Overcoming endocrine resistance in breast cancer - Are signal transduction inhibitors the answer?

Breast Cancer Research and Treatment

Volumn 108, Issue 3, 2008, Pages 307-317

  Bedard, Philippe L ^a   Freedman, Orit C ^a   Howell, Anthony ^b   Clemons, Mark ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b CHRISTIE HOSPITAL   (United Kingdom)

Author keywords

Endocrine resistance; Estrogen receptor; Signal transduction inhibitor

Indexed keywords

ANASTROZOLE; AROMATASE INHIBITOR; ERLOTINIB; ESTROGEN RECEPTOR; EXEMESTANE; FULVESTRANT; GEFITINIB; GROWTH FACTOR RECEPTOR; IMATINIB; LAPATINIB; LETROZOLE; PROGESTERONE RECEPTOR; PROTEIN TYROSINE KINASE INHIBITOR; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN; TEMSIROLIMUS; TRASTUZUMAB;

ASTHENIA; BREAST CANCER; CANCER GROWTH; CLINICAL TRIAL; DRUG RECEPTOR BINDING; HORMONAL THERAPY; HORMONE RESISTANCE; HUMAN; HYPERGLYCEMIA; METASTASIS; MULTICENTER STUDY; NEUTROPENIA; ONCOGENE NEU; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CLINICAL TRIALS AS TOPIC; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; NEOPLASMS, HORMONE-DEPENDENT; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION;

EID: 41149110156     PISSN: 01676806     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10549-007-9606-8     Document Type: Review

References (81)

