Formation of electrophilic oxidation products from mitochondrial cardiolipin in vitro and in vivo in the context of apoptosis and atherosclerosis

Redox Biology

Volumn 2, Issue 1, 2014, Pages 878-883

  Zhong, Huiqin ^a,b,c   Lu, Jianhong ^a,b,c   Xia, Lin ^a,c   Zhu, Mingjiang ^a,c   Yin, Huiyong ^a,b,c,d  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c BEIJING HOSPITAL   (China)

^d SHANGHAITECH UNIVERSITY   (China)

Author keywords

4 hydroxy 2 nonenal (4 HNE); Apoptosis; Atherosclerosis; Cardiolipin; Epoxyalcohol aldehyde CL (EAA CL); Lipid peroxidation; Liquid chromatography mass spectrometry (LC MS); Mitochondria

Indexed keywords

4 HYDROXYNONENAL; ALDEHYDE; CARDIOLIPIN; CYTOCHROME C; ELECTROPHILE; EPOXYALCOHOL ALDEHYDE CARDIOLIPIN; LIPID; LOW DENSITY LIPOPROTEIN RECEPTOR; PARACETAMOL; UNCLASSIFIED DRUG; PROTEIN BID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CELL FUNCTION; DIETARY INTAKE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE INACTIVATION; IN VITRO STUDY; IN VIVO STUDY; LIPID PEROXIDATION; LIQUID CHROMATOGRAPHY; LIVER; MASS SPECTROMETRY; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; SYNTHESIS; ANIMAL; ARTERIOSCLEROSIS; CHEMISTRY; DEFICIENCY; DRUG EFFECTS; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KNOCKOUT MOUSE; LIPID DIET; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY;

ACETAMINOPHEN; ANIMALS; APOPTOSIS; ARTERIOSCLEROSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CARDIOLIPINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIET, HIGH-FAT; LIVER; MASS SPECTROMETRY; MICE; MICE, KNOCKOUT; MITOCHONDRIA; OXIDATION-REDUCTION; RECEPTORS, LDL;

EID: 84904316136     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2014.04.003     Document Type: Article

References (41)

