Serine proteinase inhibitors; Drug development; Antithrombotic agents; Anti-inflammatory agents; Contact pathway; Factor XII
Abstract :
[en] Coagulation factor XII (FXII), a S1A serine protease, was discovered more than fifty years ago. However, its in vivo functions and its three-dimensional structure started to be disclosed in the last decade. FXII was found at the crosstalk of several physiological pathways including the intrinsic coagulation pathway, the kallikrein-kinin system, and the immune response. The FXII inhibition emerges as a therapeutic strategy for the safe prevention of artificial surface-induced thrombosis and in patients suffering from hereditary angioedema. The anti-FXII antibody garadacimab discovered by phage-display library technology is actually under phase II clinical evaluation for the prophylactic treatment of hereditary angioedema. The implication of FXII in neuro-inflammatory and neurodegenerative disorders is also an emerging research field. The FXII or FXIIa inhibitors currently under development include peptides, proteins, antibodies, RNA-based technologies, and, to a lesser extent, small-molecular weight inhibitors. Most of them are proteins, mainly isolated from hematophagous arthropods and plants. The discovery and development of these FXII inhibitors and their potential indications are discussed in the review.
Research center :
CIRM - Centre Interdisciplinaire de Recherche sur le Médicament - ULiège
Disciplines :
Chemistry Pharmacy, pharmacology & toxicology
Author, co-author :
Davoine, Clara ; Université de Liège - ULiège / Université de Namur - UNamur > Department of Pharmacy > Laboratory of Analysis of Medicines / Namur Medicine & Drug Innovation Center (NAMEDIC – NARILIS)
Bouckaert, Charlotte; Université de Namur - UNamur > Department of Pharmacy > Namur Medicine & Drug Innovation Center (NAMEDIC – NARILIS)
Fillet, Marianne ; Université de Liège - ULiège > Department of Pharmacy > Laboratory of Analysis of Medicines
Pochet, Lionel; Université de Namur - UNamur > Department of Pharmacy > Namur Medicine & Drug Innovation Center (NAMEDIC – NARILIS)
Language :
English
Title :
Factor XII/XIIa inhibitors: Their discovery, development, and potential indications
Alternative titles :
[fr] Inhibiteurs du facteur XII/XIIa: leur découverte, développement et indications potentielles
Schmaier, A.H., Stavrou, E.X., Factor XII - what's important but not commonly thought about. Res. Pract. Thromb. Haemost. 3 (2019), 599–606, 10.1002/rth2.12235.
Rawlings, N.D., Barrett, A.J., Thomas, P.D., Huang, X., Bateman, A., Finn, R.D., The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Res. 46 (2018), D624–D632, 10.1093/nar/gkx1134.
Weidmann, H., Heikaus, L., Long, A.T., Naudin, C., Schlüter, H., Renné, T., The plasma contact system, a protease cascade at the nexus of inflammation, coagulation and immunity. BBA - Mol. Cell Res. 1864 (2017), 2118–2127, 10.1016/j.bbamcr.2017.07.009.
Tillman, B., Gailani, D., Inhibition of factors XI and XII for prevention of thrombosis induced by artificial surfaces. Semin. Thromb. Hemost. 44 (2018), 60–69, 10.1055/s-0037-1603937.
Didiasova, M., Wujak, L., Schaefer, L., Wygrecka, M., Factor XII in coagulation, inflammation and beyond. Cell. Signal. 51 (2018), 257–265, 10.1016/j.cellsig.2018.08.006.
Stavrou, E., Schmaier, A.H., Factor XII: what does it contribute to our understanding of the physiology and pathophysiology of hemostasis & thrombosis. Thromb. Res. 125 (2010), 210–215, 10.1016/j.thromres.2009.11.028.
de Maat, S., Maas, C., Factor XII: form determines function. J. Thromb. Haemostasis 14 (2016), 1498–1506, 10.1111/jth.13383.
Salvesen, G.S., Catanese, J.J., Kress, L.F., Travis, J., Primary structure of the reactive site of human C1-inhibitor. J. Biol. Chem. 260 (1985), 2432–2436.
Stavrou, E.X., Fang, C., Bane, K.L., Long, A.T., Naudin, C., Kucukal, E., Gandhi, A., Brett-Morris, A., Mumaw, M.M., Izadmehr, S., Merkulova, A., Reynolds, C.C., Alhalabi, O., Nayak, L., Yu, W.M., Qu, C.K., Meyerson, H.J., Dubyak, G.R., Gurkan, U.A., Nieman, M.T., Sen Gupta, A., Renné, T., Schmaier, A.H., Factor XII and uPAR upregulate neutrophil functions to influence wound healing. J. Clin. Invest. 128 (2018), 944–959, 10.1172/JCI92880.
Zamolodchikov, D., Bai, Y., Tang, Y., McWhirter, J.R., Macdonald, L.E., Alessandri-Haber, N., A short isoform of coagulation factor XII mRNA is expressed by neurons in the human brain. Neuroscience 413 (2019), 294–307, 10.1016/j.neuroscience.2019.05.040.
Ziliotto, N., Bernardi, F., Jakimovski, D., Zivadinov, R., Coagulation pathways in neurological diseases: multiple sclerosis. Front. Neurol. 10 (2019), 1–21, 10.3389/fneur.2019.00409.
Woodruff, R.S., Sullenger, B., Becker, R.C., The many faces of the contact pathway and their role in thrombosis. J. Thromb. Thrombolysis 32 (2011), 9–20, 10.1007/s11239-011-0578-5.
Kenne, E., Renné, T., Factor XII: a drug target for safe interference with thrombosis and inflammation. Drug Discov. Today 19 (2014), 1459–1464, 10.1016/j.drudis.2014.06.024.
McMullen, B.A., Fujikawa, K., Amino acid sequence of the heavy chain of human α-factor XIIa (activated Hageman factor). J. Biol. Chem. 260 (1985), 5328–5341.
Shan, J., Baguinon, M., Zheng, L., Krishnamoorthi, R., Expression, refolding, and activation of the catalytic domain of human blood coagulation factor XII. Protein Expr. Purif 27 (2003), 143–149, 10.1016/S1046-5928(02)00608-3.
Pathak, M., Wilmann, P., Awford, J., Li, C., Hamad, B.K., Fischer, P.M., Dreveny, I., Dekker, L.V., Emsley, J., Coagulation factor XII protease domain crystal structure. J. Thromb. Haemostasis 13 (2015), 580–591, 10.1111/jth.12849.
Dementiev, A., Silva, A., Yee, C., Li, Z., Flavin, M.T., Sham, H., Partridge, J.R., Structures of human plasma β-factor XIIa cocrystallized with potent inhibitors. Blood Adv 2 (2018), 549–558, 10.1182/bloodadvances.2018016337.
Pathak, M., Manna, R., Li, C., Kaira, B.G., Hamad, B.K., Belviso, B.D., Bonturi, C.R., Dreveny, I., Fischer, P.M., Dekker, L.V., Oliva, M.L.V., Emsley, J., Crystal structures of the recombinant β-factor XIIa protease with bound Thr-Arg and Pro-Arg substrate mimetics. Acta Crystallogr. Sect. D Struct. Biol. 75 (2019), 578–591, 10.1107/S2059798319006910.
Beringer, D.X., Kroon-Batenburg, L.M.J., The structure of the FnI-EGF-like tandem domain of coagulation factor XII solved using SIRAS. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 69 (2013), 94–102, 10.1107/S1744309113000286.
Citarella, F., te Velthuis, H., Helmer-Citterich, M., Hack, C., Identification of a putative binding site for negatively charged surfaces in the fibronectin type II domain of human factor XII. Thromb. Haemostasis 84 (2000), 1057–1065, 10.1055/s-0037-1614171.
Hamad, B.K., Pathak, M., Manna, R., Fischer, P.M., Emsley, J., Dekker, L.V., Assessment of the protein interaction between coagulation factor XII and corn trypsin inhibitor by molecular docking and biochemical validation. J. Thromb. Haemostasis 15 (2017), 1818–1828, 10.1111/jth.13773.
Nickel, K.F., Long, A.T., Fuchs, T.A., Butler, L.M., Renné, T., Factor XII as a therapeutic target in thromboembolic and inflammatory diseases. Arterioscler. Thromb. Vasc. Biol. 37 (2017), 13–20, 10.1161/ATVBAHA.116.308595.
Göbel, K., Eichler, S., Wiendl, H., Chavakis, T., Kleinschnitz, C., Meuth, S.G., The coagulation factors fibrinogen, thrombin, and factor XII in inflammatory disorders-a systematic review. Front. Immunol., 9, 2018, 10.3389/fimmu.2018.01731.
Weitz, J.I., Fredenburgh, J.C., Factors XI and XII as targets for new anticoagulants. Front. Med. 4 (2017), 1–6, 10.3389/fmed.2017.00019.
DeLoughery, E.P., Olson, S.R., Puy, C., McCarty, O.J.T., Shatzel, J.J., The safety and efficacy of novel agents targeting factors XI and XII in early phase human trials. Semin. Thromb. Hemost. 45 (2019), 502–508, 10.1055/s-0039-1692439.
Farkas, H., Hereditary angioedema: examining the landscape of therapies and preclinical therapeutic targets. Expert Opin. Ther. Targets 23 (2019), 457–459, 10.1080/14728222.2019.1608949.
Philippou, H., Heavy chain of FXII: not an innocent bystander!. Blood 133 (2019), 1008–1009, 10.1182/blood-2019-01-895110.
Björkqvist, J., De Maat, S., Lewandrowski, U., Di Gennaro, A., Oschatz, C., Schönig, K., Nöthen, M.M., Drouet, C., Braley, H., Nolte, M.W., Sickmann, A., Panousis, C., Maas, C., Renné, T., Defective glycosylation of coagulation factor XII underlies hereditary angioedema type III. J. Clin. Invest. 125 (2015), 3132–3146, 10.1172/JCI77139.
