The acute-phase protein serum amyloid A induces endothelial dysfunction that is inhibited by high-density lipoprotein

Free Radical Biology and Medicine

Volumn 51, Issue 7, 2011, Pages 1390-1398

  Witting, Paul K ^a,b   Song, Changjie ^b   Hsu, Kenneth ^c   Hua, Susan ^b   Parry, Sarah N ^a   Aran, Roshanak ^a   Geczy, Carolyn ^c   Freedman, Saul Benedict ^b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Acute phase protein; Endothelial function; Free radicals; Inflammation; Nitric oxide

Indexed keywords

ACETYLCHOLINE; APOCYNIN; ARGINASE 1; CALCIUM ION; DIMER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HIGH DENSITY LIPOPROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MONOMER; NITRIC OXIDE; SERUM AMYLOID A; SUPEROXIDE; SUPEROXIDE DISMUTASE; THROMBOPLASTIN;

ANIMAL TISSUE; AORTA CONSTRICTION; ARTICLE; BIOAVAILABILITY; BLOOD VESSEL REACTIVITY; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SYNTHESIS; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ANIMALS; AORTA; ARGINASE; ATHEROSCLEROSIS; BLOTTING, WESTERN; CALCIUM; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION; HUMANS; INFLAMMATION; LIPOPROTEINS, HDL; MALE; NF-KAPPA B; NITRIC OXIDE; RATS; RATS, WISTAR; SERUM AMYLOID A PROTEIN; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; SUPEROXIDES; THROMBOPLASTIN;

EID: 80052265183     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.06.031     Document Type: Article

References (56)

