Maternal fish oil consumption has a negative impact on mammary gland tumorigenesis in C3(1) Tag mice offspring
Tóm tắt
Omega-3 fatty acids have been shown to reduce the incidence and slow the growth of mammary gland cancer in rodent models. Since exposure to dietary components during the critical developmental times of gestation and lactation may alter risk for mammary gland cancer in females, we tested whether exposure to increased levels of long-chain omega-3 fatty acids from fish oils would be preventive or promotional to mammary gland cancer in the offspring. Normal SV129 female mice were fed AIN 76 diets containing either 10% corn oil (control, 50% omega 6, n-6) or 5% of an omega-3 (n-3) fatty acid concentrate (fish oil 60% n-3) + 5% canola oil (10% n-3 + 20% n-6). Females were then mated with C(3)1 TAg transgenic mice. At weaning (3 weeks), pups were randomized to either the corn (C) or fish oil (F) diet, 15–17 mice per group. Four experimental groups were generated: FF, FC, CF and CC. Tumor incidence and multiplicity were assessed at the following time points 120, 130 and 140 days of age. A panel of genes encoding signal transduction proteins were analyzed in mammary glands at 130 days. Mice never exposed to fish oil (CC group) had a significantly higher incidence and multiplicity of mammary gland tumors than mice exposed to fish oil throughout life (FF group). Mice exposed to fish oil during a portion of life (CF or FC) had intermediate tumor incidences and multiplicities. Results also indicate that maternal consumption of fish oil increased the expression of genes associated with immune system activation (Ccl20, Cd5, Il2, Lef1, Lta). Adequate omega-3 fatty acids in the maternal diet may reduce the risk for mammary gland cancer in the offspring. If humans make dietary change by consuming more omega-3 fat instead of corn oil with 0% omega 3 fat, breast cancer may be reduced in the next generation.
Tài liệu tham khảo
https://www.wcrf.org/dietandcancer/cancer-trends/breast-cancer-statistics
De Souza RGM, Schincaglia RM, Pimente GD, Mota JF (2017) Nuts and human health outcomes: a systematic review. Nutrients 9(12). https://doi.org/10.3390/nu9121311
Li Y, Buckhaults P, Li S, Tollefsbol T (2018) Temporal efficacy of a sulforaphane-based broccoli sprout diet in prevention of breast cancer through modulation of epigenetic mechanisms. Cancer Prev Res 11(8):451–464. https://doi.org/10.1158/1940-6207.CAPR-17-04234
Aune D, Giovannucci E, Boffetta P, Fadnes LT, Keum N, Norat T, Greenwood DC, Riboli E, Vatten LJ, Tonstad S (2017) Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality-A systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol 46(3):1029–1056. https://doi:https://doi.org/10.1093/ije/dyw319
Zheng J, Zhou Y, Li Y, Xu DP, Li S, Li H Bin (2016) Spices for prevention and treatment of cancers. Nutrients 8(8). doi:https://doi.org/10.3390/nu8080495
Bojková B, Winklewski PJ, Wszedybyl-Winklewska M (2020) Dietary fat and cancer—which is good, which is bad, and the body of evidence. Int J Mol Sci 21(11):1–56. https://doi.org/10.3390/ijms21114114
Jain A, Tiwari A, Verma A, Jain SK (2017) Vitamins for cancer prevention and treatment: an insight. Curr Mol Med 17(5):321–340. https://doi.org/10.2174/1566524018666171205113329
Kim DH, Khan H, Ullah H, Hassan STS, Smejkal K, Efferth T, Mahomoodally MF, Xu S, Habtemariam S, Filosa R, Lagoa R, Rengasamy KR (2019) MicroRNA targeting by quercetin in cancer treatment and chemoprotection. Pharmacol Res 147(104346). https://doi.org/10.1016/j.phrs.2019.104346
Bostan M, Petrică-Matei G, Ion G, Radu N, Mihaila M, Hainarosie R, Brasoveanu LI, Roman V, Constantin C, Neagu MT (2019) Cisplatin effect on head and neck squamous cell carcinoma cells is modulated by ERK1/2 protein kinases. Exp Ther Med 18(6):5041–5051. https://doi.org/10.3892/etm.2019.8139
Bostan M, Petrică-Matei GG, Radu N, Hainarosie R, Stefanescu CD, Diaconu CC, Roman V (2020) The effect of resveratrol or curcumin on head and neck cancer cells sensitivity to the cytotoxic effects of cisplatin. Nutrients 12(9):2596. https://doi.org/10.3390/nu12092596
Nguyen NM, de Oliveira AF, Jin L, Zhang X, Macon M, Cruz MI, Benitez C, Wehrenberg B, Yin C, Wang X, Xuan J, de Assis S, Hilakivi-Clarke L (2017) Maternal intake of high n-6 polyunsaturated fatty acid diet during pregnancy causes transgenerational increase in mammary cancer risk in mice. Breast Cancer Res 19(1):1–13. https://doi.org/10.1186/s13058-017-0866-x
