Effects of 4-hydroxynonenal on vascular endothelial and smooth muscle cell redox signaling and function in health and disease

Redox Biology

Volumn 1, Issue 1, 2013, Pages 319-331

  Chapple, Sarah J ^a   Cheng, Xinghua ^a   Mann, Giovanni E ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

4 hydroxynonenal; Endothelial cells; Nrf2; Redox signaling; Vascular biology; Vascular smooth muscle cells

Indexed keywords

4 HYDROXYNONENAL; ALDEHYDE REDUCTASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN 72; HEME OXYGENASE 1; INTERSTITIAL COLLAGENASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE SYNTHASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN DISULFIDE ISOMERASE; PROTEIN KINASE B; PROTEIN KINASE C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RLIP76 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR ELK 1; TRANSCRIPTION FACTOR NRF2; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; 4-HYDROXY-2-NONENAL; ALDEHYDE;

APOPTOSIS; ATHEROSCLEROSIS; BIOSYNTHESIS; BLOOD VESSEL PARAMETERS; CELL DIFFERENTIATION; CELL FUNCTION; CELL METABOLISM; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONJUGATION; DIABETES MELLITUS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM CELL; ENZYME ACTIVATION; HALF LIFE TIME; HUMAN; INTRACELLULAR SIGNALING; LIPID PEROXIDATION; NERVE DEGENERATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REDOX SIGNALING; REVIEW; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASOPROTECTION; CYTOLOGY; ENDOPLASMIC RETICULUM; HEALTH; METABOLISM; MITOCHONDRION; PATHOLOGY; SIGNAL TRANSDUCTION; SMOOTH MUSCLE;

ALDEHYDES; ENDOPLASMIC RETICULUM; ENDOTHELIUM, VASCULAR; HEALTH; HUMANS; MITOCHONDRIA; MUSCLE, SMOOTH; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION;

EID: 84880251695     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.04.001     Document Type: Review

References (148)

1. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology and Medicine 1991, 11:81-128.
2. 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, 620:281-296.
3. Chung F.L., Nath R.G., Ocando J., Nishikawa A., Zhang L. Deoxyguanosine adducts of t-4-hydroxy-2-nonenal are endogenous DNA lesions in rodents and humans: detection and potential sources. Cancer Research 2000, 60:1507-1511.
4. Nair J., De Flora S., Izzotti A., Bartsch H. Lipid peroxidation-derived etheno-DNA adducts in human atherosclerotic lesions. Mutation Research 2007, 621:95-105.
5. Doorn J.A., Petersen D.R. Covalent adduction of nucleophilic amino acids by 4-hydroxynonenal and 4-oxononenal. Chemico-Biological Interactions 2003, 143-144:93-100.
6. Uchida K., Stadtman E.R. Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase. A possible involvement of intra- and intermolecular cross-linking reaction. Journal of Biological Chemistry 1993, 268:6388-6393.
7. Selley M.L., Bartlett M.R., McGuiness J.A., Hapel A.J., Ardlie N.G. Determination of the lipid peroxidation product trans-4-hydroxy-2-nonenal in biological samples by high-performance liquid chromatography and combined capillary column gas chromatography-negative-ion chemical ionisation mass spectrometry. Journal of Chromatography 1989, 488:329-340.
8. Gil L., Siems W., Mazurek B., Gross J., Schroeder P., Voss P., Grune T. Age-associated analysis of oxidative stress parameters in human plasma and erythrocytes. Free Radical Research 2006, 40:495-505.
9. Selley M.L. Determination of the lipid peroxidation product (E)-4-hydroxy-2-nonenal in clinical samples by gas chromatography--negative-ion chemical ionisation mass spectrometry of the O-pentafluorobenzyl oxime. Journal of Chromatography B: Biomedical Sciences and Applications 1997, 691:263-268.
10. Herbst U., Toborek M., Kaiser S., Mattson M.P., Hennig B. 4-Hydroxynonenal induces dysfunction and apoptosis of cultured endothelial cells. Journal of Cellular Physiology 1999, 181:295-303.
11. Ong W.Y., Jenner A.M., Pan N., Ong C.N., Halliwell B. Elevated oxidative stress, iron accumulation around microvessels and increased 4-hydroxynonenal immunostaining in zone 1 of the liver acinus in hypercholesterolemic rabbits. Free Radical Research 2009, 43:241-249.
12. Hoff H.F., O'Neil J., Chisolm G.M., Cole T.B., Quehenberger O., Esterbauer H., Jurgens G. Modification of low density lipoprotein with 4-hydroxynonenal induces uptake by macrophages. Arteriosclerosis 1989, 9:538-549.
13. Salomon R.G., Kaur K., Podrez E., Hoff H.F., Krushinsky A.V., Sayre L.M. HNE-derived 2-pentylpyrroles are generated during oxidation of LDL, are more prevalent in blood plasma from patients with renal disease or atherosclerosis, and are present in atherosclerotic plaques. Chemical Research in Toxicology 2000, 13:557-564.
