Reduction in Ki-67 in benign breast tissue of high-risk women with the lignan secoisolariciresinol diglycoside

Cancer Prevention Research

Volumn 3, Issue 10, 2010, Pages 1342-1350

  Fabian, Carol J ^a   Kimler, Bruce F ^a   Zalles, Carola M ^b   Klemp, Jennifer R ^a   Petroff, Brian K ^a   Khan, Qamar J ^a   Sharma, Priyanka ^a   Setchell, Kenneth D R ^c   Zhao, Xueheng ^c   Phillips, Teresa A ^a   Metheny, Trina ^a   Hughes, Jennifer R ^a   Yeh, Hung Wen ^a   Johnson, Karen A ^d  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b Cedar Park Regional Medical Center   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROLACTONE; ESTRADIOL; KI 67 ANTIGEN; LIGNAN DERIVATIVE; PROGESTERONE; SECOISOLARICIRESINOL DIGLYCOSIDE; SOMATOMEDIN BINDING PROTEIN 3; TESTOSTERONE; UNCLASSIFIED DRUG;

ARTICLE; ASPIRATION BIOPSY; BREAST; BREAST CANCER; BREAST HYPERPLASIA; CANCER RISK; CELL STRUCTURE; CLINICAL ARTICLE; CYTOLOGY; ESTRADIOL BLOOD LEVEL; FEMALE; FOLLICULAR PHASE; HUMAN; HUMAN TISSUE; MAMMOGRAPHY; MENSTRUAL CYCLE; PRIORITY JOURNAL; WILCOXON SIGNED RANKS TEST;

ADULT; BREAST; BUTYLENE GLYCOLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESTRADIOL; FEMALE; HUMANS; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; LIGNANS; MAMMOGRAPHY; MIDDLE AGED; PHYTOESTROGENS; PILOT PROJECTS; PREMENOPAUSE; PROGESTERONE; RISK FACTORS; TESTOSTERONE;

EID: 77958541564     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-10-0022     Document Type: Article

References (83)

1. Setchell KDR, Lawson AM, Mitchell FL, et al. Lignans in man and in animal species. Nature 1980;287:740-2.
2. Setchell KDR, Lawson AM, Borriello SP, et al. Lignan formation in man-microbial involvement and possible roles in relation to cancer. Lancet 1981;2:4-7.
3. Bergman Jungeström M, Thompson LU, Dabrosin C. Flaxseed and its lignans inhibit estradiol-induced growth, angiogenesis, and secretion of vascular endothelial growth factor in human breast cancer xenografts in vivo. Clin Cancer Res 2007;13:1061-7.
4. Penttinen P, Jaehrling J, Damdimopoulos AE, et al. Diet-derived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology 2007;148:4875-86.
5. Nesbitt PD, Lam Y, Thompson LU. Human metabolism of mammalian lignan precursors in raw and processed flaxseed. Am J Clin Nutr 1999;69:549-55.
6. 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.
7. Wang W, Higuchi CM, Zhang R. Individual and combinatory effects of soy isoflavones on the in vitro potentiation of lymphocyte activation. Nutr Cancer 1997;29:29-34.
8. Mueller SO, Simon S, Chae K, et al. Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor α (ERα) and ERβ in human cells. Toxicol Sci 2004;80:14-25.
9. Carreau C, Flouriot G, Bennetau-Pelissero C, et al. Enterodiol and enterolactone, two major diet-derived polyphenol metabolites have different impact on ERα transcriptional activation in human breast cancer cells. J Steroid Biochem Mol Biol 2008;110:176-85.
10. Thompson LU, Robb P, Serraino M, et al. Mammalian lignan production from various foods. Nutr Cancer 1991;16:43-52.
11. Thompson LU, Boucher BA, Liu Z, et al. Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan. Nutr Cancer 2006;54:184-201. (Pubitemid 44316301)
12. de Kleijn MJ, van der Schouw YT, Wilson PW, et al. Intake of dietary phytoestrogens is low in postmenopausal women in the United States: the Framingham study. J Nutr 2001;131:1826-32.