Göbel, K., Pankratz, S., Asaridou, C.M., Herrmann, A.M., Bittner, S., Merker, M., Ruck, T., Glumm, S., Langhauser, F., Kraft, P., Krug, T.F., Breuer, J., Herold, M., Gross, C.C., Beckmann, D., Korb-Pap, A., Schuhmann, M.K., Kuerten, S., Mitroulis, I., Ruppert, C., Nolte, M.W., Panousis, C., Klotz, L., Kehrel, B., Korn, T., Langer, H.F., Pap, T., Nieswandt, B., Wiendl, H., Chavakis, T., Kleinschnitz, C., Meuth, S.G., Blood coagulation factor XII drives adaptive immunity during neuroinflammation via CD87-mediated modulation of dendritic cells. Nat. Commun., 7, 2016, 11626, 10.1038/ncomms11626.
Ziliotto, N., Baroni, M., Straudi, S., Manfredini, F., Mari, R., Menegatti, E., Voltan, R., Secchiero, P., Zamboni, P., Basaglia, N., Marchetti, G., Bernardi, F., Coagulation factor XII levels and intrinsic thrombin generation in multiple sclerosis. Front. Neurol. 9 (2018), 1–8, 10.3389/fneur.2018.00245.
Zamolodchikov, D., Chen, Z.-L., Conti, B.A., Renné, T., Strickland, S., Activation of the factor XII-driven contact system in Alzheimer's disease patient and mouse model plasma. Proc. Natl. Acad. Sci. 112 (2015), 4068–4073, 10.1073/pnas.1423764112.
Zamolodchikov, D., Renné, T., Strickland, S., The Alzheimer's disease peptide β-amyloid promotes thrombin generation through activation of coagulation factor XII. J. Thromb. Haemostasis 14 (2016), 995–1007, 10.1111/jth.13209.
Chen, Z.-L., Singh, P., Norris, E.H., Strickland, S., Revenko, A.S., MacLeod, A.R., Depletion of coagulation factor XII ameliorates brain pathology and cognitive impairment in Alzheimer disease mice. Blood 129 (2017), 2547–2556, 10.1182/blood-2016-11-753202.
Hopp, S., Albert-Weissenberger, C., Mencl, S., Bieber, M., Schuhmann, M.K., Stetter, C., Nieswandt, B., Schmidt, P.M., Monoranu, C.M., Alafuzoff, I., Marklund, N., Nolte, M.W., Sirén, A.L., Kleinschnitz, C., Targeting coagulation factor XII as a novel therapeutic option in brain trauma. Ann. Neurol. 79 (2016), 970–982, 10.1002/ana.24655.
Hopp, S., Nolte, M.W., Stetter, C., Kleinschnitz, C., Sirén, A.L., Albert-Weissenberger, C., Alleviation of secondary brain injury, posttraumatic inflammation, and brain edema formation by inhibition of factor XIIa. J. Neuroinflammation, 14, 2017, 39, 10.1186/s12974-017-0815-8.
Albert-Weissenberger, C., Hopp, S., Nieswandt, B., Sirén, A.L., Kleinschnitz, C., Stetter, C., How is the formation of microthrombi after traumatic brain injury linked to inflammation?. J. Neuroimmunol. 326 (2019), 9–13, 10.1016/j.jneuroim.2018.10.011.
Maurer, M., Magerl, M., Ansotegui, I., Aygören-Pürsün, E., Betschel, S., Bork, K., Bowen, T., Balle Boysen, H., Farkas, H., Grumach, A.S., Hide, M., Katelaris, C., Lockey, R., Longhurst, H., Lumry, W.R., Martinez-Saguer, I., Moldovan, D., Nast, A., Pawankar, R., Potter, P., Riedl, M., Ritchie, B., Rosenwasser, L., Sánchez-Borges, M., Zhi, Y., Zuraw, B., Craig, T., The international WAO/EAACI guideline for the management of hereditary angioedema—the 2017 revision and update. Allergy 73 (2018), 1575–1596, 10.1111/all.13384.
Bafunno, V., Firinu, D., D'Apolito, M., Cordisco, G., Loffredo, S., Leccese, A., Bova, M., Barca, M.P., Santacroce, R., Cicardi, M., Del Giacco, S., Margaglione, M., Mutation of the angiopoietin-1 gene (ANGPT1) associates with a new type of hereditary angioedema. J. Allergy Clin. Immunol. 141 (2018), 1009–1017, 10.1016/j.jaci.2017.05.020.
Bork, K., Wulff, K., Steinmüller-Magin, L., Brænne, I., Staubach-Renz, P., Witzke, G., Hardt, J., Hereditary angioedema with a mutation in the plasminogen gene. Allergy Eur. J. Allergy Clin. Immunol. 73 (2018), 442–450, 10.1111/all.13270.
Recke, A., Massalme, E.G., Jappe, U., Steinmüller-Magin, L., Schmidt, J., Hellenbroich, Y., Hüning, I., Gillessen-Kaesbach, G., Zillikens, D., Hartmann, K., Identification of the recently described plasminogen gene mutation p.Lys330Glu in a family from Northern Germany with hereditary angioedema. Clin. Transl. Allergy, 9, 2019, 9, 10.1186/s13601-019-0247-x.
Bork, K., Wulff, K., Rossmann, H., Steinmüller-Magin, L., Brænne, I., Witzke, G., Hardt, J., Hereditary angioedema cosegregating with a novel kininogen 1 gene mutation changing the N-terminal cleavage site of bradykinin. Allergy 74 (2019), 2479–2481, 10.1111/all.13869.
Perego, F., Wu, M.A., Valerieva, A., Caccia, S., Suffritti, C., Zanichelli, A., Bergamaschini, L., Cicardi, M., Current and emerging biologics for the treatment of hereditary angioedema. Expet Opin. Biol. Ther. 19 (2019), 517–526, 10.1080/14712598.2019.1595581.
Cao, H., Biondo, M., Lioe, H., Busfield, S., Rayzman, V., Nieswandt, B., Bork, K., Harrison, L.C., Auyeung, P., Farkas, H., Csuka, D., Pelzing, M., Dower, S., Wilson, M.J., Nash, A., Nolte, M.W., Panousis, C., Antibody-mediated inhibition of FXIIa blocks downstream bradykinin generation. J. Allergy Clin. Immunol. 142 (2018), 1355–1358, 10.1016/j.jaci.2018.06.014.
Biondo, M., Cao, Z., Rayzman, V., Hardy, M., McDonald, A., Busfield, S., Nolte, M.W., Wilson, M., Nash, A., Panousis, C., Development and characterization of an anti-FXIIa monoclonal antibody for the treatment of hereditary angioedema. J. Allergy Clin. Immunol., 135, 2015, AB194, 10.1016/j.jaci.2014.12.1570.
Liu, J., Qin, J., Borodovsky, A., Racie, T., Castoreno, A., Schlegel, M., Maier, M.A., Zimmerman, T., Fitzgerald, K., Butler, J., Akinc, A., An investigational RNAi therapeutic targeting Factor XII (ALN-F12) for the treatment of hereditary angioedema. RNA 25 (2019), 255–263, 10.1261/rna.068916.118.
Scheffel, J., Mahnke, N.A., Hofman, Z.L.M., de Maat, S., Wu, J., Bonnekoh, H., Pengelly, R.J., Ennis, S., Holloway, J.W., Kirchner, M., Mertins, P., Church, M.K., Maurer, M., Maas, C., Krause, K., Cold-induced urticarial autoinflammatory syndrome related to factor XII activation. Nat. Commun., 11, 2020, 179, 10.1038/s41467-019-13984-8.
Girolami, A., Ferrari, S., Cosi, E., Girolami, B., Randi, M.L., Thrombotic events in severe FXII deficiency in comparison with unaffected family members during a long observation period. J. Thromb. Thrombolysis 47 (2019), 481–485, 10.1007/s11239-019-01819-8.
Girolami, A., Ferrari, S., Cosi, E., Randi, M.L., Heterozygous FXII deficiency is not associated with an increased incidence of thrombotic events: results of a long term study, Blood Cells. Mol. Dis. 77 (2019), 8–11, 10.1016/j.bcmd.2019.03.001.
Key, N.S., Epidemiologic and clinical data linking factors XI and XII to thrombosis. Hematology 2014 (2014), 66–70, 10.1182/asheducation-2014.1.66.
Heestermans, M., Salloum-Asfar, S., Streef, T., Laghmani, E.H., Salvatori, D., Luken, B.M., Zeerleder, S.S., Spronk, H.M.H., Korporaal, S.J., Kirchhofer, D., Wagenaar, G.T.M., Versteeg, H.H., Reitsma, P.H., Renné, T., van Vlijmen, B.J.M., Mouse venous thrombosis upon silencing of anticoagulants depends on tissue factor and platelets, not FXII or neutrophils. Blood 133 (2019), 2090–2099, 10.1182/blood-2018-06-853762.
Yau, J.W., Liao, P., Fredenburgh, J.C., Stafford, A.R., Revenko, A.S., Monia, B.P., Weitz, J.I., Selective depletion of factor XI or factor XII with antisense oligonucleotides attenuates catheter thrombosis in rabbits. Blood 123 (2014), 2102–2107, 10.1182/blood-2013-12-540872.
Yau, J.W., Stafford, A.R., Liao, P., Fredenburgh, J.C., Roberts, R., Brash, J.L., Weitz, J.I., Corn trypsin inhibitor coating attenuates the prothrombotic properties of catheters in vitro and in vivo. Acta Biomater. 8 (2012), 4092–4100, 10.1016/j.actbio.2012.07.019.
