Implications of cholesterol autoxidation products in the pathogenesis of inflammatory diseases

Biochemical and Biophysical Research Communications

Volumn 446, Issue 3, 2014, Pages 702-708

  Miyoshi, Noriyuki ^a   Iuliano, Luigi ^b   Tomono, Susumu ^a   Ohshima, Hiroshi ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Cholesterol autoxidation; Inflammation; Oxidative stress; Oxysterols; Secosterol

Indexed keywords

CHOLESTEROL; SECOSTEROL; STEROL DERIVATIVE; UNCLASSIFIED DRUG;

BIOLOGICAL ACTIVITY; DERIVATIZATION; FLUORESCENCE ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IN VIVO STUDY; INFLAMMATORY DISEASE; LIPID PEROXIDATION; LIPOGENESIS; MASS SPECTROMETRY; MOLECULAR PATHOLOGY; OXIDATIVE STRESS; OZONOLYSIS; PRIORITY JOURNAL; REVIEW; ULTRAVIOLET RADIATION;

CHOLESTEROL AUTOXIDATION; INFLAMMATION; OXIDATIVE STRESS; OXYSTEROLS; SECOSTEROL;

BIOLOGICAL MARKERS; CHEMISTRY TECHNIQUES, ANALYTICAL; CHOLESTANONES; CHOLESTEROL; FREE RADICALS; HUMANS; INFLAMMATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; OZONE; SECOSTEROIDS; SINGLET OXYGEN;

EID: 84898786240     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.12.107     Document Type: Review

References (72)