14. Gueraud F., Atalay M., Bresgen N., Cipak A., Eckl P.M., Huc L., Jouanin I., Siems W., Uchida K. Chemistry and biochemistry of lipid peroxidation products. Free Radical Research 2010, 44:1098-1124.
15. Hill B.G., Haberzettl P., Ahmed Y., Srivastava S., Bhatnagar A. Unsaturated lipid peroxidation-derived aldehydes activate autophagy in vascular smooth-muscle cells. Biochemical Journal 2008, 410:525-534.
16. Botzen D., Grune T. Degradation of HNE-modified proteins--possible role of ubiquitin. Redox Report 2007, 12:63-67.
17. Grune T., Davies K.J. The proteasomal system and HNE-modified proteins. Molecular Aspects of Medicine 2003, 24:195-204.
18. Srivastava S., Liu S.Q., Conklin D.J., Zacarias A., Srivastava S.K., Bhatnagar A. Involvement of aldose reductase in the metabolism of atherogenic aldehydes. Chemico-Biological Interactions 2001, 130-132:563-571.
19. Siems W., Grune T. Intracellular metabolism of 4-hydroxynonenal. Molecular Aspects of Medicine 2003, 24:167-175.
20. Yang Y., Yang Y., Trent M.B., He N., Lick S.D., Zimniak P., Awasthi Y.C., Boor P.J. Glutathione-S-transferase A4-4 modulates oxidative stress in endothelium: possible role in human atherosclerosis. Atherosclerosis 2004, 173:211-221.
21. Tjalkens R.B., Cook L.W., Petersen D.R. Formation and export of the glutathione conjugate of 4-hydroxy-2, 3-E-nonenal (4-HNE) in hepatoma cells. Archives of Biochemistry and Biophysics 1999, 361:113-119.
22. Siems W.G., Zollner H., Grune T., Esterbauer H. Metabolic fate of 4-hydroxynonenal in hepatocytes: 1,4-dihydroxynonene is not the main product. Journal of Lipid Research 1997, 38:612-622.
23. Whitsett J., Picklo M.J., Vasquez-Vivar J. 4-Hydroxy-2-nonenal increases superoxide anion radical in endothelial cells via stimulated GTP cyclohydrolase proteasomal degradation. Arteriosclerosis, Thrombosis, and Vascular Biology 2007, 27:2340-2347.
24. Poot M., Verkerk A., Koster J.F., Esterbauer H., Jongkind J.F. Influence of cumene hydroperoxide and 4-hydroxynonenal on the glutathione metabolism during in vitro ageing of human skin fibroblasts. European Journal of Biochemistry 1987, 162:287-291.
25. Romero F.J., Romero M.J., Bosch-Morell F., Martinez M.C., Medina P., Lluch S. 4-hydroxynonenal-induced relaxation of human mesenteric arteries. Free Radical Biology and Medicine 1997, 23:521-523.
26. Voskoboinik I., Soderholm K., Cotgreave I.A. Ascorbate and glutathione homeostasis in vascular smooth muscle cells: cooperation with endothelial cells. American Journal of Physiology 1998, 275:C1031-1039.
27. Buckley B.J., Whorton A.R. Adaptive responses to peroxynitrite: increased glutathione levels and cystine uptake in vascular cells. American Journal of Physiology-Cell Physiology 2000, 279:C1168-1176.
28. Spycher S., Tabataba-Vakili S., O'Donnell V.B., Palomba L., Azzi A. 4-hydroxy-2,3-trans-nonenal induces transcription and expression of aldose reductase. Biochemical and Biophysical Research Communications 1996, 226:512-516.
29. Ruef J., Liu S.Q., Bode C., Tocchi M., Srivastava S., Runge M.S., Bhatnagar A. Involvement of aldose reductase in vascular smooth muscle cell growth and lesion formation after arterial injury. Arteriosclerosis, Thrombosis, and Vascular Biology 2000, 20:1745-1752.
30. Poli G., Schaur R.J., Siems W.G., Leonarduzzi G. 4-hydroxynonenal: a membrane lipid oxidation product of medicinal interest. Medical Care Research and Review 2008, 28:569-631.
31. Higdon A., Diers A.R., Oh J.Y., Landar A., Darley-Usmar V.M. Cell signaling by reactive lipid species: new concepts and molecular mechanisms. Biochemical Journal 2012, 442:453-464.
32. Forman H.J., Fukuto J.M., Miller T., Zhang H., Rinna A., Levy S. The chemistry of cell signaling by reactive oxygen and nitrogen species and 4-hydroxynonenal. Archives of Biochemistry and Biophysics 2008, 477:183-195.
33. Esterbauer H. Cytotoxicity and genotoxicity of lipid-oxidation products. American Journal of Clinical Nutrition 1993, 57:779S-785S.
34. Ishii T., Itoh K., Takahashi S., Sato H., Yanagawa T., Katoh Y., Bannai S., Yamamoto M. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. Journal of Biological Chemistry 2000, 275:16023-16029.
