Functional study of elafin cleaved by Pseudomonas aeruginosa metalloproteinases

Biological Chemistry

Volumn 391, Issue 6, 2010, Pages 705-716

  Guyot, Nicolas ^a   Bergsson, Gudmundur ^a   Butler, Marcus W ^a   Greene, Catherine M ^a   Weldon, Sinéad ^b   Kessler, Efrat ^c   Levine, Rodney L ^d   O'Neill, Shane J ^a   Taggart, Clifford C ^b   McElvaney, Noel G ^a  

^a BEAUMONT HOSPITAL   (Ireland)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c TEL AVIV UNIVERSITY   (Israel)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Antimicrobials; Antiproteases; Cleavage; Microbial; Proteases; Transglutaminase

Indexed keywords

AERUGINOLYSIN; ELAFIN; FIBRONECTIN; LEUKOCYTE ELASTASE; METALLOPROTEINASE; MYELOBLASTIN; PSEUDOLYSIN; STAPHYLOLYSIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL PROTEIN;

ANTIMICROBIAL ACTIVITY; ARTICLE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOMODULATION; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; WESTERN BLOTTING; ENZYMOLOGY; HUMAN; METABOLISM;

PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELAFIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FIBRONECTINS; HUMANS; MASS SPECTROMETRY; METALLOPROTEASES; PSEUDOMONAS AERUGINOSA;

EID: 77956627266     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.066     Document Type: Article

References (41)

