Targeted subendothelial matrix oxidation by myeloperoxidase triggers myosin II-dependent de-adhesion and alters signaling in endothelial cells

Free Radical Biology and Medicine

Volumn 53, Issue 12, 2012, Pages 2344-2356

  Rees, Martin D ^a   Dang, Lei ^a   Thai, Thuan ^a   Owen, Dylan M ^a   Malle, Ernst ^b   Thomas, Shane R ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Endothelial dysfunction; Extracellular matrix; Free radicals; Myeloperoxidase; Redox signaling

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BLEBBISTATIN; FIBRONECTIN; FOCAL ADHESION KINASE; HYPOCHLOROUS ACID; MYELOPEROXIDASE; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; MYOSIN LIGHT CHAIN 2; NITRITE; PAXILLIN; PROTEIN TYROSINE KINASE; RHO KINASE; THIOCYANATE; TYROSINE;

ANIMAL CELL; ARTICLE; BIOSENSOR; CELL STRUCTURE; CONTROLLED STUDY; COVALENT BOND; CROSS LINKING; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; EXTRACELLULAR MATRIX; INFLAMMATION; LEUKOCYTE; NITRATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TENSILE STRENGTH; TRANSCYTOSIS; VASCULAR ENDOTHELIUM;

EID: 84870296165     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.10.002     Document Type: Article

References (50)

