Docosahexaenoic acid inhibits vascular endothelial growth factor (VEGF)-induced cell migration via the GPR120/PP2A/ERK1/2/eNOS signaling pathway in human umbilical vein endothelial cells

Journal of Agricultural and Food Chemistry

Volumn 62, Issue 18, 2014, Pages 4152-4158

  Chao, Che Yi ^a   Lii, Chong Kuei ^a,b   Ye, Siou Yu ^b   Li, Chien Chun ^c,d   Lu, Chia Yang ^b   Lin, Ai Hsuan ^b   Liu, Kai Li ^c,d   Chen, Haw Wen ^b  

^a ASIA UNIVERSITY   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

cell migration; docosahexaenoic acid (DHA); human umbilical vein endothelial cells (HUVECs); nitric oxide (NO); vascular endothelial growth factor (VEGF)

Indexed keywords

BIOASSAY; NITRIC OXIDE; PHOSPHORYLATION; POLYUNSATURATED FATTY ACIDS; REPAIR; CELL ENGINEERING; CELL SIGNALING; CELLS; CYTOLOGY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYMES; FATTY ACIDS; UNSATURATED FATTY ACIDS;

ANTI-OXIDANT ACTIVITIES; CELL MIGRATION; DOCOSAHEXAENOIC ACID; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; MOLECULAR MECHANISM; N-3 POLYUNSATURATED FATTY ACIDS; PHOSPHATASE ACTIVITY; VASCULAR ENDOTHELIAL GROWTH FACTOR; WOUND HEALING ASSAYS;

ENDOTHELIAL CELLS;

DOCOSAHEXAENOIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; G PROTEIN COUPLED RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 3; O3FAR1 PROTEIN, HUMAN; PHOSPHOPROTEIN PHOSPHATASE 2; VASCULOTROPIN A;

CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL;

CELL MOVEMENT; CELL PROLIFERATION; DOCOSAHEXAENOIC ACIDS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN PHOSPHATASE 2; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84900308435     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf5007165     Document Type: Article

References (46)

