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Elafin and Its Precursor Trappin-2 Still Inhibit Neutrophil Serine Proteinases when They Are Covalently Bound to Extracellular Matrix Proteins by Tissue Transglutaminase

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INSERM U618 Protéases et Vectorisation Pulmonaires and IFR 135 Imagerie Fonctionnelle, Université François Rabelais, 10 Bd Tonnellé, BP 3223, 37032 Tours Cedex, France, and UMR 6175 Physiologie de la Reproduction et des Comportements, INRA, 37380 Nouzilly, France
Cite this: Biochemistry 2005, 44, 47, 15610–15618
Publication Date (Web):November 5, 2005
https://doi.org/10.1021/bi051418i
Copyright © 2005 American Chemical Society

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    Abstract

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    Elafin and its precursor trappin-2 (also called pre-elafin) are potent protein inhibitors of neutrophil serine proteases such as leukocyte elastase and proteinase 3. Trappin-2 has unique conserved sequence motifs rich in Gln and Lys residues. These motifs are substrates for transglutaminases that may enable trappin-2 to be cross-linked to extracellular matrix proteins, thus anchoring the inhibitor at its site of action. We have used Western blotting and ELISA-based assays to demonstrate that both elafin and trappin-2 can be conjugated to various extracellular matrix proteins in vitro by a type 2 transglutaminase. Cross-linked elafin and trappin-2 still inhibited their target proteases. Surface plasmon resonance studies allowed the determination of the kinetic constants governing the interaction of fibronectin-bound elafin and trappin-2 with neutrophil elastase and proteinase 3. Both inhibitors were potent inhibitors when cross-linked to fibronectin by transglutamination, with equilibrium dissociation constants Ki for their interaction with target proteases of 0.3 nM (elastase−elafin), 20 nM (proteinase 3−elafin), 0.3 nM (elastase−trappin-2), and 12 nM (proteinase 3−trappin-2). The conjugated inhibitors reacted more slowly with their target enzymes than did the soluble inhibitors, perhaps due to their immobilization, with association rate constants of 2−7 × 105 M-1 s-1 for elastase and 1−4 × 104 M-1 s-1 for proteinase 3. We believe this is the first demonstration that transglutaminase-mediated cross-linking of serine protease inhibitors to proteins preserves their inhibitory capacities.

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     N.G. holds a doctoral fellowship from MENRT (Ministère de l'Education Nationale, de la Recherche et de la Technologie). This work was supported by the French cystic fibrosis association “Vaincre la Mucoviscidose”.

     Université François Rabelais.

    §

     INRA.

    *

     To whom correspondence should be addressed:  INSERM U 618, University François Rabelais, 10 Bd Tonnellé, 37032 Tours Cedex, France. Fax:  +33 247 366 046. Telephone: +33 2 4736 6177. E-mail: [email protected].