Larsson, M., Rayzman, V., Nolte, M.W., Nickel, K.F., Björkqvist, J., Jämsä, A., Hardy, M.P., Fries, M., Schmidbauer, S., Hedenqvist, P., Broomé, M., Pragst, I., Dickneite, G., Wilson, M.J., Nash, A.D., Panousis, C., Renné, T., A factor XIIa inhibitory antibody provides thromboprotection in extracorporeal circulation without increasing bleeding risk. Sci. Transl. Med., 6, 2014, 10.1126/scitranslmed.3006804 222ra17-222ra17.
Aimo, A., Giugliano, R.P., De Caterina, R., Non–vitamin K Antagonist oral anticoagulants for mechanical heart valves. Circulation 138 (2018), 1356–1365, 10.1161/circulationaha.118.035612.
Jaffer, I.H., Fredenburgh, J.C., Hirsh, J., Weitz, J.I., Medical device-induced thrombosis: what causes it and how can we prevent it?. J. Thromb. Haemostasis, 13, 2015, 10.1111/jth.12961 S72–S81.
Jaffer, I.H., Stafford, A.R., Fredenburgh, J.C., Whitlock, R.P., Chan, N.C., Weitz, J.I., Dabigatran is less effective than Warfarin at attenuating mechanical heart Valve-induced thrombin generation. J. Am. Heart Assoc., 4, 2015, 10.1161/JAHA.115.002322 e002322.
Jaffer, I.H., Weitz, J.I., The blood compatibility challenge part 1: blood-contacting medical devices: the scope of the problem. Acta Biomater. 94 (2019), 2–10, 10.1016/j.actbio.2019.06.021.
Renné, T., Stavrou, E.X., Roles of factor XII in innate immunity. Front. Immunol. 10 (2019), 1–9, 10.3389/fimmu.2019.02011.
Nickel, K.F., Labberton, L., Long, A.T., Langer, F., Fuchs, T.A., Stavrou, E.X., Butler, L.M., Renné, T., The polyphosphate/factor XII pathway in cancer-associated thrombosis: novel perspectives for safe anticoagulation in patients with malignancies. Thromb. Res., 141, 2016, 10.1016/S0049-3848(16)30353-X S4–S7.
Campello, E., Ilich, A., Simioni, P., Key, N.S., The relationship between pancreatic cancer and hypercoagulability: a comprehensive review on epidemiological and biological issues. Br. J. Canc. 121 (2019), 359–371, 10.1038/s41416-019-0510-x.
Campello, E., Henderson, M.W., Noubouossie, D.F., Simioni, P., Key, N.S., Contact system Activation and cancer: new insights in the pathophysiology of cancer-associated thrombosis. Thromb. Haemost 118 (2018), 251–265, 10.1160/TH17-08-0596.
Matafonov, A., Leung, P.Y., Gailani, A.E., Grach, S.L., Puy, C., Cheng, Q., Sun, M., McCarty, O.J.T., Tucker, E.I., Kataoka, H., Renné, T., Morrissey, J.H., Gruber, A., Gailani, D., Factor XII inhibition reduces thrombus formation in a primate thrombosis model. Blood 123 (2014), 1739–1746, 10.1182/blood-2013-04-499111.
Mason, S., Kenniston, J.A., Nixon, A., Sexton, D.J., Comeau, S.R., Adelman, B., A Monoclonal Antibody Inhibitor of Factor XIIa. 2019 US20190002584 A1.
Lupu, F., Keshari, R.S., Lambris, J.D., Mark Coggeshall, K., Crosstalk between the coagulation and complement systems in sepsis. Thromb. Res., 133, 2014, 10.1016/j.thromres.2014.03.014 S28–S31.
Oehmcke, S., Herwald, H., Contact system activation in severe infectious diseases. J. Mol. Med. 88 (2010), 121–126, 10.1007/s00109-009-0564-y.
Pixley, R.A., Zellis, S., Bankes, P., DeLa Cadena, R.A., Page, J.D., Scott, C.F., Kappelmayer, J., Wyshock, E.G., Kelly, J.J., Colman, R.W., Prognostic value of assessing contact system activation and factor V in systemic inflammatory response syndrome. Crit. Care Med. 23 (1995), 41–51, 10.1097/00003246-199501000-00010.
Bachler, M., Niederwanger, C., Hell, T., Höfer, J., Gerstmeyr, D., Schenk, B., Treml, B., Fries, D., Influence of factor XII deficiency on activated partial thromboplastin time (aPTT) in critically ill patients. J. Thromb. Thrombolysis 48 (2019), 466–474, 10.1007/s11239-019-01879-w.
Nuijens, J., Huijbregts, C., Cohen, M., Navis, G., de Vries, A., Eerenberg, A., Bakker, J., Hack, C., Detection of activation of the contact system of coagulation in vitro and in vivo: Quantitation of activated hageman factor-C1-inhibitor and kallikrein-C1-inhibitor complexes by specific Radioimmunoassays. Thromb. Haemostasis 58 (1987), 778–785, 10.1055/s-0038-1645969.
Nuijens, J., Huijbregts, C., Eerenberg-Belmer, A., Abbink, J., Strack van Schijndel, R., Felt-Bersma, R., Thijs, L., Hack, C., Quantification of plasma factor XIIa-Cl(-)-inhibitor and kallikrein-Cl(-)-inhibitor complexes in sepsis. Blood 72 (1988), 1841–1848, 10.1182/blood.V72.6.1841.bloodjournal7261841.
Wuillemin, W.A., Minnema, M., Meijers, J.C., Roem, D., Eerenberg, A.J., Nuijens, J.H., ten Cate, H., Hack, C.E., Inactivation of factor XIa in human plasma assessed by measuring factor XIa-protease inhibitor complexes: major role for C1-inhibitor. Blood 85 (1995), 1517–1526.
Wuillemin, W., Fijnvandraat, K., Derkx, B., Peters, M., Vreede, W., ten Cate, H., Hack, C., Activation of the intrinsic pathway of coagulation in Children with meningococcal septic shock. Thromb. Haemostasis 74 (1995), 1436–1441, 10.1055/s-0038-1649961.
Jukema, B.N., de Maat, S., Maas, C., Processing of factor XII during inflammatory reactions. Front. Med. 3 (2016), 1–7, 10.3389/fmed.2016.00052.
Pixley, R.A., De La Cadena, R., Page, J.D., Kaufman, N., Wyshock, E.G., Chang, A., Taylor, F.B., Colman, R.W., The contact system Contributes to hypotension but not disseminated intravascular coagulation in lethal bacteremia. J. Clin. Invest. 91 (1993), 61–68.
Jansen, P., Pixley, R., Brouwer, M., de Jong, I., Chang, A., Hack, C., Taylor, F.J., Colman, R., Inhibition of factor XII in septic baboons attenuates the activation of complement and fibrinolytic systems and reduces the release of interleukin-6 and neutrophil elastase. Blood 87 (1996), 2337–2344, 10.1182/blood.V87.6.2337.bloodjournal8762337.
Silasi, R., Keshari, R.S., Lupu, C., Van Rensburg, W.J., Chaaban, H., Regmi, G., Shamanaev, A., Shatzel, J.J., Puy, C., Lorentz, C.U., Tucker, E.I., Gailani, D., Gruber, A., McCarty, O.J.T., Lupu, F., Inhibition of contact-mediated activation of factor XI protects baboons against S aureus-induced organ damage and death. Blood Adv 3 (2019), 658–669, 10.1182/bloodadvances.2018029983.
Iwaki, T., Cruz-Topete, D., Castellino, F.J., A complete factor XII deficiency does not affect coagulopathy, inflammatory responses, and lethality, but attenuates early hypotension in endotoxemic mice. J. Thromb. Haemostasis 6 (2008), 1993–1995, 10.1111/j.1538-7836.2008.03142.x.
Stroo, I., Zeerleder, S., Ding, C., Luken, B., Roelofs, J., de Boer, O., Meijers, J., Castellino, F., van ’t Veer, C., van der Poll, T., Coagulation factor XI improves host defence during murine pneumonia-derived sepsis independent of factor XII activation. Thromb. Haemostasis 117 (2017), 1601–1614, 10.1160/TH16-12-0920.
Stroo, I., Ding, C., Novak, A., Yang, J., Roelofs, J.J.T.H., Meijers, J.C.M., Revenko, A.S., van't Veer, C., Zeerleder, S., Crosby, J.R., van der Poll, T., Inhibition of the extrinsic or intrinsic coagulation pathway during pneumonia derived sepsis. Am. J. Physiol.-Lung C. 315 (2018), L799–L809, 10.1152/ajplung.00014.2018.
Tucker, E.I., Verbout, N.G., Leung, P.Y., Hurst, S., McCarty, O.J.T., Gailani, D., Gruber, A., Inhibition of factor XI activation attenuates inflammation and coagulopathy while improving the survival of mouse polymicrobial sepsis. Blood 119 (2012), 4762–4768, 10.1182/blood-2011-10-386185.
Lorenzano, S., Inglese, M., Koudriavtseva, T., Editorial: role of coagulation pathways in neurological diseases. Front. Neurol. 10 (2019), 1–3, 10.3389/fneur.2019.00791.
Yamamoto-Imoto, H., Zamolodchikov, D., Chen, Z.-L., Bourne, S.L., Rizvi, S., Singh, P., Norris, E.H., Weis-Garcia, F., Strickland, S., A novel detection method of cleaved plasma high-molecular-weight kininogen reveals its correlation with Alzheimer's pathology and cognitive impairment. Alzheimer's Dement. (Amst) 10 (2018), 480–489, 10.1016/j.dadm.2018.06.008.
Segal, B., The diversity of encephalitogenic CD4+ T cells in multiple sclerosis and its animal models. J. Clin. Med., 8, 2019, 120, 10.3390/jcm8010120.
Jain, K.K., Neuroprotection in traumatic brain injury. The Handbook of Neuroprotection, 2019, Springer Protocols Handbooks, Humana, New York, NY, 281–336.
