Aromatase inhibitors: Prediction of response and nature of resistance

Expert Opinion on Pharmacotherapy

Volumn 11, Issue 11, 2010, Pages 1873-1887

  Miller, William R ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Aromatase inhibitors; Breast cancer; Endocrine therapy; Estrogens; Mechanisms of resistance; Predictive indices

Indexed keywords

ANASTROZOLE; AROMATASE INHIBITOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN; ESTROGEN RECEPTOR; LETROZOLE; PROGESTERONE RECEPTOR; TAMOXIFEN; TREFOIL PEPTIDE;

ACCURACY; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER PATIENT; CANCER SURVIVAL; CELL SURVIVAL; CLINICAL TRIAL; CROSS RESISTANCE; ESTROGEN ACTIVITY; GENETIC MARKER; HUMAN; MULTIGENE FAMILY; PHENOTYPE; PROTEIN PHOSPHORYLATION; REVIEW; TREATMENT RESPONSE; BREAST NEOPLASMS; DRUG RESISTANCE; FEMALE; GENETICS; METABOLISM; PHOSPHORYLATION;

AROMATASE INHIBITORS; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; PHOSPHORYLATION; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE;

EID: 77954766182     PISSN: 14656566     EISSN: None     Source Type: Journal    
DOI: 10.1517/14656566.2010.487863     Document Type: Review

References (95)

