Lipid peroxidation, oxidative stress genes and dietary factors in breast cancer protection: a hypothesis

We have recently proposed that lipid peroxidation may be a common mechanistic pathway by which obesity and hypertension lead to increased renal cell cancer risk. During this exercise, we noted a risk factor swap between breast and kidney cancer (oophorectomy and increased parity, detrimental for kidney, beneficial for breast; high blood pressure, detrimental for kidney, beneficial for breast when it occurs during pregnancy; alcohol, beneficial for kidney, detrimental for breast, and so on). We have subsequently proposed the hypothesis that lipid peroxidation represents a protective mechanism in breast cancer, and reviewed the evidence of the role of lipid peroxidation on established hormonal and non-hormonal factors for breast cancer. Here, we review the evidence in support of lipid peroxidation playing a role in the relationships between dietary factors and breast cancer. Available evidence implicates increased lipid peroxidation products in the anti-carcinogenic effect of suspected protective factors for breast cancer, including soy, marine n-3 fatty acids, green tea, isothiocyanates, and vitamin D and calcium. We also review the epidemiological evidence supporting a modifying effect of oxidative stress genes in dietary factor-breast cancer relationships.

[1]  D. B. Duncan MULTIPLE RANGE AND MULTIPLE F TESTS , 1955 .

[2]  Xiaofeng Meng,et al.  Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (-)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells. , 2002, Cancer research.

[3]  V. Darley-Usmar,et al.  Oxidation of human low-density lipoprotein by soybean 15-lipoxygenase in combination with copper (II) or met-myoglobin. , 1996, Free radical biology & medicine.

[4]  L. Vatten,et al.  Frequency of meat and fish intake and risk of breast cancer in a prospective study of 14,500 norwegian women , 1990, International journal of cancer.

[5]  D. C. Hurst,et al.  Modifications of response surface techniques for biological use , 1962 .

[6]  N. Probst-Hensch,et al.  The effect of cyclin D1 (CCND1) G870A-polymorphism on breast cancer risk is modified by oxidative stress among Chinese women in Singapore. , 2005, Carcinogenesis.

[7]  Thomas E Rohan,et al.  Fish Consumption and Breast Cancer Risk , 2002, Nutrition and cancer.

[8]  A. Whittemore,et al.  A Family-based Genetic Association Study of Variants in Estrogen-metabolism Genes COMT and CYP1B1 and Breast Cancer Risk , 2004, Breast Cancer Research and Treatment.

[9]  F. S. Pardo,et al.  Cyclin D1 induced apoptosis maintains the integrity of the G1/S checkpoint following ionizing radiation irradiation , 1996, Somatic cell and molecular genetics.

[10]  A. Kong,et al.  Epigallocatechin-3-gallate-induced stress signals in HT-29 human colon adenocarcinoma cells. , 2003, Carcinogenesis.

[11]  Norman L. Johnson,et al.  Cumulative Sum Control Charts for the Folded Normal Distribution , 1963 .

[12]  A. E. Rogers,et al.  Black tea and mammary gland carcinogenesis by 7,12-dimethylbenz[a]anthracene in rats fed control or high fat diets. , 1998, Carcinogenesis.

[13]  R. Pardini,et al.  Dietary menhaden oil enhances mitomycin C antitumor activity toward human mammary carcinoma MX-1 , 1995, Lipids.

[14]  P. Subbaiah,et al.  Novel Physiological Function of Sphingomyelin in Plasma , 1999, The Journal of Biological Chemistry.

[15]  X. Shu,et al.  Genetic polymorphism in the manganese superoxide dismutase gene, antioxidant intake, and breast cancer risk: results from the Shanghai Breast Cancer Study , 2004, Breast Cancer Research.

[16]  J. Freudenheim,et al.  Genetic polymorphisms in catechol-O-methyltransferase, menopausal status, and breast cancer risk. , 1998, Cancer research.

[17]  M. Lipkin,et al.  Vitamin D, calcium and prevention of breast cancer: a review. , 1999, Journal of the American College of Nutrition.

[18]  P. Boyle,et al.  Cigarette smoking, glutathione-S-transferase M1 and T1 genetic polymorphisms, and breast cancer risk (United States) , 2002, Cancer Causes & Control.

[19]  R. Lotan,et al.  Apoptosis as a novel target for cancer chemoprevention. , 2004, Journal of the National Cancer Institute.

[20]  C. McCORMICK Passive diffusion does not play a major role in the absorption of dietary calcium in normal adults. , 2002, The Journal of nutrition.