Krowarsch, D., Cierpicki, T., Jelen, F., Otlewski, J., Canonical protein inhibitors of serine proteases, Cell. Mol. Life Sci. 60 (2003), 2427–2444, 10.1007/s00018-003-3120-x.
Apostoluk, W., Otlewski, J., Variability of the canonical loop conformations in serine proteinases inhibitors and other proteins. Proteins Struct. Funct. Genet. 32 (1998), 459–474, 10.1002/(SICI)1097-0134(19980901)32:4<459::AID-PROT5>3.0.CO;2-B.
Otlewski, J., Jaskólski, M., Buczek, O., Cierpicki, T., Czapiñska, H., Krowarsch, D., Smalas, A.O., Stachowiak, D., Szpineta, A., Dadlez, M., Structure-function relationship of serine protease–protein inhibitor interaction. Acta Biochim. Pol. 48 (2001), 419–428, 10.18388/abp.2001_3926.
Sanrattana, W., Maas, C., de Maat, S., SERPINs — from trap to treatment. Front. Med. 6 (2019), 1–8, 10.3389/fmed.2019.00025.
Scott, B.M., Sheffield, W.P., Engineering the serpin α1-antitrypsin: a diversity of goals and techniques. Protein Sci. 29 (2020), 856–871, 10.1002/pro.3794.
Koh, C.Y., Modahl, C.M., Kulkarni, N., Kini, R.M., Toxins are an excellent source of therapeutic agents against Cardiovascular diseases. Semin. Thromb. Hemost. 44 (2018), 691–706, 10.1055/s-0038-1661384.
Arcà, B., Ribeiro, J.M., Saliva of hematophagous insects: a multifaceted toolkit. Curr. Opin. Insect Sci. 29 (2018), 102–109, 10.1016/j.cois.2018.07.012.
Leboulle, G., Rochez, C., Louahed, J., Ruti, B., Brossard, M., Bollen, A., Godfroid, E., Isolation of Ixodes ricinus salivary gland mRNA encoding factors induced during blood feeding. Am. J. Trop. Med. Hyg. 66 (2002), 225–233, 10.4269/ajtmh.2002.66.225.
Decrem, Y., Rath, G., Blasioli, V., Cauchie, P., Robert, S., Beaufays, J., Frère, J.-M., Feron, O., Dogné, J.-M., Dessy, C., Vanhamme, L., Godfroid, E., Ir-CPI, a coagulation contact phase inhibitor from the tick Ixodes ricinus, inhibits thrombus formation without impairing hemostasis. J. Exp. Med. 206 (2009), 2381–2395, 10.1084/jem.20091007.
Godfroid, E., Decrem, Y., Vanhamme, L., Bollen, A., Leboulle, G., Identification and Molecular Characterisation of Proteins, Expressed in the Ixodes Ricinus Salivary Glands, 2015 US9212216 B2.
Pireaux, V., Tassignon, J., Demoulin, S., Derochette, S., Borenstein, N., Ente, A., Fiette, L., Douxfils, J., Lancellotti, P., Guyaux, M., Godfroid, E., Anticoagulation with an inhibitor of factors XIa and XIIa during cardiopulmonary bypass. J. Am. Coll. Cardiol. 74 (2019), 2178–2189, 10.1016/j.jacc.2019.08.1028.
Kato, N., Iwanaga, S., Okayama, T., Isawa, H., Yuda, M., Chinzei, Y., Identification and characterization of the plasma kallikrein-kinin system inhibitor, haemaphysalin, from hard tick, Haemaphysalis longicornis. Thromb. Haemostasis 93 (2005), 359–367, 10.1160/TH04-05-0319.
Kato, N., Okayama, T., Isawa, H., Yuda, M., Chinzei, Y., Iwanaga, S., Contribution of the N-terminal and C-terminal domains of haemaphysalin to inhibition of activation of plasma kallikrein-kinin system. J. Biochem. 138 (2005), 225–235, 10.1093/jb/mvi123.
Campos, I.T.N., Amino, R., Sampaio, C.A.M., Auerswald, E.A., Friedrich, T., Lemaire, H.G., Schenkman, S., Tanaka, A.S., Infestin, a thrombin inhibitor presents in Triatoma infestans midgut, a Chagas’ disease vector: gene cloning, expression and characterization of the inhibitor. Insect Biochem. Mol. Biol. 32 (2002), 991–997, 10.1016/S0965-1748(02)00035-8.
Hagedorn, I., Schmidbauer, S., Pleines, I., Kleinschnitz, C., Kronthaler, U., Stoll, G., Dickneite, G., Nieswandt, B., Factor XIIa inhibitor recombinant human albumin infestin-4 Abolishes occlusive arterial thrombus formation without affecting bleeding. Circulation 121 (2010), 1510–1517, 10.1161/CIRCULATIONAHA.109.924761.
Campos, I.T.N., Souza, T.A.C.B., Torquato, R.J.S., De Marco, R., Tanaka-Azevedo, A.M., Tanaka, A.S., Barbosa, J.A.R.G., The Kazal-type inhibitors infestins 1 and 4 differ in specificity but are similar in three-dimensional structure. Acta Crystallogr. Sect. D Biol. Crystallogr. 68 (2012), 695–702, 10.1107/S0907444912009067.
Campos, I.T.N., Tanaka-Azevedo, A.M., Tanaka, A.S., Identification and characterization of a novel factor XIIa inhibitor in the hematophagous insect, Triatoma infestans (Hemiptera: Reduviidae). FEBS Lett. 577 (2004), 512–516, 10.1016/j.febslet.2004.10.052.
Xu, Y., Cai, T.Q., Castriota, G., Zhou, Y., Hoos, L., Jochnowitz, N., Loewrigkeit, C., Cook, J.A., Wickham, A., Metzger, J.M., Ogletree, M.L., Seiffert, D.A., Chen, Z., Factor XIIa inhibition by Infestin-4: in vitro mode of action and in vivo antithrombotic benefit. Thromb. Haemost 111 (2013), 694–704, 10.1160/TH13-08-0668.
Barbieri, C.M., Wang, X., Zhou, X., Ogawa, A.M., O'Neil, K., Wu, W., Castriota, G., Seiffert, D.A., Gutstein, D., Factor XIIa: new insights on chemical tractability and target indications from a potent and selective tool inhibitor. Arterioscler. Thromb. Vasc. Biol., 36, 2016, A523.
Isawa, H., Orito, Y., Jingushi, N., Iwanaga, S., Morita, A., Chinzei, Y., Yuda, M., Identification and characterization of plasma kallikrein-kinin system inhibitors from salivary glands of the blood-sucking insect Triatoma infestans. FEBS J. 274 (2007), 4271–4286, 10.1111/j.1742-4658.2007.05958.x.
Hernández-Vargas, M., Santibáñez-López, C., Corzo, G., An insight into the triabin protein family of American hematophagous Reduviids: functional, structural and phylogenetic analysis. Toxins, 8, 2016, 44, 10.3390/toxins8020044.
Kato, H., Jochim, R.C., Gomez, E.A., Sakoda, R., Iwata, H., Valenzuela, J.G., Hashiguchi, Y., A repertoire of the dominant transcripts from the salivary glands of the blood-sucking bug, Triatoma dimidiata, a vector of Chagas disease. Infect. Genet. Evol. 10 (2010), 184–191, 10.1016/j.meegid.2009.10.012.
Fuentes-Prior, P., Noeske-Jungblut, C., Donner, P., Schleuning, W.-D., Huber, R., Bode, W., Structure of the thrombin complex with triabin, a lipocalin-like exosite-binding inhibitor derived from a triatomine bug. Proc. Natl. Acad. Sci. 94 (1997), 11845–11850, 10.1073/pnas.94.22.11845.
Ishimaru, Y., Gomez, E.A., Zhang, F., Martini-Robles, L., Iwata, H., Sakurai, T., Katakura, K., Hashiguchi, Y., Kato, H., Dimiconin, a novel coagulation inhibitor from the kissing bug, Triatoma dimidiata, a vector of Chagas disease. J. Exp. Biol. 215 (2012), 3597–3602, 10.1242/jeb.074211.
Isawa, H., Yuda, M., Orito, Y., Chinzei, Y., A mosquito salivary protein inhibits activation of the plasma contact system by binding to factor XII and high molecular weight kininogen. J. Biol. Chem. 277 (2002), 27651–27658, 10.1074/jbc.M203505200.
Kato, H., Gomez, E.A., Fujita, M., Ishimaru, Y., Uezato, H., Mimori, T., Iwata, H., Hashiguchi, Y., Ayadualin, a novel RGD peptide with dual antihemostatic activities from the sand fly Lutzomyia ayacuchensis, a vector of Andean-type cutaneous leishmaniasis. Biochimie 112 (2015), 49–56, 10.1016/j.biochi.2015.02.011.
Calvo, E., Mans, B.J., Andersen, J.F., Ribeiro, J.M.C., Function and evolution of a mosquito salivary protein family. J. Biol. Chem. 281 (2006), 1935–1942, 10.1074/jbc.M510359200.
Kato, H., Jochim, R.C., Gomez, E.A., Uezato, H., Mimori, T., Korenaga, M., Sakurai, T., Katakura, K., Valenzuela, J.G., Hashiguchi, Y., Analysis of salivary gland transcripts of the sand fly Lutzomyia ayacuchensis, a vector of Andean-type cutaneous leishmaniasis. Infect. Genet. Evol. 13 (2013), 56–66, 10.1016/j.meegid.2012.08.024.
Harish, B.S., Uppuluri, K.B., Microbial serine protease inhibitors and their therapeutic applications. Int. J. Biol. Macromol. 107 (2018), 1373–1387, 10.1016/j.ijbiomac.2017.09.115.
Chung, C.H., Ives, H.E., Almeda, S., Goldberg, A.L., Purification from Escherichia coli of a periplasmic protein that is a potent inhibitor of pancreatic proteases. J. Biol. Chem. 258 (1983), 11032–11038.
