Proteinase 3 contributes to transendothelial migration of NB1-positive neutrophils

Journal of Immunology

Volumn 188, Issue 5, 2012, Pages 2419-2426

  Kuckleburg, Christopher J ^a   Tilkens, Sarah B ^a   Santoso, Sentot ^b   Newman, Peter J ^a  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; INTERLEUKIN 1BETA; MEMBRANE PROTEIN; MYELOBLASTIN; NB1 PROTEIN; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL JUNCTION; CONTROLLED STUDY; ENDOTHELIUM; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GPI-LINKED PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISOANTIGENS; MYELOBLASTIN; NEUTROPHILS; RECEPTORS, CELL SURFACE; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84857484531     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102540     Document Type: Article

References (55)

1. Newman, P. J., M. C. Berndt, J. Gorski, G. C. White, II, S. Lyman, C. Paddock, and W. A. Muller. 1990. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 247: 1219-1222.
2. Newman, P. J. 1994. The role of PECAM-1 in vascular cell biology. Ann. N. Y. Acad. Sci. 714: 165-174. (Pubitemid 24197788)
3. Sun, Q. H., H. M. DeLisser, M. M. Zukowski, C. Paddock, S. M. Albelda, and P. J. Newman. 1996. Individually distinct Ig homology domains in PECAM-1 regulate homophilic binding and modulate receptor affinity. J. Biol. Chem. 271: 11090-11098.
4. Newton, J. P., C. D. Buckley, E. Y. Jones, and D. L. Simmons. 1997. Residues on both faces of the first immunoglobulin fold contribute to homophilic binding sites of PECAM-1/CD31. J. Biol. Chem. 272: 20555-20563. (Pubitemid 27355613)
5. Sun, J., C. Paddock, J. Shubert, H. B. Zhang, K. Amin, P. J. Newman, and S. M. Albelda. 2000. Contributions of the extracellular and cytoplasmic domains of platelet-endothelial cell adhesion molecule-1 (PECAM-1/CD31) in regulating cell-cell localization. J. Cell Sci. 113: 1459-1469. (Pubitemid 30240563)
6. Bergom, C., C. Paddock, C. Gao, T. Holyst, D. K. Newman, and P. J. Newman. 2008. An alternatively spliced isoform of PECAM-1 is expressed at high levels in human and murine tissues, and suggests a novel role for the C-terminus of PECAM-1 in cytoprotective signaling. J. Cell Sci. 121: 1235-1242. (Pubitemid 351753507)
7. Ferrero, E., M. E. Ferrero, R. Pardi, and M. R. Zocchi. 1995. The platelet endothelial cell adhesion molecule-1 (PECAM1) contributes to endothelial barrier function. FEBS Lett. 374: 323-326.
8. Graesser, D., A. Solowiej, M. Bruckner, E. Osterweil, A. Juedes, S. Davis, N. H. Ruddle, B. Engelhardt, and J. A. Madri. 2002. Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109: 383-392. (Pubitemid 34141812)
9. Muller, W. A., S. A. Weigl, X. Deng, and D. M. Phillips. 1993. PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 178: 449-460. (Pubitemid 23218193)
10. Nakada, M. T., K. Amin, M. Christofidou-Solomidou, C. D. O'Brien, J. Sun, I. Gurubhagavatula, G. A. Heavner, A. H. Taylor, C. Paddock, Q. H. Sun, et al. 2000. Antibodies against the first Ig-like domain of human platelet endothelial cell adhesion molecule-1 (PECAM-1) that inhibit PECAM-1-dependent homophilic adhesion block in vivo neutrophil recruitment. J. Immunol. 164: 452-462. (Pubitemid 30013021)
11. Liao, F., H. K. Huynh, A. Eiroa, T. Greene, E. Polizzi, and W. A. Muller. 1995. Migration of monocytes across endothelium and passage through extracellular matrix involve separate molecular domains of PECAM-1. J. Exp. Med. 182: 1337-1343.
