Flaxseed reduces the pro-carcinogenic micro-environment in the ovaries of normal hens by altering the PG and oestrogen pathways in a dose-dependent manner

British Journal of Nutrition

Volumn 113, Issue 9, 2015, Pages 1384-1395

  Dikshit, Anushka ^a   Filho, Manoel Adrião Gomes ^b   Eilati, Erfan ^a   McGee, Stacey ^a   Small, Carrie ^a   Gao, Chunqi ^a   Klug, Thomas ^c   Hales, Dale Buchanan ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSIDADE FEDERAL RURAL DE PERNAMBUCO   (Brazil)

^c Immuna Care Corporation   (United States)

Author keywords

Flaxseed; Oestrogen; Ovarian cancer prevention; PG

Indexed keywords

16 HYDROXYESTRONE; 2 HYDROXYESTRONE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; CYTOCHROME P450 3A4; ENTERODIOL; ENTEROLACTONE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTRONE DERIVATIVE; MESSENGER RNA; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROSTAGLANDIN E2; UNCLASSIFIED DRUG; 16-HYDROXYESTRONE; 2,3-BIS(3'-HYDROXYBENZYL)BUTANE-1,4-DIOL; 2,3-BIS(3'-HYDROXYBENZYL)BUTYROLACTONE; 2-HYDROXYESTRONE; ANTINEOPLASTIC AGENT; CYTOCHROME P450 3A; GAMMA BUTYROLACTONE; LIGNAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FOOD COMPOSITION; GAS CHROMATOGRAPHY; GENE EXPRESSION; HISTOPATHOLOGY; LEGHORN CHICKEN; LINSEED; LIQUID CHROMATOGRAPHY; LIVER LEVEL; NONHUMAN; OVARY; OVARY CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; THERAPY EFFECT; TREATMENT DURATION; TUMOR MICROENVIRONMENT; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CHEMISTRY; CHICKEN; DIET; FLAX; GENETICS; LIVER; METABOLISM; OVARIAN NEOPLASMS; VETERINARY;

GALLUS GALLUS;

4-BUTYROLACTONE; ANIMALS; ANTICARCINOGENIC AGENTS; CHICKENS; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1B1; CYTOCHROME P-450 CYP3A; DIET; DIETARY SUPPLEMENTS; DINOPROSTONE; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FEMALE; FLAX; HYDROXYESTRONES; LIGNANS; LIVER; OVARIAN NEOPLASMS; OVARY; RNA, MESSENGER;

EID: 84929773650     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S000711451500029X     Document Type: Article

References (58)

