Phytochemical indicaxanthin suppresses 7-ketocholesterol-induced THP-1 cell apoptosis by preventing cytosolic Ca2+ increase and oxidative stress

British Journal of Nutrition

Volumn 110, Issue 2, 2013, Pages 230-240

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

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

7 Ketocholesterol; Apoptosis; Indicaxanthin; Macrophages; NADPH oxidase 4

Indexed keywords

7 OXOCHOLESTEROL; CALCIUM; CALCIUM ION; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDICAXANTHIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OXYSTEROL; PHOSPHATIDYLSERINE; PLANT MEDICINAL PRODUCT; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL CYCLE ARREST; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DIET SUPPLEMENTATION; DRUG ACTIVITY; DRUG BLOOD LEVEL; DRUG STRUCTURE; ENZYME ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MACROPHAGE; MEMBRANE POTENTIAL; MOLECULAR MECHANICS; MONOCYTE; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PEAR; THP 1 CELL;

APOPTOSIS; ATHEROSCLEROSIS; BETAXANTHINS; CALCIUM; CELL LINE; CYTOSOL; DIETARY SUPPLEMENTS; FRUIT; HUMANS; KETOCHOLESTEROLS; MACROPHAGES; MITOCHONDRIA; MONOCYTES; NADPH OXIDASE; NF-KAPPA B; OPUNTIA; OXIDATIVE STRESS; PHYTOTHERAPY; PLANT EXTRACTS; PLAQUE, ATHEROSCLEROTIC; PYRIDINES; REACTIVE OXYGEN SPECIES; SULFHYDRYL COMPOUNDS;

CACTACEAE; PYRUS;

EID: 84879166569     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S000711451200493X     Document Type: Article

References (79)