1. I.A. Pikuleva Cholesterol-metabolizing cytochromes P450: implications for cholesterol lowering Expert Opin. Drug Metab. Toxicol. 4 2008 1403 1414
2. I. Bjorkhem, and G. Eggertsen Genes involved in initial steps of bile acid synthesis Curr. Opin. Lipidol. 12 2001 97 103
3. I. Bjorkhem, E. Reihner, B. Angelin, S. Ewerth, J.E. Akerlund, and K. Einarsson On the possible use of the serum level of 7alpha-hydroxycholesterol as a marker for increased activity of the cholesterol 7alpha-hydroxylase in humans J. Lipid Res. 28 1987 889 894
4. A. Lovgren-Sandblom, M. Heverin, H. Larsson, E. Lundstrom, J. Wahren, U. Diczfalusy, and I. Bjorkhem Novel LC-MS/MS method for assay of 7alpha-hydroxy-4-cholesten-3-one in human plasma. Evidence for a significant extrahepatic metabolism J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 856 2007 15 19
5. U. Diczfalusy, J. Miura, H.K. Roh, R.A. Mirghani, J. Sayi, H. Larsson, K.G. Bodin, A. Allqvist, M. Jande, J.W. Kim, E. Aklillu, L.L. Gustafsson, and L. Bertilsson 4Beta-hydroxycholesterol 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
6. D. Lutjohann, O. Breuer, G. Ahlborg, I. Nennesmo, A. Siden, U. Diczfalusy, and I. Bjorkhem Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation Proc. Natl. Acad. Sci. U S A 93 1996 9799 9804
7. Y. Ohyama, S. Meaney, M. Heverin, L. Ekstrom, A. Brafman, M. Shafir, U. Andersson, M. Olin, G. Eggertsen, U. Diczfalusy, E. Feinstein, and I. Bjorkhem Studies on the transcriptional regulation of cholesterol 24-hydroxylase (CYP46A1): marked insensitivity toward different regulatory axes J. Biol. Chem. 281 2006 3810 3820
8. N.B. Javitt 25R,26-Hydroxycholesterol revisited: synthesis, metabolism, and biologic roles J. Lipid Res. 43 2002 665 670
9. N.B. Javitt Oxysteroids: a new class of steroids with autocrine and paracrine functions Trends Endocrinol. Metab. 15 2004 393 397
10. E.G. Lund, T.A. Kerr, J. Sakai, W.P. Li, and D.W. Russell CDNA cloning of mouse and human cholesterol 25-hydroxylases, polytopic membrane proteins that synthesize a potent oxysterol regulator of lipid metabolism J. Biol. Chem. 273 1998 34316 34327
11. J. Wong, C.M. Quinn, and A.J. Brown Synthesis of the oxysterol, 24(S), 25-epoxycholesterol, parallels cholesterol production and may protect against cellular accumulation of newly-synthesized cholesterol Lipids Health Dis. 6 2007 10
12. G. Segala, Medina P. de, L. Iuliano, C. Zerbinati, M.R. Paillasse, E. Noguer, F. Dalenc, B. Payre, V.C. Jordan, M. Record, S. Silvente-Poirot, and M. Poirot 5,6-Epoxy-cholesterols contribute to the anticancer pharmacology of tamoxifen in breast cancer cells Biochem. Pharmacol. 86 2013 175 189
13. L. Iuliano Pathways of cholesterol oxidation via non-enzymatic mechanisms Chem. Phys. Lipids 164 2011 457 468
14. A.W. Girotti Lipid hydroperoxide generation, turnover, and effector action in biological systems J. Lipid Res. 39 1998 1529 1542
15. O. Wintersteiner, and S. Bergström The products formed by the action of oxygen on colloidal solutions of cholesterol J. Biol. Chem. 137 1941 785 786
16. H.W. Gardner Oxygen radical chemistry of polyunsaturated fatty acids Free Radical Biol. Med. 7 1989 65 86
17. D. Neshchadin, F. Palumbo, M.S. Sinicropi, I. Andreu, G. Gescheidta, and M.A. Miranda Topological control in radical reactions of cholesterol in model dyads Chem. Sci. 4 2013 1608 1614
18. L. Xu, Z. Korade, and N.A. Porter Oxysterols from free radical chain oxidation of 7-dehydrocholesterol: product and mechanistic studies J. Am. Chem. Soc. 132 2010 2222 2232
19. W. Korytowski, M. Wrona, and A.W. Girotti Radiolabeled cholesterol as a reporter for assessing one-electron turnover of lipid hydroperoxides Anal. Biochem. 270 1999 123 132
20. J. Gumulka, and L.L. Smith Ozonization of cholesterol J. Am. Chem. Soc. 105 1983 1972 1979
