Expression of estrogen-related gene markers in breast cancer tissue predicts aromatase inhibitor responsiveness

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Moy, Irene ^a   Lin, Zhihong ^a   Rademaker, Alfred W ^b   Reierstad, Scott ^a   Khan, Seema A ^b   Bulun, Serdar E ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; AROMATASE INHIBITOR; BRCA1 PROTEIN; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; MESSENGER RNA; PROGESTERONE RECEPTOR; TAMOXIFEN;

ADULT; AKR1C3 GENE; AROMATASE GENE; ARTICLE; BREAST CARCINOMA; CANCER ADJUVANT THERAPY; CANCER RECURRENCE; CONTROLLED STUDY; DRUG RESPONSE; ESTRADIOL GENE; ESTROGEN RECEPTOR ALPHA GENE; FEMALE; GENE EXPRESSION; GENE TARGETING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MARKER GENE; MIDDLE AGED; PATIENT SELECTION; POSTMENOPAUSE; PREDICTIVE VALUE; PRIMARY TUMOR; PROGESTERONE RECEPTOR GENE; PROTEIN EXPRESSION; SENSITIVITY AND SPECIFICITY; TUMOR GENE; TUMOR SUPPRESSOR GENE;

3-HYDROXYSTEROID DEHYDROGENASES; ANTINEOPLASTIC AGENTS, HORMONAL; AROMATASE; AROMATASE INHIBITORS; BRCA1 PROTEIN; BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; DRUG RESISTANCE, NEOPLASM; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC MARKERS; HUMANS; HYDROXYPROSTAGLANDIN DEHYDROGENASES; MIDDLE AGED; NITRILES; RECEPTORS, PROGESTERONE; ROC CURVE; TAMOXIFEN; TREATMENT OUTCOME; TRIAZOLES; TUMOR MARKERS, BIOLOGICAL;

EID: 84892389544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077543     Document Type: Article

References (52)

