NSP4 is stored in azurophil granules and released by activated neutrophils as active endoprotease with restricted specificity

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2700-2707

  Perera, Natascha C ^a   Wiesmüller, Karl Heinz ^b   Larsen, Maria Torp ^c   Schacher, Beate ^d   Eickholz, Peter ^d   Borregaard, Niels ^c   Jenne, Dieter E ^a,e  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b EMC MICROCOLLECTIONS GMBH   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d GOETHE UNIVERSITY   (Germany)

^e MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIPEPTIDYL PEPTIDASE I; MESSENGER RNA; NEUTROPHIL SERINE PROTEASE 4; RECOMBINANT PROTEIN; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

AMINO ACID ANALYSIS; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; COVALENT BOND; ENZYME SPECIFICITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKOCYTE ACTIVATION; MYELOBLAST; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN PROCESSING; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ADOLESCENT; AMINO ACID SEQUENCE; BLOTTING, WESTERN; CATHEPSIN C; CYTOPLASMIC GRANULES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HAPTOGLOBINS; HUMANS; MALE; MOLECULAR SEQUENCE DATA; MUTATION; NEUTROPHIL ACTIVATION; NEUTROPHILS; PAPILLON-LEFEVRE DISEASE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERINE ENDOPEPTIDASES;

EID: 84883325868     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301293     Document Type: Article

References (32)