35. Ishii T., Itoh K., Ruiz E., Leake D.S., Unoki H., Yamamoto M., Mann G.E. Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circulation Research 2004, 94:609-616.
36. Suc I., Meilhac O., Lajoie-Mazenc I., Vandaele J., Jurgens G., Salvayre R., Negre-Salvayre A. Activation of EGF receptor by oxidized LDL. FASEB Journal 1998, 12:665-671.
37. Natarajan V., Scribner W.M., Vepa S. Phosphatase inhibitors potentiate 4-hydroxynonenal-induced phospholipase D activation in vascular endothelial cells. American Journal of Respiratory Cell and Molecular Biology 1997, 17:251-259.
38. McDermott M., Wakelam M.J., Morris A.J., Phospholipase D. Biochemistry and Cell Biology 2004, 82:225-253.
39. Parinandi N.L., Scribner W.M., Vepa S., Shi S., Natarajan V. Phospholipase D activation in endothelial cells is redox sensitive. Antioxidants and Redox Signaling 1999, 1:193-210.
40. Akiba S., Kumazawa S., Yamaguchi H., Hontani N., Matsumoto T., Ikeda T., Oka M., Sato T. Acceleration of matrix metalloproteinase-1 production and activation of platelet-derived growth factor receptor beta in human coronary smooth muscle cells by oxidized LDL and 4-hydroxynonenal. Biochimica et Biophysica Acta 2006, 1763:797-804.
41. Lee S.J., Seo K.W., Yun M.R., Bae S.S., Lee W.S., Hong K.W., Kim C.D. 4-Hydroxynonenal enhances MMP-2 production in vascular smooth muscle cells via mitochondrial ROS-mediated activation of the Akt/NF-kappaB signaling pathways. Free Radical Biology and Medicine 2008, 45:1487-1492.
42. Seo K.W., Lee S.J., Kim C.E., Yun M.R., Park H.M., Yun J.W., Bae S.S., Kim C.D. Participation of 5-lipoxygenase-derived LTB(4) in 4-hydroxynonenal-enhanced MMP-2 production in vascular smooth muscle cells. Atherosclerosis 2010, 208:56-61.
43. Ruef J., Rao G.N., Li F., Bode C., Patterson C., Bhatnagar A., Runge M.S. Induction of rat aortic smooth muscle cell growth by the lipid peroxidation product 4-hydroxy-2-nonenal. Circulation 1998, 97:1071-1078.
44. Lee T.J., Lee J.T., Moon S.K., Kim C.H., Park J.W., Kwon T.K. Age-related differential growth rate and response to 4-hydroxynonenal in mouse aortic smooth muscle cells. International Journal of Molecular Medicine 2006, 17:29-35.
45. Ramana K.V., Bhatnagar A., Srivastava S., Yadav U.C., Awasthi S., Awasthi Y.C., Srivastava S.K. Mitogenic responses of vascular smooth muscle cells to lipid peroxidation-derived aldehyde 4-hydroxy-trans-2-nonenal (HNE): role of aldose reductase-catalyzed reduction of the HNE-glutathione conjugates in regulating cell growth. Journal of Biological Chemistry 2006, 281:17652-17660.
46. Paola D., Domenicotti C., Nitti M., Vitali A., Borghi R., Cottalasso D., Zaccheo D., Odetti P., Strocchi P., Marinari U.M., Tabaton M., Pronzato M.A. Oxidative stress induces increase in intracellular amyloid beta-protein production and selective activation of betaI and betaII PKCs in NT2 cells. Biochemical and Biophysical Research Communications 2000, 268:642-646.
47. Marinari U.M., Nitti M., Pronzato M.A., Domenicotti C. Role of PKC-dependent pathways in HNE-induced cell protein transport and secretion. Molecular Aspects of Medicine 2003, 24:205-211.
48. Gopalakrishna R., Jaken S. Protein kinase C signaling and oxidative stress. Free Radical Biology and Medicine 2000, 28:1349-1361.
49. Usatyuk P.V., Natarajan V. Role of mitogen-activated protein kinases in 4-hydroxy-2-nonenal-induced actin remodeling and barrier function in endothelial cells. Journal of Biological Chemistry 2004, 279:11789-11797.
50. Cheng X., Siow R.C., Mann G.E. Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway. Antioxidants and Redox Signaling 2011, 14:469-487.
51. Chapple S.J., Siow R.C., Mann G.E. Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging. International Journal of Biochemistry and Cell Biology 2012, 44:1315-1320.
52. Levonen A.L., Landar A., Ramachandran A., Ceaser E.K., Dickinson D.A., Zanoni G., Morrow J.D., rley-Usmar V.M. Cellular mechanisms of redox cell signaling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochemical Journal 2004, 378:373-382.
