Review: Aromatase in human breast carcinoma as a key regulator of intratumoral sex steroid concentrations

Endocrine Journal

Volumn 55, Issue 3, 2008, Pages 455-463

  Suzuki, Takashi ^a   Miki, Yasuhiro ^b   Akahira, Jun Ichi ^b   Moriya, Takuya ^c   Ohuchi, Noriaki ^b   Sasano, Hironobu ^b  

^a TOHOKU UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c KAWASAKI MEDICAL SCHOOL   (Japan)

Author keywords

Androgen; Aromatase; Breast carcinoma; Estrogen

Indexed keywords

ANASTROZOLE; ANDROGEN; ANDROSTANOLONE; ANTIESTROGEN; AROMATASE; AROMATASE INHIBITOR; ESTROGEN; EXEMESTANE; FULVESTRANT; GESTAGEN; GOSERELIN; LETROZOLE; LEUPRORELIN; MEDROGESTONE; SEX HORMONE; STERYL SULFATASE; TAMOXIFEN; TOREMIFENE;

ADIPOCYTE; BREAST CARCINOMA; CANCER PATIENT; CANCER TISSUE; CARCINOMA CELL; CELL TYPE; ENZYME LOCALIZATION; ENZYME REGULATION; ESTROGEN SYNTHESIS; HUMAN; NONHUMAN; OVARIECTOMY; PROTEIN EXPRESSION; REVIEW; STROMA CELL; BIOLOGICAL MODEL; BREAST TUMOR; CARCINOMA; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; OSMOLARITY; PHYSIOLOGY; TISSUE DISTRIBUTION;

AROMATASE; BREAST NEOPLASMS; CARCINOMA; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GONADAL STEROID HORMONES; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS, HORMONE-DEPENDENT; OSMOLAR CONCENTRATION; TISSUE DISTRIBUTION;

EID: 46749108473     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.K07E-053     Document Type: Review

References (57)