Ulmer, J.S., Lindquist, R.N., Dennis, M.S., Lazarus, R.A., Ecotin is a potent inhibitor of the contact system proteases factor XIIa and plasma kallikrein. FEBS Lett. 365 (1995), 159–163, 10.1016/0014-5793(95)00466-M.
Seymour, J.L., Lindquist, R.N., Dennis, M.S., Moffat, B., Yansura, D., Reilly, D., Wessinger, M.E., Lazarus, R.A., Ecotin is a potent anticoagulant and Reversible Tight-binding inhibitor of factor Xa. Biochemistry 33 (1994), 3949–3958, 10.1021/bi00179a022.
Lauwereys, M.J., Lambeir, A.-M.V.R., Ecotin as a Factor Xa, XIa, and XIIa Inhibitor. 1996 US5585259.
Gillmor, S.A., Takeuchi, T., Yang, S.Q., Craik, C.S., Fletterick, R.J., Compromise and accommodation in ecotin, a dimeric macromolecular inhibitor of serine proteases. J. Mol. Biol. 299 (2000), 993–1003, 10.1006/jmbi.2000.3812.
Eggers, C.T., Wang, S.X., Fletterick, R.J., Craik, C.S., The role of ecotin dimerization in protease inhibition. J. Mol. Biol. 308 (2001), 975–991, 10.1006/jmbi.2001.4754.
Jin, L., Pandey, P., Babine, R.E., Gorga, J.C., Seidl, K.J., Gelfand, E., Weaver, D.T., Abdel-Meguid, S.S., Strickler, J.E., Crystal structures of the FXIa catalytic domain in complex with ecotin mutants reveal substrate-like interactions. J. Biol. Chem. 280 (2005), 4704–4712, 10.1074/jbc.M411309200.
Mcgrath, M.E., Gillmor, S.A., Fletterick, R.J., Ecotin: lessons on survival in a protease-filled world. Protein Sci. 4 (1995), 141–148, 10.1002/pro.5560040201.
McGrath, M.E., Hines, W.M., Sakanari, J.A., Fletterick, R.J., Craik, C.S., The sequence and reactive site of ecotin: a general inhibitor of pancreatic serine proteases from Escherichia coli. J. Biol. Chem. 266 (1991), 6620–6625.
Shin, D.H., Song, H.K., Seong, I.S., Suh, S.W., Lee, C.S., Chung, C.H., Crystal structure analyses of uncomplexed ecotin in two crystal forms: implications for its function and stability. Protein Sci. 5 (1996), 2236–2247, 10.1002/pro.5560051110.
Lazarus R.A., Dennis M.S., Ulmer J.S., DNA Encoding Ecotin Homologs, 1998 US5719041.
Yang, S.Q., Wang, C.I., Gillmor, S.A., Fletterick, R.J., Craik, C.S., Ecotin: a serine protease inhibitor with two distinct and interacting binding sites. J. Mol. Biol. 279 (1998), 945–957, 10.1006/jmbi.1998.1748.
Stoop, A.A., Craik, C.S., Engineering of a macromolecular scaffold to develop specific protease inhibitors. Nat. Biotechnol. 21 (2003), 1063–1068, 10.1038/nbt860.
Tanabe, M., Asano, T., Moriya, N., Sugino, H., Kakinuma, A., Isolation and characterization of Streptoverticillium anticoagulant (SAC), a novel protein inhibitor of blood coagulation produced by Streptoverticillium cinnamoneum subsp. cinnamoneum. J. Biochem. 115 (1994), 743–751, 10.1093/oxfordjournals.jbchem.a124405.
Tanabe, M., Kawahara, K., Asano, T., Kato, K., Kakinuma, A., Primary structure and reactive site of Streptoverticillium anticoagulant (SAC), a novel protein inhibitor of blood coagulation produced by Streptoverticillium cinnamoneum subsp. cinnamoneum. J. Biochem. 115 (1994), 752–761, 10.1093/oxfordjournals.jbchem.a124406.
Hellinger, R., Gruber, C.W., Peptide-based protease inhibitors from plants. Drug Discov. Today 24 (2019), 1877–1889, 10.1016/j.drudis.2019.05.026.
Sampaio, C.A.M., Oliva, M.L.V., Sampaio, M.U., Batista, I.F.C., Bueno, N.R., Tanaka, A.S., Auerswald, E.A., Fritz, H., Plant serine proteinase inhibitors. Structure and biochemical applications on plasma kallikrein and related enzymes. Immunopharmacology 32 (1996), 62–66, 10.1016/0162-3109(96)00073-2.
V Oliva, M.L., Andrade, S.A., Juliano, M.A., Sallai, R.C., Torquato, R.J., Sampaio, M.U., Pott, V.J., Sampaio, C.A.M., Kinetic characterization of factor Xa binding using a quenched fluorescent substrate based on the reactive site of factor Xa inhibitor from Bauhinia ungulata seeds. Curr. Med. Chem. 10 (2003), 1085–1093, 10.2174/0929867033457548.
Mahoney, W.C., Hermodson, M.A., Jones, B., Powers, D.D., Corfman, R.S., Reeck, G.R., Amino acid sequence and secondary structural analysis of the corn inhibitor of trypsin and activated Hageman factor. J. Biol. Chem. 259 (1984), 8412–8416.
Chong, G.L., Reeck, G.R., Interaction of trypsin, β-factor XIIa, and plasma kallikrein with a trypsin inhibitor isolated from barley seeds: a comparison with the corn inhibitor of activated hageman factor. Thromb. Res. 48 (1987), 211–221, 10.1016/0049-3848(87)90418-X.
Hayashi, K., Takehisa, T., Hamato, N., Takano, R., Hara, S., Miyata, T., Kato, H., Inhibition of serine proteases of the blood squash family protease inhibitors coagulation system by squash family inhibitors. J. Biochem. 116 (1994), 1013–1018, 10.1093/oxfordjournals.jbchem.a124621.
Bode, W., Greyling, H.J., Huber, R., Otlewski, J., Wilusz, T., The refined 2.0 Å X-ray crystal structure of the complex formed between bovine β-trypsin and CMTI-I, a trypsin inhibitor from squash seeds (Cucurbita maxima). FEBS Lett. 242 (1989), 285–292, 10.1016/0014-5793(89)80486-7.
Hernandez, J.F., Gagnon, J., Chiche, L., Nguyen, T.M., Andrieu, J.P., Heitz, A., Hong, T.T., Pham, T.T.C., Le Nguyen, D., Squash trypsin inhibitors from Momordica cochinchinensis exhibit an atypical macrocyclic structure. Biochemistry 39 (2000), 5722–5730, 10.1021/bi9929756.
Elena Felizmenio-Quimio, M., Daly, N.L., Craik, D.J., Circular proteins in plants. Solution structure of a novel macrocyclic trypsin inhibitor from Momordica cochinchinensis. J. Biol. Chem. 276 (2001), 22875–22882, 10.1074/jbc.M101666200.
Gray, K., Elghadban, S., Thongyoo, P., Owen, K.A., Szabo, R., Bugge, T.H., Tate, E.W., Leatherbarrow, R.J., Ellis, V., Potent and specific inhibition of the biological activity of the type-II transmembrane serine protease matriptase by the cyclic microprotein MCoTI-II. Thromb. Haemostasis 112 (2014), 402–411, 10.1160/TH13-11-0895.
Mahatmanto, T., Review seed biopharmaceutical cyclic peptides: from discovery to applications. Biopolymers 104 (2015), 804–814, 10.1002/bip.22741.
Thongyoo, P., Bonomelli, C., Leatherbarrow, R.J., Tate, E.W., Potent inhibitors of β-tryptase and human leukocyte elastase based on the MCoTI-II scaffold. J. Med. Chem. 52 (2009), 6197–6200, 10.1021/jm901233u.
Swedberg, J.E., Ghani, H.A., Harris, J.M., de Veer, S.J., Craik, D.J., Potent, selective, and cell-penetrating inhibitors of kallikrein-related peptidase 4 based on the cyclic peptide MCoTI-II. ACS Med. Chem. Lett. 9 (2018), 1258–1262, 10.1021/acsmedchemlett.8b00422.
Swedberg, J.E., Mahatmanto, T., Abdul Ghani, H., de Veer, S.J., Schroeder, C.I., Harris, J.M., Craik, D.J., Substrate-guided design of selective FXIIa inhibitors based on the plant-derived Momordica cochinchinensis trypsin inhibitor-II (MCoTI-II) scaffold. J. Med. Chem. 59 (2016), 7287–7292, 10.1021/acs.jmedchem.6b00557.
Gosalia, D.N., Denney, W.S., Salisbury, C.M., Ellman, J.A., Diamond, S.L., Functional phenotyping of human plasma using a 361-fluorogenic substrate biosensing microarray. Biotechnol. Bioeng. 94 (2006), 1099–1110, 10.1002/bit.20927.
Gosalia, D.N., Salisbury, C.M., Ellman, J.A., Diamond, S.L., High Throughput substrate specificity profiling of serine and Cysteine proteases using solution-phase fluorogenic peptide microarrays. Mol. Cell. Proteomics 4 (2005), 626–636, 10.1074/mcp.m500004-mcp200.
de Veer, S.J., Wang, C.K., Harris, J.M., Craik, D.J., Swedberg, J.E., Improving the selectivity of engineered protease inhibitors: optimizing the P2 prime residue using a Versatile cyclic peptide library. J. Med. Chem. 58 (2015), 8257–8268, 10.1021/acs.jmedchem.5b01148.
Krishnamoorthi, R., Gong, Y., Richardson, M., A new protein inhibitor of trypsin and activated Hageman factor from pumpkin (Cucurbita maxima) seeds. FEBS Lett. 273 (1990), 163–167, 10.1016/0014-5793(90)81075-y.