53. Ricart K.C., Bolisetty S., Johnson M.S., Perez J., Agarwal A., Murphy M.P., Landar A. The permissive role of mitochondria in the induction of haem oxygenase-1 in endothelial cells. Biochemical Journal 2009, 419:427-436.
54. Itoh K., Mochizuki M., Ishii Y., Ishii T., Shibata T., Kawamoto Y., Kelly V., Sekizawa K., Uchida K., Yamamoto M. Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-Delta(12,14)-prostaglandin j(2). Molecular and Cellular Biology 2004, 24:36-45.
55. Ishikado A., Nishio Y., Morino K., Ugi S., Kondo H., Makino T., Kashiwagi A., Maegawa H. Low concentration of 4-hydroxy hexenal increases heme oxygenase-1 expression through activation of Nrf2 and antioxidative activity in vascular endothelial cells. Biochemical and Biophysical Research Communications 2010, 402:99-104.
56. Motohashi H., Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends in Molecular Medicine 2004, 10:549-557.
57. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes and Development 1999, 13:76-86.
58. Kang M.I., Kobayashi A., Wakabayashi N., Kim S.G., Yamamoto M. Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. Proceedings of the National Academy of Sciences of U.S.A 2004, 101:2046-2051.
59. McMahon M., Itoh K., Yamamoto M., Hayes J.D. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. Journal of Biological Chemistry 2003, 278:21592-21600.
60. Sekhar K.R., Rachakonda G., Freeman M.L. Cysteine-based regulation of the CUL3 adaptor protein Keap1. Toxicology and Applied Pharmacology 2010, 244:21-26.
61. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proceedings of the National Academy of Sciences of U.S.A 2002, 99:11908-11913.
62. Yamamoto T., Suzuki T., Kobayashi A., Wakabayashi J., Maher J., Motohashi H., Yamamoto M. Physiological significance of reactive cysteine residues of Keap1 in determining Nrf2 activity. Molecular and Cellular Biology 2008, 28:2758-2770.
63. Jung K.A., Choi B.H., Nam C.W., Song M., Kim S.T., Lee J.Y., Kwak M.K. Identification of aldo-keto reductases as NRF2-target marker genes in human cells. Toxicological Letters 2013, 218:39-49.
64. Macleod A.K., McMahon M., Plummer S.M., Higgins L.G., Penning T.M., Igarashi K., Hayes J.D. Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds. Carcinogenesis 2009.
65. Vanduyn N., Settivari R., Wong G., Nass R. SKN-1/Nrf2 inhibits dopamine neuron degeneration in a Caenorhabditis elegans model of methylmercury toxicity. Toxicological Sciences 2010, 118:613-624.
66. Chanas S.A., Jiang Q., McMahon M., McWalter G.K., McLellan L.I., Elcombe C.R., Henderson C.J., Wolf C.R., Moffat G.J., Itoh K., Yamamoto M., Hayes J.D. Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochemical Journal 2002, 365:405-416.
67. Carbone D.L., Doorn J.A., Kiebler Z., Petersen D.R. Cysteine modification by lipid peroxidation products inhibits protein disulfide isomerase. Chemical Research in Toxicology 2005, 18:1324-1331.
68. Miller C.J., Gounder S.S., Kannan S., Goutam K., Muthusamy V.R., Firpo M.A., Symons J.D., Paine R., Hoidal J.R., Rajasekaran N.S. Disruption of Nrf2/ARE signaling impairs antioxidant mechanisms and promotes cell degradation pathways in aged skeletal muscle. Biochimica et Biophysica Acta 2012, 1822:1038-1050.
69. Suh J.H., Shenvi S.V., Dixon B.M., Liu H., Jaiswal A.K., Liu R.M., Hagen T.M. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proceedingsof the National Academy of Sciences of U.S.A 2004, 101:3381-3386.
70. Chen Z.H., Yoshida Y., Saito Y., Noguchi N., Niki E. Adaptive response induced by lipid peroxidation products in cell cultures. FEBS Letters 2006, 580:479-483.
71. Landar A., Zmijewski J.W., Dickinson D.A., Le G.C., Johnson M.S., Milne G.L., Zanoni G., Vidari G., Morrow J.D., rley-Usmar V.M. Interaction of electrophilic lipid oxidation products with mitochondria in endothelial cells and formation of reactive oxygen species. American Journal of Physiology-Heart and Circulatory Physiology 2006, 290:H1777-H1787.
72. Ruef J., Moser M., Bode C., Kubler W., Runge M.S. 4-hydroxynonenal induces apoptosis, NF-kappaB-activation and formation of 8-isoprostane in vascular smooth muscle cells. Basic Research in Cardiology 2001, 96:143-150.
73. Hattori Y., Hattori S., Kasai K. 4-hydroxynonenal prevents NO production in vascular smooth muscle cells by inhibiting nuclear factor-kappaB-dependent transcriptional activation of inducible NO synthase. Arteriosclerosis Thrombosis and Vascular Biology 2001, 21:1179-1183.
74. Kakishita H., Hattori Y. Vascular smooth muscle cell activation and growth by 4-hydroxynonenal. Life Science 2001, 69:689-697.
