Emerging approaches for treating HER2-positive metastatic breast cancer beyond trastuzumab

Annals of Oncology

Volumn 24, Issue 10, 2013, Pages 2492-2500

  Gradishar, W J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Her inhibitors; Her2 positive; Metastatic breast cancer; Monoclonal antibodies; Neoadjuvant therapy; Trastuzumab

Indexed keywords

AFATINIB; ANTINEOPLASTIC AGENT; CAPECITABINE; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; LAPATINIB; LETROZOLE; MM 111; NAVELBINE; NERATINIB; PACLITAXEL; PB 272; PERTUZUMAB; PLACEBO; TEMSIROLIMUS; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; UNCLASSIFIED DRUG;

ALOPECIA; ANEMIA; ASTHENIA; BACKACHE; BRAIN METASTASIS; BRAIN SURGERY; BREAST CANCER; BREAST METASTASIS; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CARDIOTOXICITY; CENTRAL NERVOUS SYSTEM METASTASIS; DIARRHEA; DRUG EFFICACY; DRUG HYPERSENSITIVITY; DRUG RESPONSE; DRUG SAFETY; DYSPNEA; FATIGUE; FEBRILE NEUTROPENIA; GASTROINTESTINAL TOXICITY; HAND FOOT SYNDROME; HUMAN; HYPERTRANSAMINASEMIA; HYPOKALEMIA; LEFT VENTRICULAR SYSTOLIC DYSFUNCTION; LEUKOPENIA; LIVER TOXICITY; METABOLIC DISORDER; MONOTHERAPY; NAUSEA; NAUSEA AND VOMITING; NEUTROPENIA; PNEUMONIA; PRIORITY JOURNAL; PRURITUS; RASH; REVIEW; SKIN MANIFESTATION; STOMATITIS; THROMBOCYTOPENIA; TREATMENT OUTCOME; VOMITING;

HER INHIBITORS; HER2-POSITIVE; METASTATIC BREAST CANCER; MONOCLONAL ANTIBODIES; NEOADJUVANT THERAPY; TRASTUZUMAB;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; FEMALE; HUMANS; MAYTANSINE; NEOADJUVANT THERAPY; NEOPLASM METASTASIS; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, ERBB-2;

EID: 84884718594     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdt217     Document Type: Review

References (68)