1. Banda, M.J., Clark, E.J., and Werb, Z. (1980). Limited proteolysis by macrophage elastase inactivates human α-1-proteinase inhibitor. J. Exp. Med. 152, 1563-1570. (Pubitemid 11210337)
2. Baranger, K., Zani, M.L., Chandenier, J., Dallet-Choisy, S., and Moreau, T. (2008). The antibacterial and antifungal properties of trappin-2 (pre-elafin) do not depend on its protease inhibitory function. FEBS J. 275, 2008-2020. (Pubitemid 351569543)
3. Beatty, K., Bieth, J., and Travis, J. (1980). Kinetics of association of serine proteinases with native and oxidized α-1-proteinase inhibitor and α-1-antichymotrypsin. J. Biol. Chem. 255, 3931-3934.
4. Bellemare, A., Vernoux, N., Morisset, D., and Bourbonnais, Y. (2008). Human pre-elafin inhibits a Pseudomonas aeruginosasecreted peptidase and prevents its proliferation in complex media. Antimicrob. Agents Chemother. 52, 483-490. (Pubitemid 351170818)
5. Bingle, L., Tetley, T.D., and Bingle, C.D. (2001). Cytokine-mediated induction of the human elafin gene in pulmonary epithelial cells is regulated by nuclear factor-κB. Am. J. Respir. Cell Mol. Biol. 25, 84-91. (Pubitemid 32682709)
6. Boudier, C. and Bieth, J.G. (1994). Oxidized mucus proteinase inhibitor: a fairly potent neutrophil elastase inhibitor. Biochem. J. 303, 61-68. (Pubitemid 24302900)
7. Brown, A., Farmer, K., MacDonald, L., Kalsheker, N., Pritchard, D., Haslett, C., Lamb, J., and Sallenave, J.M. (2003). House dust mite Der p 1 downregulates defenses of the lung by inactivating elastase inhibitors. Am. J. Respir. Cell Mol. Biol. 29, 381-389. (Pubitemid 37093997)
8. Butler, M.W., Robertson, I., Greene, C.M., O'Neill, S.J., Taggart, C.C., and McElvaney, N.G. (2006). Elafin prevents lipopolysaccharide- induced AP-1 and NF-κB activation via an effect on the ubiquitin-proteasome pathway. J. Biol. Chem. 281, 34730-34735. (Pubitemid 46036512)
9. Döring, G., Goldstein, W., Röll, A., Schiøtz, P.O., Høiby, N., and Botzenhart, K. (1985). Role of Pseudomonas aeruginosa exoenzymes in lung infections of patients with cystic fibrosis. Infect. Immun. 49, 557-562.
10. Francart, C., Dauchez, M., Alix, A.J., and Lippens, G. (1997). Solution structure of R-elafin, a specific inhibitor of elastase. J. Mol. Biol. 268, 666-677. (Pubitemid 27208084)
11. Guyot, N., Zani, M.L., Berger, P., Dallet-Choisy, S., and Moreau, T. (2005a). Proteolytic susceptibility of the serine protease inhibitor trappin-2 (pre-elafin): evidence for tryptase-mediated generation of elafin. Biol. Chem. 386, 391-399. (Pubitemid 41447602)
12. Guyot, N., Zani, M.L., Maurel, M.C., Dallet-Choisy, S., and Moreau, T. (2005b). Elafin and its precursor trappin-2 still inhibit neutrophil serine proteinases when they are covalently bound to extracellular matrix proteins by tissue transglutaminase. Biochemistry 44, 15610-15618. (Pubitemid 41706146)
13. Guyot, N., Butler, M.W., McNally, P., Weldon, S., Greene, C.M., Levine, R.L., O'Neill, S.J., Taggart, C.C., and McElvaney, N.G. (2008). Elafin, an elastase specific inhibitor, is cleaved by its cognate enzyme neutrophil elastase in sputum from individuals with cystic fibrosis. J. Biol. Chem. 283, 32377-32385.
14. Henriksen, P.A., Hitt, M., Xing, Z., Wang, J., Haslett, C., Riemersma, R.A., Webb, D.J., Kotelevtsev, Y.V., and Sallenave, J.M. (2004). Adenoviral gene delivery of elafin and secretory leukocyte protease inhibitor attenuates NF-κB-dependent inflammatory responses of human endothelial cells and macrophages to atherogenic stimuli. J. Immunol. 172, 4535-4544. (Pubitemid 38375271)
15. Johnson, D.A., Carter-Hamm, B., and Dralle, W.M. (1982). Inactivation of human bronchial mucosal proteinase inhibitor by Pseudomonas aeruginosa elastase. Am. Rev. Respir. Dis. 126, 1070-1073. (Pubitemid 13202263)
16. Kantyka, T., Latendorf, T., Wiedow, O., Bartels, J., Glaser, R., Dubin, G., Schroder, J.M., Potempa, J., and Meyer-Hoffert, U. (2009). Elafin is specifically inactivated by RgpB from Porphyromonas gingivalis by distinct proteolytic cleavage. Biol. Chem. 390, 1313-1320.
17. Krowarsch, D., Cierpicki, T., Jelen, F., and Otlewski, J. (2003). Canonical protein inhibitors of serine proteases. Cell. Mol. Life Sci. 60, 2427-2444. (Pubitemid 37487262)
18. Laskowski, M., Jr., Qasim, M.A., and Lu, S.M. (2000). Interaction of standard mechanism, canonical protein inhibitors with serine proteinases. In: Protein-Protein Recognition: The Frontiers in Molecular Biology Series, C. Kleanthouse, ed. (Oxford, UK: Oxford University Press), pp. 228-279.
19. Liu, X., Shu, S., Hong, M.S., Levine, R.L., and Korn, E.D. (2006). Phosphorylation of actin Tyr-53 inhibits filament nucleation and elongation and destabilizes filaments. Proc. Natl. Acad. Sci. USA 103, 13694-13699. (Pubitemid 44413969)
20. Mast, A.E., Enghild, J.J., Nagase, H., Suzuki, K., Pizzo, S.V., and Salvesen, G. (1991). Kinetics and physiologic relevance of the inactivation of α-1-proteinase inhibitor, α-1-antichymotrypsin, and antithrombin III by matrix metalloproteinases-1 (tissue collagenase), -2 (72-kDa gelatinase/type IV collagenase), and -3 (stromelysin). J. Biol. Chem. 266, 15810-15816. (Pubitemid 21907729)