75. Awasthi Y.C., Sharma R., Cheng J.Z., Yang Y., Sharma A., Singhal S.S., Awasthi S. Role of 4-hydroxynonenal in stress-mediated apoptosis signaling. Molecular Aspects of Medicine 2003, 24:219-230.
76. Sharma R., Yang Y., Sharma A., Dwivedi S., Popov V.L., Boor P.J., Singhal S.S., Awasthi S., Awasthi Y.C. Mechanisms and physiological significance of the transport of the glutathione conjugate of 4-hydroxynonenal in human lens epithelial cells. Investigative Ophthalmology and Visual Science 2003, 44:3438-3449.
77. Sharma R., Sharma A., Yang Y., Awasthi S., Singhal S.S., Zimniak P., Awasthi Y.C. Functional reconstitution of Ral-binding GTPase activating protein, RLIP76, in proteoliposomes catalyzing ATP-dependent transport of glutathione conjugate of 4-hydroxynonenal. Acta Biochimica Polonica 2002, 49:693-701.
78. Margutti P., Matarrese P., Conti F., Colasanti T., Delunardo F., Capozzi A., Garofalo T., Profumo E., Rigano R., Siracusano A., Alessandri C., Salvati B., Valesini G., Malorni W., Sorice M., Ortona E. Autoantibodies to the C-terminal subunit of RLIP76 induce oxidative stress and endothelial cell apoptosis in immune-mediated vascular diseases and atherosclerosis. Blood 2008, 111:4559-4570.
79. Singhal J., Singhal S.S., Yadav S., Suzuki S., Warnke M.M., Yacoub A., Dent P., Bae S., Sharma R., Awasthi Y.C., Armstrong D.W., Awasthi S. RLIP76 in defense of radiation poisoning. International Journal of Radiation Oncology, Biology, Physics 2008, 72:553-561.
80. Singhal J., Nagaprashantha L., Vatsyayan R., Awasthi S., Singhal S.S. RLIP76, a glutathione-conjugate transporter, plays a major role in the pathogenesis of metabolic syndrome. PLoS One 2011, 6:e24688.
81. Davies K.J. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001, 83:301-310.
82. Farout L., Mary J., Vinh J., Szweda L.I., Friguet B. Inactivation of the proteasome by 4-hydroxy-2-nonenal is site specific and dependant on 20S proteasome subtypes. Archives of Biochemistry and Biophysics 2006, 453:135-142.
83. Vieira O., Escargueil-Blanc I., Jurgens G., Borner C., Almeida L., Salvayre R., Negre-Salvayre A. Oxidized LDLs alter the activity of the ubiquitin-proteasome pathway: potential role in oxidized LDL-induced apoptosis. FASEB Journal 2000, 14:532-542.
84. Pickering A.M., Linder R.A., Zhang H., Forman H.J., Davies K.J. Nrf2-dependent induction of proteasome and Pa28alphabeta regulator are required for adaptation to oxidative stress. Journal of Biological Chemistry 2012, 287:10021-10031.
85. Uchida K., Toyokuni S., Nishikawa K., Kawakishi S., Oda H., Hiai H., Stadtman E.R. Michael addition-type 4-hydroxy-2-nonenal adducts in modified low-density lipoproteins: markers for atherosclerosis. Biochemistry 1994, 33:12487-12494.
86. Carbone D.L., Doorn J.A., Petersen D.R. 4-Hydroxynonenal regulates 26S proteasomal degradation of alcohol dehydrogenase. Free Radical Biology and Medicine 2004, 37:1430-1439.
87. Radu A., Moldovan N. 4-Hydroxynonenal reduces junctional communication between endothelial cells in culture. Experimental Cell Research 1991, 196:121-126.
88. Usatyuk P.V., Parinandi N.L., Natarajan V. Redox regulation of 4-hydroxy-2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. Journal of Biological Chemistry 2006, 281:35554-35566.
89. Usatyuk P.V., Natarajan V. Hydroxyalkenals and oxidized phospholipids modulation of endothelial cytoskeleton, focal adhesion and adherens junction proteins in regulating endothelial barrier function. Microvascular Research 2012, 83:45-55.
90. Go Y.M., Halvey P.J., Hansen J.M., Reed M., Pohl J., Jones D.P. Reactive aldehyde modification of thioredoxin-1 activates early steps of inflammation and cell adhesion. American Journal of Pathology 2007, 171:1670-1681.
91. Quintero M., Colombo S.L., Godfrey A., Moncada S. Mitochondria as signaling organelles in the vascular endothelium. Proceedings of the National Academy of Sciences of USA 2006, 103:5379-5384.
92. Lin T.K., Hughes G., Muratovska A., Blaikie F.H., Brookes P.S., Darley-Usmar V., Smith R.A., Murphy M.P. Specific modification of mitochondrial protein thiols in response to oxidative stress: a proteomics approach. Journal of Biological Chemistry 2002, 277:17048-17056.