1. N. Utoguchi, K. Ikeda, K. Saeki, N. Oka, H. Mizuguchi, K. Kubo, S. Nakagawa, and T. Mayumi Ascorbic acid stimulates barrier function of cultured endothelial cell monolayer J. Cell. Physiol. 163 1995 393 399
2. P.L. Ludmer, A.P. Selwyn, T.L. Shook, R.R. Wayne, G.H. Mudge, R.W. Alexander, and P. Ganz Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries N. Engl. J. Med. 315 1986 1046 1051 (Pubitemid 17170620)
3. J.A. Panza, C.E. Garcia, C.M. Kilcoyne, A.A. Quyyumi, and R.O. Cannon Impaired endothelium-dependent vasodilation in patients with essential hypertension: evidence that nitric oxide abnormality is not localized to a single signal transduction pathway Circulation 91 1995 1732 1738
4. L.J. Ignarro, G.M. Buga, K.S. Wood, R.E. Byrns, and G. Chaudhuri Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide Proc. Natl. Acad. Sci. U.S.A. 84 1987 9265 9269
5. H. Azuma, M. Ishikawa, and S. Sekizaki Endothelium-dependent inhibition of platelet aggregation Br. J. Pharmacol. 88 1986 411 415 (Pubitemid 16123105)
6. P. Kubes, M. Suzuki, and D.N. Granger Nitric oxide: an endogenous modulator of leukocyte adhesion Proc. Natl. Acad. Sci. U.S.A. 88 1991 4651 4655 (Pubitemid 21914599)
7. F.C. Tanner, P. Meier, H. Greutert, C. Champion, E.G. Nabel, and T.F. Luscher Nitric oxide modulates expression of cell cycle regulatory proteins: a cytostatic strategy for inhibition of human vascular smooth muscle cell proliferation Circulation 10 2000 1982 1989 (Pubitemid 30225281)
8. C.M. Uhlar, and A.S. Whitehead Serum amyloid A, the major vertebrate acute-phase reactant Eur. J. Biochem. 265 1999 501 523 (Pubitemid 29488982)
9. S. Urieli-Shoval, R.P. Linke, and Y. Matzner Expression and function of serum amyloid A in normal and disease states Curr. Opin. Hematol. 7 2000 64 69 (Pubitemid 30007690)
10. S. Hua, C. Song, C.L. Geczy, S.B. Freedman, and P.K. Witting A role for acute-phase serum amyloid A and high-density lipoprotein in oxidative stress, endothelial dysfunction and atherosclerosis Redox Rep. 14 2009 187 196
11. M. Erren, H. Reinecke, R. Junker, M. Fobker, H. Schulte, J.O. Schurek, J. Kropf, S. Kerber, G. Breithardt, G. Assmann, and P. Cullen Systemic inflammatory parameters in patients with atherosclerosis of the coronary and peripheral arteries Arterioscler. Thromb. Vasc. Biol. 19 1999 2355 2363 (Pubitemid 29477836)
12. P. Jousilahti, V. Salomaa, V. Rasi, E. Vahtera, and T. Palosuo The association of C-reactive protein, serum amyloid A and fibrinogen with prevalent coronary heart disease-baseline findings of the PAIS project Atherosclerosis 156 2001 451 456 (Pubitemid 32522927)
13. R.L. Meek, S. Urieli-Shoval, and E.P. Benditt Expression of apolipoprotein serum amyloid A mRNA in human atherosclerotic lesions and cultured vascular cells, implications for serum amyloid A function Proc. Natl. Acad. Sci. U.S.A. 91 1994 3186 3190 (Pubitemid 24130200)
14. C. Song, Y. Shen, E. Yamen, K. Hsu, W. Yan, P.K. Witting, C.L. Geczy, and S.B. Freedman Serum amyloid A may potentiate prothrombotic and pro-inflammatory events in acute coronary syndromes Atherosclerosis 202 2009 596 604
15. X. Wang, H. Chai, Z. Wang, P.H. Lin, Q. Yao, and C. Chen Serum amyloid A induces endothelial dysfunction in porcine coronary arteries and human coronary artery endothelial cells Am. J. Physiol. Heart Circ. Physiol. 295 2008 H2399 H2408
16. E.J. Yavin, L. Preciado-Patt, O. Rosen, M. Yaron, R.D. Suessmuth, D. Levartowsky, G. Jung, O. Lider, and M. Fridkin Serum amyloid A-derived peptides, present in human rheumatic synovial fluids, induce the secretion of interferon-gamma by human CD(4)(+) T-lymphocytes FEBS Lett. 472 2000 259 262 (Pubitemid 30224475)
17. R. Badolato, J.M. Wang, S.L. Stornello, A.N. Ponzi, M. Duse, and T. Musso Serum amyloid A is an activator of PMN antimicrobial functions: induction of degranulation, phagocytosis, and enhancement of anti-Candida activity J. Leukoc. Biol. 67 2000 381 386
