Aromatase inhibitors and breast cancer

Hormone Molecular Biology and Clinical Investigation

Volumn 9, Issue 2, 2012, Pages 119-126

  Chumsri, Saranya ^a   Brodie, Angela ^b  

^a UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

aromatase inhibitors; breast cancer; hormone therapy

Indexed keywords

AROMATASE; AROMATASE INHIBITOR; LETROZOLE; TAMOXIFEN; TRASTUZUMAB;

AROMATIZATION; BREAST CANCER; CANCER HORMONE THERAPY; CANCER RESISTANCE; CEREBROVASCULAR ACCIDENT; DRUG EFFICACY; DRUG MECHANISM; ENDOMETRIUM CANCER; ESTROGEN SYNTHESIS; EVENT FREE SURVIVAL; HUMAN; IMMUNOBLOTTING; OSTEOLYSIS; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW; STEROIDOGENESIS;

EID: 84928300675     PISSN: 18681883     EISSN: 18681891     Source Type: Journal    
DOI: 10.1515/hmbci-2012-0001     Document Type: Article

References (64)

1. Society AC. Breast Cancer Facts & Figures, 2011–2012.
2. Beatson G. On the treatment of inoperable cases of carcinoma of the mamma: suggestions for a new method of treatment with illustrative cases. Lancet 1898;ii:104–107.
3. Love RR, Philips J. Oophorectomy for breast cancer: history revisited. J Natl Cancer Inst 2002;94:1433–1434.
4. Thompson EA Jr., Siiteri PK. Utilization of oxygen and reduced nicotinamide adenine dinucleotide phosphate by human placental microsomes during aromatization of androstenedione. J Biol Chem 1974;249:5364–5372.
5. Burstein HJ, Prestrud AA, Seidenfeld J, Anderson H, Buchholz TA, Davidson NE, Gelmon KE, Giordano SH, Hudis CA, Malin J, Mamounas EP, Rowden D, Solky AJ, Sowers MR, Stearns V, Winer EP, Somerfi eld MR, Griggs JJ. American Society of Clinical Oncology clinical practice guideline: update on adjuvant endocrine therapy for women with hormone receptor-positive breast cancer. J Clin Oncol 2010;28:3784–3796.
6. Chen SA, Besman MJ, Sparkes RS, Zollman S, Klisak I, Mohandas T, Hall PF, Shively JE. Human aromatase: cDNA cloning, southern blot analysis, and assignment of the gene to chromosome 15. DNA 1988; 7:27–38.
7. Macedo LF, Sabnis G, Brodie A. Aromatase inhibitors and breast cancer. Ann N Y Acad Sci 2009;1155:162–173.
8. Ghosh D, Griswold J, Erman M, Pangborn W. Structural basis for androgen specifi city and oestrogen synthesis in human aromatase. Nature 2009; 457: 219–223.
9. Smith IE, Dowsett M. Aromatase inhibitors in breast cancer. N Engl J Med 2003; 348: 2431–2442.
10. Harada N. Aberrant expression of aromatase in breast cancer tissues. J Steroid Biochem Mol Biol 1997;61:175–184.
11. Fisher B, Costantino JP, Redmond CK, Fisher ER, Wickerham DL, Cronin WM. Endometrial cancer in tamoxifen-treated breast cancer patients: fi ndings from the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14. J Natl Cancer Inst 1994; 86: 527–537.
12. Jordan VC. Tamoxifen: toxicities and drug resistance during the treatment and prevention of breast cancer. Annu Rev Pharmacol Toxicol 1995;35:195–211.
13. Brodie AM, Schwarzel WC, Shaikh AA, Brodie HJ. The effect of an aromatase inhibitor, 4-hydroxy-4-androstene-3,17-dione, on estrogen-dependent processes in reproduction and breast cancer. Endocrinology 1977;100:1684–1695.
14. Santen RJ, Brodie H, Simpson ER, Siiteri PK, Brodie A. History of aromatase: saga of an important biological mediator and therapeutic target. Endocr Rev 2009;30:343–375.
15. Hong Y, Yu B, Sherman M, Yuan YC, Zhou D, Chen S. Molecular basis for the aromatization reaction and exemestane-mediated irreversible inhibition of human aromatase. Mol Endocrinol 2007; 21: 401–414.
