The role of docosahexaenoic acid (DHA) in the control of obesity and metabolic derangements in breast cancer

International Journal of Molecular Sciences

Volumn 17, Issue 4, 2016, Pages

  Molfino, Alessio ^a   Amabile, Maria Ida ^a   Monti, Massimo ^a   Arcieri, Stefano ^a   Fanelli, Filippo Rossi ^a   Muscaritoli, Maurizio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Breast cancer; Diet; Docosahexaenoic acid (DHA); Food component; Inflammation; Obesity

Indexed keywords

ADIPONECTIN; ANDROGEN; AROMATASE; C REACTIVE PROTEIN; DOCOSAHEXAENOIC ACID; EPITHELIAL CELL ADHESION MOLECULE; ESTROGEN; ICOSAPENTAENOIC ACID; INTERLEUKIN 2; INTERLEUKIN 6; LEPTIN; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROTEIN KINASE B; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; BODY WEIGHT; BREAST CANCER; CANCER GROWTH; CANCER MORTALITY; CANCER RECURRENCE; CELL GROWTH; CELL PROLIFERATION; CLINICAL TRIAL (TOPIC); COMORBIDITY; HUMAN; INFLAMMATION; INSULIN RESISTANCE; LIPID PEROXIDATION; META ANALYSIS (TOPIC); METABOLIC DISORDER; NONHUMAN; OBESITY; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SURVIVAL RATE; ANIMAL; BREAST NEOPLASMS; COMPLICATION; DIET; DIET THERAPY; DIETARY SUPPLEMENT; FEMALE; IMMUNOLOGY; METABOLISM; TUMOR RECURRENCE;

ANIMALS; BREAST NEOPLASMS; DIET; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; FATTY ACIDS, OMEGA-3; FEMALE; HUMANS; INSULIN RESISTANCE; NEOPLASM RECURRENCE, LOCAL; OBESITY;

EID: 84962626110     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17040505     Document Type: Review

References (64)

