Physical and chemical modulation of lipid rafts by a dietary n-3 polyunsaturated fatty acid increases ethanol-induced oxidative stress

Free Radical Biology and Medicine

Volumn 51, Issue 11, 2011, Pages 2018-2030

  Aliche Djoudi, Fatiha ^a   Podechard, Normand ^a   Chevanne, Martine ^a   Nourissat, Philippe ^a   Catheline, Daniel ^b   Legrand, Philippe ^b   Dimanche Boitrel, Marie Thérèse ^a   Lagadic Gossmann, Dominique ^a   Sergent, Odile ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

^b AGROCAMPUS OUEST   (France)

Author keywords

Eicosapentaenoic acid; Ethanol; Free radicals; Hepatocyte; Lipid raft; Liver; Low molecular weight iron; Lysosome; Membrane fluidity; Oxidative stress; Phospholipase C; Toxicity

Indexed keywords

ALCOHOL; CHOLESTEROL; EDIBLE OIL; ICOSAPENTAENOIC ACID; IRON; PHOSPHOLIPASE C GAMMA;

ANIMAL CELL; ARTICLE; CELL MEMBRANE FLUIDITY; CONTROLLED STUDY; LIPID RAFT; LIVER CELL; LYSOSOME; MODULATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT;

ANIMALS; CELL DEATH; CELLS, CULTURED; DIETARY FATS, UNSATURATED; EICOSAPENTAENOIC ACID; ETHANOL; HEPATOCYTES; MEMBRANE MICRODOMAINS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80255123296     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.08.031     Document Type: Article

References (55)

1. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1 2000 31 39
2. A.Y. Zhang, F. Yi, G. Zhang, E. Gulbins, and P.-L. Li Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells Hypertension 47 2006 74 80 (Pubitemid 43177818)
3. K. Hossain, A.A. Akhand, Y. Kawamoto, J. Du, K. Takeda, J. Wu, M. Yoshihara, H. Tsuboi, M. Kato, H. Suzuki, and I. Nakashima Caspase-activation is accelerated by the inhibition of arsenite-induced, membrane rafts-dependent Akt activation Free Radical Biol. Med. 34 2003 598 606 (Pubitemid 36254833)
4. R. Gniadecki, N. Christoffersen, and H.C. Wulf Cholesterol-rich plasma membrane domains (lipid rafts) in keratinocytes: importance in the baseline and UVA-induced generation of reactive oxygen species J. Invest. Dermatol. 118 2002 582 588 (Pubitemid 34309976)
5. L. Zuo, M. Ushio-Fukai, S. Ikeda, L. Hilenski, N. Patrushev, and R.W. Alexander Caveolin-1 is essential for activation of rac1 and NAD(P)H oxidase after angiotensin II type 1 receptor stimulation in vascular smooth muscle cells: role in redox signaling and vascular hypertrophy Arterioscler. Thromb. Vasc. Biol. 25 2005 1824 1830 (Pubitemid 41243449)
6. R. Reinehr, S. Becker, V. Keitel, A. Eberle, S. Grether-Beck, and D. Häussinger Bile salt-induced apoptosis involves NADPH oxidase isoform activation Gastroenterology 129 2005 2009 2031 (Pubitemid 41772977)
7. K.M. Boini, C. Zhang, M. Xia, W.Q. Han, C. Brimson, J.L. Poklis, and P.L. Li Visfatin-induced lipid raft redox signaling platforms and dysfunction in glomerular endothelial cells Biochim. Biophys. Acta 1801 2010 1294 1304
8. M. Zampagni, E. Evangelisti, R. Cascella, G. Liguri, M. Becatti, A. Pensalfini, D. Uberti, G. Cenini, M. Memo, S. Bagnoli, B. Nacmias, S. Sorbi, and C. Cecchi Lipid rafts are primary mediators of amyloid oxidative attack on plasma membrane J. Mol. Med. 88 2010 597 608
9. P. Nourissat, M. Travert, M. Chevanne, X. Tekpli, A. Rebillard, G. Le Moigne-Muller, M. Rissel, J. Cillard, M.-T. Dimanche-Boitrel, D. Lagadic-Gossmann, and O. Sergent Ethanol induces oxidative stress in primary rat hepatocytes through the early involvement of lipid raft clustering Hepatology 47 2008 59 70 (Pubitemid 351171042)
10. C. Zhang, and P.-L. Li Membrane raft redox signalosomes in endothelial cells Free. Radic. Res. 44 2010 831 842
11. Y.S. Tarahosky, E.N. Muzafarov, and Y.A. Kim Rafts making and rafts braking: how plant flavonoids may control membrane heterogeneity Mol. Cell. Biochem. 314 2008 65 71
12. S.R. Wassal, and W. Stillwell Polyunsaturated fatty-acid-cholesterol interactions: domain formation in membranes Biochim. Biophys. Acta 1788 2009 24 32
13. 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
14. 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)
15. Y.-Y. Fan, L.H. Ly, R. Barhoumi, D.N. McMurray, and R.S. Chapkin Dietary docosahexaenoic acid suppresses T cell protein kinase Cθ lipid raft recruitment and IL-2 production J. Immunol. 173 2004 6151 6160 (Pubitemid 39487772)
16. 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)
17. S.W. Wong, M.-J. Kwon, A.M.K. Choi, H.-P. Kim, K. Nakahira, and D.H. Hwang Fatty acids modulate toll-like receptor 4 activation through regulation of receptor dimerization and recruitment into lipid rafts in a reactive oxygen species-dependent manner J. Biol. Chem. 284 2009 27384 27392
18. 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)
19. D.W. Ma, J. Seo, L.A. Davidson, E.S. Callaway, Y.Y. Fan, J.R. Lupton, and R.S. Chapkin n-3 PUFA alter caveolae lipid composition and resident protein localization in mouse colon FASEB J. 18 2004 1040 1042 (Pubitemid 39561518)
