Formation of cholesterol ozonolysis products in vitro and in vivo through a myeloperoxidase-dependent pathway

Journal of Lipid Research

Volumn 52, Issue 1, 2011, Pages 87-97

  Tomono, Susumu ^a,c   Miyoshi, Noriyuki ^a,c   Shiokawa, Hidemi ^a,c   Iwabuchi, Tomoe ^a,c   Aratani, Yasuaki ^a,d   Higashi, Tatsuya ^b,c   Nukaya, Haruo ^a,c   Ohshima, Hiroshi ^a,c,e  

^a Laboratory of Biochemistry   (Japan)

^b Graduate School of Nutritional   (Japan)

^c Global Center of Excellence (COE) Program   (Japan)

^d UNIVERSITY OF SHIZUOKA   (Japan)

^e YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Infl ammation; Myeloperoxidase; Neutrophils; Secosterol

Indexed keywords

3BETA HYDROXY 5 OXO SECOCHOLESTAN 6 OIC ACID; CHOLESTEROL; MYELOPEROXIDASE; REACTIVE OXYGEN METABOLITE; SECOSTEROL A; SECOSTEROL B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRAIN HL 60; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEUKEMIA CELL; LIVER; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATION; OZONOLYSIS; PRIORITY JOURNAL;

ANIMALS; CELL DIFFERENTIATION; CHOLESTANOL; CHOLESTANONES; CHOLESTEROL; HL-60 CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; NORSTEROIDS; OXIDATION-REDUCTION; OZONE; PEROXIDASE; REACTIVE OXYGEN SPECIES; SECOSTEROIDS; SIGNAL TRANSDUCTION;

EID: 78650864074     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M006775     Document Type: Article

References (34)

