Dietary docosahexaenoic acid proposed to sensitize breast tumors to locally delivered drug

Clinical Lipidology

Volumn 5, Issue 2, 2010, Pages 233-243

  Chevalier, Stephan ^a,b   Goupille, Caroline ^a,c   Mahéo, Karine ^a,b   Domingo, Isabelle ^a   Dussiau, Charles ^a,b   Renoux, Brigitte ^d   Bougnoux, Philippe ^a,c   Papot, Sébastien ^d  

^a CHRU de Tours   (France)

^b UNIVERSITÉ DE TOURS   (France)

^c CHU BRETONNEAU   (France)

^d UNIVERSITÉ DE POITIERS   (France)

Author keywords

Breast cancer; Chemosensitization; Docosahexaenoic acid; Glucuronide prodrug; Nutrition; Oxidative stress; PUFA

Indexed keywords

ANTHRACYCLINE DERIVATIVE; ANTINEOPLASTIC AGENT; CYTOTOXIC AGENT; DOCETAXEL; DOCOSAHEXAENOIC ACID; DOXORUBICIN; EPIRUBICIN; FISH OIL; GEMTUZUMAB OZOGAMICIN; GLUCURONIDE; ICOSAPENTAENOIC ACID; LIPOSOME; MITOXANTRONE; N (4 BETA GLUCURONYL 3 NITROBENZYLOXYCARBONYL)DOXORUBICIN; PACLITAXEL; POLYMER; POLYUNSATURATED FATTY ACID; PRODRUG; TAXANE DERIVATIVE; TRASTUZUMAB;

ANTIOXIDANT ACTIVITY; BREAST CANCER; BREAST SURGERY; BREAST TUMOR; CANCER CELL CULTURE; CANCER RADIOTHERAPY; CANCER THERAPY; CARDIOTOXICITY; CELL MEMBRANE; CHEMOSENSITIZATION; CLINICAL TRIAL; DIET SUPPLEMENTATION; DRUG DELIVERY SYSTEM; DRUG DOSE INCREASE; DRUG MECHANISM; DRUG POTENTIATION; DRUG SELECTIVITY; DRUG SENSITIZATION; DRUG STRUCTURE; DRUG TISSUE LEVEL; DRUG UPTAKE; HEMATOLOGIC MALIGNANCY; HUMAN; IN VIVO STUDY; MEMBRANE STRUCTURE; METASTASIS; NONHUMAN; OUTCOMES RESEARCH; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; STRUCTURE ACTIVITY RELATION; TREATMENT OUTCOME; TUMOR CELL; UNSPECIFIED SIDE EFFECT;

EID: 77950275572     PISSN: 17460875     EISSN: None     Source Type: Journal    
DOI: 10.2217/clp.10.12     Document Type: Review

References (59)