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    15. J. Muto, N. Fujimoto, K. Ono, T. Kobayashi, K.R. Chen, S. Suzuki, H. Wachi, S. Tajima. Deposition of elafin in the involved vascular wall of neutrophil‐mediated cutaneous vasculitis. Journal of the European Academy of Dermatology and Venereology 2016, 30 (9) , 1544-1549. https://doi.org/10.1111/jdv.13650
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    29. Anna G. Drannik, Kakon Nag, Xiao-Dan Yao, Bethany M. Henrick, Jean-Michel Sallenave, Kenneth L. Rosenthal, . Trappin-2/Elafin Modulate Innate Immune Responses of Human Endometrial Epithelial Cells to PolyI∶C. PLoS ONE 2012, 7 (4) , e35866. https://doi.org/10.1371/journal.pone.0035866
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    40. Jean-Michel Sallenave. Secretory Leukocyte Protease Inhibitor and Elafin/Trappin-2. American Journal of Respiratory Cell and Molecular Biology 2010, 42 (6) , 635-643. https://doi.org/10.1165/rcmb.2010-0095RT
    41. Paula Tejera, Zhaoxi Wang, Rihong Zhai, Li Su, Chau-Chyun Sheu, Deanne M. Taylor, Feng Chen, Michelle N. Gong, B. Taylor Thompson, David C. Christiani. Genetic Polymorphisms of Peptidase Inhibitor 3 ( Elafin ) Are Associated with Acute Respiratory Distress Syndrome. American Journal of Respiratory Cell and Molecular Biology 2009, 41 (6) , 696-704. https://doi.org/10.1165/rcmb.2008-0410OC
    42. L. Marischen, D. Wesch, J.‐M. Schröder, O. Wiedow, D. Kabelitz. Human γδ T Cells Produce the Protease Inhibitor and Antimicrobial Peptide Elafin. Scandinavian Journal of Immunology 2009, 70 (6) , 547-552. https://doi.org/10.1111/j.1365-3083.2009.02337.x
    43. Marie‐Louise Zani, Kévin Baranger, Nicolas Guyot, Sandrine Dallet‐Choisy, Thierry Moreau. Protease inhibitors derived from elafin and SLPI and engineered to have enhanced specificity towards neutrophil serine proteases. Protein Science 2009, 18 (3) , 579-594. https://doi.org/10.1002/pro.64
    44. Zhaoxi Wang, Feng Chen, Rihong Zhai, Lingsong Zhang, Li Su, Xihong Lin, Taylor Thompson, David C. Christiani, . Plasma Neutrophil Elastase and Elafin Imbalance Is Associated with Acute Respiratory Distress Syndrome (ARDS) Development. PLoS ONE 2009, 4 (2) , e4380. https://doi.org/10.1371/journal.pone.0004380
    45. Nicolas Guyot, Marcus W. Butler, Paul McNally, Sinead Weldon, Catherine M. Greene, Rodney L. Levine, Shane J. O'Neill, Clifford C. Taggart, Noel G. McElvaney. Elafin, an Elastase-specific Inhibitor, Is Cleaved by Its Cognate Enzyme Neutrophil Elastase in Sputum from Individuals with Cystic Fibrosis. Journal of Biological Chemistry 2008, 283 (47) , 32377-32385. https://doi.org/10.1074/jbc.M803707200
    46. Hin C. Lee, Mitomu Kioi, Jing Han, Raj K. Puri, Jesse L. Goodman. Anaplasma phagocytophilum-induced gene expression in both human neutrophils and HL-60 cells. Genomics 2008, 92 (3) , 144-151. https://doi.org/10.1016/j.ygeno.2008.05.005
    47. Zhaoxi Wang, Douglas Beach, Li Su, Rihong Zhai, David C. Christiani. A Genome-Wide Expression Analysis in Blood Identifies Pre-Elafin as a Biomarker in ARDS. American Journal of Respiratory Cell and Molecular Biology 2008, 38 (6) , 724-732. https://doi.org/10.1165/rcmb.2007-0354OC
    48. Kévin Baranger, Marie‐Louise Zani, Jacques Chandenier, Sandrine Dallet‐Choisy, Thierry Moreau. The antibacterial and antifungal properties of trappin‐2 (pre‐elafin) do not depend on its protease inhibitory function. The FEBS Journal 2008, 275 (9) , 2008-2020. https://doi.org/10.1111/j.1742-4658.2008.06355.x
    49. Ali Roghanian, Jean-Michel Sallenave. Neutrophil Elastase (NE) and NE Inhibitors: Canonical and Noncanonical Functions in Lung Chronic Inflammatory Diseases (Cystic Fibrosis and Chronic Obstructive Pulmonary Disease). Journal of Aerosol Medicine and Pulmonary Drug Delivery 2008, 21 (1) , 125-144. https://doi.org/10.1089/jamp.2007.0653
    50. Ali Roghanian, Jean-Michel Sallenave. Neutrophil Elastase (NE) and NE Inhibitors: Canonical and Noncanonical Functions in Lung Chronic Inflammatory Diseases (Cystic Fibrosis and Chronic Obstructive Pulmonary Disease). Journal of Aerosol Medicine 2008, Article ASAP.
    51. Thierry Moreau, Kévin Baranger, Sébastien Dadé, Sandrine Dallet-Choisy, Nicolas Guyot, Marie-Louise Zani. Multifaceted roles of human elafin and secretory leukocyte proteinase inhibitor (SLPI), two serine protease inhibitors of the chelonianin family. Biochimie 2008, 90 (2) , 284-295. https://doi.org/10.1016/j.biochi.2007.09.007
    52. Emer Kelly, Catherine M Greene, Noel G McElvaney. Targeting neutrophil elastase in cystic fibrosis. Expert Opinion on Therapeutic Targets 2008, 12 (2) , 145-157. https://doi.org/10.1517/14728222.12.2.145
    53. Jun Muto, Kei Kuroda, Hiroshi Wachi, Shigehisa Hirose, Shingo Tajima. Accumulation of Elafin in Actinic Elastosis of Sun-Damaged Skin: Elafin Binds to Elastin and Prevents Elastolytic Degradation. Journal of Investigative Dermatology 2007, 127 (6) , 1358-1366. https://doi.org/10.1038/sj.jid.5700647
    54. Rebecca L. Rich, David G. Myszka. Survey of the year 2005 commercial optical biosensor literature. Journal of Molecular Recognition 2006, 19 (6) , 478-534. https://doi.org/10.1002/jmr.808

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