1. Perera, N. C., O. Schilling, H. Kittel, W. Back, E. Kremmer, and D. E. Jenne. 2012. NSP4, an elastase-related protease in human neutrophils with arginine specificity. Proc. Natl. Acad. Sci. USA 109: 6229-6234.
2. Schechter, I., and A. Berger. 1967. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27: 157-162.
3. Tang, T., L. Li, J. Tang, Y. Li, W. Y. Lin, F. Martin, D. Grant, M. Solloway, L. Parker, W. L. Ye, et al. 2010. A mouse knockout library for secreted and transmembrane proteins. Nat. Biotechnol. 28: 749-755.
4. Nathan, C. 2006. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6: 173-182.
5. Segal, A.W. 2005. How neutrophils kill microbes. Annu. Rev. Immunol. 23: 197-223.
6. Klebanoff, S. J. 2005. Myeloperoxidase: friend and foe. J. Leukoc. Biol. 77: 598-625.
7. Pham, C. T. N. 2008. Neutrophil serine proteases fine-tune the inflammatory response. Int. J. Biochem. Cell Biol. 40: 1317-1333.
8. Borregaard, N., M. Sehested, B. S. Nielsen, H. Sengeløv, and L. Kjeldsen. 1995. Biosynthesis of granule proteins in normal human bone marrow cells. Gelatinase is a marker of terminal neutrophil differentiation. Blood 85: 812-817.
9. Theilgaard-Mönch, K., L. C. Jacobsen, R. Borup, T. Rasmussen, M. D. Bjerregaard, F. C. Nielsen, J. B. Cowland, and N. Borregaard. 2005. The transcriptional program of terminal granulocytic differentiation. Blood 105: 1785-1796.
10. Borregaard, N., J. M. Heiple, E. R. Simons, and R. A. Clark. 1983. Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation. J. Cell Biol. 97: 52-61.
11. Rørvig, S., C. Honore, L.-I. Larsson, S. Ohlsson, C. C. Pedersen, L. C. Jacobsen, J. B. Cowland, P. Garred, and N. Borregaard. 2009. Ficolin-1 is present in a highly mobilizable subset of human neutrophil granules and associates with the cell surface after stimulation with fMLP. J. Leukoc. Biol. 86: 1439-1449.
12. Kjeldsen, L., H. Sengeløv, and N. Borregaard. 1999. Subcellular fractionation of human neutrophils on Percoll density gradients. J. Immunol. Methods 232: 131-143.
13. Udby, L., and N. Borregaard. 2007. Subcellular fractionation of human neutrophils and analysis of subcellular markers. Methods Mol. Biol. 412: 35-56.
14. Noack, B., H. Görgens, B. Schacher, M. Puklo, P. Eickholz, T. Hoffmann, and H. K. Schackert. 2008. Functional Cathepsin C mutations cause different Papillon-Lefèvre syndrome phenotypes. J. Clin. Periodontol. 35: 311-316.
15. Le Cabec, V., J. B. Cowland, J. Calafat, and N. Borregaard. 1996. Targeting of proteins to granule subsets is determined by timing and not by sorting: The specific granule protein NGAL is localized to azurophil granules when expressed in HL-60 cells. Proc. Natl. Acad. Sci. USA 93: 6454-6457.
16. Stavridi, E. S., K. O'Malley, C. M. Lukacs, W. T. Moore, J. D. Lambris, D. W. Christianson, H. Rubin, and B. S. Cooperman. 1996. Structural change in alpha-chymotrypsin induced by complexation with alpha 1-antichymotrypsin as seen by enhanced sensitivity to proteolysis. Biochemistry 35: 10608-10615.
17. Huntington, J. A., R. J. Read, and R. W. Carrell. 2000. Structure of a serpinprotease complex shows inhibition by deformation. Nature 407: 923-926.
18. Nie, J., and D. Pei. 2004. Rapid inactivation of alpha-1-proteinase inhibitor by neutrophil specific leukolysin/membrane-type matrix metalloproteinase 6. Exp. Cell Res. 296: 145-150.
19. Liu, Z., X. Zhou, S. D. Shapiro, J. M. Shipley, S. S. Twining, L. A. Diaz, R. M. Senior, and Z. Werb. 2000. The serpin alpha1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 102: 647-655.
20. Jochum, M., S. Lander, N. Heimburger, and H. Fritz. 1981. Effect of human granulocytic elastase on isolated human antithrombin III. Hoppe Seylers Z. Physiol. Chem. 362: 103-112.
21. Jordan, R. E., J. Kilpatrick, and R. M. Nelson. 1987. Heparin promotes the inactivation of antithrombin by neutrophil elastase. Science 237: 777-779.
22. Adkison, A. M., S. Z. Raptis, D. G. Kelley, and C. T. N. Pham. 2002. Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J. Clin. Invest. 109: 363-371.
23. Pham, C. T. N., J. L. Ivanovich, S. Z. Raptis, B. Zehnbauer, and T. J. Ley. 2004. Papillon-Lefèvre syndrome: correlating the molecular, cellular, and clinical consequences of cathepsin C/dipeptidyl peptidase I deficiency in humans. J. Immunol. 173: 7277-7281.
24. Theilgaard-Mönch, K., L. C. Jacobsen, M. J. Nielsen, T. Rasmussen, L. Udby, M. Gharib, P. D. Arkwright, A. F. Gombart, J. Calafat, S. K. Moestrup, et al. 2006. Haptoglobin is synthesized during granulocyte differentiation, stored in specific granules, and released by neutrophils in response to activation. Blood 108: 353-361.
25. Fouret, P., R. M. du Bois, J. F. Bernaudin, H. Takahashi, V. J. Ferrans, and R. G. Crystal. 1989. Expression of the neutrophil elastase gene during human bone marrow cell differentiation. J. Exp. Med. 169: 833-845.
26. du Bois, R. M., J. F. Bernaudin, P. Paakko, R. Hubbard, H. Takahashi, V. Ferrans, and R. G. Crystal. 1991. Human neutrophils express the alpha 1-antitrypsin gene and produce alpha 1-antitrypsin. Blood 77: 2724-2730.
27. Mason, D. Y., E. M. Cramer, J. M. Massé, R. Crystal, J. M. Bassot, and J. Breton-Gorius. 1991. Alpha 1-antitrypsin is present within the primary granules of human polymorphonuclear leukocytes. Am. J. Pathol. 139: 623-628.
28. Chaillan-Huntington, C. E., and P. A. Patston. 1998. Influence of the P5 residue on alpha1-proteinase inhibitor mechanism. J. Biol. Chem. 273: 4569-4573.
29. Scott, C. F., R. W. Carrell, C. B. Glaser, F. Kueppers, J. H. Lewis, and R. W. Colman. 1986. Alpha-1-antitrypsin-Pittsburgh. A potent inhibitor of human plasma factor XIa, kallikrein, and factor XIIf. J. Clin. Invest. 77: 631-634.
30. Wachtfogel, Y. T., R. Bischoff, R. Bauer, C. E. Hack, J. H. Nuijens, U. Kucich, S. Niewiarowski, L. H. Edmunds, Jr., and R. W. Colman. 1994. Alpha 1-antitrypsin Pittsburgh (Met358 - >Arg) inhibits the contact pathway of intrinsic coagulation and alters the release of human neutrophil elastase during simulated extracorporeal circulation. Thromb. Haemost. 72: 843-847.
31. Korkmaz, B., A. Lesner, S. Letast, Y. K. Mahdi, M.-L. Jourdan, S. Dallet-Choisy, S. Marchand-Adam, C. Kellenberger, M.-C. Viaud-Massuard, D. E. Jenne, and F. Gauthier. 2013. Neutrophil proteinase 3 and dipeptidyl peptidase I (cathepsin C) as pharmacological targets in granulomatosis with polyangiitis (Wegener granulomatosis). Semin. Immunopathol. 35: 411-421 (Epub ahead of print).
32. Guay, D., C. Beaulieu, and M. D. Percival. 2010. Therapeutic utility and medicinal chemistry of cathepsin C inhibitors. Curr. Top. Med. Chem. 10: 708-716.