1. Thompson L, Boucher B, Liu Z, et al. (2006) Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan. Nutr Cancer 54, 184-201.
2. Axelson M, Sjovall J, Gustafsson BE, et al. (1982) Origin of lignans in mammals and identification of a precursor from plants. Nature 298, 659-660.
3. Prasad K (2000) Oxidative stress as a mechanism of diabetes in diabetic BB prone rats: effect of secoisolariciresinol diglucoside (SDG). Mol Cell Biochem 209, 89-96.
4. Daun JK, Barthet VJ, Chornick T, et al. (2003) Structure, composition, and variety development of flaxseed. In Flaxseed in Human Nutrition, 2nd ed., pp. 1-40 [L Thompson and SC Cunnane, editors]. Urbana, IL: AOCS Publishing.
5. Thompson L & Cunnane S (2003) Flaxseed, lignans, and cancer. In Flaxseed in Human Nutrition, 2nd ed., pp. 194-222 [L Thompson and SC Cunnane, editors]. Urbana, IL: AOCS Publishing.
6. 2 in hens. Gynecol Oncol 3, 620-628.
7. Ambros V & Chen X (2007) The regulation of genes and genomes by small RNAs. Development 134, 1635-1641.
8. Gupta RA, Tejada LV, Tong BJ, et al. (2003) Cyclooxygenase-1 is overexpressed and promotes angiogenic growth factor production in ovarian cancer. Cancer Res 63, 906-911.
9. Eilati E, Pan L, Bahr JM, et al. (2012) Age dependent increase in prostaglandin pathway coincides with onset of ovarian cancer in laying hens. Prostaglandins Leukot Essent Fatty Acids 87, 177-184.
10. Hales DB, Zhuge Y, Lagman JAJ, et al. (2008) Cyclooxygenases expression and distribution in the normal ovary and their role in ovarian cancer in the domestic hen (Gallus domesticus). Endocrine 33, 235-244.
11. Giles JR, Olson LM & Johnson PA (2006) Characterization of ovarian surface epithelial cells from the hen: a unique model for ovarian cancer. Exp Biol Med 231, 1718-1725.
12. Vane JR, Bakhle YS & Botting RM (1998) Cyclooxgenase 1 and 2. Annu Rev Pharmacol Toxicol 38, 97-120.
13. Ristimäki A, Honkanen N, Jänkälä H, et al. (1997) Expression of cyclooxygenase-2 in human gastric carcinoma. Cancer Res 57, 1276-1280.
14. Eberhart C, Coffey R, Radhika A, et al. (1994) Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 107, 1183-1188.
15. Parrett M, Harris R, Joarder F, et al. (1997) Cyclooxygenase-2 gene expression in human breast cancer. Int J Oncol 10, 503-507.
16. Gupta S, Srivastava M, Ahmad N, et al. (2000) Over-expression of cyclooxygenase-2 in human prostate adenocarcinoma. Prostate 42, 73-78.
17. Kulkarni S, Rader JS, Zhang F, et al. (2001) Cyclooxygenase-2 is overexpressed in human cervical cancer. Clin Cancer Res 7, 429-434.
18. Molina MA, Sitja-Arnau M, Lemoine MG, et al. (1999) Increased cyclooxygenase-2 expression in human pancreatic carcinomas and cell lines growth inhibition by nonsteroidal anti-inflammatory drugs. Cancer Res 59, 4356-4362.
19. Hida T, Kozaki K-i, Muramatsu H, et al. (2000) Cyclooxygenase-2 inhibitor induces apoptosis and enhances cytotoxicity of various anticancer agents in non-small cell lung cancer cell lines. Clin Cancer Res 6, 2006-2011.
20. Wang L-Q, Meselhy MR, Li Y, et al. (2000) Human intestinal bacteria capable of transforming secoisolariciresinol diglucoside to mammalian lignans, enterodiol and enterolactone. Chem Pharm Bull (Tokyo) 48, 1606-1610.
21. Buck K, Zaineddin AK, Vrieling A, et al. (2010) Meta-analyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr 92, 141-153.
22. Velentzis L, Cantwell M, Cardwell C, et al. (2009) Lignans and breast cancer risk in pre- and post-menopausal women: meta-analyses of observational studies. Br J Cancer 100, 1492-1498.
23. McCann SE, Moysich KB, Freudenheim JL, et al. (2002) The risk of breast cancer associated with dietary lignans differs by CYP17 genotype in women. J Nutr 132, 3036-3041.
24. McCann SE, Muti P, Vito D, et al. (2004) Dietary lignan intakes and risk of pre- and postmenopausal breast cancer. Int J Cancer 111, 440-443.
25. O'Donnell AJ, Macleod KG, Burns DJ, et al. (2005) Estrogen receptor-α mediates gene expression changes and growth response in ovarian cancer cells exposed to estrogen. Endocr Relat Cancer 12, 851-866.
26. Mueller SO, Simon S, Chae K, et al. (2004) Phytoestrogens and their human metabolites show distinct agonistic and antagonistic properties on estrogen receptor a (ERa) and ERb in human cells. Toxicol Sci 80, 14-25.
27. Matsuda A & Katanoda K (2014) Five-year relative survival rate of ovarian cancer in the USA, Europe and Japan. Jpn J Clin Oncol 44, 196.
28. Barua A, Bitterman P, Abramowicz JS, et al. (2009) Histopathology of ovarian tumors in laying hens: a preclinical model of human ovarian cancer. Int J Gynecol Cancer 19, 531-539.
