Eicosopentaneoic acid and other free fatty acid receptor agonists inhibit lysophosphatidic acidand epidermal growth factor-induced proliferation of human breast cancer cells

Journal of Clinical Medicine

Volumn 5, Issue 2, 2016, Pages

  Hopkins, Mandi M ^a   Zhang, Zhihong ^a   Liu, Ze ^a   Meier, Kathryn E ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Epidermal growth factor; Free fatty acid receptors; G protein coupled receptors; Lysophosphatidic acid; Reast cancer; 3 fatty acids

Indexed keywords

EICOSOPENTANEOIC ACID; EPIDERMAL GROWTH FACTOR; G PROTEIN COUPLED RECEPTOR; LYSOPHOSPHATIDIC ACID; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 85114280754     PISSN: None     EISSN: 20770383     Source Type: Journal    
DOI: 10.3390/jcm5020016     Document Type: Article

References (53)

1. Liu, Z.; Hopkins, M.M.; Zhang, Z.; Quisenberry, C.B.; Fix, L.C.; Galvan, B.M.; Meier, K.E. ω-3 Fatty acids and other FFA4 agonists inhibit growth factor signaling in human prostate cancer cells. J. Pharm. Exp. Ther. 2015, 352, 1-15. [CrossRef] [PubMed]
2. Hopkins, M.M.; Meier, K.E. ω-3 Fatty acids and their impact on prostate cancer risk. Curr. Nutr. Rep. 2015. in press.
3. Hardman,W.E. ω-3 Fatty acids to augment cancer therapy. J. Nutr. 2002, 132, 3509S-3512S.
4. Zheng, J.S.; Hu, X.J.; Zao, 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. Br. Med. J. 2013, 346, f3706. [CrossRef] [PubMed]
5. Schley, P.D.; Jijon, H.B.; Robinson, L.E.; Field, C.J. Mechanisms of ω-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells. Breast Cancer Res. Treat. 2005, 92, 187-195. [CrossRef] [PubMed]
6. Pogash, T.J.; el-Bayoumy, K.; Amin, S.; Gowda, K.; de Cicco, R.L.; Barton, M.; Su, Y.; Russo, I.H.; Himmelberger, J.A.; Slifker, M.; et al. Oxidized derivative of docosahexaenoic acid preferentially inhibit cell proliferation in triple negative over luminal breas cancer cells. Vitro Cell Dev. Biol. Anim. 2015, 52, 121-127. [CrossRef] [PubMed]
7. Karmali, R.A.; Marsh, J.; Ruchs, C. Effect of ω-3 fatty acids on growth of a rat mammary tumor. J. Natl. Cancer Inst. 1984, 73, 457-461. [PubMed]
8. Rose, D.P.; Connolly, J.M. Effects of dietary ω-3 fatty acids on human breast cancer growth and metastases in nude mice. J. Natl. Caner Inst. 1993, 85, 1743-1747. [CrossRef]
9. Sauer, L.A.; Dauchy, R.T.; Blask, D.E.; Krause, J.A.; Davidson, L.K.; Dauchy, E.M. Eicosapenaenoic acid suppresses cell proliferation in MCF-7 human breast cancer xenografts in nude rats via a pertussis toxin-sensitive signal transduction pathway. J. Nutr. 2005, 135, 2124-2129. [PubMed]
10. Jiang,W.; Zhu, Z.; McGinley, J.N.; el Bayouny, K.; Manni, A.; Thompson, J.H. Identification of a molecular signature underlying inhibition of mammary carcinoma growth by dietary n-3 fatty acids. Cancer Res. 2012, 72, 3795-3806. [CrossRef] [PubMed]
11. Dwivedi, S.; Patel, S.; Jain, K. The what, where, and how of resolvins. AsPac J. Mol. Biol. Biotechnol. 2010, 20, 45-54.
12. Zhang, M.J.; Spite, M. Resolvins: Anti-inflammatory and pro-resolving mediators derived from ω-3 polyunsaturated fatty acids. Annu. Rev. Nutr. 2012, 32, 203-227. [CrossRef] [PubMed]
13. Janakiram, N.B.; Mohammed, A.; Rao, C.V. Role of lipoxins, resolvins, and other bioactive lipids in colon and pancreatic cancer. Cancer Metastasis Rev. 2011, 30, 507-523. [CrossRef] [PubMed]