1. Leonarduzzi G, Sottero B & Poli G (2010) Targeting tissue oxidative damage by means of cells signaling modulators: the antioxidant concept revisited. Pharmacol Therap 128, 336-374.
2. Strack D, Vogt T & Schliemann W (2003) Recent advances in betalain research. Phytochemistry 62, 247-249.
3. Stintzing FC & Carle R (2005) Cactus stems (Opuntia spp.): a review of their chemistry, technology, and uses. Mol Nutr Food Res 49, 175-194.
4. Butera D, Tesoriere L, Di Gaudio F, et al. (2002) Antioxidant activities of Sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: betanin and indicaxanthin. J Agric Food Chem 50, 6895-6801.
5. Tesoriere L, Allegra M, Butera D, et al. (2007) Kinetics of the lipoperoxyl radical-scavenging activity of indicaxanthin in solution and unilamellar liposomes. Free Radic Res 41, 226-233.
6. Turco Liveri ML, Sciascia L, Allegra M, et al. (2009) Partition of indicaxanthin in membrane biomimetic systems. A kinetic and modeling approach. J Agric Food Chem 57, 10959-10963.
7. Turco-Liveri ML, Sciascia L, Lombardo R, et al. (2007) Spectrophotometric evidence for the solubilization site of betalain pigments in membrane biomimetic systems. J Agric Food Chem 55, 2836-2840.
8. Gentile C, Tesoriere L, Allegra M, et al. (2004) Antioxidant betalains from cactus pear (Opuntia ficus-indica) inhibit endothelial ICAM-1 expression. Ann N Y Acad Sci 1028, 481-486.
9. Tesoriere L, Butera D, Allegra M, et al. (2005) Distribution of betalain pigments in red blood cells after consumption of cactus pear fruits and increased resistance of the cells to ex vivo induced oxidative hemolysis in humans. J Agric Food Chem 53, 1266-1270.
10. Tesoriere L, Allegra M, Butera D, et al. (2006) Cytoprotective effects of the antioxidant phytochemical indicaxanthin in beta-thalassemia red blood cells. Free Radic Res 40, 753-761.
11. Baldassano S, Tesoriere L, Rotondo A, et al. (2010) Inhibition of the mechanical activity of mouse ileum by cactus pear (Opuntia ficus indica, L, Mill.) fruit extract and its pigment indicaxanthin. J Agric Food Chem 58, 7565-7571.
12. Baldassano S, Rotondo A, Serio R, et al. (2011) Inhibitory effects of indicaxanthin on mouse ileal contractility: analysis of the mechanism of action. Eur J Pharmacol 658, 200-205.
13. Tesoriere L, Fazzari M, Angileri F, et al. (2008) In vitro digestion of betalainic foods. Stability and bioaccessibility of betaxanthins and betacyanins and antioxidative potential of food digesta. J Agric Food Chem 56, 10487-10492.
14. Tesoriere L, Gentile C, Angileri F, et al. (2012) Trans-epithelial transport of the betalain pigments indicaxanthin and betanin across Caco-2 cell monolayers and influence of food matrix. Eur J Nutr (Epublication ahead of print version 18 July 2012).
15. Reynoso RC, Giner TV & Gonzalez de Mejia E (1999) Stability of betalain pigments from a cactacea fruit. Food Chem Toxicol 37, 825-830.
16. Tesoriere L, Allegra M, Butera D, et al. (2004) Absorption, excretion, and distribution of dietary antioxidant betalains in LDLs: potential health effects of betalains in humans. Am J Clin Nutr 80, 941-945.
17. Brown AJ & Jessup W (2009) Oxysterols: sources, cellular storage and metabolism, and new insights into their roles in cholesterol homeostasis. Mol Aspects Med 30, 111-122.
18. Kandutsch AA & Chen HW (1974) Inhibition of sterol synthesis in cultured mouse cells by cholesterol derivatives oxygenated in the side chain. J Biol Chem 249, 6057-6061.
19. Brown MS & Goldstein JL (1974) Suppression of 3-hydroxy-3- methylglutaryl coenzyme A reductase activity and inhibition of growth of human fibroblasts by 7-ketocholesterol. J Biol Chem 249, 7306-7314.
20. Danielsson H, Kalles I & Wikvall K (1984) Regulation of hydroxylations in biosynthesis of bile acids. Isolation of a protein from rat liver cytosol stimulating reconstituted cholesterol 7 alpha-hydroxylase activity. J Biol Chem 259, 4258-4262.
21. Bjorkhem I, Andersson O, Diczfalusy U, et al. (1994) Atherosclerosis and sterol 27-hydroxylase: evidence for a role of this enzyme in elimination of cholesterol from human macrophages. Proc Natl Acad Sci U S A 91, 8592-8596.
22. Brown AJ & Jessup W (1999) Oxysterols and atherosclerosis. Atherosclerosis 142, 1-28.
23. Colles SM, Maxson JM, Carlson SG, et al. (2001) Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cardiovasc Med 11, 131-138.
24. Pedruzzi E, Guichard C, Ollivier V, et al. (2004) 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, 10703-10717.