29. Lengyel E, Burdette J, Kenny H, et al. (2013) Epithelial ovarian cancer experimental models. Oncogene 33, 3619-3633.
30. Johnson KA (2009) The standard of perfection: thoughts about the laying hen model of ovarian cancer. Cancer Prev Res (Phila) 2, 97-99.
31. Johnson PA & Giles JR (2006) Use of genetic strains of chickens in studies of ovarian cancer. Poult Sci 85, 246-250.
32. Ansenberger K, Richards C, Zhuge Y, et al. (2010) Decreased severity of ovarian cancer and increased survival in hens fed a flaxseed-enriched diet for 1 year. Gynecol Oncol 117, 341-347.
33. Lynch MJRS, Mellor LD, Spare PD & Inwood MJ (1969) Medical Laboratory Technology and Clinical Pathology, 2nd ed. Philadelphia, PA/London/Toronto: WB Saunders Company.
34. Sheehan D & Hrapchak B (1980) Theory and Practice of Histology. St Louis, MO: CV Mosby Company.
35. 2 in laying hen ovaries. Prostaglandins Leukot Essent Fatty Acids 89, 179-187.
36. Eilati E, Small CC, McGee SR, et al. (2013) Anti-inflammatory effects of fish oil in ovaries of laying hens target prostaglandin pathways. Lip Health Dis 12, 152.
37. Muir AD & Westcott ND (2000) Quantitation of the lignan secoisolariciresinol diglucoside in baked goods containing flax seed or flax meal. J Agric Food Chem 48, 4048-4052.
38. Tsuchiya Y, Nakajima M, Kyo S, et al. (2004) Human CYP1B1 is regulated by estradiol via estrogen receptor. Cancer Res 64, 3119-3125.
39. Yager J & Leihr J (1996) Molecular mechanisms of estrogen carcinogenesis. Annu Rev Pharmacol Toxicol 36, 203-232.
40. Larsson SC, Kumlin M, Ingelman-Sundberg M, et al. (2004) Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms. Am J Clin Nutr 79, 935-945.
41. 2 in experimental inflammatory bowel disease is mediated through the IL-23 → IL-17 axis. J Immunol 178, 8138-8147.
42. Arico S, Pattingre S, Bauvy C, et al. (2002) Celecoxib induces apoptosis by inhibiting 3-phosphoinositide-dependent protein kinase-1 activity in the human colon cancer HT-29 cell line. J Biol Chem 277, 27613-27621.
43. Tsuchiya Y, Nakajima M & Yokoi T (2005) Cytochrome P450-mediated metabolism of estrogens and its regulation in human. Cancer Lett 227, 115-124.
44. Lee K & Bahr J (1994) Utilization of substrates for testosterone and estradiol-17β production by small follicles of the chicken ovary. Domest Anim Endocrinol 11, 307-314.
45. Zhuge Y, Lagman JA, Ansenberger K, et al. (2009) CYP1B1 expression in ovarian cancer in the laying hen Gallus domesticus. Gynecol Oncol 112, 171-178.
46. Telang NT, Suto A, Wong GY, et al. (1992) Induction by estrogen metabolite 16α-hydroxyestrone of genotoxic damage and aberrant proliferation in mouse mammary epithelial cells. J Natl Cancer Inst 84, 634-638.
47. Davis DL, Bradlow HL, Wolff M, et al. (1993) Medical hypothesis: xenoestrogens as preventable causes of breast cancer. Environ Health Perspect 101, 372-377.
48. Liehr JG, Wan-Fen F, Sirbasku DA, et al. (1986) Carcinogenicity of catechol estrogens in Syrian hamsters. J Steroid Biochem 24, 353-356.
49. Martin ME, Haourigui M, Pelissero C, et al. (1995) Interactions between phytoestrogens and human sex steroid binding protein. Life Sci 58, 429-436.
50. LaVallee TM, Zhan XH, Herbstritt CJ, et al. (2002) 2-Methoxyestradiol inhibits proliferation and induces apoptosis independently of estrogen receptors α and β. Cancer Res 62, 3691-3697.
51. Bradlow HL, Hershcopf RJ, Martucci CP, et al. (1985) Estradiol 16α-hydroxylation in the mouse correlates with mammary tumor incidence and presence of murine mammary tumor virus: a possible model for the hormonal etiology of breast cancer in humans. Proc Natl Acad Sci U S A 82, 6295-6299.
52. Bradlow H, Hershcopf R, Martucci C, et al. (1986) 16a-Hydroxylation of estradiol: a possible risk marker for breast cancer. Ann N Y Acad Sci 464, 138-151.
53. 0-nitro-N-nitrosoguanidine. Cancer Lett 211, 1-9.
54. Bell MC, Crowley-Nowick P, Bradlow HL, et al. (2000) Placebo-controlled trial of indole-3-carbinol in the treatment of CIN. Gynecol Oncol 78, 123-129.
55. Ho S-M (2003) Estrogen, progesterone and epithelial ovarian cancer. Reprod Biol Endocrinol 1, 73.
56. Spillman MA, Manning NG, Dye WW, et al. (2010) Tissuespecific pathways for estrogen regulation of ovarian cancer growth and metastasis. Cancer Res 70, 8927-8936.
57. Zhang L, Savas Ü, Alexander DL, et al. (1998) Characterization of the mouse CYP1B1 gene identification of an enhancer region that directs aryl hydrocarbon receptor-mediated constitutive and induced expression. J Biol Chem 273, 5174-5183.
58. Brasseur K, Leblanc V, Fabi F, et al. (2013) ERa-targeted therapy in ovarian cancer cells by a novel estradiol-platinum (II) hybrid. Endocrinology 154, 2281-2295.