[21]  B. Stoll n-3 Fatty acids and lipid peroxidation in breast cancer inhibition , 2002, British Journal of Nutrition.

[22]  M. Kundi,et al.  Genotoxic effects of methyl isothiocyanate. , 2001, Mutation research.

[23]  E. Espinosa,et al.  Implications of Oxidative Stress and Cell Membrane Lipid Peroxidation in Human Cancer (Spain) , 2004, Cancer Causes & Control.

[24]  R. C. Bose,et al.  Simultaneous Confidence Interval Estimation , 1953 .

[25]  F. Kassie,et al.  Genotoxic effects of benzyl isothiocyanate, a natural chemopreventive agent. , 1999, Mutagenesis.

[26]  W. N. Everitt Two Theorems in Matrix Theory , 1962 .

[27]  E. Lehmann A General Concept of Unbiasedness , 1951 .

[28]  E. Germain,et al.  Effect of an a-Linolenic Acid-Rich Diet on Rat Mammary Tumor Growth Depends on the Dietary Oxidative Status , 2000, Nutrition and cancer.

[29]  R. Millikan,et al.  Catechol-O-methyltransferase and breast cancer risk. , 1998, Carcinogenesis.

[30]  D. Rose,et al.  Effects of dietary omega-3 fatty acids on human breast cancer growth and metastases in nude mice. , 1993, Journal of the National Cancer Institute.

[31]  A. Wu,et al.  Tea intake, COMT genotype, and breast cancer in Asian-American women. , 2003, Cancer research.

[32]  S. S. Wilks CERTAIN GENERALIZATIONS IN THE ANALYSIS OF VARIANCE , 1932 .

[33]  W. Willett,et al.  Meat and dairy food consumption and breast cancer: a pooled analysis of cohort studies. , 2002, International journal of epidemiology.

[34]  P. Parodi Dairy Product Consumption and the Risk of Breast Cancer , 2005, Journal of the American College of Nutrition.

[35]  A TEST OF WHETHER TWO PARALLEL REGRESSION LINES ARE THE SAME WHEN THE VARIANCES MAY BE UNEQUAL1 , 1962 .

[36]  R. Lerner,et al.  On signal sequence polymorphisms and diseases of distribution. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  J. A. White Chapter 9 – SIMULATION OF QUEUEING SYSTEMS , 1975 .

[38]  D. Horrobin,et al.  Polyunsaturated fatty acid-induced cytotoxicity against tumor cells and its relationship to lipid peroxidation. , 1988, Journal of the National Cancer Institute.

[39]  A. James Normal Multivariate Analysis and the Orthogonal Group , 1954 .

[40]  V. Steele,et al.  Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. , 1995, Anticancer research.

[41]  Y. Choo,et al.  Oxidative susceptibility of low density lipoprotein from rabbits fed atherogenic diets containing coconut, palm, or soybean oils , 1995, Lipids.

[42]  M. Gerber,et al.  Relationship between vitamin E and polyunsaturated fatty acids in breast cancer. Nutritional and metabolic aspects , 1989, Cancer.

[43]  Koichi Ito,et al.  Asymptotic Formulae for the Distribution of Hotelling's Generalized $T_0^2$ Statistic. II , 1956 .

[44]  K. Naidu Eugenol--an inhibitor of lipoxygenase-dependent lipid peroxidation. , 1995, Prostaglandins, leukotrienes, and essential fatty acids.

[45]  R. Koren,et al.  Vitamin D is a prooxidant in breast cancer cells. , 2001, Cancer research.

[46]  P. Kendell,et al.  Estimation of the mean life of the exponential distribution from grouped data when the sample is censored: With application to life-testing , 1963 .

[47]  B. Stoll Breast cancer and the western diet: role of fatty acids and antioxidant vitamins. , 1998, European journal of cancer.

[48]  V. Beral,et al.  Soya foods and breast cancer risk: a prospective study in Hiroshima and Nagasaki, Japan , 1999, British Journal of Cancer.

[49]  D. Bell,et al.  An association between the allele coding for a low activity variant of catechol-O-methyltransferase and the risk for breast cancer. , 1997, Cancer research.

[50]  M. Hirose,et al.  Effects of green tea catechins on the progression or late promotion stage of mammary gland carcinogenesis in female Sprague-Dawley rats pretreated with 7,12-dimethylbenz(a)anthracene. , 1997, Cancer letters.

[51]  J. Marsh,et al.  Effect of omega-3 fatty acids on growth of a rat mammary tumor. , 1984, Journal of the National Cancer Institute.