1. S.R. Thomas, P.K. Witting, and G.R. Drummond Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities Antioxid. Redox Signal. 10 2008 1713 1765
2. H. Lum, and K.A. Roebuck Oxidant stress and endothelial cell dysfunction Am. J. Physiol. Cell Physiol 280 2001 C719 C741
3. Y. Komarova, and A.B. Malik Regulation of endothelial permeability via paracellular and transcellular transport pathways Annu. Rev. Physiol. 72 2010 463 493
4. A.W. Orr, R. Stockton, M.B. Simmers, J.M. Sanders, I.J. Sarembock, B.R. Blackman, and M.A. Schwartz Matrix-specific p21-activated kinase activation regulates vascular permeability in atherogenesis J. Cell Biol. 176 2007 719 727 (Pubitemid 46333985)
5. C. Sun, M.H. Wu, and S.Y. Yuan Nonmuscle myosin light-chain kinase deficiency attenuates atherosclerosis in apolipoprotein E-deficient mice via reduced endothelial barrier dysfunction and monocyte migration Circulation 124 2011 48 57
6. J.A. Vita, M.L. Brennan, N. Gokce, S.A. Mann, M. Goormastic, M.H. Shishehbor, M.S. Penn, J.F. Keaney Jr, and S.L. Hazen Serum myeloperoxidase levels independently predict endothelial dysfunction in humans Circulation 110 2004 1134 1139 (Pubitemid 39319014)
7. S. Baldus, T. Heitzer, J.P. Eiserich, D. Lau, H. Mollnau, M. Ortak, S. Petri, B. Goldmann, H.J. Duchstein, J. Berger, U. Helmchen, B.A. Freeman, T. Meinertz, and T. Munzel Myeloperoxidase enhances nitric oxide catabolism during myocardial ischemia and reperfusion Free Radic. Biol. Med. 37 2004 902 911 (Pubitemid 39078559)
8. S. Baldus, C. Heeschen, T. Meinertz, A.M. Zeiher, J.P. Eiserich, T. Munzel, M.L. Simoons, and C.W. Hamm Myeloperoxidase serum levels predict risk in patients with acute coronary syndromes Circulation 108 2003 1440 1445 (Pubitemid 37176448)
9. M.L. Brennan, M.S. Penn, F. Van Lente, V. Nambi, M.H. Shishehbor, R.J. Aviles, M. Goormastic, M.L. Pepoy, E.S. McErlean, E.J. Topol, S.E. Nissen, and S.L. Hazen Prognostic value of myeloperoxidase in patients with chest pain N. Engl. J. Med. 349 2003 1595 1604 (Pubitemid 37288567)
10. J.P. Eiserich, S. Baldus, M.L. Brennan, W. Ma, C. Zhang, A. Tousson, L. Castro, A.J. Lusis, W.M. Nauseef, C.R. White, and B.A. Freeman Myeloperoxidase, a leukocyte-derived vascular NO oxidase Science 296 2002 2391 2394 (Pubitemid 34734213)
11. T.K. Rudolph, S. Wipper, B. Reiter, V. Rudolph, A. Coym, C. Detter, D. Lau, A. Klinke, K. Friedrichs, T. Rau, M. Pekarova, D. Russ, K. Knoll, M. Kolk, B. Schroeder, K. Wegscheider, H. Andresen, E. Schwedhelm, R. Boeger, H. Ehmke, and S. Baldus Myeloperoxidase deficiency preserves vasomotor function in humans Eur. Heart J. 33 2012 1625 1634
12. G. Zabucchi, M.R. Soranzo, R. Menegazzi, P. Bertoncin, E. Nardon, and P. Patriarca Uptake of human eosinophil peroxidase and myeloperoxidase by cells involved in the inflammatory process J. Histochem. Cytochem. 37 1989 499 508 (Pubitemid 19086847)
13. S. Baldus, J.P. Eiserich, A. Mani, L. Castro, M. Figueroa, P. Chumley, W. Ma, A. Tousson, C.R. White, D.C. Bullard, M.L. Brennan, A.J. Lusis, K.P. Moore, and B.A. Freeman Endothelial transcytosis of myeloperoxidase confers specificity to vascular ECM proteins as targets of tyrosine nitration J. Clin. Invest. 108 2001 1759 1770 (Pubitemid 34015121)
14. C. Tiruppathi, T. Naqvi, Y. Wu, S.M. Vogel, R.D. Minshall, and A.B. Malik Albumin mediates the transcytosis of myeloperoxidase by means of caveolae in endothelial cells Proc. Natl. Acad. Sci. USA 101 2004 7699 7704 (Pubitemid 38658092)
15. J.M. Astern, W.F. Pendergraft 3rd, R.J. Falk, J.C. Jennette, A.H. Schmaier, F. Mahdi, and G.A. Preston Myeloperoxidase interacts with endothelial cell-surface cytokeratin 1 and modulates bradykinin production by the plasma kallikrein-kinin system Am. J. Pathol. 171 2007 349 360 (Pubitemid 47339251)
16. H.M. Abu-Soud, and S.L. Hazen Nitric oxide is a physiological substrate for mammalian peroxidases J. Biol. Chem. 275 2000 37524 37532 (Pubitemid 32004861)
17. S. Baldus, V. Rudolph, M. Roiss, W.D. Ito, T.K. Rudolph, J.P. Eiserich, K. Sydow, D. Lau, K. Szocs, A. Klinke, L. Kubala, L. Berglund, S. Schrepfer, T. Deuse, M. Haddad, T. Risius, H. Klemm, H.C. Reichenspurner, T. Meinertz, and T. Heitzer Heparins increase endothelial nitric oxide bioavailability by liberating vessel-immobilized myeloperoxidase Circulation 113 2006 1871 1878 (Pubitemid 43739399)
18. M.C. Vissers, and C. Thomas Hypochlorous acid disrupts the adhesive properties of subendothelial matrix Free Radic. Biol. Med. 23 1997 401 411 (Pubitemid 27276776)
19. M.D. Rees, E.C. Kennett, J.M. Whitelock, and M.J. Davies Oxidative damage to extracellular matrix and its role in human pathologies Free Radic. Biol. Med. 44 2008 1973 2001
20. M.D. Rees, J.M. Whitelock, E. Malle, C.Y. Chuang, R.V. Iozzo, A. Nilasaroya, and M.J. Davies Myeloperoxidase-derived oxidants selectively disrupt the protein core of the heparan sulfate proteoglycan perlecan Matrix Biol. 29 2010 63 73
21. M.B. Hampton, A.J. Kettle, and C.C. Winterbourn Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing Blood 92 1998 3007 3017 (Pubitemid 28492304)
22. M.J. Davies, C.L. Hawkins, D.I. Pattison, and M.D. Rees Mammalian heme peroxidases: from molecular mechanisms to health implications Antioxid. Redox Signal. 10 2008 1199 1234 (Pubitemid 351634397)