1. Early Breast Cancer Trialists Group. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005;365:1687-1717
2. Winer EP, Hudis C, Burstein HJ, et al. American Society of Clinical Oncology technology assessment on the use of aromatase inhibitors as adjuvant therapy for postmenopausal women with hormone receptor-positive breast cancer: status report 2004. J Clin Oncol 2005;23:619-629
3. Miller WR. Aromatase inhibitors and breast cancer. Minerva Endocrinol 2006;31:27-46
4. Lonning PE. Pharmacology of new aromatase inhibitors. Breast 1996;5:202-206
5. Geisler J, Haynes B, Anker G, et al. Influence of letrozole and anastrozole on total body aromatization and plasma estrogen levels in postmenopausal breast cancer patients evaluated in a randomized, cross-over study. J Clin Oncol 2002;20:751-757
6. Dowsett M. Preoperative models to evaluate endocrine strategies for breast cancer. Clin Cancer Res 2003;9:502-10s
7. Anderson TJ, Dixon JM, Stuart M, et al. Effect of neoadjuvant treatment with anastrozole on tumour histology in postmenopausal women with large operable breast cancer. Br J Cancer 2002;87:334-338
8. Dixon JM. Neoadjuvant therapy: surgical perspectives. In: Miller WR, Ingle JN, editors, Endocrine therapy in breast cancer. Marcel Dekker, New York; 2002. p. 197-212
9. Miller WR, Jackson J. The therapeutic potential of aromatase inhibitors. Expert Opin Investig Drugs 2003;12:1-12
10. ATAC (Arimidex, Tamoxifen Alone or in Combination) Trialists Group. Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvant treatment of postmenopausal women with early breast cancer: first results of the ATAC randomised trial. Lancet 2002;359:2131-2139
11. Goss PE, Ingle JN, Martino S, et al. Randomized trial of letrozole following tamoxifen as extended adjuvant therapy in receptor-positive breast cancer: updated findings from NCIC CTG MA.17. J Natl Cancer Inst 2005;97:1262-1269
12. Coombes RC, Kilburn LS, Snowdon CF, et al. Survival and safety of exemestane versus tamoxifen after 2 - 3 years' tamoxifen treatment (Intergroup Exemestane Study): a randomized controlled trial. Lancet 2007;365:559-570
13. Eiermann W, Paepke S, Appfelstaedt J, et al. Preoperative treatment of postmenopausal breast cancer patients with letrozole: a randomized double-blind multicenter study. Ann Oncol 2001;12:1527-1532
14. Smith IE, Dowsett M, Ebbs SR, et al. Neoadjuvant treatment of postmenopausal breast cancer with anastrozole, tamoxifen, or both in combination: the Immediate Preoperative Anastrozole, Tamoxifen, or Combined with Tamoxifen (IMPACT) multicenter double-blind randomized trial. J Clin Oncol 2005;23:5108-5116
15. Semiglazov V, Kletsel A, Semiglazov V, et al. Exemestane (E) versus tamoxifen (T) as neoadjuvant endocrine therapy for postmenopausal women with ER+ breast cancer (T2N1-2, T3N0-1, T4N0M0) [abstract 530]. J Clin Oncol 2005;23(16 Suppl):11s
16. Mouridsen H, Gershanovich M, Sun Y, et al. Phase III study of letrozole versus tamoxifen as first-line therapy of advanced breast cancer in postmenopausal women: analysis of survival and update of efficacy from the International Letrozole Breast Cancer Group. J Clin Oncol 2003;21:2101-2109
17. Johnston SR, Martin LA, Head J, et al. Aromatase inhibitors: combinations with fulvestrant or signal transduction inhibitors as a strategy to overcome endocrine resistance. J Steroid Biochem Mol Biol 2005;95:173-181
18. Jonat W, Gnant M, Boccardo F, et al. Effectiveness of switching from adjuvant tamoxifen to anastrozole in postmenopausal women with hormone-sensitive early-stage breast cancer: a meta-analysis. Lancet Oncol 2006;7:991-996
19. Dowsett M, Cuzick J, Ingle J, et al. Meta-analysis of breast cancer outcomes in adjuvant trials of aromatase inhibitors versus tamoxifen. J Clin Oncol 2010;28(3):509-518
20. Miller WR. Prediction of estrogen sensitivity/dependence. In: Miller WR, editor, Estrogen and breast cancer. RG Landes, Austen, TX; 1996. p. 151-170
21. Dixon JM. Prospects of neoadjuvant aromatase inhibitor therapy in breast cancer. Expert Rev Anticancer Ther 2008;8:453-463
22. Kaufmann M, von Minckwitz G, Bear HD, et al. Recommendations from an international expert panel on the use of neoadjuvant (primary) systemic treatment of operable breast cancer: new perspectives 2006. Ann Oncol 2007;18:1927-1934
23. Ma CX, Ellis MJ. Neoadjuvant endocrine therapy for locally advanced breast cancer. Semin Oncol 2006;33:650-656