16. Miller WR, Bartlett J, Brodie AM, Brueggemeier RW, di Salle E, Lønning PE, Llombart A, Maass N, Maudelonde T, Sasano H, Goss PE. Aromatase inhibitors: are there differences between steroidal and nonsteroidal aromatase inhibitors and do they matter ? Oncologist 2008;13:829–837.
17. Goss PE, Hadji P, Subar M, Abreu P, Thomsen T, Banke-Bochita J. Effects of steroidal and nonsteroidal aromatase inhibitors on markers of bone turnover in healthy postmenopausal women. Breast Cancer Res 2007;9:R52.
18. Johannessen DC, Engan T, Di Salle E, Zurlo MG, Paolini J, Ornati G, Piscitelli G, Kvinnsland S, Lonning PE. Endocrine and clinical effects of exemestane (PNU 155971), a novel steroidal aromatase inhibitor, in postmenopausal breast cancer patients: a phase I study. Clin Cancer Res 1997;3:1101–1108.
19. Goss PE, Ingle JN, Ales-Martinez JE, Cheung AM, Chlebowski RT, Wactawski-Wende J, McTiernan A, Robbins J, Johnson KC, Martin LW, Winquist E, Sarto GE, Garber JE, Fabian CJ, Pujol P, Maunsell E, Farmer P, Gelmon KA, Tu D, Richardson H. Exemestane for breast-cancer prevention in postmenopausal women. N Engl J Med 2011;364:2381–2391.
20. Nabholtz JM, Buzdar A, Pollak M, Harwin W, Burton G, Mangalik A, Steinberg M, Webster A, von Euler M. Anastrozole is superior to tamoxifen as fi rst-line therapy for advanced breast cancer in postmenopausal women: results of a North American multicenter randomized trial. Arimidex Study Group. J Clin Oncol 2000;18:3758–3767.
21. Bonneterre J, Buzdar A, Nabholtz JM, Robertson JF, Thürlimann B, von Euler M, Sahmoud T, Webster A, Steinberg M. Anastrozole is superior to tamoxifen as first-line therapy in hormone receptor positiveadvanced breast carcinoma. Cancer 2001;92:2247–2258.
22. Forbes JF, Cuzick J, Buzdar A, Howell A, Tobias JS, Baum M. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial. Lancet Oncol 2008;9:45–53.
23. Brufsky A, Bundred N, Coleman R, Lambert-Falls R, Mena R, Hadji P, Jin L, Schenk N, Ericson S, Perez EA. Integrated analysis of zoledronic acid for prevention of aromatase inhibitor-associated bone loss in postmenopausal women with early breast cancer receiving adjuvant letrozole. Oncologist 2008;13:503–514.
24. Stopeck AT, Lipton A, Body JJ, Steger GG, Tonkin K, de Boer RH, Lichinitser M, Fujiwara Y, Yardley DA, Viniegra M, Fan M, Jiang Q, Dansey R, Jun S, Braun A. Denosumab compared with zoledronic acid for the treatment of bone metastases in patients with advanced breast cancer: a randomized, double-blind study. J Clin Oncol 2010; 28: 5132–5139.
25. Ellis GK, Bone HG, Chlebowski R, Paul D, Spadafora S, Smith J, Fan M, Jun S. Randomized trial of denosumab in patients receiving adjuvant aromatase inhibitors for nonmetastatic breast cancer. J Clin Oncol 2008;26:4875–4882.
26. Geisler J, Haynes B, Anker G, Dowsett M, Lønning PE. Infl uence 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.
27. Mouridsen HT. Aromatase inhibitors in advanced breast cancer. Semin Oncol 2004;31:3–8.
28. Bonneterre J, Thurlimann B, Robertson JF, Krzakowski M, Mauriac L, Koralewski P, Vergote I, Webster A, Steinberg M, von Euler M. Anastrozole versus tamoxifen as fi rst-line therapy for advanced breast cancer in 668 postmenopausal women: results of the Tamoxifen or Arimidex Randomized Group Effi cacyand Tolerability study. J Clin Oncol 2000;18:3748–3757.