1. Osborne CK, Schiff R (2005) Estrogen-receptor biology: continuing progress and therapeutic implications. J Clin Oncol 23:1616-1622
2. Normanno N, Di Maio M, De Maio E et al (2005) Mechanisms of endocrine resistance and novel therapeutic strategies in breast cancer. Endocr Relat Cancer 12:721-747
3. Yager JD, Davidson NE (2006) Estrogen carcinogenesis in breast cancer. N Engl J Med 354:270-282
4. Speirs V (1997) Oestrogen receptor in breast cancer: good, bad or still too early to tell? J Pathol 197:143-147
5. Jacob J, Sebastian KS, Devassy S et al (2006) Membrane estrogen receptors: genomic actions and post transcriptional regulation. Mol Cell Endocrinol 246:34-41
6. Filardo EJ, Thomas P (2005) GPR30: a seven-transmembrane-spanning estrogen receptor that triggers estrogen release. Trends Endocrinol Metab 16:362-367
7. Kahlert S, Nuedling S, van Eickels M et al (2000) Estrogen receptor alpha rapidly activates the IGF-1 receptor pathway. J Biol Chem 16:18447-18453
8. Barletta F, Wong CW, McNally C et al (2004) Characterization of the interactions of estrogen receptor and MNAR in the activation of Src. Mol Endocrinol 18:1096-1108
9. Johnston SR, Head J, Pancholi S et al (2003) Integration of signal transduction inhibitors with endocrine therapy: an approach to overcoming hormone resistance in breast cancer. Clin Cancer Res Jan(9): 524s-533s
10. Font de Mora J, Brown M (2000) AIB1 is a conduit for kinase mediated growth factor signaling to estrogen receptor. Mol Cell Biol 20:5041-5047
11. Simoncini T, Hafezi-Moghadam A, Brazil DP et al (2000) Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407(6803):538-541
12. Pietras RJ (2006) Biologic basis of sequential and combination therapies for hormone-resistant breast cancer. Oncologist 11:704-717
13. Ring A, Dowsett M (2004) Mechanisms of tamoxifen resistance. Endo Relat Cancer 11:643-658
14. Steger GG, Bartsch R, Wenzel C et al (2005) Fulvestrant ('Faslodex') in pre-treated patients with advanced breast cancer: a single-centre experience. Eur J Cancer 41(17):2655-2661
15. Gradishar W, Chia S, Piccart M, on behalf of the EFECT writing committee (2006) Fulvestrant versus exemestane following prior non-steroidal aromatase inhibitor therapy: first results from EFECT, a randomized, phase III trial in postmenopausal women with advanced breast cancer SABCS 2006: Abstr 12
16. Nkoy FL, Hammond E, Rees W et al (2005) Day of surgery affects estrogen receptor test results in women with breast cancer SABCS 2005: Abst 5107
17. Kuukasjarvi T, Kononen J, Helin H et al (1996) Loss of estrogen receptor in recurrent breast cancer is associated with poor response to endocrine therapy J Clin Oncol 14:2584-2589
18. Achuthan R, Bell SM, Roberts P et al (2001) Genetic events during the transformation of a tamoxifen sensitive human breast cancer cell line into a drug resistant clone. Cancer Genet Cytogenet 130:166-172
19. Hernyk MH, Fuqua SA (2004) Endocr Rev 25(6):869-898
20. Omoto Y, Kobayashi S, Inoue S et al (2002) Evaluation of oestrogen receptor ß wild-type and variant protein expression, and relationship with clinicopathological factors in breast cancers. Eur J Cancer 38:380-386
21. Saji S, Omoto Y, Shimizu C et al (2002) Clinical impact of assay of estrogen receptor β cx in breast cancer. Breast Cancer 9:303-307
22. Johnson MD, Zuo H, Lee KH et al (2004) Pharmacological characterization of 4-hydroxy-N-desmethyl tamoxifen, a novel active metabolite of tamoxifen. Breast Cancer Res Treat 85:151-159
23. Goetz MP, Rae JM, Suman VJ et al (2005) Pharmacogenetics of tamoxifen biotransformation is associated with clinical outcomes of efficacy and hot flashes. J Clin Oncol 23:9312-9318
24. Bonanni B, Macis D, Maisonneuve P et al (2006) Polymorphism in the CYP2D6 tamoxifen-metabolizing gene influences clinical effect but not hot flashes: data from the Italian tamoxifen trial. J Clin Oncol 24:3708-3709
25. Santen RJ, Song RX, Zhang Z et al (2004) Adaptive hypersensitivity to estrogen: mechanism for sequential responses to hormonal therapy in breast cancer Clin Cancer Res 10:337s-345s
26. Johnston SR, Dowsett M (2002) Aromatase inhibitors for breast cancer: lessons from the laboratory. Nat Rev Cancer 3:821-883
27. Berstein LM, Wang J-P, Zheng H et al (2004) Long-term exposure to tamoxifen induces hypersensitivity to estradiol. Clin Cancer Res 10:1530-1534
28. Yarden RI, Wilson MA, Chrysogelos SA (2001) Estrogen of EGFR expression in breast cancer cells: a possible mechanism to modulate growth. J Cell Biochem 81:232-246
29. Salvatori L, Pallante P, Ravenna L et al (2003) Oestrogens and selection estrogen receptor (ER) modulators regulate EGF receptor gene expression through ER-alpha and beta subtypes via an SP-1 site. Oncogene 22:4875-4881
30. Gutierrez MC, Detre S, Johnston S et al (2005) Molecular changes in tamoxifen-resistant breast cancer: relationship between estrogen receptor, HER-2, and p38 mitogen-activated protein kinase. J Clin Oncol 23:2469-2476
31. Mass R (2000) The role of HER-2 expression in predicting response to therapy in breast cancer. Semin Oncol 27:46-52