24. Murray J, Miller WR, Dixon JM. Neoadjuvant endocrine therapy models. Methods Mol Med 2006;120:489-502
25. Macaskill EJ, Dixon JM. Neoadjuvant use of endocrine therapy in breast cancer. Breast J 2007;13:243-250
26. Miller WR, Larionov A, Renshaw L, et al. Gene expression profiles differentiating between breast cancers clinically responsive or resistant to letrozole. J Clin Oncol 2009;27:1382-1387
27. Miller WR, Larionov AA, Renshaw L, et al. Changes in breast cancer transcriptional profiles after treatment with the aromatase inhibitor, letrozole. Pharmacogenet Genomics 2007;17:813-826
28. Forouhi P, Walsh JS, Anderson TJ, Chetty U. Ultrasonography as a method of measuring breast tumour size and monitoring response to primary systemic treatment. Br J Surg 1994;81:223-225
29. Kuerer HM, Newman LA, Smith TL, et al. Clinical course of breast cancer patients with complete pathologic primary tumor and axillary lymph node response to doxorubicinbased neoadjuvant chemotherapy. J Clin Oncol 1999;17:460-469
30. Dixon JM, Love CD, Renshaw L, et al. Lessons from the use of aromatase inhibitors in the neoadjuvant setting. Endocr Relat Cancer 1999;6:227-230
31. Sasano H, Suzuki T, Moriya T. Pathology of breast cancer following neoadjuvant therapy. In: Miller WR, Ingle JN, editors, Endocrine therapy in breast cancer. Marcel Dekker, New York; 2002. p. 213-222
32. Miller WR, Dixon JM, MacFarlane L, et al. Pathological features of breast cancer response following neoadjuvant treatment with either letrozole or tamoxifen. Eur J Cancer 2003;39:462-468
33. Miller WR, Dixon JM, Cameron DA, Anderson TJ. Biological and clinical effects of aromatase inhibitors in neoadjuvant therapy. J Steroid Biochem Mol Biol 2001;79:103-107
34. Miller WR, White S, Dixon JM, et al. Proliferation, steroid receptors and clinical/pathological response in breast cancer treated with letrozole. Br J Cancer 2006;94:1051-1056
35. Dowsett M, Smith IE, Ebbs SR, et al. Short-term changes in Ki-67 during neoadjuvant treatment of primary breast cancer with anastrozole or tamoxifen alone or combined correlate with recurrence-free survival. Clin Cancer Res 2005;11:S951-8
36. Tao Y, Klause A, Vickers A, et al. Clinical and biomarker endpoint analysis in neoadjuvant endocrine therapy trials. J Steroid Biochem Mol Biol 2005;95:91-95
37. Dowsett M, Salter J, Hills M, et al. Short-term presurgical treatment for all? Breast Cancer Res 2007;9(Suppl 2):S13
38. Itoh T, Karlsberg K, Kijima I, et al. Letrozole-, anastrozole- and tamoxifen-responsive genes in MCF-7aro cells: a microarray approach. Mol Cancer Res 2005;3:203-218
39. Harvey HA. Emerging role of aromatase inhibitors in the treatment of breast cancer. Oncology 1998;12:32-35
40. Smith IE, Dowsett M. Aromatase inhibitors in breast cancer. N Engl J Med 2003;348:2431-2442
41. Hurvitz SA, Pietras RJ. Rational management of endocrine resistance in breast cancer. Cancer 2008;113:2385-2397
42. Johnston SRD. Advanced disease and resistance modulation. In: Ellis MJ, editor, Aromatase inhibitors for the treatment of breast cancer. CMP Healthcare Media, New York; 2005. p. 73-90
43. Miller WR, Bartlett J, Brodie AM, et al. Aromatase inhibitors: are there differences between steroidal and nonsteroidal aromatase inhibitors and do they matter? Oncologist 2008;13:829-837
44. Johnston SRD, Dowsett M. Aromatase inhibitors for breast cancer: lessons from the laboratory. Nat Rev Cancer 2003;3:821-831 (Pubitemid 37376980)
45. Musgrove EA, Sutherland RL. Biological determinants of endocrine resistance in breast cancer. Nat Rev Cancer 2009;9:631-643
46. Elledge RM, Osborne CK. Oestrogen receptors and breast cancer. BMJ 1997;314(7098):1843-1844
47. Dowsett M. Biology of estrogen-dependent breast cancer. In: Ellis MJ, editor, Aromatase inhibitors for the treatment of breast cancer. CMP Healthcare Media, New York; 2005. p. 1-13
48. Ma CX, Sanchez CG, Ellis MJ. Predicting endocrine therapy responsiveness in breast cancer. Oncology (Williston Park) 2009;23:133-142
49. Miller WR, Anderson TJ, Iqbal S, Dixon JM. Neoadjuvant therapy: prediction of response. In: Miller WR, Ingle JN, editors, Endocrine therapy in breast cancer. Marcel Dekker, New York; 2002. p. 223-229