21. Meyer-Hoffert, U., Wichmann, N., Schwichtenberg, L., White, P.C., and Wiedow, O. (2003). Supernatants of Pseudomonas aeruginosa induce the Pseudomonas-specific antibiotic elafin in human keratinocytes. Exp. Dermatol. 12, 418-425. (Pubitemid 36992416)
22. Michaelis, J., Vissers, M.C., and Winterbourn, C.C. (1990). Human neutrophil collagenase cleaves α-1-antitrypsin. Biochem. J. 270, 809-814.
23. Molhuizen, H.O., Alkemade, H.A., Zeeuwen, P.L., De Jongh, G.J., Wieringa, B., and Schalkwijk, J. (1993). SKALP/elafin: an elastase inhibitor from cultured human keratinocytes. Purification, cDNA sequence, and evidence for transglutaminase cross-linking. J. Biol. Chem. 268, 12028-12032. (Pubitemid 23168166)
24. Moreau, T., Baranger, K., Dade, S., Dallet-Choisy, S., Guyot, N., and Zani, M.L. (2008). Multifaceted roles of human elafin and secretory leukocyte proteinase inhibitor (SLPI), two serine protease inhibitors of the chelonianin family. Biochimie 90, 284-295. (Pubitemid 351172573)
25. Morihara, K., Tsuzuki, H., and Oda, K. (1979). Protease and elastase of Pseudomonas aeruginosa: inactivation of human plasma α- 1-proteinase inhibitor. Infect. Immun. 24, 188-193. (Pubitemid 9156281)
26. Muto, J., Kuroda, K., Wachi, H., Hirose, S., and Tajima, S. (2007). Accumulation of elafin in actinic elastosis of sun-damaged skin: elafin binds to elastin and prevents elastolytic degradation. J. Invest. Dermatol. 127, 1358-1366. (Pubitemid 46762965)
27. Nara, K., Ito, S., Ito, T., Suzuki, Y., Ghoneim, M.A., Tachibana, S., and Hirose, S. (1994). Elastase inhibitor elafin is a new type of proteinase inhibitor which has a transglutaminase-mediated anchoring sequence termed 'cementoin'. J. Biochem. 115, 441-448. (Pubitemid 24096454)
28. Nobar, S.M., Zani, M.L., Boudier, C., Moreau, T., and Bieth, J.G. (2005). Oxidized elafin and trappin poorly inhibit the elastolytic activity of neutrophil elastase and proteinase 3. FEBS J. 272, 5883-5893. (Pubitemid 41689360)
29. Pfundt, R., Wingens, M., Bergers, M., Zweers, M., Frenken, M., and Schalkwijk, J. (2000). TNF-a and serum induce SKALP/ elafin gene expression in human keratinocytes by a p38 MAP kinase-dependent pathway. Arch. Dermatol. Res. 292, 180-187. (Pubitemid 30237519)
30. Reid, P.T., Marsden, M.E., Cunningham, G.A., Haslett, C., and Sallenave, J.M. (1999). Human neutrophil elastase regulates the expression and secretion of elafin (elastase-specific inhibitor) in type II alveolar epithelial cells. FEBS Lett. 457, 33-37. (Pubitemid 29387404)
31. Sallenave, J.M. and Ryle, A.P. (1991). Purification and characterization of elastase-specific inhibitor. Sequence homology with mucus proteinase inhibitor. Biol. Chem. Hoppe-Seyler 372, 13-21.
32. Sallenave, J.M., Shulmann, J., Crossley, J., Jordana, M., and Gauldie, J. (1994). Regulation of secretory leukocyte proteinase inhibitor (SLPI) and elastase-specific inhibitor (ESI/elafin) in human airway epithelial cells by cytokines and neutrophilic enzymes. Am. J. Respir. Cell Mol. Biol. 11, 733-741.
33. Schalkwijk, J., Chang, A., Janssen, P., De Jongh, G.J., and Mier, P.D. (1990). Skin-derived antileucoproteases (SKALPs): characterization of two new elastase inhibitors from psoriatic epidermis. Br. J. Dermatol. 122, 631-641. (Pubitemid 20153661)
34. Schechter, I. and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
35. Simpson, A.J., Maxwell, A.I., Govan, J.R., Haslett, C., and Sallenave, J.M. (1999). Elafin (elastase-specific inhibitor) has antimicrobial activity against Gram-positive and Gram-negative respiratory pathogens. FEBS Lett. 452, 309-313. (Pubitemid 29301766)
36. Simpson, A.J., Cunningham, G.A., Porteous, D.J., Haslett, C., and Sallenave, J.M. (2001). Regulation of adenovirus-mediated elafin transgene expression by bacterial lipopolysaccharide. Hum. Gene Ther. 12, 1395-1406. (Pubitemid 32881345)
37. Taggart, C.C., Lowe, G.J., Greene, C.M., Mulgrew, A.T., O'Neill, S.J., Levine, R.L., and McElvaney, N.G. (2001). Cathepsin B, L, and S cleave and inactivate secretory leucoprotease inhibitor. J. Biol. Chem. 276, 33345-33352.
38. Tsunemi, M., Matsuura, Y., Sakakibara, S., and Katsube, Y. (1996). Crystal structure of an elastase-specific inhibitor elafin complexed with porcine pancreatic elastase determined at 1.9 Å resolution. Biochemistry 35, 11570-11576. (Pubitemid 26303673)
39. Wiedow, O., Schroder, J.M., Gregory, H., Young, J.A., and Christophers, E. (1990). Elafin: an elastase-specific inhibitor of human skin. Purification, characterization, and complete amino acid sequence. J. Biol. Chem. 265, 14791-14795.
40. Ying, Q.L. and Simon, S.R. (1993). Kinetics of the inhibition of human leukocyte elastase by elafin, a 6-kilodalton elastase-specific inhibitor from human skin. Biochemistry 32, 1866-1874. (Pubitemid 23066461)
41. Zani, M.L., Nobar, S.M., Lacour, S.A., Lemoine, S., Boudier, C., Bieth, J.G., and Moreau, T. (2004). Kinetics of the inhibition of neutrophil proteinases by recombinant elafin and pre-elafin (trappin-2) expressed in Pichia pastoris. Eur. J. Biochem. 271, 2370-2378. (Pubitemid 38813567)