25. Nishio E & Watanabe Y (1996) Oxysterols induced apoptosis in cultured smooth muscle cells through CPP32 protease activation and bcl-2 protein downregulation. Biochem Biophys Res Commun 226, 928-934.
26. Luthra S, Dong J, Gramajo AL, et al. (2008) 7-Ketocholesterol activates caspases-3/7,-8, and-12 in human microvascular endothelial cells in vitro. Microvasc Res 75, 343-350.
27. Lizard G, Monier S, Cordelet C, et al. (1999) 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, 1190-1200.
28. Lemaire S, Lizard G, Monier S, et al. (1998) Different patterns of IL-1b secretion, adhesion molecule expression and apoptosis induction in human endothelial cells treated with 7a-, 7b-hydroxycholesterol, or 7-ketocholesterol. FEBS Lett 440, 434-439.
29. O'Callaghan YC, Woods JA & O'Brien NM (1999) Oxysterolinduced cell death in U937 and HepG2 cells at reduced and normal serum concentrations. Eur J Nutr 38, 255-262.
30. Lemaire-Ewing S, Prunet C, Montange T, et al. (2005) Comparison of the cytotoxic, prooxidant and pro-inflammatory characteristics of different oxysterols. Cell Biol Toxicol 21, 97-114.
31. Miguet-Alfonsi C, Prunet C, Monier S, et al. (2002) 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 pro-apoptotic chemicals. Biochem Pharmacol 64, 527-541.
32. Hulten LM, Lindmark H, Diczfalusy U, et al. (1996) Oxysterols present in atherosclerotic tissue decrease the expression of lipoprotein lipase messenger RNA in human monocytederived macrophages. J Clin Invest 97, 461-468.
33. Garcia-Cruset S, Carpenter KL, Guardiola F, et al. (2001) Oxysterol profiles of normal human arteries, fatty streaks and advanced lesions. Free Radic Res 35, 31-41.
34. Vaya J, Aviram M, Mahmood S, et al. (2001) Selective distribution of oxysterols in atherosclerotic lesions and human plasma lipoproteins. Free Radic Res 34, 485-487.
35. Stintzing FC, Schieber A & Carle R (2002) Identification of betalains from yellow beet (Beta vulgaris L.) and cactus pear [Opuntia ficus-indica (L.) Mill.] by high-performance liquid chromatography-electrospray ionization mass spectrometry. J Agric Food Chem 50, 2302-2307.
36. Piattelli M, Minale L & Prota G (1964) Isolation structure and absolute configuration of indicaxanthin. Tetrahedron 20, 2325-2329.
37. Martyn KD, Frederick LM, von Loehneysen K, et al. (2006) Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18, 69-82.
38. Palozza P, Simone R, Catalano A, et al. (2010) Lycopene prevents 7-ketocholesterol-induced oxidative stress, cell cycle arrest and apoptosis in human macrophages. J Nutr Biochem 21, 34-46.
39. Palozza P, Serini S, Verdecchia S, et al. (2007) Redox regulation of 7-ketocholesterol-induced apoptosis by betacarotene in human macrophages. Free Radic Biol Med 42, 1579-1590.
40. Leonarduzzi G, Vizio B, Sottero B, et al. (2006) Early involvement of ROS overproduction in apoptosis induced by 7-ketocholesterol. Antioxid Redox Signal 8, 375-380.
41. Huang Z, Liu Q, Li W, et al. (2010) 7-Ketocholesterol induces cell apoptosis by activation of nuclear factor kappa B in mouse macrophages. Acta Med Okayama 64, 85-93.
42. Berthier A, Lemaire-Ewing S, Prunet C, et al. (2004) 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 Differen 11, 897-805.
43. Zha J, Harada H, Yang E, et al. (1996) Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not Bcl-XL. Cell 87, 619-628.
44. Wang HG, Pathan N, Ethell IM, et al. (1999) Ca2-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284, 339-343.
45. Yang E, Zha J, Jockel J, et al. (1995) Bad, a heterodimeric partner for Bcl-XL and Bcl-2 displaces Bax and promotes cell death. Cell 80, 285-291.
46. Biasi F, Leonarduzzi G, Vizio B, et al. (2004) Oxysterol mixtures prevent proapoptotic effects of 7-ketocholesterol in macrophages: implications for proatherogenic gene modulation. FASEB J 18, 693-405.
47. Larsson DA, Baird S, Nyhalah JD, et al. (2006) Oxysterol mixtures, in atheroma-relevant proportions, display synergistic and proapoptotic effects. Free Radic Biol Med 41, 902-910.
48. Lizard G, Gueldry S, Sordet O, et al. (1998) Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production. FASEB J 12, 1651-1663.
49. Tabas I (2010) Macrophage death and defective inflammation resolution in atherosclerosis. Nature 10, 36-45.
50. Massey JB & Pownall HJ (2006) Structures of biologically active oxysterols determine their differential effects on phospholipid membranes. Biochemistry 45, 10747-10758.