[52]  M. Pike,et al.  Role of Lipid Peroxidation in the Epidemiology and Prevention of Breast Cancer , 2005, Cancer Epidemiology Biomarkers & Prevention.

[53]  X. Shu,et al.  Urinary isothiocyanate levels, brassica, and human breast cancer. , 2003, Cancer research.

[54]  D. Liebler,et al.  Antioxidant chemistry of green tea catechins. Identification of products of the reaction of (-)-epigallocatechin gallate with peroxyl radicals. , 1999, Chemical research in toxicology.

[55]  Richard Bellman,et al.  Introduction to Matrix Analysis , 1972 .

[56]  S. Kulling,et al.  Antioxidant activity of isoflavones and their major metabolites using different in vitro assays. , 2006, Journal of agricultural and food chemistry.

[57]  J. Wolfowitz The Power of the Classical Tests Associated with the Normal Distribution , 1949 .

[58]  M. Fay,et al.  Effect of different types and amounts of fat on the development of mammary tumors in rodents: a review. , 1997, Cancer research.

[59]  N. Probst-Hensch,et al.  The effect of the cyclin D1 (CCND1) A870G polymorphism on colorectal cancer risk is modified by glutathione-S-transferase polymorphisms and isothiocyanate intake in the Singapore Chinese Health Study. , 2006, Carcinogenesis.

[60]  R. C. Bose Strongly regular graphs, partial geometries and partially balanced designs. , 1963 .

[61]  E. Acton,et al.  Further studies on the generation of reactive oxygen species from activated anthracyclines and the relationship to cytotoxic action and cardiotoxic effects. , 1982, Biochemical pharmacology.

[62]  G A Colditz,et al.  Dietary carotenoids and vitamins A, C, and E and risk of breast cancer. , 1999, Journal of the National Cancer Institute.

[63]  T. Byers,et al.  Diet in the epidemiology of breast cancer. , 1982, American journal of epidemiology.

[64]  C. Carlberg,et al.  Potentiation by vitamin D analogs of TNFα and ceramide-induced apoptosis in MCF-7 cells is associated with activation of cytosolic phospholipase A2 , 1999, Cell Death and Differentiation.

[65]  B. Pence Role of calcium in colon cancer prevention: experimental and clinical studies. , 1993, Mutation research.

[66]  P. Boyle,et al.  Glutathione S-transferase M1 and T1 genetic polymorphisms, alcohol consumption and breast cancer risk , 2003, British Journal of Cancer.

[67]  Frank Fish On networks of queues , 1962 .

[68]  R. Koren,et al.  1,25-Dihydroxyvitamin D3 enhances the susceptibility of breast cancer cells to doxorubicin-induced oxidative damage. , 1999, Cancer research.

[69]  A. Vercesi,et al.  Ca2+‐induced oxidative stress in brain mitochondria treated with the respiratory chain inhibitor rotenone , 2003, FEBS letters.

[70]  J. Liehr,et al.  Catechol-O-methyltransferase-catalyzed rapid O-methylation of mutagenic flavonoids. Metabolic inactivation as a possible reason for their lack of carcinogenicity in vivo. , 1994, The Journal of biological chemistry.

[71]  J. Srivastava On the monotonicity property of the three main tests for multivariate analysis of variance , 1964 .

[72]  W. Willett,et al.  Specific fatty acids and risks of breast and prostate cancer: dietary intake. , 1997, The American journal of clinical nutrition.

[73]  C. Clark Cockerham,et al.  The effect of field blocking on gain from selection , 1966 .

[74]  K. Egan,et al.  MnSOD polymorphism and breast cancer in a population-based case-control study. , 2003, Cancer letters.

[75]  Sander Greenland,et al.  The Value of Risk-Factor (“Black-Box”) Epidemiology , 2004, Epidemiology.

[76]  G. Mingrone,et al.  Serum and biliary lipid pattern in rabbits feeding a diet enriched with unsaturated fatty acids. , 1990, Experimental pathology.

[77]  C. González,et al.  The European Prospective Investigation into Cancer and Nutrition (EPIC) , 2004, Public Health Nutrition.

[78]  O. Blokhina,et al.  Antioxidants, oxidative damage and oxygen deprivation stress: a review. , 2003, Annals of botany.

[79]  M. Gerber,et al.  Relationship between vitamin E and poly-unsaturated fatty acids in breast cancer , 1990 .