1. American Cancer Society. Cancer Facts & Figures, 2013. Atlanta, GA: American Cancer Society 2013.
2. Malvezzi M, Bertuccio P, Levi F et al European cancer mortality predictions for the year 2013. Ann Oncol 2013; 24: 792-800.
3. National Compreshensive Cancer Network. NCCN Breast Cancer Version 1 2013. pdf. http://www.nccn.org/professionals/physician_gls/PDF/breast.pdf. (21 February 2013, date last accessed).
4. Slamon DJ, Clark GM, Wong SG et al Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235: 177-182.
5. Gonzalez-Angulo AM, Litton JK, Broglio KR et al High risk of recurrence for patients with breast cancer who have human epidermal growth factor receptor 2-positive, node-negative tumors 1 cm or smaller. J Clin Oncol 2009; 27: 5700-5706.
6. HERCEPTIN® (Trastuzumab) Intravenous Infusion [package insert]. South San Francisco, CA: Genentech, Inc. 2009.
7. TYKERB® (lapatinib) tablets [package insert]. Research Triangle Park, NC: GlaxoSmithKline 2012.
8. Geyer CE, Forster J, Lindquist D et al Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006; 355: 2733-2743.
9. Cameron D, Casey M, Oliva C et al Lapatinib plus capecitabine in women with HER-2-positive advanced breast cancer: final survival analysis of a phase III randomized trial. Oncologist 2010; 15: 924-934.
10. Blackwell KL, Burstein HJ, Storniolo AM et al Randomized study of lapatinib alone or in combination with trastuzumab in women with ErbB2-positive, trastuzumabrefractory metastatic breast cancer. J Clin Oncol 2010; 28: 1124-1130.
11. Wilken JA, Maihle NJ. Primary trastuzumab resistance: new tricks for an old drug. Ann N Y Acad Sci 2010; 1210: 53-65.
12. Garrett JT, Arteaga CL. Resistance to HER2-directed antibodies and tyrosine kinase inhibitors: mechanisms and clinical implications. Cancer Biol Ther 2011; 11: 793-800.
13. Bria E, Cuppone F, Fornier M et al Cardiotoxicity and incidence of brain metastases after adjuvant trastuzumab for early breast cancer: the dark side of the moon? A metaanalysis of the randomized trials. Breast Cancer Res Treat 2008; 109: 231-239.
14. Von Minckwitz G, du Bois A, Schmidt M et al Trastuzumab beyond progression in human epidermal growth factor receptor 2-positive advanced breast cancer: a German breast group 26/breast international group 03-05 study. J Clin Oncol 2009; 27: 1999-2006.
15. Von Minckwitz G, Schwedler K, Schmidt M et al Trastuzumab beyond progression: Overall survival analysis of the GBG 26/BIG 3-05 phase III study in HER2-positive breast cancer. Eur J Cancer 2011; 47: 2273-2281.
16. Mannocci A, De FE, de WC et al Use of trastuzumab in HER2-positive metastatic breast cancer beyond disease progression: a systematic review of published studies. Tumori 2010; 96: 385-391.
17. Extra JM, Antoine EC, Vincent-Salomon A et al Efficacy of trastuzumab in routine clinical practice and after progression for metastatic breast cancer patients: the observational Hermine study. Oncologist 2010; 15: 799-809.
18. Di Leo A, Gomez HL, Aziz Z et al Phase III, double-blind, randomized study comparing lapatinib plus paclitaxel with placebo plus paclitaxel as first-line treatment for metastatic breast cancer. J Clin Oncol 2008; 26: 5544-5552.
19. Johnston S, Pippen J, Jr, Pivot X et al Lapatinib combined with letrozole versus letrozole and placebo as first-line therapy for postmenopausal hormone receptorpositive metastatic breast cancer. J Clin Oncol 2009; 27: 5538-5546.
20. Amir E, Ocana A, Seruga B et al Lapatinib and HER2 status: results of a metaanalysis of randomized phase III trials in metastatic breast cancer. Cancer Treat Rev 2010; 36: 410-415.
21. Yip AY, Tse LA, Ong EY et al Survival benefits from lapatinib therapy in women with HER2-overexpressing breast cancer: a systematic review. Anticancer Drugs 2010; 21: 487-493.