1. Ghose, A.; Kundu, R.; Toumeh, A.; Hornbeck, C.; Mohamed, I. A review of obesity, insulin resistance and the role of exercise in breast cancer patients. Nutr. Cancer 2015, 67, 197-202. [CrossRef] [Pubmed]
2. Makarem, N.; Chandran, U.; Bandera, E.V.; Parekh, N. Dietary fat in breast cancer survival. Annu. Rev. Nutr. 2013, 33, 319-348. [CrossRef] [Pubmed]
3. Benedetto, C.; Salvagno, F.; Canuto, E.M.; Gennarelli, G. Obesity and female malignancies. Best Pract. Res. Clin. Obst. Gyn. 2015, 29, 528-540. [CrossRef] [Pubmed]
4. Monk, J.M.; Turk, H.F.; Liddle, D.M.; de Boer, A.A.; Power, K.A.; Ma, D.W.; Robinson, L.E. n-3 polyunsaturated fatty acids and mechanisms to mitigate inflammatory paracrine signaling in obesityassociated breast cancer. Nutrients 2014, 6, 4760-4793. [CrossRef]
5. Ferguson, R.D.; Gallagher, E.J.; Scheinman, E.J.; Damouni, R.; LeRoith, D. The epidemiology and molecular mechanisms linking obesity, diabetes, and cancer. Vitam. Horm. 2013, 93, 51-98. [CrossRef]
6. Rose, D.P.; Vona-Davis, L. Biochemical and molecular mechanisms for the association between obesity, chronic inflammation, and breast cancer. BioFactors 2014, 40, 1-12. [CrossRef] [Pubmed]
7. Macaulay, V.M.; Nicholls, J.E.; Gledhill, J.; Rowlands, M.G.; Dowsett, M.; Ashworth, A. Biological effects of stable overexpression of aromatase in human hormone-dependent breast cancer cells. Br. J. Cancer 1994, 69, 77-83. [CrossRef] [Pubmed]
8. Simpson, E.R.; Mahendroo, M.S.; Nichols, J.E.; Bulun, S.E. Aromatase gene expression in adipose tissue: Relationship to breast cancer. Int. J. Fertil. Menopausal Stud. 1994, 39, S75-S83.
9. Daling, J.R.; Malone, K.E.; Doody, D.R.; Johnson, L.G.; Gralow, J.R.; Porter, P.L. Relation of body mass index to tumor markers and survival among young women with invasive ductal breast carcinoma. Cancer 2001, 92, 720-729. [CrossRef]
10. Fagherazzi, G.; Chabbert-Buffet, N.; Fabre, A.; Guillas, G.; Boutron-Ruault, M.C.; Mesrine, S.; Clavel-Chapelon, F. Hip circumference is associated with the risk of premenopausal ER-/PR-breast cancer. Int. J. Obes. 2012, 36, 431-439. [CrossRef] [Pubmed]
11. Laviano, A.; Rianda, S.; Molfino, A.; Rossi Fanelli, F. Omega-3 fatty acid in cancer. Curr. Opin. Clin. Nutr. Metab. Care 2013, 16, 156-161. [CrossRef] [Pubmed]
12. Bougnoux, P.; Hajjaji, N.; Maheo, K.; Couet, C.; Chevalier, S. Fatty acids and breast cancer: Sensitization to treatments and prevention of metastatic re-growth. Prog. Lipid Res. 2010, 49, 76-86. [CrossRef] [Pubmed]
13. Bougnoux, P.; Hajjaji, N.; Ferrasson, M.N.; Giraudeau, B.; Couet, C.; Le, F.O. Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: A phase II trial. Br. J. Cancer 2009, 101, 1978-1985. [CrossRef] [Pubmed]
14. Patterson, R.E.; Flatt, S.W.; Newman, V.A.; Natarajan, L.; Rock, C.L.; Thomson, C.A.; Caan, B.J.; Parker, B.A.; Pierce, J.P. Marine fatty acid intake is associated with breast cancer prognosis. J. Nutr. 2011, 141, 201-206. [CrossRef] [Pubmed]
15. Makhoul, Z.; Kristal, A.R.; Gulati, R.; Luick, B.; Bersamin, A.; Boyer, B.; Mohatt, G.V. Associations of very high intakes of eicosapentaenoic and docosahexaenoic acids with biomarkers of chronic disease risk among Yup’ik Eskimos. Am. J. Clin. Nutr. 2011, 91, 777-785. [CrossRef] [Pubmed]
16. Alfano, C.M.; Imayama, I.; Neuhouser, M.L.; Kiecolt-Glaser, J.K.; Smith, A.W.; Meeske, K.; McTiernan, A.; Bernstein, L.; Baumgartner, K.B.; Ulrich, C.M.; et al. Fatigue, inflammation, and ω-3 and ω-6 fatty acid intake among breast cancer survivors. J. Clin. Oncol. 2012, 30, 1280-1287. [CrossRef] [Pubmed]