[80]  D. Kang,et al.  Polymorphic catechol-O-methyltransferase gene and breast cancer risk. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[81]  R. Bouillon,et al.  Vitamin D endocrine system : structural, biological, genetic and clinical aspects : proceedings of the Eleventh Workshop on Vitamin D, Nashville, Tennessee, USA, May 27-June 1, 2000 , 2000 .

[82]  P. Hsu,et al.  On the Limiting Distribution of Roots of a Determinantal Equation , 1941 .

[83]  M. Gago-Domínguez,et al.  Lipid peroxidation and renal cell carcinoma: further supportive evidence and new mechanistic insights. , 2006, Free radical biology & medicine.

[84]  H. Bush,et al.  Breast Cancer Research , 1978, British Journal of Cancer.

[85]  M. Nesheim,et al.  What is the research base for the use of dietary supplements? , 1999, Public Health Nutrition.

[86]  D. Grobbee,et al.  Phytoestrogens and breast cancer risk. Review of the epidemiological evidence. , 2003, Breast cancer research and treatment.

[87]  C. Welsch The role of lipid peroxidation in growth suppression of human breast carcinoma by dietary fish oil. , 1997, Advances in experimental medicine and biology.

[88]  N. Terry MSJAMA: Access vs quality assurance: the e-health conundrum. , 2001, JAMA.

[89]  W. C. Guenther,et al.  Analysis of variance , 1968, The Mathematical Gazette.

[90]  C. Guégan,et al.  Programmed cell death in amyotrophic lateral sclerosis. , 2003, The Journal of clinical investigation.

[91]  M. Mattson,et al.  Calcium and reactive oxygen species mediate staurosporine‐induced mitochondrial dysfunction and apoptosis in PC12 cells , 1998, Journal of neuroscience research.

[92]  Ames,et al.  Cohort studies of fat intake and the risk of breast cancer--a pooled analysis. , 2000 .

[93]  F. Révillion,et al.  Vitamin‐D3 derivatives and breast‐tumor cell growth: Effect on intracellular calcium and apoptosis , 1995, International journal of cancer.

[94]  M. Uusitupa,et al.  Fatty acid composition of breast adipose tissue in breast cancer patients and in patients with benign breast disease. , 1995, Nutrition and cancer.

[95]  R. Shewfelt,et al.  TOWARD A COMPREHENSIVE MODEL FOR LIPID PEROXIDATION IN PLANT TISSUE DISORDERS , 1993, HortScience.

[96]  W. Koh,et al.  Marine n-3 fatty acid intake, glutathione S-transferase polymorphisms and breast cancer risk in post-menopausal Chinese women in Singapore. , 2004, Carcinogenesis.

[97]  W. Willett,et al.  Glutathione S-transferase mu and theta polymorphisms and breast cancer susceptibility. , 1999, Journal of the National Cancer Institute.

[98]  D. Gewirtz,et al.  The vitamin D3 analog EB 1089 enhances the response of human breast tumor cells to radiation. , 1999, Radiation research.

[99]  S. N. Roy Some remarks on normal multivariate analysis of variance , 1961 .

[100]  P. Hoel Confidence Regions for Linear Regression , 1951 .

[101]  H. Nishi,et al.  Polymorphisms in the SOD2 and HLA-DRB1 genes are associated with nonfamilial idiopathic dilated cardiomyopathy in Japanese. , 1999, Biochemical and biophysical research communications.

[102]  L. Wattenberg Inhibition of carcinogen-induced neoplasia by sodium cyanate, tert-butyl isocyanate, and benzyl isothiocyanate administered subsequent to carcinogen exposure. , 1981, Cancer research.

[103]  C. Huang,et al.  Protein insufficiency aggravates the enhanced lipid peroxidation and reduced activities of antioxidative enzymes in rats fed diets high in polyunsaturated fat. , 1992, The Journal of nutrition.

[104]  J. Potter,et al.  Soyfood intake during adolescence and subsequent risk of breast cancer among Chinese women. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[105]  A. Wald On the Power Function of the Analysis of Variance Test , 1942 .

[106]  M. Matheson,et al.  GSTT1 null genotype increases risk of premenopausal breast cancer. , 2002, Cancer letters.

[107]  D. Christiani,et al.  Manganese superoxide dismutase alanine-to-valine polymorphism at codon 16 and lung cancer risk. , 2001, Journal of the National Cancer Institute.

[108]  Ewan S. Page A Note on Assignment Problems , 1963, Comput. J..

[109]  E. Bresnick,et al.  Reduction in mammary tumorigenesis in the rat by cabbage and cabbage residue. , 1990, Carcinogenesis.

