Peroxynitrite modifies the structure and function of the extracellular matrix proteoglycan perlecan by reaction with both the protein core and the heparan sulfate chains

Free Radical Biology and Medicine

Volumn 49, Issue 2, 2010, Pages 282-293

  Kennett, Eleanor C ^a   Rees, Martin D ^a   Malle, Ernst ^b   Hammer, Astrid ^b   Whitelock, John M ^c   Davies, Michael J ^a,d  

^a HEART RESEARCH INSTITUTE   (Australia)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d University of Sydney   (Australia)

Author keywords

Atherosclerosis; Cell adhesion; Cell proliferation; Extracellular matrix; Heparan sulfate proteoglycans; Inflammation; Perlecan; Peroxynitrite; Plaque rupture

Indexed keywords

3 NITROTYROSINE; ANTIBODY; BICARBONATE; CORE PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; HEPARAN SULFATE; PERLECAN; PEROXYNITRITE; PROTEOGLYCAN;

ARTICLE; ATHEROSCLEROSIS; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY ARTERY; CROSS LINKING; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPOSURE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

CELL LINE; CELL PROLIFERATION; CORONARY ARTERY DISEASE; CORONARY VESSELS; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HEPARAN SULFATE PROTEOGLYCANS; HEPARITIN SULFATE; HUMANS; IMMUNOHISTOCHEMISTRY; OXIDATIVE STRESS; PEROXYNITROUS ACID; PROTEIN BINDING; PROTEIN MULTIMERIZATION; TUNICA INTIMA;

EID: 77953539416     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.04.018     Document Type: Article

References (67)

