Bone morphogenic protein-4-induced oxidant signaling via protein carbonylation for endothelial dysfunction

Free Radical Biology and Medicine

Volumn 75, Issue , 2014, Pages 178-190

  Wong, Chi Ming ^a   Zhang, Yang ^a   Huang, Yu ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

BMP 4; Diabetes mellitus; Endothelial dysfunction; Oxidant signaling; Protein carbonylation

Indexed keywords

ALPHA ENOLASE; BONE MORPHOGENETIC PROTEIN 4; DEFEROXAMINE; DYNAMIN I; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HYDRALAZINE; INTEGRIN LINKED KINASE; LIPOCORTIN 2; N(G) NITROARGININE METHYL ESTER; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN DISULFIDE ISOMERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SEPTIN; TRIOSEPHOSPHATE ISOMERASE; VIMENTIN; ACETYLCHOLINE; ANTIHYPERTENSIVE AGENT; BMP4 PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE; VASODILATOR AGENT;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; HUMAN TISSUE; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBONYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RENAL ARTERY; SIGNAL TRANSDUCTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; AORTA; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DIABETIC ANGIOPATHY; DRUG EFFECTS; HYPERGLYCEMIA; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; PHYSIOLOGY; RAT; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; VASODILATATION;

ACETYLCHOLINE; ANIMALS; ANTIHYPERTENSIVE AGENTS; AORTA; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 4; CELLS, CULTURED; DEFEROXAMINE; DIABETES MELLITUS; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HYDRALAZINE; HYPERGLYCEMIA; MICE; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN CARBONYLATION; RATS; REACTIVE OXYGEN SPECIES; VASODILATION; VASODILATOR AGENTS;

EID: 84906776688     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.07.035     Document Type: Article

References (60)

