Down-regulation of lipid raft-associated onco-proteins via cholesterol-dependent lipid raft internalization in docosahexaenoic acid-induced apoptosis

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 1, 2014, Pages 190-203

  Lee, Eun Jeong ^a   Yun, Un Jung ^a   Koo, Kyung Hee ^a   Sung, Jee Young ^a   Shim, Jaegal ^a   Ye, Sang Kyu ^b   Hong, Kyeong Man ^a   Kim, Yong Nyun ^a  

^a National Cancer Center   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

Author keywords

Akt; Cholesterol; Docosahexaenoic acid (DHA); EGFR; Hsp90; Lipid raft

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; DOCOSAHEXAENOIC ACID; EPIDERMAL GROWTH FACTOR; HEAT SHOCK PROTEIN 90; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; ONCOPROTEIN; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INTERNALIZATION; INTRACELLULAR SIGNALING; LIPID RAFT; LYSOSOME; ONCOGENE SRC; PRIORITY JOURNAL;

EID: 84887588021     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.10.006     Document Type: Article

References (71)

1. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1 2000 31 39
2. K. Jacobson, O.G. Mouritsen, and R.G. Anderson Lipid rafts: at a crossroad between cell biology and physics Nat. Cell Biol. 9 2007 7 14 (Pubitemid 46024188)
3. J.F. Hancock Lipid rafts: contentious only from simplistic standpoints Nat. Rev. Mol. Cell Biol. 7 2006 456 462 (Pubitemid 44050099)
4. S.K. Patra Dissecting lipid raft facilitated cell signaling pathways in cancer Biochim. Biophys. Acta 1785 2008 182 206
5. T. Nieto-Miguel, C. Gajate, F. Gonzalez-Camacho, and F. Mollinedo Proapoptotic role of Hsp90 by its interaction with c-Jun N-terminal kinase in lipid rafts in edelfosine-mediated antileukemic therapy Oncogene 27 2008 1779 1787 (Pubitemid 351380270)
6. L. Zhuang, J. Kim, R.M. Adam, K.R. Solomon, and M.R. Freeman Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts J. Clin. Invest. 115 2005 959 968 (Pubitemid 40489400)
7. Y.C. Li, M.J. Park, S.K. Ye, C.W. Kim, and Y.N. Kim Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents Am. J. Pathol. 168 2006 1107 1118 (quiz 1404-1105)
8. K. Simons, and R. Ehehalt Cholesterol, lipid rafts, and disease J. Clin. Invest. 110 2002 597 603 (Pubitemid 34988781)
9. E.K. Park, E.J. Lee, S.H. Lee, K.H. Koo, J.Y. Sung, E.H. Hwang, J.H. Park, C.W. Kim, K.C. Jeong, B.K. Park, and Y.N. Kim Induction of apoptosis by the ginsenoside Rh2 by internalization of lipid rafts and caveolae and inactivation of Akt Br. J. Pharmacol. 160 2010 1212 1223
10. T.M. Stulnig, J. Huber, N. Leitinger, E.M. Imre, P. Angelisova, P. Nowotny, and W. Waldhausl Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition J. Biol. Chem. 276 2001 37335 37340
11. W. Stillwell, S.R. Shaikh, M. Zerouga, R. Siddiqui, and S.R. Wassall Docosahexaenoic acid affects cell signaling by altering lipid rafts Reprod. Nutr. Dev. 45 2005 559 579 (Pubitemid 41511882)
12. Q. Li, M. Wang, L. Tan, C. Wang, J. Ma, N. Li, Y. Li, G. Xu, and J. Li Docosahexaenoic acid changes lipid composition and interleukin-2 receptor signaling in membrane rafts J. Lipid Res. 46 2005 1904 1913 (Pubitemid 41248487)
13. Q. Li, L. Tan, C. Wang, N. Li, Y. Li, G. Xu, and J. Li Polyunsaturated eicosapentaenoic acid changes lipid composition in lipid rafts Eur. J. Nutr. 45 2006 144 151
14. P.D. Schley, D.N. Brindley, and C.J. Field (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 2007 548 553 (Pubitemid 46397481)
15. K.R. Rogers, K.D. Kikawa, M. Mouradian, K. Hernandez, K.M. McKinnon, S.M. Ahwah, and R.S. Pardini Docosahexaenoic acid alters epidermal growth factor receptor-related signaling by disrupting its lipid raft association Carcinogenesis 31 2010 1523 1530
16. Y. Duraisamy, D. Lambert, C.A. O'Neill, and P.J. Padfield Differential incorporation of docosahexaenoic acid into distinct cholesterol-rich membrane raft domains Biochem. Biophys. Res. Commun. 360 2007 885 890 (Pubitemid 47077404)