32. Ciocca DR, Elledge R (2000) Molecular markers for predicting response to tamoxifen in breast cancer patients. Endocrine 13:1-10
33. De Laurentiis M, Arpino G, Massarelli E et al (2005) A meta-analysis on the interaction between HER-2 expression and response to endocrine treatment in advanced breast cancer. Clin Cancer Res 11:4741-4748
34. Font de Mora J, Brown M (2000) A1B1 is a conduit for kinase-mediated growth factor signaling to the estrogen receptor. Mol Cell Biol 20:5041-5047
35. Osborne CK, Bardou V, Hopp TA et al (2003) Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J Natl Cancer Inst 95(5):353-361
36. Fleming FJ, Myers E, Kelly G et al (2004) Expression of SRC-1, AIB1, and PEA3 in HER2 mediated endocrine resistant breast cancer; a predictive role for SRC-1. J Clin Pathol 57:1069-1074
37. Ellis MJ, Coop A, Singh B et al (2001) 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 19:3808-3816
38. Smith IE, Dowsett M, Ebbs SR et al (2005) 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 23:5108-5116
39. Mauriac L, Keshaviah A, Debled M et al (2007) Predictors of early relapse in postmenopausal women with hormone receptor-positive breast cancer in the BIG 1-98 trial. Ann Oncology (advanced e-publishing)
40. McGuire WL, Horwitz KB, Pearson OH et al (1977) Current status of estrogen and progesterone receptors in breast cancer. Cancer 39:2934-2947
41. Ravdin PM, Green S, Dorr TM et al (1992) Prognostic significance of progesterone receptor levels in estrogen receptor-positive patients with metastatic breast cancer treated with tamoxifen: results of a prospective Southwest Oncology Group study. J Clin Oncol 10:1284-1291
42. Bardou VJ, Arpino G, Elledge RM et al (2003) Progesterone receptor status significantly improves outcome prediction over estrogen receptor status alone for adjuvant endocrine therapy in two large breast cancer databases. J Clin Oncol 21:1973-1979
43. Cui X, Schiff R, Arpino G et al (2005) Biology of progesterone receptor loss in breast cancer and its implications for endocrine therapy. J Clin Oncol 23:7721-7735
44. Dowsett M, Cuzick J, Wale C et al (2005) Retrospective analysis of time to recurrence in the ATAC trial according to hormone receptor status: an hypothesis-generating study. J Clin Oncol 23:7512-7517
45. Coombes RC, Hall E, Gibson LJ et al (2004) A randomized trial of exemestane after two to three years of tamoxifen therapy in postmenopausal women with primary breast cancer. N Engl J Med 350:1081-1092
46. Thürlimann B, Keshaviah A, Coates AS et al (2005) A comparison of letrozole and tamoxifen in postmenopausal women with early breast cancer. N Engl J Med 353:2747-2757
47. Jakesz R, Jonat W, Gnant M et al (2005) Switching of postmenopausal women with endocrine-responsive early breast cancer to anastrozole after 2 years' adjuvant tamoxifen: combined results of ABCSG trial 8 and ARNO 95 trial. Lancet 366:455-462
48. Cui X, Zhang P, Deng W et al (2003) Insulin-like growth factor-I inhibits progesterone receptor expression in breast cancer cells via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway: progesterone receptor as a potential indicator of growth factor activity in breast cancer Mol Endocrinol 17:575-588
49. Arpino G, Weiss H, Lee AV et al (2005) Estrogen receptor-positive, progesterone receptor negative breast cancer: association with growth factor receptor expression and tamoxifen resistance. J Natl Cancer Inst 97:1254-1261
50. Balleine RL, Earl MJ, Greenberg ML et al (1999) Absence of progesterone receptor associated with secondary breast cancer in postmenopausal women. Br J Cancer 79:1564-1571
51. Bamberger AM, Milde-Langosch K, Schulte HM et al (2000) Progesterone receptor isoforms, PR-B and PR-A, in breast cancer: correlations with clinicopathologic tumor parameters and expression of AP-1 factors. Horm Res 54:32-37
52. Dowsett M, Harper-Wynne C, Boeddinghaus I et al (2001) HER-2 amplification impedes the antiproliferative effects of hormone therapy in estrogen receptor-positive primary breast cancer. Cancer Res 61:8452-8458
53. Shi W, Zhang X, Pintilie M et al (2003) Dysregulated PTEN-PKB and negative receptor status in human breast cancer. Int J Cancer 104:195-203
54. Kirkegaard T, Witton CJ, McGlynn LM et al (2005) AKT activation predicts outcome in breast cancer patients treated with tamoxifen. J Pathol 207:139-146
55. Perez-Tenorio G, Stal O (2002) Activation of AKT/PKB in breast cancer predicts a worse outcome among endocrine treated patients. Br J Cancer 86:540-545
56. Gross GE, Clark GM, Chamness GC et al (1984) Multiple progesterone receptor assays in human breast cancer. Cancer Res 44:836-840
57. Nicholson RI, Staka C, Boyns F et al (2004) Growth-factor driven mechanisms associated with resistance to estrogen deprivation in breast cancer: new opportunities for therapy. Endo-Relat Cancer 11:623-641
58. Stoica A, Saceda M, Fakhro A, Salomon HB et al (1997) The role of transforming growth factor-beta in regulation of estrogen receptor expression in the MCF-7 breast cancer cell line. Endocrinology 138:1498-1505