29. Mouridsen H, Gershanovich M, Sun Y, Pérez-Carrión R, Boni C, Monnier A, Apffelstaedt J, Smith R, Sleeboom HP, Jänicke F, Pluzanska A, Dank M, Becquart D, Bapsy PP, Salminen E, Snyder R, Lassus M, Verbeek JA, Staffl er B, Chaudri-Ross HA, Dugan M. Superior efficacy of letrozole versus tamoxifen as first-line therapy for postmenopausal women with advanced breast cancer: results of a phase III study of the International Letrozole Breast Cancer Group. J Clin Oncol 2001;19:2596–2606.
30. Paridaens RTP, Dirix L. First line hormonal treatment for metastatic breast cancer with exemestane or tamoxifen in postmenopausal patients: s randomized phase III trial of the EORTC Breast Group, Proc Am Soc Clin Oncol, 2004, pp. 6.
31. Buzdar A, Douma J, Davidson N, Elledge R, Morgan M, Smith R, Porter L, Nabholtz J, Xiang X, Brady C.Phase III, multicenter, double-blind, randomized study of letrozole, an aromatase inhibitor, for advanced breast cancer versus megestrol acetate. J Clin Oncol 2001; 19: 3357–3366.
32. Buzdar A, Jonat W, Howell A, Jones SE, Blomqvist C, Vogel CL, Eiermann W, Wolter JM, Azab M, WebsterA, Plourde PV. Anastrozole, a potent and selective aromatase inhibitor, versus megestrol acetate in postmenopausal women with advanced breast cancer: results of overview analysis of two phase III trials. Arimidex Study Group. J Clin Oncol 1996;14: 2000–2011.
33. Dombernowsky P, Smith I, Falkson G, Leonard R, Panasci L, Bellmunt J, Bezwoda W, Gardin G, Gudgeon A, Morgan M, Fornasiero A, Hoffmann W, Michel J, Hatschek T, Tjabbes T, Chaudri HA, Hornberger U, Trunet PF. Letrozole, a new oral aromatase inhibitor for advanced breast cancer: double-blind randomized trial showing a dose effect and improved effi cacy and tolerability compared with megestrol acetate. J Clin Oncol 1998;16:453–461.
34. Kaufmann M, Bajetta E, Dirix LY, Fein LE, Jones SE, Zilembo N, Dugardyn JL, Nasurdi C, Mennel RG, Cervek J, Fowst C, Polli A, di Salle E, Arkhipov A, Piscitelli G, Miller LL, Massimini G. Exemestane is superior to megestrol acetate after tamoxifen failure in postmenopausal women with advanced breast cancer: results of a phase III randomized double-blind trial. The Exemestane Study Group. J Clin Oncol 2000;18: 1399–1411.
35. Goss PE, Winer EP, Tannock IF, Schwartz LH. Randomized phase III trial comparing the new potent and selective third-generation aromatase inhibitor vorozole with megestrol acetate in postmenopausal advanced breast cancer patients. North American Vorozole Study Group. J Clin Oncol 1999; 17: 52–63.
36. Thurlimann B, Keshaviah A, Coates AS, Mouridsen H, Mauriac L, Forbes JF, Paridaens R, Castiglione-Gertsch M, Gelber RD, Rabaglio M, Smith I, Wardley A, Price KN, Goldhirsch A. A comparison of letrozole and tamoxifen in postmenopausal women with early breast cancer. N Engl J Med 2005;353: 2747–2757.
37. Mouridsen H, Giobbie-Hurder A, Goldhirsch A, Thürlimann B, Paridaens R, Smith I, Mauriac L, Forbes JF, Price KN, Regan MM, Gelber RD, Coates AS. Letrozole therapy alone or in sequence with tamoxifen in women with breast cancer. N Engl J Med 2009; 361:766–776.
38. Gnant M, Mlineritsch B, Schippinger W, Luschin-Ebengreuth G, Pöstlberger S, Menzel C, Jakesz R, Seifert M, Hubalek M, Bjelic-Radisic V, Samonigg H, Tausch C, Eidtmann H, Steger G, Kwasny W, Dubsky P, Fridrik M, Fitzal F, Stierer M, Rücklinger E, Greil R. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009; 360: 679–691.
39. Jakesz R, Gnant M, Greil R. The benefits of sequencing adjuvant tamoxifen and anastrozole in postmenopausal women with hormone responsive early breast cancer: 5 year-analysis of ABCSG Trial 8, the 28th Annual San Antonio Breast Cancer Symposium. San Antonio, TX, 2005.