17. J.B. Ewaschuk, M. Newell, and C.J. Field Docosahexanoic acid improves chemotherapy efficacy by inducing CD95 translocation to lipid rafts in ER(-) breast cancer cells Lipids 47 2012 1019 1030
18. V. Blanckaert, L. Ulmann, V. Mimouni, J. Antol, L. Brancquart, and B. Chenais Docosahexaenoic acid intake decreases proliferation, increases apoptosis and decreases the invasive potential of the human breast carcinoma cell line MDA-MB-231 Int. J. Oncol. 36 2010 737 742
19. G. Calviello, F. Resci, S. Serini, E. Piccioni, A. Toesca, A. Boninsegna, G. Monego, F.O. Ranelletti, and P. Palozza Docosahexaenoic acid induces proteasome-dependent degradation of beta-catenin, down-regulation of survivin and apoptosis in human colorectal cancer cells not expressing COX-2 Carcinogenesis 28 2007 1202 1209 (Pubitemid 47062678)
20. S. Serini, S. Trombino, F. Oliva, E. Piccioni, G. Monego, F. Resci, A. Boninsegna, N. Picci, F.O. Ranelletti, and G. Calviello Docosahexaenoic acid induces apoptosis in lung cancer cells by increasing MKP-1 and down-regulating p-ERK1/2 and p-p38 expression Apoptosis 13 2008 1172 1183
21. Y. Hu, H. Sun, R.T. Owens, Z. Gu, J. Wu, Y.Q. Chen, J.T. O'Flaherty, and I.J. Edwards Syndecan-1-dependent suppression of PDK1/Akt/bad signaling by docosahexaenoic acid induces apoptosis in prostate cancer Neoplasia 12 2010 826 836
22. P.D. Schley, H.B. Jijon, L.E. Robinson, and C.J. Field Mechanisms of omega-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells Breast Cancer Res. Treat. 92 2005 187 195 (Pubitemid 40933584)
23. K. Lim, C. Han, Y. Dai, M. Shen, and T. Wu Omega-3 polyunsaturated fatty acids inhibit hepatocellular carcinoma cell growth through blocking beta-catenin and cyclooxygenase-2 Mol. Cancer Ther. 8 2009 3046 3055
24. K.S. Kang, P. Wang, N. Yamabe, M. Fukui, T. Jay, and B.T. Zhu 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 2010 e10296
25. M. Wu, K.A. Harvey, N. Ruzmetov, Z.R. Welch, L. Sech, K. Jackson, W. Stillwell, G.P. Zaloga, and R.A. Siddiqui Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway Int. J. Cancer 117 2005 340 348 (Pubitemid 41429556)
26. D.P. Rose, J.M. Connolly, J. Rayburn, and M. Coleman Influence of diets containing eicosapentaenoic or docosahexaenoic acid on growth and metastasis of breast cancer cells in nude mice J. Natl. Cancer Inst. 87 1995 587 592
27. H. Gleissman, L. Segerstrom, M. Hamberg, F. Ponthan, M. Lindskog, J.I. Johnsen, and P. Kogner Omega-3 fatty acid supplementation delays the progression of neuroblastoma in vivo Int. J. Cancer 128 2011 1703 1711
28. N. Hajjaji, and P. Bougnoux Selective sensitization of tumors to chemotherapy by marine-derived lipids: a review Cancer Treat. Rev. 39 2013 473 488
29. S.A. Schonberg, A.G. Lundemo, T. Fladvad, K. Holmgren, H. Bremseth, A. Nilsen, O. Gederaas, K.E. Tvedt, K.W. Egeberg, and H.E. Krokan Closely related colon cancer cell lines display different sensitivity to polyunsaturated fatty acids, accumulate different lipid classes and downregulate sterol regulatory element-binding protein 1 FEBS J. 273 2006 2749 2765
30. J.A. Akinsete, G. Ion, T.R. Witte, and W.E. Hardman Consumption of high omega-3 fatty acid diet suppressed prostate tumorigenesis in C3(1) Tag mice Carcinogenesis 33 2012 140 148
31. H. Gleissman, J.I. Johnsen, and P. Kogner Omega-3 fatty acids in cancer, the protectors of good and the killers of evil? Exp. Cell Res. 316 2010 1365 1373
32. J.L. Toit-Kohn, L. Louw, and A.M. Engelbrecht Docosahexaenoic acid induces apoptosis in colorectal carcinoma cells by modulating the PI3 kinase and p38 MAPK pathways J. Nutr. Biochem. 20 2009 106 114
33. H. Sun, Y. Hu, Z. Gu, R.T. Owens, Y.Q. Chen, and I.J. Edwards 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 32 2011 1518 1524
