α-Tocopherol impairs 7-ketocholesterol-induced caspase-3-dependent apoptosis involving GSK-3 activation and Mcl-1 degradation on 158N murine oligodendrocytes

Chemistry and Physics of Lipids

Volumn 164, Issue 6, 2011, Pages 469-478

  Ragot, Kévin ^a   Delmas, Dominique ^a   Athias, Anne ^b   Nury, Thomas ^a   Baarine, Mauhamad ^a   Lizard, Gérard ^a,c  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b HÔPITAL DU BOCAGE   (France)

^c Chu   (France)

Author keywords

Tocopherol; 158N murine oligodendrocytes; 7 Ketocholesterol; Akt; Apoptosis; GSK3; Lipid rafts; Mcl 1

Indexed keywords

7 OXOCHOLESTEROL; ALPHA TOCOPHEROL; CASPASE 3; DNA; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; PROTEIN MCL 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL LINE; CELL MEMBRANE DEPOLARIZATION; CELL NUCLEUS; CONTROLLED STUDY; DEPHOSPHORYLATION; DNA FRAGMENTATION; ENZYME ACTIVATION; ENZYME ACTIVITY; MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ALPHA-TOCOPHEROL; ANIMALS; APOPTOSIS; CASPASE 3; CELL PROLIFERATION; CELL SURVIVAL; CYTOCHROMES C; ENZYME ACTIVATION; GLYCOGEN SYNTHASE KINASE 3; KETOCHOLESTEROLS; MEMBRANE MICRODOMAINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; OLIGODENDROGLIA; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; TIME FACTORS;

MURINAE;

EID: 80051472674     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2011.04.014     Document Type: Article

References (68)