23. S. Baldus, J.P. Eiserich, M.L. Brennan, R.M. Jackson, C.B. Alexander, and B.A. Freeman Spatial mapping of pulmonary and vascular nitrotyrosine reveals the pivotal role of myeloperoxidase as a catalyst for tyrosine nitration in inflammatory diseases Free Radic. Biol. Med. 33 2002 1010
24. L.J. Hazell, L. Arnold, D. Flowers, G. Waeg, E. Malle, and R. Stocker Presence of hypochlorite-modified proteins in human atherosclerotic lesions J. Clin. Invest. 97 1996 1535 1544 (Pubitemid 26097044)
25. E. Malle, G. Waeg, R. Schreiber, E.F. Grone, W. Sattler, and H.J. Grone Immunohistochemical evidence for the myeloperoxidase/H2O2/halide system in human atherosclerotic lesions: colocalization of myeloperoxidase and hypochlorite-modified proteins Eur. J. Biochem. 267 2000 4495 4503 (Pubitemid 30461082)
26. S. Sugiyama, Y. Okada, G.K. Sukhova, R. Virmani, J.W. Heinecke, and P. Libby Macrophage myeloperoxidase regulation by granulocyte macrophage colony-stimulating factor in human atherosclerosis and implications in acute coronary syndromes Am. J. Pathol. 158 2001 879 891 (Pubitemid 32221781)
27. K. Solly, X. Wang, X. Xu, B. Strulovici, and W. Zheng Application of real-time cell electronic sensing (RT-CES) technology to cell-based assays Assay Drug Dev. Technol. 2 2004 363 372 (Pubitemid 39276278)
28. E. Malle, L. Hazell, R. Stocker, W. Sattler, H. Esterbauer, and G. Waeg Immunologic detection and measurement of hypochlorite-modified LDL with specific monoclonal antibodies Arterioscler. Thromb. Vasc. Biol. 15 1995 982 989
29. M.C. Vissers, and C.C. Winterbourn Oxidative damage to fibronectin. I. The effects of the neutrophil myeloperoxidase system and HOCl Arch. Biochem. Biophys. 285 1991 53 59
30. C.J. van Dalen, M.W. Whitehouse, C.C. Winterbourn, and A.J. Kettle Thiocyanate and chloride as competing substrates for myeloperoxidase Biochem. J. 327 Pt 2 1997 487 492 (Pubitemid 27477827)
31. C.J. van Dalen, C.C. Winterbourn, R. Senthilmohan, and A.J. Kettle Nitrite as a substrate and inhibitor of myeloperoxidase. Implications for nitration and hypochlorous acid production at sites of inflammation J. Biol. Chem. 275 2000 11638 11644 (Pubitemid 30237723)
32. W.A. Prutz, H. Monig, J. Butler, and E.J. Land Reactions of nitrogen dioxide in aqueous model systems: oxidation of tyrosine units in peptides and proteins Arch. Biochem. Biophys. 243 1985 125 134
33. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat. Rev. Mol. Cell. Biol. 10 2009 21 33
34. M.C. Brown, and C.E. Turner Paxillin: adapting to change Physiol. Rev. 84 2004 1315 1339 (Pubitemid 39287952)
35. R. Zaidel-Bar, R. Milo, Z. Kam, and B. Geiger A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions J. Cell Sci 120 2007 137 148 (Pubitemid 46206656)
36. M. Vicente-Manzanares, X. Ma, R.S. Adelstein, and A.R. Horwitz Non-muscle myosin II takes centre stage in cell adhesion and migration Nat. Rev. Mol. Cell. Biol. 10 2009 778 790
37. S.L. Bellis, J.T. Miller, and C.E. Turner Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase J. Biol. Chem. 270 1995 17437 17441
38. E. Giannoni, M.L. Taddei, and P. Chiarugi Src redox regulation: again in the front line Free Radic. Biol. Med. 49 2010 516 527
39. J.S. Alexander, Y. Zhu, J.W. Elrod, B. Alexander, L. Coe, T.J. Kalogeris, and J. Fuseler Reciprocal regulation of endothelial substrate adhesion and barrier function Microcirculation 8 2001 389 401 (Pubitemid 33646594)
40. P.V. Usatyuk, and V. Natarajan Regulation of reactive oxygen species-induced endothelial cell-cell and cell-matrix contacts by focal adhesion kinase and adherens junction proteins Am. J. Physiol. Lung Cell Mol. Physiol 289 2005 L999 L1010
41. Y. Xu, S. Szep, and Z. Lu The antioxidant role of thiocyanate in the pathogenesis of cystic fibrosis and other inflammation-related diseases Proc. Natl. Acad. Sci. USA 106 2009 20515 20519
42. Z. Wang, S.J. Nicholls, E.R. Rodriguez, O. Kummu, S. Horkko, J. Barnard, W.F. Reynolds, E.J. Topol, J.A. DiDonato, and S.L. Hazen Protein carbamylation links inflammation, smoking, uremia and atherogenesis Nat. Med 13 2007 1176 1184 (Pubitemid 47530630)
43. M.T. Ashby, A.C. Carlson, and M.J. Scott Redox buffering of hypochlorous acid by thiocyanate in physiologic fluids J. Am. Chem. Soc. 126 2004 15976 15977 (Pubitemid 39627604)
44. B. Wildt, D. Wirtz, and P.C. Searson Programmed subcellular release for studying the dynamics of cell detachment Nat. Methods 6 2009 211 213
45. M.A. Loza-Coll, S. Perera, W. Shi, and J. Filmus A transient increase in the activity of Src-family kinases induced by cell detachment delays anoikis of intestinal epithelial cells Oncogene 24 2005 1727 1737 (Pubitemid 40461129)
46. E. Giannoni, F. Buricchi, G. Grimaldi, M. Parri, F. Cialdai, M.L. Taddei, G. Raugei, G. Ramponi, and P. Chiarugi Redox regulation of anoikis: reactive oxygen species as essential mediators of cell survival Cell Death Differ. 15 2008 867 878 (Pubitemid 351524429)
47. A. Aghajanian, E.S. Wittchen, S.L. Campbell, and K. Burridge Direct activation of RhoA by reactive oxygen species requires a redox-sensitive motif PLoS One 4 2009 e8045
48. G.A. Knock, and J.P. Ward Redox regulation of protein kinases as a modulator of vascular function Antioxid. Redox Signal. 15 2011 1531 1547
49. C.C. Winterbourn Reconciling the chemistry and biology of reactive oxygen species Nat. Chem. Biol. 4 2008 278 286 (Pubitemid 351550893)
50. C.C. Winterbourn, and M.B. Hampton Thiol chemistry and specificity in redox signaling Free Radic. Biol. Med. 45 2008 549 561