1. Babior , B. M. , C. Takeuchi , J. Ruedi , A. Gutierrez , and P. J. Wentworth . 2003 . Investigating antibody-catalyzed ozone generation by human neutrophils. Proc. Natl. Acad. Sci. USA . 100 : 3031-3034.
2. Nieva , J. , and P. J. Wentworth . 2004 . The antibody-catalyzed water oxidation pathway-a new chemical arm to immune defense? Trends Biochem. Sci. 29 : 274-278.
3. Yamashita , K. , T. Miyoshi , T. Arai , N. Endo , H. Itoh , K. Makino , K. Mizugishi , T. Uchiyama , and M. Sasada . 2008 . Ozone production by amino acids contributes to killing of bacteria. Proc. Natl. Acad. Sci. USA . 105 : 16912-16917.
4. Kettle , A. J. , B. M. Clark , and C. C. Winterbourn . 2004 . Superoxide converts indigo carmine to isatin sulfonic acid: implications for the hypothesis that neutrophils produce ozone. J. Biol. Chem. 279 : 18521-18525.
5. Kettle , A. J. , and C. C. Winterbourn . 2005 . Do neutrophils produce ozone? An appraisal of current evidence. Biofactors . 24 : 41-45.
6. Gumulka , J. , and L. L. Smith . 1983 . Ozonization of cholesterol . J. Am. Chem. Soc. 105 : 1972-1979.
7. Jaworski , K. , and L. L. Smith . 1988 . Ozonization of cholesterol in nonparticipating solvents . J. Org. Chem. 53 : 545-554.
8. Paryzek , Z. , J. Martynow , and W. Swoboda . 1990 . The reaction of cholesterol with ozone and alcohols: a revised mechanism and structure of the principal product . J. Chem. Soc., Perkin Trans. 1 : 1222-1223.
9. Wentworth , A. D. , B. D. Song , J. Nieva , A. Shafton , S. Tripurenani , and P. Wentworth, Jr . 2009 . The ratio of cholesterol 5,6-secosterols formed from ozone and singlet oxygen offers insight into the oxidation of cholesterol in vivo. Chem. Commun. (Camb.) ( 21): 3098-3100.
10. Wentworth , P. , Jr., J. Nieva , C. Takeuchi , R. Galve , A. D. Wentworth , R. B. Dilley , G. A. DeLaria , A. Saven , B. M. Babior , K. D. Janda , et al . 2003 . Evidence for ozone formation in human atherosclerotic arteries. Science . 302 : 1053-1056.
11. Zhang , Q. , E. T. Powers , J. Nieva , M. E. Huff , M. A. Dendle , J. Bieschke , C. G. Glabe , A. Eschenmoser , P. J. Wentworth , R. A. Lerner , et al . 2004 . Metabolite-initiated protein misfolding may trigger Alzheimer's disease. Proc. Natl. Acad. Sci. USA . 101 : 4752-4757.
12. Bosco , D. A. , D. M. Fowler , Q. Zhang , J. Nieva , E. T. Powers , P. J. Wentworth , R. A. Lerner , and J. W. Kelly . 2006 . Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fi brilization. Nat. Chem. Biol. 2 : 249-253.
13. Brinkhorst , J. , S. J. Nara , and D. A. Pratt . 2008 . Hock cleavage of cholesterol 5alpha-hydroperoxide: an ozone-free pathway to the cholesterol ozonolysis products identifi ed in arterial plaque and brain tissue. J. Am. Chem. Soc. 130 : 12224-12225.
14. Uemi , M. , G. E. Ronsein , S. Miyamoto , M. H. G. Medeiros , and P. Di Mascio . 2009 . Generation of cholesterol carboxyaldehyde by the reaction of singlet molecular oxygen [O2 (1Delta(g))] as well as ozone with cholesterol. Chem. Res. Toxicol. 22 : 875-884.
15. Tomono , S. , N. Miyoshi , K. Sato , Y. Ohba , and H. Ohshima . 2009 . Formation of cholesterol ozonolysis products through an ozonefree mechanism mediated by the myeloperoxidase-H 2 O 2 -chloride system. Biochem. Biophys. Res. Commun. 383 : 222-227.
16. Bieschke , J. , Q. Zhang , E. T. Powers , R. A. Lerner , and J. W. Kelly . 2005 . Oxidative metabolites accelerate Alzheimer's amyloidogenesis by a two-step mechanism, eliminating the requirement for nucleation. Biochemistry . 44 : 4977-4983.
17. Bieschke , J. , Q. Zhang , D. A. Bosco , R. A. Lerner , E. T. Powers , P. J. Wentworth , and J. W. Kelly . 2006 . Small molecule oxidation products trigger disease-associated protein misfolding. Acc. Chem. Res. 39 : 611-619.
18. Spillantini , M. G. , and M. Goedert . 2000 . The alpha- synucleinopathies: Parkinson's disease, dementia with Lewy bodies, and multiple system atrophy. Ann. N. Y. Acad. Sci. 920 : 16-27.
19. Sathishkumar , K. , S. N. Murthy , and R. M. Uppu . 2007 . Cytotoxic effects of oxysterols produced during ozonolysis of cholesterol in murine GT1-7 hypothalamic neurons. Free Radic. Res. 41 : 82-88.
20. Sathishkumar , K. , M. Haque , T. E. Perumal , J. Francis , and R. M. Uppu . 2005 . A major ozonation product of cholesterol, 3betahydroxy- 5-oxo-5,6-secocholestan-6-al, induces apoptosis in H9c2 cardiomyoblasts. FEBS Lett. 579 : 6444-6450.
21. Collins , S. J. , F. W. Ruscetti , R. E. Gallagher , and R. C. Gallo . 1978 . Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc. Natl. Acad. Sci. USA . 75 : 2458-2462.
22. Aratani , Y. , H. Koyama , S. Nyui , K. Suzuki , F. Kura , and N. Maeda . 1999 . Severe impairment in early host defense against Candida albicans in mice defi cient in myeloperoxidase. Infect. Immun. 67 : 1828-1836.
23. Higashi , T. , T. Ichikawa , S. Inagaki , J. Z. Min , T. Fukushima , and T. Toyo'oka . 2010 . Simple and practical derivatization procedure for enhanced detection of carboxylic acids in liquid chromatography- electrospray ionization-tandem mass spectrometry. J. Pharm. Biomed. Anal. 52 : 809-818.
24. Stewart , C. R. , L. M. Wilson , Q. Zhang , C. L. Pham , L. J. Waddington , M. K. Staples , D. Stapleton , J. W. Kelly , and G. J. Howlett . 2007 . Oxidized cholesterol metabolites found in human atherosclerotic lesions promote apolipoprotein C-II amyloid fi bril formation. Biochemistry . 46 : 5552-5561.
25. Bjorkhem , I. , O. Andersson , U. Diczfalusy , B. Sevastik , R. J. Xiu , C. Duan , and E. Lund . 1994 . Atherosclerosis and sterol 27-hydroxylase: evidence for a role of this enzyme in elimination of cholesterol from human macrophages. Proc. Natl. Acad. Sci. USA . 91 : 8592-8596.
26. Salonen , J. T. , K. Nyyssonen , R. Salonen , E. Porkkala-Sarataho , T. P. Tuomainen , U. Diczfalusy , and I. Bjorkhem . 1997 . Lipoprotein oxidation and progression of carotid atherosclerosis. Circulation . 95 : 840-845. (Pubitemid 27091523)
27. Brown , A. J. , and W. Jessup . 1999 . Oxysterols and atherosclerosis. Atherosclerosis . 142 : 1-28.
28. Larsson , D. A. , S. Baird , J. D. Nyhalah , X-M. Yuan , and W. Li . 2006 . Oxysterol mixtures, in atheroma-relevant proportions, display synergistic and proapoptotic effects. Free Radic. Biol. Med. 41 : 902-910.
29. Vaya , J. , and H. M. Schipper . 2007 . Oxysterols, cholesterol homeostasis, and Alzheimer disease. J. Neurochem. 102 : 1727-1737.
30. Kha , H. T. , B. Basseri , D. Shouhed , J. Richardson , S. Tetradis , T. J. Hahn , and F. Parhami . 2004 . Oxysterols regulate differentiation of mesenchymal stem cells: pro-bone and anti-fat. J. Bone Miner. Res. 19 : 830-840.
31. Shouhed , D. , H. T. Kha , J. A. Richardson , C. M. Amantea , T. J. Hahn , and F. Parhami . 2005 . Osteogenic oxysterols inhibit the adverse effects of oxidative stress on osteogenic differentiation of marrow stromal cells. J. Cell. Biochem. 95 : 1276-1283.
32. Liu , H. , L. Yuan , S. Xu , K. Wang , and T. Zhang . 2005 . Cholestane- 3beta,5alpha,6beta-triol inhibits osteoblastic differentiation and promotes apoptosis of rat bone marrow stromal cells. J. Cell. Biochem. 96 : 198-208
33. Nicholls , S. J. , and S. L. Hazen . 2009 . Myeloperoxidase, modifi ed lipoproteins, and atherogenesis. J. Lipid Res. 50 : S346-S351.
34. Maki , R. A. , V. A. Tyurin , R. C. Lyon , R. L. Hamilton , S. T. DeKosky , V. E. Kagan , and W. F. Reynolds . 2009 . Aberrant expression of myeloperoxidase in astrocytes promotes phospholipid oxidation and memory defi cits in a mouse model of Alzheimer disease. J. Biol. Chem. 284 : 3158-3169.