17. Fay, M.; Freedman, L.; Clifford, C.; Midthune, D. Effect of different types and amounts of fat on the development of mammary tumors in rodents: A review. Cancer Res. 1997, 57, 3979-3988. [CrossRef]
18. Carmichael, A.R. Obesity and prognosis of breast cancer. Obes. Rev. 2006, 7, 333-340. [CrossRef] [Pubmed]
19. DeSantis, C.; Siegel, R.; Bandi, P.; Jemal, A. Breast cancer statistics, 2011. CA Cancer J. Clin. 2011, 61, 409-418. [CrossRef] [Pubmed]
20. Chlebowski, R.T.; Aiello, E.; McTiernan, A. Weight loss in breast cancer patient management. J. Clin. Oncol. 2002, 20, 1128-1143. [CrossRef] [Pubmed]
21. Chlebowski, R.T. Nutrition and physical activity influence on breast cancer incidence and outcome. Breast 2013, 22, 30-37. [CrossRef] [Pubmed]
22. Rooney, M.; Wald, A. Interventions for the management of weight and body composition changes in women with breast cancer. Clin. J. Oncol. Nurs. 2007, 11, 41-52. [CrossRef] [Pubmed]
23. Chan, D.S.; Norat, T. Obesity and breast cancer: not only a risk factor of the disease. Curr. Treat. Opt. Oncol. 2015, 16. [CrossRef] [Pubmed]
24. Heideman, W.H.; Russell, N.S.; Gundy, C.; Rookus, M.A.; Voskuil, D.W. The frequency, magnitude and timing of post-diagnosis body weight gain in Dutch breast cancer survivors. Eur. J. Cancer 2009, 45, 119-126. [CrossRef] [Pubmed]
25. Ibrahim, E.M.; Al-Homaidh, A. Physical activity and survival after breast cancer diagnosis: Meta-analysis of published studies. Med. Oncol. 2011, 28, 753-765. [CrossRef] [Pubmed]
26. Patterson, R.E.; Cadmus, L.A.; Emond, J.A.; Pierce, J.P. Physical activity, diet, adiposity and female breast cancer prognosis: A review of the epidemiologic literature. Maturitas 2010, 66, 5-15. [CrossRef] [Pubmed]
27. Bradshaw, P.T.; Ibrahim, J.G.; Stevens, J.; Cleveland, R.; Abrahamson, P.E.; Satia, J.A.; Teitelbaum, S.L.; Neugut, A.I.; Gammon, M.D. Postdiagnosis change in bodyweight and survival after breast cancer diagnosis. Epidemiology 2012, 23, 320-327. [CrossRef] [Pubmed]
28. Howe, L.R.; Subbaramaiah, K.; Hudis, C.A.; Dannenberg, A.J. Molecular pathways: Adipose inflammation as a mediator of obesity-associated cancer. Clin. Cancer Res. 2013, 19, 6074-6083. [CrossRef] [Pubmed]
29. Baumgarten, S.C.; Frasor, J. Inflammation: An instigator of more aggressive estrogen receptor (ER) positive breast cancers. Mol. Endocrinol. 2012, 26, 360-371. [CrossRef] [Pubmed]
30. Grivennikov, S.I.; Karin, M. Inflammatory cytokines in cancer: Tumour necrosis factor and interleukin 6 take the stage. Ann. Rheum. Dis. 2011, 70, i104-i108. [CrossRef] [Pubmed]
31. Horng, T.; Hotamisligil, G.S. Linking the inflammasome to obesity-related disease. Nat. Med. 2011, 17, 164-165. [CrossRef] [Pubmed]
32. Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 2006, 444, 860-867. [CrossRef] [Pubmed]
33. Pasanisi, P.; Berrino, F.; de Petris, M.; Venturelli, E.; Mastroianni, A.; Panico, S. Metabolic syndrome as a prognostic factor for breast cancer recurrences. Int. J. Cancer 2006, 119, 236-238. [CrossRef] [Pubmed]
34. Widjaja, A.; Stratton, I.M.; Horn, R.; Holman, R.R.; Turner, R.; Brabant, G. UKPDS 20: Plasma leptin, obesity, and plasma insulin in type 2 diabetic subjects. J. Clin. Endocrinol. Metab. 1997, 82, 654-657. [CrossRef] [Pubmed]
35. Jarde, T.; Caldefie-Chezet, F.; Damez, M.; Mishellany, F.; Penault-Llorca, F.; Guillot, J.; Vasson, M.P. Leptin and leptin receptor involvement in cancer development: A study on human primary breast carcinoma. Oncol. Rep. 2008, 19, 905-911. [CrossRef] [Pubmed]