1. Iozzo R.V., Cohen I.R., GrÀssel S., Murdoch A.D. The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem. J. 1994, 302:625-639.
2. Murdoch A., Dodge G., Cohen I., Tuan R., Iozzo R. Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Biol. Chem. 1992, 267:8544-8557.
3. Whitelock J.M., Iozzo R.V. Heparan sulfate: A complex polymer charged with biological activity. Chem. Rev. 2005, 105:2745-2764.
4. Iozzo R.V. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell. Biol. 2005, 6:646-656.
5. Whitelock J.M., Graham L.D., Melrose J., Murdoch A.D., Iozzo R.V., Underwood P.A. Human perlecan immunopurified from different endothelial cell sources has different adhesive properties for vascular cells. Matrix Biol. 1999, 18:163-178.
6. Knox S., Fosang A.J., Last K., Melrose J., Whitelock J. Perlecan from human epithelial cells is a hybrid heparan/chondroitin/keratan sulfate proteoglycan. FEBS Lett. 2005, 579:5019-5023.
7. Melrose J., Hayes A.J., Whitelock J.M., Little C.B. Perlecan, the "jack of all trades" proteoglycan of cartilaginous weight-bearing connective tissues. Bioessays 2008, 30:457-469.
8. Costell M., Carmona R., Gustafsson E., Gonzalez-Iriarte M., Fassler R., Munoz-Chapuli R. Hyperplastic conotruncal endocardial cushions and transposition of great arteries in perlecan-null mice. Circ. Res. 2002, 91:158-164.
9. Ross R. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 1999, 340:115-126.
10. Stocker R., Keaney J.F. Role of oxidative modifications in atherosclerosis. Physiol. Rev. 2004, 84:1381-1478.
11. Woods A.A., Linton S.M., Davies M.J. Detection of HOCl-mediated protein oxidation products in the extracellular matrix of human atherosclerotic plaques. Biochem. J. 2003, 370:729-735.
12. Nakashima Y., Fujii H., Sumiyoshi S., Wight T.N., Sueishi K. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1159-1165.
13. Davies M.J., Thomas A.C. Plaque fissuring - the cause of acute myocardial-infarction, sudden ischemic death, and crescendo angina. Br. Heart J. 1985, 53:363-373.
14. Raines E.W. The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int. J. Exp. Pathol. 2000, 81:173-182.
15. Kolodgie F.D., Burke A.P., Wight T.N., Virmani R. The accumulation of specific types of proteoglycans in eroded plaques: a role in coronary thrombosis in the absence of rupture. Curr. Opin. Lipidol. 2004, 15:575-582.
16. Kolodgie F.D., Burke A.P., Farb A., Weber D.K., Kutys R., Wight T.N., Virmani R. Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion. Arterioscler. Thromb. Vasc. Biol. 2002, 22:1642-1648.
17. Kinsella M.G., Tran P.K., Weiser-Evans M.C., Reidy M., Majack R.A., Wight T.N. Changes in perlecan expression during vascular injury: role in the inhibition of smooth muscle cell proliferation in the late lesion. Arterioscler. Thromb. Vasc. Biol. 2003, 23:608-614.
18. Rees M.D., Kennett E.C., Whitelock J.M., Davies M.J. Oxidative damage to extracellular matrix and its role in human pathologies. Free Radic. Biol. Med. 2008, 44:1973-2001.
19. Huie R.E., Padmaja S. The reaction of NO with superoxide. Free Radic. Res. Commun. 1993, 18:195-199.
20. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc. Natl. Acad. Sci. USA 1990, 87:1620-1624.
21. Millar T.M. Peroxynitrite formation from the simultaneous reduction of nitrite and oxygen by xanthine oxidase. FEBS Lett. 2004, 562:129-133.
22. Vásquez-Vivar J., Kalyanaraman B., Martásek P. The role of tetrahydrobiopterin in superoxide generation from eNOS: enzymology and physiological implications. Free Radic. Res. 2003, 37:121-127.
23. Beckman J.S., Ye Y.Z., Anderson P.G., Chen J., Accavitti M.A., Tarpey M.M., White C.R. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe-Seyler 1994, 375:81-88.
24. Pennathur S., Bergt C., Shao B., Byun J., Kassim S.Y., Singh P., Green P.S., McDonald T.O., Brunzell J., Chait A., Oram J.F., O'Brien K., Geary R.L., Heinecke J.W. Human atherosclerotic intima and blood of patients with established coronary artery disease contain high density lipoprotein damaged by reactive nitrogen species. J. Biol. Chem. 2004, 279:42977-42983.
25. Leeuwenburgh C., Hardy M.M., Hazen S.L., Wagner P., Ohishi S., Steinbrecher U.P., Heinecke J.W. Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J. Biol. Chem. 1997, 272:1433-1436.
26. Li M., Rosenfeld L., Vilar R.E., Cowman M.K. Degradation of hyaluronan by peroxynitrite. Arch. Biochem. Biophys. 1997, 341:245-250.
27. Kennett E.C., Davies M.J. Degradation of matrix glycosaminoglycans by peroxynitrite/peroxynitrous acid: evidence for a hydroxyl-radical-like mechanism. Free Radic. Biol. Med. 2007, 42:1278-1289.
28. Kennett E.C., Davies M.J. Glycosaminoglycans are fragmented by hydroxyl, carbonate, and nitrogen dioxide radicals in a site-selective manner: implications for peroxynitrite-mediated damage at sites of inflammation. Free Radic. Biol. Med. 2009, 47:389-400.
29. Kennett E.C., Davies M.J. Degradation of extracellular matrix by peroxynitrite/peroxynitrous acid. Free Radic. Biol. Med. 2008, 45:716-725.
30. 2-chloride system. Am. J. Pathol. 1993, 143:907-917.
31. Rees M.D., McNiven T.N., Davies M.J. Degradation of extracellular matrix and its components by hypobromous acid. Biochem. J. 2007, 401:587-596.
32. Rees M.D., Whitelock J.M., Malle E., Chuang C.Y., Iozzo R.V., Nilasaroya A., Davies M.J. Myeloperoxidase-derived oxidants selectively disrupt the protein core of the heparan sulfate proteoglycan perlecan. Matrix Biol. 2010, 29:63-73.
33. Uppu R.M., Pryor W.A. Synthesis of peroxynitrite in a two-phase system using isoamyl nitrite and hydrogen peroxide. Anal. Biochem. 1996, 236:242-249.
34. Knox S., Merry C., Stringer S., Melrose J., Whitelock J. Not all perlecans are created equal - interactions with fibroblast growth factor (FGF) 2 and FGF receptors. J. Biol. Chem. 2002, 277:14657-14665.
35. Knox S., Melrose J., Whitelock J. Electrophoretic, biosensor, and bioactivity analyses of perlecans of different cellular origins. Proteomics 2001, 1:1534-1541.
