Effects of cholesterol oxides on cell death induction and calcium increase in human neuronal cells (SK-N-BE) and evaluation of the protective effects of docosahexaenoic acid (DHA; C22:6 n-3)

Steroids

Volumn 99, Issue PB, 2015, Pages 238-247

  Zarrouk, Amira ^a,b,c   Nury, Thomas ^a   Samadi, Mohammad ^d   O'Callaghan, Yvonne ^c   Hammami, Mohamed ^b   O'Brien, Nora M ^c   Lizard, Gérard ^a   Mackrill, John J ^c  

^a Faculté des Sciences Gabriel   (France)

^b UNIVERSITY OF MONASTIR   (Tunisia)

^c UNIVERSITY COLLEGE CORK   (Ireland)

^d UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Calcium; Cell death; Oxidative stress; Oxysterols; SK N BE

Indexed keywords

24 HYDROXYCHOLESTEROL; 26 HYDROXYCHOLESTEROL; 4ALPHA HYDROXYCHOLESTEROL; 4BETA HYDROXYCHOLESTEROL; 6ALPHA HYDROXYCHOLESTEROL; 6BETA HYDROXYCHOLESTEROL; 7 OXOCHOLESTEROL; 7ALPHA HYDROXYCHOLESTEROL; 7BETA HYDROXYCHOLESTEROL; CALCIUM ION; CATALASE; CHOLESTEROL; CHOLESTEROL OXIDE; DOCOSAHEXAENOIC ACID; FURA 2; OXYSTEROL; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; ANTIOXIDANT; BIOLOGICAL MARKER; CALCIUM; NEUROPROTECTIVE AGENT; OXIDE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRION; NERVE CELL; NERVE DEGENERATION; NEUROBLASTOMA CELL LINE; NEUROPROTECTION; NEUROTOXICITY; OXIDATIVE STRESS; STAINING; VIDEO MICROSCOPY; AUTOPHAGY; CELL LINE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; METABOLISM;

ANTIOXIDANTS; APOPTOSIS; AUTOPHAGY; BIOMARKERS; CALCIUM; CELL LINE; CELL PROLIFERATION; CHOLESTEROL; DOCOSAHEXAENOIC ACIDS; HUMANS; MITOCHONDRIA; NEURONS; NEUROPROTECTIVE AGENTS; OXIDES; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 84937390884     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2015.01.018     Document Type: Article

References (64)