12. Wong, C. W., G. Wiedle, C. Ballestrem, B. Wehrle-Haller, S. Etteldorf, M. Bruckner, B. Engelhardt, R. H. Gisler, and B. A. Imhof. 2000. PECAM-1/CD31 trans-homophilic binding at the intercellular junctions is independent of its cytoplasmic domain; evidence for heterophilic interaction with integrin alphavbeta3 in Cis. Mol. Biol. Cell 11: 3109-3121. (Pubitemid 32107087)
13. Deaglio, S., M. Morra, R. Mallone, C. M. Ausiello, E. Prager, G. Garbarino, U. Dianzani, H. Stockinger, and F. Malavasi. 1998. Human CD38 (ADP-ribosyl cyclase) is a counter-receptor of CD31, an Ig superfamily member. J. Immunol. 160: 395-402. (Pubitemid 28116754)
14. Sachs, U. J., C. L. Andrei-Selmer, A. Maniar, T. Weiss, C. Paddock, V. V. Orlova, E. Y. Choi, P. J. Newman, K. T. Preissner, T. Chavakis, and S. Santoso. 2007. The neutrophil-specific CD177 is a counter-receptor for platelet endothelial cell adhesion molecule-1 (CD31). J. Biol. Chem. 282: 23603-23612. (Pubitemid 47311956)
15. Göhring, K., J. Wolff, W. Doppl, K. L. Schmidt, K. Fenchel, H. Pralle, U. Sibelius, and J. Bux. 2004. Neutrophil CD177 (NB1 gp, HNA-2a) expression is increased in severe bacterial infections and polycythaemia vera. Br. J. Haematol. 126: 252-254. (Pubitemid 38961945)
16. Kissel, K., S. Santoso, C. Hofmann, D. Stroncek, and J. Bux. 2001. Molecular basis of the neutrophil glycoprotein NB1 (CD177) involved in the pathogenesis of immune neutropenias and transfusion reactions. Eur. J. Immunol. 31: 1301-1309. (Pubitemid 32454678)
17. Kissel, K., S. Scheffler, M. Kerowgan, and J. Bux. 2002. Molecular basis of NB1 (HNA-2a, CD177) deficiency. Blood 99: 4231-4233. (Pubitemid 35332073)
18. Lalezari, P., G. B. Murphy, and F. H. Allen, Jr. 1971. NB1 a new neutrophil-specific involved in the pathogenesis of neonatal neutropenia. J. Clin. Invest. 50: 1108-1115.
19. Newton, J. P., A. P. Hunter, D. L. Simmons, C. D. Buckley, and D. J. Harvey. 1999. CD31 (PECAM-1) exists as a dimer and is heavily N-glycosylated. Biochem. Biophys. Res. Commun. 261: 283-291. (Pubitemid 29392470)
20. Bayat, B., S. Werth, U. J. Sachs, D. K. Newman, P. J. Newman, and S. Santoso. 2010. Neutrophil transmigration mediated by the neutrophil-specific CD177 is influenced by the endothelial S536N dimorphism of platelet endothelial cell adhesion molecule-1. J. Immunol. 184: 3889-3896.
21. von Vietinghoff, S., G. Tunnemann, C. Eulenberg, M. Wellner, M. Cristina Cardoso, F. C. Luft, and R. Kettritz. 2007. NB1 mediates surface expression of the ANCA proteinase 3 on human neutrophils. Blood 109: 4487-4493. (Pubitemid 46743419)
22. Kao, R. C., N. G. Wehner, K. M. Skubitz, B. H. Gray, and J. R. Hoidal. 1988. Proteinase 3: a distinct human polymorphonuclear leukocyte proteinase that produces emphysema in hamsters. J. Clin. Invest. 82: 1963-1973. (Pubitemid 19054944)
23. Lüdemann, J., B. Utecht, and W. L. Gross. 1990. Anti-neutrophil cytoplasm antibodies in Wegener's granulomatosis recognize an elastinolytic enzyme. J. Exp. Med. 171: 357-362. (Pubitemid 20040624)
24. Lüdemann, J., B. Utecht, and W. L. Gross. 1991. Anti-cytoplasmic antibodies in Wegener's granulomatosis are directed against proteinase 3. Adv. Exp. Med. Biol. 297: 141-150.
25. Dolman, K. M., A. Jager, A. Sonnenberg, A. E. von dem Borne, and R. Goldschmeding. 1995. Proteolysis of classic anti-neutrophil cytoplasmic autoantibodies (C-ANCA) by neutrophil proteinase 3. Clin. Exp. Immunol. 101: 8-12.