1. Parkin DM, Bray FI, Devesa SS: Cancer burden in the year 2000. The global picture. Eur. J. Cancer. 37(Suppl. 8), S4-S66 (2001).
2. Lippman SM, Hong WK: Cancer prevention by delay. Commentary: O'Shaughnessy JA et al.: Treatment and prevention of intraepithelial neoplasia: an important target for accelerated new agent development. Clin. Cancer Res., 8, 314-346 (2002).
3. Clin. Cancer Res. 8, 305-313 (2002).
4. Cardoso F, Bedard PL, Winer EP et al.: International guidelines for management of metastatic breast cancer: combination vs sequential single-agent chemotherapy. J. Natl Cancer Inst. 101, 1174-1181 (2009).
5. Kratz F, Muller IA, Ryppa C, Warnecke A: Prodrug strategies in anticancer chemotherapy. Chem. Med. Chem. 3, 20-53 (2008).
6. Rock CL, Demark-Wahnefried W: Nutrition and survival after the diagnosis of breast cancer: a review of the evidence. J. Clin. Oncol. 20, 3302-3316 (2002).
7. Chlebowski RT, Blackburn GL, Thomson CA et al.: Dietary fat reduction and breast cancer outcome: interim efficacy results from the Women's Intervention Nutrition Study. J. Natl Cancer Inst. 98, 1767-1776 (2006).
8. Biondo PD, Brindley DN, Sawyer MB, Field CJ: The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy. J. Nutr. Biochem. 19, 787-796 (2008).
9. Bougnoux P, Hajjaji N, Ferrasson MN et al.: Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: a Phase II trial. Br. J. Cancer 101, 1978-1985 (2009).
10. 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. 49, 76-86 (2010).
11. Colas S, Paon L, Denis F et al.: Enhanced radiosensitivity of rat autochthonous mammary tumors by dietary docosahexaenoic acid. Int. J. Cancer 109, 449-454 (2004).
12. Colas S, Germain E, Arab K et al.: a-tocopherol suppresses mammary tumor sensitivity to anthracyclines in fish oil-fed rats. Nutr. Cancer 51, 178-183 (2005).
13. Germain E, Chajes V, Cognault S, Lhuillery C, Bougnoux P: Enhancement of doxorubicin cytotoxicity by polyunsaturated fatty acids in the human breast tumor cell line MDA-MB-231: relationship to lipid peroxidation. Int. J. Cancer 75, 578-583 (1998).
14. Bougnoux P: n-3 polyunsaturated fatty acids and cancer. Curr. Opin Clin. Nutr. Metab. Care 2, 121-126 (1999).
15. Colas S, Maheo K, Denis F et al.: Sensitization by dietary docosahexaenoic acid of rat mammary carcinoma to anthracycline: a role for tumor vascularization. Clin. Cancer Res. 12, 5879-5886 (2006).
16. Hardman WE, Avula CP, Fernandes G, Cameron IL: Three percent dietary fish oil concentrate increased efficacy of doxorubicin against MDA-MB 231 breast cancer xenografts. Clin. Cancer Res. 7, 2041-2049 (2001).
17. Shao Y, Pardini L, Pardini RS: Intervention of transplantable human mammary carcinoma MX-1 chemotherapy with dietary menhaden oil in athymic mice: increased therapeutic effects and decreased toxicity of cyclophosphamide. Nutr. Cancer 28, 63-73 (1997).
18. Vargo-Gogola T, Rosen JM: Modelling breast cancer: one size does not fit all. Nat. Rev. Cancer 7, 659-672 (2007).
19. Benchekroun MN, Robert J: Measurement of doxorubicin-induced lipid peroxidation under the conditions that determine cytotoxicity in cultured tumor cells. Anal. Biochem. 201, 326-330 (1992).
20. McGrogan BT, Gilmartin B, Carney DN, McCann A: Taxanes, microtubules and chemoresistant breast cancer. Biochim. Biophys. Acta 1785, 96-132 (2008).
21. Joyce JA, Pollard JW: Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252 (2009).
22. Bougnoux P, Koscielny S, Chajes V et al.: a-Linolenic acid content of adipose breast tissue: a host determinant of the risk of early metastasis in breast cancer. Br. J. Cancer 70, 330-334 (1994).
23. Kohlmeier L, Kohlmeier M: Adipose tissue as a medium for epidemiologic exposure assessment. Environ. Health Perspect. 103(Suppl. 3), 99-106 (1995).
24. Bougnoux P, Germain E, Chajes V et al.: Cytotoxic drugs efficacy correlates with adipose tissue docosahexaenoic acid level in locally advanced breast carcinoma. Br. J. Cancer 79, 1765-1769 (1999).
25. Bougnoux P, Hajjaji N, Baucher MA et al.: Docosahexaenoic acid (DHA) intake during first line chemotherapy improves survival in metastatic breast cancer. Proc. Amer. Ass. Cancer Res. 47, 5276 (2006).
26. Senkal M, Haaker R, Linseisen J et al.: Preoperative oral supplementation with long-chain omega-3 fatty acids beneficially alters phospholipid fatty acid patterns in liver, gut mucosa, and tumor tissue. JPEN J. Parenter. Enteral. Nutr. 29, 236-240 (2005).
27. Shao Y, Pardini L, Pardini RS: Dietary menhaden oil enhances mitomycin C antitumor activity toward human mammary carcinoma MX-1. Lipids 30, 1035-1045 (1995).
28. Borgeson CE, Pardini L, Pardini RS, Reitz RC: Effects of dietary fish oil on human mammary carcinoma and on lipid-metabolizing enzymes. Lipids 24, 290-295 (1989).
29. Germain E, Bonnet P, Aubourg L et al.: Anthracycline-induced cardiac toxicity is not increased by dietary omega-3 fatty acids. Pharmacol. Res. 47, 111-117 (2003).