13. Boker LK, Van der Schouw YT, De Kleijn MJ, et al. Intake of dietary phytoestrogens by Dutch women. J Nutr 2002;132:1319-28.
14. Thompson LU, Seidl MM, Rickard SE, et al. Antitumorigenic effect of a mammalian lignan precursor from flaxseed. Nutr Cancer 1996;26: 159-65.
15. Rickard SE, Yuan YV, Chen J, et al. Dose effects of flaxseed and its lignan on N-methyl-N-nitrosourea-induced mammary tumorigenesis in rats. Nutr Cancer 1999;35:50-7.
16. Chen J, Wang L, Thompson LU. Flaxseed and its components reduce metastasis after surgical excision of solid human breast tumor in nude mice. Cancer Lett 2006;234:168-75.
17. Wang L, Chen J, Thompson LU. The inhibitory effect of flaxseed on the growth and metastasis of estrogen receptor negative human breast cancer xenografts is attributed to both its lignan and oil components. Int J Cancer 2005;116:793-8. (Pubitemid 41099712)
18. Pietinen P, Stumpf K, Männistö S, et al. Serum enterolactone and risk of breast cancer: a case-control study in eastern Finland. Cancer Epidemiol Biomarkers Prev 2001;10:339-44. (Pubitemid 32703218)
19. Linseisan J, Piller R, Hermann S, et al. Dietary phytoestrogen intake and premenopausal breast cancer risk in a German case-control study. Int J Cancer 2004;110:284-90. (Pubitemid 38580404)
20. McCann SE, Muti P, Vito D, et al. Dietary lignan intakes and risk of pre- and postmenopausal breast cancer. Int J Cancer 2004;111: 440-3.
21. Boccardo F, Lunardi G, Guglielmini P, et al. Serum enterolactone levels and the risk of breast cancer in women with palpable cysts. Eur J Cancer 2004;40:84-9.
22. Zeleniuch-Jacquotte A, Adlercreutz H, Shore RE, et al. Circulating enterolactone and risk of breast cancer: a prospective study in New York. Br J Cancer 2004;91:99-105. (Pubitemid 39013052)
23. Olsen A, Knudsen KE, Thomsen BL, et al. Plasma enterolactone and breast cancer incidence by estrogen receptor status. Cancer Epidemiol Biomarkers Prev 2004;13:2084-9. (Pubitemid 40054302)
24. Piller R, Verla-Tebit E, Wang-Gohrke S, et al. CYP17 genotype modifies the association between lignan supply and premenopausal breast cancer risk in humans. J Nutr 2006;136:1596-603. (Pubitemid 43765368)
25. McCann SE, Kulkarni S, Trevisan M, et al. Dietary lignan intakes and risk of breast cancer by tumor estrogen receptor status. Breast Cancer Res Treat 2006;99:309-11. (Pubitemid 44337923)
26. Thanos J, Cotterchio M, Boucher BA, et al. Adolescent dietary phytoestrogen intake and breast cancer risk (Canada). Cancer Causes Control 2006;17:1253-61.
27. Touillaud MS, Thiébaut AC, Fournier A, et al. Dietary lignan intake and postmenopausal breast cancer risk by estrogen and progesterone receptor status. J Natl Cancer Inst 2007;99:475-86. (Pubitemid 47078736)
28. Sonestedt E, Ericson U, Gullberg B, et al. Variation in fasting and non-fasting serum enterolactone concentrations in women of the Malmö Diet and Cancer cohort. Eur J Clin Nutr 2008;62:1005-9.
