The protective association of high plasma enterolactone with breast cancer is reasonably robust in women with polymorphisms in the estrogen receptor α and β genes

Journal of Nutrition

Volumn 139, Issue 5, 2009, Pages 993-1001

  Sonestedt, Emily ^a   Ivarsson, Malin I L ^a   Harlid, Sophia ^a   Ericson, Ulrika ^a   Gullberg, Bo ^a   Carlson, Joyce ^a   Olsson, Håkan ^a   Adlercreutz, Herman ^b   Wirfält, Elisabet ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROLACTONE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; 2,3 BIS(3' HYDROXYBENZYL)BUTYROLACTONE; 2,3-BIS(3'-HYDROXYBENZYL)BUTYROLACTONE; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; LIGNAN; PHYTOESTROGEN;

ADULT; AGED; ALLELE; ARTICLE; BLOOD; BLOOD LEVEL; BREAST CANCER; CANCER RISK; CONTROLLED STUDY; FEMALE; GENE INTERACTION; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; INTRON; MAJOR CLINICAL STUDY; MALE; NUCLEOTIDE SEQUENCE; POPULATION BASED CASE CONTROL STUDY; BREAST TUMOR; COHORT ANALYSIS; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; PROSPECTIVE STUDY; SINGLE NUCLEOTIDE POLYMORPHISM;

4-BUTYROLACTONE; AGED; BREAST NEOPLASMS; COHORT STUDIES; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LIGNANS; MIDDLE AGED; PHYTOESTROGENS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSPECTIVE STUDIES;

EID: 65349156844     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.108.101691     Document Type: Article

References (60)