[110]  Walter L. Smith On the elementary renewal theorem for non-identically distributed variables , 1964 .

[111]  M. Jarman A radical approach to cancer , 1991, Nature.

[112]  D. Bell,et al.  Association between glutathione S-transferase M1, P1, and T1 genetic polymorphisms and development of breast cancer. , 1998, Journal of the National Cancer Institute.

[113]  W. Willett,et al.  N-acetyl transferase 2 genotypes, meat intake and breast cancer risk. , 1999, International journal of cancer.

[114]  M. Dianzani,et al.  4-hydroxynonenal and regulation of cell cycle: effects on the pRb/E2F pathway. , 2004, Free radical biology & medicine.

[115]  J. Brisson,et al.  Vitamin D, calcium, and mammographic breast densities. , 2004, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[116]  V. Chajès,et al.  Influence of n-3 fatty acids on the growth of human breast cancer cellsin vitro: Relationship to peroxides and Vitamin-E , 1995, Breast Cancer Research and Treatment.

[117]  Michael J. González,et al.  Effect of dietary fat on growth of MCF-7 and MDA-MB231 human breast carcinomas in athymic nude mice: relationship between carcinoma growth and lipid peroxidation product levels. , 1991, Carcinogenesis.

[118]  G. Stoewsand,et al.  Protective effect of dietary brussels sprouts against mammary carcinogenesis in Sprague-Dawley rats. , 1988, Cancer letters.

[119]  E. Lehmann Ordered Families of Distributions , 1955 .

[120]  J. O'kelly,et al.  Vitamin D analogs and breast cancer. , 2003, Recent results in cancer research. Fortschritte der Krebsforschung. Progres dans les recherches sur le cancer.

[121]  A Trichopoulou,et al.  Diet and breast cancer: A case‐control study in Greece , 1986, International journal of cancer.

[122]  G A Colditz,et al.  Association of dietary intake of fat and fatty acids with risk of breast cancer. , 1999, JAMA.

[123]  C. Rose,et al.  Induction by beta-bungarotoxin of apoptosis in cultured hippocampal neurons is mediated by Ca(2+)-dependent formation of reactive oxygen species. , 2003, Journal of Neurochemistry.

[124]  S. London,et al.  Fatty acid composition of the subcutaneous adipose tissue and risk of proliferative benign breast disease and breast cancer. , 1993, Journal of the National Cancer Institute.

[125]  E. S. Page Controlling the Standard Deviation by Cusums and Warning Lines , 1963 .

[126]  Jian-Min Yuan,et al.  Dietary isothiocyanates, glutathione S-transferase polymorphisms and colorectal cancer risk in the Singapore Chinese Health Study. , 2002, Carcinogenesis.

[127]  R. Yacobi,et al.  1,25-Dihydroxyvitamin D3 increases the sensitivity of human renal carcinoma cells to tumor necrosis factor α but not to interferon α or lymphokine-activated killer cells , 1996 .

[128]  J. Freudenheim,et al.  Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. , 2004, The Journal of nutrition.

[129]  Emma Lehmer,et al.  Inverse Tables of Probabilities of Errors of the Second Kind , 1944 .

[130]  Mitch Dowsett,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. , 2004, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[131]  R. Curi,et al.  NADPH‐oxidase activity and lipid peroxidation in neutrophils from rats fed fat‐rich diets , 1999, Cell biochemistry and function.

[132]  S. Abraham,et al.  Effect of dietary menhaden oil on tumor cell loss and the accumulation of mass of a transplantable mammary adenocarcinoma in BALB/c mice. , 1986, Journal of the National Cancer Institute.

[133]  E. Masini,et al.  Histamine release from rat mast cells induced by metabolic activation of polyunsaturated fatty acids into free radicals. , 1990, Biochemical pharmacology.

[134]  Keshav K. Singh,et al.  Polymorphisms in genes related to oxidative stress (MPO, MnSOD, CAT) and survival after treatment for breast cancer. , 2005, Cancer research.

[135]  E. Röhrdanz,et al.  Alterations of antioxidant enzyme expression in response to hydrogen peroxide. , 1998, Free radical biology & medicine.

[136]  H. O. Hartley,et al.  Guide to Tables in Mathematical Statistics , 1962 .

[137]  J. Hayes,et al.  Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. , 1999, Free radical research.

[138]  J. Sethuraman Some limit distributions connected with fixed interval analysis , 1963 .