93. Pignatelli M., Sanchez-Rodriguez J., Santos A., Perez-Castillo A. 15-deoxy-Delta-12,14-prostaglandin J2 induces programmed cell death of breast cancer cells by a pleiotropic mechanism. Carcinogenesis 2005, 26:81-92.
94. Ceaser E.K., Ramachandran A., Levonen A.L., rley-Usmar V.M. Oxidized low-density lipoprotein and 15-deoxy-delta 12,14-PGJ2 increase mitochondrial complex I activity in endothelial cells. American Journal of Physiology-Heart and Circular Physiology 2003, 285:H2298-H2308.
95. Echtay K.S., Esteves T.C., Pakay J.L., Jekabsons M.B., Lambert A.J., Portero-Otin M., Pamplona R., Vidal-Puig A.J., Wang S., Roebuck S.J., Brand M.D. A signaling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. EMBO Journal 2003, 22:4103-4110.
96. Lee J.Y., Jung G.Y., Heo H.J., Yun M.R., Park J.Y., Bae S.S., Hong K.W., Lee W.S., Kim C.D. 4-Hydroxynonenal induces vascular smooth muscle cell apoptosis through mitochondrial generation of reactive oxygen species. Toxicology Letters 2006, 166:212-221.
97. Sansbury B.E., Jones S.P., Riggs D.W., Darley-Usmar V.M., Hill B.G. Bioenergetic function in cardiovascular cells: the importance of the reserve capacity and its biological regulation. Chemico-Biological Interactions 2011, 191:288-295.
98. Lo S.C., Hannink M. PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Experimental Cell Research 2008, 314:1789-1803.
99. Han Z., Varadharaj S., Giedt R.J., Zweier J.L., Szeto H.H., Alevriadou B.R. Mitochondria-derived reactive oxygen species mediate heme oxygenase-1 expression in sheared endothelial cells. Journal of Pharmacology and Experimental Therapeutics 2009, 329:94-101.
100. Diers A.R., Higdon A.N., Ricart K.C., Johnson M.S., Agarwal A., Kalyanaraman B., Landar A., Darley-Usmar V.M. Mitochondrial targeting of the electrophilic lipid 15-deoxy-Delta12,14-prostaglandin J2 increases apoptotic efficacy via redox cell signaling mechanisms. Biochemical Journal 2010, 426:31-41.
101. Imhoff B.R., Hansen J.M. Extracellular redox status regulates Nrf2 activation through mitochondrial reactive oxygen species. Biochemical Journal 2009, 424:491-500.
102. Scheuner D., Kaufman R.J. The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocrine reviews 2008, 29:317-333.
103. Higa A., Chevet E. Redox signaling loops in the unfolded protein response. Cellular Signaling 2012, 24:1548-1555.
104. Fujita E., Kouroku Y., Isoai A., Kumagai H., Misutani A., Matsuda C., Hayashi Y.K., Momoi T. Two endoplasmic reticulum-associated degradation (ERAD) systems for the novel variant of the mutant dysferlin: ubiquitin/proteasome ERAD(I) and autophagy/lysosome ERAD(II). Human Molecular Genetics 2007, 16:618-629.
105. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nature Cell Biology 2000, 2:326-332.
106. Marciniak S.J., Ron D. Endoplasmic reticulum stress signaling in disease. Physiological Reviews 2006, 86:1133-1149.
107. Vladykovskaya E., Sithu S.D., Haberzettl P., Wickramasinghe N.S., Merchant M.L., Hill B.G., McCracken J., Agarwal A., Dougherty S., Gordon S.A., Schuschke D.A., Barski O.A., O'Toole T., D'Souza S.E., Bhatnagar A., Srivastava S. Lipid peroxidation product 4-hydroxy-trans-2-nonenal causes endothelial activation by inducing endoplasmic reticulum stress. Journal of Biological Chemistry 2012, 287:11398-11409.
108. Sanson M., Auge N., Vindis C., Muller C., Bando Y., Thiers J.C., Marachet M.A., Zarkovic K., Sawa Y., Salvayre R., Negre-Salvayre A. Oxidized low-density lipoproteins trigger endoplasmic reticulum stress in vascular cells: prevention by oxygen-regulated protein 150 expression. Circulation Research 2009, 104:328-336.
109. Cullinan S.B., Diehl J.A. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. Journal of Biological Chemistry 2004, 279:20108-20117.
110. Muller C., Bandemer J., Vindis C., Camare C., Mucher E., Gueraud F., Larroque-Cardoso P., Bernis C., Auge N., Salvayre R., Negre-Salvayre A. Protein disulfide isomerase modification and inhibition contribute to ER stress and apoptosis induced by oxidized low density lipoproteins. Antioxidants and Redox Signaling 2013, 18:731-742.
111. Cullinan S.B., Zhang D., Hannink M., Arvisais E., Kaufman R.J., Diehl J.A. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Molecular and Cellular Biology 2003, 23:7198-7209.