22. Bachelot T, Romieu G, Campone M et al Lapatinib plus capecitabine in patients with previously untreated brain metastases from HER2-positive metastatic breast cancer (LANDSCAPE): a single-group phase 2 study. Lancet Oncol 2013; 14: 64-71.
23. Gelmon KA, Boyle F, Kaufman B et al Open-label phase III randomized controlled trial comparing taxane-based chemotherapy (Tax) with lapatinib (L) or trastuzumab (T) as first-line therapy for women with HER2+ metastatic breast cancer: Interim analysis (IA) of NCIC CTG MA.31/GSK EGF 108919. J Clin Oncol 2012; 30: Abstract LBA671.
24. Goss PE, Smith IE, O'Shaughnessy J et al Adjuvant lapatinib for women with earlystage HER2-positive breast cancer: a randomised, controlled, phase 3 trial. Lancet Oncol 2013; 14: 88-96.
25. Agus DB, Akita RW, Fox WD et al Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer Cell 2002; 2: 127-137.
26. Franklin MC, Carey KD, Vajdos FF et al Insights into ErbB signaling from the structure of the ErbB2-pertuzumab complex. Cancer Cell 2004; 5: 317-328.
27. PERJETA™(pertuzumab) Injection, for intravenous use [package insert]. South San Francisco, CA: Genentech, Inc. 2012.
28. Scheuer W, Friess T, Burtscher H et al Strongly enhanced antitumor activity of trastuzumab and pertuzumab combination treatment on HER2-positive human xenograft tumor models. Cancer Res 2009; 69: 9330-9336.
29. Nahta R, Hung MC, Esteva FJ. The HER-2-targeting antibodies trastuzumab and pertuzumab synergistically inhibit the survival of breast cancer cells. Cancer Res 2004; 64: 2343-2346.
30. Agus DB, Gordon MS, Taylor C et al Phase I clinical study of pertuzumab, a novel HER dimerization inhibitor, in patients with advanced cancer. J Clin Oncol 2005; 23: 2534-2543.
31. Yamamoto N, Yamada Y, Fujiwara Y et al Phase I and pharmacokinetic study of HER2-targeted rhuMAb 2C4 (Pertuzumab, RO4368451) in Japanese patients with solid tumors. Jpn J Clin Oncol 2009; 39: 260-266.
32. Baselga J, Gelmon KA, Verma S et al Phase II trial of pertuzumab and trastuzumab in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer that progressed during prior trastuzumab therapy. J Clin Oncol 2010; 28: 1138-1144.
33. Cortes J, Fumoleau P, Bianchi GV et al Pertuzumab monotherapy after trastuzumab-based treatment and subsequent reintroduction of trastuzumab: activity and tolerability in patients with advanced human epidermal growth factor receptor 2-positive breast cancer. J Clin Oncol 2012; 30: 1594-1600.
34. Baselga J, Cortes J, Kim SB et al Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012; 366: 109-119.
35. Ellis PA, Barrios CH, Im Y et al MARIANNE: A phase III, randomized study of trastuzumab-DM1 (T-DM1) with or without pertuzumab (P) compared with trastuzumab (H) plus taxane for first-line treatment of HER2-positive, progressive, or recurrent locally advanced or metastatic breast cancer (MBC). J Clin Oncol 2011; 29: Abstract TPS102.
36. Genentech. FDA Grants Genentech's pertuzumab priority review for previously untreated HER2-positive metastatic breast cancer. February 7, 2012. http://www.gene.com/gene/news/press-releases/display.do?method=detail&id=13847. (7 February 2012, date last accessed).
37. Munoz-Mateu M, Urruticoechea A, Separovic R et al Trastuzumab plus capecitabine with or without pertuzumab in patients with HER2-positive MBC whose disease has progressed during or following trastuzumab-based therapy for first-line metastatic disease: a multicenter, randomized, two-arm, phase II study (PHEREXA). J Clin Oncol 2011; 29: Abstract TPS118.
38. KADCYLA™(ado-trastuzumab emtansine) for injection, for intravenous use [package insert]. South San Francisco, CA: Genentech, Inc. 2013.