29. Suzuki R, Rylander-Rudqvist T, Saji S, et al. Dietary lignans and postmenopausal breast cancer risk by oestrogen receptor status: a prospective cohort study of Swedish women. Br J Cancer 2008; 98:636-40. (Pubitemid 351214515)
30. Cotterchio M, Boucher BA, Kreiger N, et al. Dietary phytoestrogen intake - lignans and isoflavones - and breast cancer risk (Canada). Cancer Causes Control 2008;19:259-72.
31. Sonestedt E, Borgquist S, Ericson U, et al. Enterolactone is differently associated with estrogen receptor β-negative and ER-positive breast cancer in a Swedish nested case-control study. Cancer Epidemiol Biomarkers Prev 2008;17:3241-51.
32. Velentzis LS, Cantwell MM, Cardwell C, et al. Lignans and breast cancer risk in pre- and post-menopausal women: meta-analyses of observational studies. Br J Cancer 2009;100:1492-8.
33. Kilkkinen A, Stumpf K, Pietinen P, et al. Determinants of serum enterolactone concentration. Am J Clin Nutr 2001;73:1094-100.
34. Kilkkinen A, Pietinen P, Klaukka T, et al. Use of oral antimicrobials decreases serum enterolactone concentration. Am J Epidemiol 2002;155:472-7. (Pubitemid 34174159)
35. Lampe JW. Isoflavonoid and lignan phytoestrogens as dietary biomarkers. J Nutr 2003;133:956-64S.
36. French MR, Thompson LU, Hawker GA. Validation of a phytoestrogen food frequency questionnaire with urinary concentrations of isoflavones and lignan metabolites in premenopausal women. J Am Coll Nutr 2007;26:76-82.
37. Morisset AS, Lemieux S, Veilleux A, et al. Impact of a lignan-rich diet on adiposity and insulin sensitivity in post-menopausal women. Br J Nutr 2009;102:195-200.
38. McCann SE, Moysich KB, Freudenheim JL, et al. The risk of breast cancer associated with dietary lignans differs by CYP17 genotype in women. J Nutr 2002;132:3036-41.
39. Feigelson HS, Shames LS, Pike MC, Coetzee GA, Stanczyk FZ, Henderson BE. Cytochrome P450c17α gene (CYP17) polymorphism is associated with serum estrogen and progesterone concentrations. Cancer Res 1998;58:585-7.
40. Preston-Martin S, Pike MC, Ross RK, et al. Increased cell division as a cause of human cancer. Cancer Res 1990;50:7415-21.
41. Shaaban AM, Sloane JP, West CR, et al. Breast cancer risk in usual ductal hyperplasia is defined by estrogen receptor-α and Ki-67 expression. Am J Pathol 2002;160:597-604.
42. Santisteban M, Reynolds C, Barr Fritcher EG, et al. Ki67: a time-varying biomarker of risk of breast cancer in atypical hyperplasia. Breast Cancer Res Treat 2010;121:431-7.
43. Urruticoechea A, Smith IE, Dowsett M. Proliferation marker Ki-67 in early breast cancer. J Clin Oncol 2005;23:7212-20. (Pubitemid 46260309)
44. Dowsett M, Smith IE, Ebbs SR, et al. Prognostic value of Ki67 expression after short-term presurgical endocrine therapy for primary breast cancer. J Natl Cancer Inst 2007;99:167-70.
45. Fabian CJ, Kimler BF, Zalles CM, et al. Short-term breast cancer prediction by random periareolar fine-needle aspiration cytology and the Gail risk model. J Natl Cancer Inst 2000;92:1217-27.
46. Khan QJ, Kimler BF, Clark J, et al. Ki-67 expression in benign breast ductal cells obtained by random periareolar fine needle aspiration. Cancer Epidemiol Biomarkers Prev 2005;14:786-9.
47. Masood S, Frykberg ER, McLellan GL, et al. Prospective evaluation of radiologically directed fine needle aspiration biopsy of non-palpable breast lesions. Cancer 1990;66:1480-7.
