Neutrophil serine proteases mediate inflammatory cell recruitment by glomerular endothelium and progression towards dysfunction

Nephrology Dialysis Transplantation

Volumn 27, Issue 12, 2012, Pages 4331-4338

  Kuravi, Sahithi J ^a   Bevins, Anne ^a   Satchell, Simon C ^b   Harper, Lorraine ^a   Williams, Julie M ^c   Ed Rainger, G ^a   Savage, Caroline O S ^a   Tull, Samantha P ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c QUEEN ELIZABETH HOSPITAL   (United Kingdom)

Author keywords

adhesion; elastase; neutrophils; platelets; proteinase 3

Indexed keywords

CASPASE 3; ELASTASE; INTERLEUKIN 8; MYELOBLASTIN; PADGEM PROTEIN; PROTEIN P21;

ARTICLE; CELL ADHESION; CELL DAMAGE; CELL MEMBRANE; CELL VIABILITY; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; GLOMERULONEPHRITIS; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATORY CELL; NEUTROPHIL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; THROMBOCYTE ADHESION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULITIC GLOMERULONEPHRITIS;

HUMANS; INFLAMMATION; KIDNEY GLOMERULUS; MYELOBLASTIN; NEUTROPHIL INFILTRATION; PANCREATIC ELASTASE; UROTHELIUM;

EID: 84865602319     PISSN: 09310509     EISSN: 14602385     Source Type: Journal    
DOI: 10.1093/ndt/gfs180     Document Type: Article

References (53)