1. Gonzalvez F., Gottlieb E. Cardiolipin: setting the beat of apoptosis. Apoptosis: An international Journal on Programmed Cell Death 2007, 12(5):877-885. http://www.ncbi.nlm.nih.gov/pubmed/17294083, 10.1007/s10495-007-0718-8.
2. Kiebish M.A., Yang K., Sims H.F., Jenkins C.M., Liu X., Mancuso D.J., Zhao Z., Guan S., Abendschein D.R., Han X., et al. Myocardial regulation of lipidomic flux by cardiolipin synthase: setting the beat for bioenergetic efficiency. Journal of Biological Chemistry 2012, 287(30):25086-25097. http://www.ncbi.nlm.nih.gov/pubmed/22584571, 10.1074/jbc.M112.340521.
3. Yin H., Zhu M. Free radical oxidation of cardiolipin: chemical mechanisms, detection and implication in apoptosis, mitochondrial dysfunction and human diseases. Free Radical Research 2012, 46(8):959-974. http://www.ncbi.nlm.nih.gov/pubmed/22468920, 10.3109/10715762.2012.676642.
4. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nature Chemical Biology 2005, 1(4):223-232. http://www.ncbi.nlm.nih.gov/pubmed/16408039, 10.1038/nchembio727.
5. Chu C.T., Ji J., Dagda R.K., Jiang J.F., Tyurina Y.Y., Kapralov A.A., Tyurin V.A., Yanamala N., Shrivastava I.H., Mohammadyani D., et al. Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nature Cell Biology 2013, 15(10):1197-1205. http://www.ncbi.nlm.nih.gov/pubmed/24036476, 10.1038/ncb2837.
6. 2+ in mitochondrial dysfunction and disease. Cell Calcium 2009, 45(6):643-650. http://www.ncbi.nlm.nih.gov/pubmed/19368971, 10.1016/j.ceca.2009.03.012.
7. Kagan V.E., Bayir H.A., Belikova N.A., Kapralov O., Tyurina Y.Y., Tyurin V.A., Jiang J., Stoyanovsky D.A., Wipf P., Kochanek P.M., et al. Cytochrome c/cardiolipin relations in mitochondria: a kiss of death. Free Radical Biology and Medicine 2009, 46(11):1439-1453. http://www.ncbi.nlm.nih.gov/pubmed/19285551, 10.1016/j.freeradbiomed.2009.03.004.
8. Yin H., Xu L., Porter N.A. Free radical lipid peroxidation: mechanisms and analysis. Chemical Reviews 2011, 111(10):5944-5972. http://www.ncbi.nlm.nih.gov/pubmed/21861450, 10.1021/cr200084z.
9. Lee S., Birukov K.G., Romanoski C.E., Springstead J.R., Lusis A.J., Berliner J.A. Role of phospholipid oxidation products in atherosclerosis. Circulation Research 2012, 111(6):778-799. http://www.ncbi.nlm.nih.gov/pubmed/22935534, 10.1161/CIRCRESAHA.111.256859.
10. West J.D., Marnett L.J. Endogenous reactive intermediates as modulators of cell signaling and cell death. Chemical Research in Toxicology 2006, 19(2):173-194. http://www.ncbi.nlm.nih.gov/pubmed/16485894, 10.1021/tx050321u.
11. Poli G., Biasi F., Leonarduzzi G. 4-Hydroxynonenal-protein adducts:a reliable biomarker of lipid oxidation in liver diseases. Molecular Aspects of Medicine 2008, 29(1-2):67-71. http://www.ncbi.nlm.nih.gov/pubmed/18158180, 10.1016/j.mam.2007.09.016.
12. Yun M.R., Im D.S., Lee S.J., Park H.M., Bae S.S., Lee W.S., Kim C.D. 4-Hydroxynonenal enhances CD36 expression on murine macrophages via p38 MAPK-mediated activation of 5-lipoxygenase. Free Radical Biologyand Medicine 2009, 46(5):692-698. http://www.ncbi.nlm.nih.gov/pubmed/19135147, 10.1016/j.freeradbiomed.2008.12.013.
13. Schneider C., Porter N.A., Brash A.R. Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. Journal of Biological Chemistry 2008, 283(23):15539-15543. http://www.ncbi.nlm.nih.gov/pubmed/18285327, 10.1074/jbc.R800001200.
14. Schneider C., Tallman K.A., Porter N.A., Brash A.R. Two distinct pathways of formation of 4-hydroxynonenal. Mechanisms of nonenzymatic transformation of the 9- and 13-hydroperoxides of linoleic acid to 4-hydroxyalkenals. Journal of Biological Chemistry 2001, 276(24):20831-20838. http://www.ncbi.nlm.nih.gov/pubmed/11259420, 10.1074/jbc.M101821200.