1. B.S. Berlett, and E.R. Stadtman Protein oxidation in aging, disease, and oxidative stress J. Biol. Chem. 272 1997 20313 20316 (Pubitemid 27355575)
2. B. Halliwell, and J. Gutteridge Free radicals in biology and medicine 2007 Oxford University Press Oxford
3. B.A. Freeman, and J.D. Crapo Biology of disease: free radicals and tissue injury Lab. Invest. 47 1982 412 426 (Pubitemid 13229679)
4. Y.J. Suzuki, H.J. Forman, and A. Sevanian Oxidants as stimulators of signal transduction Free Radic. Biol. Med. 22 1997 269 285 (Pubitemid 26399334)
5. S.G. Rhee, Y.S. Bae, S.R. Lee, and J. Kwon Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation Sci. STKE 2000 2000 pe1
6. 2 accumulation for cell signaling Cell 140 2010 517 528
7. T.H. Truong, and K.S. Carroll Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation Biochemistry 51 2012 9954 9965
8. H.J. Forman, M. Maiorino, and F. Ursini Signaling functions of reactive oxygen species Biochemistry 49 2010 835 842
9. J.R. Burgoyne, M. Madhani, F. Cuello, R.L. Charles, J.P. Brennan, E. Schröder, D.D. Browning, and P. Eaton Cysteine redox sensor in PKGIα enables oxidant-induced activation Science 317 2007 1393 1397 (Pubitemid 47417480)
10. T. Finkel Signal transduction by reactive oxygen species J. Cell. Biol. 194 2011 7 15
11. C.M. Wong, A.K. Cleema, L. Zhang, and Y.J. Suzuki Protein carbonylation as a novel mechanism in redox signaling Circ. Res. 102 2008 310 318 (Pubitemid 351271651)
12. C.M. Wong, L. Marcocci, L. Liu, and Y.J. Suzuki Cell signaling by protein carbonylation and decarbonylation Antioxid. Redox Signal. 12 2010 393 404
13. L. Liu, L. Marcocci, C.M. Wong, A.M. Park, and Y.J. Suzuki Serotonin-mediated protein carbonylation in the right heart Free Radic. Biol. Med. 45 2008 847 854
14. G. Bansal, C.M. Wong, L. Liu, and Y.J. Suzuki Oxidant signaling for interleukin-13 gene expression in lung smooth muscle cells Free Radic. Biol. Med. 52 2012 1552 1559
15. G. Bansal, D. Das, C.Y. Hsieh, Y.H. Wang, C.M. Wong, and Y.J. Suzuki IL-22 activates oxidant signaling in pulmonary artery smooth muscle cells Cell. Signal. 25 2013 2727 2733
16. R.L. Levine Carbonyl modified proteins in cellular regulation, aging, and disease Free Radic. Biol. Med. 32 2002 790 796 (Pubitemid 34439249)
17. I. Dalle-Donne, G. Aldini, M. Carini, R. Colombo, R. Rossi, and A. Milzani Protein carbonylation, cellular dysfunction, and disease progression J. Cell. Mol. Med. 10 2006 389 406 (Pubitemid 44870187)
18. Y.J. Suzuki, M. Carini, and D.A. Butterfield Protein carbonylation Antioxid. Redox Signal. 12 2010 323 325
19. D.A. Butterfield, M. Perluigi, T. Reed, T. Muharib, C.P. Hughes, R.A. Robinson, and R. Sultana Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications Antioxid. Redox Signal. 17 2012 1610 1655
20. E. Barreiro, and S.N. Hussain Protein carbonylation in skeletal muscles: impact on function Antioxid. Redox Signal. 12 2010 417 429
21. T. Nyström Role of oxidative carbonylation in protein quality control and senescence EMBO J. 24 2005 1311 1317 (Pubitemid 40593052)
22. A.M. Park, C. Wong, L. Jelinkova, L. Liu, H. Nagase, and Y.J. Suzuki Pulmonary hypertension-induced GATA4 activation in the right ventricle Hypertension 56 2010 1145 1151
23. R.L. Levine, J.A. Williams, E.R. Stadtman, and E. Shacter Carbonyl assays for determination of oxidatively modified proteins Methods Enzymol. 233 1994 346 357
24. R.L. Levine, N. Wehr, J.A. Williams, E.R. Stadtman, and E. Shacter Determination of carbonyl groups in oxidized proteins Methods Mol. Biol. 99 2000 15 24
25. E. Shacter, J.A. Williams, M. Lim, and R.L. Levine Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay Free Radic. Biol. Med. 17 1994 429 437 (Pubitemid 24320292)