48. Zalles C, Kimler BF, Kamel S, et al. Cytologic patterns in random aspirates from women at high and low risk for breast cancer. Breast J 1995;1:343-9.
49. Fabian CJ, Kimler BF, Mayo MS, et al. Breast-tissue sampling for risk assessment and prevention. Endocr Relat Cancer 2005;12:185-213.
50. Eliasson C, Kamal-Eldin A, Andersson R, et al. High-performance liquid chromatographic analysis of secoisolariciresinol diglucoside and hydroxycinnamic acid glucosides in flaxseed by alkaline extraction. J Chromatogr A 2003;1012:151-9. (Pubitemid 37297595)
51. Almada AL. SDG precision standardized flaxseed extract. Scientific Research Monograph; 2003. Available from: www.lignan.com.
52. Gail MH, Brinton LA, Byar DP, et al. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Natl Cancer Inst 1989;81:1879-86.
53. Dabrosin C. Increase of free insulin-like growth factor-1 in normal human breast in vivo late in the menstrual cycle. Breast Cancer Res Treat 2003;80:193-8.
54. Micheli A, Muti P, Secreto G, et al. Endogenous sex hormones and subsequent breast cancer in premenopausal women. Int J Cancer 2004;112:312-8. (Pubitemid 39244371)
55. Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 1999;84:3666-72. (Pubitemid 30645223)
56. Endogenous Hormones and Breast Cancer Collaborative Group. Free estradiol and breast cancer risk in postmenopausal women: comparison of measured and calculated values. Cancer Epidemiol Biomarkers Prev 2003;12:1457-61.
57. Byng JW, Boyd NF, Fishell E, et al. The quantitative analysis of mam-mographic densities. Phys Med Biol 1994;39:1629-38.
58. Setchell KDR, Childress C, Zimmer-Nechemias L, et al. Method for measurement of dietary secoisolariciresinol using HPLC with multi-channel electrochemical detection. J Med Food 1999;2:193-8. (Pubitemid 30133565)
59. Setchell KD, Lawson AM, McLaughlin LM, et al. Measurement of enterolactone and enterodiol, the first mammalian lignans, using stable isotope dilution and gas chromatography mass spectrometry. Biomed Mass Spectrom 1983;10:227-35.
60. Thompson LU, Chen JM, Li T, et al. Dietary flaxseed alters tumor biological markers in postmenopausal breast cancer. Clin Cancer Res 2005;11:3828-35. (Pubitemid 40685603)
61. Prasad K. Antioxidant activity of secoisolariciresinol diglucoside-derived metabolites, secoisolariciresinol, enterodiol, and enterolactone. Int J Angiol 2000;9:220-5.
62. Tan KP, Chen J, Ward WE, et al. Mammary gland morphogenesis is enhanced by exposure to flaxseed or its major lignan during suckling in rats. Exp Biol Med 2004;229:147-57. (Pubitemid 38146558)
63. Vissac-Sabatier C, Coxam V, Déchelotte P, et al. Phytoestrogen-rich diets modulate expression of Brca1 and Brca2 tumor suppressor genes in mammary glands of female Wistar rats. Cancer Res 2003; 63:6607-12. (Pubitemid 37322938)
64. Adlercreutz H, Bannwart C, Wahala K, et al. Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol 1993;44:147-53. (Pubitemid 23072266)
65. Brooks JD, Thompson LU. Mammalian lignans and genistein decrease the activities of aromatase and 17β-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem Mol Biol 2005;94:461-7.
66. Yokota T, Matsuzaki Y, Koyama M, et al. Sesamin, a lignan of sesame, down-regulates cyclin D1 protein expression in human tumor cells. Cancer Sci 2007;98:1447-53. (Pubitemid 47241769)
67. Fukumitsu S, Aida K, Ueno N, et al. Flaxseed lignan attenuates high-fat diet-induced fat accumulation and induces adiponectin expression in mice. Br J Nutr 2008;100:669-76.
