DNA-bound elastase of neutrophil extracellular traps degrades plasminogen, reduces plasmin formation, and decreases fibrinolysis: proof of concept in septic shock plasma.
disseminated intravascular coagulation
elastase inhibitors
fibrinolytic failure
multiorgan dysfunction
neutrophil proteases
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
pubmed:
5
11
2019
medline:
9
6
2020
entrez:
5
11
2019
Statut:
ppublish
Résumé
Activation of platelets and neutrophils in septic shock results in the formation of microvascular clots containing an intricate scaffold of fibrin with neutrophil extracellular traps (NETs) DNA. NETs contain multiple components that might impact endogenous fibrinolysis, resulting in failure to lyse clots in the microcirculation and residual systemic microthrombosis. We propose herein that the reservoir of human neutrophil elastase (HNE) on NETs may directly interfere with the fibrinolytic mechanism
Identifiants
pubmed: 31682515
doi: 10.1096/fj.201901363RRR
doi:
Substances chimiques
Plasminogen
9001-91-6
Pancreatic Elastase
EC 3.4.21.36
Fibrinolysin
EC 3.4.21.7
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14270-14280Références
Longstaff, C., and Kolev, K. (2015) Basic mechanisms and regulation of fibrinolysis. J. Thromb. Haemost. 13 (Suppl 1), S98-S105
Xue, Y., Bodin, C., and Olsson, K. (2012) Crystal structure of the native plasminogen reveals an activation-resistant compact conformation. J. Thromb. Haemost. 10, 1385-1396
Fleury, V., and Anglés-Cano, E. (1991) Characterization of the binding of plasminogen to fibrin surfaces: the role of carboxyterminal lysines. Biochemistry 30, 7630-7638
Scapini, P., Nesi, L., Morini, M., Tanghetti, E., Belleri, M., Noonan, D., Presta, M., Albini, A., and Cassatella, M. A. (2002) Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils. J. Immunol. 168, 5798-5804
Moroz, L. A. (1981) Mini-plasminogen: a mechanism for leukocyte modulation of plasminogen activation by urokinase. Blood 58, 97-104
Beatty, K., Bieth, J., and Travis, J. (1980) Kinetics of association of serine proteinases with native and oxidized alpha-1-proteinase inhibitor and alpha-1-antichymotrypsin. J. Biol. Chem. 255, 3931-3934
Korkmaz, B., Attucci, S., Jourdan, M. L., Juliano, L., and Gauthier, F. (2005) Inhibition of neutrophil elastase by alpha1-protease inhibitor at the surface of human polymorphonuclear neutrophils. J. Immunol. 175, 3329-3338
Owen, C. A., Campbell, M. A., Sannes, P. L., Boukedes, S. S., and Campbell, E. J. (1995) Cell surface-bound elastase and cathepsin G on human neutrophils: a novel, non-oxidative mechanism by which neutrophils focus and preserve catalytic activity of serine proteinases. J. Cell Biol. 131, 775-789
Belorgey, D., and Bieth, J. G. (1998) Effect of polynucleotides on the inhibition of neutrophil elastase by mucus proteinase inhibitor and alpha 1-proteinase inhibitor. Biochemistry 37, 16416-16422
Belorgey, D., and Bieth, J. G. (1995) DNA binds neutrophil elastase and mucus proteinase inhibitor and impairs their functional activity. FEBS Lett. 361, 265-268
Duranton, J., Belorgey, D., Carrère, J., Donato, L., Moritz, T., and Bieth, J. G. (2000) Effect of DNase on the activity of neutrophil elastase, cathepsin G and proteinase 3 in the presence of DNA. FEBS Lett. 473, 154-156
Duranton, J., Boudier, C., Belorgey, D., Mellet, P., and Bieth, J. G. (2000) DNA strongly impairs the inhibition of cathepsin G by alpha(1)-antichymotrypsin and alpha(1)-proteinase inhibitor. J. Biol. Chem. 275, 3787-3792
Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., and Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535
Kenny, E. F., Herzig, A., Krüger, R., Muth, A., Mondal, S., Thompson, P. R., Brinkmann, V., Bernuth, H.V., and Zychlinsky, A. (2017) Diverse stimuli engage different neutrophil extracellular trap pathways. Elife 6, e24437
Fuchs, T.A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V., and Zychlinsky, A. (2007) Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241
Urban, C.F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., Brinkmann, V., Jungblut, P. R., and Zychlinsky, A. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5, e1000639
Thomas, M. P., Whangbo, J., McCrossan, G., Deutsch, A. J., Martinod, K., Walch, M., and Lieberman, J. (2014) Leukocyte protease binding to nucleic acids promotes nuclear localization and cleavage of nucleic acid binding proteins. J. Immunol. 192, 5390-5397