1. Anderson WF, Chatterjee N, Ershler WB, Brawley OW (2002) Estrogen receptor breast cancer phenotypes in the Surveillance, Epidemiology, and End Results Database. Breast Cancer Res Treat 76: 27-36.
2. Osborne CK, McGuire WL (1980) Hormone receptors in primary and advanced breast cancer. Clin Endocrinol Metab 9: 361-368.
3. Miller WR, Anderson TJ, Evans DB, Krause A, Hampton G, et al. (2003) An integrated view of aromatase and its inhibition. J Steroid Biochem Mol Biol 86: 413-42.
4. Nadji M, Gomez-Fernandez C, Ganjei-Azar R, Morales AR. (2005) Immuno-histochemistry of estrogen and progesterone receptors reconsidered: experience with 5993 breast cancers. Am J Clin Pathol 123: 21-27.
5. Possinger K (2004) Fulvestrant: a new treatment for postmenopausal women with hormone-sensitive advanced breast cancer. Expert Opin Pharacother 5: 2549-2558.
6. Dowsett M (2003) Origin and characteristics of adverse events in aromatase inhibition therapy for breast cancer. Semin Oncol 30: 58-69.
7. Miller WR (2010) Aromatase inhibitors: prediction of response and nature of resistance. Expert Opin Pharmacother 11: 1873-1887.
8. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, et al. (2004) Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 96: 926-935.
9. Allred DC, Harvey JM, Berardo MD, Clark GM (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11: 155-168.
10. Mohsino SK, Weiss J, Havighurst T, Clark GM, Roanh le D, et al. (2004) Progesterone receptor by immunohistochemistry and clinical outcome in breast cancer: a validation study. Mod Pathol 17: 1545-1554.
11. Miller WR, Larionov A, Renshaw L, Anderson TJ, Walker JR, et al. (2009) Gene expression profiles differentiating between breast cancers clinically responsive or resistant to letrozole. J Clin Oncol 27: 1382-1387.
12. Baum M, Budzar AU, Cuzick J, Forbes J, Houghton JH, et al. (2002) 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 randomized trial. Lancet 359: 2131-2139.
13. Baum M, Buzdar A, Cuzick J, Forbes J, Houghton J, et al. (2003) Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvant treatment of postmenopausal women with early-stage breast cancer: results of the ATAC (Arimidex, Tamoxifen Alone or in Combination) trial efficacy and safety update analyses. Cancer 98: 1802-1810.
14. Goss PE, Ingle JN, Martino S, Robert NJ, Muss HB, et al. (2003) A randomized trial of letrozole in postmenopausal women after five years of tamoxifen therapy for early-stage breast cancer. N Engl J Med 349: 1793-1802.
15. Paridaens R, Dirix L, Lohrisch C, Beex L, Nooij M, et al. (2003) Mature results of a randomized phase II multicenter study of exemestane versus tamoxifen as first-line hormone therapy for postmenopausal women with metastatic breast cancer. Ann Oncol 14: 1391-1398.
16. Milla-Santos A, Milla L, Portella J, Rallo L, Pons M, et al. (2003) Anastrozole versus tamoxifen as first-line therapy in postmenopausal patients with hormonedependent advanced breast cancer: a prospective, randomized, phase III study. Am J Clin Oncol 26: 317-322.
17. Bernhard J, Thurlimann B, Schimtz SF, Castiglione-Gertsch M, Cavalli F, et al. (1999): Defining clinical benefit in postmenopausal patients with breast cancer under second-line endocrine treatment: Does quality of life matter? J Clin Oncol 17: 1672-1679.
18. Ishikawa H, Reierstad S, Demura M, Rademaker AW, Kasai T, et al. (2009) High aromatase expression in uterine leiomyoma tissues of African-American women. J Clin Endocrinol Metab 94: 1752-1756.
19. Amin SA, Huang CC, Reierstad S, Lin Z, Arbieva Z, et al. (2006) Paracrine-stimulated gene expression profile favors estradiol production in breast tumors. Mol Cell Endocrinol 253: 44-55.
20. Lu M, Chen D, Lin Z, Reierstad S, Trauernicht AM, et al. (2006) BRCA1 negatively regulates the cancer-associated aromatase promoters I.3 and II in breast adipose fibroblasts and malignant epithelial cells. J Clin Endocrinol Metab 91: 4514-4519.
21. Imir AG, Lin Z, Yin P, Deb S, Yilmaz B, et al. (2007) Aromatase expression in uterine leiomyomata is regulated primarily by proximal promoters I.3/II. J Clin Endocrinol Metab 92: 1979-1982.
22. Anderson H, Bulun S, Smith I, Dowsett M. (2007) Predictors of response to aromatase inhibitors. J Steroid Biochem Mol Biol 106: 49-54.
23. Dowsett M, Ebbs SR, Dixon JM, Skene A, Griffith C, et al. (2005) 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 23: 2477-2492.
24. Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, et al. (2010) American Society of Clinical/Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. Arch Pathol Lab Med 134: e48-72.
25. Andersen J, Orntoft TF, Poulsen HS (1988) Immunohistochemical demonstration of estrogen receptor (ER) in formalin-fixed, paraffin-embedded human breast cancer tissue by use of a monoclonal antibody to ER. J Histochem Cytochem 36: 1553-1560.
26. Amin SA, Huang CC, Reierstad S, Lin Z, Arbieva Z, et al. (2006) Paracrine-stimulated gene expression profile favors estradiol production in breast tumors. Mol Cell Endocrinol 253: 44-55.
27. Bulun SE, Lin Z, Imir G, Amin S, Demura M, et al. (2005) Regulation of aromatase expression in estrogen-responsive breast and uterine diseases: from bench to treatment. Pharmacol Rev 57: 359-383.