40. Kaufmann M, Jonat W, Hilfrich J, Eidtmann H, Gademann G, Zuna I, von Minckwitz G. Improved overall survival in postmenopausal women with early breast cancer after anastrozole initiated after treatmentwith tamoxifen compared with continued tamoxifen: the ARNO 95 Study. J Clin Oncol 2007;25: 2664–2670.
41. Boccardo F, Rubagotti A, Guglielmini P, Fini A, Paladini G, Mesiti M, Rinaldini M, Scali S, Porpiglia M, Benedetto C, Restuccia N, Buzzi F, Franchi R, Massidda B, Distante V, Amadori D, Sismondi P. Switching to anastrozole versus continued tamoxifen treatment of early breast cancer. Updated results of the Italian tamoxifen anastrozole (ITA) trial. Ann Oncol 2006;17(Suppl 7): vii10–4.
42. Coombes RC, Kilburn LS, Snowdon CF, Paridaens R, Coleman RE, Jones SE, Jassem J, Van de Velde CJ, Delozier T, Alvarez I, Del Mastro L, Ortmann O, Diedrich K, Coates AS, Bajetta E, Holmberg SB, Dodwell D, Mickiewicz E, Andersen J, Lønning PE, Cocconi G, Forbes J, Castiglione M, Stuart N, Stewart A, Fallowfi eld LJ, Bertelli G, Hall E, Bogle RG, Carpentieri M, Colajori E, Subar M, Ireland E, Bliss JM. Survival and safety of exemestane versus tamoxifen after 2–3 years' tamoxifen treatment (Intergroup Exemestane Study): a randomised controlled trial. Lancet 2007;369:559–570.
43. Cometta A, Kern W. [Treatment with oral antibiotics of febrile neutropenia in onco-haematology. The experience of the EORTC antimicrobial group]. Presse Med 2004;33:327–329.
44. Johnston SR, Head J, Pancholi S, Detre S, Martin LA, Smith IE, Dowsett M. Integration of signal transduction inhibitors with endocrine therapy: an approach to overcoming hormone resistance in breast cancer. Clin Cancer Res 2003;9:524S–532S.
45. Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000; 103: 843–852.
46. Brodie A, Jelovac D, Long BJ. Predictions from a preclinical model: studies of aromatase inhibitors and antiestrogens. Clin Cancer Res 2003;9:455S-9S.
47. Lin NU, Winer EP. Advances in adjuvant endocrine therapy for postmenopausal women. J Clin Oncol 2008;26:798–805.
48. Rea D, Hasenburg A, Seynaeve C. Five years of exemestane as initial therapy compared to 5 years of tamoxifen followed by exemestane: The TEAM Trial, a prospective, randomized, phase III trial in postmenopausal women with hormone-sensitive early breast cancer, the 32nd Annual San Antonio Breast Cancer Symposium. San Antonio, TX, 2009.
49. Jakesz R, Greil R, Gnant M, Schmid M, Kwasny W, Kubista E, Mlineritsch B, Tausch C, Stierer M, Hofbauer F, Renner K, Dadak C, Rücklinger E, Samonigg H. Extended adjuvant therapy with anastrozole among postmenopausal breast cancer patients: results from the randomized Austrian Breast and Colorectal Cancer Study Group Trial 6a. J Natl Cancer Inst 2007;99:1845–1853.
50. Goss PE, Ingle JN, Martino S, Robert NJ, Muss HB, Piccart MJ, Castiglione M, Tu D, Shepherd LE, Pritchard KI, Livingston RB, Davidson NE, Norton L, Perez EA, Abrams JS, Cameron DA, Palmer MJ, Pater JL. Effi cacy of letrozole extended adjuvant therapy according to estrogen receptor and progesterone receptor status of the primary tumor: National Cancer Institute of Canada Clinical Trials Group MA.17. J Clin Oncol 2007;25:2006–2011.