14. Al-Zaubai, N.; Johnstone, C.N.; Leong, M.M.; Li, J.; Rizzacasa, M.; Stewart, A.G. Resolvin D2 supports MCF-7 cell proliferation via activation of estrogen receptor. J. Pharmacol. Exp. Ther. 2014, 351, 172-180. [CrossRef] [PubMed]
15. Oh, D.Y.; Talukdar, S.; Bae, E.J.; Imamura, T.; Morinaga, H.; Fan, W.Q.; Li, P.; Wendell, J.L.; Watkins, S.M.; Olefsky, J.M. GRP120 is anω-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2012, 143, 687-698.
16. Hara, T.; Hirasawa, A.; Ichimura, A.; Kimura, I.; Tsujimoto, G. Free fatty acid receptors FFAR1 and GPR120 as novel therapeutic targets for metabolic disorders. J. Pharm. Sci. 2011, 100, 3594-3601. [CrossRef] [PubMed]
17. Holliday, N.D.;Watson, S.J.; Brown, A.J.H. Drug discovery opportunities and challenges at G protein coupled receptors for long chain free fatty acids. Front. Endocrinol. 2011, 2, 1-12. [CrossRef] [PubMed]
18. Dranse, H.J.; Kelly, M.E.; Hudson, B.D. Drugs or diet? Developing novel therapeutic strategies targeting the free fatty acid family of GPCRs. Br. J. Pharmacol. 2013, 170, 695-711. [CrossRef] [PubMed]
19. Hudson, B.D.; Shimpukade, B.; Mackenzie, A.E.; Butcher, A.J.; Pediani, J.D.; Christiansen, E.; Heathcote, H.; Tobin, A.B.; Ulven, T.; Milligan, G. The pharmacology of TUG-891, a potent and selective agonist of the free fatty acid receptor 4 (FFA4/GPR120), demonstrates both potential opportunity and possible challenges to therapeutic agonism. Mol. Pharmacol. 2013, 84, 710-725. [CrossRef] [PubMed]
20. Wu, M.; Harvey, K.A.; Ruzmetov, N.;Welch, Z.R.; Sech, L.; Jackson, K.; Stillwell,W.; Zaloga, G.P. Siddiqui RA (2005) ω-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway. Int. J. Cancer 2015, 117, 340-348. [CrossRef] [PubMed]
21. Bernard-Gallon, D.J.; Vissac-Sabatier, C.; Antoine-Vincent, D.; Rio, P.G.; Maruizis, J.C.; Fustier, P.; Bignon, Y.J. Differential effects of n-3 and n-6 polyunsaturated fatty acids on BRCA1 and BRCA2 gene expression in breast cell lines. Br. J. Nutr. 2002, 87, 281-289. [CrossRef] [PubMed]
22. Ghosh-Choudhury, T.; Mandall, C.C.; Woodruff, K.; St. Clair, P.; Fernandes, G.; Chouhury, G.; Ghosh-Choudhury, N. Fish oil targets PTEN to regulate NFκB for downregulation of anti-apoptotic genes in breast tumor growth. Breast Cancer Res. Treat. 2009, 118, 213-228. [CrossRef] [PubMed]
23. 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 obesity-Associated breast cancer. Nutrients 2014, 5, 4760-4793. [CrossRef] [PubMed]
24. Yonezawa, T.; Katoh, K.; Obara, Y. Existence of GPR40 functioning in a human breast cancer cell line, MCF-7. Biochem. Biophys. Res. Commun. 2004, 314, 805-809. [CrossRef] [PubMed]
25. Soto-Guzman, A.; Tobledo, T.; Lopez-Perez, M.; Salazar, E.P. Oleic acid induces ERK1/2 activation and AP-1 DNA binding activity through a mechanism involving Src kinase and EGFR transactivation in breast cancer cells. Mol. Cell. Endocrinol. 2008, 294, 81-91. [CrossRef] [PubMed]
26. Navarro-Tito, N.; Robledo, T.; Salazar, E.P. Arachidonic acid promotes FAK activation and migration in MDA-MB-231 breast cancer cells. Exp. Cell. Res. 2008, 314, 3340-3355. [CrossRef] [PubMed]