1. K. Blennow, M.J. de Leon, and H. Zetterberg Alzheimer's disease Lancet 368 2006 387 403
2. C.R. Jack, V.J. Lowe, S.D. Weigand, H.J. Wiste, M.L. Senjem, D.S. Knopman, and et al. Alzheimer's disease neuroimaging initiative, serial PIB and MRI in normal, mild cognitive impairment and Alzheimer's disease, implications for sequence of pathological events in Alzheimer's disease Brain 132 2009 1355 1365
3. C.R. Jack, D.S. Knopman, W.J. Jagust, L.M. Shaw, P.S. Aisen, M.W. Weiner, and et al. Up-regulation of β-amyloidogenesis in neuron-like human cells by both 24- and 27-hydroxycholesterol: protective effect of N-acetyl-cysteine Aging Cell 13 2014 561 572
4. A. Zarrouk, A. Vejux, J. Mackrill, Y. O'Callaghan, M. Hammami, N. O'Brien, and et al. Involvement of oxysterols in age-related diseases and ageing processes Ageing Res Rev 18C 2014 148 162
5. L. Bretillon, U. Diczfalusy, I. Bjorkhem, M.A. Maire, L. Martine, C. Joffre, and et al. Cholesterol-24S-hydroxylase (CYP46A1) is specifically expressed in neurons of the neural retina Curr Eye Res 32 2007 361 366
6. U. Diczfalusy, J. Miura, H.K. Roh, R.A. Mirghani, J. Sayi, H. Larsson, and et al. 4-betahydroxycholesterol is a new endogenous CYP3A marker: relationship to CYP3A5 genotype, quinine 3-hydroxylation and sex in Koreans, Swedes and Tanzanians Pharmacogenet Genomics 18 2008 201 208
7. Y. Maeda, H. Nagatomo, F. Uchiyama, J. Nagatomo, M. Yamada, H. Shiotsuki, and et al. A comparative study of the conversion of 7-hydroxycholesterol in rabbit, guinea pig, rat, hamster, and chicken Steroids 67 2002 703 708
8. N. Miyoshi, L. Iuliano, S. Tomono, and H. Ohshima Implications of cholesterol autoxidation products in the pathogenesis of inflammatory diseases Biochem Biophys Res Commun 446 2014 702 708
9. G.J. Schroepfer Jr. Oxysterols: modulators of cholesterol metabolism and other processes Physiol Rev 80 2000 361 554
10. S. Lemaire-Ewing, C. Prunet, T. Montange, A. Vejux, A. Berthier, G. Bessede, and et al. Comparison of the cytotoxic, pro-oxidant and pro-inflammatory characteristics of different oxysterols Cell Biol Toxicol 21 2005 97 114
11. P. Gamba, M. Guglielmotto, G. Testa, D. Monteleone, C. Zerbinati, S. Gargiulo, and et al. Up-regulation of β-amyloidogenesis in neuron-like human cells by both 24- and 27-hydroxycholesterol: protective effect of N-acetyl-cysteine Aging Cell 13 2014 561 572
12. J.R. Prasanthi, A. Huls, S. Thomasson, A. Thompson, E. Schommer, and O. Ghribi Differential effects of 24S-hydroxycholesterol and 27-hydroxycholesterol on beta-amyloid precursor protein levels and processing in human neuroblastoma SH-SY5Y cells Mol Neurodegener 4 2009 1
13. C. Miguet-Alfonsi, C. Prunet, S. Monier, G. Bessede, S. Lemaire-Ewing, A. Berthier, and et al. Analysis of oxidative processes and of myelin figures formation before and after the loss of mitochondrial transmembrane potential during 7beta-hydroxycholesterol and 7-ketocholesterol-induced apoptosis: comparison with various proapoptotic chemicals Biochem Pharmacol 64 2002 527 541
14. E. Pedruzzi, C. Guichard, V. Ollivier, F. Driss, M. Fay, C. Prunet, and 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
15. G. Lizard, S. Gueldry, O. Sordet, S. Monier, A. Athias, C. Miguet, and et al. 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
16. C. Prunet, S. Lemaire-Ewing, F. Menetrier, D. Neel, and G. Lizard Activation of caspase-3-dependent and -independent pathways during 7-ketocholesterol- and 7beta-hydroxycholesterol-induced cell death: a morphological and biochemical study J Biochem Mol Toxicol 19 2005 311 326
17. G. Lizard, S. Monier, C. Cordelet, L. Gesquiere, V. Deckert, S. Gueldry, and et al. Characterization and comparison of the mode of cell death, apoptosis versus necrosis, induced by 7beta-hydroxycholesterol and 7-ketocholesterol in the cells of the vascular wall Am J Pathol 19 1999 1190 1200
18. N. Noguchi, Y. Saito, and Y. Urano Diverse functions of 24S-hydroxycholesterol in the brain Biochem Biophys Res Commun 446 2014 692 696
19. L. Ryan, Y.C. O'Callaghan, and N.M. O'Brien Involvement of calcium in 7β-hydroxycholesterol and cholesterol-5β, 6β-epoxide-induced apoptosis Int J Toxicol 25 2006 35 39
20. W. Martinet, M. De Bie, D.M. Schrijvers, G.R. De Meyer, A.G. Herman, and M.M. Kockx 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