112. Scull C.M., Tabas I. Mechanisms of ER stress-induced apoptosis in atherosclerosis. Arteriosclerosis Thrombosis and Vascular Biology 2011, 31:2792-2797.
113. Karlhuber G.M., Bauer H.C., Eckl P.M. Cytotoxic and genotoxic effects of 4-hydroxynonenal in cerebral endothelial cells. Mutation Research 1997, 381:209-216.
114. Braekke K., Harsem N.K., Staff A.C. Oxidative stress and antioxidant status in fetal circulation in preeclampsia. Pediatric Research 2006, 60:560-564.
115. Gveric-Ahmetasevic S., Sunjic S.B., Skala H., Andrisic L., Stroser M., Zarkovic K., Skrablin S., Tatzber F., Cipak A., Jaganjac M., Waeg G., Gveric T., Zarkovic N. Oxidative stress in small-for-gestational age (SGA) term newborns and their mothers. Free Radical Research 2009, 43:376-384.
116. Leonarduzzi G., Chiarpotto E., Biasi F., Poli G. 4-Hydroxynonenal and cholesterol oxidation products in atherosclerosis. Molecular Nutrition and Food Research 2005, 49:1044-1049.
117. Sakuraba H., Mizukami H., Yagihashi N., Wada R., Hanyu C., Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients. Diabetologia 2002, 45:85-96.
118. Zarkovic K. 4-hydroxynonenal and neurodegenerative diseases. Molecular Aspects of Medicine 2003, 24:293-303.
119. Chamy V.M., Lepe J., Catalan A., Retamal D., Escobar J.A., Madrid E.M. Oxidative stress is closely related to clinical severity of pre-eclampsia. Biological Research 2006, 39:229-236.
120. Negre-Salvayre A., Auge N., Ayala V., Basaga H., Boada J., Brenke R., Chapple S., Cohen G., Feher J., Grune T., Lengyel G., Mann G.E., Pamplona R., Poli G., Portero-Otin M., Riahi Y., Salvayre R., Sasson S., Serrano J., Shamni O., Siems W., Siow R.C., Wiswedel I., Zarkovic K., Zarkovic N. Pathological aspects of lipid peroxidation. Free Radical Research 2010, 44:1125-1171.
121. Lian I.A., Loset M., Mundal S.B., Fenstad M.H., Johnson M.P., Eide I.P., Bjorge L., Freed K.A., Moses E.K., Austgulen R. Increased endoplasmic reticulum stress in decidual tissue from pregnancies complicated by fetal growth restriction with and without pre-eclampsia. Placenta 2011, 32:823-829.
122. Illsinger S., Janzen N., Sander S., Schmidt K.H., Bednarczyk J., Mallunat L., Bode J., Hagebolling F., Hoy L., Lucke T., Hass R., Das A.M. Preeclampsia and HELLP syndrome: impaired mitochondrial function in umbilical endothelial cells. Reproductive Sciences 2010, 17:219-226.
123. Padmini E., Lavanya S., Uthra V. Preeclamptic placental stress and over expression of mitochondrial HSP70. Clinical Chemistry and Laboratory Medicine 2009, 47:1073-1080.
124. Benderdour M., Charron G., DeBlois D., Comte B., Des Rosiers C. Cardiac mitochondrial NADP+-isocitrate dehydrogenase is inactivated through 4-hydroxynonenal adduct formation: an event that precedes hypertrophy development. Journal of Biological Chemistry 2003, 278:45154-45159.
125. Zeng L., Zampetaki A., Margariti A., Pepe A.E., Alam S., Martin D., Xiao Q., Wang W., Jin Z.G., Cockerill G., Mori K., Li Y.S., Hu Y., Chien S., Xu Q. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proceedings of the National Academy of Sciences of USA 2009, 106:8326-8331.
126. Civelek M., Manduchi E., Riley R.J., Stoeckert C.J., Davies P.F. Chronic endoplasmic reticulum stress activates unfolded protein response in arterial endothelium in regions of susceptibility to atherosclerosis. Circulation Research 2009, 105:453-461.
127. Song B., Scheuner D., Ron D., Pennathur S., Kaufman R.J. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. Journal of Clinical Investigation 2008, 118:3378-3389.
128. Fu D., Wu M., Zhang J., Du M., Yang S., Hammad S.M., Wilson K., Chen J., Lyons T.J. Mechanisms of modified LDL-induced pericyte loss and retinal injury in diabetic retinopathy. Diabetologia 2012, 55:3128-3140.
129. Wu M., Yang S., Elliott M.H., Fu D., Wilson K., Zhang J., Du M., Chen J., Lyons T. Oxidative and endoplasmic reticulum stresses mediate apoptosis induced by modified LDL in human retinal Muller cells. Investigative Ophthalmology and Visual Science 2012, 53:4595-4604.
130. Lashin O.M., Szweda P.A., Szweda L.I., Romani A.M. Decreased complex II respiration and HNE-modified SDH subunit in diabetic heart. Free Radical Biology and Medicine 2006, 40:886-896.