Bateman, K.S., James, M.N.G., Plant protein proteinase Inhibitors: structure and mechanism of inhibition. Curr. Protein Pept. Sci. 12 (2011), 341–347, 10.2174/138920311796391124.
Liu, J., Gong, W.X.I., Prakash, O.M., Wen, L., Lee, I., Huang, J.K., Krishnamoorthi, R., NMR studies of internal dynamics of serine proteinase protein inhibitors: Binding region mobilities of intact and reactive-site hydrolyzed Cucurbita maxima trypsin inhibitor (CMTI)-III of the squash family and comparison with those of counterparts of CMTI-V of the potato I family. Protein Sci. 7 (1998), 132–141, 10.1002/pro.5560070114.
Grosse-Holz, F.M., van der Hoorn, R.A.L., Juggling jobs: roles and mechanisms of multifunctional protease inhibitors in plants. New Phytol. 210 (2016), 794–807, 10.1111/nph.13839.
Tanaka, A.S., Sampaio, M.U., Sampaio, C.A., Oliva, M.L., Purification and preliminary characterization of Torresea cearensis trypsin inhibitor. Brazilian J. Med. Biol. Res. 22 (1989), 1069–1071.
Tanaka, A.S., Sampaio, M.U., Mentele, R., Auerswald, E.A., Sampaio, C.A.M., Sequence of a new Bowman-Birk inhibitor from Torresea acreana seeds and comparison with Torresea cearensis trypsin inhibitor (TcTI2). J. Protein Chem. 15 (1996), 553–560, 10.1007/BF01908537.
Tanaka, A.S., Sampaio, M.U., Marangoni, S., de Oliveira, B., Novelle, J.C., Oliva, M.L.V., Fink, E., Sampaio, C.A.M., Purification and primary structure determination of a bowman-Birk Trypsin inhibitor from Torresea cearensis seeds. Biol. Chem. 378 (1997), 273–282, 10.1515/bchm.1997.378.3-4.273.
Shinde, P., Banerjee, P., Mandhare, A., Marine natural products as source of new drugs: a patent review (2015–2018). Expert Opin. Ther. Pat. 29 (2019), 283–309, 10.1080/13543776.2019.1598972.
Mayer, A.M.S., Glaser, K.B., Cuevas, C., Jacobs, R.S., Kem, W., Little, R.D., McIntosh, J.M., Newman, D.J., Potts, B.C., Shuster, D.E., The odyssey of marine pharmaceuticals: a current pipeline perspective. Trends Pharmacol. Sci. 31 (2010), 255–265, 10.1016/j.tips.2010.02.005.
Malve, H., Exploring the ocean for new drug developments: marine pharmacology. J. Pharm. Bioall. Sci., 8, 2016, 83, 10.4103/0975-7406.171700.
Rajapakse, N., Jung, W., Mendis, E., Moon, S., Kim, S., A novel anticoagulant purified from fish protein hydrolysate inhibits factor XIIa and platelet aggregation. Life Sci. 76 (2005), 2607–2619, 10.1016/j.lfs.2004.12.010.
Indumathi, P., Mehta, A., A novel anticoagulant peptide from the Nori hydrolysate. J. Funct. Foods 20 (2016), 606–617, 10.1016/j.jff.2015.11.016.
Syed, A.A., Venkatraman, K.L., Mehta, A., An anticoagulant peptide from Porphyra yezoensis inhibits the activity of factor XIIa: in vitro and in silico analysis. J. Mol. Graph. Model. 89 (2019), 225–233, 10.1016/j.jmgm.2019.03.019.
Huber, R., Carrell, R.W., Implications of the three-dimentional structure of α1-antitrypsin for structure and function of serpins. Biochemistry 28 (1989), 8951–8966, 10.1021/bi00449a001.
Scott, C.F., Carrell, R.W., Glaser, C.B., Kueppers, F., Lewis, J.H., Colman, R.W., Alpha-1-antitrypsin-Pittsburgh : a potent inhibitor of human plasma factor XIa, kallikrein, and factor Xllf. J. Clin. Invest. 77 (1986), 631–634, 10.1172/JCI112346.
Schapira, M., Ramus, M., Jallat, S., Carvallo, D., Courtney, M., Recombinant alpha 1-antitrypsin Pittsburgh (Met 358—-Arg) is a potent inhibitor of plasma kallikrein and activated factor XII fragment. J. Clin. Invest. 77 (1986), 635–637, 10.1172/JCI112347.
de Maat, S., Sanrattana, W., Mailer, R.K., Parr, N.M.J., Hessing, M., Koetsier, R.M., Meijers, J.C.M., Pasterkamp, G., Renné, T., Maas, C., Design and characterization of α1-antitrypsin variants for treatment of contact system-driven thromboinflammation. Blood 134 (2019), 1658–1669, 10.1182/blood.2019000481.
Baeriswyl, V., Calzavarini, S., Gerschheimer, C., Diderich, P., Angelillo-Scherrer, A., Heinis, C., Development of a selective peptide macrocycle inhibitor of coagulation factor XII toward the generation of a safe antithrombotic therapy. J. Med. Chem. 56 (2013), 3742–3746, 10.1021/jm400236j.
Angelini, A., Cendron, L., Chen, S., Touati, J., Winter, G., Zanotti, G., Heinis, C., Bicyclic peptide inhibitor reveals large contact interface with a protease target. ACS Chem. Biol. 7 (2012), 817–821, 10.1021/cb200478t.
van de Langemheen, H., Korotkovs, V., Bijl, J., Wilson, C., Kale, S.S., Heinis, C., Liskamp, R.M.J., Polar hinges as functionalized conformational constraints in (Bi)cyclic peptides. Chembiochem 18 (2017), 387–395, 10.1002/cbic.201600612.
Wilbs, J., Middendorp, S.J., Heinis, C., Improving the binding affinity of in-vitro-evolved cyclic peptides by inserting Atoms into the macrocycle backbone. Chembiochem 17 (2016), 2299–2303, 10.1002/cbic.201600336.
Middendorp, S.J., Wilbs, J., Quarroz, C., Calzavarini, S., Angelillo-Scherrer, A., Heinis, C., Peptide macrocycle inhibitor of coagulation factor XII with subnanomolar affinity and high target selectivity. J. Med. Chem. 60 (2017), 1151–1158, 10.1021/acs.jmedchem.6b01548.
Zorzi, A., Middendorp, S.J., Wilbs, J., Deyle, K., Heinis, C., Acylated heptapeptide binds albumin with high affinity and application as tag furnishes long-acting peptides. Nat. Commun., 8, 2017, 16092, 10.1038/ncomms16092.
Philippou, H., Foster, R., Fishwick, C., Revill, C., Yule, I., Taylor, R., Naylor, A., Fallon, P.S., Crosby, S., Hopkins, A., Stewart, M.R., Winfield, N.L., FACTOR XIIa INHIBITORS. 2019 WO/2019/211585.
Bouckaert, C., Serra, S., Rondelet, G., Dolušić, E., Wouters, J., Dogné, J.M., Frédérick, R., Pochet, L., Synthesis, evaluation and structure-activity relationship of new 3-carboxamide coumarins as FXIIa inhibitors. Eur. J. Med. Chem. 110 (2016), 181–194, 10.1016/j.ejmech.2016.01.023.
Bouckaert, C., Zhu, S., Govers-Riemslag, J.W.P., Depoorter, M., Diamond, S.L., Pochet, L., Discovery and assessment of water soluble coumarins as inhibitors of the coagulation contact pathway. Thromb. Res. 157 (2017), 126–133, 10.1016/j.thromres.2017.07.015.
Sinha, U., Ku, P., Malinowski, J., Zhu, B.Y., Scarborough, R.M., Marlowe, C.K., Wong, P.W., Lin, P.H., Hollenbach, S.J., Antithrombotic and hemostatic capacity of factor Xa versus thrombin inhibitors in models of venous and arteriovenous thrombosis. Eur. J. Pharmacol. 395 (2000), 51–59, 10.1016/S0014-2999(00)00219-3.
Stürzebecher, A., Dönnecke, D., Schweinitz, A., Schuster, O., Steinmetzer, P., Stürzebecher, U., Kotthaus, J., Clement, B., Stürzebecher, J., Steinmetzer, T., Highly potent and selective substrate Analogue factor Xa inhibitors ContainingD-homophenylalanine Analogues as P3 residue: Part 2. ChemMedChem 2 (2007), 1043–1053, 10.1002/cmdc.200700031.
Pâques, E.-P., Römisch, J., Comparative study on the in vitro effectiveness of antithrombotic agents. Thromb. Res. 64 (1991), 11–21, 10.1016/0049-3848(91)90201-7.
Hitomi, Y., Ikari, N., Fujii, S., Inhibitory effect of a new synthetic protease inhibitor (FUT-175) on the coagulation system. Haemostasis 15 (1985), 164–168, 10.1159/000215139.
Tans, G., Janssen-Claessen, T., Rosing, J., Griffin, J.H., Studies on the effect of serine protease inhibitors on activated contact factors Application in amidolytic assays for factor XIIa, plasma kallikrein and factor XIa. Eur. J. Biochem. 164 (1987), 637–642, 10.1111/j.1432-1033.1987.tb11174.x.
Nakamura, K., Johmura, A., Oda, M., Ino, Y., Uchiyama, H., Ohtani, H., Miyazaki, H., Kurumi, M., Akizawa, Y., Oka, T., Inhibitory effects of sepimostat mesilate (FUT-187) on the activities of trypsin-like serine proteases in vitro. Yakugaku Zasshi 115 (1995), 201–212, 10.1248/yakushi1947.115.3_201.
Nakayama, T., Taira, S., Ikeda, M., Ashizawa, H., Oda, M., Arakawa, K., Fujii, S., Synthesis and structure-activity of protease inhibitors. V. Chemical modification of 6-Amidino-2-naphtyl 4-guanidinobenzoate. Chem. Pharm. Bull. 41 (1993), 117–125, 10.1248/cpb.41.117.