18. S. Hayat, and J.G. Raynes Acute phase serum amyloid A protein increases high density lipoprotein binding to human peripheral blood mononuclear cells and an endothelial cell line Scand. J. Immunol. 51 2000 141 146 (Pubitemid 30095760)
19. A. Artl, G. Marsche, S. Lestavel, W. Sattler, and E. Malle Role of serum amyloid A during metabolism of acute-phase HDL by macrophages Arterioscler. Thromb. Vasc. Biol. 20 2000 763 772 (Pubitemid 30151692)
20. E. Malle, and F.C. De Beer Human serum amyloid A (SAA) protein: a prominent acute-phase reactant for clinical practice Eur. J. Clin. Invest. 26 1996 427 435 (Pubitemid 26226404)
21. D. Ashby, J. Gamble, M. Vadas, N. Fidge, S. Siggins, K. Rye, and P.J. Barter Lack of effect of serum amyloid A (SAA) on the ability of high-density lipoproteins to inhibit endothelial cell adhesion molecule expression Atherosclerosis 154 2001 113 121 (Pubitemid 32008570)
22. P.G. Wilson, J.C. Thompson, N.R. Webb, F.C. de Beer, V.L. King, and L.R. Tannock Serum amyloid A, but not C-reactive protein, stimulates vascular proteoglycan synthesis in a pro-atherogenic manner Am. J. Pathol. 173 2008 1902 1910
23. A.M. Gotto Jr. , and E.A. Brinton Assessing low levels of high-density lipoprotein cholesterol as a risk factor in coronary heart disease: a working group report and update J. Am. Coll. Cardiol. 43 2004 717 724 (Pubitemid 38296465)
24. P.J. Barter, S. Nicholls, K.A. Rye, G.M. Anantharamaiah, M. Navab, and A.M. Fogelman Anti-inflammatory properties of HDL Circ. Res. 95 2004 764 772
25. A. Negre-Salvayre, N. Dousset, G. Ferretti, T. Bacchetti, G. Curatola, and R. Salvayre Antioxidant and cytoprotective properties of HDL in vascular cells Free Radic. Biol. Med. 41 2006 1031 1040 (Pubitemid 44348872)
26. H. Cai, C. Song, I. Endoh, J. Goyette, W. Jessup, S.B. Freedman, H.P. McNeil, and C.L. Geczy Serum amyloid A induces monocyte tissue factor J. Immunol. 178 2007 1852 1860 (Pubitemid 46154658)
27. C. Song, K. Hsu, E. Yamen, W. Yan, J. Fock, P.K. Witting, C.L. Geczy, and S.B. Freedman SAA induction of cytokines in monocytes/macrophages and lymphocytes Atherosclerosis 207 2009 374 383
28. P.K. Witting, D. Mohr, and R. Stocker Assessment of prooxidant activity of vitamin E in human low-density lipoprotein and plasma Methods Enzymol. 299 1999 362 375
29. A.K. Lau, S.B. Leichtweis, P. Hume, R. Mashima, J.Y. Hou, X. Chaufour, B. Wilkinson, N.H. Hunt, D.S. Celermajer, and R. Stocker Probucol promotes functional reendothelialization in balloon-injured rabbit aortas Circulation 107 2003 2031 2036 (Pubitemid 36506079)
30. P.K. Witting, B.S. Rayner, B.J. Wu, N.A. Ellis, and R. Stocker Hydrogen peroxide promotes endothelial dysfunction by stimulating multiple sources of superoxide anion radical production and decreasing nitric oxide bioavailability Cell. Physiol. Biochem. 20 2007 255 268 (Pubitemid 47340589)
31. S.R. Thomas, K. Chen, and J.F. Keaney Jr. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signalling pathway J. Biol. Chem. 277 2002 6017 6024 (Pubitemid 34968385)
32. 2, promotes metal-ion efflux in aortic endothelial cells: elemental mapping by a hard X-ray microprobe Biochemistry 45 2006 12500 12509 (Pubitemid 44583692)
33. J. Surapisitchat, K.I. Jeon, C. Yan, and J.A. Beavo Differential regulation of endothelial cell permeability by cGMP via phosphodiesterases 2 and 3 Circ. Res. 101 2007 811 888
34. B.S. Rayner, S. Hua, T. Sabaretnam, and P.K. Witting Nitric oxide stimulates myoglobin gene and protein expression in vascular smooth muscle Biochem. J. 423 2009 169 177
35. R. Stocker, A. Huang, E. Jeranian, J.Y. Hou, T.T. Wu, S.R. Thomas, and J.F. Keaney Jr. Hypochlorous acid impairs endothelium-derived nitric oxide bioactivity through a superoxide-dependent mechanism Arterioscler. Thromb. Vasc. Biol. 24 2004 2028 2033 (Pubitemid 39482425)
36. E.H. Shin, H.Y. Lee, S.D. Kim, S.H. Jo, M.K. Kim, K.S. Park, H. Lee, and Y.S. Bae Trp-Arg-Trp-Trp-Trp-Trp antagonizes formyl peptide receptor-like 2-mediated signaling Biochem. Biophys. Res. Commun. 341 2006 1317 1322 (Pubitemid 43221806)