Hardman WE, Ion G, Akinsete JA, Witte TR (2011) Dietary walnut suppressed mammary gland tumorigenesis in the C(3)1 TAg mouse. Nutr Cancer 63(6):960–970. https://doi.org/10.1080/01635581.2011.589959
Govindarajah V, Leung YK, Ying J, Gear R, Bornschein RL, Medvedovic M, Shuk-Mei Ho SM (2016) In utero exposure of rats to high-fat diets perturbs geneexpression profiles and cancer susceptibility of prepubertal mammary glands. J Nutr Biochem 29:73–82. https://doi.org/10.1016/j.jnutbio.2015.11.003
De Assis S, Warri A, Cruz MI, Laja O, Tian Y, Zhang B, Wang Y, Huang THM, Hilakivi-Clarke L (2012) High-fat or ethinyl-oestradiol intake during pregnancy increases mammary cancer risk in several generations of offspring. Nat Commun 3:1053. https://doi.org/10.1038/ncomms2058
Zhang X, de Oliveira AF, Zhang H, Cruz I, Clarke R, Gaur P, Verma V, Hilakivi-Clarke L (2020) Maternal obesity increases offspring’s mammary cancer recurrence and impairs tumor immune response. Endocr Relat Cancer 27(9):469–482. https://doi.org/10.1530/ERC-20-0065
Lomas-Soria C, Reyes-Castro LA, Rodríguez-González GL, Ibanez CA, Bautista CJ, Cox LA, Nathanielsz PW, Zambrano E (2018) Maternal obesity has sex-dependent effects on insulin, glucose and lipid metabolism and the liver transcriptome in young adult rat offspring. J Physiol 596(19):4611–4628. https://doi.org/10.1113/JP276372
Kossoy G, Stark A, Tendler Y, Ben-Hur H, Beniashvili D, Madar Z, Zusman I (2002) Transplacental effects of high fat diets on functional activity of the spleen and lymph nodes, cell kinetics and apoptosis in mammary gland tumors in female rat offspring. Int J Mol Med 10(6):773–778. https://doi.org/10.3892/ijmm.10.6.773
Radzikowska U, Rinaldi AO, Çelebi Sözener Z, Karaguzel D, Wojcik M, Cypryk K, Akdis M, Akdis CA, Sokolowska M (2019) The influence of dietary fatty acids on immune responses. Nutrients 11(12):2990. https://doi.org/10.3390/nu11122990
Richard C, Lewis ED, Field CJ (2016) Evidence for the essentiality of arachidonic and docosahexaenoic acid in the postnatal maternal and infant diet for the development of the infant’s immune system early in life. Appl Physiol Nutr Metab 41(5):461–475. https://doi.org/10.1139/apnm-2015-0660
Chung H, Lee YS, Mayoral R, Oh DY, Siu JT, Webster NJ, Sears DD, Olefsky JM, Ellies LG (2015) Omega-3 fatty acids reduce obesity-induced tumor progression independent of GPR120 in a mouse model of postmenopausal breast cancer. Oncogene 34(27):3504–3513. https://doi.org/10.1038/onc.2014.283
da Paixão EMS, de Oliveira ACM, Pizato N, Muniz-Junqueira MI, Magalhães KG, Nakano EY, Ito MK (2017) The effects of EPA and DHA enriched fish oil on nutritional and immunological markers of treatment naïve breast cancer patients: a randomized double-blind controlled trial. Nutr J 16(1):71. https://doi.org/10.1186/s12937-017-0295-9
Hill EM, Esper RM, Sen A, Simon BR, Aslam MN, Jiang Y, Dame MK, McClintock SD, Colacino JA, Djuric Z, Wicha MS, Smith WL, Brenner DE (2019) Dietary polyunsaturated fatty acids modulate adipose secretome and is associated with changes in mammary epithelial stem cell self-renewal. J Nutr Biochem 71:45–53. https://doi.org/10.1016/j.jnutbio.2019.05.007
Zanoaga O, Jurj A, Raduly L, Cojocneanu-Petric R, Fuentes-Mattei E, Wu O, Braicu C, Gherman CD, Berindan-Neagoe I (2018) Implications of dietary ω-3 and ω-6 polyunsaturated fatty acids in breast cancer (review). Exp Ther Med 15(2):1167–1176. https://doi.org/10.3892/etm.2017.5515
Simopoulos AP (2016) An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity. Nutrients 8(3):1–17. https://doi.org/10.3390/nu8030128
Fabian CJ, Kimler BF, Hursting SD (2015) Omega-3 fatty acids for breast cancer prevention and survivorship. Breast Cancer Res 17(1):1–11. https://doi.org/10.1186/s13058-015-0571-6
Fahrmann JF, Ballester OF, Ballester G, Witte TR, Salazar AJ, Kordusky B, Cowen KG, Ion G, Primerano DA, Boskovic G, Denvir J, Hardman WE (2013) Inhibition of nuclear factor kappa B activation in early-stage chronic lymphocytic leukemia by omega-3 fatty acids. Cancer Invest 31(1):29–43. https://doi.org/10.3109/07357907.2012.743553
Maroulakou IG, Anver M, Garrett L, Green JE (1994) Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene. Proc Natl Acad Sci USA 91(23):11236–11240. https://doi.org/10.1073/pnas.91.23.11236
Ion G, Akinsete JA, Hardman WE (2010) Maternal consumption of canola oil suppressed mammary gland tumorigenesis in C3(1) TAg mice offspring. BMC Cancer 10:81. https://doi.org/10.1186/1471-2407-10-81
http://www.protocol-online.org/cgi-bin/prot/view_cache.cgi?ID=2149.