20. O. Diaz, A. Berquand, M. Dubois, S. Di Agostino, C. Sette, S. Bourgoin, M. Lagarde, G. Némoz, and A.-F. Prigent The mechanism of docosahexaenoic acid-induced phospholipase D activation in human lymphocytes involves exclusion of the enzyme from lipid rafts J. Biol. Chem. 277 2002 39368 39378 (Pubitemid 35190910)
21. S.R. Shaikh, A.C. Dumaual, A. Castillo, D. LoCascio, R.A. Siddiqui, W. Stillwell, and S.R. Wassal Oleic and docosahexaenoic acid differentially phase separate from lipid raft molecules: a comparative NMR, DSC, AFM, and detergent extraction study Biophys. J. 87 2004 1752 1766 (Pubitemid 39167031)
22. R.S. Chapkin, N. Wang, Y.Y. Fan, J.R. Lupton, and I.A. Prior Docosahexaenoic acid alters the size and distribution of cell surface microdomains Biochim. Biophys. Acta 1778 2008 466 471
23. C. Guguen-Guillouzo, B. Clement, G. Baffet, C. Beaumont, E. Morel-Chany, D. Glaise, and A. Guillouzo Maintenance and reversibility of active albumin secretion by adult rat hepatocytes co-cultured with another liver epithelial cell type Exp. Cell Res. 143 1983 47 54 (Pubitemid 13145162)
24. V. Rioux, P. Lemarchal, and P. Legrand Myristic acid, unlike palmitic acid, is rapidly metabolized in cultured rat hepatocytes J. Nutr. Biochem. 11 2000 198 207 (Pubitemid 30301711)
25. O. Sergent, M. Pereira, C. Belhomme, M. Chevanne, L. Huc, and D. Lagadic-Gossmann Role for membrane fluidity in ethanol-induced oxidative stress of primary rat hepatocytes J. Pharmacol. Exp. Ther. 313 2005 104 111 (Pubitemid 40411333)
26. A. Gomes, E. Fernandes, and J.L.F.C. Lima Fluorescence probes used for detection of reactive oxygen species J. Biochem. Biophys. Methods 65 2005 45 80 (Pubitemid 41827578)
27. O. Sergent, J.-P. Anger, G. Lescoat, N. Pasdeloup, P. Cillard, and J. Cillard EPR determination of low molecular weight iron content applied to whole rat hepatocytes Cell. Mol. Biol. (Noisy-le-grand) 43 1997 793 800
28. D. Gilot, P. Loyer, A. Corlu, D. Glaise, D. Lagadic-Gossmann, A. Atfi, F. Morel, H. Ichijo, and C. Guguen-Guillouzo Liver protection from apoptosis requires both blockage of initiator caspase activities and inhibition of ASK1/JNK pathway via glutathione S-transferase regulation J. Biol. Chem. 277 2002 49220 49229 (Pubitemid 36014351)
29. E. Albano Oxidative mechanisms in the pathogenesis of alcoholic liver disease Mol. Aspects Med. 29 2008 9 16 (Pubitemid 351312214)
30. A.I. Cederbaum, Y. Lu, and D. Wu Role of oxidative stress in alcohol-induced liver injury Arch. Toxicol. 83 2009 519 548
31. F. Petrat, U. Rauen, and H. De Groot Determination of the chelatable iron pool of isolated rat hepatocytes by digital fluorescence microscopy using the fluorescent probe, phen green SK Hepatology 29 1999 1171 1179 (Pubitemid 29168752)
32. Z. Yu, H.L. Persson, J.W. Eaton, and U.T. Brunk Intralysosomal iron: a major determinant of oxidant-induced cell death Free Radical Biol. Med. 34 2003 1243 1252 (Pubitemid 36513967)
33. M. Morimoto, M.A. Zern, A.L. Hagbjork, M. Ingelman-Sundberg, and S.W. French Fish oil, alcohol, and liver pathology: role of cytochrome P450 2E1 Proc. Soc. Exp. Biol. Med. 207 1994 197 205 (Pubitemid 24323768)
34. A.A. Nanji Role of different fatty acids in the pathogenesis of experimental alcoholic liver disease Alcohol 34 2004 21 25
35. T.M. Donohue, T.V. Curry-McCoy, A.A. Nanji, K.K. Kharbanda, N.A. Osna, S.J. Radio, S.L. Todero, R.L. White, and C.A. Casey Lysosomal leakage and lack of adaptation of hepatoprotective enzyme contribute to enhanced susceptibility to ethanol-induced liver injury in female rats Alcohol. Clin. Exp. Res. 31 2007 1944 1952 (Pubitemid 47609649)
36. N. Nieto Ethanol and fish oil induce NFkappaB transactivation of the collagen alpha2(I) promoter through lipid peroxidation-driven activation of the PKC-PI3K-Akt pathway Hepatology 45 2007 1433 1445 (Pubitemid 46918327)