51. Mamounas EP, Jeong JH, Wickerham DL, Smith RE, Ganz PA, Land SR, Eisen A, Fehrenbacher L, Farrar WB,Atkins JN, Pajon ER, Vogel VG, Kroener JF, Hutchins LF, Robidoux A, Hoehn JL, Ingle JN, Geyer CE Jr,Costantino JP, Wolmark N. Benefit from exemestane as extended adjuvant therapy after 5 years of adjuvant tamoxifen: intention-to-treat analysis of the National Surgical Adjuvant Breast And Bowel Project B-33 trial. J Clin Oncol 2008;26:1965–1971.
52. Chia S, Gradishar W, Mauriac L, Bines J, Amant F, Federico M, Fein L, Romieu G, Buzdar A, Robertson JF, Brufsky A, Possinger K, Rennie P, Sapunar F, Lowe E, Piccart M. Double-blind, randomized placebo controlled trial of fulvestrant compared with exemestane after prior nonsteroidal aromatase inhibitor therapy in postmenopausal women with hormone receptor-positive, advanced breast cancer: results from EFECT. J Clin Oncol 2008;26:1664–1670.
53. Macedo LF, Sabnis G, Brodie A. Preclinical modeling of endocrine response and resistance: focus on aromatase inhibitors. Cancer 2008;112:679–688.
54. Jelovac D, Sabnis G, Long BJ, Macedo L, Goloubeva OG, Brodie AM. Activation of mitogen-activated protein kinase in xenografts and cells during prolonged treatment with aromatase inhibitor letrozole. Cancer Res 2005;65:5380–5389.
55. Macedo LF, Sabnis GJ, Goloubeva OG, Brodie A. Combination of anastrozole with fulvestrant in the intratumoral aromatase xenograft model. Cancer Res 2008;68:3516–3522.
56. Wu RC, Qin J, Yi P, Wong J, Tsai SY, Tsai MJ, O'Malley BW. Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic responses to multiple cellular signaling pathways. Mol Cell 2004;15:937–949.
57. Font de Mora J, Brown M. AIB1 is a conduit for kinasemediated growth factor signaling to the estrogen receptor. Mol Cell Biol 2000;20:5041–5047.
58. Johnston SR. Enhancing the effi cacy of hormonal agents with selected targeted agents. Clin Breast Cancer 2009;9(Suppl 1): S28–36.
59. Fan P, Wang J, Santen RJ, Yue W. Long-term treatment with tamoxifen facilitates translocation of estrogen receptor alpha out of the nucleus and enhances its interaction with EGFR in MCF-7 breast cancer cells. Cancer Res 2007;67:1352–1360.
60. Sabnis G, Goloubeva O, Gilani R, Brodie A. Sensitivity to the aromatase inhibitor letrozole is prolonged after a “break” in treatment. Mol Cancer Ther 2010;9:46–56.
61. Sabnis G, Schayowitz A, Goloubeva O, Macedo L, Brodie A. Trastuzumab reverses letrozole resistance and amplifies the sensitivity of breast cancer cells to estrogen. Cancer Res 2009;69:1416–1428.
62. Sabnis G, Goloubeva O, Jelovac D, Schayowitz A, Brodie A. Inhibition of the phosphatidylinositol 3-kinase/Akt pathway improves response of long-term estrogen-deprived breast cancer xenografts to antiestrogens. Clin Cancer Res 2007;13:2751–2757.
63. Johnston S, Pippen J Jr, Pivot X, Lichinitser M, Sadeghi S, Dieras V, Gomez HL, Romieu G, Manikhas A, Kennedy MJ, Press MF, Maltzman J, Florance A, O'Rourke L, Oliva C, Stein S, Pegram M. Lapatinib combined with letrozole versus letrozole and placebo as fi rst-line therapy for postmenopausal hormone receptor-positive metastatic breast cancer. J Clin Oncol 2009;27:5538–5546.
64. Baselga J, Campone M, Baselga J, Campone M, Piccart-Gebhart MJ, Burris HA, Rugo HS, Noguchi S, Gnant M, Pritchard KI, Lebrun F, Beck JT, Ito Y, Yardley DA, Deleu I, Perez A, Bachelot TD, Vittori L, Mukhopadhyay P, Weber D, Sahmoud T, Hortobagyi GN. Everolimus in combination with exemestane for postmenopausal women with advanced breast cancer who are refractory to letrozole or anastrozole: results of the BOLERO-2 phase III trial ESMO, 2011.