51. Lordan S, Mackrill JJ & O'Brien NM (2009) Oxysterols and mechanisms of apoptotic signaling: implications in the pathology of degenerative diseases. J Nutr Biochem 20, 321-336.
52. Vejux A, Malvitte L & Lizard G (2008) Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis. Braz J Med Biol Res 41, 545-556.
53. Olkkonen VM & Hynynen R (2009) Interactions of oxysterols with membranes and proteins. Mol Aspects Med 30, 123-133.
54. Massey JB & Pownall HJ (2005) The polar nature of 7-ketocholesterol determines its location within membrane domains and the kinetics of membrane microsolubilization by apolipoprotein A-I. Biochemistry 44, 10423-10433.
55. Han W, Li H, Villar VA, et al. (2008) Lipid rafts keep NADPH oxidase in the inactive state in human renal proximal tubule cells. Hypertension 51, 481-487.
56. Shao D, Segal AW & Dekker LV (2003) Lipid rafts determine efficiency of NADPH oxidase activation in neutrophils. FEBS Lett 550, 101-106.
57. Katsuyama M, Matsuno K & Yabe-Nishimura C (2012) Physiological roles of NOX/NADPH oxidase, the superoxide-generating enzyme. J Clin Biochem Nutr 50, 9-22.
58. Lee CF, Qiao M, Schroder K, et al. (2010) Nox4 is a novel inducible source of reactive oxygen species in monocytes and macrophages and mediates oxidized low density lipoprotein-induced macrophage death. Circ Res 106, 1489-1497.
59. Leto TL, Morand S, Hurt D, et al. (2009) Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid Redox Signal 11, 2607-2619.
60. Rhee SG, Kang SW, Jeong W, et al. (2005) Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 17, 183-189.
61. Serrander L, Cartier L, Bedard K, et al. (2007) NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406, 105-114.
62. Mignotte B & Vayssiere JL (1999) Mitochondria and apoptosis. Eur J Biochem 252, 1-15.
63. Hall AG (1999) The role of glutathione in the regulation of apoptosis. Eur J Clin Invest 29, 238-245.
64. Anilkumar N, Weber R, Zhang M, et al. (2008) Nox4 and Nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 28, 1347-1354.
65. Mahadev K, Motoshima H, Wu X, et al. (2004) The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol 24, 1844-1854.
66. Lee S, Gharavi NM, Honda H, et al. (2009) A role for NADPH oxidase 4 in the activation of vascular endothelial cells by oxidized phospholipids. Free Radic Biol Med 47, 145-151.
67. Zhang F, Jin S, Yi F, et al. (2008) Local production of O2 2 by NAD(P)H oxidase in the sarcoplasmic reticulum of coronary arterial myocytes: cADPR-mediated Ca2 regulation. Cell Signal 20, 637-644.
68. Chen K, Craige SE & Keaney JF Jr (2009) Downstream targets and intracellular compartmentalization in Nox signaling. Antioxid Redox Signal 11, 2467-2480.
69. Schreck R, Rieber P & Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10, 2247-2258.
70. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82, 47-95.
71. Mackrill JJ (2011) Oxysterols and calcium signal transduction. Chem Phys Lip 164, 488-495.
72. Lordan S, O'Brien NM & Mackrill JJ (2009) The role of calcium in apoptosis induced by 7beta-hydroxycholesterol and cholesterol-5beta,6beta- epoxide. J Biochem Mol Toxicol 23, 324-332.
73. Panini SR & Sinensky MS (2001) Mechanisms of oxysterolinduced apoptosis. Curr Opin Lipidol 12, 529-533.
74. Massey JB (2006) Membrane and protein interactions of oxysterols. Curr Opin Lipidol 17, 296-301.
75. Ermak G & Davies KJ (2002) Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 38, 713-721.
76. Bogeski I, Kappl R, Kummerow C, et al. (2011) Redox regulation of calcium ion channels: chemical and physiological aspects. Cell Calcium 50, 407-423.
77. Lizard G, Miguet C, Bessede G, et al. (2000) Impairment with various antioxidants of the loss of mitochondrial transmembrane potential and of the cytosolic release of cytochrome c occuring during 7-ketocholesterol-induced apoptosis. Free Radic Biol Med 28, 743-753.
78. Tesoriere L, Butera D, Pintaudi AM, et al. (2004) Supplementation with cactus pear (Opuntia ficus-indica) fruit decreases oxidative stress in healthy humans: a comparative study with vitamin C. Am J Clin Nutr 80, 391-395.
79. Tesoriere L, Fazzari M, Allegra M, et al. (2005) Biothiols, taurine, and lipid-soluble antioxidants in the edible pulp of Sicilian cactus pear (Opuntia ficus-indica) fruits and changes of bioactive juice components upon industrial processing. J Agric Food Chem 20, 7851-7855.