Phospholipidosis and down-regulation of the PI3-K/PDK-1/Akt signalling pathway are vitamin E inhibitable events associated with 7-ketocholesterol-induced apoptosis

Journal of Nutritional Biochemistry

Volumn 20, Issue 1, 2009, Pages 45-61

  Vejux, Anne ^a   Guyot, Stéphane ^c   Montange, Thomas ^a,b   Riedinger, Jean Marc ^d   Kahn, Edmond ^e   Lizard, Gérard ^a,b  

^a Chu   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d Centre Anti Cancer GF Leclerc   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

7 ketocholesterol; Akt; Phospholipidosis; PI3 K; Vitamin E

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 3 METHYLADENINE; 7 OXOCHOLESTEROL; ALPHA TOCOPHEROL; MEROCYANINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PROTEIN KINASE B;

ANISOTROPY; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL INCLUSION; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LIPID STORAGE; LIPIDOSIS; MEMBRANE FLUIDITY; PROTEIN PHOSPHORYLATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; BENZIMIDAZOLES; DOWN-REGULATION; HUMANS; KETOCHOLESTEROLS; MICROSCOPY, ELECTRON, TRANSMISSION; OXAZINES; PHOSPHOLIPIDS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PYRIMIDINONES; SIGNAL TRANSDUCTION; U937 CELLS; VITAMIN E;

EID: 57049189735     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2007.12.001     Document Type: Article

References (77)