26. E.R. Stadtman, and B.S. Berlett Fenton chemistry. Amino acid oxidation J. Biol. Chem. 266 1991 17201 17211 (Pubitemid 21907925)
27. E.R. Stadtman, and R.L. Levine Protein oxidation Ann. N. Y. Acad. Sci 899 2000 191 208 (Pubitemid 30352787)
28. J. Hwang, A. Saha, Y.C. Boo, G.P. Sorescu, J.S. McNally, and S.M. Holland et al. Oscillatory shear stress stimulates endothelial production of O2- from p47 phox-dependent NAD(P)H oxidases, leading to monocyte adhesion J. Biol. Chem. 278 2003 47291 47298 (Pubitemid 37452318)
29. G.P. Sorescu, M. Sykes, D. Weiss, M.O. Platt, A. Saha, J. Hwang, N. Boyd, Y.C. Boo, J.D. Vega, W.R. Taylor, and H. Jo Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress stimulates an inflammatory response J. Biol. Chem. 278 2003 31128 31135 (Pubitemid 36994628)
30. M. Kiyono, and M. Shibuya Inhibitory Smad transcription factors protect arterial endothelial cells from apoptosis induced by BMP4 Oncogene 25 2006 7131 7137 (Pubitemid 44764182)
31. M. Kiyono, and M. Shibuya Bone morphogenetic protein 4 mediates apoptosis of capillary endothelial cells during rat pupillary membrane regression Mol. Cell. Biol. 23 2003 4627 4636 (Pubitemid 36734751)
32. X.Y. Tian, L.H. Yung, W.T. Wong, J. Liu, F.P. Leung, L. Liu, Y. Chen, S.K. Kong, K.M. Kwan, S.M. Ng, P.B.S. Lai, L.M. Yung, X. Yao, and Y. Huang Bone morphogenic protein-4 induces endothelial cell apoptosis through oxidative stress-dependent p38MAPK and JNK pathway J. Mol. Cell. Cardiol. 52 2012 237 244
33. A. Csiszar, N. Labinskyy, H. Jo, P. Ballabh, and Z. Ungvari Differential proinflammatory and prooxidant effects of bone morphogenetic protein-4 in coronary and pulmonary arterial endothelial cells Am. J. Physiol. Heart Circ. Physiol. 295 2008 H569 H577
34. S. Miriyala, M.C. Gongora Nieto, C. Mingone, D. Smith, S. Dikalov, D.G. Harrison, and H. Jo Bone morphogenic protein-4 induces hypertension in mice: role of noggin, vascular NADPH oxidases, and impaired vasorelaxation Circulation 113 2006 2818 2825 (Pubitemid 44305294)
35. W.T. Wong, X.Y. Tian, Y. Chen, F.P. Leung, L. Liu, H.K. Lee, C.F. Ng, A. Xu, X. Yao, P.M. Vanhoutte, G.L. Tipoe, and Y. Huang Bone morphogenic protein-4 impairs endothelial function through oxidative stress-dependent cyclooxygenase-2 upregulation Cir. Res. 107 2010 984 991
36. Y. Zhang, J. Liu, X.Y. Tian, W.T. Wong, Y. Chen, L. Wang, J. Luo, W.S. Cheang, C.W. Lau, K.M. Kwan, N. Wang, X. Yao, and Y. Huang Inhibition of bone morphogenic protein 4 restores endothelial function in db/db diabetic mice Arterioscler. Thromb. Vasc. Biol. 34 2014 152 159
37. J. Hu, J. Liu, M.W.T. Kwok, R.H.L. Wong, Y. Huang, and S. Wan Bone morphogenic protein-4 contributes to venous endothelial dysfunction in patients with diabetes undergoing coronary revascularization Ann. Thoracic Surg 95 2013 1331 1339
38. American Diabetes Association Standards of medical care in diabetes - 2011 Diabetes Care 34 2011 S11 S61
39. W.S. Cheang, W.T. Wong, X.Y. Tian, Q. Yang, H.K. Lee, G.W. He, X. Yao, and Y. Huang Endothelial nitric oxidase synthase enhancer reduces oxidative stress and restores endothelial function in db/db mice Cardiovasc. Res. 92 2011 267 275
40. G. Li, X. Zhang, H. Wang, X. Wang, C. Meng, C. Chan, D.T.W. Yew, K.S. Tsang, K. Li, S. Tsai, S. Ngai, Z.C. Han, M.C. Lin, M. He, and H. Kung Comparative proteomic analysis of mesenchymal stem cells derived from human bone marrow, umbilical cord, and placenta: implication in the migration Proteomics 9 2009 20 30
41. E.R. Stadtman Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions Annu. Rev. Biochem. 62 1993 797 821 (Pubitemid 23237888)