30. Hardman WE, Moyer MP, Cameron IL: Efficacy of treatment of colon, lung and breast human carcinoma xenografts with: doxorubicin, cisplatin, irinotecan or topotecan. Anticancer Res. 19, 2269-2274 (1999).
31. Kato T, Hancock RL, Mohammadpour H et al.: Influence of omega-3 fatty acids on the growth of human colon carcinoma in nude mice. Cancer Lett. 187, 169-177 (2002).
32. Xue H, Sawyer MB, Field CJ, Dieleman LA, Baracos VE: Nutritional modulation of antitumor efficacy and diarrhea toxicity related to irinotecan chemotherapy in rats bearing the ward colon tumor. Clin. Cancer Res. 13, 7146-7154 (2007).
33. Schley PD, Brindley DN, Field CJ: (n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells. J. Nutr. 137, 548-553 (2007).
34. Maheo K, Vibet S, Steghens JP et al.: Differential sensitization of cancer cells to doxorubicin by DHA: a role for lipoperoxidation. Free Radic. Biol. Med. 39, 742-751 (2005).
35. Vibet S, Maheo K, Gore J et al.: Differential subcellular distribution of mitoxantrone in relation to chemosensitization in two human breast cancer cell lines. Drug Metab. Dispos. 35, 822-828 (2007).
36. Abulrob AN, Mason M, Bryce R, Gumbleton M: The effect of fatty acids and analogues upon intracellular levels of doxorubicin in cells displaying P-glycoprotein mediated multidrug resistance. J. Drug Target. 8, 247-256 (2000).
37. Girotti AW: Lipid hydroperoxide generation, turnover, and effector action in biological systems. J. Lipid Res. 39, 1529-1542 (1998).
38. Noto V, Taper HS, Jiang YH et al.: Effects of sodium ascorbate (vitamin C) and 2-methyl- 1,4-naphthoquinone (vitamin K3) treatment on human tumor cell growth in vitro. I. Synergism of combined vitamin C and K3 action. Cancer 63, 901-906 (1989).
39. Menendez JA, 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. 14, 263-270 (2005).
40. Oberley TD: Oxidative damage and cancer. Am. J. Pathol. 160, 403-408 (2002).
41. Oberley TD, Oberley LW: Antioxidant enzyme levels in cancer. Histol. Histopathol. 12, 525-535 (1997).
42. Murawaki Y, Tsuchiya H, Kanbe T et al.: Aberrant expression of selenoproteins in the progression of colorectal cancer. Cancer Lett. 259, 218-230 (2008).
43. Sun W, Kalen AL, Smith BJ, Cullen JJ, Oberley LW: Enhancing the antitumor activity of adriamycin and ionizing radiation. Cancer Res. 69, 4294-4300 (2009).
44. Vibet S, Goupille C, Bougnoux P et al.: Sensitization by docosahexaenoic acid (DHA) of breast cancer cells to anthracyclines through loss of glutathione peroxidase (GPx1) response. Free Radic. Biol. Med. 44, 1483-1491 (2008).
45. Ding WQ, Vaught JL, Yamauchi H, Lind SE: Differential sensitivity of cancer cells to docosahexaenoic acid-induced cytotoxicity: the potential importance of down-regulation of superoxide dismutase 1 expression. Mol. Cancer Ther. 3, 1109-1117 (2004).
46. Ding WQ, Lind SE: Phospholipid hydroperoxide glutathione peroxidase plays a role in protecting cancer cells from docosahexaenoic acid-induced cytotoxicity. Mol. Cancer Ther. 6, 1467-1474 (2007).
47. Stasi R: Gemtuzumab ozogamicin: an anti-CD33 immunoconjugate for the treatment of acute myeloid leukaemia. Expert Opin Biol. Ther. 8, 527-540 (2008).
48. Bosslet K, Czech J, Hoffmann D: A novel one-step tumor-selective prodrug activation system. Tumor Targeting 1, 45-50 (1995).
49. Niculescu-Duvaz I, Springer CJ: Introduction to the background, principles, and state of the art in suicide gene therapy. Mol. Biotechnol. 30, 71-88 (2005).
50. Naylor MA, Thomson P: Recent advances in bioreductive drug targeting. Mini. Rev. Med. Chem. 1, 17-29 (2001).
51. de Graaf M, Boven E, Scheeren HW, Haisma HJ, Pinedo HM: b-glucuronidase-mediated drug release. Curr. Pharm. Des. 8, 1391-1403 (2002).
52. Florent JC, Dong X, Gaudel G et al.: Prodrugs of anthracyclines for use in antibody-directed enzyme prodrug therapy. J. Med. Chem. 41, 3572-3581 (1998).
53. Papot S, Tranoy I, Tillequin F, Florent JC, Gesson JP: Design of selectively activated anticancer prodrugs: elimination and cyclization strategies. Curr. Med. Chem. Anticancer Agents 2, 155-185 (2002).
54. Tranoy-Opalinski I, Fernandes A, Thomas M, Gesson JP, Papot S: Design of self-immolative linkers for tumour-activated prodrug therapy. Anticancer Agents Med. Chem. 8, 618-637 (2008).
55. Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods. 65, 55-63 (1983).
56. Bosslet K, Straub R, Blumrich M et al.: Elucidation of the mechanism enabling tumor selective prodrug monotherapy. Cancer Res. 58, 1195-1201 (1998).
57. Beem EP, Hillebrand MJ, Benckhuijsen C, Overdijk B: Origin of the increased activity of beta-glucuronidase in the soluble fraction of rat mammary tumors during ovariectomy-induced regression. Cancer Res. 47, 3980-3987 (1987).
58. Murdter TE, Friedel G, Backman JT et al.: Dose optimization of a doxorubicin prodrug (HMR 1826) in isolated perfused human lungs: low tumor pH promotes prodrug activation by b-glucuronidase. J. Pharmacol. Exp. Ther. 301, 223-228 (2002).
59. Brot FE, Bell CE Jr, Sly WS: Purification and properties of b-glucuronidase from human placenta. Biochemistry 17, 385-391 (1978).