Brinkmann, V., and Zychlinsky, A. (2007) Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 5, 577-582
Kessenbrock, K., Krumbholz, M., Schönermarck, U., Back, W., Gross, W. L., Werb, Z., Gröne, H. J., Brinkmann, V., and Jenne, D. E. (2009) Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15, 623-625
Engelmann, B., and Massberg, S. (2013) Thrombosis as an intravascular effector of innate immunity. Nat. Rev. Immunol. 13, 34-45
Fuchs, T. A., Brill, A., Duerschmied, D., Schatzberg, D., Monestier, M., Myers, D. D., Jr., Wrobleski, S. K., Wakefield, T. W., Hartwig, J. H., and Wagner, D. D. (2010) Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. USA 107, 15880-15885
Grässle, S., Huck, V., Pappelbaum, K. I., Gorzelanny, C., Aponte-Santamaría, C., Baldauf, C., Gräter, F., Schneppenheim, R., Obser, T., and Schneider, S. W. (2014) von Willebrand factor directly interacts with DNA from neutrophil extracellular traps. Arterioscler. Thromb. Vasc. Biol. 34, 1382-1389
De Boer, O. J., Li, X., Teeling, P., Mackaay, C., Ploegmakers, H. J., van der Loos, C. M., Daemen, M. J., de Winter, R. J., and van der Wal, A. C. (2013) Neutrophils, neutrophil extracellular traps and interleukin-17 associate with the organisation of thrombi in acute myocardial infarction. Thromb. Haemost. 109, 290-297
Riegger, J., Byrne, R. A., Joner, M., Chandraratne, S., Gershlick, A. H., Ten Berg, J. M., Adriaenssens, T., Guagliumi, G., Godschalk, T. C., Neumann, F. J., Trenk, D., Feldman, L. J., Steg, P. G., Desmet, W., Alfonso, F., Goodall, A. H., Wojdyla, R., Dudek, D., Philippi, V., Opinaldo, S., Titova, A., Malik, N., Cotton, J., Jhagroe, D. A., Heestermans, A. A., Sinnaeve, P., Vermeersch, P., Valina, C., Schulz, C., Kastrati, A., and Massberg, S.; Prevention of Late Stent Thrombosis by an Interdisciplinary Global European Effort (PRESTIGE) Investigators. (2016) Histopathological evaluation of thrombus in patients presenting with stent thrombosis. A multicenter European study: a report of the prevention of late stent thrombosis by an interdisciplinary global European effort consortium. Eur. Heart J. 37, 1538-1549
Laridan, E., Denorme, F., Desender, L., François, O., Andersson, T., Deckmyn, H., Vanhoorelbeke, K., and De Meyer, S. F. (2017) Neutrophil extracellular traps in ischemic stroke thrombi. Ann. Neurol. 82, 223-232
Longstaff, C., Variú, I., Sótonyi, P., Szabó, L., Krumrey, M., Hoell, A., Bóta, A., Varga, Z., Komorowicz, E., and Kolev, K. (2013) Mechanical stability and fibrinolytic resistance of clots containing fibrin, DNA, and histones. J. Biol. Chem. 288, 6946-6956
Gould, T. J., Vu, T.T., Stafford, A.R., Dwivedi, D. J., Kim, P.Y., Fox-Robichaud, A. E., Weitz, J. I., and Liaw, P. C. (2015) Cell-free DNA modulates clot structure and impairs fibrinolysis in sepsis. Arterioscler. Thromb. Vasc. Biol. 35, 2544-2553
Varjú, I., Longstaff, C., Szabó, L., Farkas, A. Z., Varga-Szabó, V. J., Tanka-Salamon, A., Machovich, R., and Kolev, K. (2015) DNA, histones and neutrophil extracellular traps exert anti-fibrinolytic effects in a plasma environment. Thromb. Haemost. 113, 1289-1298
Fuchs, T. A., Brill, A., and Wagner, D. D. (2012) Neutrophil extracellular trap (NET) impact on deep vein thrombosis. Arterioscler. Thromb. Vasc. Biol. 32, 1777-1783
Singer, M. (2016) The new sepsis consensus definitions (Sepsis-3) : the good, the not-so-bad, and the actually-quite-pretty. Intensive Care Med. 42, 2027-2029
Iba, T., Di Nisio, M., Thachil, J., Wada, H., Asakura, H., Sato, K., Kitamura, N., and Saitoh, D. (2016) Revision of the Japanese Association for Acute Medicine (JAAM) disseminated intravascular coagulation (DIC) diagnostic criteria using antithrombin activity. Crit. Care 20, 287
Holvoet, P., Lijnen, H. R., and Collen, D. (1985) A monoclonal antibody specific for Lys-plasminogen. Application to the study of the activation pathways of plasminogen in vivo. J. Biol. Chem. 260, 12106-12111
Grailhe, P., Nieuwenhuizen, W., and Anglés-Cano, E. (1994) Study of tissue-type plasminogen activator binding sites on fibrin using distinct fragments of fibrinogen. Eur. J. Biochem. 219, 961-967
Fleury, V., Loyau, S., Lijnen, H. R., Nieuwenhuizen, W., and Anglés-Cano, E. (1993) Molecular assembly of plasminogen and tissue-type plasminogen activator on an evolving fibrin surface. Eur. J. Biochem. 216, 549-556