Tucker DK, Foley JF, Bouknight SA, Fenton SE (2017) Sectioning mammary gland whole mounts for lesion identification. J Vis Exp 125:1–8. https://doi.org/10.3791/55796
Patterson E, Wall R, Fitzgerald GF, Ross RP, Stanton C (2012) Health implications of high dietary omega-6 polyunsaturated fatty acids. J Nutr Metab 2012:1–16. https://doi.org/10.1155/2012/539426
Ghazali R, Mehta KJ, Bligh SWA, Tewfik I, Clemens D, Patel VB (2020) High omega arachidonic acid/docosahexaenoic acid ratio induces mitochondrial dysfunction and altered lipid metabolism in human hepatoma cells. World J Hepatol 12(3):84–98. https://doi.org/10.4254/wjh.v12.i3.84
Hoge A, Tabar V, Donneau AF, Dardenne N, Degée S, Timmermans M, Nisolle M, Guillaume M, Castronovo V (2019) Imbalance between omega-6 and omega-3 polyunsaturated fatty acids in early pregnancy is predictive of postpartum depression in a Belgian cohort. Nutrients 11(4):876. https://doi.org/10.3390/nu11040876
AL-Jawadi A, Moussa H, Ramalingam L, Dharmawardhane S, Gollahon L, Gunaratne P, Rahman RL, Moustaid-Moussa N (2018) Protective properties of n-3 fatty acids and implications in obesity-associated breast cancer. J Nutr Biochem 53:1–8. https://doi.org/10.1016/j.jnutbio.2017.09.018
Green JE, Shibata MA, Yoshidome K, Liu ML, Jorcyk C, Anver MR, Wigginton J, Wiltrout R, Shibata E, Kaczmarczyk S, Wang W, Liu ZY, Calvo A, Couldrey C (2000) The C3(1)/SV40 T-antigen transgenic mouse model of mammary cancer: ductal epithelial cell targeting with multistage progression to carcinoma. Oncogene 19(8):1020–1027. https://doi.org/10.1038/sj.onc.1203280
Turbitt WJ, Black AJ, Collins SD, Meng H, Xu H, Washington S, Aliaga C, El-Bayoumy K, Manni A, Rogers CJ (2015) Fish oil enhances T cell function and tumor infiltration and is correlated with a cancer prevention effect in HER-2/neu but not PyMT transgenic mice. Nutr Cancer 67(6):965–975. https://doi.org/10.1080/01635581.2015.1060351
Keleher MR, Zaidi R, Shah S, Oakley MS, Pavlatos C, El Idrissi S, Xing X, Li D, Wang T, Cheverud JM (2018) Maternal high-fat diet associated with altered gene expression, DNA methylation, and obesity risk in mouse offspring. PLoS ONE 13(2):1–28. https://doi.org/10.1371/journal.pone.0192606
Li J, Li K, Gao J, Guo X, Lu M, Li Z, Li D (2018) Maternal exposure to an n-3 polyunsaturated fatty acid diet decreases mammary cancer risk of female offspring in adulthood. Food Funct 9(11):5768–5777. https://doi.org/10.1039/C8FO01006D
Montales MTE, Melnyk SB, Simmen FA, Simmen RCM (2014) Maternal metabolic perturbations elicited by high-fat diet promote Wnt-1-induced mammary tumor risk in adult female offspring via long-term effects on mammary and systemic phenotypes. Carcinogenesis 35(9):2102–2112. https://doi.org/10.1093/carcin/bgu106
Ion G, Fazio K, Akinsete JA, Hardman WE (2011) Effects of canola and corn oil mimetic on Jurkat cells. Lipids Health Dis 10:1–9. https://doi.org/10.1186/1476-511X-10-90
Calder PC (2015) Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance. Biochim Biophys Acta-Mol Cell Biol Lipids 1851(4):469–484. https://doi.org/10.1016/j.bbalip.2014.08.010
Allam-Ndoul B, Guénard F, Barbier O, Vohl MC (2016) Effect of n-3 fatty acids on the expression of inflammatory genes in THP-1 macrophages. Lipids Health Dis 15(69):1–8. https://doi.org/10.1186/s12944-016-0241-4
Lee HS, Barraza-Villarreal A, Hernandez-Vargas H, Sly PD, Biessy C, Ramakrishnan U, Romieu I, Herceg Z (2013) Modulation of DNA methylation states and infant immune system by dietary supplementation with v-3 PUFA during pregnancy in an intervention study. Am J Clin Nutr 98(2):480–487. https://doi.org/10.3945/ajcn.112.052241