1. Mattisson I, Wirfalt E, Johansson U, Gullberg B, Olsson H, Berglund G. Intakes of plant foods, fibre and fat and risk of breast cancer-a prospective study in the Malmo Diet and Cancer cohort. Br J Cancer. 2004;90:122-7.
2. Milder IE, Arts IC, van de Putte B, Venema DP, Hollman PC. Lignan contents of Dutch plant foods: a database including lariciresinol, pinoresinol, secoisolariciresinol and matairesinol. Br J Nutr. 2005;93:393-402.
3. Penalvo JL, Haajanen KM, Botting N, Adlercreutz H. Quantification of lignans in food using isotope dilution gas chromatography/mass spectrometry. J Agric Food Chem. 2005;53:9342-7.
4. Mazur W. Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab. 1998;12:729-42.
5. Heinonen S, Nurmi T, Liukkonen K, Poutanen K, Wahala K, Deyama T, Nishibe S, Adlercreutz H. In vitro metabolism of plant lignans: new precursors of mammalian lignans enterolactone and enterodiol. J Agric Food Chem. 2001;49:3178-86.
6. Adlercreutz H. Phytoestrogens and breast cancer. J Steroid Biochem Mol Biol. 2002;83:113-8.
7. Adlercreutz H. Lignans and human health. Crit Rev Clin Lab Sci. 2007;44:483-525.
8. Ingram D, Sanders K, Kolybaba M, Lopez D. Case-control study of phyto-oestrogens and breast cancer. Lancet. 1997;350:990-4.
9. Pietinen P, Stumpf K, Mannisto S, Kataja V, Uusitupa M, Adlercreutz H. Serum enterolactone and risk of breast cancer: a case-control study in eastern Finland. Cancer Epidemiol Biomarkers Prev. 2001;10:339-44.
10. Olsen A, Knudsen KE, Thomsen BL, Loft S, Stripp C, Overvad K, Moller S, Tjonneland A. Plasma enterolactone and breast cancer incidence by estrogen receptor status. Cancer Epidemiol Biomarkers Prev. 2004;13:2084-9.
11. Hulten K, Winkvist A, Lenner P, Johansson R, Adlercreutz H, Hallmans G. An incident case-referent study on plasma enterolactone and breast cancer risk. Eur J Nutr. 2002;41:168-76.
12. Kilkkinen A, Virtamo J, Vartiainen E, Sankila R, Virtanen MJ, Adlercreutz H, Pietinen P. Serum enterolactone concentration is not associated with breast cancer risk in a nested case-control study. Int J Cancer. 2004;108:277-80.
13. den Tonkelaar I, Keinan-Boker L, Veer PV, Arts CJ, Adlercreutz H, Thijssen JH, Peeters PH. Urinary phytoestrogens and postmenopausal breast cancer risk. Cancer Epidemiol Biomarkers Prev. 2001;10:223-8.
14. Verheus M, van Gils CH, Keinan-Boker L, Grace PB, Bingham SA, Peeters PH. Plasma phytoestrogens and subsequent breast cancer risk. J Clin Oncol. 2007;25:648-55.
15. Grace PB, Taylor JI, Low YL, Luben RN, Mulligan AA, Botting NP, Dowsett M, Welch AA, Khaw KT, et al. Phytoestrogen concentrations in serum and spot urine as biomarkers for dietary phytoestrogen intake and their relation to breast cancer risk in European prospective investigation of cancer and nutrition-norfolk. Cancer Epidemiol Bio-markers Prev. 2004;13:698-708.
16. Sonestedt E, Borgquist S, Ericson U, Gullberg B, Olsson H, Adlercreutz H, Landberg G, Wirfalt E. Enterolactone is differently associated with estrogen receptor {beta}-negative and -positive breast cancer in a swedish nested case-control study. Cancer Epidemiol Biomarkers Prev. 2008;17:3241-51.
17. Key T, Appleby P, Barnes I, Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective
18. studies. J Natl Cancer Inst. 2002;94:606-16.
19. Collaborative Group on Hormonal Factors in Breast Cancer. Breast-cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Collaborative Group on Hormonal Factors in Breast Cancer. Lancet. 1997;350:1047-59.
20. Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med. 2006;354:270-82.
21. Adlercreutz H, Bannwart C, Wahala K, Makela T, Brunow G, Hase T, Arosemena PJ, Kellis JT Jr, Vickery LE. Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol. 1993;44:147-53.
22. Wang C, Makela T, Hase T, Adlercreutz H, Kurzer MS. Lignans and flavonoids inhibit aromatase enzyme in human preadipocytes. J Steroid Biochem Mol Biol. 1994;50:205-12.
23. Brooks JD, Thompson LU. Mammalian lignans and genistein decrease the activities of aromatase and 17beta-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem Mol Biol. 2005;94:461-7.
24. Low YL, Dunning AM, Dowsett M, Folkerd E, Doody D, Taylor J, Bhaniani A, Luben R, Khaw KT, et al. Phytoestrogen exposure is associated with circulating sex hormone levels in postmenopausal women and interact with ESR1 and NR1I2 gene variants. Cancer Epidemiol Biomarkers Prev. 2007;16:1009-16.
25. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology. 1998;139:4252-63.
26. Mueller SO, Simon S, Chae K, Metzler M, Korach KS. Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor alpha (ERalpha) and ERbeta in human cells. Toxicol Sci. 2004;80:14-25.
27. Penttinen P, Jaehrling J, Damdimopoulos AE, Inzunza J, Lemmen JG, van der Saag P, Pettersson K, Gauglitz G, Makela S, et al. Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology. 2007;148:4875-86.
28. Mousavi Y, Adlercreutz H. Enterolactone and estradiol inhibit each other's proliferative effect on MCF-7 breast cancer cells in culture. J Steroid Biochem Mol Biol. 1992;41:615-9.
29. Saji S, Hirose M, Toi M. Clinical significance of estrogen receptor beta in breast cancer. Cancer Chemother Pharmacol. 2005;56Suppl 1:21-6.
30. Duffy MJ. Estrogen receptors: role in breast cancer. Crit Rev Clin Lab Sci. 2006;43:325-47.