Montes, R., Páramo, J. A., Anglès-Cano, E., and Rocha, E. (1996) Development and clinical application of a new ELISA assay to determine plasmin-alpha2-antiplasmin complexes in plasma. Br. J. Haematol. 92, 979-985
Grenier, A., Dehoux, M., Boutten, A., Arce-Vicioso, M., Durand, G., Gougerot-Pocidalo, M. A., and Chollet-Martin, S. (1999) Oncostatin M production and regulation by human polymorphonuclear neutrophils. Blood 93, 1413-1421
Angles-Cano, E., and Sultan, Y. (1984) A solid-phase fibrin immunoassay for the specific detection of monoclonal antibodies against different epitopic determinants of tissue-plasminogen activators. J. Immunol. Methods 69, 115-127
Dominguez, M., Montes, R., Páramo, J. A., and Anglés-Cano, E. (2002) Bivalency of plasminogen monoclonal antibodies is required for plasminogen bridging to fibrin and enhanced plasmin formation. Biochim. Biophys. Acta 1598, 165-176
Koppert, P. W., Huijsmans, C. M., and Nieuwenhuizen, W. (1985) A monoclonal antibody, specific for human fibrinogen, fibrinopeptide A-containing fragments and not reacting with free fibrinopeptide A. Blood 66, 503-507
Rylatt, D.B., Blake, A.S., Cottis, L.E., Massingham, D.A., Fletcher, W.A., Masci, P.P., Whitaker, A.N., Elms, M., Bunce, I., and Webber, A. J., et al. (1983) An immunoassay for human D dimer using monoclonal antibodies. Thromb. Res. 31, 767-778
Bangert, K., and Thorsen, S. (2000) Assay of functional plasminogen in rat plasma applicable to experimental studies of thrombolysis. Thromb. Haemost. 84, 299-306
Pouit, L., Hudry-Clergeon, G., and Suscillon, M. (1973) Electron microscopy study of positive charges on fibrin fibres. Biochim. Biophys. Acta 317, 99-105
Campbell, E. J., and Owen, C. A. (2007) The sulfate groups of chondroitin sulfate- and heparan sulfate-containing proteoglycans in neutrophil plasma membranes are novel binding sites for human leukocyte elastase and cathepsin G. J. Biol. Chem. 282, 14645-14654
Warejcka, D. J., and Twining, S. S. (2005) Specific conformational changes of plasminogen induced by chloride ions, 6-aminohexanoic acid and benzamidine, but not the overall openness of plasminogen regulate, production of biologically active angiostatins. Biochem. J. 392, 703-712
Massberg, S., Grahl, L., von Bruehl, M. L., Manukyan, D., Pfeiler, S., Goosmann, C., Brinkmann, V., Lorenz, M., Bidzhekov, K., Khandagale, A.B., Konrad, I., Kennerknecht, E., Reges, K., Holdenrieder, S., Braun, S., Reinhardt, C., Spannagl, M., Preissner, K. T., and Engelmann, B. (2010) Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat. Med. 16, 887-896
Clark, S. R., Ma, A. C., Tavener, S. A., McDonald, B., Goodarzi, Z., Kelly, M. M., Patel, K. D., Chakrabarti, S., McAvoy, E., Sinclair, G. D., Keys, E.M., Allen-Vercoe, E., Devinney, R., Doig, C. J., Green, F.H., and Kubes, P. (2007) Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13, 463-469
McDonald, B., Davis, R.P., Kim, S. J., Tse, M., Esmon, C.T., Kolaczkowska, E., and Jenne, C. N. (2017) Platelets and neutrophil extracellular traps collaborate to promote intravascular coagulation during sepsis in mice. Blood 129, 1357-1367
Delabranche, X., Stiel, L., Severac, F., Galoisy, A. C., Mauvieux, L., Zobairi, F., Lavigne, T., Toti, F., Anglès-Cano, E., Meziani, F., and Boisramé-Helms, J. (2017) Evidence of netosis in septic shock-induced disseminated intravascular coagulation. Shock 47, 313-317
Maruchi, Y., Tsuda, M., Mori, H., Takenaka, N., Gocho, T., Huq, M. A., and Takeyama, N. (2018) Plasma myeloperoxidase-conjugated DNA level predicts outcomes and organ dysfunction in patients with septic shock. Crit. Care 22, 176
Li, X., and Ma, X. (2018) A brief comment on the predictive value of myeloperoxidase-conjugated DNA level in patients with septic shock. Crit. Care 22, 294
Kumar, S., Gupta, E., Kaushik, S., Srivastava, V. K., Saxena, J., Mehta, S., and Jyoti, A. (2019) Quantification of NETs formation in neutrophil and its correlation with the severity of sepsis and organ dysfunction. Clin. Chim. Acta 495, 606-610
Abrams, S.T., Morton, B., Alhamdi, Y., Alsabani, M., Lane, S., Welters, I. D., Wang, G., and Toh, C. H. (2019) A novel assay for neutrophil extracellular traps (NETs) formation independently predicts disseminated intravascular coagulation and mortality in critically ill patients. [E-pub ahead of print] Am. J. Respir. Crit. Care Med.