50. Elledge RM, Green S, Pugh R, et al. Estrogen receptor (ER) and progesterone receptor (PgR), by ligand-binding assay compared with ER, PgR and pS2, by immuno-histochemistry in predicting response to tamoxifen in metastatic breast cancer: a Southwest Oncology Group Study. Int J Cancer 2000;89:111-117
51. Ellis MJ, Coop A, Singh B, et al. Letrozole is more effective neoadjuvant endocrine therapy than tamoxifen for ErbB-1- and/or ErbB-2-positive, estrogen receptor-positive primary breast cancer: evidence from a phase III randomized trial. J Clin Oncol 2001;19:3808-3816
52. Fuqua SA, Allred DC, Elledge RM, et al. The ER-positive/PgR-negative breast cancer phenotype is not associated with mutations within the DNA binding domain. Breast Cancer Res Treat 1993;26:191-202
53. Masiakowski P, Breathnach R, Bloch J, et al. Cloning of cDNA sequences of hormone regulated genes from MCF-7 human breast cancer cell line. Nucleic Acids Res 1982;10:7895-7903
54. Mackay A, Urruticoechea A, Dixon JM, et al. Molecular response to aromatase inhibitor treatment in primary breast cancer. Breast Cancer Res 2007;9:R37
55. Dowsett M, Houghton J, Iden C, et al. Benefit from adjuvant tamoxifen therapy in primary breast cancer patients according oestrogen receptor, progesterone receptor, EGF receptor and HER2 status. Ann Oncol 2006;17:818-826
56. Dowsett M, Ebbs SR, Dixon JM, et al. Biomarker changes during neoadjuvant anastrozole, tamoxifen, or the combination: influence of hormonal status and HER-2 in breast cancer - a study from the IMPACT trialists. J Clin Oncol 2005;23:2477-2492
57. Lal P, Tan LK, Chen B. Correlation of HER-2 status with estrogen and progesterone receptors and histologic features in 3,655 invasive breast carcinomas. Am J Clin Pathol 2005;123:541-546
58. Generali D, Buffa FM, Berruti A, et al. Phosphorylated ERalpha, HIF-1alpha, and MAPK signaling as predictors of primary endocrine treatment response and resistance in patients with breast cancer. J Clin Oncol 2009;27:227-234
59. Yamashita H, Takahashi S, Ito Y, et al. Predictors of response to exemestane as primary endocrine therapy in estrogen receptor-positive breast cancer. Cancer Sci 2009;100:2028-2033
60. Buyse M, Loi S, van't Veer L, et al. Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. J Natl Cancer Inst 2006;98:1183-1192
61. Sparano JA, Paik S. Development of the 21-gene assay and its application in clinical practice and clinical trials. J Clin Oncol 2008;26:721-728
62. Miller WR, Larionov A, Anderson TJ, et al. Predicting response and resistance to endocrine therapy: profiling patients on aromatase inhibitors. Cancer 2008;112(3 Suppl):689-694
63. Dowsett M, Johnston S, Martin LA, et al. Growth factor signalling and response to endocrine therapy: the Royal Marsden experience. Endocr Relat Cancer 2005;12(Suppl 1):S113-17
64. Shim WS, Conaway M, Masamura S, et al. Estradiol hypersensitivity and MAP kinase expression in long term estrogen deprived human breast cancer cells in vivo. Endocrinology 2000;141:396-405
65. Chan CM, Martin LA, Johnston SR, et al. Molecular changes associated with the acquisition of oestrogen hypersensitivity in MCF-7 breast cancer cells on long-term oestrogen deprivation. J Steroid Biochem Mol Biol 2002;81:333-341
66. Martin LA, Farmer I, Johnston SR, et al. Enhanced estrogen receptor (ER) alpha, ERBB2, and MAPK signal transduction pathways operate during the adaptation of MCF-7 cells to long term estrogen deprivation. J Biol Chem 2003;278:30458-30468
67. Masri S, Phung S, Wang X, et al. Genome-wide analysis of aromatase inhibitor-resistant, tamoxifen-resistant, and long-term estrogen-deprived cells reveals a role for estrogen receptor. Cancer Res 2008;68:4910-4918
68. Geisler J, Lonning PE. Resistance to endocrine therapy of breast cancer: recent advances and tomorrow's challenges. Clin Breast Cancer 2001;1:297-308
69. Perey L, Paridaens R, Nole F, et al. Fulestrant as hormonal treatment in postmenopausal women with advanced breast cancer progressing after treatment with tamoxifen and aromatase inhibitors: update of a phase II SAKK trial. Breast Cancer Res Treat 2004;18:S236
70. Johnston S. Fulvestrant and the sequential endocrine cascade for advanced breast cancer. Br J Cancer 2004;90(Suppl 1):S15-S18
71. Miller WR. Controversies in breast cancer 2008. Breast Cancer Res 2008;10(Suppl 4):S1
72. Miller WR, Larionov A, Renshaw L, et al. Aromatase inhibitors - gene discovery. J Steroid Biochem Mol Biol 2007;106:130-142