1. Robertson JF, Blarney RW (2003) The use of gonadot-rophin-releasing hormone (GnRH) agonists in early and advanced breast cancer in pre- and perimenopausal women. Eur J Cancer 39: 861-869.
2. Eneman JD, Wood ME, Muss HB (2004) Selecting adjuvant endocrine therapy for breast cancer. Oncology (Huntingt) 18: 1733-1744, discussion 1744-1744, 1748, 1751-1754.
3. Sasano H, Harada N (1998) Intratumoral aromatase in human breast, endometrial, and ovarian malignancies. Endocr Rev 19: 593-607.
4. Miller WR, Hawkins RA, Forrest AM (1982) Significance of aromatase activity in human breast cancer. Cancer Res 42: 3365s-3368s.
5. Miller WR (1991) Aromatase activity in breast tissue. J Steroid Biochem Mol Biol 39: 783-790.
6. Miyoshi Y, Ando A, Shiba E, Taguchi T, Tamaki Y, Noguchi S (2001) Involvement of up-regulation of 17beta-hydroxysteroid dehydrogenase type 1 in maintenance of intratumoral high estradiol levels in post-menopausal breast cancers, Int J Cancer 94: 685-689.
7. Chetrite GS, Cortes-Prieto J, Philippe JC, Wright F, Pasqualini JR (2000) Comparison of estrogen concentrations, estrone sulfatase and aromatase activities in normal, and in cancerous, human breast tissues. J Steroid Biochem Mol Biol 72: 23-27.
8. Labrie F, Luu-The V, Labrie C, Belanger A, Simard J, Lin SX, Pelletier G (2003) Endocrine and intracrine sources of androgens in women: inhibition of breast cancer and other roles of androgens and their precursor dehydroepiandrosterone. Endocr Rev 24: 152-182.
9. Brueggemeier RW, Hackett JC, Diaz-Cruz ES (2005) Aromatase inhibitors in the treatment of breast cancer. Endocr Rev 26: 331-345.
10. Geisler J, Lonning PE (2005) Endocrine effects of aromatase inhibitors and inactivators in vivo: review of data and method limitations. J Steroid Biochem Mol Biol 95: 75-81.
11. Geisler J (2003) Breast cancer tissue estrogens and their manipulation with aromatase inhibitors and inactivators. J Steroid Biochem Mol Biol 86: 245-253.
12. Baum M, Budzar AU, Cuzick J, Forbes J, Houghton JH, Klijn JG & Sahmoud T; ATAC Trialists' Group (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 randomised trial. Lancet 359: 2131-2139.
13. 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, Therasse P, Palmer MJ, Pater JL (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.
14. Baum M (2004) Current status of aromatase inhibitors in the management of breast cancer and critique of the MCIC MA-17 Trial. Cancer Control 11: 217-221.
15. Coombes RC, Hall E, Gibson LJ, Paridaens R, Jassem J, Delozier T, Jones SE, Alvarez I, Bertelli G, Ortmann O, Coates AS, Bajetta E, Dodwell D, Coleman RE, Fallowfield LJ, Mickiewicz E, Andersen J, Lonning PE, Cocconi G, Stewart A, Stuart N, Snowdon CF, Carpentieri M, Massimini G, Bliss JM; Intergroup Exemestane Study (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.
16. Howell A, Cuzick J, Baum M, Buzdar A, Dowsett M, Forbes JF, Hoctin-Boes G, Houghton J, Locker GY, Tobias JS; ATAC Trialists' Group (2005) Results of the ATAC (Arimidex, Tamoxifen, Alone or in Combination) trial after completion of 5 years' adjuvant treatment for breast cancer. Lancet 365: 60-62.
17. Miller WR, O'Neill J (1987) The importance of local synthesis of estrogen within the breast. Steroids 50: 537-548.
18. Bezwoda WR, Mansoor N, Dansey R, Esser D (1987) Correlation of breast tumour aromatase activity and response to aromatase inhibition with aminoglute-thimide. Oncology 44: 345-349.
19. Suzuki T, Miki Y, Nakamura Y, Moriya T, Ito K, Ohuchi N, Sasano H (2005) Sex steroid-producing enzymes in human breast cancer. Endocr Relat Cancer 12: 701-720.
20. Utsumi T, Harada N, Maruta M, Takagi Y (1996) Presence of alternatively spliced transcripts of aromatase gene in human breast cancer. J Clin Endocrinol Metab 81: 2344-2349.
21. Suzuki T, Miki Y, Moriya T, Akahira J, Hirakawa H, Ohuchi N, Sasano H (2007) In situ production of sex steroids in human breast carcinoma. Med Mol Morphol 40: 121-127.