1. P.B. Addis, H.A. Emanuel, S.D. Bergmann, and J.H. Zavoral Capillary GC quantification of cholesterol oxidation products in plasma lipoproteins of fasted humans Free Radic. Biol. Med. 7 1989 179 182 (Pubitemid 19220717)
2. C. Akgul Mcl-1 is a potential therapeutic target in multiple types of cancer Cell. Mol. Life Sci. 66 2009 1326 1336
3. N. Arbour, J.L. Vanderluit, J.N. Le Grand, A. Jahani-Asl, V.A. Ruzhynsky, E.C. Cheung, M.A. Kelly, A.E. MacKenzie, D.S. Park, J.T. Opferman, and R.S. Slack Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage J. Neurosci. 28 2008 6068 6078
4. M. Arca, S. Natoli, F. Micheletta, S. Riggi, E. Di Angelantonio, A. Montali, T.M. Antonini, R. Antonini, U. Diczfalusy, and L. Iuliano Increased plasma levels of oxysterols, in vivo markers of oxidative stress, in patients with familial combined hyperlipidemia: reduction during atorvastatin and fenofibrate therapy Free Radic. Biol. Med. 42 2007 698 705 (Pubitemid 46205153)
5. M. Baarine, K. Ragot, E.C. Genin, H. El Hajj, D. Trompier, P. Andreoletti, M.S. Ghandour, F. Menetrier, M. Cherkaoui-Malki, S. Savary, and G. Lizard Peroxisomal and mitochondrial status of two murine oligodendrocytic cell lines (158N, 158JP): potential models for the study of peroxisomal disorders associated with dysmyelination processes J. Neurochem. 111 2009 119 131
6. M. Baarine, 2010. Etude des activités cytotoxiques et pro-oxydantes d'acides gras trs longue chaîne (AGTLC) sur des oligodendrocytes murins sauvages et déficients en Abcd1 et Acox1: application la physiopathologie de l'X-ALD et de la P-NALD. PhD Thesis, University of Burgundy, Dijon, France.
7. M.H. Barnett, and J.W. Prineas Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion Ann. Neurol. 55 2004 458 468 (Pubitemid 38391962)
8. N. Baumann, and D. Pham-Dinh Biology of oligodendrocyte and myelin in the mammalian central nervous system Physiol. Rev. 81 2001 871 927 (Pubitemid 32267079)
9. E. Bedner, P. Smolewski, P. Amstad, and Z. Darzynkiewicz Activation of caspases measured in situ by binding of fluorochrome-labeled inhibitors of caspases (FLICA): Correlation with DNA fragmentation Exp. Cell Res. 259 2000 308 313
10. E. Beurel, and R.S. Jope The paradoxical pro- and anti-apoptotic actions of GSK3 in the intrinsic and extrinsic apoptosis signaling pathways Prog. Neurobiol. 79 2006 173 189 (Pubitemid 44331500)
11. I. Björkhem, A. Cedazo-Minguez, V. Leoni, and S. Meaney Oxysterols and neurodegenerative diseases Mol. Aspects Med. 30 2009 171 179
12. I. Björkhem, M. Heverin, V. Leoni, S. Meaney, and U. Diczfalusy Oxysterols and Alzheimer's disease Acta Neurol. Scand. Suppl. 185 2006 43 49 (Pubitemid 44015224)
13. I. Björkhem, and S. Meaney Brain cholesterol: long secret life behind a barrier Arterioscler. Thromb. Vasc. Biol. 24 2004 806 815 (Pubitemid 38620856)
14. I. Björkhem Crossing the barrier: oxysterols as cholesterol transporters and metabolic modulators in the brain J. Intern. Med. 260 2006 493 508 (Pubitemid 44772369)
15. I. Björkhem Rediscovery of cerebrosterol Lipids 42 2007 5 14 (Pubitemid 46490739)
16. R. Brigelius-Flohé Vitamin E: the shrew waiting to be tamed Free Radic. Biol. Med. 46 2009 543 554
17. A. Brunet, S.R. Datta, and M.E. Greenberg Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway Curr. Opin. Neurobiol. 11 2001 297 305 (Pubitemid 32524094)
18. K.A. Burns, and J.P. Vanden Heuvel Modulation of PPAR activity via phosphorylation Biochim. Biophys. Acta 1771 2007 952 960 (Pubitemid 47198547)
19. G.M. Cohen Caspases: the executioners of apoptosis Biochem. J. 326 Pt 1 1997 1 16 (Pubitemid 27386911)
20. P. Cohen, and M. Goedert GSK3 inhibitors: development and therapeutic potential Nat. Rev. 3 2004 479 487 (Pubitemid 38807530)
21. R.W. Craig MCL1 provides a window on the role of the BCL2 family in cell proliferation, differentiation and tumorigenesis Leukemia 16 2002 444 454 (Pubitemid 34449724)
22. A. De Laurentiis, L. Donovan, and A. Arcaro Lipid rafts and caveolae in signaling by growth factor receptors Open Biochem. J. 1 2007 12 32
23. H.A. Emanuel, C.A. Hassel, P.B. Addis, S.D. Bergmann, and J.H. Zavoral Plasma cholesterol oxidation products in human subjects fed a meal rich in oxysterols J. Food Sci. 56 1991 843 847
24. S.R. Farmer Regulation of PPAR gamma activity during adipogenesis Int. J. Obes. 29 Suppl. 1 2005 S13 16
25. A.C. Feutz, D. Pham-Dinh, B. Allinquant, M. Miehe, and M.S. Ghandour An immortalized jimpy oligodendrocyte cell line: defects in cell cycle and cAMP pathway Glia 34 2001 241 252 (Pubitemid 32579447)
26. J. Grabarek, L. Du, G.L. Johnson, B.W. Lee, D.J. Phelps, and Z. Darzynkiewicz Sequential activation of caspases and serine proteases (serpases) during apoptosis Cell Cycle 1 2002 124 131