28. Murphy CG, Moynahan ME (2010) BRCA gene structure and function in tumor suppression: a repair centric perspective. Cancer J 16: 39-47.
29. Ma YX, Tomita Y, Fan S, Wu K, Tong Y, et al. (2005) Structural determinants of the BRCA1: estrogen receptor interaction. Oncogene 24: 1831-1846.
30. Zheng L, Annab LA, Afshari CA, Lee WH, Boyer TG (2001) BRCA1 mediates ligand-independent transcriptional repression of the estrogen receptor. Proc Natl Acad Sci 98: 9587-9592.
31. Chand AL, Simpson E, Clyne CD (2009) Aromatase expression is increased in BRCA1 mutation carriers. BMC Cancer 9: 148.
32. Fan S, Ma YX, Wang C, Yuan RQ, Meng Q, et al. (2001) Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene 20: 77-87.
33. Yamashita H, Nishio M, Kobayashi S, Ando Y, Sugiura H, et al. (2005) Phosphorylation of estrogen receptor alpha serine 167 is predictive of response to endocrine therapy and increases postrelapse survival in metastatic breast cancer. Breast Cancer Res 7: R753-R764.
34. Yamashita J, Nishio M, Toyama T, Sugiura H, Kondo N, et al. (2008) Low phosphorylation of estrogen receptor alpha (ERalpha) serine 118 and high phosphorylation of ERalpha serine 167 improve survival in ER-positive breast cancer. Endocr Relat Cancer 15: 755-763.
35. Zhang Z, Yamashita H, Toyama T, Omoto Y, Suguira H, et al. (2003) Quantitative determination, by real-time reverse transcription polymerase chain reaction, of aromatase mRNA in invasive ductal carcinoma of the breast. Breast Cancer Res 5: R250-R256.
36. Yamashita J, Nishio M, Toyama T, Sugiura H, Zhang Z, et al. (2004) Coexistence of HER2 over-expression and p53 protein accumulation is a strong prognostic molecular marker in breast cancer. Breast Cancer Res 6: R24-R30.
37. Mita K, Zhang A, Ando Y, Toyama T, Hamaguchi M, et al. (2007) Prognostic significance of insulin-like growth factor binding protein (IGFBP)-4 and IGFBP-5 expression in breast cancer. Jpn J Clin Oncol 37: 575-582.
38. Dowsett M, Cuzick J, Wale C, Forbes J, Mallon EA, et al. (2010) Prediction of risk of distant recurrence using the 21-gene recurrence score in node-negative and node-positive postmenopausal patients with breast cancer treated with anastrozole or tamoxifen: a TransATAC study. J Clin Oncol 28(11): 1829-1834.
39. ATAC Trialists Group; Forbes JF, Cuzick J, Buzdar A, Howell A, et al. (2008) Effect of anastrozole and tamoxifen as adjuvant treatment for early breast cancer: 100 month analysis of the ATAC trial. Lancet Oncol 9: 45-53.
40. Breast International Group (BIG) 1-98 collaborative group (2005) A comparison of letrozole and tamoxifen in postmenopausal women with early breast cancer. N Engl J Med 353: 2747-2757.
41. Coombes RC, Kilburn LS, Snowdon CF, Paridaens R, Coleman RE, et al. (2007) Survival and safety of exemestane versus tamoxifen after 2-3 years' tamoxifen treatment (Intergroup Exemestane Study): a randomized controlled trial. Lancet 369: 559-570.
42. Jakesz R, Jonat W, Gnant M, Mittlboeck M, Greil R, 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 9 and ARNO 95 trial. Lancet 366: 455-462.
43. Buzdar AU (2004) The ATAC (Arimidex, Tamoxifen, Alone or in Combination) Trial: an update. Clin Breast Cancer 5: S6-S12.
44. Buzdar AU, Powell KC, Blumenschein GR (1982) Aminoglutethimide after tamoxifen therapy in advanced breast cancer: MD Anderson Hospital experience. Cancer Res 42: 3448s-3450s.
45. Mathews AW (2008) Bad cancer tests drawing scrutiny. Wall Street Journal.
46. Rhodes A, Jasani B, Balaton AJ, Miller KD (2000) Immunohistochemical demonstration of estrogen and progesterone receptors: correlation of standards achieved on in house tumors with that achieved on external quality assessment material in over 150 laboratories from 26 countries. J Clin Pathol 53: 292-301.
47. Febbo PG, Ladanyi M, Aldape KD, De Marzo AM, Hammond ME, et al. (2011) NCCN Task Force report: evaluating the clinical utility of tumor markers in oncology. J Natl Compr Canc Netw 9: S1-32.
48. Cronin M, Pho M, Dutta D, Stephans JC, Shak S, et al. (2004) Measurement of gene expression in archival paraffin-embedded tissues: development and performance of a 92-gene reverse transcriptase-polymerase chain reaction assay. Am J Pathol 164: 35-42.
49. Esteva FJ, Sahin AA, Cristofanilli M, Coombes K, Lee SJ, et al. (2005) Prognostic role of a multigene reverse transcriptase-PCR assay in patients with node-negative breast cancer not receiving adjuvant systemic therapy. Clin Cancer Res 11: 3315-3319.
50. Mina L, Soule SE, Badve S, Baehner FL, Baker J, et al. (2007) Predicting response to primary chemotherapy: Gene expression profiling of paraffinembedded core biopsy tissue. Breast Cancer Res Treat 103: 197-208.
51. Baehner FL, Habel LA, Quesenberry CP (2006) Quantitative RT-PCR analysis of ER and PR by Oncotype DX indicates distinct and different associations with prognosis and prediction of tamoxifen benefit. Presented at the 29th Annual San Antonio Breast Cancer Symposium, San Antonio, TX, December 14-17(Abstract).
52. Ma XJ, Hilsenbeck SG, Wang W, Ding L, Sgroi DC, et al. (2006) The HOXB13:IL17BR expression index is a prognostic factor in early-stage breast cancer. J Clin Oncol 24: 4611-4619.