1. Smith L. Review of progress in sterol oxidations: 1987-1995. Lipids 31 (1996) 453-457
2. Colles S.M., Maxson J.M., Carlson S.G., and Chilsolm G.M. Oxidized LDL-induced injury and apoptosis in atherosclerosis. Trends Cardiovasc Med 11 (2001) 131-138
3. Schroepfer G.J. Oxysterols: modulators of cholesterol metabolism and other processes. Physiol Rev 80 (2000) 361-554
4. Diczfalusy U. Analysis of cholesterol oxidation products in biological samples. J AOAC Int 87 (2004) 467-473
5. Lemaire-Ewing S., Prunet C., Montange T., Vejux A., Berthier A., Bessède G., et al. Comparison of the cytotoxic, pro-oxidant and pro-inflammatory characteristics of different oxysterols. Cell Biol Toxicol 21 (2005) 97-114
6. Prunet C., Montange T., Véjux A., Laubriet A., Rohmer J.F., Riedinger J.M., et al. 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
7. Tedgui A., and Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86 (2006) 515-581
8. Vejux A., Kahn E., Ménétrier F., Montange T., Lherminier J., Riedinger J.M., et al. Cytotoxic oxysterols induce caspase-independent myelin figure formation and caspase-dependent polar lipid accumulation. Histochem Cell Biol 127 (2007) 609-624
9. Kahn E., Vejux A., Lizard G., Bessède G., Frouin F., Prunet C., et al. Analysis of the fluorescence of monodansylcadaverine-positive cytoplasmic structures during 7-ketocholesterol-induced cell death. Anal Quant Cytol Histol 26 (2004) 47-56
10. Hariri M., Millane G., Guimond M.P., Guay G., Dennis J.W., and Nabi I.R. Biogenesis of multilamellar bodies via autophagy. Mol Biol Cell 11 (2000) 255-268
11. Miguet-Alfonsi C., Prunet C., Monier S., Bessède G., Lemaire-Ewing S., Berthier A., et al. Analysis of oxidative processes and of myelin figure formation before and after the loss of mitochondrial potential during 7b-hydroxycholesterol and 7-ketocholesterol-induced apoptosis: comparison with various pro-apoptotic chemicals. Biochem Pharmacol 64 (2002) 527-541
12. Martinet W., De Bie M., Schrijvers D.M., De Meyer G.R., Herman A.G., and Kockx M.M. 7-ketocholesterol induces protein ubiquitination, myelin figure formation, and light chain 3 processing in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24 (2004) 2296-2301
13. Bauvy C., Gane P., Arico S., Codogno P., and Ogier-Denis E. Autophagy delays sulindac sulfide-induced apoptosis in the human intestinal colon cancer cell line HT-29. Exp Cell Res 268 (2001) 139-149
14. Petiot A., Ogier-Denis E., Blommaart E.F., Meijer A.J., and Codogno P. Distinct classes of phosphatidylinositol 3¢-kinases are involved in signaling pathways that control macro-autophagy in HT-29 cells. J Biol Chem 275 (2000) 992-998
15. Datta S.R., Brunet A., and Greenberg M.E. Cellular survival: a play in three Akts. Gene Dev 13 (1999) 2905-2927
16. Neri L.M., Borgatti P., Capitani S., and Martelli A.M. The nuclear phosphoinositide 3-kinase/Akt pathway: a new second messenger system. Biochim Biophys Acta 1584 (2002) 73-80
17. Berthier A., Lemaire-Ewing S., Prunet C., Monier S., Athias A., Bessède G., et al. Involvement of a calcium-dependent dephosphorylation of BAD associated with the localization of Trpc-1 within lipid rafts in 7-ketocholesterol-induced THP-1 cell apoptosis. Cell Death Differ 11 (2004) 897-905
18. Lizard G., Miguet C., Bessède G., Monier S., Gueldry S., Néel D., et al. 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
19. Rusinol A.E., Thewke D., Liu J., Freeman N., Panini S.R., and Sinensky M.S. AKT/protein kinase B regulation of BCL family members during oxysterol-induced apoptosis. J Biol Chem 279 (2004) 1392-1399
20. Reasor M.J., and Kacew S. Drug-induced phospholipidosis: are there functional consequences?. Exp Biol Med 226 (2001) 825-830
21. Anderson N., and Borlak J. Drug-induced phospholipidosis. FEBS Lett 580 (2006) 5533-5540
22. Blommaart E.F.C., Luiken J.J.F.P., and Meijer A.J. Autophagic proteolysis: control and specificity. Histochem J 29 (1997) 365-385
23. Grabarek J., Amstad P., and Darzynkiewicz Z. Use of fluorescently labeled caspase inhibitors as affinity labels to detect activated caspases. Hum Cell 15 (2002) 1-12
24. Vejux A., Lizard G., Tourneur Y., Riedinger J.M., Frouin F., and Kahn E. Effects of caspase inhibitors (z-VAD-fmk, z-VDVAD-fmk) on Nile Red fluorescence pattern in 7-ketocholesterol-treated cells: investigation by flow cytometry and spectral imaging microscopy. Cytometry A 71 (2007) 550-562
25. Lizard G., Fournel S., Genestier L., Dhedin N., Chaput C., Flacher M., et al. Kinetics of plasma membrane and mitochondrial alterations in cells undergoing apoptosis. Cytometry 21 (1995) 275-283
26. Biederbick A., Kern H.F., and Elsässer H.P. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66 (1995) 3-14
27. Klinkner A.M., Bugelski P.J., Waites R., Louden C., Hart T.K., and Kerns W.D. A novel technique for mapping the lipid composition of atherosclerotic fatty streaks by en face fluorescence microscopy. J Histochem Cytochem 45 (1997) 743-753