37. S.R. Wassal, M.R. Brzustowicz, S.R. Shaikh, V. Cherezov, M. Caffrey, and W. Stillwell Order from disorder, corralling cholesterol with chaotic lipids: the role of polyunsaturated lipids in membrane raft formation Chem. Phys. Lipids 132 2004 79 88 (Pubitemid 39458322)
38. J. Atkinson, T. Harroun, S.R. Wassal, W. Stillwell, and J. Katsaras The location and behavior of alpha-tocopherol in membranes Mol. Nutr. Food Res. 54 2010 641 651
39. A. Colell, C. Garcia-Ruiz, A. Morales, A. Ballestta, M. Ookhtens, J. Rodés, N. Kaplowitz, and J.C. Fernandez-Checa Transport of reduced glutathione in hepatic mitochondria and mitoplasts from ethanol-treated rats: effect of membrane physical properties and S-adenosyl-L-methionine Hepatology 26 1997 699 708 (Pubitemid 27392362)
40. J.M. Lluis, A. Colell, C. Garcia-Ruiz, N. Kaplowitz, and J.C. Fernandez-Checa Acetaldehyde impairs mitochondrial glutathione transport in HepG2 cells through endoplasmic reticulum stress Gastroenterology 124 2003 708 724 (Pubitemid 36268490)
41. O. Coll, A. Colell, C. Garcia-Ruiz, N. Kaplowitz, and J.C. Fernandez-Checa Sensitivity of the 2-oxoglutarate carrier to alcohol intake contributes to mitochondrial glutathione depletion Hepatology 38 2003 692 702 (Pubitemid 37052156)
42. A. Colell, O. Coll, C. Garcia-Ruiz, R. Paris, C. Tiribelli, N. Kaplowitz, and J.C. Fernandez-Checa Tauroursodeoxycholic acid protects hepatocytes from ethanol-fed rats against tumor necrosis factor-induced cell death by replenishing mitochondrial glutathione Hepatology 34 2001 964 971 (Pubitemid 33032031)
43. A. Colquhoun Mechanisms of action of eicosapentaenoic acid in bladder cancer cells in vitro: alterations in mitochondrial metabolism, reactive oxygen species generation and apoptosis induction J. Urol. 181 2009 1885 1893
44. T. Kurz, A. Terman, B. Gustaffsson, and U.T. Brunk Lysosomes and oxidative stress in aging and apoptosis Biochim. Biophys. Acta 1780 2008 1291 1303
45. W.-X. Ding, M. Li, X. Chen, H.-M. Ni, C.-W. Lin, W. Gao, B. Lu, D.B. Stolz, D.L. Clemens, and X.M. Yin Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice Gastroenterology 139 2010 1740 1752
46. 2 is a consequence of lysosomal rupture Biochem. J. 356 2001 549 555 (Pubitemid 32532368)
47. T. Kurz, B. Gustafsson, and U.T. Brunk Intralysosomal iron chelation protects against oxidative stress-induced cellular damage FEBS J. 273 2006 3106 3117
48. A. Torriglia, C. Leprêtre, L. Padron-Barthe, S. Chahory, and E. Martin Molecular mechanism of L-DNase II activation and function as a molecular switch in apoptosis Biochem. Pharmacol. 76 2008 1490 1502
49. J.Y. Brossas, R. Tanguy, F. Brignole-Baudouin, Y. Courtois, A. Torriglia, and J. Treton L-DNase II associated with active process during ethanol induced cell death in ARPE-19 Mol. Vis. 10 2004 65 72
50. R. Autelli, S. Crepaldi, D. De Stefanis, M. Parola, G. Bonelli, and F.M. Baccino Intracellular free iron and acidic pathways mediate TNF-induced death of rat hepatoma cells Apoptosis 10 2005 777 786 (Pubitemid 41187076)
51. P.G. Arthur, X. Niu, P. Rigby, J.H. Steer, and G.P. Jeffrey Oxidative stress causes a decline in lysosomal integrity during hypothermic incubation of rat hepatocytes Free Radical Biol. Med. 44 2008 24 33 (Pubitemid 350138625)
52. H.L. Persson Iron-dependent lysosomal destabilization initiates silica-induced apoptosis in murine macrophages Toxicol. Lett. 159 2005 124 133 (Pubitemid 41330931)
53. J.L. Chen, H.H. Lin, K.J. Kim, A. Lin, H.J. Forman, and D.K. Ann Novel roles for protein kinase C delta-dependent signaling pathways in acute hypoxic stress-induced autophagy J. Biol. Chem. 283 2008 34432 34444
54. 2+ increase Cell. Signalling 22 2010 914 925
55. P. Yaqoob The nutritional significance of lipid rafts Annu. Rev. Nutr. 29 2009 257 282