21. T. Nury, A. Zarrouk, A. Vejux, M. Doria, J.M. Riedinger, R. Delage-Mourroux, and et al. Induction of oxiapoptophagy, a mixed mode of cell death associated with oxidative stress, apoptosis and autophagy, on 7-ketocholesterol-treated 158N murine oligodendrocytes: impairment by α-tocopherol Biochem Biophys Res Commun 446 2014 714 719
22. S. Monier, M. Samadi, C. Prunet, M. Denance, A. Laubriet, A. Athias, and et al. Impairment of the cytotoxic and oxidative activities of 7 beta-hydroxycholesterol and 7-ketocholesterol by esterification with oleate Biochem Biophys Res Commun 303 2003 814 824
23. S. Agrawal, M.L. Agarwal, M. Chatterjee-Kishore, G.R. Stark, and G.M. Chisolm Stat1-dependent, p53-independent expression of p21(waf1) modulates oxysterol-induced apoptosis Mol Cell Biol 22 2002 1981 1992
24. F. Biasi, G. Leonarduzzi, B. Vizio, D. Zanetti, A. Sevanian, B. Sottero, and et al. Oxysterol mixtures prevent proapoptotic effects of 7-ketocholesterol in macrophages: implications for proatherogenic gene modulation FASEB J 18 2004 693 695
25. 2+ channel blockers verapamil and nifedipine inhibit apoptosis induced by 25-hydroxycholesterol in human aortic smooth muscle cells J Lipid Res 38 1997 2049 2061
26. 2+ oscillations, MAP kinase activation and apoptosis in human aortic smooth muscle cells Atherosclerosis 153 2000 23 35
27. A. Berthier, S. Lemaire-Ewing, C. Prunet, S. Monier, A. Athias, G. Bessède, and 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
28. M.P. Mattson Free radicals and disruption of neuronal ion homeostasis in AD: a role for amyloid β-peptide? Neurobiol Aging 16 1995 679 682
29. L.L. Dugan, S.L. Sensi, L.M.T. Canzoniero, S.D. Handran, S.M. Rothman, T.S. Lin, and et al. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-d-aspartate J Neurosci 15 1995 6377 6388
30. I.J. Reynolds, and T.G. Hastings Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation J Neurosci 15 1995 3318 3327
31. W.J. Lukiw, and N.G. Bazan Docosahexaenoic acid and the aging brain J Nutr 138 2008 2510 2514
32. G. Lizard, O. Rouaud, J. Demarquoy, M. Cherkaoui-Malki, and L. Iuliano Potential roles of peroxisomes in Alzheimer's disease and in dementia of the Alzheimer's type J Alzheimer's Dis 29 2012 241 254
33. T. Nury, M. Samadi, A. Zarrouk, J.M. Riedinger, and G. Lizard Improved synthesis and in vitro evaluation of the cytotoxic profile of oxysterols oxidized at C4 (4α- and 4β-hydroxycholesterol) and C7 (7-ketocholesterol, 7α- and 7β-hydroxycholesterol) on cells of the central nervous system Eur J Med Chem 70 2013 558 567
34. 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
35. I. Singh, and Y. Kishimoto Effect of cyclodextrins on the solubilization of lignoceric acid, ceramide, and cerebroside, and on the enzymatic reactions involving these compounds J Lipid Res 24 1983 662 665
36. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Methods 65 1983 55 63
37. G. Lizard, S. Fournel, L. Genestier, N. Dhedin, C. Chaput, M. Flacher, and et al. Kinetics of plasma membrane and mitochondrial alterations in cells undergoing apoptosis Cytometry 21 1995 275 283
38. L. Dubrez, I. Savoy, A. Hamman, and E. Solary Pivotal role of a DEVD-sensitive step in etoposide-induced and Fas-mediated apoptotic pathways EMBO J 15 1996 5504 5512
39. D.A. Bass, J.W. Parce, L.R. Dechatelet, P. Szejda, M.C. Seeds, and M. Thomas Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation J Immunol 130 1983 1910 1917
40. G. Rothe, and G. Valet Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2',7'-dichlorofluorescin J Leukoc Biol 47 1990 440 448
41. P. Baudhuin, H. Beaufay, Y. Rahman-Li, O.Z. Sellinger, R. Wattiaux, P. Jacques, and et al. Tissue fractionation studies. 17. Intracellular distribution of monoamineoxidase, aspartate aminotransferase, alanine aminotransferase, D-amino acidoxidase and catalase in rat-liver tissue Biochem J 92 1964 179 184
42. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 1976 248 254
43. H.P. Misra, and I. Fridovich Superoxide dismutase and peroxidase: a positive activity stain applicable to polyacrylamide gel electropherograms Arch Biochem Biophys 183 1977 511 515
44. Y. Hammoud, T. Rice, and J.J. Mackrill Oxysterols modulate calcium signalling in the A7r5 aortic smooth muscle cell-line Biochimie 95 2013 568 577