42. A. Amici, R.L. Levine, L. Tsai, and E.R. Stadtman Conversion of amino acid residues in proteins and amino acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions J. Biol. Chem. 264 1989 3341 3346 (Pubitemid 19063388)
43. J.R. Requena, C.C. Chao, R.L. Levine, and E.R. Stadtman Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins Proc. Natl. Acad. Sci. USA 98 2001 69 74 (Pubitemid 32095865)
44. C.M. Wong, L. Marcocci, D. Das, X. Wang, H. Luo, M. Zungu-Edmondson, and Y.J. Suzuki Mechanism of protein decarbonylation Free Radic. Biol. Med. 65 2013 1126 1133
45. C.M. Wong, I.R. Preston, N.S. Hill, and Y.J. Suzuki Iron chelation inhibits the development of pulmonary vascular remodelling Free Radic. Biol. Med. 53 2012 1738 1747
46. R.L. Levine, C.N. Oliver, R.M. Fulks, and E.R. Stadtman Turnover of bacterial glutamine synthetase: oxidative inactivation proceeds proteolysis Proc. Natl. Acad. Sci. USA 78 1981 2120 2124
47. M. Cattaruzza, and M. Hecker Protein carbonylation and decarbonylation: a new Twist to the complex response of vascular cells to oxidative stress Circ. Res. 102 2008 273 274 (Pubitemid 351271644)
48. C.M. Wong, G. Bansal, L. Marcocci, and Y.J. Suzuki Proposed role of primary protein carbonylation in cell signaling Redox Rep. 17 2012 90 94
49. J.M. Li, and A.M. Shah Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 2004 R1014 R1030
50. M. Ushio-Fukai, Y. Tang, T. Fukai, S.I. Dikalov, Y. Ma, M. Fujimoto, M.T. Quinn, P.J. Pagano, C. Johnson, and R.W. Alexander Novel role of gp91(phox)-conatining NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis Circ. Res. 91 2002 1160 1167 (Pubitemid 36076365)
51. L.J. Yan, and M.J. Forster Chemical probes for analysis of carbonylated proteins: a review J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 879 2011 1308 1315
52. R.L. Levine Oxidative modification of glutamine synthetase I. Interaction is due to loss of one histidine residue J. Biol. Chem. 258 1983 11823 11827
53. C.N. Oliver Inactivation of enzymes and oxidative modification of proteins by stimulated neutrophils Arch. Biochem. Biophys. 253 1987 62 72 (Pubitemid 17025213)
54. C. Lii, A. Lin, S. Lee, H. Chen, and T. Wang Oxidative modifications of proteins by sodium arsenite in human umbilical vein endothelial cells Environ. Toxicol. 26 2011 459 471
55. C.E. Jessop, S. Chakravarthi, R.H. Watkins, and N.J. Bulleid Oxidative protein folding in the mammalian endoplasmic reticulum Biochem. Soc. Trans. 32 2004 655 658 (Pubitemid 39529767)
56. Y. Li, K. Okumura, S. Nomura, N. Maeda, T. Miyasho, and H. Yokota Oxidatively damaged proteins in the early stage of testicular toxicities in male rats by orally administered with a synthetic oestrogen, diethylstilbestrol Reprod. Toxicol. 31 2011 26 34
57. E.J. Nuss, B.K. Choksi, H.J. DeFord, and J. Papaconstantinou Decreased enzyme activities of chaperone pdi and bip in aged mouse livers Biochem. Biophys. Res. Commun. 365 2008 355 361 (Pubitemid 350137297)
58. T. Tanaka, S. Akatsuka, M. Ozeki, T. Shirase, H. Hiai, and S. Toyokuni Redox regulation of annexin 2 and its implications for oxidative stress-induced renal carcinogenesis and metastasis Oncogene 23 2004 3980 3989 (Pubitemid 38747926)
59. S. Persad, S. Attwell, V. Gray, N. Mawji, J.T. Deng, D. Leung, J. Yan, J. Sanghera, M.P. Walsh, and S. Dedhar Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase activity and amino acids arginine 211 and serine 343 J. Biol. Chem. 276 2001 27462 27469
60. C. Vecchione, D. Carnevale, A. Di Pardo, M.T. Gentile, A. Damato, G. Cocozza, G. Antenucci, G. Mascio, U. Bettarini, A. Landolfi, L. Iorio, A. Maffei, and G. Lembo Pressure-induced vascular oxidative stress is mediated through activation of integrin-linked kinase 1/betaPIX/Rac-1 pathway Hypertension 54 2009 1028 1034