37. Y.-S. Bae, H.Y. Lee, E.J. Jo, J.I. Kim, H.-K. Kang, R.D. Ye, J.-Y. Kwak, and S.H. Ryu Identification of peptides that antagonize formyl peptide receptor-like 1-mediated signaling J. Immunol. 173 2004 607 614 (Pubitemid 38797390)
38. M. Warnken, S. Haag, S. Matthiesen, U.R. Juergens, and K. Racké Species differences in expression pattern of arginase isoenzymes and differential effects of arginase inhibition on collagen synthesis in human and rat pulmonary fibroblasts Naunyn Schmiedebergs Arch. Pharmacol. 381 2010 297 304
39. D.M. Levine, T.S. Parker, T.M. Donnelly, A. Walsh, and A.L. Rubin In vivo protection against endotoxin by plasma high-density lipoprotein Proc. Natl. Acad. Sci. U.S.A. 90 1993 12040 12044 (Pubitemid 24008776)
40. L. Björkman, A. Karlsson, M.J. Rabiet, F. Boulay, H. Fu, J. Byland, and C. Dahlgren Serum amyloid A mediates human neutrophil production of reactive oxygen species through a receptor independent formyl peptide receptor like-1 J. Leukoc. Biol. 83 2008 245 253 (Pubitemid 351225604)
41. 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
42. L.E. Jensen, and A.S. Whitehead Regulation of serum amyloid A protein expression during the acute-phase response Biochem. J. 334 1998 489 503 (Pubitemid 28457193)
43. L. Perségol, B. Vergès, M. Foissac, P. Gambert, and L. Duvillard Inability of HDL from type 2 diabetic patients to counteract the inhibitory effect of oxidised LDL on endothelium-dependent vasorelaxation Diabetologia 49 2006 1380 1386
44. T.S. Liang, J.-M. Wang, P.M. Murphy, and J.-L. Gao Serum amyloid A is a chemotactic agonist at FPR2, a low-affinity N-formylpeptide receptor on mouse neutrophils Biochem. Biophys. Res. Commun. 270 2000 331 335 (Pubitemid 30446837)
45. N. Cheng, R. He, J. Tian, P.P. Ye, and R.D. Ye Cutting edge: TLR2 is a functional receptor for acute-phase serum amyloid A J. Immunol. 181 2008 22 26
46. S. Hiratsuka, A. Watanabe, Y. Sakurai, S. Akashi-Takamura, S. Ishibashi, K. Miyake, M. Shibuya, S. Akira, H. Aburatani, and Y. Maru The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase Nat. Cell Biol. 10 2008 1349 1355
47. 2+ store depletion in bovine vascular endothelial cells J. Physiol. 523 2000 549 559 (Pubitemid 30153817)
48. C. Zhang, J. Wu, X. Xu, B.J. Potter, and X. Gao Direct relationship between levels of TNF-alpha expression and endothelial dysfunction in reperfusion injury Basic Res. Cardiol. 105 2010 453 464
49. H. Li, C.J. Meininger, K.A. Kelly, J.R. Hawker Jr. , S.M. Morris Jr. , and G. Wu Activities of arginase I and II are limiting for endothelial cell proliferation Am. J. Physiol. Regul. Integr. Comp. Physiol. 282 2002 R64 R69 (Pubitemid 34663912)
50. D.T. Golenbock, R.R. Bach, H. Lichenstein, T.S. Juan, A. Tadavarthy, and C.F. Moldow Soluble CD14 promotes LPS activation of CD14-deficient PNH monocytes and endothelial cells J. Lab. Clin. Med. 125 1995 662 671
51. L. Perségol, B. Vergès, P. Gambert, and L. Duvillard Inability of HDL from abdominally obese subjects to counteract the inhibitory effect of oxidized LDL on vasorelaxation J. Lipid Res. 48 2007 1396 1401 (Pubitemid 47312042)
52. N. Eriksen, and E.P. Benditt Isolation and characterization of the amyloid-related apoprotein (SAA) from human high-density lipoprotein Proc. Natl. Acad. Sci. U.S.A. 77 1980 6860 6864 (Pubitemid 11219045)
53. Y. Kumon, Y. Nakauchi, K. Kidawara, M. Fukushima, S. Kobayashi, and Y. Ikeda A longitudinal analysis of alteration in lecithin-cholesterol acyltransferase and paraoxonase activities following laparoscopic cholecystectomy relative to other parameters of HDL function and the acute phase response Scand. J. Immunol. 48 1988 419 424
54. K. O'Brien, and A. Chait Serum amyloid A: the "other" inflammatory protein Curr. Atheroscler. Rep. 8 2006 62 68 (Pubitemid 43675756)
55. T. Yamada, J. Sato, and Y. Okuda Differential affinity of serum amyloid A1 isotypes for high-density lipoprotein Amyloid 16 2009 196 200
56. P.A. Barter, P. Gotto, A.M. LaRosa, J.C. Maroni, J. Szarek, M. Grundy, S.M. Kastelein, and J.J.P. Bittner HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events N. Engl. J. Med. 357 2007 1301 1310