21. L.J. Athelstan, J. Beckwith, A.G. Davies, I.G.E. Davison, A. Maccoll, and M.H. Mruzek The mechanism of the rearrangement of allylic hydroperoxides 5α-hydroperoxy-3-β-hydroxycholest-6ene- and 7α-hydroperoxy-3- beta-hydroxycholest-5-ene J. Chem. Soc., Perkin Trans. 22 1989 815 824
22. W. Korytowski, G.J. Bachowski, and A.W. Girotti Photoperoxidation of cholesterol in homogeneous solution, isolated membranes, and cells: comparison of the 5 alpha- and 6 beta-hydroperoxides as indicators of singlet oxygen intermediacy Photochem. Photobiol. 56 1992 1 8
23. W. Korytowski, P.G. Geiger, and A.W. Girotti Lipid hydroperoxide analysis by high-performance liquid chromatography with mercury cathode electrochemical detection Methods Enzymol. 300 1999 23 33
24. J.P. Thomas, and A.W. Girotti Photooxidation of cell membranes in the presence of hematoporphyrin derivative: reactivity of phospholipid and cholesterol hydroperoxides with glutathione peroxidase Biochim. Biophys. Acta 962 1988 297 307
25. J.P. Thomas, M. Maiorino, F. Ursini, and A.W. Girotti Protective action of phospholipid hydroperoxide glutathione peroxidase against membrane-damaging lipid peroxidation. In situ reduction of phospholipid and cholesterol hydroperoxides J. Biol. Chem. 265 1990 454 461
26. J.P. Thomas, P.G. Geiger, M. Maiorino, F. Ursini, and A.W. Girotti Enzymatic reduction of phospholipid and cholesterol hydroperoxides in artificial bilayers and lipoproteins Biochim. Biophys. Acta 1045 1990 252 260
27. S. Tomono, N. Miyoshi, H. Shiokawa, T. Iwabuchi, Y. Aratani, T. Higashi, H. Nukaya, and H. Ohshima Formation of cholesterol ozonolysis products in vitro and in vivo through a myeloperoxidase-dependent pathway J. Lipid Res. 52 2011 87 97
28. N. Miyoshi, N. Iwasaki, S. Tomono, T. Higashi, and H. Ohshima Occurrence of cytotoxic 9-oxononanoyl secosterol aldehydes in human low-density lipoprotein Free Radical Biol. Med. 60 2013 73 79
29. P. Wentworth Jr., J. Nieva, C. Takeuchi, R. Galve, A.D. Wentworth, R.B. Dilley, G.A. DeLaria, A. Saven, B.M. Babior, K.D. Janda, A. Eschenmoser, and R.A. Lerner Evidence for ozone formation in human atherosclerotic arteries Science 302 2003 1053 1056
30. Q. Zhang, E.T. Powers, J. Nieva, M.E. Huff, M.A. Dendle, J. Bieschke, C.G. Glabe, A. Eschenmoser, P. Wentworth Jr., R.A. Lerner, and J.W. Kelly Metabolite-initiated protein misfolding may trigger Alzheimer's disease Proc. Natl. Acad. Sci. U S A 101 2004 4752 4757
31. D.A. Bosco, D.M. Fowler, Q. Zhang, J. Nieva, E.T. Powers, P. Wentworth Jr., R.A. Lerner, and J.W. Kelly Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization Nat. Chem. Biol. 2 2006 249 253
32. P. Wentworth Jr., J.E. McDunn, A.D. Wentworth, C. Takeuchi, J. Nieva, T. Jones, C. Bautista, J.M. Ruedi, A. Gutierrez, K.D. Janda, B.M. Babior, A. Eschenmoser, and R.A. Lerner Evidence for antibody-catalyzed ozone formation in bacterial killing and inflammation Science 298 2002 2195 2199
33. B.M. Babior, C. Takeuchi, J. Ruedi, A. Gutierrez, and P. Wentworth Jr. Investigating antibody-catalyzed ozone generation by human neutrophils Proc. Natl. Acad. Sci. U S A 100 2003 3031 3034
34. K. Yamashita, T. Miyoshi, T. Arai, N. Endo, H. Itoh, K. Makino, K. Mizugishi, T. Uchiyama, and M. Sasada Ozone production by amino acids contributes to killing of bacteria Proc. Natl. Acad. Sci. U S A 105 2008 16912 16917
35. H. Sies Ozone in arteriosclerotic plaques: searching for the "smoking gun" Angew. Chem., Int. Ed. Engl. 43 2004 3514 3515
36. L.L. Smith Oxygen, oxysterols, ouabain, and ozone: a cautionary tale Free Radical Biol. Med. 37 2004 318 324
37. W.A. Pryor, K.N. Houk, C.S. Foote, J.M. Fukuto, L.J. Ignarro, G.L. Squadrito, and K.J. Davies Free radical biology and medicine: it's a gas, man! Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 2006 R491 R511
38. g)] as well as ozone with cholesterol Chem. Res. Toxicol. 22 2009 875 884
39. 2-chloride system Biochem. Biophys. Res. Commun. 383 2009 222 227