59. Stoica A, Saceda M, Fakhro A et al (2000) Role of insulin-like growth factor-I in regulating estrogen receptor-alpha gene expression. J Cell Biochem 76:605-614
60. Stoica A, Saceda M, Doraiswamy VL et al (2000) Regulation of estrogen receptor-alpha gene expression by epidermal growth factor. J Endocrinol 165:371-378
61. Pink JJ, Jordan VC (1996) Models of estrogen receptor regulation by estrogens and antiestrogens in breast cancer cell lines. Cancer Res 56:2321-2330
62. Murphy CS, Pink JJ, Jordan VC (1990) Characterization of a receptor-negative, hormone-nonresponsive clone derived from a T47D human breast cancer cell line kept under estrogen-free conditions. Cancer Res 50:7285-7292
63. Pink JJ, Bilimoria MM, Assikis J et al (1996) Irreversible loss of the estrogen receptor in T47D breast cancer cells following prolonged estrogen deprivation. Br J Cancer 74:1227-1236
64. Marcom PK, Isaacs C, Harris L et al (2005) A phase II trial of letrozole and trastuzumab for ER and/or PgR and Her2 positive metastatic breast cancer: final results. J Clin Oncol 23:596
65. Kaufmann B, Mackey J, Clemons M et al (2006) Trastuzumab plus anastrozole prolongs progression-free survival in postmenopausal women with her2-positive, harmone-dependent metastatic breast cancer (MBC). Ann Oncol 17(Suppl 9): LBA2
66. Pietras RJ, Marquez DC, Chen H et al (2006) Improved antitumour therapy by dual targeting of estrogen and growth factor receptor signaling in human breast cancer cells. J Clin Oncol 24(18 Suppl):637
67. Dowsett M, Smith I, Skene A et al (2006) (Study 0223) Biological and clinical outcomes from a phase II placebo controlled neoadjuvant study of anastrozole alone or with gefitinib in postmenopausal women with ER/PGR+ breast cancer. J Clin Oncol 24(18 Suppl):515
68. Polychronis A, Sinnett HD, Hadjiminas D et al (2006) Anti-proliferative and molecular effects of neoadjuvant (pre-operative) gefitinib alone or in combination with anastrozole in epidermal growth factor receptor (EGFR) positive, estrogen receptor alpha (ERa) positive patients with primary breast cancer. J Clin Oncol 23(16 Suppl):552
69. Chow LW, Yip AY, Toi M (2006) Evaluation of neoadjuvant inhibition of aromatase activity and signal transduction in breast cancer Ann Oncol 17(Suppl 9): Abs422P
70. Mayer IA, Granja NM, Shyr Y et al (2006) A phase II trial of letrozole plus erlotinib in postmenopausal women with hormone sensitive matestatic breast cancer: preliminary results of toxicities and correlative studies. SABCS 2006: Abs4052
71. Johnson SRD, Semiglazov V, Manikhav G et al (2005) A randomized, blinded, phase II study of tipifarnib (Zarnestra) combined with letrozole in the treatment of advanced breast cancer after antiestrogen therapy. SABCS 2005: Abstr 5087
72. Dolenc F, Lacroix-Tikri M, Mourey L et al (2005) Tipifarnib with tamoxifen as a rescue for tamoxifen acquired clinical resistance for metastatic ER and/or PgR positive breast cancer after relapse under tamoxifen. Preliminary results SABCS 2005: Abstr 5098
73. Traina TA, Rugo H, Caravelli J et al (2006) Letrozole with bevacizumab is feasible in patients with hormone receptor positive metastatic breast cancer. J Clin Oncol 24(18 Suppl):3050
74. Carpenter JT, Roche H, Campone M et al (2005) Randomized 3-arm, phase 2 study of temsirolimus (CCI-779) in combination with letrozole in postmenopausal women with locally advanced or metastatic breast cancer. J Clin Oncol 23(16 Suppl):564
75. Chow LWC, Sun Y, Jassem J et al (2006) Phase III study of temsirolimus with letrozole or letrozole alone in postmenopausal women with locally advanced or metastatic breast cancer SABCS 2006: Abstr 6091
76. Farmer I, Evans DB, Lane HA et al (2006) Preclinical studies of the combination of RAD001 with tamoxifen or letrozole in breast cancer. Eur J Cancer Supplements 4(2):142: Abstr 324
77. Kai K, Nishimura R, Matsuda M et al (2005) P53 overexpression is a significant factor in predicting resistance to 3rd generation aromatase inhibitors (AIs) in hormone-sensitive recurrent or advanced breast cancer. J Clin Oncol 23(16 Suppl):715
78. Ellis MJ, Too Y, Lin L et al (2006) High nuclear (N) p27kip1 levels predict sensitivity to neoadjuvant letrozole in ER+ breast cancer independent of AKT levels, PIK3CA mutation status, and cell cycle effects: a potential role for p27kip1 in predicting enhanced autophagocytosis in response to aromatase inhibitor therapy. SABCS 2006: Abstr 4048
79. Finn RS, Dering J, Ginther C et al (2006) ER+ PR- breast cancer defines a unique subtype of breast cancer that is driven by growth factor signaling and may be more likely to respond to EGFR targeted therapies. J Clin Oncol 24(18 Suppl):514
80. Sakurada A, Shepherd FA, Tsao M-S (2006) Epidermal growth factor receptor tyrosine kinase inhibitors in lung cancer: impact of primary or secondary mutations. Clin Lung Cancer 7(Suppl 4):S138-S144
81. Hanneman J, Oosterkamp HM, Bosch CAJ et al (2006) Changes in gene expression associated with response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 23:3331-3342