[139]  C. la Vecchia,et al.  Dietary factors and breast cancer risk in Vaud, Switzerland. , 1993, Nutrition and cancer.

[140]  S. Masuda,et al.  Redox regulation of glutathione S-transferase induction by benzyl isothiocyanate: correlation of enzyme induction with the formation of reactive oxygen intermediates. , 2000, Cancer research.

[141]  C. Welsch,et al.  Review of the effects of dietary fat on experimental mammary gland tumorigenesis: role of lipid peroxidation. , 1995, Free radical biology & medicine.

[142]  V. Kosma,et al.  Association between manganese superoxide dismutase (MnSOD) gene polymorphism and breast cancer risk. , 2001, Carcinogenesis.

[143]  F. Lu,et al.  Growth Inhibition and Induction of Apoptosis in MCF-7 Breast Cancer Cells by Fermented Soy Milk , 2002, Nutrition and cancer.

[144]  P. K. Bhattacharya On an Analog of Regression Analysis , 1963 .

[145]  R. Vannucci Experimental Biology of Cerebral Hypoxia-Ischemia: Relation to Perinatal Brain Damage , 1990, Pediatric Research.

[146]  G. Colditz Epidemiology and Prevention of Breast Cancer , 2005, Cancer Epidemiology Biomarkers & Prevention.

[147]  J. Hirsch,et al.  Breast cancer risk and fatty acids in the breast and abdominal adipose tissues. , 1994, Journal of the National Cancer Institute.

[148]  Michael J. González,et al.  Dietary fish oil inhibits human breast carcinoma growth: A function of increased lipid peroxidation , 1993, Lipids.

[149]  A. Conney,et al.  Is 2-methoxyestradiol an endogenous estrogen metabolite that inhibits mammary carcinogenesis? , 1998, Cancer research.

[150]  F. Speizer,et al.  Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. , 2001, JAMA.

[151]  R. Kale,et al.  Role of Ca2+ in radiation‐induced damage in murine splenocytes , 2003, International journal of radiation biology.

[152]  P. Kris-Etherton,et al.  Polyunsaturated fatty acids in the food chain in the United States. , 2000, The American journal of clinical nutrition.

[153]  L. Hutchins,et al.  Polymorphisms in glutathione S-transferases (GSTM1 and GSTT1) and survival after treatment for breast cancer. , 2001, Cancer research.

[154]  N. Parinandi,et al.  Free radical-induced alterations of myocardial membrane proteins. , 1991, Archives of biochemistry and biophysics.

[155]  T. Obata Calcium overload enhances hydroxyl radical generation by 1-methyl-4 phenylpyridinium ion (MPP+) in rat striatum , 2003, Brain Research.

[156]  J. Witte,et al.  Diet and premenopausal bilateral breast cancer: A case-control study , 1997, Breast Cancer Research and Treatment.

[157]  E. S. Pearson,et al.  CONTRIBUTIONS TO THE THEORY OF TESTING STATISTICAL HYPOTHESES , 1967, Joint Statistical Papers.

[158]  P. Hsu ON GENERALIZED ANALYSIS OF VARIANCE. (I) , 1940 .

[159]  I. Andrulis,et al.  Genetic Variants of GPX1 and SOD2 and Breast Cancer Risk at the Ontario Site of the Breast Cancer Family Registry , 2004, Cancer Epidemiology Biomarkers & Prevention.

[160]  B. Ponder,et al.  A Systematic Review Of Genetic Polymorphisms and Breast Cancer Risk 1 , 2000 .

[161]  C. Astre,et al.  Tumor progression and oxidant-antioxidant status. , 1997, Cancer letters.

[162]  H. Hotelling The Generalization of Student’s Ratio , 1931 .

[163]  D. Acosta,et al.  Mitochondrial regulation of superoxide by Ca2+: an alternate mechanism for the cardiotoxicity of doxorubicin. , 1991, Toxicology and applied pharmacology.

[164]  R. Koren,et al.  1,25-Dihydroxyvitamin d3 potentiates the cytotoxic effect of TNF on human breast cancer cells , 1994, Molecular and Cellular Endocrinology.

[165]  M. Yadin,et al.  Queueing Systems with a Removable Service Station , 1963 .

[166]  Anthony W. Norman,et al.  Calcium and Calpain as Key Mediators of Apoptosis-like Death Induced by Vitamin D Compounds in Breast Cancer Cells* , 2002, The Journal of Biological Chemistry.