27. Chung, H.; Lee, Y.S.; Mayoral, R.; Oh, D.Y.;Webster, N.J.; Sears, D.D.; Olefsky, J.M.; Ellies, L.G.ω-3 Fatty acids reduce obesity-induced tumor progression independent of GPR120 in a mouse model of postmenopausal breast cancer. Oncogene 2014, 34, 3504-3513. [CrossRef] [PubMed]
28. Zhang, Z.; Knoepp, S.M.; Sansbury, H.M.; Han, S.; Ku, H.; Xie, Y.; Hallman, M.; Meier, K.E. Differential expression of FAK and Pyk2 in phorbol ester-sensitive and -resistant EL4 thymoma cells. Clin. Expt. Metastasis 2011, 28, 551-565. [CrossRef] [PubMed]
29. Papupinthu, N.; Lee, H.Y.; Mills, G.B. Lysophosphatidic acid production and action: Critical new players in breast cancer initiation and progression. Br. J. Cancer 2010, 102, 941-946. [CrossRef] [PubMed]
30. Masuda, H.; Zhang, D.; Bartholomeusz, C.; Doihara, H.; Hortobagyi, G.N.; Ueno, N.T. Role of epidermal growth factor receptor in breast cancer. Breast Cancer Res. Treat. 2012, 136, 331-345. [CrossRef] [PubMed]
31. O'Kelly, J.; Chung, A.; Lemp, N.; Chumakova, K.; Yin, D.; Wang, H.J.; Said, J.; Gui, D.; Miller, C.W.; Karlan, B.Y.; et al. Functional domains of CCN1 (Cyr61) regulate breast cancer progression. Int. J. Oncol. 2008, 33, 59-67. [CrossRef] [PubMed]
32. Jun, J.I.; Lau, L.F. Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nature Rev. Drug Discov. 2011, 10, 945-963. [CrossRef] [PubMed]
33. Boucharaba, A.; Serre, C.M.; Gres, S.; Saulnier-Blache, J.S.; Bordet, J.C.; Guglielmi, J.; Clezardin, P.; Peyruchaud, O. Platelet-derived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. J. Clin. Invest. 2004, 114, 1714-1725. [CrossRef] [PubMed]
34. Chen, M.; Towers, L.N.; O'Connor, K.L. LPA2 (EDG4) mediates Rho-dependent chemotaxis with lower efficacy than LPA1 (EDG2) in breast carcinoma cells. Am. J. Physiol. Cell. Physiol. 2007, 292, C1947-C1933. [CrossRef] [PubMed]
35. Li, T.T.; Alemayehu, M.; Aziziyeh, A.; Pape, C.; Pampilio, M.; Postovit, L.M.; Mills, G.B.; Babway, A.V.; Bhattacharya, M. Beta-arrestin/Ral signaling regulates lysophosphatidic acid-mediated migration and invasion of human breast tumor cells. Mol. Cancer Res. 2009, 7, 1064-1077. [CrossRef] [PubMed]
36. Swaney, J.S.; Chapman, C.; Correa, L.D.; Stebbins, K.J.; Bundey, R.A.; Prodanovich, P.C.; Fagan, P.; Baccei, C.S.; Santini, A.M.; Hutchinson, J.H.; et al. A novel, orally active LPA1 receptor antagonist inhibits lung fibrosis in the mouse bleomycin model. Br. J. Pharmacol. 2010, 160, 1699-1713. [CrossRef] [PubMed]
37. Alemayehu, M.; Dragan, M.; Pape, C.; Siddiqui, I.; Sacks, D.B.; di Guglielmo, G.M.; Babway, A.V.; Bhattacharya, M. β-Arrestin2 regulates lysophosphatidic acid-induced human breast tumor cell migration and invasion via Rap1 and IQGAP1. PLoS ONE 2013, 8, e56174. [CrossRef] [PubMed]
38. Sun, K.; Cai, H.; Duan, X.; Yang, Y.; Li, M.; Wu, J.; Zhang, X.; Wang, J. Aberrant expression and potential therapeutic target of lysophosphatidic acid receptor 3 in triple-negative breast cancers. Clin. Exp. Med. 2014. [CrossRef] [PubMed]
39. Ohta, H.; Sata, K.; Murata, N.; Damirin, A.; Malchinkhuu, E.; Kon, J.; Kimura, T.; Tobo, M.; Yamazaki, Y.; Watanabe, T.; et al. Ki16425, a subtype-selective antagonist for EDG-family lysophosphatidic acid receptors. Mol. Pharmacol. 2003, 64, 994-1005. [CrossRef] [PubMed]