31. Matthews J, Gustafsson JA. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol Interv. 2003;3:281-92.
32. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 1997;138:863-70.
33. Herrington DM, Howard TD, Brosnihan KB, McDonnell DP, Li X, Hawkins GA, Reboussin DM, Xu J, Zheng SL, et al. Common estrogen receptor polymorphism augments effects of hormone replacement therapy on E-selectin but not C-reactive protein. Circulation. 2002;105:1879-82.
34. Einarsdottir K, Darabi H, Li Y, Low YL, Li YQ, Bonnard C, Sjolander A, Czene K, Wedren S, et al. ESR1 and EGF genetic variation in relation to breast cancer risk and survival. Breast Cancer Res. 2008;10:R15.
35. Gold B, Kalush F, Bergeron J, Scott K, Mitra N, Wilson K, Ellis N, Huang H, Chen M, et al. Estrogen receptor genotypes and haplotypes associated with breast cancer risk. Cancer Res. 2004;64:8891-900.
36. Wedren S, Lovmar L, Humphreys K, Magnusson C, Melhus H, Syvanen AC, Kindmark A, Landegren U, Fermer ML, et al. Oestrogen receptor alpha gene haplotype and postmenopausal breast cancer risk: a case control study. Breast Cancer Res. 2004;6:R437-49.
37. Onland-Moret NC, van Gils CH, Roest M, Grobbee DE, Peeters PH. The estrogen receptor alpha gene and breast cancer risk (The Netherlands). Cancer Causes Control. 2005;16:1195-202.
38. Cox DG, Bretsky P, Kraft P, Pharoah P, Albanes D, Altshuler D, Amiano P, Berglund G, Boeing H, et al. Haplotypes of the estrogen receptor beta gene and breast cancer risk. Int J Cancer. 2008;122:387-92.
39. Giacinti L, Claudio PP, Lopez M, Giordano A. Epigenetic information and estrogen receptor alpha expression in breast cancer. Oncologist. 2006;11:1-8.
40. Manjer J, Carlsson S, Elmstahl S, Gullberg B, Janzon L, Lindstrom M, Mattisson I, Berglund G. The Malmo Diet and Cancer Study: representativity, cancer incidence and mortality in participants and non-participants. Eur J Cancer Prev. 2001;10:489-99.
41. Berglund G, Elmstahl S, Janzon L, Larsson SA. The Malmo Diet and Cancer Study. Design and feasibility. J Intern Med. 1993;233:45-51.
42. Hirata S, Shoda T, Kato J, Hoshi K. Isoform/variant mRNAs for sex steroid hormone receptors in humans. Trends Endocrinol Metab: TEM. 2003;14:124-9.
43. Entrez SNP [cited 200±Oct]. Available from: http://www.ncbi.nlm. nih.gov/.
44. HapMap genome browser [cited 200±Oct]. Available from: http://www.hapmap.org/.
45. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21:263-5.
46. Pero RW, Olsson A, Berglund G, Janzon L, Larsson SA, Elmstahl S. The Malmo biological bank. J Intern Med. 1993;233:63-7.
47. Pero RW, Olsson A, Bryngelsson C, Carlsson S, Janzon L, Berglund G, Elmstahl S. Quality control program for storage of biologically banked blood specimens in the Malmo Diet and Cancer Study. Cancer Epidemiol Biomarkers Prev. 1998;7:803-8.
48. Adlercreutz H, Wang GJ, Lapcik O, Hampl R, Wahala K, Makela T, Lusa K, Talme M, Mikola H. Time-resolved fluoroimmunoassay for plasma enterolactone. Anal Biochem. 1998;265:208-15.
49. Stumpf K, Uehara M, Nurmi T, Adlercreutz H. Changes in the time-resolved fluoroimmunoassay of plasma enterolactone. Anal Biochem. 2000;284:153-7.
50. Merlo J, Berglund G, Wirfalt E, Gullberg B, Hedblad B, Manjer J, Hovelius B, Janzon L, Hanson BS, et al. Self-administered questionnaire compared with a personal diary for assessment of current use of hormone therapy: an analysis of 16,060 women. Am J Epidemiol. 2000;152:788-92.
51. Davey Smith G, Ebrahim S. 'Mendelian randomization': can genetic epidemiology contribute to understanding environmental determinants of disease? Int J Epidemiol. 2003;32:1-22.
52. Greenland S, Pearl J, Robins JM. Causal diagrams for epidemiologic research. Epidemiology. 1999;10:37-48.
53. Lampe JW. Isoflavonoid and lignan phytoestrogens as dietary bio-markers. J Nutr. 2003;133 Suppl 3:S956-64.
54. Kilkkinen A, Stumpf K, Pietinen P, Valsta LM, Tapanainen H, Adlercreutz H. Determinants of serum enterolactone concentration. Am J Clin Nutr. 2001;73:1094-100.
55. Johnsen NF, Hausner H, Olsen A, Tetens I, Christensen J, Knudsen KE, Overvad K, Tjonneland A. Intake of whole grains and vegetables determines the plasma enterolactone concentration of Danish women. J Nutr. 2004;134:2691-7.
56. Kilkkinen A, Pietinen P, Klaukka T, Virtamo J, Korhonen P, Adlercreutz H. Use of oral antimicrobials decreases serum enterolactone concentration. Am J Epidemiol. 2002;155:472-7.
57. Sonestedt E, Ericson U, Gullberg B, Penalvo JL, Adlercreutz H, Wirfalt E. Variation in fasting and non-fasting serum enterolactone concentrations in women of the Malmo Diet and Cancer cohort. Eur J Clin Nutr. 2008;62:1005-9.
58. Zeleniuch-Jacquotte A, Adlercreutz H, Akhmedkhanov A, Toniolo P. Reliability of serum measurements of lignans and isoflavonoid phytoe-strogens over a two-year period. Cancer Epidemiol Biomarkers Prev. 1998;7:885-9.
59. Vineis P. Sources of variation in biomarkers. In: Toniolo P, Boffetta P, Shuker DEG, Rothman N, Hulka B, Pearce N, editors. Application of biomarkers in cancer epidemiology. Lyon: IARC Sci Publ; 1997. p. 59-71.
60. Hedelin M, Balter KA, Chang ET, Bellocco R, Klint A, Johansson JE, Wiklund F, Thellenberg-Karlsson C, Adami HO, et al. Dietary intake of phytoestrogens, estrogen receptor-beta polymorphisms and the risk of prostate cancer. Prostate. 2006;66:1512-20.