27. D.K. Hartline What is myelin? Neuron Glia Biol. 4 2008 153 163
28. E.M. Hur, and F.Q. Zhou GSK3 signalling in neural development Nat. Rev. Neurosci. 11 2010 539 551
29. L. Iuliano, F. Micheletta, S. Natoli, S. Ginanni Corradini, M. Iappelli, W. Elisei, L. Giovannelli, F. Violi, and U. Diczfalusy Measurement of oxysterols and alpha-tocopherol in plasma and tissue samples as indices of oxidant stress status Anal. Biochem. 312 2003 217 223 (Pubitemid 36151134)
30. Iuliano, L., Monticolo, R., Straface, G., Spoletini, I., Gianni, W., Caltagirone, C., Boss, P., Spalletta, G., 2010. Vitamin E and enzymatic/oxidative stress-driven oxysterols in amnestic mild cognitive impairment subtypes and Alzheimer's disease. J. Alzheimers Dis. (PMID: 20693621), 21, 1383-1392.
31. R.S. Jope, and M.S. Roh Glycogen synthase kinase-3 (GSK3) in psychiatric diseases and therapeutic interventions Curr. Drug Targets 7 2006 1421 1434 (Pubitemid 44718302)
32. E. Kahn, M. Baarine, A. Dauphin, K. Ragot, N. Tissot, A. Seguin, F. Ménétrier, Z. Kattan, C.M. Bachelet, F. Frouin, and G. Lizard Lipid membrane organization during 7-ketocholesterol and very long chain fatty acid induced cell death on murine oligodendrocytes characterized by LAURDAN color shift, mono- and bi-photon spectral imaging confocal microscopy and Factor Analysis of Medical Image Sequences (FAMIS) Cytometry A 79 2011 293 305
33. M.H. Kang, and C.P. Reynolds Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy Clin. Cancer Res. 15 2009 1126 1132
34. S. Kemp, and R. Wanders Biochemical aspects of X-linked adrenoleukodystrophy Brain Pathol. 20 2010 831 837
35. H. Kölsch, R. Heun, F. Jessen, J. Popp, F. Hentschel, W. Maier, and D. Lütjohann Alterations of cholesterol precursor levels in Alzheimer's disease Biochim. Biophys. Acta 1801 2010 945 950
36. H. Larsson, Y. Böttiger, L. Iuliano, and U. Diczfalusy In vivo interconversion of 7beta-hydroxycholesterol and 7-ketocholesterol, potential surrogate markers for oxidative stress Free Radic. Biol. Med. 43 2007 695 701 (Pubitemid 47102124)
37. V. Leoni, D. Lütjohann, and T. Masterman Levels of 7-oxocholesterol in cerebrospinal fluid are more than one thousand times lower than reported in multiple sclerosis J. Lipid Res. 46 2005 191 195 (Pubitemid 40271081)
38. V. Leoni, T. Masterman, F.S. Mousavi, B. Wretlind, L.O. Wahlund, U. Diczfalusy, J. Hillert, and I. Björkhem Diagnostic use of cerebral and extracerebral oxysterols Clin. Chem. Lab. Med. 42 2004 186 191 (Pubitemid 38401447)
39. V. Leoni, T. Masterman, P. Patel, S. Meaney, U. Diczfalusy, and I. Björkhem Side chain oxidized oxysterols in cerebrospinal fluid and the integrity of blood-brain and blood-cerebrospinal fluid barriers J. Lipid Res. 44 2003 793 799 (Pubitemid 37279681)
40. D.C. Liebler, J.A. Burr, L. Philips, and A.J. Ham Gas chromatography-mass spectrometry analysis of vitamin E and its oxidation products Anal. Biochem. 236 1996 27 34 (Pubitemid 26103104)
41. G. Lizard, V. Deckert, L. Dubrez, M. Moisant, P. Gambert, and L. Lagrost Induction of apoptosis in endothelial cells treated with cholesterol oxides Am. J. Pathol. 148 1996 1625 1638 (Pubitemid 26135902)
42. G. Lizard, S. Fournel, L. Genestier, N. Dhedin, C. Chaput, M. Flacher, M. Mutin, G. Panaye, and J.P. Revillard Kinetics of plasma membrane and mitochondrial alterations in cells undergoing apoptosis Cytometry 21 1995 275 283
43. G. Lizard, S. Gueldry, O. Sordet, S. Monier, A. Athias, C. Miguet, G. Bessede, S. Lemaire, E. Solary, and P. Gambert Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production FASEB J. 12 1998 1651 1663 (Pubitemid 28553660)
44. G. Lizard, C. Miguet, G. Besséde, S. Monier, S. Gueldry, D. Neel, and P. Gambert Impairment with various antioxidants of the loss of mitochondrial transmembrane potential and of the cytosolic release of cytochrome c occurring during 7-ketocholesterol-induced apoptosis Free Radic. Biol. Med. 28 2000 743 753 (Pubitemid 30171288)
45. S. Lordan, J.J. Mackrill, and N.M. O'Brien Oxysterols and mechanisms of apoptotic signaling: implications in the pathology of degenerative diseases J. Nutr. Biochem. 20 2009 321 336
46. F. Micheletta, S. Natoli, M. Misuraca, E. Sbarigia, U. Diczfalusy, and L. Iuliano Vitamin E supplementation in patients with carotid atherosclerosis: reversal of altered oxidative stress status in plasma but not in plaque Arterioscler. Thromb. Vasc. Biol. 24 2004 136 140 (Pubitemid 38082424)
47. C. Miguet, S. Monier, A. Bettaieb, A. Athias, G. Besséde, A. Laubriet, S. Lemaire, D. Néel, P. Gambert, and G. Lizard Ceramide generation occurring during 7 beta-hydroxycholesterol- and 7-ketocholesterol- induced apoptosis is caspase independent and is not required to trigger cell death Cell Death Differ. 8 2001 83 99 (Pubitemid 32162224)