36. Hawkins C.L., Morgan P.E., Davies M.J. Quantification of protein modification by oxidants. Free Radic. Biol. Med. 2009, 46:965-988.
37. Goldberg H.A., Warner K.J. The staining of acidic proteins on polyacrylamide gels: Enhanced sensitivity and stability of ''stains-all'' staining in combination with silver nitrate. Anal. Biochem. 1997, 251:227-233.
38. Stary H.C., Chandler A.B., Dinsmore R.E., Fuster V., Glagov S., Insull W., Rosenfeld M.E., Schwartz C.J., Wagner W.D., Wissler R.W. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 1995, 15:1512-1531.
39. Marsche G., Hammer A., Oskolkova O., Kozarsky K.F., Sattler W., Malle E. Hypochlorite-modified high density lipoprotein, a high affinity ligand to scavenger receptor class B, type I, impairs high density lipoprotein-dependent selective lipid uptake and reverse cholesterol transport. J. Biol. Chem. 2002, 277:32172-32179.
40. Malle E., Marsche G., Panzenboeck U., Sattler W. Myeloperoxidase-mediated oxidation of high-density lipoproteins: fingerprints of newly recognized potential proatherogenic lipoproteins. Arch. Biochem. Biophys. 2006, 445:245-255.
41. Hammer A., Desoye G., Dohr G., Sattler W., Malle E. Myeloperoxidase-dependent generation of hypochlorite-modified proteins in human placental tissues during normal pregnancy. Lab. Invest. 2001, 81:543-554.
42. Rees M.D., Pattison D.I., Davies M.J. Oxidation of heparan sulphate by hypochlorite: role of N-chloro derivatives and dichloramine-dependent fragmentation. Biochem. J. 2005, 391:125-134.
43. Al-Assaf S., Navaratnam S., Parsons B.J., Phillips G.O. Chain scission of hyaluronan by carbonate and dichloride radical anions: Potential reactive oxidative species in inflammation?. Free Radic. Biol. Med. 2006, 40:2018-2027.
44. Chen S.N., Hoffman M.Z., Parsons G.H. Reactivity of the carbonate radical toward aromatic compounds in aqueous solution. J. Phys. Chem. 1975, 79:1911-1912.
45. Chen S.N., Hoffman M.Z. Rate constants for the reaction of the carbonate radical with compounds of biochemical interest in neutral aqueous solution. Radiat. Res. 1973, 56:40-47.
46. +-ATPases. J. Biol. Chem. 1997, 272:29810-29820.
47. Jankowski A., Scott C.C., Grinstein S. Determinants of the phagosomal pH in neutrophils. J. Biol. Chem. 2002, 277:6059-6066.
48. Deng H. Nitrite anions induce nitrosative deamination of peptides and proteins. Rapid Commun. Mass Spectrom. 2006, 20:3634-3638.
49. Lymar S.V., Hurst J.K. Rapid reaction between peroxonitrite ion and carbon dioxide: Implications for biological activity. J. Am. Chem. Soc. 1995, 117:8867-8868.
50. Radi R., Peluffo G., Alvarez M.N., Naviliat M., Cayota A. Unraveling peroxynitrite formation in biological systems. Free Radic. Biol. Med. 2001, 30:463-488.
51. Chen S.N., Hoffman M.Z. Reactivity of the carbonate radical in aqueous solution. Tryptophan and its derivatives. J. Phys. Chem. 1974, 78:2099-2102.
52. Szabo C., Ischiropoulos H., Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 2007, 6:662-680.
53. van den Born J., Salmivirta K., Henttinen T., Ostman N., Ishimaru T., Miyaura S., Yoshida K., Salmivirta M. Novel heparan sulfate structures revealed by monoclonal antibodies. J. Biol. Chem. 2005, 280:20516-20523.
54. Mani K., Cheng F., Sandgren S., van den Born J., Havsmark B., Ding K., Fransson L.-A. The heparan sulfate-specific epitope 10E4 is NO-sensitive and partly inaccessible in glypican-1. Glycobiology 2004, 14:599-607.
55. Murdoch A., Liu B., Schwarting R., Tuan R., Iozzo R. Widespread expression of perlecan proteoglycan in basement membranes and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization. J. Histochem. Cytochem. 1994, 42:239-249.
56. Whitelock J.M., Murdoch A.D., Iozzo R.V., Underwood P.A. The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J. Biol. Chem. 1996, 271:10079-10086.
57. Koenig W., Khuseyinova N. Biomarkers of atherosclerotic plaque instability and rupture. Arterioscler. Thromb. Vasc. Biol. 2007, 27:15-26.
58. Malmstrom J., Larsen K., Hansson L., Lofdahl C.G., Norregard-Jensen O., Marko-Varga G., Westergren-Thorsson G. Proteoglycan and proteome profiling of central human pulmonary fibrotic tissue utilizing miniaturized sample preparation: a feasibility study. Proteomics 2002, 2:394-404.
59. Alvarez B., Ferrer-Sueta G., Freeman B.A., Radi R. Kinetics of peroxynitrite reaction with amino acids and human serum albumin. J. Biol. Chem. 1999, 274:842-848.
60. Gow A., Duran D., Thom S.R., Ischiropoulos H. Carbon dioxide enhancement of peroxynitrite-mediated protein tyrosine nitration. Arch. Biochem. Biophys. 1996, 333:42-48.
61. Andrekopoulos C., Zhang H., Kalivendi S., Kalyanaraman B. Bicarbonate enhances α-synuclein oligomerization and nitration: Intermediacy of carbonate radical anion and nitrogen dioxide radical. Biochem. J. 2003, 378:435-447.
62. Neta P., Huie R.E., Ross A.B. Rate constants for reactions of inorganic radicals in aqueous solution. J. Phys. Chem. Ref. Data 1988, 17:1027-1284.
63. Al-Assaf S., Navaratnam S., Parsons B.J., Phillips G.O. Chain scission of hyaluronan by peroxynitrite. Arch. Biochem. Biophys. 2003, 411:73-82.
64. Hultgardh-Nilsson A., Durbeej M. Role of the extracellular matrix and its receptors in smooth muscle cell function: implications in vascular development and disease. Curr. Opin. Lipidol. 2007, 18:540-545.
65. Hayashi K., Madri J., Yurchenco P. Endothelial cells interact with the core protein of basement membrane perlecan through beta 1 and beta 3 integrins: an adhesion modulated by glycosaminoglycan. J. Cell Biol. 1992, 119:945-959.
66. Folkman J., Klagsbrun M., Sasse J., Wadzinski M., Ingber D., Vlodavsky I. A heparin-binding angiogenic protein-basic fibroblast growth factor-is stored within basement membrane. Am. J. Pathol. 1988, 130:393-400.
67. Saksela O., Moscatelli D., Sommer A., Rifkin D. Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell Biol. 1988, 107:743-751.