1. Yang, Y. C.; Lii, C. K.; Wei, Y. L.; Li, C. C.; Lu, C. Y.; Liu, K. L.; Chen, H. W. Docosahexaenoic acid inhibition of inflammation is partially via cross-talk between Nrf2/heme oxygenase 1 and IKK/NF-κB pathways J. Nutr. Biochem. 2013, 24, 204-212
2. Simopoulos, A. P. Omega-3 fatty acids in inflammation and autoimmune diseases J. Am. Coll. Nutr. 2002, 21, 495-505
3. Chen, H. W.; Chao, C. Y.; Lin, L. L.; Lu, C. Y.; Liu, K. L.; Lii, C. K.; Li, C. C. Inhibition of matrix metalloproteinase-9 expression by docosahexaenoic acid mediated by heme oxygenase 1 in 12- O -tetradecanoylphorbol-13-acetate- induced MCF-7 human breast cancer cells Arch. Toxicol. 2013, 87, 857-869
4. American Cancer Society. Cancer Facts & Figures 2007; American Cancer Society: Atlanta, GA, USA, 2007.
5. Brasky, T. M.; Lampe, J. W.; Potter, J. D.; Patterson, R. E.; White, E. Specialty supplements and breast cancer risk in the VITamins And Lifestyle (VITAL) Cohort. Cancer epidemiology, biomarkers and prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2010, 19, 1696-1708
6. Wolk, A.; Larsson, S. C.; Johansson, J. E.; Ekman, P. Long-term fatty fish consumption and renal cell carcinoma incidence in women JAMA, J. Am. Med. Assoc. 2006, 296, 1371-1376
7. Matesanz, N.; Park, G.; McAllister, H.; Leahey, W.; Devine, A.; McVeigh, G. E.; Gardiner, T. A.; McDonald, D. M. Docosahexaenoic acid improves the nitroso-redox balance and reduces VEGF-mediated angiogenic signaling in microvascular endothelial cells Invest. Ophthalmol. Vis. Sci. 2010, 51, 6815-6825
8. Ulloa-Aguirre, A.; Stanislaus, D.; Janovick, J. A.; Conn, P. M. Structure-activity relationships of G protein-coupled receptors Arch. Med. Res. 1999, 30, 420-435
9. Gether, U. Uncovering molecular mechanisms involved in activation of G protein-coupled receptors Endocr. Rev. 2000, 21, 90-113
10. Schulte, G.; Fredholm, B. B. Signaling from adenosine receptors to mitogen-activated protein kinases Cell. Signal. 2003, 15, 813-827
11. Oh, D. Y.; Talukdar, S.; Bae, E. J.; Imamura, T.; Morinaga, H.; Fan, W.; Li, P.; Lu, W. J.; Watkins, S. M.; Olefsky, J. M. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects Cell 2010, 142, 687-698
12. Fischer, C.; Schneider, M.; Carmeliet, P. Principles and therapeutic implications of angiogenesis, vasculogenesis and arteriogenesis Handb. Exp. Pharmacol. 2006, 157-212
13. Griffioen, A. W.; Molema, G. Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation Pharmacol. Rev. 2000, 52, 237-268
14. Nakagawa, K.; Shibata, A.; Saito, T.; Sookwong, P.; Kato, S.; Tsuduki, T.; Matsubara, K.; Miyazawa, T. Phosphatidylcholine hydroperoxide promotes VEGF-induced angiogenesis in endothelial cells and rat aorta ring cultures Biochim. Biophys. Acta 2011, 1810, 1205-1211
15. Hoeben, A.; Landuyt, B.; Highley, M. S.; Wildiers, H.; Van Oosterom, A. T.; De Bruijn, E. A. Vascular endothelial growth factor and angiogenesis Pharmacol. Rev. 2004, 56, 549-580
16. Giles, F. J. The vascular endothelial growth factor (VEGF) signaling pathway: a therapeutic target in patients with hematologic malignancies Oncologist 2001, 6 (Suppl. 5) 32-39
17. Duda, D. G.; Fukumura, D.; Jain, R. K. Role of eNOS in neovascularization: NO for endothelial progenitor cells Trends Mol. Med. 2004, 10, 143-145
18. Fleming, I. Molecular mechanisms underlying the activation of eNOS Pflugers Archiv. 2010, 459, 793-806
19. Shi, Y. Assembly and structure of protein phosphatase 2A Sci. China Ser. C, Life Sci./Chinese Acad. Sci. 2009, 52, 135-146
20. Janssens, V.; Goris, J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling Biochem. J. 2001, 353, 417-439
21. Miglietta, A.; Bozzo, F.; Gabriel, L.; Bocca, C.; Canuto, R. A. Extracellular signal-regulated kinase 1/2 and protein phosphatase 2A are involved in the antiproliferative activity of conjugated linoleic acid in MCF-7 cells Br. J. Nutr. 2006, 96, 22-27
22. Zhao, B.; Sun, L.; Haas, M.; Denenberg, A. G.; Wong, H. R.; Shanley, T. P. PP2A regulates upstream members of the c-jun N-terminal kinase mitogen-activated protein kinase signaling pathway Shock 2008, 29, 181-188
23. Lee, T.; Kim, S. J.; Sumpio, B. E. Role of PP2A in the regulation of p38 MAPK activation in bovine aortic endothelial cells exposed to cyclic strain J. Cell. Physiol. 2003, 194, 349-355
24. Neviani, P.; Santhanam, R.; Trotta, R.; Notari, M.; Blaser, B. W.; Liu, S.; Mao, H.; Chang, J. S.; Galietta, A.; Uttam, A.; Roy, D. C.; Valtieri, M.; Bruner-Klisovic, R.; Caligiuri, M. A.; Bloomfield, C. D.; Marcucci, G.; Perrotti, D. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein Cancer Cell 2005, 8, 355-368