28. Vejux A., Kahn E., Dumas D., Bessède G., Ménétrier F., Athias A., et al. 7-Ketocholesterol favors lipid accumulation and colocalizes with Nile Red positive cytoplasmic structures formed during 7-ketocholesterol-induced apoptosis: analysis by flow cytometry, FRET biphoton spectral imaging microscopy, and subcellular fractionation. Cytometry A 64 (2005) 87-100
29. Schlegel R.A., Stevens M., Lumley-Sapanski K., and Williamson P. Altered lipid packing identifies apoptotic cells. Immunol Lett 36 (1993) 283-288
30. Laakko T., King L., and Fraker P. Versatility of merocyanine 540 for the flow cytometric detection of apoptosis in human and murine cells. J Immunol Methods 61 (2002) 129-139
31. Ball R.Y., Carpenter K.L.H., and Mitchinson M.J. Ceroid accumulation by murine peritoneal macrophages exposed to artificial lipoproteins: ultrastructural observations. Br J Exp Pathol 69 (1988) 43-56
32. Harman D. Lipofuscin and ceroid formation: the cellular recycling system. In: Porta E.A. (Ed). Lipofuscin and Ceroid Pigments (1990), Plenum Press, New York 3-15
33. Olsson G.M., Rungby J., Rundquist I., and Brunk U.T. Evaluation of lysosomal stability in living culture macrophages by cytofluorometry. Effect of silver lactate and hypotonic solutions. Virchows Arch - B: Cell Pathol 56 (1989) 263-269
34. Yuan X.M., Li W., Brunk U.T., Dalen H., Chang Y.H., and Sevanian A. Lysosomal destabilisation during macrophage damage induced by cholesterol oxidation products. Free Radic Biol Med 28 (2000) 208-218
35. Van Ginkel G., van Langen H., and Levine Y.K. The membrane fluidity concept revised by polarized fluorescence spectroscopy on different models membranes containing unsaturated lipids and sterols. Biochimie 71 (1989) 23-32
36. Folch J., Lees M., and Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226 (1957) 497-509
37. Becart I., Chevalier C., and Biesse J.P. Quantitative analysis of phospholipids by HPLC with a light scattering evaporating detector: application to raw materials for cosmetic use. J High Resolut Chromatogr 13 (1990) 126-129
38. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of protein using bicinchoninic acid. Anal Biochem 150 (1985) 76-85
39. Györkey F., Shimamura T., and O'Neal R. The fine structure of ceroid in human atheroma. J Histochem Cytochem 15 (1968) 732-736
40. Kroemer G., Petit P., Zamzami N., Vayssière J.L., and Mignotte B. The biochemistry of programmed cell death. FASEB J 9 (1995) 1277-1287
41. Shore N.L., Zilversmit D.B., and Ackerman R.F. Plasma phospholipid deposition in human serum and atherosclerotic lesions. Am J Physiol 181 (1995) 527-531
42. Kummerow F.A., Cook L.S., Wasowicz E., and Jelen H. Changes in the phospholipid composition of the arterial cell can result in severe atherosclerotic lesions. J Nutr Biochem 12 (2001) 602-607
43. Bron D., and Amis R. Vitamin E and the prevention of atherosclerosis. Int J Vitam Nutr Res 71 (2001) 18-24
44. Kahn E., Lizard G., Frouin F., Bernengo J.C., Souchier C., Bessède G., et al. Confocal analysis of phosphatidylserine externalization with the use of biotinylated annexin V revealed with streptavidin FITC, -europium, -phycoerythrin or -Texas Red in oxysterol-treated apoptotic cells. Anal Quant Cytol Histol 23 (2001) 47-55
45. Stanley D.W. Biological membrane deterioration and associated quality losses in food tissues. Crit Rev Food Sci Nutr 30 (1991) 487-6053
46. Chapman D. Phase transitions and fluidity characteristics of lipids and cell membranes. Q Rev Biophys 8 (1975) 185-235
47. Mely-Goubert B., and Freedman M.H. Lipid fluidity and membrane protein monitoring using 1,6-diphenyl-1,3,5-hexatriene. Biochim Biophys Acta 601 (1980) 315-327
48. Arico S., Petiot A., Bauvy C., Dubbelhuis P.F., Meijer A.J., Codogno P., et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem 276 (2001) 35243-35246
49. Uddin S., Hussain A.R., Al-Hussein K.A., Manogaran P., Wickrema A., Gutierriez M.I., et al. Inhibition of phosphatidylinositol 3¢-kinase/AKT signaling promotes apoptosis of primary effusion lymphoma cells. Clin Cancer Res 11 (2005) 3102-3108
50. Prunet C., Lemaire-Ewing S., Ménétrier F., Néel D., and Lizard G. Activation of caspase-3 dependent and independent pathways during 7-ketocholesterol- and 7b-hydroxycholesterol-induced cell death: a morphological and biochemical study. J Biochem Mol Toxicol 19 (2005) 311-326
51. Emanuel H.A., Hassel C.A., Addis P.B., Bergmann S.D., and Zavoral J.H. Plasma cholesterol oxidation products (oxysterols) in human subjects fed a meal rich in oxysterols. J Food Sci 56 (1991) 843-847
52. Vine F., Mamo J.C.L., Beilin L.J., Mori T.A., and Croft K.D. Dietary oxysterols are involved in plasma triglyceride rich lipoproteins, increase their susceptibility to oxidation and increase aortic cholesterol concentration in rabbits. J Lipid Res 39 (1998) 1995-2004