45. K. Ragot, J.J. Mackrill, A. Zarrouk, T. Nury, V. Aires, A. Jacquin, and et al. Absence of correlation between oxysterol accumulation in lipid raft microdomains, calcium increase, and apoptosis induction on 158N murine oligodendrocytes Biochem Pharmacol 86 2013 67 79
46. 2+ mobilization in human SH-SY5Y neuroblastoma cells is independent of phosphoinositide signalling, but dependent on sphingosine kinase activation Biochem J 343 1999 45 52
47. M. Relucenti, R. Heyn, L. Petruzziello, G. Pugliese, M. Taurino, and G. Familiari Detecting microcalcifications in atherosclerotic plaques by a simple trichromic staining method for epoxy embedded carotid endarterectomies Eur J Histochem 54 2010 e33
48. R.G. Cutler, J. Kelly, K. Storie, W.A. Pedersen, A. Tammara, K. Hatanpaa, and et al. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease Proc Natl Acad Sci USA 101 2004 2070 2075
49. N. Bogdanovic, L. Bretillon, E.G. Lund, U. Diczfalusy, L. Lannfelt, B. Winblad, and et al. On the turnover of brain cholesterol in patients with Alzheimer's disease. Abnormal induction of the cholesterol-catabolic enzyme CYP46 in glial cells Neurosci Lett 314 2001 45 48
50. J. Brown, C. Theisler, S. Silberman, D. Magnuson, N. Gottardi-Littell, J.M. Lee, and et al. Differential expression of cholesterol hydroxylases in Alzheimer's disease J Biol Chem 279 2004 34674 34681
51. D. Lütjohann, O. Breuer, G. Ahlborg, I. Nennesmo, A. Siden, U. Diczfalusy, and et al. Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation Proc Natl Acad Sci USA 93 1996 9799 9804
52. M. Heverin, S. Meaney, D. Lütjohann, U. Diczfalusy, J. Wahren, and I. Björkhem Crossing the barrier: Net flux of 27-hydroxycholesterol into the human brain J Lipid Res 46 2005 1047 1052
53. P. Ferrera, O. Mercado-Gomez, M. Silva-Aguilar, M. Valverde, and C. Arias Cholesterol potentiates beta-amyloid-induced toxicity in human neuroblastoma cells: involvement of oxidative stress Neurochem Res 33 2008 1509 1517
54. K. Ragot, D. Delmas, A. Athias, T. Nury, M. Baarine, and G. Lizard Α-Tocopherol impairs 7-ketocholesterol-induced caspase-3-dependent apoptosis involving GSK-3 activation and Mcl-1 degradation on 158N murine oligodendrocytes Chem Phys Lipids 164 2011 469 478
55. C.C. Gregorio-King, T. Gough, G.J. Van Der Meer, J.B. Hosking, C.M. Waugh, J.L. McLeod, and et al. Mechanisms of resistance to the cytotoxic effects of oxysterols in human leukemic cells J Steroid Biochem Mol Biol 88 2004 311 320
56. A. Okabe, Y. Urano, S. Itoh, N. Suda, R. Kotani, Y. Nishimura, and et al. Adaptive responses induced by 24S-hydroxycholesterol through liver X receptor pathway reduce 7-ketocholesterol-caused neuronal cell death Redox Biol 2 2013 28 35
57. H. Kölsch, M. Ludwig, D. Lütjohann, and M.L. Rao Neurotoxicity of 24S-hydroxycholesterol, an important cholesterol elimination product of the brain, may be prevented by vitamin E and estradiol-17β J Neural Transm 108 2001 475 488
58. P. Gamba, G. Leonarduzzi, E. Tamagno, M. Guglielmotto, G. Testa, B. Sottero, and et al. Interaction between 24S-hydroxycholesterol, oxidative stress, and amyloid-b in amplifying neuronal damage in Alzheimer's disease: three partners in crime Aging Cell 10 2011 403 417
59. J.P. Rantham Prabhakara, G. Feist, S. Thomasson, A. Thompson, E. Schommer, and O. Ghribi Differential effects of 24S-hydroxycholesterol and 27-hydroxycholesterol on tyrosine hydroxylase and alpha-synuclein in human neuroblastoma SH-SY5Y cells J Neurochem 107 2008 1722 1729
60. S. Sharma, R.P. Prasanthi, E. Schommer, G. Feist, and O. Ghribi Hypercholesterolemia-induced A[beta] accumulation in rabbit brain is associated with alteration in IGF-1 signaling Neurobiol Dis 32 2008 426 432
61. O. Ghribi, E. Schommer, and J.R.P. Prasanthi 27-hydroxycholestrol as the missing link between circulating cholesterol and AD-like pathology Alzheimer's & Dementia 5 2009 180
62. S. Smaili, H. Hirata, R. Ureshino, P.T. Monteforte, A.P. Morales, and M.L. Muler Calcium and cell death signaling in neurodegeneration and aging An Acad Bras Cienc 81 2009 467 475
63. X.M. Yuan, W. Li, U.T. Brunk, H. Dalen, Y.H. Chang, and A. Sevanian Lysosomal destabilization during macrophage damage induced by cholesterol oxidation products Free Radic Biol Med 28 2000 208 218
64. T. Oster, and T. Pillot Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice Biochim Biophys Acta 1801 2010 791 798