40. Hopkins, M.M.; Liu, Z.; Meier, K.E. Cross-talk between lysophosphatidic acid receptor a, free fatty acid receptor 4, and epidermal growth factor receptor in human prostate cancer cells. 2015, Submitted.
41. Boucharaba, A.; Guillet, B.; Menaa, F.; Hneino, M.; van Wijnen, A.J.; Clezardin, P.; Peyruchaud, O. Bioactive lipids lysophosphatidic acid and sphingosine 1-phosphate mediate breast cancer cell biological functions through distinct mechanisms. Oncol. Res. 2009, 18, 173-184. [CrossRef] [PubMed]
42. Du, S.; Sun, C.; Hu, Z.; Yang, Y.; Zhu, Y.; Zheng, D.; Gu, L.; Lu, X. Lysophosphatidic acid induces MDA-MB-231 breast cancer cells migration through activation of PI3K/PAK1/ERK signaling. PLoS ONE 2010, 5, e15940. [CrossRef] [PubMed]
43. Swamydas, M.; Nguyen, D.; Allen, L.D.; Eddy, J.; Dreau, D. Progranulin stimulated by LPA promotes the migration of aggressive breast cancer cells. Cell. Commun. Adhes. 2010, 18, 119-130. [CrossRef] [PubMed]
44. Sun, K.; Duan, X.; Cai, H.; Liu, X.; Yang, Y.; Li, M.; Zhang, X.; Wang, J. Curcumin inhibits LPA-induced invasion by attenuating RhoA/ROCK/MMPs pathway in MCF7 breast cancer cells. Clin. Exp. Med. 2015, 1-11. [CrossRef] [PubMed]
45. Zhang, H.; Xu, X.; Gajewiak, J.; Tsukahara, R.; Fujiwara, Y.; Liu, J.; Fells, J.I.; Perygin, D.; Parrill, A.L.; Tigyi, G.; et al. Dual activity lysophosphatidic acid receptor pan-antagonist/autotaxin inhibitor reduces breast cancer cell migration in vitro and causes tumor regression. Cancer Res. 2009, 69, 5441-5449. [CrossRef] [PubMed]
46. Liu, S.; Umezu-Goto, M.; Murph, M.; Lu, Y.; Liu,W.; Zhang, F.; Yu, S.; Stephens, L.C.; Cui, X.; Murrow, G.; et al. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell. 2009, 15, 539-550. [CrossRef] [PubMed]
47. Daaka, Y. Mitogenic action of LPA in prostate. Biochim. Biophys. Acta. 2002, 1582, 265-269. [CrossRef]
48. Marshall, J.C.A.; Collins, J.W.; Nakayama, J.; Horak, C.E.; Liewehr, D.J.; Steinberg, S.M.; Albaugh, M.; Vidal-Vanaclocha, F.; Palmieri, D.; Marbier, M.; et al. Effects of inhibition of the lysophosphatidic acid receptor 1 on metastasis and metastatic dormancy in breast cancer. J. Natl. Cancer Inst. 2012, 104, 1306-1319. [CrossRef] [PubMed]
49. Kue, P.F.; Taub, J.S.; Harrington, L.B.; Polakiewicz, R.D.; Ullrich, A.; Daaka, Y. Lysophosphatidic acid-regulated mitogenic ERK signaling in androgen-insensitive prostate cancer PC-3 cells. Int. J. Cancer 2002, 102, 572-579. [CrossRef] [PubMed]
50. Bektas, M.; Payne, S.G.; Liu, H.; Goparaju, S.; Milstien, S.; Spiegel, S. A novel acylglycerol kinase that produces lysophophatidic modulates cross talk with EGFR in prostate cancer cells. J. Cell. Biol. 2005, 169, 801-811. [CrossRef] [PubMed]
51. Snider, A.J.; Zhang, Z.; Xie, Y.; Meier, K.E. Epidermal growth factor increases lysophosphatidic acid production in human ovarian cancer cells: Roles for phospholipase D2 and receptor transactivation. Am. J. Physiol. Cell. Physiol. 2009, 298, C163-C170. [CrossRef] [PubMed]
52. Mausbacher, N.; Schreiber, T.B.; Daub, H. Glycoprotein capture and quantitative phosphoproteomics indicate coordinated regulation of cell migration upon lysophosphatidic acid stimulation. Mol. Cell. Proteom. 2010, 9, 2337-2353. [CrossRef] [PubMed]
53. 1 receptor function and phosphorylation state. Biochim. Biophys. Acta 2011, 1810, 1170-1177. [CrossRef] [PubMed]