Silverberg, M., Kaplan, A.P., Enzymatic activities of activated and zymogen forms of human Hageman factor (factor XII). Blood 60 (1982), 64–70.
Robert, S., Bertolla, C., Masereel, B., Dogné, J.M., Pochet, L., Novel 3-carboxamide-coumarins as potent and selective FXIIa inhibitors. J. Med. Chem. 51 (2008), 3077–3080, 10.1021/jm8002697.
Doucet, C., Pochet, L., Thierry, N., Pirotte, B., Delarge, J., Rebound-Ravaux, M., 6-Substituted 2-oxo-2H-1-benzopyran-3-carboxylic acid as a core structure for specific inhibitors of human leukocyte elastase. J. Med. Chem. 42 (1999), 4161–4171, 10.1021/jm990070k.
Pochet, L., Doucet, C., Dive, G., Wouters, J., Masereel, B., Reboud-Ravaux, M., Pirotte, B., Coumarinic derivatives as mechanism-based inhibitors of α-chymotrypsin and human leukocyte elastase. Bioorg. Med. Chem. 8 (2000), 1489–1501, 10.1016/S0968-0896(00)00071-7.
Pochet, L., Doucet, C., Schynts, M., Thierry, N., Boggetto, N., Pirotte, B., Jiang, K.Y., Masereel, B., de Tullio, P., Delarge, J., Reboud-Ravaux, M., Esters and amides of 6-(Chloromethyl)-2-oxo-2 H -1-benzopyran-3-carboxylic acid as inhibitors of α-chymotrypsin: significance of the “aromatic” nature of the novel ester-type coumarin for strong inhibitory activity. J. Med. Chem. 39 (1996), 2579–2585, 10.1021/jm960090b.
Pochet, L., Frederick, R., Masereel, B., Coumarin and isocoumarin as serine protease inhibitors. Curr. Pharmaceut. Des. 10 (2004), 3781–3796, 10.2174/1381612043382684.
Frédérick, R., Charlier, C., Robert, S., Wouters, J., Masereel, B., Pochet, L., Investigation of mechanism-based thrombin inhibitors: implications of a highly conserved water molecule for the binding of coumarins within the S pocket. Bioorg. Med. Chem. Lett 16 (2006), 2017–2021, 10.1016/j.bmcl.2005.12.070.
Frédérick, R., Robert, S., Charlier, C., De Ruyck, J., Wouters, J., Pirotte, B., Masereel, B., Pochet, L., 3,6-Disubstituted coumarins as mechanism-based inhibitors of thrombin and factor Xa. J. Med. Chem. 48 (2005), 7592–7603, 10.1021/jm050448g.
Frédérick, R., Robert, S., Charlier, C., Wouters, J., Masereel, B., Pochet, L., Mechanism-based thrombin inhibitors: design, synthesis, and molecular docking of a new selective 2-oxo-2H-1-benzopyran derivative. J. Med. Chem. 50 (2007), 3645–3650, 10.1021/jm061368v.
Kraft, P., Schwarz, T., Pochet, L., Stoll, G., Kleinschnitz, C., COU254, a specific 3-carboxamide-coumarin inhibitor of coagulation factor XII, does not protect mice from acute ischemic stroke. Exp. Transl. Stroke Med., 2, 2010, 5, 10.1186/2040-7378-2-5.
Chen, J.J.F., Visco, D.P., Identifying novel factor XIIa inhibitors with PCA-GA-SVM developed vHTS models. Eur. J. Med. Chem. 140 (2017), 31–41, 10.1016/j.ejmech.2017.08.056.
Zhu, B.-Y., Huang, W., Su, T., Marlowe, C., Sinha, U., Hollenbach, S., Scarborough, R., Discovery of transition state factor Xa inhibitors as potential anticoagulant agents. Curr. Top. Med. Chem. 1 (2001), 101–119, 10.2174/1568026013395425.
Rewinkel, J.B.M., Adang, A.E.P., Towards the ideal orally active thrombin inhibitor. Curr. Pharmaceut. Des. 5 (1999), 1043–1075.
Kleinschnitz, C., Stoll, G., Bendszus, M., Schuh, K., Pauer, H.-U., Burfeind, P., Renné, C., Gailani, D., Nieswandt, B., Renné, T., Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J. Exp. Med. 203 (2006), 513–518, 10.1084/jem.20052458.
Kettner, C., Shaw, E., Inactivation of trypsin-like enzymes with peptides of arginine chloromethyl ketone. Methods Enzymol. 80 (1981), 826–842, 10.1016/S0076-6879(81)80065-1.
Muramatu, M., Onishi, T., Makino, S., Fujii, S., Yamamura, Y., Inhibition of Caseinolytic activity of plasmin by various synthetic inhibitors. J. Biochem. 57 (1965), 402–406, 10.1093/oxfordjournals.jbchem.a128094.
Muramatu, M., Onishi, T., Makino, S., Fujii, S., Yamamura, Y., Inhibition of fibrinolytic activity of plasmin by various synthetic inhibitors. J. Biochem. 57 (1965), 450–453, 10.1093/oxfordjournals.jbchem.a128100.
Muramatu, M., Fujii, S., Inhibitory effects of ω-guanidino acid esters on trypsin, plasmin, thrombin and plasma kallikrein. J. Biochem. 64 (1968), 807–814, 10.1093/oxfordjournals.jbchem.a128963.
Muramatu, M., Fujii, S., Inhibitory effects of ω-amino acid esters on trypsin, plasmin, plasma kallikrein and thrombin. Biochim. Biophys. Acta 242 (1971), 203–208, 10.1016/0005-2744(71)90100-8.
Muramatu, M., Fujii, S., Inhibitory effects of ω-guanidino acid esters on trypsin, plasmin, plasma kallikrein and thrombin. BBA - Enzymol. 268 (1972), 221–224, 10.1016/0005-2744(72)90218-5.
Mares-Guia, M., Shaw, E., The specific inactivation of trypsin by ethyl p-guanidinobenzoate. J. Biol. Chem. 242 (1967), 5782–5788.
Chase, T., Shaw, E., Comparison of the esterase activities of trypsin, plasmin, and thrombin on guanidinobenzoate esters. Titration of the enzymes. Biochemistry 8 (1969), 2212–2224, 10.1021/bi00833a063.
Tamura, Y., Hirado, M., Okamura, K., Minato, Y., Fujii, S., Synthetic inhibitors of trypsin, plasmin, kallikrein, thrombin, C1r, and C1 esterase. BBA - Enzymol 484 (1977), 417–422, 10.1016/0005-2744(77)90097-3.
Fujii, S., Hitomi, Y., New synthetic inhibitors of Clr, Clesterase, thrombin, plasmin, kallikrein and trypsin. Japanese J. Clin. Chem. 10 (1981), 248–252, 10.14921/jscc1971b.10.3_248.
Bennett, C.F., Swayze, E.E., RNA targeting therapeutics: molecular mechanisms of antisense oligonucleotides as a therapeutic platform. Annu. Rev. Pharmacol. Toxicol. 50 (2010), 259–293, 10.1146/annurev.pharmtox.010909.105654.
Tillman, B.F., Gruber, A., Mccarty, O.J.T., Gailani, D., Plasma contact factors as therapeutic targets. Blood Rev. 32 (2018), 433–448, 10.1016/j.blre.2018.04.001.
Watts, J.K., The medicinal Chemistry of antisense oligonucleotides. Ferrari, N., Seguin, R., (eds.) Oligonucleotide-Based Drugs Ther, first ed., 2018, John Wiley & Sons, Inc., Hoboken, NJ, USA, 39–90, 10.1002/9781119070153.ch2.
Khvorova, A., Watts, J.K., The chemical evolution of oligonucleotide therapies of clinical utility. Nat. Biotechnol. 35 (2017), 238–248, 10.1038/nbt.3765.
Smith, C.I.E., Zain, R., Therapeutic oligonucleotides: state of the Art. Annu. Rev. Pharmacol. Toxicol. 59 (2019), 605–630, 10.1146/annurev-pharmtox-010818-021050.
Hagedorn, P.H., Hansen, B.R., Koch, T., Lindow, M., Managing the sequence-specificity of antisense oligonucleotides in drug discovery. Nucleic Acids Res. 45 (2017), 2262–2282, 10.1093/nar/gkx056.
Revenko, A.S., Gao, D., Crosby, J.R., Bhattacharjee, G., Zhao, C., May, C., Gailani, D., Monia, B.P., MacLeod, A.R., Selective depletion of plasma prekallikrein or coagulation factor XII inhibits thrombosis in mice without increased risk of bleeding. Blood 118 (2011), 5302–5311, 10.1182/blood-2011-05-355248.
Bhattacharjee, G., Revenko, A.S., Crosby, J.R., May, C., Gao, D., Zhao, C., Monia, B.P., MacLeod, A.R., Inhibition of vascular permeability by antisense-mediated inhibition of plasma kallikrein and coagulation factor 12. Nucleic Acid Therapeut. 23 (2013), 175–187, 10.1089/nat.2013.0417.
Vu, T.T., Zhou, J., Leslie, B.A., Stafford, A.R., Fredenburgh, J.C., Ni, R., Qiao, S., Vaezzadeh, N., Jahnen-Dechent, W., Monia, B.P., Gross, P.L., Weitz, J.I., Arterial thrombosis is accelerated in mice deficient in histidine-rich glycoprotein. Blood 125 (2015), 2712–2719, 10.1182/blood-2014-11-611319.
Egli, M., Pallan, P.S., Crystallographic studies of chemically modified nucleic acids: a backward glance. Chem. Biodivers. 7 (2010), 60–89, 10.1002/cbdv.200900177.
