Oxysterol mixture in hypercholesterolemia-relevant proportion causes oxidative stress-dependent eryptosis

Cellular Physiology and Biochemistry

Volumn 34, Issue 4, 2014, Pages 1075-1089

  Tesoriere, Luisa ^a   Attanzio, Alessandro ^a   Allegra, Mario ^a   Cilla, Antonio ^b   Gentile, Carla ^a   Livrea, Maria A ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Eryptosis; Human red blood cell; Hypercholesterolemia; Oxidative stress; Oxysterols

Indexed keywords

7 OXOCHOLESTEROL; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; CALCIUM; CALCIUM CHANNEL; CALPHOSTIN C; CARRIER PROTEIN; CASPASE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FLUORESCEIN DIACETATE; GLUTATHIONE; HYDROPEROXIDE; OXYSTEROL; PHOSPHATIDYLSERINE; PROSTAGLANDIN E2; PROTEIN KINASE C; STAUROSPORINE; 7-KETOCHOLESTEROL; ANTIOXIDANT; CHOLESTEROL DERIVATIVE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL VOLUME; CONTROLLED STUDY; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYPTOSIS; ERYTHROCYTE; EX VIVO STUDY; FLUORESCENCE; HEMOLYSIS; HUMAN; HUMAN CELL; HYPERCHOLESTEROLEMIA; LIPID OXIDATION; NORMAL HUMAN; OXIDATIVE STRESS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANTIOXIDANTS; APOPTOSIS; CALCIUM; CALCIUM CHANNELS; CASPASES; DINOPROSTONE; ERYTHROCYTES; HUMANS; HYPERCHOLESTEROLEMIA; KETOCHOLESTEROLS; OXIDATIVE STRESS; PHOSPHATIDYLSERINES; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES;

EID: 84908609487     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000366322     Document Type: Article

References (72)