22. Sasano H, Nagura H, Harada N, Goukon Y, Kimura M (1994) Immunolocalization of aromatase and other steroidogenic enzymes in human breast disorders. Hum Pathol 5: 530-533.
23. Santen RJ, Martel J, Hoagland M, Naftolin F, Roa L, Harada N, Hafer L, Zaino R, Santner SJ (1994) Stromal spindle cells contain aromatase in human breast tumors. J Clin Endocrinol Metab 79: 627-632.
24. Esteban JM, Warsi Z, Haniu M, Hall P, Shively JE, Chen S (1992) Detection of intratumoral aromatase in breast carcinomas. An immunohistochemical study with clinicopathologic correlation. Am J Pathol 140: 337-343.
25. Brodie AM, Lu Q, Long BJ, Fulton A, Chen T, Macpherson N, DeJong PC, Blankenstein MA, Nortier JW, Slee PH, van de Ven J, van Gorp JM, Elbers JR, Schipper ME, Blijham GH, Thijssen JH (2001) Aromatase and COX-2 expression in human breast cancers. J Steroid Biochem Mol Biol 79: 41-47.
26. Sasano H, Edwards DP, Anderson TJ, Silverberg SG, Evans DB, Santen RJ, Ramage P, Simpson ER, Bhatnagar AS, Miller WR (2003) Validation of new aromatase monoclonal antibodies for immunohis-tochemistry: progress report. J Steroid Biochem Mol Biol 86: 239-244.
27. Zhou J, Gurates B, Yang S, Sebastian S, Bulun SE (2001) Malignant breast epithelial cells stimulate aromatase expression via promoter II in human adipose fibroblasts: an epithelial-stromal interaction in breast tumors mediated by CCAAT/enhancer binding protein beta. Cancer Res 61: 2328-2334.
28. Zhao Y, Agarwal VR, Mendelson CR, Simpson ER (1996) Estrogen biosynthesis proximal to a breast tumor is stimulated by PGE2 via cyclic AMP, leading to activation of promoter II of the CYP19 (aromatase) gene. Endocrinol 137: 5739-5742.
29. Reed MJ, Purohit A, Woo LW, Newman SP, Potter BV (2005) Steroid sulfatase: molecular biology, regulation, and inhibition. Endocr Rev 26: 171-202.
30. Ryde CM, Nicholls JE, Dowsett M (1992) Steroid and growth factor modulation of aromatase activity in MCF7 and T47D breast carcinoma cell lines. Cancer Res 52: 1411-1415.
31. Zhang Y, Kulp SK, Sugimoto Y, Farrar WB, Brueggemeier RW, Lin YC (1998) Keratinocyte growth factor (KGF) induces aromatase activity in cultured MCF-7 human breast cancer cells. Anticancer Res 18: 2541-2546.
32. Miki Y, Suzuki T, Tazawa C, Yamaguchi Y, Kitada K, Honma S, Moriya T, Hirakawa H, Evans DB, Hayashi S, Ohuchi N, Sasano H (2007) Aromatase localization in human breast cancer tissues: possible interactions between intratumoral stromal and parenchymal cells. Cancer Res 67: 3945-3954.
33. Clyne CD, Speed CJ, Zhou J, Simpson ER (2002) Liver receptor homologue-1 (LRH-1) regulates expression of aromatase in preadipocytes. J Biol Chem 277: 20591-20597.
34. Zhou J, Suzuki T, Kovacic A, Saito R, Miki Y, Ishida T, Moriya T, Simpson ER, Sasano H, Clyne CD (2005) Interactions between prostaglandin E(2), liver receptor homologue-1, and aromatase in breast cancer. Cancer Res 65: 657-663.
35. Miki Y, Clyne CD, Suzuki T, Moriya T, Nakamura Y, Ishida T, Yabuki N, Kitada K, Hayashi S, Sasano H(2006) Immunolocalization of liver receptor homologue-1 (LRH-1) in human breast carcinoma: possible regulator of in situ steroidogenesis. Cancer Lett 244: 24-33.
36. Yang C, Zhou D, Chen S (1998) Modulation of aromatase expression in the breast tissue by ERRa-1 orphan receptor. Cancer Res 58: 5695-5700.
37. Suzuki T, Miki Y, Moriya T, Shimada N, Ishida T, Hirakawa H, Ohuchi N, Sasano H (2004) Estrogenrelated receptor a in human breast carcinoma as a potent prognostic factor. Cancer Res 64: 4670-676.
38. de Launoit Y, Dauvois S, Dufour M, Simard J, Labrie F (1991) Inhibition of cell cycle kinetics and proliferation by the androgen 5 alpha- dihydrotestosterone and antiestrogen N,n-butyl-N-methyl-l 1-[16′ alpha-chloro-3′,17 beta-dihydroxy-estra-r,3′,5′-(10′) triene-7′ alpha-yl] undecanamide in human breast cancer ZR-75-1 cells. Cancer Res 51: 2797-2802.