1. Tervaert JW, Mulder L, Stegeman C et al. Occurrence of autoantibodies to human leucocyte elastase in Wegener's granulomatosis and other inflammatory disorders. Ann Rheum Dis 1993; 52: 115-120.
2. Ludemann J, Utecht B, Gross WL. Anti-neutrophil cytoplasm antibodies in Wegener's granulomatosis recognize an elastinolytic enzyme. J Exp Med 1990; 171: 357-362.
3. Goldschmeding R, van der Schoot CE, ten Bokkel Huinink D et al. Wegener's granulomatosis autoantibodies identify a novel diisopropylfluorophosphate- binding protein in the lysosomes of normal human neutrophils. J Clin Invest 1989; 84: 1577-1587.
4. Falk RJ, Jennette JC. Anti-neutrophil cytoplasmic autoantibodies with specificity for myeloperoxidase in patients with systemic vasculitis and idiopathic necrotizing and crescentic glomerulonephritis. N Engl J Med 1988; 318: 1651-1657.
5. Haubitz M, Schulzeck P, Schellong S et al. Complexed plasma elastase as an in vivo marker for leukocyte activation in antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheum 1997; 40: 1680-1684.
6. Henshaw TJ, Malone CC, Gabay JE et al. Elevations of neutrophil proteinase 3 in serum of patients with Wegener's granulomatosis and polyarteritis nodosa. Arthritis Rheum 1994; 37: 104-112.
7. Johnson RJ, Couser WG, Alpers CE et al. The human neutrophil serine proteinases, elastase and cathepsin-G, can mediate glomerular injury in vivo. J Exp Med 1988; 168: 1169-1174.
8. Brinkmann V, Reichard U, Goosmann C et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303: 1532-1535.
9. Kessenbrock K, Krumbholz M, Schonermarck U et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 2009; 15: 623-625.
10. Pilette C, Ouadrhiri Y, Dimanche F et al. Secretory component is cleaved by neutrophil serine proteinases but its epithelial production is increased by neutrophils through NF-kappa B-and p38 mitogenactivated protein kinase-dependent mechanisms. Am J Respir Cell Mol Biol 2003; 28: 485-498.
11. Boehme MWJ, Galle P, Stremmel W. Kinetics of thrombomodulin release and endothelial cell injury by neutrophil-derived proteases and oxygen radicals. Immunology 2002; 107: 340-349.
12. Preston GA, Zarella CS, Pendergraft WF et al. Novel effects of neutrophil-derived proteinase 3 and elastase on the vascular endothelium involve in vivo cleavage of NF-kappa B and proapoptotic changes in JNK, ERK, and p38 MAPK signaling pathways. J Am Soc Nephrol 2002; 13: 2840-2849.
13. Hakkim A, Furnrohr BG, Amann K et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci USA 2010; 107: 9813-9818.
14. Witko-Sarsat V, Lesavre P, Lopez S et al. A large subset of neutrophils expressing membrane proteinase 3 is a risk factor for vasculitis and rheumatoid arthritis. J Am Soc Nephrol 1999; 10: 1224-1233.
15. Schreiber A, Luft FC, Kettritz R. Membrane proteinase 3 expression and ANCA-induced neutrophil activation. Kidney Int 2004; 65: 2172-2183.
16. Muller Kobold AC, Kallenberg CG, Tervaert JW. Leucocyte membrane expression of proteinase 3 correlates with disease activity in patients with Wegener/'s granulomatosis. Br J Rheumatol 1998; 37: 901-907.
17. Campbell EJ, Campbell MA, Owen CA. Bioactive proteinase 3 on the cell surface of human neutrophils: quantification, catalytic activity, and susceptibility to inhibition. J Immunol 2000; 165: 3366-3374.
18. King WJ, Adu D, Daha MR et al. Endothelial-cells and renal epithelial-cells do not express the Wegeners autoantigen, Proteinase-3. Clin Exp Immunol 1995; 102: 98-105.
19. Taekema-Roelvink MEJ, Van Kooten C, Heemskerk E et al. Proteinase 3 interacts with a 111-kD membrane molecule of human umbilical vein endothelial cells. J Am Soc Nephrol 2000; 11: 640-648.
20. Pendergraft WF, Alcorta DA, Segelmark M et al. ANCA antigens, proteinase 3 and myeloperoxidase, are not expressed in endothelial cells. Kidney Int 2000; 57: 1981-1990.
21. Ballieux H, Klar-Mohamad N, Hagen EC et al. Detachment and cytolysis of human endothelial cells by proteinase 3. Eur J Immunol 1994; 24: 3211-3215.
22. Yang JJ, Kettritz R, Falk RJ et al. Apoptosis of endothelial cells induced by the neutrophil serine proteases proteinase 3 and elastase. Am J Pathol 1996; 149: 1617-1626.
23. Yang JJ, Preston GA, Pendergraft WF et al. Internalization of proteinase 3 is concomitant with endothelial cell apoptosis and internalization of myeloperoxidase with generation of intracellular oxidants. Am J Pathol 2001; 158: 581-592.
24. Brachemi S, Mambole A, Fakhouri F et al. Increased membrane expression of proteinase 3 during neutrophil adhesion in the presence of anti proteinase 3 antibodies. J Am Soc Nephrol 2007; 18: 2330-2339.
25. Calderwood JW, Williams JM, Morgan MD et al. ANCA induces beta(2) integrin and CXC chemokine-dependent neutrophil-endothelial cell interactions that mimic those of highly cytokine-activated endothelium. J Leukoc Biol 2005; 77: 33-43.
