Omega-3 fatty acids induce apoptosis in human breast cancer cells and mouse mammary tissue through syndecan-1 inhibition of the MEK-Erk pathway

Carcinogenesis

Volumn 32, Issue 10, 2011, Pages 1518-1524

  Sun, Haiguo ^a   Hu, Yunping ^a   Gu, Zhennan ^a   Owens, Rick T ^b   Chen, Yong Q ^a   Edwards, Iris J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b LIFECELL CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; DOCOSAHEXAENOIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROTEIN BAD; PROTEIN P42; PROTEIN P44; SMALL INTERFERING RNA; SYNDECAN 1; SYNDECAN 1 SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; BLOTTING, WESTERN; BREAST NEOPLASMS; CADHERINS; DOCOSAHEXAENOIC ACIDS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNDECAN-1; TUMOR CELLS, CULTURED;

EID: 80053163425     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgr132     Document Type: Article

References (57)

1. Sasaki,S. et al. (1993) An ecological study of the relationship between dietary fat intake and breast cancer mortality. Prev. Med., 22, 187-202.
2. Kaizer,L. et al. (1989) Fish consumption and breast cancer risk: an ecological study. Nutr. Cancer, 12, 61-68.
3. Hursting,S.D. et al. (1990) Types of dietary fat and the incidence of cancer at five sites. Prev. Med., 19, 242-253.
4. Rose,D.P. et al. (1993) Effects of dietary omega-3 fatty acids on human breast cancer growth and metastases in nude mice. J. Natl Cancer Inst., 85, 1743-1747.
5. Rose,D.P. et al. (1995) Influence of diets containing eicosapentaenoic or docosahexaenoic acid on growth and metastasis of breast cancer cells in nude mice. J. Natl Cancer Inst., 87, 587-592.
6. Kang,K.S. et al. (2010) Docosahexaenoic acid induces apoptosis in MCF-7 cells in vitro and in vivo via reactive oxygen species formation and caspase 8 activation. PLoS One, 5, e10296.
7. Jurkowski,J.J. et al. (1985) Dietary effects of menhaden oil on the growth and membrane lipid composition of rat mammary tumors. J. Natl Cancer Inst., 74, 1145-1150.
8. Braden,L.M. et al. (1986) Dietary polyunsaturated fat in relation to mammary carcinogenesis in rats. Lipids, 21, 285-288.
9. Hardman,W.E. et al. (2001) Three percent dietary fish oil concentrate increased efficacy of doxorubicin against MDA-MB 231 breast cancer xenografts. Clin. Cancer Res., 7, 2041-2049.
10. Shao,Y. et al. (1995) Dietary menhaden oil enhances mitomycin C antitumor activity toward human mammary carcinoma MX-1. Lipids, 30, 1035-1045.
11. Burns,C.P. et al. (1986) Adriamycin transport and sensitivity in fatty acidmodified leukemia cells. Biochim. Biophys. Acta, 888, 10-17.
12. Germain,E. et al. (1998) 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.
13. Bougnoux,P. et al. (2009) Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: a phase II trial. Br. J. Cancer, 101, 1978-1985.
14. Edwards,I.J. et al. (2004) Differential effects of delivery of omega-3 fatty acids to human cancer cells by low-density lipoproteins versus albumin. Clin. Cancer Res., 10, 8275-8283.
15. Inki,P. et al. (1994) Immunohistochemical localization of syndecan-1 in normal and pathological human uterine cervix. J. Pathol., 172, 349-355.
16. Mukunyadzi,P. et al. (2002) The level of syndecan-1 expression is a distinguishing feature in behavior between keratoacanthoma and invasive cutaneous squamous cell carcinoma. Mod. Pathol., 15, 45-49.
17. Kumar-Singh,S. et al. (1998) Syndecan-1 expression in malignant mesothelioma: correlation with cell differentiation, WT1 expression, and clinical outcome. J. Pathol., 186, 300-305.
18. Mikami,S. et al. (2001) Loss of syndecan-1 and increased expression of heparanase in invasive esophageal carcinomas. Jpn. J. Cancer Res., 92, 1062-1073.
19. Anttonen,A. et al. (1999) Syndecan-1 expression has prognostic significance in head and neck carcinoma. Br. J. Cancer, 79, 558-564.
20. Pulkkinen,J.O. et al. (1997) Syndecan-1: a new prognostic marker in laryngeal cancer. Acta Otolaryngol., 117, 312-315.
21. Numa,F. et al. (2002) Syndecan-1 expression in cancer of the uterine cervix: association with lymph node metastasis. Int. J. Oncol., 20, 39-43.
22. Matsumoto,A. et al. (1997) Reduced expression of syndecan-1 in human hepatocellular carcinoma with high metastatic potential. Int. J. Cancer, 74, 482-491.
23. Nackaerts,K. et al. (1997) Heparan sulfate proteoglycan expression in human lung-cancer cells. Int. J. Cancer, 74, 335-345.
24. Mali,M. et al. (1994) Suppression of tumor cell growth by syndecan-1 ectodomain. J. Biol. Chem., 269, 27795-27798.
25. Dhodapkar,M.V. et al. (1998) Syndecan-1 is a multifunctional regulator of myeloma pathobiology: control of tumor cell survival, growth, and bone cell differentiation. Blood, 91, 2679-2688.
26. Sun,H. et al. (2005) Omega-3 polyunsaturated fatty acids regulate syndecan-1 expression in human breast cancer cells. Cancer Res., 65, 4442-4447.