34. S.R. Shaikh, and H. Teague N-3 fatty acids and membrane microdomains: from model membranes to lymphocyte function Prostaglandins Leukot. Essent. Fatty Acids 87 2012 205 208
35. P. Yaqoob, and S.R. Shaikh The nutritional and clinical significance of lipid rafts Curr. Opin. Clin. Nutr. Metab. Care 13 2010 156 166
36. P.A. Corsetto, A. Cremona, G. Montorfano, I.E. Jovenitti, F. Orsini, P. Arosio, and A.M. Rizzo Chemical-physical changes in cell membrane microdomains of breast cancer cells after omega-3 PUFA incorporation Cell Biochem. Biophys. 64 2012 45 59
37. P.A. Corsetto, G. Montorfano, S. Zava, I.E. Jovenitti, A. Cremona, B. Berra, and A.M. Rizzo Effects of n-3 PUFAs on breast cancer cells through their incorporation in plasma membrane Lipids Health Dis. 10 2011 73
38. E.K. Park, M.J. Park, S.H. Lee, Y.C. Li, J. Kim, J.S. Lee, J.W. Lee, S.K. Ye, J.W. Park, C.W. Kim, B.K. Park, and Y.N. Kim Cholesterol depletion induces anoikis-like apoptosis via FAK down-regulation and caveolae internalization J. Pathol. 218 2009 337 349
39. J.F. Dermine, S. Duclos, J. Garin, F. St-Louis, S. Rea, R.G. Parton, and M. Desjardins Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes J. Biol. Chem. 276 2001 18507 18512
40. Y.N. Kim, P. Dam, and P.J. Bertics Caveolin-1 phosphorylation in human squamous and epidermoid carcinoma cells: dependence on ErbB1 expression and Src activation Exp. Cell Res. 280 2002 134 147 (Pubitemid 35230374)
41. Y.N. Kim, G.J. Wiepz, A.G. Guadarrama, and P.J. Bertics Epidermal growth factor-stimulated tyrosine phosphorylation of caveolin-1. Enhanced caveolin-1 tyrosine phosphorylation following aberrant epidermal growth factor receptor status J. Biol. Chem. 275 2000 7481 7491 (Pubitemid 30159643)
42. W. Chen, D.B. Jump, W.J. Esselman, and J.V. Busik Inhibition of cytokine signaling in human retinal endothelial cells through modification of caveolae/lipid rafts by docosahexaenoic acid Invest. Ophthalmol. Vis. Sci. 48 2007 18 26 (Pubitemid 47251381)
43. P. Csermely, T. Schnaider, C. Soti, Z. Prohaszka, and G. Nardai The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review Pharmacol. Ther. 79 1998 129 168 (Pubitemid 28380440)
44. S. Bellyei, A. Szigeti, A. Boronkai, E. Pozsgai, E. Gomori, B. Melegh, T. Janaky, Z. Bognar, E. Hocsak, B. Sumegi, and F. Gallyas Jr. Inhibition of cell death by a novel 16.2 kD heat shock protein predominantly via Hsp90 mediated lipid rafts stabilization and Akt activation pathway Apoptosis 12 2007 97 112 (Pubitemid 46009507)
45. S. Chen, D. Bawa, S. Besshoh, J.W. Gurd, and I.R. Brown Association of heat shock proteins and neuronal membrane components with lipid rafts from the rat brain J. Neurosci. Res. 81 2005 522 529 (Pubitemid 41297389)
46. D. Picard Heat-shock protein 90, a chaperone for folding and regulation Cell. Mol. Life Sci. 59 2002 1640 1648 (Pubitemid 35346967)
47. H. Schulze, T. Kolter, and K. Sandhoff Principles of lysosomal membrane degradation: cellular topology and biochemistry of lysosomal lipid degradation Biochim. Biophys. Acta 1793 2009 674 683
48. I. Vivanco, and C.L. Sawyers The phosphatidylinositol 3-kinase AKT pathway in human cancer Nat. Rev. Cancer 2 2002 489 501 (Pubitemid 37328931)
49. G.R. Ravacci, M.M. Brentani, T. Tortelli Jr., R.S. Torrinhas, T. Saldanha, E.A. Torres, and D.L. Waitzberg Lipid raft disruption by docosahexaenoic acid induces apoptosis in transformed human mammary luminal epithelial cells harboring HER-2 overexpression J. Nutr. Biochem. 24 2013 505 515
50. I.M. Berquin, I.J. Edwards, and Y.Q. Chen Multi-targeted therapy of cancer by omega-3 fatty acids Cancer Lett. 269 2008 363 377
51. P.D. Biondo, D.N. Brindley, M.B. Sawyer, and C.J. Field The potential for treatment with dietary long-chain polyunsaturated n-3 fatty acids during chemotherapy J. Nutr. Biochem. 19 2008 787 796
52. D.H. Jho, S.M. Cole, E.M. Lee, and N.J. Espat Role of omega-3 fatty acid supplementation in inflammation and malignancy Integr. Cancer Ther. 3 2004 98 111 (Pubitemid 38669043)