39. Lewis Phillips GD, Li G, Dugger DL et al Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate. Cancer Res 2008; 68: 9280-9290.
40. Burris HA, III, Rugo HS, Vukelja SJ et al Phase II study of the antibody drug conjugate trastuzumab-DM1 for the treatment of human epidermal growth factor receptor 2 (HER2)-positive breast cancer after prior HER2-directed therapy. J Clin Oncol 2011; 29: 398-405.
41. Verma S, Miles D, Gianni L et al Updated overall survival results from EMILIA, a phase 3 study of trastuzumab emtansine (T-DM1) vs capecitabine (X) and lapatinib (L) in HER2-positive locally advanced or metastatic breast cancer (MBC). Ann Oncol 2012; 23: ixe5-ixe6. Abstract LBA12.
42. Blackwell KL, Miles D, Gianni L et al Primary results from EMILIA, a phase III study of trastuzumab emtansine (T-DM1) versus capecitabine (X) and lapatinib (L) in HER2-positive locally advanced or metastatic breast cancer (MBC) previously treated with trastuzumab (T) and a taxane. J Clin Oncol 2012; 30: Abstract LBA1.
43. Miller K, Gianni L, Andre F et al A phase Ib/II trial of trastuzumab-DM1 (T-DM1) with pertuzumab (P) for women with HER2-positive, locally advanced or metastatic breast cancer (BC) who were previously treated with trastuzumab (T). J Clin Oncol 2010; 28: Abstract 1012.
44. Higgins MJ, Gabrail NY, Miller K et al A phase I/II study of MM-111, a novel bispecific antibody that targets the ErB2/ErB3 heterodimer, in combination with trastuzumab in advanced refractory HER2-positive breast cancer. J Clin Oncol 2011; 29: Abstract suppl; abstr TPS119.
45. Denlinger CS, Beeram M, Tolcher AW et al A Phase 1-2 and Pharmacologic Study of MM-111 in Patients with Advanced, Refractory HER2-Positive (HER-2+) Cancers. Presented at the 46th Annual Meeting of the American Society of Clinical Oncology, June 4-8, 2010, Chicago, IL, 2010.
46. Li D, Ambrogio L, Shimamura T et al BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene 2008; 27: 4702-4711.
47. Solca F, Dahl G, Zoephel A et al Target binding properties and cellular activity of afatinib (BIBW 2992), an irreversible ErbB family blocker. J Pharmacol Exp Ther 2012; 343: 342-350.
48. Lin NU, Winer EP, Wheatley D et al A phase II study of afatinib (BIBW 2992), an irreversible ErbB family blocker, in patients with HER2-positive metastatic breast cancer progressing after trastuzumab. Breast Cancer Res Treat 2012; 133: 1057-1065.
49. Harbeck N, Im S-A, Huang CS et al LUX-breast 1: Randomized, phase III trial of afatinib and vinorelbine versus trastuzumab and vinorelbine in patients with HER2-overexpressing metastatic breast cancer (MBC) failing one prior trastuzumab treatment. J Clin Oncol 2012; 30: Abstract TPS649.
50. Hickish T, Tseng L-M, Mehta AO et al LUX-breast 2: Phase II, open-label study of oral afatinib in HER2-overexpressing metastatic breast cancer (MBC) patients (pts) who progressed on prior trastuzumab (T) and/or lapatanib (L). J Clin Oncol 2012; 30: Abstract TPS651.
51. Joensuu H, Kaci MO. LUX-breast 3: Randomized phase II study of afatinib alone or with vinorelbine versus investigator's choice of treatment in patients (pts) with HER2-positive breast cancer (BC) with progressive brain metastases (BM) after trastuzumab or lapatinib-based therapy. J Clin Oncol 2012; 30: Abstract TPS647.
52. Puma Biotechnology Inc. Puma Biotechnology Announces Licensing Agreement with Pfizer for the Development and Commercialization of Neratinib, an Investigational PanHER Inhibitor; Closes $55 Million Private Placement and Completes Merger. http://www.pumabiotechnology.com/pr20111005.html. (16 February 2012, date last accessed).