73. Thurlimann B, Paridaens R, Serin D, et al. Third-line hormonal treatment with exemestane in postmenopausal patients with advanced breast cancer progressing on aminoglutethimde: a phase II multicentre multi-national trial. Eur J Cancer 1997;33:1767-1773
74. Ingle JN. Pharmacogenetics and pharmacogenomics of endocrine agents for breast cancer. Breast Cancer Res 2008;10(Suppl 4):S17
75. Santen RJ, Misbin RI. Aminoglutethimide: review of pharmacology and clinical use. Pharmacology 1981;1:95-120
76. Dowsett M, Pfister C, Johnston SRD, et al. Impact of tamoxifen on the pharmacokinetics and endocrine effects of the aromatase inhibitor letrozole in postmenopausal women with breast cancer. Clin Cancer Res 1999;5:2338-2343
77. Dowsett M, Tobias JS, Howell A, et al. The effect of anastrozole on the pharmacokinetics of tamoxifen in post-menopausal women with early breast cancer. Br J Cancer 1999;79:311-315
78. ATAC Trialists Group. Pharmacokinetics of anastrozole and tamoxifen alone, and in combination, during adjuvant endocrine therapy for early breast cancer in postmenopausal women: sub-protocol of the 'Arimidex TM and Tamoxifen alone or in combination' (ATAC) trial. Br J Cancer 2001;85:317-324
79. Lazarus P, Sun D. Potential role of UGT pharmacogenetics in cancer treatment and prevention: focus on tamoxifen and aromatase inhibitors. Drug Metab Rev 2010;42:176-188
80. Goss PE, Strasser-Weippl K. Prevention strategies with aromatase inhibitors. Clin Cancer Res 2004;10:372S-9S
81. Miller WR. Biological rationale for endocrine therapy in breast cancer. Best Pract Res Clin Endocrinol Metab 2004;18:1-32
82. Kadohama N, Yarborough C, Zhou D, et al. Kinetic properties of aromatase mutants Pro308Phe, Asp309Asn, and Asp309Ala and their interactions with aromatase inhibitors. J Steroid Biochem Mol Biol 1992;43:693-701
83. Miller WR. In vitro and in vivo effects of 4-hydroxyandrostenedione on steroid and tumour metabolism. In: Coombes RC, Dowsett M, editors, 4-hydroxyandrostenedione - A new approach to hormone-dependent cancer. Royal Society of Medicine Services Ltd, London; 1991. p. 45-49
84. Sourdaine P, Parker MG, Telford J, Miller WR. Analysis of the aromatase cytochrome P450 gene in human breast cancers. J Mol Endocrinol 1994;13:331-337
85. Wang L, Ellsworth KA, Moon I, et al. Functional genetic polymorphisms in the aromatase gene CYP19 vary the response of breast cancer patients to neoadjuvant therapy with aromatase inhibitors. Cancer Res 2010;70:319-328
86. Miller WR, Anderson TJ, Hawkins RA, et al. Neoadjuvant endocrine treatment: the Edinburgh experience. In: Dowsett M, Howell A, editors, Primary medical therapy for breast cancer: clinical and biological aspects. Elsevier, Amsterdam; 1999. p. 89-99
87. Fuqua SA, Cui Y. Estrogen and progesterone receptor isoforms: clinical significance in breast cancer. Breast Cancer Res Treat 2004;87(Suppl 1):3-10
88. Bunone G, Briand PA, Miksicek RJ, Picard D. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 1996;15:2174-2183
89. Dowsett M, Harper-Wynne C, Boeddinghaus I, et al. HER-2 amplification impedes the antiproliferative effects of hormone therapy in estrogen receptor-positive primary breast cancer. Cancer Res 2001;61:8452-8458
90. Ellis MJ, Tao Y, Young O, et al. Estrogen-independent proliferation is present in estrogen-receptor HER2-positive primary breast cancer after neoadjuvant letrozole. J Clin Oncol 2006;24:3019-3025
91. Miller WR, Anderson TJ, White S, et al. Growth factor signalling in clinical breast cancer and its impact on response to conventional therapies: the Edinburgh experience. Endocr Relat Cancer 2005;12(Suppl 1):119-123
92. Zhu L, Chow LWC, Loo WTY, et al. Her2/neu expression predicts the response to antiaromatase neoadjuvant therapy in primary breast cancer: subgroup analysis from Celecoxib antiaromatase neoadjuvant trial. Clin Cancer Res 2004;10:4639-4644
93. Johnston SRD, Martin LA, Head J, et al. Aromatase inhibitors: combinations with fulvestrant or signal transduction inhibitors as a strategy to overcome endocrine resistance. J Steroid Biochem Mol Biol 2007;106:180-186
94. Robertson JF. Oestrogen receptor: a stable phenotype in breast cancer. Br J Cancer 1996;73:5-12
95. Allred DC, Harvey JM, Berardo M, Clark GM. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 1998;11:155-168