27. Sun,H. et al. (2008) Peroxisome proliferator-activated receptor gammamediated up-regulation of syndecan-1 by n-3 fatty acids promotes apoptosis of human breast cancer cells. Cancer Res., 68, 2912-2919.
28. Santen,R.J. et al. (2002) The role of mitogen-activated protein (MAP) kinase in breast cancer. J. Steroid Biochem. Mol. Biol., 80, 239-256.
29. McCubrey,J.A. et al. (2007) Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim. Biophys. Acta, 1773, 1263-1284.
30. Gorjao,R. et al. (2007) Regulation of interleukin-2 signaling by fatty acids in human lymphocytes. J. Lipid Res., 48, 2009-2019.
31. Seti,H. et al. (2009) Effects of omega-3 and omega-6 fatty acids on IGF-I receptor signalling in colorectal cancer cells. Arch. Physiol. Biochem., 115, 127-136.
32. Yusufi,A.N. et al. (2003) Differential effects of low-dose docosahexaenoic acid and eicosapentaenoic acid on the regulation of mitogenic signaling pathways in mesangial cells. J. Lab. Clin. Med., 141, 318-329.
33. Viklund,L. et al. (2002) Expression and characterization of minican, a recombinant syndecan-1 with extensively truncated core protein. Biochem. Biophys. Res. Commun., 290, 146-152.
34. Kang,J.X. et al. (2004) Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature, 427, 504.
35. Ma,D.W. et al. (2006) N-3 polyunsaturated fatty acids endogenously synthesized in fat-1 mice are enriched in the mammary gland. Lipids, 41, 35-39.
36. Orr,S.K. et al. (2010) The fat-1 mouse has brain docosahexaenoic acid levels achievable through fish oil feeding. Neurochem. Res., 35, 811-819.
37. Sun,H. et al. (2011) Endogenous synthesis of n-3 polyunsaturated fatty acids in fat-1 mice is associated with increased mammary gland and liver syndecan-1. PLoS One, 6, e20502.
38. Alexander,C.M. et al. (2000) Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet., 25, 329-332.
39. McQuillan,D.J. et al. (2001) Recombinant expression of proteoglycans in mammalian cells. Utility and advantages of the vaccinia virus/T7 bacteriophage hybrid expression system. Methods Mol. Biol., 171, 201-219.
40. Berquin,I.M. et al. (2007) Modulation of prostate cancer genetic risk by omega-3 and omega-6 fatty acids. J. Clin. Invest., 117, 1866-1875.
41. Conquer,J.A. et al. (1998) Effect of supplementation with different doses of DHA on the levels of circulating DHA as non-esterified fatty acid in subjects of Asian Indian background. J. Lipid Res., 39, 286-292.
42. Edwards,I.J. et al. (2008) In vivo and in vitro regulation of syndecan 1 in prostate cells by N-3 polyunsaturated fatty acids. J. Biol. Chem., 283, 18441-18449.
43. Forman,B.M. et al. (1997) Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc. Natl Acad. Sci. USA, 94, 4312-4317.
44. Shao,D. et al. (1998) Interdomain communication regulating ligand binding by PPAR-gamma. Nature, 396, 377-380.
45. Sebolt-Leopold,J.S. et al. (1999) Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat. Med., 5, 810-816.
46. Scheid,M.P. et al. (1999) Regulation of bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase. J. Biol. Chem., 274, 31108-31113.
47. Sivaraman,V.S. et al. (1997) Hyperexpression of mitogen-activated protein kinase in human breast cancer. J. Clin. Invest., 99, 1478-1483.
48. Salh,B. et al. (1999) Investigation of the Mek-MAP kinase-Rsk pathway in human breast cancer. Anticancer Res., 19, 731-740.
49. Mueller,H. et al. (2000) Potential prognostic value of mitogen-activated protein kinase activity for disease-free survival of primary breast cancer patients. Int. J. Cancer, 89, 384-388.
50. Sebolt-Leopold,J.S. (2000) Development of anticancer drugs targeting the MAP kinase pathway. Oncogene, 19, 6594-6599.
51. Endo,K. et al. (2003) Cleavage of syndecan-1 bymembrane typematrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem., 278, 40764-40770.
52. Wang,Z. et al. (2005) Constitutive and accelerated shedding of murine syndecan-1 is mediated by cleavage of its core protein at a specific juxtamembrane site. Biochemistry, 44, 12355-12361.
53. Li,Q. et al. (2002) Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell, 111, 635-646.
54. Brule,S. et al. (2006) The shedding of syndecan-4 and syndecan-1 from HeLa cells and human primary macrophages is accelerated by SDF-1/CXCL12 and mediated by the matrix metalloproteinase-9. Glycobiology, 16, 488-501.
55. Ding,K. et al. (2005) Growth factor-induced shedding of syndecan-1 confers glypican-1 dependence on mitogenic responses of cancer cells. J. Cell Biol., 171, 729-738.
56. Purushothaman,A. et al. (2008) Heparanase stimulation of protease expression implicates it as a master regulator of the aggressive tumor phenotype in myeloma. J. Biol. Chem., 283, 32628-32636.
57. Nikolova,V. et al. (2009) Differential roles for membrane-bound and soluble syndecan-1 (CD138) in breast cancer progression. Carcinogenesis, 30, 397-407.