53. Rabindran SK, Discafani CM, Rosfjord EC et al Antitumor activity of HKI-272, an orally active, irreversible inhibitor of the HER-2 tyrosine kinase. Cancer Res 2004; 64: 3958-3965.
54. Tsou HR, Overbeek-Klumpers EG, Hallett WA et al Optimization of 6,7-disubstituted-4-(arylamino)quinoline-3-carbonitriles as orally active, irreversible inhibitors of human epidermal growth factor receptor-2 kinase activity. J Med Chem 2005; 48: 1107-1131.
55. Burstein HJ, Sun Y, Dirix LY et al Neratinib, an irreversible ErbB receptor tyrosine kinase inhibitor, in patients with advanced ErbB2-positive breast cancer. J Clin Oncol 2010; 28: 1301-1307.
56. Swaby R, Blackwell K, Jiang Z et al Neratinib in combination with trastuzumab for the treatment of advanced breast cancer: a phase I/II study. J Clin Oncol 2009; 27: 1004.
57. Staroslawska E, Dirix L, Luu T et al Safety and Efficacy of Neratinib (HKI-272) Plus Vinorelbine in the Treatment of Patients with ErbB2+ Metastatic Breast Cancer Pretreated with Anti-HER2 Therapy. Presented at 33rd Annual San Antonio Breast Cancer Symposium, December 8-12, 2010, San Antonio, TX, 2010. Abstract P3-14-05.
58. Gajria D, King T, Pannu H et al Combined Inhibition of mTORC1 with Temsirolimus and HER2 with Neratinib: A Phase I/II Study in Patients with Metastatic HER2-Amplified or Triple-Negative Breast Cancer. Cancer Res 2011; 71: 152s. Abstract PD09-08.
59. Saura C, Garcia-Saenz JA, Xu B et al Safety and Efficacy of Neratinib in Combination with Capecitabine in Patients with ErbB2-Positive Breast Cancer. Cancer Res 2011; 71: 225s. Abstract P1-12-09.
60. Martin M, Bonneterre J, Geyer CE, Jr. et al. A Phase 2, Randomized, Open-Label, Study of Neratinib (HKI-272) vs Lapatinib Plus Capecitabine for 2nd/3rd-Line Treatment of HER2+ Locally Advanced or Metastatic Breast Cancer. Cancer Res 2011; 71: 113s. Abstract S5-7.
61. Abramson V, Arteaga CL. New strategies in HER2-overexpressing breast cancer: many combinations of targeted drugs available. Clin Cancer Res 2011; 17: 952-958.
62. Baselga J, Bradbury I, Eidtmann H et al Lapatinib with trastuzumab for HER2-positive early breast cancer (NeoALTTO): a randomised, open-label, multicentre, phase 3 trial. Lancet 2012; 379: 633-640.
63. Gianni L, Pienkowski T, Im YH et al Efficacy and safety of neoadjuvant pertuzumab and trastuzumab in women with locally advanced, inflammatory, or early HER2-positive breast cancer (NeoSphere): a randomised multicentre, open-label, phase 2 trial. Lancet Oncol 2012; 13: 25-32.
64. Guarneri V, Frassoldati A, Bottini A et al Final results of a phase II randomized trial of neoadjuvant anthracycline-taxane chemotherapy plus lapatinib, trastuzumab, or both in HER2-positive breast cancer (CHER-LOB trial). J Clin Oncol 2011; 29: Abstract 507.
65. Chang JCN, Mayer IA, Forero-Torres A et al TBCRC 006: A multicenter phase II study of neoadjuvant lapatinib and trastuzumab in patients with HER2-overexpressing breast cancer. J Clin Oncol 2011; 29: Abstract 505.
66. Robidoux A, Tang G, Rastogi P et al Evaluation of lapatinib as a component of neoadjuvant therapy for HER2+ operable breast cancer: NSABP protocol B-41. J Clin Oncol 2012; 30: Abstract LBA506.
67. Schneeweiss A, Chia S, Hickish T et al Neoadjuvant Pertuzumab and Trastuzumab Concurrent or Sequential with an Anthracycline-Containing or Concurrent with an Anthracycline-Free Standard Regimen: A Randomized Phase II Study (TRYPHAENA). Presented at the San Antonio Breast Cancer Symposium, December 9-10, 2011, San Antonio, TX, 2011. Abstract S5-6.
68. Awada A, Dirix L, Manso SL et al Safety and efficacy of neratinib (HKI-272) plus vinorelbine in the treatment of patients with ErbB2-positive metastatic breast cancer pretreated with anti-HER2 therapy. Ann Oncol 2013; 24: 109-116.