[167]  R. Koren,et al.  Synergistic anticancer activity of 1,25-dihydroxyvitamin D3 and immune cytokines: the involvement of reactive oxygen species , 2000, The Journal of Steroid Biochemistry and Molecular Biology.

[168]  B. Zhu Catechol-O-Methyltransferase (COMT)-mediated methylation metabolism of endogenous bioactive catechols and modulation by endobiotics and xenobiotics: importance in pathophysiology and pathogenesis. , 2002, Current drug metabolism.

[169]  Salvatore Panico,et al.  Fish consumption and breast cancer risk. The European Prospective Investigation into Cancer and Nutrition (EPIC) , 2006, International journal of cancer.

[170]  J. Sethuraman FIXED INTERVAL ANALYSIS AND FRACTILE ANALYSIS , 1965 .

[171]  A TEST OF WHETHER TWO REGRESSION LINES ARE PARALLEL WHEN THE VARIANCES MAY BE UNEQUAL1 , 1962 .

[172]  P. Bougnoux,et al.  n-3 polyunsaturated fatty acids and cancer. , 1999, Current opinion in clinical nutrition and metabolic care.

[173]  M. Hirose,et al.  Post-initiation inhibitory effects of green tea catechins on 7,12-dimethylbenz[a]anthracene-induced mammary gland carcinogenesis in female Sprague-Dawley rats. , 1997, Cancer letters.

[174]  X. Shu,et al.  Dietary Calcium Intake and Breast Cancer Risk Among Chinese Women in Shanghai , 2003, Nutrition and cancer.

[175]  R. Stocker,et al.  Oxidation of Free Fatty Acids in Low Density Lipoprotein by 15-Lipoxygenase Stimulates Nonenzymic, α-Tocopherol-mediated Peroxidation of Cholesteryl Esters* , 1997, The Journal of Biological Chemistry.

[176]  H Vainio,et al.  Glutathione S-transferase M1, M3, P1, and T1 genetic polymorphisms and susceptibility to breast cancer. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[177]  Mimi C. Yu,et al.  Opposing effects of dietary n-3 and n-6 fatty acids on mammary carcinogenesis: The Singapore Chinese Health Study , 2003, British Journal of Cancer.

[178]  H Adlercreutz,et al.  Urinary phytoestrogens and postmenopausal breast cancer risk. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[179]  E. Riboli,et al.  Consumption of Meat, Animal Products, Protein, and Fat and Risk of Breast Cancer: A Prospective Cohort Study in New York , 1994, Epidemiology.

[180]  W. Willett,et al.  Types of dietary fat and breast cancer: A pooled analysis of cohort studies , 2001, International journal of cancer.

[181]  I. Rowland,et al.  Influence of dietary components associated with high or low risk of colon cancer on apoptosis in the rat colon. , 2002, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[182]  W. Rhoten,et al.  Regulation of intracellular calcium in human breast cancer cells , 1998, Endocrine.

[183]  J. N. Srivastava,et al.  Incomplete multiresponse designs , 1971 .

[184]  W. Willett,et al.  Dietary factors and the survival of women with breast carcinoma , 1999, Cancer.

[185]  H. Ohigashi,et al.  Involvement of the Mitochondrial Death Pathway in Chemopreventive Benzyl Isothiocyanate-induced Apoptosis* , 2002, The Journal of Biological Chemistry.

[186]  D. Noh,et al.  Alcohol consumption, glutathione S-transferase M1 and T1 genetic polymorphisms and breast cancer risk. , 2000, Pharmacogenetics.

[187]  F. Lallemand,et al.  Cyclin D1 overexpression enhances radiation-induced apoptosis and radiosensitivity in a breast tumor cell line. , 1999, Cancer research.

[188]  C. la Vecchia,et al.  Role of different types of vegetables and fruit in the prevention of cancer of the colon, rectum, and breast. , 1998, Epidemiology.

[189]  Somesh Das Gupta,et al.  On the optimum properties of some classification rules , 1962 .

[190]  Richard F. Potthoff,et al.  On testing for independence of unbiased coin tosses lumped in groups too small to use x2 , 1963 .

[191]  S. Wiseman,et al.  Antioxidants in tea. , 1997, Critical reviews in food science and nutrition.

[192]  S. Orrenius,et al.  Regulation of intracellular calcium compartmentation: studies with isolated hepatocytes and t-butyl hydroperoxide. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[193]  Jian-Min Yuan,et al.  Green tea, black tea and breast cancer risk: a meta-analysis of epidemiological studies. , 2006, Carcinogenesis.