25. Spencer, L.; Mann, C.; Metcalfe, M.; Webb, M.; Pollard, C.; Spencer, D.; Berry, D.; Steward, W.; Dennison, A. The effect of omega-3 FAs on tumour angiogenesis and their therapeutic potential Eur. J. Cancer 2009, 45, 2077-2086
26. Lamalice, L.; Le Boeuf, F.; Huot, J. Endothelial cell migration during angiogenesis Circ. Res. 2007, 100, 782-794
27. Gill, S. E.; Parks, W. C. Metalloproteinases and their inhibitors: regulators of wound healing Int. J. Biochem. Cell Biol. 2008, 40, 1334-1347
28. Liu, S.; Rockey, D. C. Cicletanine stimulates eNOS phosphorylation and NO production via Akt and MAP kinase/Erk signaling in sinusoidal endothelial cells Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 305, G163-G171
29. Zhang, J.; Lu, A.; Beech, D.; Jiang, B.; Lu, Y. Suppression of breast cancer metastasis through the inhbition of VEGF-mediated tumor angiogenesis Cancer Ther. 2007, 5, 273-286
30. Feliers, D.; Chen, X.; Akis, N.; Choudhury, G. G.; Madaio, M.; Kasinath, B. S. VEGF regulation of endothelial nitric oxide synthase in glomerular endothelial cells Kidney Int. 2005, 68, 1648-1659
31. Greif, D. M.; Kou, R.; Michel, T. Site-specific dephosphorylation of endothelial nitric oxide synthase by protein phosphatase 2A: evidence for crosstalk between phosphorylation sites Biochemistry 2002, 41, 15845-15853
32. Hirasawa, A.; Tsumaya, K.; Awaji, T.; Katsuma, S.; Adachi, T.; Yamada, M.; Sugimoto, Y.; Miyazaki, S.; Tsujimoto, G. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120 Nat. Med. 2005, 11, 90-94
33. Hsu, Y. H.; Chen, Y. C.; Chen, T. H.; Sue, Y. M.; Cheng, T. H.; Chen, J. R.; Chen, C. H. Far-infrared therapy induces the nuclear translocation of PLZF which inhibits VEGF-induced proliferation in human umbilical vein endothelial cells PLoS One 2012, 7, e30674
34. Cooke, J. P.; Losordo, D. W. Nitric oxide and angiogenesis Circulation 2002, 105, 2133-2135
35. Kim, H. J.; Vosseler, C. A.; Weber, P. C.; Erl, W. Docosahexaenoic acid induces apoptosis in proliferating human endothelial cells J. Cell. Physiol. 2005, 204, 881-888
36. Rose, D. P.; Connolly, J. M. Antiangiogenicity of docosahexaenoic acid and its role in the suppression of breast cancer cell growth in nude mice Int. J. Oncol. 1999, 15, 1011-1015
37. Tsuzuki, T.; Shibata, A.; Kawakami, Y.; Nakagaya, K.; Miyazawa, T. Anti-angiogenic effects of conjugated docosahexaenoic acid in vitro and in vivo Biosci., Biotechnol., Biochem. 2007, 71, 1902-1910
38. Zajdel, A.; Wilczok, A.; Chodurek, E.; Gruchlik, A.; Dzierzewicz, Z. Polyunsaturated fatty acids inhibit melanoma cell growth in vitro Acta Polym. Pharm. 2013, 70, 365-369
39. Zhuang, W.; Wang, G.; Li, L.; Lin, G.; Deng, Z. Omega-3 polyunsaturated fatty acids reduce vascular endothelial growth factor production and suppress endothelial wound repair J. Cardiovasc. Transl. Res. 2013, 6, 287-293
40. Calviello, G.; Di Nicuolo, F.; Gragnoli, S.; Piccioni, E.; Serini, S.; Maggiano, N.; Tringali, G.; Navarra, P.; Ranelletti, F. O.; Palozza, P. n-3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1α induction pathway Carcinogenesis 2004, 25, 2303-2310
41. Szymczak, M.; Murray, M.; Petrovic, N. Modulation of angiogenesis by omega-3 polyunsaturated fatty acids is mediated by cyclooxygenases Blood 2008, 111, 3514-3521
42. Kornfeld, S.; Goupille, C.; Vibet, S.; Chevalier, S.; Pinet, A.; Lebeau, J.; Tranquart, F.; Bougnoux, P.; Martel, E.; Maurin, A.; Richard, S.; Champeroux, P.; Mahéo, K. Reducing endothelial NOS activation and interstitial fluid pressure with n-3 PUFA offset tumor chemoresistance Carcinogenesis 2012, 33, 260-267
43. Michaud, S. E.; Dussault, S.; Groleau, J.; Haddad, P.; Rivard, A. Cigarette smoke exposure impairs VEGF-induced endothelial cell migration: role of NO and reactive oxygen species J. Mol. Cell. Cardiol. 2006, 41, 275-284
44. Janssens, V.; Goris, J.; Van Hoof, C. PP2A: the expected tumor suppressor Curr. Opin. Genet. Dev. 2005, 15, 34-41
45. Schmidt, A.; Wenzel, D.; Thorey, I.; Werner, S.; Fleischmann, B. K.; Bloch, W. Endostatin down-regulates soluble guanylate cyclase (sGC) in endothelial cells in vivo: influence of endostatin on vascular endothelial growth factor (VEGF) signaling Endothelium 2005, 12, 251-257
46. Urbich, C.; Reissner, A.; Chavakis, E.; Dernbach, E.; Haendeler, J.; Fleming, I.; Zeiher, A. M.; Kaszkin, M.; Dimmeler, S. Dephosphorylation of endothelial nitric oxide synthase contributes to the anti-angiogenic effects of endostatin FASEB J. 2002, 16, 706-708