produces durable responses in a subset of HER2 positive and ER positive advanced breast cancers. Breast Cancer Res Treat 2007; 102:43–9.
44. Kaufman B, Mackey JR, Clemens MR, Bapsy PP, Vaid A, Wardley A, et al. Trastuzumab plus anastrozole versus anastrozole alone for the treatment of postmenopausal women with human epidermal growth factor receptor 2-positive, hormone receptor-positive metastatic breast cancer: results from the randomized phase III TAnDEM study. J Clin Oncol 2009;27:5529–37.