1. Poli G, Biasi F, Leonarduzzi G: Oxysterols in the pathogenesis of major chronic diseases. Redox Biol 2013;1:125-130.
2. Addis PB, Emanuel HA, Bergmann SD, Zavoral JH: Capillary quantification of cholesterol oxidation products in plasma lipoproteins of fasted humans. Free Radic Biol Med 1989;7:179-182.
3. Sevanian A, Seraglia R, Traldi P, Rossato P, Ursini F, Hodis H: Analysis of plasma cholesterol oxidation products using gas- and high performance liquid chromatography/mass spectrometry. Free Radic Biol Med 1994;17:397-409.
4. Dzeletovic S, Breuer O, Lund E, Diczfalusy U: Determination of cholesterol oxidation products in human plasma by isotope dilution-mass spectrometry. Anal Biochem 1995;225:73-80.
5. Chang YH, Abdalla DS, Sevanian A: Characterization of cholesterol oxidation products formed by oxidative modification of low density lipoprotein. Free Radic Biol Med 1997;23:202-214.
6. Brown A J, Jessup W: Oxysterols and atherosclerosis. Atherosclerosis 1999;142:1-28.
7. Vaya J, Schipper HM: Oxysterols, cholesterol homeostasis, and Alzheimer disease. J Neurochem 2007;102:1727-1737.
8. Lordan S, Mackrill JJ, O'Brien NM: Oxysterols and mechanisms of apoptotic signaling: implications in the pathology of degenerative diseases. J Nutr Biochem 2009;20:321-336.
9. Larsson DA, Baird S, Nyhalah JD, Yuan XM, Li W: Oxysterol mixtures, in atheroma-relevant proportions, display synergistic and proapoptotic effects. Free Radic Biol Med 2006;4:902-910.
10. Nishio E, Watanabe Y: Oxysterols induced apoptosis in cultured smooth muscle cells through CPP32 protease activation and bcl-2 protein downregulation. Biochem Biophys Res Commun 1996;226:928-934.
11. Lizard G, Monier S, Cordelet C, Gesquiere L, Deckert V, Gueldry S, Lagrost L, Gambert P: 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 ThrombVasc Biol 1999;19:1190-1200.
12. Lemaire S, Lizard G, Monier S, Miguet C, Gueldry S, Volot F, Gambert P, Neel D: Different patterns of IL-1beta secretion, adhesion molecule expression and apoptosis induction in human endothelial cells treated with 7alpha-, 7beta-hydroxycholesterol, or 7-ketocholesterol. FEBS Lett 1998;440:434-439.
13. Aupeix K, Weltin V, Mejia JE, Christ M, Marchal J, Freyssinet JM, Bischoff P: Oxysterols-induced apoptosis in human monocytic cell lines. Immunobiology 1995;194:415-428.
14. O'Callaghan YC, Woods JA, O'Brien NM: Oxysterol-induced cell death in U937 and HepG2 cells at reduced and normal serum concentrations. Eur J Nutr 1999;38:255-262.
15. Mascia C, Maina M, Chiarpotto E, Leonarduzzi G, Poli G, Biasi F: Pro-inflammatory effect of cholesterol and its oxidation products on CaCo-2 human enterocyte-like cells: Effective protection by epigallocatechin-3-gallate. Free Radic Biol Med 2010;49:2049-2057.
16. Biasi F, Chiarpotto E, Sottero B, Maina M, Mascia C, Guina T, Gamba P, Gargiulo S, Testa G, Leonarduzzi G, Poli G: Evidence of cell damage induced by major components of a diet-compatible mixture of oxysterols in human colon cancer CaCo-2 cell line. Biochimie 2013;95:632-640.
17. Trousson A, Makoukji J, Petit PX, Bernard S, Slomianny C, Schumacher M, Massaad C: Cross-talk between oxysterols and glucocorticoids: differential regulation of secreted phopholipase A2 and impact on oligodendrocyte death. PLoS One 2009;4:e8080.
18. Lang F, Gulbins E, Lerche H, Huber SM, Kempe DS, Foller M: Eryptosis, a window to systemic disease. Cell Physiol Biochem 2008;22:373-380.
19. Bonomini M, Sirolli V, Settefrati N, Dottori S, Di Liberato L, Arduini A: Increased erythrocyte phosphatidylserine exposure in chronic renal failure. J Am Soc Nephrol 1999;10:1982-1990.
20. Wood BL, Gibson DF, Tait JF: Increased erythrocyte phosphatidylserine exposure in sickle cell disease: Flow-cytometric measurement and clinical associations. Blood1996;88:1873-1880.
21. Basu S, Banerjee D, Chandra S, Chakrabarti A: Eryptosis in hereditary spherocytosis and thalassemia: role of glycoconjugates. Glycoconj J 2010;27:717-722.
22. Calderon-Salinas JV, Munoz-Reyes EG, Guerrero-Romero JF, Rodriguez-Moran M, Bracho-Riquelme RL, Carrera-Gracia MA, Quintanar-Escorza M: Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol Cell Biochem 2011;357:171-179.
23. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS, Chung JH: Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 2007;27:414-421.
24. Andrews DA, Low PS: Role of red blood cells in thrombosis. Curr Opin Hematol 1999;6:76-82.