40. A.L. Garner, C.M. St Croix, B.R. Pitt, G.D. Leikauf, S. Ando, and K. Koide Specific fluorogenic probes for ozone in biological and atmospheric samples Nat. Chem. 1 2009 316 321
41. A.D. Wentworth, B.D. Song, J. Nieva, A. Shafton, S. Tripurenani, and P. Wentworth Jr. The ratio of cholesterol 5,6-secosterols formed from ozone and singlet oxygen offers insight into the oxidation of cholesterol in vivo Chem. Commun. (Cambridge, U.K.) 21 2009 3098 3100
42. C.R. Stewart, L.M. Wilson, Q. Zhang, C.L. Pham, L.J. Waddington, M.K. Staples, D. Stapleton, J.W. Kelly, and G.J. Howlett Oxidized cholesterol metabolites found in human atherosclerotic lesions promote apolipoprotein C-II amyloid fibril formation Biochemistry 46 2007 5552 5561
43. D.M. Hatters, C.E. MacPhee, L.J. Lawrence, W.H. Sawyer, and G.J. Howlett Human apolipoprotein C-II forms twisted amyloid ribbons and closed loops Biochemistry 39 2000 8276 8283
44. C. Rocken, J. Tautenhahn, F. Buhling, D. Sachwitz, S. Vockler, A. Goette, and T. Burger Prevalence and pathology of amyloid in atherosclerotic arteries Arterioscler. Thromb. Vasc. Biol. 26 2006 676 677
45. L.A. Medeiros, T. Khan, J.B. El Khoury, C.L. Pham, D.M. Hatters, G.J. Howlett, R. Lopez, K.D. O'Brien, and K.J. Moore Fibrillar amyloid protein present in atheroma activates CD36 signal transduction J. Biol. Chem. 279 2004 10643 10648
46. P.D. Mehta, T. Pirttila, B.A. Patrick, M. Barshatzky, and S.P. Mehta Amyloid beta protein 1-40 and 1-42 levels in matched cerebrospinal fluid and plasma from patients with Alzheimer disease Neurosci. Lett. 304 2001 102 106
47. J. Bieschke, Q. Zhang, E.T. Powers, R.A. Lerner, and J.W. Kelly Oxidative metabolites accelerate Alzheimer's amyloidogenesis by a two-step mechanism, eliminating the requirement for nucleation Biochemistry 44 2005 4977 4983
48. K. Usui, J.D. Hulleman, J.F. Paulsson, S.J. Siegel, E.T. Powers, and J.W. Kelly Site-specific modification of Alzheimer's peptides by cholesterol oxidation products enhances aggregation energetics and neurotoxicity Proc. Natl. Acad. Sci. U S A 106 2009 18563 18568
49. K. Karu, M. Hornshaw, G. Woffendin, K. Bodin, M. Hamberg, G. Alvelius, J. Sjovall, J. Turton, Y. Wang, and W.J. Griffiths Liquid chromatography-mass spectrometry utilizing multi-stage fragmentation for the identification of oxysterols J. Lipid Res. 48 2007 976 987
50. H. Komatsu, L. Liu, I.V. Murray, and P.H. Axelsen A mechanistic link between oxidative stress and membrane mediated amyloidogenesis revealed by infrared spectroscopy Biochim. Biophys. Acta 1768 2007 1913 1922
51. I.V. Murray, L. Liu, H. Komatsu, K. Uryu, G. Xiao, J.A. Lawson, and P.H. Axelsen Membrane-mediated amyloidogenesis and the promotion of oxidative lipid damage by amyloid beta proteins J. Biol. Chem. 282 2007 9335 9345
52. N.K. Cygan, J.C. Scheinost, T.D. Butters, and P. Wentworth Jr. Adduction of cholesterol 5,6-secosterol aldehyde to membrane-bound myelin basic protein exposes an immunodominant epitope Biochemistry 50 2011 2092 2100
53. J. Nieva, B.D. Song, J.K. Rogel, D. Kujawara, L. Altobel III, A. Izharrudin, G.E. Boldt, R.K. Grover, A.D. Wentworth, and P. Wentworth Jr. Cholesterol secosterol aldehydes induce amyloidogenesis and dysfunction of wild-type tumor protein p53 Chem. Biol. 18 2011 920 927
54. J. Nieva, A. Shafton, L.J. Altobell III, S. Tripuraneni, J.K. Rogel, A.D. Wentworth, R.A. Lerner, and P. Wentworth Jr. Lipid-derived aldehydes accelerate light chain amyloid and amorphous aggregation Biochemistry 47 2008 7695 7705
55. J.C. Scheinost, D.P. Witter, G.E. Boldt, J. Offer, and P. Wentworth Jr. Cholesterol secosterol adduction inhibits the misfolding of a mutant prion protein fragment that induces neurodegeneration Angew. Chem., Int. Ed. Engl. 48 2009 9469 9472