Cai, T.Q., Wu, W., Shin, M.K., Xu, Y., Jochnowitz, N., Zhou, Y., Hoos, L., Bentley, R., Strapps, W., Thankappan, A., Metzger, J.M., Ogletree, M.L., Tadin-Strapps, M., Seiffert, D.A., Chen, Z., Factor XII full and partial null in rat confers robust antithrombotic efficacy with no bleeding. Blood Coagul. Fibrinolysis 26 (2015), 893–902, 10.1097/MBC.0000000000000337.
Heestermans, M., de Jong, A., van Tilburg, S., Reitsma, P.H., Versteeg, H.H., Spronk, H.M., van Vlijmen, B.J.M., Use of “C9/11 mismatch” Control small interfering RNA reveals sequence-related off-target effect on coagulation of an small interfering RNA targeting mouse coagulation factor XII. Nucleic Acid Therapeut. 29 (2019), 218–223, 10.1089/nat.2018.0767.
Heestermans, M., Salloum-Asfar, S., Salvatori, D., Laghmani, E.H., Luken, B.M., Zeerleder, S.S., Spronk, H.M.H., Korporaal, S.J., Wagenaar, G.T.M., Reitsma, P.H., van Vlijmen, B.J.M., Retraction note: role of platelets, neutrophils, and factor XII in spontaneous venous thrombosis in mice. Blood, 131, 2018, 2996, 10.1182/blood-2018-05-854596.
Li, Z., RNAi subcutaneous delivery platform development and ARO-F12. Asia TIDES, Kyoto, 2017.
Huang, Y., Preclinical and clinical Advances of GalNAc-decorated nucleic acid therapeutics. Mol. Ther. Nucleic Acids 6 (2017), 116–132, 10.1016/j.omtn.2016.12.003.
Melquist, S., Wakefield, D., Hamilton, H., Chu, Q., Almeida, A., Almeida, L., Walters, M., Montez, J., Hegge, J., Klein, J., Hazlett, C., Milarch, T., Bertin, S., Andersen, A., Doss, E., Schmidt, R., Goth, L., Ferger, S., Rozema, D., Hamilton, J., Lewis, D., Kanner, S., Targeting factor 12 (F12) with a novel RNAi delivery platform as a prophylactic treatment for hereditary angioedema (HAE). J. Allergy Clin. Immunol., 137, 2016, AB251, 10.1016/j.jaci.2015.12.905.
Turner, A.M., Stolk, J., Bals, R., Lickliter, J.D., Hamilton, J., Christianson, D.R., Given, B.D., Burdon, J.G., Loomba, R., Stoller, J.K., Teckman, J.H., Hepatic-targeted RNA interference provides robust and persistent knockdown of alpha-1 antitrypsin levels in ZZ patients. J. Hepatol. 69 (2018), 378–384, 10.1016/j.jhep.2018.03.012.
Melquist, S., Pei, T., Hamilton, H., Chu, Q., Schienebeck, C., Chapman, C., Hagen, C., Walters, M., Milarch, T., Trilling, Z., Andersen, A., Christensen, G., Casper, J., Klas, C., Hegge, J., Li, Z., Kanner, S., Factor XII RNAi-based therapeutic as a prophylactic anti-thrombotic therapy. Arterioscler. Thromb. Vasc. Biol., 37, 2017.
Arrowhead Pharmaceuticals. Pipeline - Arrowhead pharmaceuticals, inc. https://arrowheadpharma.com/pipeline/, 2019. (Accessed 3 July 2020)
Liu, J., Qin, J., Cooley, B.C., Akinc, A., Butler, J., Qin, J., Reduction of hepatic factor XII expression in mice by ALN-F12 inhibits thrombosis without increasing bleeding risk. ISTH, 2017.
Foster, D.J., Brown, C.R., Shaikh, S., Trapp, C., Schlegel, M.K., Qian, K., Sehgal, A., Rajeev, K.G., Jadhav, V., Manoharan, M., Kuchimanchi, S., Maier, M.A., Milstein, S., Advanced siRNA designs further improve in vivo performance of GalNAc-siRNA conjugates. Mol. Ther. 26 (2018), 708–717, 10.1016/j.ymthe.2017.12.021.
Mayer, G., The chemical biology of aptamers. Angew. Chem. Int. Ed. 48 (2009), 2672–2689, 10.1002/anie.200804643.
Wilson, C., Keefe, A.D., Building oligonucleotide therapeutics using non-natural chemistries. Curr. Opin. Chem. Biol. 10 (2006), 607–614, 10.1016/j.cbpa.2006.10.001.
Woodruff, R.S., Xu, Y., Layzer, J., Wu, W., Ogletree, M.L., Sullenger, B.A., Inhibiting the intrinsic pathway of coagulation with a factor XII-targeting RNA aptamer. J. Thromb. Haemostasis 11 (2013), 1364–1373, 10.1111/jth.12302.
Dausse, E., Da Rocha Gomes, S., Toulmé, J.J., Aptamers: a new class of oligonucleotides in the drug discovery pipeline?. Curr. Opin. Pharmacol. 9 (2009), 602–607, 10.1016/j.coph.2009.07.006.
Blind, M., Blank, M., Aptamer selection technology and recent Advances. Mol. Ther. Nucleic Acids, 4, 2015, e223, 10.1038/mtna.2014.74.
Kovacevic, K.D., Gilbert, J.C., Jilma, B., Pharmacokinetics, pharmacodynamics and safety of aptamers. Adv. Drug Deliv. Rev. 134 (2018), 36–50, 10.1016/j.addr.2018.10.008.
Liu, J.K.H., The history of monoclonal antibody development - progress, remaining challenges and future innovations. Ann. Med. Surg. 3 (2014), 113–116, 10.1016/j.amsu.2014.09.001.
Samoilovich, S.R., Dugan, C.B., Macario, A.J.L., Hybridoma technology: new developments of practical interest. J. Immunol. Methods 101 (1987), 153–170, 10.1016/0022-1759(87)90147-5.
Pixley, R.A., Stumpo, L.G., Birkmeyer, K., Silver, L., Colman, R.W., A monoclonal antibody recognizing an icosapeptide sequence in the heavy chain of human factor XII inhibits surface-catalyzed activation. J. Biol. Chem. 262 (1987), 10140–10145.
Small, E.J., Katzmann, J.A., Tracy, R.P., Ratnoff, O.D., Goldsmith, G.J., Everson, B., A monoclonal antibody that inhibits activation of human Hageman factor (factor XII). Blood 65 (1985), 202–210.
Saito, H., Ishihara, T., Suzuki, H., Watanabe, T., Production and characterization of a murine monoclonal antibody against a heavy chain of Hageman factor (factor XII). Blood 65 (1985), 1263–1268.
Nuijens, J.H., Hijbregts, C.C.M., Eerenberg-Belmer, A.J.M., Meijers, J.C.M., Bouma, B.N., Hack, C.E., Activation of the contact system of coagulation by a monoclonal antibody directed against a neodeterminant in the heavy chain region of human coagulation factor XII (Hageman factor). J. Biol. Chem. 264 (1989), 12941–12949.
Nuijens, J.H., Huijbregts, C., Hack, C.E., Inhibitors of Factor XII Activation and Applications Thereof. 1991 WO9117258.
Dors, D., Nuijens, J., Huijbregts, C., Hack, C., A novel sensitive assay for functional factor XII based on the generation of kallikrein-C1-lnhibitor complexes in factor xll-deficient plasma by glass-bound factor XII. Thromb. Haemost 67 (1992), 644–648, 10.1055/s-0038-1648516.
Pixley, R.A., Monoclonal Antibodies to the Light Chain Region of Human Factor XII and Methods of Preparing and Using the Same. 1989 WO8911865.
Matafonov, A., Gailani, A.E., Grach, S.L., Leung, P.Y., Cheng, Q., Geng, Y., McCarty, O.J.T., Tucker, E.I., Renne, T., Morrissey, J.H., Gruber, A., Gailani, D., Antibodies to human factor XII with antithrombotic properties. Blood, 120, 2012, 10.1182/blood.V120.21.1106.1106 1106–1106.
Kokoye, Y., Ivanov, I., Cheng, Q., Matafonov, A., Dickeson, S.K., Mason, S., Sexton, D.J., Renné, T., Mccrae, K., Feener, E.P., Gailani, D., A comparison of the effects of factor XII deficiency and prekallikrein deficiency on thrombus formation. Thromb. Res. 140 (2016), 118–124, 10.1016/j.thromres.2016.02.020.
Comeau, S.R., Nixon, A., Kastrapeli, N., Kenniston, J.A., Conley, G.P., Mason, S., Lindberg, A.P., Kopacz, K., Adelman, B., Bispecific Antibodies against Plasma Kallikrein and Factor XII. 2018 WO2016109774A1.
Kenniston, J.A., Faucette, R.R., Martik, D., Comeau, S.R., Lindberg, A.P., Kopacz, K.J., Conley, G.P., Chen, J., Viswanathan, M., Kastrapeli, N., Cosic, J., Mason, S., DiLeo, M., Abendroth, J., Kuzmic, P., Ladner, R.C., Edwards, T.E., TenHoor, C., Adelman, B.A., Nixon, A.E., Sexton, D.J., Inhibition of plasma kallikrein by a highly specific active site blocking antibody. J. Biol. Chem. 289 (2014), 23596–23608, 10.1074/jbc.M114.569061.
Clarke, B.J., Cote, H.C.F., Cool, D.E., Clark-Lewis, I., Saito, H., Pixley, R.A., Colman, R.W., MacGillivray, R.T.A., Mapping of a putative surface-binding site of human coagulation factor XII. J. Biol. Chem. 264 (1989), 11497–11502.
Worm, M., Köhler, E.C., Panda, R., Long, A., Butler, L.M., Stavrou, E.X., Nickel, K.F., Fuchs, T.A., Renné, T., The factor XIIa blocking antibody 3F7: a safe anticoagulant with anti-inflammatory activities. Ann. Transl. Med., 3, 2015, 247, 10.3978/j.issn.2305-5839.2015.09.07.