26. Raife, T. J., W. Cao, B. S. Atkinson, B. Bedell, R. R. Montgomery, S. R. Lentz, G. F. Johnson, and X. L. Zheng. 2009. Leukocyte proteases cleave von Willebrand factor at or near the ADAMTS13 cleavage site. Blood 114: 1666-1674.
27. Rao, N. V., N. G. Wehner, B. C. Marshall, W. R. Gray, B. H. Gray, and J. R. Hoidal. 1991. Characterization of proteinase-3 (PR-3), a neutrophil serine proteinase: structural and functional properties. J. Biol. Chem. 266: 9540-9548. (Pubitemid 21906690)
28. Ying, Q. L., and S. R. Simon. 2002. Elastolysis by proteinase 3 and its inhibition by alpha(1)-proteinase inhibitor: a mechanism for the incomplete inhibition of ongoing elastolysis. Am. J. Respir. Cell Mol. Biol. 26: 356-361.
29. Ranes, J., and J. K. Stoller. 2005. A review of alpha-1 antitrypsin deficiency. Semin. Respir. Crit. Care Med. 26: 154-166. (Pubitemid 40617294)
30. Yan, H. C., J. M. Pilewski, Q. Zhang, H. M. DeLisser, L. Romer, and S. M. Albelda. 1995. Localization of multiple functional domains on human PECAM-1 (CD31) by monoclonal antibody epitope mapping. Cell Adhes. Commun. 3: 45-66.
31. Korkmaz, B., S. Attucci, M. A. Juliano, T. Kalupov, M. L. Jourdan, L. Juliano, and F. Gauthier. 2008. Measuring elastase, proteinase 3 and cathepsin G activities at the surface of human neutrophils with fluorescence resonance energy transfer substrates. Nat. Protoc. 3: 991-1000. (Pubitemid 351818687)
32. Korkmaz, B., S. Attucci, T. Moreau, E. Godat, L. Juliano, and F. Gauthier. 2004. Design and use of highly specific substrates of neutrophil elastase and proteinase 3. Am. J. Respir. Cell Mol. Biol. 30: 801-807. (Pubitemid 38736903)
33. Kuckleburg, C. J., C. M. Yates, N. Kalia, Y. Zhao, G. B. Nash, S. P. Watson, and G. E. Rainger. 2011. Endothelial cell-borne platelet bridges selectively recruit monocytes in human and mouse models of vascular inflammation. Cardiovasc. Res. 91: 134-141.
34. Vaporciyan, A. A., H. M. DeLisser, H. C. Yan, I. I. Mendiguren, S. R. Thom, M. L. Jones, P. A. Ward, and S. M. Albelda. 1993. Involvement of platelet-endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 262: 1580-1582. (Pubitemid 24036117)
35. Tonnesen, M. G., D. C. Anderson, T. A. Springer, A. Knedler, N. Avdi, and P. M. Henson. 1989. Adherence of neutrophils to cultured human microvascular endothelial cells: stimulation by chemotactic peptides and lipid mediators and dependence upon the Mac-1, LFA-1, p150,95 glycoprotein family. J. Clin. Invest. 83: 637-646. (Pubitemid 19061188)
36. Lawrence, M. B., and T. A. Springer. 1991. Leukocytes roll on a selectin at physiologic flow rates: distinction from and prerequisite for adhesion through integrins. Cell 65: 859-873. (Pubitemid 121001317)
37. Korkmaz, B., A. Kuhl, B. Bayat, S. Santoso, and D. E. Jenne. 2008. A hydrophobic patch on proteinase 3, the target of autoantibodies in Wegener granulomatosis, mediates membrane binding via NB1 receptors. J. Biol. Chem. 283: 35976-35982.
38. Carden, D., F. Xiao, C. Moak, B. H. Willis, S. Robinson-Jackson, and S. Alexander. 1998. Neutrophil elastase promotes lung microvascular injury and proteolysis of endothelial cadherins. Am. J. Physiol. 275: H385-H392. (Pubitemid 128734405)
39. Carden, D. L., and R. J. Korthuis. 1996. Protease inhibition attenuates microvascular dysfunction in postischemic skeletal muscle. Am. J. Physiol. 271: H1947-H1952.