53. P.C. Calder n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases Am. J. Clin. Nutr. 83 2006 1505S 1519S (Pubitemid 44713092)
54. S.R. Shaikh, B.D. Rockett, M. Salameh, and K. Carraway Docosahexaenoic acid modifies the clustering and size of lipid rafts and the lateral organization and surface expression of MHC class I of EL4 cells J. Nutr. 139 2009 1632 1639
55. S.R. Wassall, and W. Stillwell Polyunsaturated fatty acid-cholesterol interactions: domain formation in membranes Biochim. Biophys. Acta 1788 2009 24 32
56. J.A. Williams, S.E. Batten, M. Harris, B.D. Rockett, S.R. Shaikh, W. Stillwell, and S.R. Wassall Docosahexaenoic and eicosapentaenoic acids segregate differently between raft and nonraft domains Biophys. J. 103 2012 228 237
57. S. Sebastian, J. Settleman, S.J. Reshkin, A. Azzariti, A. Bellizzi, and A. Paradiso The complexity of targeting EGFR signalling in cancer: from expression to turnover Biochim. Biophys. Acta 1766 2006 120 139 (Pubitemid 44175636)
58. S. Sigismund, T. Woelk, C. Puri, E. Maspero, C. Tacchetti, P. Transidico, P.P. Di Fiore, and S. Polo Clathrin-independent endocytosis of ubiquitinated cargos Proc. Natl. Acad. Sci. U. S. A. 102 2005 2760 2765 (Pubitemid 40299866)
59. H.F. Turk, R. Barhoumi, and R.S. Chapkin Alteration of EGFR spatiotemporal dynamics suppresses signal transduction PLoS One 7 2012 e39682
60. S.K. Wandinger, K. Richter, and J. Buchner The Hsp90 chaperone machinery J. Biol. Chem. 283 2008 18473 18477
61. L. Whitesell, and S.L. Lindquist HSP90 and the chaperoning of cancer Nat. Rev. Cancer 5 2005 761 772 (Pubitemid 41400776)
62. I. Hostein, D. Robertson, F. DiStefano, P. Workman, and P.A. Clarke Inhibition of signal transduction by the Hsp90 inhibitor 17-allylamino-17- demethoxygeldanamycin results in cytostasis and apoptosis Cancer Res. 61 2001 4003 4009 (Pubitemid 32720963)
63. I.A. Vasilevskaya, T.V. Rakitina, and P.J. O'Dwyer Geldanamycin and its 17-allylamino-17-demethoxy analogue antagonize the action of cisplatin in human colon adenocarcinoma cells: differential caspase activation as a basis for interaction Cancer Res. 63 2003 3241 3246 (Pubitemid 36735878)
64. M. Nomura, N. Nomura, E.W. Newcomb, Y. Lukyanov, C. Tamasdan, and D. Zagzag Geldanamycin induces mitotic catastrophe and subsequent apoptosis in human glioma cells J. Cell. Physiol. 201 2004 374 384 (Pubitemid 39453123)
65. W.G. An, T.W. Schulte, and L.M. Neckers The heat shock protein 90 antagonist geldanamycin alters chaperone association with p210bcr-abl and v-src proteins before their degradation by the proteasome Cell Growth Differ. 11 2000 355 360 (Pubitemid 30619563)
66. S.H. Oh, J.K. Woo, Y.D. Yazici, J.N. Myers, W.Y. Kim, Q. Jin, S.S. Hong, H.J. Park, Y.G. Suh, K.W. Kim, W.K. Hong, and H.Y. Lee Structural basis for depletion of heat shock protein 90 client proteins by deguelin J. Natl. Cancer Inst. 99 2007 949 961 (Pubitemid 47073501)
67. M. Osaki, M. Oshimura, and H. Ito PI3K-Akt pathway: its functions and alterations in human cancer Apoptosis 9 2004 667 676 (Pubitemid 40941196)
68. A.S. Clark, K. West, S. Streicher, and P.A. Dennis Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells Mol. Cancer Ther. 1 2002 707 717
69. C. Page, H.J. Lin, Y. Jin, V.P. Castle, G. Nunez, M. Huang, and J. Lin Overexpression of Akt/AKT can modulate chemotherapy-induced apoptosis Anticancer Res. 20 2000 407 416 (Pubitemid 30189787)
70. R. Lasserre, X.J. Guo, F. Conchonaud, Y. Hamon, O. Hawchar, A.M. Bernard, S.M. Soudja, P.F. Lenne, H. Rigneault, D. Olive, G. Bismuth, J.A. Nunes, B. Payrastre, D. Marguet, and H.T. He Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation Nat. Chem. Biol. 4 2008 538 547
71. L. Neckers Heat shock protein 90: the cancer chaperone J. Biosci. 32 2007 517 530 (Pubitemid 46708702)