131. Mogensen M., Sahlin K., Fernstrom M., Glintborg D., Vind B.F., Beck-Nielsen H., Hojlund K. Mitochondrial respiration is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 2007, 56:1592-1599.
132. Qin Z., Hu D., Han S., Reaney S.H., Di Monte D.A., Fink A.L. Effect of 4-hydroxy-2-nonenal modification on alpha-synuclein aggregation. Journal of Biological Chemistry 2007, 282:5862-5870.
133. Slodzinski H., Moran L.B., Michael G.J., Wang B., Novoselov S., Cheetham M.E., Pearce R.K., Graeber M.B. Homocysteine-induced endoplasmic reticulum protein (herp) is up-regulated in parkinsonian substantia nigra and present in the core of Lewy bodies. Clinical Neuropathology 2009, 28:333-343.
134. Macedo B., Magalhaes J., Batista A.R., Saraiva M.J. Carvedilol treatment reduces transthyretin deposition in a familial amyloidotic polyneuropathy mouse model. Pharmacological Research 2010, 62:514-522.
135. Teixeira P.F., Cerca F., Santos S.D., Saraiva M.J. Endoplasmic reticulum stress associated with extracellular aggregates. Evidence from transthyretin deposition in familial amyloid polyneuropathy. Journal of Biological Chemistry 2006, 281:21998-22003.
136. Lee W.C., Wong H.Y., Chai Y.Y., Shi C.W., Amino N., Kikuchi S., Huang S.H. Lipid peroxidation dysregulation in ischemic stroke: plasma 4-HNE as a potential biomarker?. Biochemical and Biophysical Research Communications 2012, 425:842-847.
137. Sompol P., Ittarat W., Tangpong J., Chen Y., Doubinskaia I., Batinic-Haberle I., Abdul H.M., Butterfield D.A., Clair D.K. A neuronal model of Alzheimer's disease: an insight into the mechanisms of oxidative stress-mediated mitochondrial injury. Neuroscience 2008, 153:120-130.
138. Noguchi N. Role of oxidative stress in adaptive responses in special reference to atherogenesis. Journal of Clinical Biochemistry and Nutrition 2008, 43:131-138.
139. Polak M., Zagorski Z. Lipid peroxidation in diabetic retinopathy. Annales Universitatis Mariae Curie-Sklodowska. Sectio D: Medicina 2004, 59:434-437.
140. Srivastava S.K., Ramana K.V., Bhatnagar A. Role of aldose reductase and oxidative damage in diabetes and the consequent potential for therapeutic options. Endocrine Reviews 2005, 26:380-392.
141. Natarajan V., Scribner W.M., Taher M.M. 4-Hydroxynonenal, a metabolite of lipid peroxidation, activates phospholipase D in vascular endothelial cells. Free Radical Biology and Medicine 1993, 15:365-375.
142. Ho T.C., Chen S.L., Yang Y.C., Chen C.Y., Feng F.P., Hsieh J.W., Cheng H.C., Tsao Y.P. 15-deoxy-Delta(12,14)-prostaglandin J2 induces vascular endothelial cell apoptosis through the sequential activation of MAPKS and p53. Journal of Biological Chemistry 2008, 283:30273-30288.
143. Hosoya T., Maruyama A., Kang M.I., Kawatani Y., Shibata T., Uchida K., Warabi E., Noguchi N., Itoh K., Yamamoto M. Differential responses of the Nrf2-Keap1 system to laminar and oscillatory shear stresses in endothelial cells. Journal of Biological Chemistry 2005, 280:27244-27250.
144. Oh J.Y., Giles N., Landar A., Darley-Usmar V. Accumulation of 15-deoxy-delta(12,14)-prostaglandin J2 adduct formation with Keap1 over time: effects on potency for intracellular antioxidant defence induction. Biochemical Journal 2008, 411:297-306.
145. Levonen A.L., Dickinson D.A., Moellering D.R., Mulcahy R.T., Forman H.J., Darley-Usmar V.M. Biphasic effects of 15-deoxy-delta(12,14)-prostaglandin J(2) on glutathione induction and apoptosis in human endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 2001, 21:1846-1851.
146. Moldovan N.I., Lupu F., Moldovan L., Simionescu N. 4-Hydroxynonenal induces membrane perturbations and inhibition of basal prostacyclin production in endothelial cells, and migration of monocytes. Cell Biology International 1994, 18:985-992.
147. Kaneko T., Kaji K., Matsuo M. Cytotoxicities of a linoleic acid hydroperoxide and its related aliphatic aldehydes toward cultured human umbilical vein endothelial cells. Chemico-Biological Interactions 1988, 67:295-304.
148. de Jongh R., Haenen G.R., van Koeveringe G.A., Dambros M., van Kerrebroeck P.E. Lipid peroxidation product 4-hydroxynonenal contributes to bladder smooth muscle damage. Urology 2008, 71:974-978.