25. Closse C, Dachary-Prigent J, Boisseau MR: Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999;107:300-302.
26. Pandolfi A, Di Pietro N, Sirolli V, Giardinelli A, Di Silvestre S, Amoroso L, Di Tomo P, Capani F, Consoli A, Bonomini M: Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J Cell Physiol 2007;213:699-709.
27. Borst O, Abed M, Alesutan I, Towhid ST, Qadri SM, Foller M, Gawaz M, Lang F: Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Physiol Cell Physiol 2012;302:C644-C651.
28. Meaney S, Bodin K, Diczfalusy U, Björkhem I: On the rate of translocation in vitro and kinetics in vivo of the major oxysterols in human circulation: critical importance of the position of the oxygen function. J Lipid Res 2002;43:2130-2135.
29. Leonarduzzi G, Poli G, Sottero B, Biasi F: Activation of the mitochondrial pathway of apoptosis by oxysterols. Front Biosci 2007;12:791-799.
30. Gargiulo S, Gamba P, Testa G, Sottero B, Maina M, Guina T, Biasi F, Poli G, Leonarduzzi G: Molecular Signaling Involved in Oxysterol-Induced ß1-Integrin Over-Expression in Human Macrophages. Int J Mol Sci 2012;13:14278-14293.
31. Hu ML: Measurement of protein thiol groups and glutathione in plasma; In Packer L (ed): Methods in Enzymology, Academic Press, San Diego, CA, 1994, vol 233, pp 380-385.
32. Pryor WA, Castle L: Chemical methods for detection of lipid hydroperoxides; In Packer L (ed): Methods in Enzymology, Academic Press, San Diego,Ca, 1984, vol. 105, pp203-208.
33. Lang E, Qadri SM, Lang F: Killing me softly-Suicidal erythrocyte death. Int J Biochem Cell Biol 2012;44:1236-1243.
34. Lang F, Qadri SM: Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif 2012;33:125-130.
35. Lang PA, Kempe DS, Myssina S, Tanneur V, Birka C, Laufer S, Lang F, Wieder T, Huber SM: PGE2 in the regulation of programmed erythrocyte death. Cell Death Differ 2005;12:415-428.
36. Woon LA, Holland JW, Kable EP, Roufogalis BD: Ca2+ sensitivity of phospholipid scrambling in human red cell ghosts. Cell Calcium 1999;25:313-320.
37. De Jong K, Rettig MP, Low PS, Kuypers F A: Protein kinase C activation induces phosphatidylserine exposure on red blood cells. Biochemistry 2002;41:12562-12567.
38. Chung SM, Bae ON, Lim KM, Noh J Y, Lee MY, Jung YS, Chung JH: Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 2007;27:414-421.
39. Mandal D, Moitra PK, Saha S, Basu J: Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Letters 2002;513:184-188.
40. Mandal D, Mazumder A, Das P. Kundu M, Basu J: Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem 2005;280:39460-39467.
41. Devaux PF, Herrmann A, Ohlwein N, Kozlov MM: How lipid flippases can modulate membrane structure. Biochim Biophys Acta 2008;1778:1591-1600.
42. Uemura M, Manabe H, Yoshida N, Fujita N, Ochiai J, Matsumoto N, Takagi T, Naito Y, Yoshikawa T: Alpha-tocopherol prevents apoptosis of vascular endothelial cells via a mechanism exceeding that of mere antioxidation. Eur J Pharmacol 2002;456:29-37.
43. Li W, Hellsten A, Xu LH, Zhuang DM, Jansson K, Brunk UT, Yuan X M: Foam cell death induced by 7beta-hydroxycholesterol is mediated by labile iron-driven oxidative injury: mechanisms underlying induction of ferritin in human atheroma. Free Radic Biol Med 2005;39:864-875.
44. Lang F, Lang E, Foller M: Physiology and pathophysiology of eryptosis. Transfus Med Hemother 2012;39:308-314.
45. Olkkonen VM, Hynynen R: Interactions of oxysterols with membranes and proteins. Mol Aspects Med 2009;30:123-133.
46. Massey JB: Membrane and protein interactions of oxysterols. Curr Opin Lipidol 2006;17:296-301.
47. Foller M, Kasinathan RS, Koka S, Lang C, Shumilina E, Birnbaumer L, Lang F, Huber SM: TRPC6 contributes to the Ca(2+) leak of human erythrocytes. Cell Physiol Biochem 2008;21:183-192.
48. Andrews DA, Yang L, Low PS: Phorbol ester stimulates a protein kinase C-mediated agatoxin-TK-sensitive calcium permeability pathway in human red blood cells. Blood 2002; 100:3392-3399.
49. Wagner-Britz L, Wang J, Kaestner L, Bernhardt I: Protein kinase Ca and P-type Ca channel CaV2.1 in red blood cell calcium signalling. Cell Physiol Biochem 2013;31:883-891.
50. Dyrda A, Cytlak U, Ciuraszkiewicz A, Lipinska A, Cueff A, Bouyer G, Egée S, Bennekou P, Lew VL, Thomas SL: Local membrane deformations activate Ca2+-dependent K+ and anionic currents in intact human red blood cells. PLoS One 2010;5:e9447.