56. E. Wachtel, D. Bach, R.F. Epand, A. Tishbee, and R.M. Epand A product of ozonolysis of cholesterol alters the biophysical properties of phosphatidylethanolamine membranes Biochemistry 45 2006 1345 1351
57. D. Bach, E. Wachtel, and I.R. Miller Kinetics of Schiff base formation between the cholesterol ozonolysis product 3-beta-hydroxy-5-oxo-5,6- secocholestan-6-al and phosphatidylethanolamine Chem. Phys. Lipids 157 2009 51 55
58. D. Bach, R.F. Epand, R.M. Epand, I.R. Miller, and E. Wachtel The oxysterol 3beta-hydroxy-5-oxo-5,6-secocholestan-6-al changes the phase behavior and structure of phosphatidylethanolamine-phosphatidylcholine mixtures Chem. Phys. Lipids 164 2011 672 679
59. T.C. Genaro-Mattos, P.P. Appolinario, K.C. Mugnol, C. Bloch Jr., I.L. Nantes, Mascio.P. Di, and S. Miyamoto Covalent binding and anchoring of cytochrome c to mitochondrial mimetic membranes promoted by cholesterol carboxyaldehyde Chem. Res. Toxicol. 26 2013 1536 1544
60. Y.L. Lai, S. Tomono, N. Miyoshi, and H. Ohshima Inhibition of endothelial- and neuronal-type, but not inducible-type, nitric oxide synthase by the oxidized cholesterol metabolite secosterol aldehyde: implications for vascular and neurodegenerative diseases J. Clin. Biochem. Nutr. 50 2012 84 89
61. K. Sathishkumar, S.N. Murthy, and R.M. Uppu Cytotoxic effects of oxysterols produced during ozonolysis of cholesterol in murine GT1-7 hypothalamic neurons Free Radical Res. 41 2007 82 88
62. K. Sathishkumar, M. Haque, T.E. Perumal, J. Francis, and R.M. Uppu A major ozonation product of cholesterol, 3β-hydroxy-5-oxo-5,6-secocholestan- 6-al, induces apoptosis in H9c2 cardiomyoblasts FEBS Lett. 579 2005 6444 6450
63. K. Sathishkumar, X. Gao, A.C. Raghavamenon, N. Parinandi, W.A. Pryor, and R.M. Uppu Cholesterol secoaldehyde induces apoptosis in H9c2 cardiomyoblasts through reactive oxygen species involving mitochondrial and death receptor pathways Free Radical Biol. Med. 47 2009 548 558
64. K. Sathishkumar, X. Xi, R. Martin, and R.M. Uppu Cholesterol secoaldehyde, an ozonation product of cholesterol, induces amyloid aggregation and apoptosis in murine GT1-7 hypothalamic neurons J. Alzheimers Dis. 11 2007 261 274
65. S. Anticoli, M. Arciello, A. Mancinetti, Martinis.M. De, L. Ginaldi, L. Iuliano, and C. Balsano 7-Ketocholesterol and 5,6-secosterol modulate differently the stress-activated mitogen-activated protein kinases (MAPKs) in liver cells J. Cell Physiol. 222 2010 586 595
66. S. Tomono, Y. Yasue, N. Miyoshi, and H. Ohshima Cytotoxic effects of secosterols and their derivatives on several cultured cells Biosci. Biotechnol. Biochem. 77 2013 651 653
67. K. Wang, E. Bermudez, and W.A. Pryor The ozonation of cholesterol: separation and identification of 2,4-dinitrophenylhydrazine derivatization products of 3 beta-hydroxy-5-oxo-5,6-secocholestan-6-al Steroids 58 1993 225 229
68. F.V. Mansano, R.M. Kazaoka, G.E. Ronsein, F.M. Prado, T.C. Genaro-Mattos, M. Uemi, Mascio.P. Di, and S. Miyamoto Highly sensitive fluorescent method for the detection of cholesterol aldehydes formed by ozone and singlet molecular oxygen Anal. Chem. 82 2010 6775 6781
69. S. Tomono, N. Miyoshi, M. Ito, T. Higashi, and H. Ohshima A highly sensitive LC-ESI-MS/MS method for the quantification of cholesterol ozonolysis products secosterol-A and secosterol-B after derivatization with 2-hydrazino-1-methylpyridine J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 879 2011 2802 2808
70. D. Datta, N. Vaidehi, X. Xu, and W.A. Goddard III Mechanism for antibody catalysis of the oxidation of water by singlet dioxygen Proc. Natl. Acad. Sci. U S A 99 2002 2636 2641
71. A.D. Wentworth, L.H. Jones, P. Wentworth Jr., K.D. Janda, and R.A. Lerner Antibodies have the intrinsic capacity to destroy antigens Proc. Natl. Acad. Sci. U S A 97 2000 10930 10935
72. W.A. Pryor, K. Wang, and E. Bermudez Cholesterol ozonation products as biomarkers for ozone exposure in rats Biochem. Biophys. Res. Commun. 188 1992 618 623