68. Kim K, Baek A, Hwang J, et al. Adiponectin-activated AMPK stimulates dephosphorylation at AKT through protein phosphatase 2A activation. Cancer Res 2009;69:4018-26.
69. Power KA, Chen JM, Saarinen NM, et al. Changes in biomarkers of estrogen receptor and growth factor signaling pathways in MCF-7 tumors after short- and long-term treatment with soy and flaxseed. J Steroid Biochem Mol Biol 2008;112:13-9.
70. Youngren JF, Gable K, Penaranda C, et al. Nordihydroguaiaretic acid (NDGA) inhibits the IGF-1 and c-erbB2/HER2/neu receptors and suppresses growth in breast cancer cells. Breast Cancer Res Treat 2005; 94:37-46. (Pubitemid 41416940)
71. Boyd NF, Byng JW, Jong RA, et al. Quantitative classification of mammographic densities and breast cancer risk: results from the Canadian National Breast Screening Study. J Natl Cancer Inst 1995; 87:670-5.
72. Stuedal A, Gram IT, Bremnes Y, et al. Plasma levels of enterolactone and percentage mammographic density among postmenopausal women. Cancer Epidemiol Biomarkers Prev 2005;14:2154-9. (Pubitemid 41603261)
73. Khan QJ, Kimler BF, O'Dea AP, et al. Mammographic density does not correlate with Ki-67 expression or cytomorphology in benign breast cells obtained by random periareolar fine needle aspiration from women at high risk for breast cancer. Breast Cancer Res 2007;9:R35.
74. Stomper PC, Penetrante RB, Edge SB, et al. Cellular proliferative activity of mammographic normal dense and fatty tissue determined by DNA S phase percentage. Breast Cancer Res Treat 1996;37:229-36.
75. Hawes D, Downey S, Pearce CL, et al. Dense breast stromal tissue shows greatly increased concentration of breast epithelium but no increase in its proliferative activity. Breast Cancer Res 2006;8:R24.
76. Cuzick J, Warwick J, Pinney E, et al. Tamoxifen and breast density in women at increased risk of breast cancer. J Natl Cancer Inst 2004; 96:621-8.
77. Kimler BF, Ursin G, Fabian CJ, et al. Effect of the third generation selective estrogen receptor modulator arzoxifene on mammographic breast density [abstract 562]. J Clin Oncol 2006;24:18s.
78. Cigler T, Yaffe MJ, Johnston D, et al. A placebo-controlled trial examining the effects of letrozole on mammographic breast density and bone and lipid metabolism [abstract 2082]. San Antonio Breast Cancer Symposium, 2007.
79. Fabian CJ, Kimler BF, Zalles CM, et al. Reduction in proliferation with six months of letrozole in women on hormone replacement therapy. Breast Cancer Res Treat 2007;106:75-84.
80. Kimler BF, Metheny T, Hughes J, et al. Validation of Ki-67 as a response biomarker in prevention trials of women at high risk for development of breast cancer [abstract 2993]. Proceedings of the 100th Annual Meeting of the American Association for Cancer Research, April 18-22, 2009, Denver, Colorado. Philadelphia (PA): AACR; 2009, p. 723-4.
81. Ibarra-Drendall C, Wilke LG, Zalles C, et al. Reproducibility of random periareolar fine needle aspiration in a multi-institutional Cancer and Leukemia Group B (CALGB) cross-sectional study. Cancer Epidemiol Biomarkers Prev 2009;18:1379-85.
82. Goss PE, Li T, Theriault M, et al. Effects of dietary flaxseed in women with cyclical mastalgia. Breast Cancer Res Treat 2000;64:49.
83. Rosolowich V, Saettler E, Szuck B, et al, Society of Obstetricians and Gynecologists of Canada (SOGC). Mastalgia. J Obstet Gynaecol Can 2006;28:49-71.