39. Ortmann J, Prifti S, Bohlmann MK, Rehberger-Schneider S, Strowitzki T, Rabe T (2002) Testosterone and 5 alpha-dihydrotestosterone inhibit in vitro growth of human breast cancer cell lines. Gynecol Endocrinol 16: 113-120.
40. Mistry P, Griffiths K, Maynard PV (1986) Endogenous C19-steroids and oestradiol levels in human primary breast tumour tissues and their correlation with androgen and oestrogen receptors. J Steroid Biochem 24: 1117-1125.
41. Recchione C, Venturelli E, Manzari A, Cavalleri A, Martinetti A, Secreto G (1995) Testosterone, dihy-drotestosterone and oestradiol levels in postmenopausal breast cancer tissues. J Steroid Biochem Mol Biol 52: 541-546.
42. Suzuki T, Miki Y, Moriya T, Akahira J, Ishida T, Hirakawa H, Yamaguchi Y, Hayashi S, Sasano H (2007) 5a-reductase type 1 and aromatase in breast carcinoma as regulators of in situ androgen production. Int J Cancer 20: 285-291.
43. Isola JJ (1993) Immunohistochemical demonstration of androgen receptor in breast cancer and its relationship to other prognostic factors. J Pathol 170: 31-35.
44. Suzuki T, Darnel AD, Akahira JI, Ariga N, Ogawa S, Kaneko C, Takeyama J, Moriya T, Sasano H (2001) 5a-reductases in human breast carcinoma: possible modulator of in situ androgenic actions. J Clin Endocrinol Metab 86: 2250-2257.
45. Moinfar F, Okcu M, Tsybrovskyy O, Regitnig P, Lax SF, Weybora W, Ratschek M, Tavassoli FA, Denk H (2003) Androgen receptors frequently are expressed in breast carcinomas: potential relevance to new therapeutic strategies. Cancer 98: 703-711.
46. Spinola PG, Marchetti B, Merand Y, Belanger A, Labrie F (1988) Effects of the aromatase inhibitor 4-hydroxyandrostenedione and the antiandrogen flutamide on growth and steroid levels in DMBA-induced rat mammary tumors. Breast Cancer Res Treat 12: 287-296.
47. Sonne-Hansen K, Lykkesfeldt AE (2005) Endogenous aromatization of testosterone results in growth stimulation of the human MCF-7 breast cancer cell line. J Steroid Biochem Mol Biol 93: 25-34.
48. Saeki T, Takashima S, Sasaki H, Hanai N, Salomon DS (1999) Localization of estrone sulfatase in human breast carcinomas. Breast Cancer 6: 331-337.
49. Suzuki T, Nakata T, Miki Y, Kaneko C, Moriya T, Ishida T, Akinaga S, Hirakawa H, Kimura M, Sasano H (2003) Estrogen sulfotransferase and steroid sulfatase in human breast carcinoma. Cancer Res 63: 2762-2770.
50. Sasano H, Frost AR, Saitoh R, Harada N, Poutanen M, Vihko R, Bulun SE, Silverberg SG, Nagura H (1996) Aromatase and 17beta-hydroxysteroid dehydrogenase type 1 in human breast carcinoma. J Clin Endocrinol Metab 81: 4042-4046.
51. Suzuki T, Moriya T, Ariga N, Kaneko C, Kanazawa M, Sasano H (2000) 17b-hydroxysteroid dehydrogenase type 1 and type 2 in human breast carcinoma: a correlation to clinicopathological parameters. Br J Cancer 82: 518-523.
52. Reed MJ, Purohit A (2001) Aromatase regulation and breast cancer. Clin Endocrinol 54: 563-571.
53. Stanway SJ, Purohit A, Woo LW, Sufi S, Vigushin D, Ward R, Wilson RH, Stanczyk FZ, Dobbs N, Kulinskaya E, Elliott M, Potter BV, Reed MJ, Coombes RC (2006) Phase 1 study of STX 64 (667 Coumate) in breast cancer patients: the first study of a steroid sulfatase inhibitor. Clin Cancer Res 12: 1585-1589.
54. Qiu W, Campbell RL, Gangloff A, Dupuis P, Boivin RP, Tremblay MR, Poirier D, Lin SX (2002) A concerted, rational design of type 1 17beta-hydroxysteroid dehydrogenase inhibitors: estradiol-adenosine hybrids with high affinity. FASEB J 16: 1829-1831.
55. Poirier D (2003) Inhibitors of 17 beta-hydroxysteroid dehydrogenases. Curr Med Chem 10: 453-477.
56. Fischer DS, Allan GM, Bubert C, Vicker N, Smith A, Tutill HJ, Purohit A, Wood L, Packham G, Mahon MF, Reed MJ, Potter BV (2005) E-ring modified steroids as novel potent inhibitors of 17b-hydroxysteroid dehydrogenase type 1. J Med Chem 48: 5749-5770.
57. Pasqualini JR (2003) Differential effects of progestins on breast tissue enzymes. Maturitas 46: S45-54.