36. Simopoulos, A.P. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed. Pharmacother. 2002, 56, 365-379. [CrossRef]
37. Kalupahana, N.S.; Claycombe, K.; Newman, S.J.; Stewart, T.; Siriwardhana, N.; Matthan, N.; Lichtenstein, A.H.; Moustaid-Moussa, N. Eicosapentaenoic acid prevents and reverses insulin resistance in high-fat diet-induced obese mice via modulation of adipose tissue inflammation. J. Nutr. 2010, 140, 1915-1922. [CrossRef] [Pubmed]
38. Laviano, A.; Seelaender, M.; Sanchez-Lara, K.; Gioulbasanis, I.; Molfino, A.; Rossi Fanelli, F. Beyond anorexia-cachexia. Nutrition and modulation of cancer patients’ metabolism: Supplementary, complementary or alternative anti-neoplastic therapy? Eur. J. Pharmacol. 2011, 668, s87-s90. [CrossRef] [Pubmed]
39. Park, J.; Morley, T.S.; Kim, M.; Clegg, D.J.; Scherer, P.E. Obesity and cancer—Mechanisms underlying tumour progression and recurrence. Nat. Rev. Endocrinol. 2014, 10, 455-465. [CrossRef] [Pubmed]
40. Bouwens, M.; van de Rest, O.; Dellschaft, N.; Bromhaar, M.G.; de Groot, L.C.; Geleijnse, J.M.; Muller, M.; Afman, L.A. Fish-oil supplementation induces antiinflammatory gene expression profiles in human blood mononuclear cells. Am. J. Clin. Nutr. 2009, 90, 415-424. [CrossRef] [Pubmed]
41. Puglisi, M.J.; Hasty, A.H.; Saraswathi, V. The role of adipose tissue in mediating the beneficial effects of dietary fish oil. J. Nutr. Biochem. 2011, 22, 101-108. [CrossRef] [Pubmed]
42. Flock, M.R.; Skulas-Ray, A.C.; Harris, W.S.; Gaugler, T.L.; Fleming, J.A.; Kris-Etherton, P.M. Effects of supplemental long-chain omega-3 fatty acids and erythrocyte membrane fatty acid content on circulating inflammatory markers in a randomized controlled trial of healthy adults. Prostaglandins Leukot. Essent. Fatty Acids 2014, 91, 161-168. [CrossRef] [Pubmed]
43. Wall, R.; Ross, R.P.; Fitzgerald, G.F.; Stanton, C. Fatty acids from fish: The anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr. Rev. 2010, 68, 280-289. [CrossRef] [Pubmed]
44. Simopoulos, A.P. An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity. Nutrients 2016, 2. [CrossRef] [Pubmed]
45. Hawkins, R.A.; Sangster, K.; Arends, M.J. Apoptotic death of pancreatic cancer cells induced by polyunsaturated fatty acids varies with double bond number and involves an oxidative mechanism. J. Pathol. 1998, 185, 61-70. [CrossRef]
46. Grammatikos, S.I.; Subbaiah, P.V.; Victor, T.A.; Miller, W.M. n-3 and n-6 fatty acid processing and growth effects in neoplastic and non-cancerous human mammary epithelial cell lines. Br. J. Cancer 1994, 70, 219-227. [CrossRef] [Pubmed]
47. Gonzalez, M.J.; Schemmel, R.A.; Dugan, L., Jr.; Gray, J.I.; Welsch, C.W. Dietary fish oil inhibits human breast carcinoma growth: A function of increased lipid peroxidation. Lipids 1993, 28, 827-832. [CrossRef] [Pubmed]
48. Roy, J.; le Guennec, J.Y.; Galano, J.M.; Thireau, J.; Bultel-Poncé, V.; Demion, M.; Oger, C.; Lee, J.C.; Durand, T. Non-enzymatic cyclic oxygenated metabolites of omega-3 polyunsaturated fatty acid: Bioactive drugs? Biochimie 2016, 120, 56-61. [CrossRef] [Pubmed]
49. Roy, J.; Oliveira, L.T.; Oger, C.; Galano, J.M.; Bultel-Poncé, V.; Richard, S.; Guimaraes, A.G.; Vilela, J.M.; Andrade, M.S.; Durand, T. et al. Polymeric nanocapsules prevent oxidation of core-loaded molecules: Evidence based on the effects of docosahexaenoic acid and neuroprostane on breast cancer cells proliferation. J. Exp. Clin. Cancer Res. 2015, 34. [CrossRef] [Pubmed]
50. Gago-Dominguez, M.; Yuan, J.M.; Sun, C.L.; Lee, H.P.; Yu, M.C. Opposing effects of dietary n-3 and n-6 fatty acids on mammary carcinogenesis: The Singapore Chinese Health Study. Br. J. Cancer 2003, 89, 1686-1692. [CrossRef] [Pubmed]