40. Cepinskas, G., R. Noseworthy, and P. R. Kvietys. 1997. Transendothelial neutrophil migration: role of neutrophil-derived proteases and relationship to transendothelial protein movement. Circ. Res. 81: 618-626. (Pubitemid 27432750)
41. Korthuis, R. J., D. L. Carden, P. R. Kvietys, D. Shepro, and J. Fuseler. 1991. Phalloidin attenuates postischemic neutrophil infiltration and increased microvascular permeability. J. Appl. Physiol. 71: 1261-1269.
42. Kvietys, P. R., and D. N. Granger. 1997. Endothelial cell monolayers as a tool for studying microvascular pathophysiology. Am. J. Physiol. 273: G1189-G1199.
43. Lewis, R. E., and H. J. Granger. 1988. Diapedesis and the permeability of venous microvessels to protein macromolecules: the impact of leukotriene B4 (LTB4). Microvasc. Res. 35: 27-47. (Pubitemid 18036804)
44. Weiss, S. J. 1989. Tissue destruction by neutrophils. N. Engl. J. Med. 320: 365-376. (Pubitemid 19106873)
45. Woodman, R. C., P. H. Reinhardt, S. Kanwar, F. L. Johnston, and P. Kubes. 1993. Effects of human neutrophil elastase (HNE) on neutrophil function in vitro and in inflamed microvessels. Blood 82: 2188-2195. (Pubitemid 23294005)
46. Zimmerman, B. J., and D. N. Granger. 1990. Reperfusion-induced leukocyte infiltration: role of elastase. Am. J. Physiol. 259: H390-H394. (Pubitemid 20259412)
47. Young, R. E., M. B. Voisin, S. Wang, J. Dangerfield, and S. Nourshargh. 2007. Role of neutrophil elastase in LTB4-induced neutrophil transmigration in vivo assessed with a specific inhibitor and neutrophil elastase deficient mice. Br. J. Pharmacol. 151: 628-637. (Pubitemid 47016294)
48. Young, R. E., R. D. Thompson, K. Y. Larbi, M. La, C. E. Roberts, S. D. Shapiro, M. Perretti, and S. Nourshargh. 2004. Neutrophil elastase (NE)-deficient mice demonstrate a nonredundant role for NE in neutrophil migration, generation of proinflammatory mediators, and phagocytosis in response to zymosan particles in vivo. J. Immunol. 172: 4493-4502. (Pubitemid 38375266)
49. Cepinskas, G., M. Sandig, and P. R. Kvietys. 1999. PAF-induced elastase-dependent neutrophil transendothelial migration is associated with the mobilization of elastase to the neutrophil surface and localization to the migrating front. J. Cell Sci. 112: 1937-1945. (Pubitemid 29338818)
50. Cepinskas, G., R. Noseworthy, and P. R. Kvietys. 1997. Transendothelial neutrophil migration: role of neutrophil-derived proteases and relationship to transendothelial protein movement. Circ. Res. 81: 618-626. (Pubitemid 27432750)
51. Wang, S., M. B. Voisin, K. Y. Larbi, J. Dangerfield, C. Scheiermann, M. Tran, P. H. Maxwell, L. Sorokin, and S. Nourshargh. 2006. Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J. Exp. Med. 203: 1519-1532. (Pubitemid 43877612)
52. Allport, J. R., W. A. Muller, and F. W. Luscinskas. 2000. Monocytes induce reversible focal changes in vascular endothelial cadherin complex during transendothelial migration under flow. J. Cell Biol. 148: 203-216. (Pubitemid 30046793)
53. Kessenbrock, K., L. Fröhlich, M. Sixt, T. Lämmermann, H. Pfister, A. Bateman, A. Belaaouaj, J. Ring, M. Ollert, R. Fässler, and D. E. Jenne. 2008. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J. Clin. Invest. 118: 2438-2447. (Pubitemid 351949772)
54. Zen, K., Y. L. Guo, L. M. Li, Z. Bian, C. Y. Zhang, and Y. Liu. 2011. Cleavage of the CD11b extracellular domain by the leukocyte serprocidins is critical for neutrophil detachment during chemotaxis. Blood 117: 4885-4894.
55. Steppich, B. A., I. Seitz, G. Busch, A. Stein, and I. Ott. 2008. Modulation of tissue factor and tissue factor pathway inhibitor-1 by neutrophil proteases. Thromb. Haemost. 100: 1068-1075.