15. Yin H., Vergeade A., Shi Q., Zackert W.E., Gruenberg K.C., Bokiej M., Amin T., Ying W., Masterson T.S., Zinkel S.S., et al. Acetaminophen inhibits cytochrome c redox cycling induced lipid peroxidation. Biochemical and Biophysical Research Communications 2012, 423(2):224-228. http://www.ncbi.nlm.nih.gov/pubmed/22634010, 10.1016/j.bbrc.2012.05.058.
16. Saraswathi V., Gao L., Morrow J.D., Chait A., Niswender K.D., Hasty A.H. Fish oil increases cholesterol storage in white adipose tissue with concomitant decreases in inflammation, hepatic steatosis, and atherosclerosis in mice. Journal of Nutrition 2007, 137(7):1776-1782. http://www.ncbi.nlm.nih.gov/pubmed/17585030.
17. Liu W., Porter N.A., Schneider C., Brash A.R., Yin H. Formation of 4-hydroxynonenal from cardiolipin oxidation: intramolecular peroxyl radical addition and decomposition. Free Radical Biologyand Medicine 2011, 50(1):166-178. http://www.ncbi.nlm.nih.gov/pubmed/21047551, 10.1016/j.freeradbiomed.2010.10.709.
18. Frezza C., Cipolat S., Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nature Protocols 2007, 2(2):287-295. http://www.ncbi.nlm.nih.gov/pubmed/17406588, 10.1038/nprot.2006.478.
19. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Developmental Cell 2002, 2(1):55-67. http://www.ncbi.nlm.nih.gov/pubmed/11782314, 10.1016/S1534-5807(01)00116-2.
20. Steinberg D., Parhasarathy S., Carew T.E., Khoo J.C., Witztum J.L. Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. New England Journal of Medicine 1989, 320:915-924. http://www.ncbi.nlm.nih.gov/pubmed/2648148.
21. Mali V.R., Palaniyandi S.S. Regulation and therapeutic strategies of 4-hydroxy-2-nonenal metabolism in heart disease. Free Radical Research 2014, 48:251-263. http://www.ncbi.nlm.nih.gov/pubmed/24237196.
22. Benedetti A., Comporti M., Esterbauer H. Identification of 4-hydroxynonenal as a cytotoxic product originating from the peroxidation of liver microsomal lipids. Biochimica et Biophysica Acta 1980, 620(2):281-296. http://www.ncbi.nlm.nih.gov/pubmed/6254573, 10.1016/0005-2760(80)90209-X.
23. Schneider C., Boeglin W.E., Yin H., Porter N.A., Brash A.R. Intermolecular peroxyl radical reactions during autoxidation of hydroxy and hydroperoxy arachidonic acids generate a novel series of epoxidized products. Chemical Research in Toxicology 2008, 21(4):895-903. http://www.ncbi.nlm.nih.gov/pubmed/18324788, 10.1021/tx700357u.
24. Schneider C., Porter N.A., Brash A.R. Routes to 4-hydroxynonenal: fundamental issues in the mechanisms of lipid peroxidation. Journal of Biological Chemistry 2008, 283(23):15539-15543. http://www.ncbi.nlm.nih.gov/pubmed/18285327, 10.1074/jbc.R800001200.
25. 2 synthases. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:7130-7135. http://www.ncbi.nlm.nih.gov/pubmed/12011469, 10.1073/pnas.102588199.
26. Boutaud O., Moore K.P., Reeder B.J., Harry D., Howie A.J., Wang S., Carney C.K., Masterson T.S., Amin T., Wright D.W., et al. Acetaminophen inhibits hemoprotein-catalyzed lipid peroxidation and attenuates rhabdomyolysis-induced renal failure. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(6):2699-2704. http://www.ncbi.nlm.nih.gov/pubmed/20133658, 10.1073/pnas.0910174107.
27. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nature Chemical Biology 2005, 1(4):223-232. http://www.ncbi.nlm.nih.gov/pubmed/16408039, 10.1038/nchembio727.
28. Ji J., Kline A.E., Amoscato A., Samhan-Arias A.K., Sparvero L.J., Tyurin V.A., Tyurina Y.Y., Fink B., Manole M.D., Puccio A.M., et al. Lipidomics identifies cardiolipin oxidation as a mitochondrial target for redox therapy of brain injury. Nature Neuroscience 2012, 15(10):1407-1413. http://www.ncbi.nlm.nih.gov/pubmed/22922784, 10.1038/nn.3195.