48. F. Natella, A. Macone, A. Ramberti, M. Forte, F. Mattivi, R.M. Matarese, and C. Scaccini Red wine prevents the postprandial increase in plasma cholesterol oxidation products: a pilot study Br. J. Nutr. 4 2011 1 6
49. A. Petit-Paitel GSK-3beta: a central kinase for neurodegenerative diseases? Med. Sci. (Paris) 26 2010 516 521
50. P. Polychronopoulos, P. Magiatis, A.L. Skaltsounis, V. Myrianthopoulos, E. Mikros, A. Tarricone, A. Musacchio, S.M. Roe, L. Pearl, M. Leost, P. Greengard, and L. Meijer Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases J. Med. Chem. 47 2004 935 946 (Pubitemid 38176796)
51. F.D. Porter, D.E. Scherrer, M.H. Lanier, S.J. Langmade, V. Molugu, S.E. Gale, D. Olzeski, R. Sidhu, D.J. Dietzen, R. Fu, C.A. Wassif, N.M. Yanjanin, S.P. Marso, J. House, C. Vite, J.E. Schaffer, and D.S. Ory Cholesterol oxidation products are sensitive and specific blood-based biomarkers for Niemann-Pick C1 disease Sci. Transl. Med. 2 2010 56ra81
52. C. Prunet, T. Montange, A. Véjux, A. Laubriet, J.F. Rohmer, J.M. Riedinger, A. Athias, S. Lemaire-Ewing, D. Néel, J.M. Petit, E. Steinmetz, R. Brenot, P. Gambert, and G. Lizard Multiplexed flow cytometric analyses of pro- and anti-inflammatory cytokines in the culture media of oxysterol-treated human monocytic cells and in the sera of atherosclerotic patients Cytometry A 69 2006 359 373 (Pubitemid 44651349)
53. V. Riendeau, and C. Garenc Effect of 27-hydroxycholesterol on survival and death of human macrophages and vascular smooth muscle cells Free Radic. Res. 43 2009 1019 1028
54. I.R. Rodríguez, and I.M. Larrayoz Cholesterol oxidation in the retina: implications of 7KCh formation in chronic inflammation and age-related macular degeneration J. Lipid Res. 51 2010 2847 2862
55. M.C. Royer, S. Lemaire-Ewing, C. Desrumaux, S. Monier, J.P. Pais de Barros, A. Athias, D. Néel, and L. Lagrost 7-Ketocholesterol incorporation into sphingolipid/cholesterol-enriched (lipid raft) domains is impaired by vitamin E: a specific role for alpha-tocopherol with consequences on cell death J. Biol. Chem. 284 2009 15826 15834
56. E.M. Sale, and G.J. Sale Protein kinase B: signalling roles and therapeutic targeting Cell. Mol. Life Sci. 65 2008 113 127 (Pubitemid 351152227)
57. M.B. Shah, and P.B. Sehgal Nondetergent isolation of rafts Methods Mol. Biol. 398 2007 21 28
58. E.H. Shroff, C. Snyder, and N.S. Chandel Role of Bcl-2 family members in anoxia induced cell death Cell Cycle 6 2007 807 809 (Pubitemid 46572619)
59. I. Singh, and A. Pujol Pathomechanisms underlying X-adrenoleukodystrophy: a three-hit hypothesis Brain Pathol. 20 2010 838 844
60. S.T. Smiley, M. Reers, C. Mottola-Hartshorn, M. Lin, A. Chen, T.W. Smith, G.D. Steele Jr., and L.B. Chen Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1 Proc. Natl. Acad. Sci. U.S.A. 88 1991 3671 3675 (Pubitemid 21916685)
61. P.H. Sugden, S.J. Fuller, S.C. Weiss, and A. Clerk Glycogen synthase kinase 3 (GSK3) in the heart: a point of integration in hypertrophic signalling and a therapeutic target? A critical analysis Br. J. Pharmacol. 153 Suppl. 1 2008 S137 S153
62. D.M. Van Reyk, A.J. Brown, L.M. Hult'en, R.T. Dean, and W. Jessup Oxysterols in biological systems: sources, metabolism and pathophysiological relevance Redox Rep. 11 2006 255 262 (Pubitemid 46062350)
63. J. Vaya, and H.M. Schipper Oxysterols, cholesterol homeostasis, and Alzheimer disease J. Neurochem. 102 2007 1727 1737 (Pubitemid 47329280)
64. A. Vejux, S. Guyot, T. Montange, J.M. Riedinger, E. Kahn, and G. Lizard Phospholipidosis and down-regulation of the PI3-K/PDK-1/Akt signalling pathway are vitamin E inhibitable events associated with 7-ketocholesterol-induced apoptosis J. Nutr. Biochem. 20 2009 45 61
65. A. Vejux, and G. Lizard Cytotoxic effects of oxysterols associated with human diseases: induction of cell death (apoptosis and/or oncosis), oxidative and inflammatory activities, and phospholipidosis Mol. Aspects Med. 30 2009 153 170
66. A. Vejux, L. Malvitte, and G. Lizard Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis Braz. J. Med. Biol. Res. 41 2008 545 556
67. K. Wide, H. Larsson, L. Bertilsson, and U. Diczfalusy Time course of the increase in 4beta-hydroxycholesterol concentration during carbamazepine treatment of paediatric patients with epilepsy Br. J. Clin. Pharmacol. 65 2008 708 715 (Pubitemid 351535081)
68. C.G. Yeh, B. His, and W.P. Faulk Propidium iodide as a nuclear marker in immunofluorescence. II. Use with cellular identification and viability studies J. Immunol. Methods 43 1981 269 275 (Pubitemid 11126341)