51. Hirose, K.; Takezaki, T.; Hamajima, N.; Miura, S.; Tajima, K. Dietary factors protective against breast cancer in Japanese premenopausal and postmenopausal women. Int. J. Cancer 2003, 107, 276-282. [CrossRef] [Pubmed]
52. Wakai, K.; Tamakoshi, K.; Date, C.; Fukui, M.; Suzuki, S.; Lin, Y.; Niwa, Y.; Nishio, K.; Yatsuya, H.; Kondo, T.; et al. Dietary intakes of fat and fatty acids and risk of breast cancer: A prospective study in Japan. Cancer Sci. 2005, 96, 590-599. [CrossRef] [Pubmed]
53. Chajes, V.; Torres-Mejía, G.; Biessy, C.; Ortega-Olvera, C.; Angeles-Llerenas, A.; Ferrari, P.; Lazcano-Ponce, E.; Romieu, I. ω-3 and ω-6 polyunsaturated fatty acid intakes and the risk of breast cancer in Mexican women: Impact of obesity status. Cancer Epidemiol. Biomark. Prev. 2011, 21, 319-326. [CrossRef] [Pubmed]
54. MacLean, C.H.; Newberry, S.J.; Mojica, W.A.; Khanna, P.; Issa, A.M.; Suttorp, M.J.; Lim, Y.W.; Traina, S.B.; Hilton, L.; Garland, R. et al. Effects of omega-3 fatty acids on cancer risk: A systematic review. JAMA 2006, 295, 403-415. [CrossRef] [Pubmed]
55. Zheng, J.S.; Hu, X.J.; Zhao, Y.M.; Yang, J.; Li, D. Intake of fish and marine n-3 polyunsaturated fatty acids and risk of breast cancer: Meta-analysis of data from 21 independent prospective cohort studies. BMJ 2013, 346. [CrossRef] [Pubmed]
56. Cheraghi, Z.; Poorolajal, J.; Hashem, T.; Esmailnasab, N.; Doosti Irani, A. Effect of body mass index on breast cancer during premenopausal and postmenopausal periods: A meta-analysis. PLoS ONE 2012, 7, e51446. [CrossRef] [Pubmed]
57. Thiebaut, A.C.; Chajes, V.; Gerber, M.; Boutron-Ruault, M.C.; Joulin, V.; Lenoir, G.; Berrino, F.; Riboli, E.; Benichou, J.; Clavel-Chapelon, F. Dietary intakes of omega-6 and omega-3 polyunsaturated fatty acids and the risk of breast cancer. Int. J. Cancer 2009, 124, 924-931. [CrossRef] [Pubmed]
58. Pierce, J.P.; Natarajan, L.; Caan, B.J.; Parker, B.A.; Greenberg, E.R.; Flatt, S.W.; Rock, C.L.; Kealey, S.; Al-Delaimy, W.K.; Bardwell, W.A. et al. Influence of a diet very high in vegetables, fruit, and fiber and low in fat on prognosis following treatment for breast cancer: The Women’s Healthy Eating and Living (WHEL) randomized trial. JAMA 2007, 298, 289-298. [CrossRef] [Pubmed]
59. Menendez, J.A.; Lupu, R.; Colomer, R. Exogenous supplementation with omega-3 polyunsaturated fatty acid docosahexaenoic acid (DHA; 22:6n-3) synergistically enhances taxane cytotoxicity and downregulates Her-2/neu (c-erbB-2) oncogene expression in human breast cancer cells. Eur. J. Cancer Prev. 2005, 14, 263-270. [CrossRef] [Pubmed]
60. MacLennan, M.B.; Clarke, S.E.; Perez, K.; Wood, G.A.; Muller, W.J.; Kang, J.X.; Ma, D.W. Mammary tumor development is directly inhibited by lifelong n-3 polyunsatured fatty acids. J. Nutr. Biochem. 2013, 24, 388-395. [CrossRef] [Pubmed]
61. Laviano, A.; Molfino, A.; Rossi Fanelli, F. Cancer treatment toxicity: Can nutrition help? Nat. Rev. Clin. Oncol. 2012, 9. [CrossRef] [Pubmed]
62. McCullough, M.L.; Giovannucci, E.L. Diet and cancer prevention. Oncogene 2004, 23, 6349-6364. [CrossRef] [Pubmed]
63. Flock, M.R.; Rogers, C.J.; Prabhu, K.S.; Kris-Etherton, P.M. Immunometabolic role of long-chain omega-3 fatty acids in obesity-induced inflammation. Diabetes Metab. Res. Rev. 2013, 29, 431-445. [CrossRef] [Pubmed]
64. Fabian, C.J.; Kimler, B.F.; Hursting, S.D. Omega-3 fatty acids for breast cancer prevention and survivorship. Breast Cancer Res. 2015, 17. [CrossRef] [Pubmed]