[194]  F. Lallemand,et al.  Cyclin D 1 Overexpression Enhances Radiation-induced Apoptosis and Radiosensitivity in a Breast Tumor Cell Line 1 , 1999 .

[195]  A M Nomura,et al.  Tofu and risk of breast cancer in Asian-Americans. , 1996, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[196]  J. Cerhan,et al.  GSTM1 and GSTT1 polymorphisms and postmenopausal breast cancer risk , 2002, Breast Cancer Research and Treatment.

[197]  D. Alberts,et al.  Research and public health implications of the intricate relationship between calcium and vitamin D in the prevention of colorectal neoplasia. , 2004, Journal of the National Cancer Institute.

[198]  Calyampudi R. Rao,et al.  Advanced Statistical Methods in Biometric Research. , 1953 .

[199]  K. H. Chi,et al.  Menadione-induced DNA damage in a human tumor cell line. , 1991, Biochemical pharmacology.

[200]  H. Scheffé A METHOD FOR JUDGING ALL CONTRASTS IN THE ANALYSIS OF VARIANCE , 1953 .

[201]  P. van’t Veer,et al.  Adipose tissue omega-3 and omega-6 fatty acid content and breast cancer in the EURAMIC study. European Community Multicenter Study on Antioxidants, Myocardial Infarction, and Breast Cancer. , 1998, American journal of epidemiology.

[202]  Melvin R. Novick,et al.  A Bayesian Indifference Procedure , 1965 .

[203]  Chung S. Yang Inhibition of carcinogenesis by tea , 1997, Nature.

[204]  P. Naor,et al.  On discretionary priority queueing , 1964 .

[205]  P. Ferrari,et al.  N‐3 and N‐6 fatty acids in breast adipose tissue and relative risk of breast cancer in a case‐control study in Tours, France , 2002, International journal of cancer.

[206]  U. Das Essential fatty acids, lipid peroxidation and apoptosis. , 1999, Prostaglandins, leukotrienes, and essential fatty acids.

[207]  J W Waterbor,et al.  Understanding meta-analysis in cancer epidemiology: dietary fat and breast cancer. , 1999, Cancer detection and prevention.

[208]  C. Astre,et al.  Tumor progression and oxidant-antioxidant status. , 1996, Cancer letters.

[209]  G. Habermehl,et al.  Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumour necrosis factor-alpha. , 1989, The Biochemical journal.

[210]  A. Wolk,et al.  Brassica vegetables and breast cancer risk. , 2001, JAMA.

[211]  M. Kendall,et al.  The advanced theory of statistics , 1945 .

[212]  M. Lipkin,et al.  Effect of added dietary calcium on colonic epithelial-cell proliferation in subjects at high risk for familial colonic cancer. , 1985, The New England journal of medicine.

[213]  V. Fazio,et al.  Control of neoplastic cell proliferation and differentiation by restoration of 4-hydroxynonenal physiological concentrations. , 1993, Molecular aspects of medicine.

[214]  E. Bowman,et al.  Manganese superoxide dismutase (MnSOD) genetic polymorphisms, dietary antioxidants, and risk of breast cancer. , 1999, Cancer research.

[215]  J. Kalinich,et al.  4-Hydroxynonenal, an end-product of lipid peroxidation, induces apoptosis in human leukemic T- and B-cell lines , 2000, Free radical research.

[216]  R. Salganik The Benefits and Hazards of Antioxidants: Controlling Apoptosis and Other Protective Mechanisms in Cancer Patients and the Human Population , 2001, Journal of the American College of Nutrition.

[217]  C. Rose,et al.  Induction by β‐bungarotoxin of apoptosis in cultured hippocampal neurons is mediated by Ca2+‐dependent formation of reactive oxygen species , 2003 .

[218]  Y. Mizuno,et al.  Structural dimorphism in the mitochondrial targeting sequence in the human manganese superoxide dismutase gene. A predictive evidence for conformational change to influence mitochondrial transport and a study of allelic association in Parkinson's disease. , 1996, Biochemical and biophysical research communications.

[219]  Jian-Min Yuan,et al.  Lipid peroxidation: a novel and unifying concept of the etiology of renal cell carcinoma (United States) , 2002, Cancer Causes & Control.

[220]  S. N. Roy On a Heuristic Method of Test Construction and its use in Multivariate Analysis , 1953 .

[221]  I. Ulmanen,et al.  Kinetics of human soluble and membrane-bound catechol O-methyltransferase: a revised mechanism and description of the thermolabile variant of the enzyme. , 1995, Biochemistry.