Noubouossie, D.F., Reeves, B.N., Strahl, B.D., and Key, N. S. (2019) Neutrophils: back in the thrombosis spotlight. Blood 133, 2186-2197
Ducroux, C., Di Meglio, L., Loyau, S., Delbosc, S., Boisseau, W., Deschildre, C., Ben Maacha, M., Blanc, R., Redjem, H., Ciccio, G., Smajda, S., Fahed, R., Michel, J. B., Piotin, M., Salomon, L., Mazighi, M., Ho-Tin-Noe, B., and Desilles, J. P. (2018) Thrombus neutrophil extracellular traps content impair tPA-induced thrombolysis in acute ischemic stroke. Stroke 49, 754-757
Kolaczkowska, E., Jenne, C. N., Surewaard, B. G., Thanabalasuriar, A., Lee, W. Y., Sanz, M. J., Mowen, K., Opdenakker, G., and Kubes, P. (2015) Molecular mechanisms of NET formation and degradation revealed by intravital imaging in the liver vasculature. Nat. Commun. 6, 6673
Rouy, D., Koschinsky, M. L., Fleury, V., Chapman, J., and Anglés-Cano, E. (1992) Apolipoprotein(a) and plasminogen interactions with fibrin: a study with recombinant apolipoprotein(a) and isolated plasminogen fragments. Biochemistry 31, 6333-6339
Lamanuzzi, L. B., Mtairag, M., Pepe, G., and Anglés-Cano, E. (2004) Neutrophils stimulated by apolipoprotein(a) generate fragments that are stronger inhibitors of plasmin formation than apo(a). Thromb. Haemost. 92, 1066-1075
Thorsen, S., Clemmensen, I., Sottrup-Jensen, L., and Magnusson, S. (1981) Adsorption to fibrin of native fragments of known primary structure from human plasminogen. Biochim. Biophys. Acta 668, 377-387
Plow, E. F., and Edgington, T. S. (1975) An alternative pathway for fibrinolysis. I. The cleavage of fibrinogen by leukocyte proteases at physiologic pH. J. Clin. Invest. 56, 30-38
Machovich, R., and Owen, W. G. (1989) An elastase-dependent pathway of plasminogen activation. Biochemistry 28, 4517-4522
Wu, K., Urano, T., Ihara, H., Takada, Y., Fujie, M., Shikimori, M., Hashimoto, K., and Takada, A. (1995) The cleavage and inactivation of plasminogen activator inhibitor type 1 by neutrophil elastase: the evaluation of its physiologic relevance in fibrinolysis. Blood 86, 1056-1061
Duboscq, C., Genoud, V., Parborell, M. F., and Kordich, L. C. (1997) Impaired clot lysis by rt-PA catalyzed mini-plasminogen activation. Thromb. Res. 86, 505-513
Suenson, E., Lützen, O., and Thorsen, S. (1984) Initial plasmin-degradation of fibrin as the basis of a positive feed-back mechanism in fibrinolysis. Eur. J. Biochem. 140, 513-522
Herren, T., Burke, T. A., Das, R., and Plow, E. F. (2006) Identification of histone H2B as a regulated plasminogen receptor. Biochemistry 45, 9463-9474
Duboscq, C., Quintana, I., Bassilotta, E., Bergonzelli, G. E., Porterie, P., Sassetti, B., Haedo, A. S., Wainsztein, N., Kruithof, E. K., and Kordich, L. (1997) Plasminogen: an important hemostatic parameter in septic patients. Thromb. Haemost. 77, 1090-1095