29. Ji C., Amarnath V., Pietenpol J.A., Marnett L.J. 4-Hydroxynonenal induces apoptosis via caspase-3 activation and cytochrome c release. Chemical Research in Toxicology 2001, 14(8):1090-1096. http://www.ncbi.nlm.nih.gov/pubmed/11511183, 10.1021/tx000186f.
30. Ma H., Guo R., Yu L., Zhang Y., Ren J. Aldehyde dehydrogenase 2 (ALDH2) rescues myocardial ischaemia/reperfusion injury: role of autophagy paradox and toxic aldehyde. European Heart Journal 2011, 32(8):1025-1038. http://www.ncbi.nlm.nih.gov/pubmed/20705694, 10.1093/eurheartj/ehq253.
31. Su J., Frostegård A.G., Hua X., Gustafsson T., Jogestrand T., Hafström I., Frostegård J. Low levels of antibodies against oxidized but not nonoxidized cardiolipin and phosphatidylserine are associated with atherosclerotic plaques in systemic lupus erythematosus. Journal of Rheumatology 2013, 40(11):1856-1864. http://www.ncbi.nlm.nih.gov/pubmed/24037548, 10.3899/jrheum.121173.
32. Wall S.B., Smith M.R., Ricart K., Zhou F., Vayalil P.K., Oh J.-Y., Landar A. Detection of electrophile-sensitive proteins. Biochimica et Biophysica Acta 2014, 1840:913-922. http://www.ncbi.nlm.nih.gov/pubmed/24021887.
33. Wang H.-Y.J., Jackson S.N., Woods A.S. Direct MALDI-MS analysis of cardiolipin from rat organs sections. Journal of the American Society for Mass Spectrometry 2007, 18(3):567-577. http://www.ncbi.nlm.nih.gov/pubmed/17157526, 10.1016/j.jasms.2006.10.023.
34. Hoye A.T., Davoren J.E., Wipf P., Fink M.P., Kagan V.E. Targeting mitochondria. Accounts of Chemical Research 2008, 41(1):87-97. http://www.ncbi.nlm.nih.gov/pubmed/18193822, 10.1021/ar700135m.
35. Belikova N.A., Tyurina Y.Y., Borisenko G., Tyurin V., Samhan Arias A.K., Yanamala N., Furtmuller P.G., Klein-Seetharaman J., Obinger C., Kagan V.E. Heterolytic reduction of fatty acid hydroperoxides by cytochrome c/cardiolipin complexes: antioxidant function in mitochondria. Journal of the American Chemical Society 2009, 131(32):11288-11289. http://www.ncbi.nlm.nih.gov/pubmed/19627079, 10.1021/ja904343c.
36. Liang H., Ran Q., Jang Y.C., Holstein D., Lechleiter J., McDonald-Marsh T., Musatov A., Song W., Van Remmen H., Richardson A. Glutathione peroxidase 4 differentially regulates the release of apoptogenic proteins from mitochondria. Free Radical Biologyand Medicine 2009, 47(3):312-320. http://www.ncbi.nlm.nih.gov/pubmed/19447173, 10.1016/j.freeradbiomed.2009.05.012.
37. Milne G.L., Yin H., Morrow J.D. Human biochemistry of the isoprostane pathway. Journal of Biological Chemistry 2008, 283(23):15533-15537. http://www.ncbi.nlm.nih.gov/pubmed/18285331, 10.1074/jbc.R700047200.
38. Milne G.L., YinH., Hardy K.D., Davies S.S., Roberts L.J. Isoprostane generation and function. Chemical Reviews 2011, 111(10):5973-5996. http://www.ncbi.nlm.nih.gov/pubmed/21848345, 10.1021/cr200160h.
39. 2 by overexpressing peroxiredoxin 3 improves glucose tolerance in mice. Aging Cell 2008, 7(6):866-878. http://www.ncbi.nlm.nih.gov/pubmed/18778410, 10.1111/j.1474-9726.2008.00432.x.
40. Ouellet M., Percival M.D. Mechanism of acetaminophen inhibition of cyclooxygenase isoforms. Archives of Biochemistry and Biophysics 2001, 387(2):273-280. http://www.ncbi.nlm.nih.gov/pubmed/11370851, 10.1006/abbi.2000.2232.
41. Boutaud O., Moore K.P., Reeder B.J., Harry D., Howie A.J., Wang S., Carney C.K., Masterson T.S., Amin T., Wright D.W., et al. Acetaminophen inhibits hemoprotein-catalyzed lipid peroxidation and attenuates rhabdomyolysis-induced renal failure. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(6):2699-2704. http://www.ncbi.nlm.nih.gov/pubmed/20133658, 10.1073/pnas.0910174107.