53. Lizard G., Monier S., Cordelet C., Gesquière L., Deckert V., Gueldry S., et al. Characterization and comparison of the mode of cell death, apoptosis versus necrosis, induced by 7b-hydroxycholesterol and 7-ketocholesterol in the cells of the vascular wall. Arterioscler Thromb Vasc Biol 19 (1999) 1190-1200
54. Stoll G., and Bendszus M. Inflammation and atherosclerosis: novel insight into plaque formation and destabilization. Stroke 37 (2006) 1923-1932
55. Piccotti J.R., LaGattuta M.S., Knight S.A., Gonzales A.J., and Bleavins M.R. Induction of apoptosis by cationic amphiphilic drugs amiodarone and imipramine. Drug Chem Toxicol 28 (2005) 117-133
56. Feng B., Yao P.M., Li Y., Devlin C.M., Zhang D., Harding H.P., et al. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat Cell Biol 5 (2003) 781-792
57. Li W., Dalen H., Eaton J.W., and Yuan X.M. Apoptotic death of inflammatory cells in human atheroma. Arterioscler Thromb Vasc Biol 21 (2001) 1124-1130
58. Unger R.H., and Orci L. Lipoapoptosis: its mechanism and its diseases. Biochim Biophys Acta 15 (2002) 202-212
59. Koopman G., Reutelingsperger C.P.M., Kuijten G.A.M., Keehnen R.M.J., Pals S.T., and van Oers M.H.J. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84 (1994) 1415-1420
60. Alessi D.R., Caudwell F.B.N., Andjelkovic M., Hemmings B.A., and Cohen P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAP kinase-1 and p70 S6 kinase. FEBS Lett 399 (1996) 333-338
61. Hill M.M., and Hemmings B.A. Inhibition of protein kinase B/Akt: implication for cancer therapy. Pharmacol Ther 93 (2002) 243-251
62. Maor I., Mandel H., and Aviram M. Macrophage uptake of oxidized LDL inhibits lysosomal sphingomyelinase, thus causing the accumulation of unesterified cholesterol-sphingomyelin-rich particles in the lysosomes. A possible role for 7-ketocholesterol. J Lipid Res 15 (1995) 1378-1387
63. Shiratori Y., Houweling M., Zha X., and Tabas I. Stimulation of CTP:phosphocholine cytidylyltransferase by free cholesterol loading of macrophages involves signaling through protein dephosphorylation. J Biol Chem 270 (1995) 29894-29903
64. Simons K., and Toomre D. Lipid rafts and signal transduction. Nat rev 1 (2000) 31-41
65. Singh U., Devaraj S., and Jialal I. Vitamin E, oxidative stress, and inflammation. Annu Rev Nutr 25 (2005) 151-174
66. Azzi A., Gysin R., Kempna P., Munteanu A., Villacorta L., Visarius T., et al. Vitamin E mediates cell signaling and regulation of gene expression. Ann N Y Acad Sci 1031 (2004) 86-95
67. Zingg J.M., and Azzi A. Non-oxidant activities of Vitamin E. Curr Med Chem 11 (2004) 1113-1133
68. Miguet C., Monier S., Bettaieb A., Athias A., Bessède G., Laubriet A., et al. Ceramide generation occurring during 7b-hydroxycholesterol- and 7-ketocholesterol-induced apoptosis is caspase independent and is not required to trigger cell death. Cell Death Differ 8 (2001) 83-99
69. Lucy J.A. Structural interactions between vitamin E and polyunsaturated lipids. World Rev Nutr Diet 31 (1978) 184-189
70. Honegger U.E., Scuntaro I., and Wiesman U.N. Vitamin E reduces accumulation of amiodarone and desethylamiodarone and inhibits phospholipidosis in cultured human cells. Biochem Pharmacol 49 (1995) 1741-1745
71. Yin K.J., Hsu C.Y., Hu X.Y., Chen H., Chen S.W., Xu J., et al. Protein phosphatase 2A regulates bim expression via the Akt/FKHRL1 signaling pathway in amyloid-beta peptide-induced cerebrovascular endothelial cell death. J Neurosci 26 (2006) 2290-2299
72. Cuschieri J., Bulger E., Biligren J., Garcia I., and Maier R.V. Vitamin E inhibits endotoxin-mediated transport of phosphatases to lipid rafts. Shock 27 (2007) 19-24
73. Richardson J.A., Amantea C.M., Kianmahd B., Tetradis S., Lieberman J.R., Hahn T.J., et al. Oxysterol-induced osteoblastic differentiation of pluripotent mesenchymal cells is mediated through a PKC- and PKA-dependent pathway. J Cell Biochem 100 (2007) 1131-1145
74. He M.A., Cheng L.X., Jiang C.Z., Zeng H.S., Wang J., Wang F., et al. Association of polymorphism of P22(phox) C242T, plasma levels of Vitamin E, and smoking with coronary heart disease in China. Am Heart J 153 (2007) 640-646
75. Schneider M., Vergès B., Klein A., Miller E.R., Deckert V., Desrumaux C., et al. Alterations in plasma vitamin E distribution in type 2 diabetic patients with elevated plasma phospholipid transfer protein activity. Diabetes 53 (2004) 2633-2639
76. Lizard G., Moisant M., Cordelet C., Monier S., Gambert P., and Lagrost L. Induction of similar features of apoptosis in human and bovine vascular endothelial cells treated by 7-ketocholesterol. J Pathol 183 (1997) 330-338
77. Pedruzzi E., Guichard C., Ollivier V., Driss F., Fay M., Prunet C., et al. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol 24 (2004) 10703-10717