51. Rosenblat M, Aviram M: Oxysterol-induced activation of macrophage NADPH-oxidase enhances cell-mediated oxidation of LDL in the atherosclerotic apolipoprotein E deficient mouse: inhibitory role for vitamin E. Atherosclerosis 2002;160:69-80.
52. Panini SR, Yang L, Rusinol AE, Sinensky MS, Bonventre JV, Leslie CC: Arachidonate metabolism and the signaling pathway of induction of apoptosis by oxidized LDL/oxysterol. J Lipid Res 2001;42:1678-1686.
53. Lahoua Z, Vial H, Michel F, Crastes de Paulet A, Astruc ME: Oxysterol activation of arachidonic acid release and prostaglandin E2 biosynthesis in NRK 49F cells is partially dependent on protein kinase C activity. Cell Signal 1991;3:559-567.
54. Maher AD, Kuchel PW: The Gárdos channel: a review of the Ca2+-activated K+ channel in human erythrocytes. Int J Biochem Cell Biol 2003;35:1182-1197.
55. Jilani K, Qadri SM, Lang F: Geldanamycin-induced phosphatidylserine translocation in the erythrocyte membrane. Cell Physiol Biochem 2013;32:1600-1609.
56. Rosenblat M, Belinky P, Vaya J, Levy R, Hayek T, Coleman R, Merchav S, Aviram M: Macrophage enrichment with the isoflavan glabridin inhibits NADPH oxidase-induced cell-mediated oxidation of low density lipoprotein. A possible role for protein kinase C. J Biol Chem 1999;274:13790-13799.
57. Biasi F, Leonarduzzi G, Vizio B, Zanetti D, Sevanian A, Sottero B, Verde V, Zingaro B, Chiarpotto E, Poli G: Oxysterol mixtures prevent proapoptotic effects of 7-ketocholesterol in macrophages: implications for proatherogenic gene modulation. FASEB J 2004;18:693-695.
58. Tesoriere L, Attanzio A, Allegra M, Gentile C, Livrea MA: Phytochemical indicaxanthin suppresses 7-ketocholesterol-induced THP-1 cell apoptosis by preventing cytosolic Ca2+ increase and oxidative stress. Br J Nutr 2013;110:230-240.
59. Mahmud H, Qadri SM, Föller M, Lang F Inhibition of suicidal erythrocyte death by vitamin C. Nutrition 2010;26:671-676.
60. Shaik N, Lupescu A, Lang F: Inhibition of suicidal erythrocyte death by probucol. J Cardiovasc Pharmacol 2013;61:120-126.
61. Bevers EM, Williamson PL: Phospholipid scramblase: an update. FEBS Lett 2010;584:2724-2730.
62. Bratton DL, Fadok VA, Richter DA, Kailey JM, Guthrie LA, Henson PM: Appearance of phosphatidylserine on apoptotic cells requires calcium-mediated nonspecific flip-flop and is enhanced by loss of the aminophospholipid translocase. J Biol Chem 1997;272:26159-26165.
63. López-Revuelta A, Sánchez-Gallego JI, García-Montero AC, Hernández-Hernández A, Sánchez-Yagüe J, Llanillo M: Membrane cholesterol in the regulation of aminophospholipid asymmetry and phagocytosis in oxidized erythrocytes. Free Radic Biol Med 2007;42:1106-1118.
64. Nguyen DB, Wagner-Britz L, Maia S, Steffen P, Wagner C, Kaestner L, Bernhardt I: Regulation of phosphatidylserine exposure in red blood cells. Cell Physiol Biochem 2011;28:847-856.
65. Lupescu A, Bissinger R, Jilani K, Lang F: Triggering of suicidal erythrocyte death by celecoxib. Toxins 2013;5:1543-1554.
66. Abed M, Towhid ST, Shaik N, Lang F: Stimulation of suicidal death of erythrocytes by rifampicin. Toxicology 2012;302:123-128.
67. Govekar RB, Zingde SM: Protein kinase C isoforms in human erythrocytes. Annals of Hematology 2001;80:531-534.
68. Dekkers DW, Comfurius P, Schroit AJ, Bevers EM, Zwaal RF: Transbilayer movement of NBD-labeled phospholipids in red blood cell membranes: outward-directed transport by the multidrug resistance protein 1 (MRP1). Biochemistry.1998;37:14833-14837.
69. Tyurina YY, Shvedova AA, Kawai K, Tyurin VA, Kommineni C, Quinn PJ, Schor NF, Fabisiak JP, Kagan VE: Phospholipid signaling in apoptosis: peroxidation and externalization of phosphatidylserine. Toxicology 2000;148:93-101.
70. Hermann A, Devaux PF: Alteration of the aminophospholipid translocase activity during in vivo and artificial aging of human erythrocytes. Biochim Biophys Acta 1990;1027:41-46.
71. Miguet C, Monier S, Bettaieb A, Athias A, Besséde G, Laubriet A, Lemaire S, Néel D, Gambert P, Lizard G: Ceramide generation occurring during 7beta-hydroxycholesterol- and 7-ketocholesterol-induced apoptosis is caspase independent and is not required to trigger cell death. Cell Death Differ 2001;8:83-99.
72. Duchnowicz P, Novwicka A, Koter-Michalak M, Broncel M: In vivo influence of extract from Aronia Melanocarpa on the erythrocyte membranes in patients with hypercholesterolemia. Med Sci Monit 2012;18:CR569-574.