26. Rao NV, Wehner NG, Marshall BC et al. Characterization of proteinase-3 (PR-3), a neutrophil serine proteinase. J Biol Chem 1991; 266: 9540-9548.
27. Renesto P, Si-Tahar M, Moniatte M. Specific inhibition of thrombininduced cell activation by the neutrophil proteinases elastase, cathepsin G, and proteinase 3: evidence for distinct cleavage sites within the aminoterminal domain of the thrombin receptor. Blood 1997; 89: 1944-1953.
28. Satchell SC, Tasman CH, Singh A et al. Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF. Kidney Int 2006; 69: 1633-1640.
29. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63.
30. Tull SP, Anderson SI, Hughan SC et al. Cellular pathology of atherosclerosis: smooth muscle cells promote adhesion of platelets to cocultured endothelial cells. Circ Res 2006; 98: 98-104.
31. Cooke BM, Usami S, Perry I et al. A simplified method for culture of endothelial cells and analysis of adhesion of blood cells under conditions of flow. Microvasc Res 1993; 45: 33-45.
32. Bath PMW, Booth RFG, Hassall DG. Monocyte-lymphocyte discrimination in a new microtitre-based adhesion assay. J Immunol Methods 1989; 118: 59-65.
33. Schierwagen C, Bylundfellenius AC, Lundberg C. Improved method for quantification of tissue Pmn accumulation measured by myeloperoxidase activity. J Pharmacol Methods 1990; 23: 179-186.
34. Sud'ina GF, Mirzoeva OK, Galkina SI et al. Involvement of ecto-ATPase and extracellular ATP in polymorphonuclear granulocyteendothelial interactions. FEBS Lett 1998; 423: 243-248.
35. de Bono DP, Yang WD. Exposure to low concentrations of hydrogen peroxide causes delayed endothelial cell death and inhibits proliferation of surviving cells. Atherosclerosis 1995; 114: 235-245.
36. Varani J, Ginsburg I, Schuger L et al. Endothelial-cell killing by neutrophils-synergistic interaction of oxygen products and proteases. Am J Pathol 1989; 135: 435-438.
37. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med 1989; 320: 365-376.
38. Pall AA, Savage COS. Mechanisms of endothelial cell injury in vasculitis. Springer Semin Immunopathol 1994; 16: 23-37.
39. Yamada O, Moldow CF, Sacks T et al. Deleterious effects of endotoxin on cultured endothelial cells: An in vitro model of vascular injury. Inflammation 1981; 5: 115-126.
40. Zeck-Kapp G, Kapp A, Busse R et al. Interaction of granulocytes and endothelial cells upon stimulation with tumor necrosis factoralpha: an ultrastructural study. Immunobiology 1990; 181: 267-75.
41. Padrines M, Wolf M, Walz A et al. Interleukin-8 processing by neutrophil elastase, cathepsin G and proteinase-3. FEBS Lett 1994; 352: 231-235.
42. Hunt BJ, Jurd KM. Endothelial cell activation. BMJ 1998; 316: 1328-1329.
43. Haubitz M, Gerlach M, Kruse HJ et al. Endothelial tissue factor stimulation by proteinase 3 and elastase. Clin Exp Immunol 2001; 126: 584-588.
44. Berger SP, Seelen MAJ, Hiemstra PS et al. Proteinase 3, the major autoantigen of Wegener's granulomatosis, enhances IL-8 production by endothelial cells in vitro. J Am Soc Nephrol 1996; 7: 694-701.
45. Taekema-Roelvink MEJ, Van Kooten C, Van der Kooij S et al. Proteinase 3 enhances endothelial monocyte chemoattractant protein-1 production and induces increased adhesion of neutrophils to endothelial cells by upregulating intercellular cell adhesion molecule-1. J Am Soc Nephrol 2001; 12: 932-940.
46. Pendergraft WF, Rudolph EH, Falk RJ et al. Proteinase 3 sidesteps caspases and cleaves p21(Waf1/Cip1/Sdi1) to induce endothelial cell apoptosis. Kidney Int 2004; 65: 75-84.
47. Koster R, di Pietro A, Timmer-Bosscha H et al. Cytoplasmic p21 expression levels determine cisplatin resistance in human testicular cancer. J Clin Invest 2010; 120: 3594-3605.
48. Moon DO, Choi YH, Kim GY. Role of p21 in SP600125-induced cell cycle arrest, endoreduplication, and apoptosis. Cell Mol Life Sci 2011; 68: 3249-3260.
49. Stefansson S, Yepes M, Gorlatova N et al. Mutants of plasminogen activator inhibitor-1 designed to inhibit neutrophil elastase and cathepsin g are more effective in vivo than their endogenous inhibitors. J Biol Chem 2004; 279: 29981-29987.
50. Zani ML, Baranger K, Guyot N et al. Protease inhibitors derived from elafin and SLPI and engineered to have enhanced specificity towards neutrophil serine proteases. Protein Sci 2009; 18: 579-594.
51. Grimstein C, Choi YK, Satoh M et al. Combination of alpha-1 antitrypsin and doxycycline suppresses collagen-induced arthritis. J Gene Med 2010; 12: 35-44.
52. Korkmaz B, Horwitz MS, Jenne DE et al. Neutrophil elastase, proteinase 3, and cathepsin G as therapeutic targets in human diseases. Pharmacol Rev 2010; 62: 726-759.
53. Novick D, Rubinstein M, Azam T et al. Proteinase 3 is an IL-32 binding protein. Proc Natl Acad Sci USA 2006; 103: 3316-3321.