Heparinoids Danaparoid and Sulodexide as clinically used drugs

Alaez-Verson, 2017, Heparin: new life for an old drug, Nanomedicine (Lond), 12, 1727, 10.2217/nnm-2017-0127 Torri, 2016, Heparin centenary—an ever-young life-saving drug, Int J Cardiol, 212, S1, 10.1016/S0167-5273(16)12001-7 Wardrop, 2008, The story of the discovery of heparin and warfarin, Br J Haematol, 141, 757, 10.1111/j.1365-2141.2008.07119.x Jaques, 1979, Heparins—anionic polyelectrolyte drugs, Pharmacol Rev, 31, 99 Zhang, 2010, Glycosaminoglycan (GAG) biosynthesis and GAG-binding proteins, Prog Mol Biol Transl Sci, 93, 1, 10.1016/S1877-1173(10)93001-9 Griffin, 1995, Isolation and characterization of heparan sulfate from crude porcine intestinal mucosal peptidoglycan heparin, Carbohydr Res, 276, 183, 10.1016/0008-6215(95)00166-Q Farrugia, 2015, Can we produce heparin/heparan sulfate biomimetics using “mother-nature” as the gold standard?, Molecules, 20, 4254, 10.3390/molecules20034254 Casu, 2001, Structure and biological interactions of heparin and heparan sulfate, Adv Carbohydr Chem Biochem, 57, 159, 10.1016/S0065-2318(01)57017-1 Mulloy, 2016, Pharmacology of heparin and related drugs, Pharmacol Rev, 68, 76, 10.1124/pr.115.011247 Schick, 2010, Serglycin proteoglycan deletion in mouse platelets: physiological effects and their implications for platelet contributions to thrombosis, inflammation, atherosclerosis, and metastasis, Prog Mol Biol Transl Sci, 93, 235, 10.1016/S1877-1173(10)93011-1 Saito, 2007, Analysis of plasma proteins that bind to glycosaminoglycans, Biochim Biophys Acta, 1770, 241, 10.1016/j.bbagen.2006.10.015 Ori, 2011, A systems biology approach for the investigation of the heparin/heparan sulfate interactome, J Biol Chem, 286, 19892, 10.1074/jbc.M111.228114 Peysselon, 2014, Heparin-protein interactions: from affinity and kinetics to biological roles. Application to an interaction network regulating angiogenesis, Matrix Biol, 35, 73, 10.1016/j.matbio.2013.11.001 Esko, 2015, Proteins that bind sulfated glycosaminoglycans, 493 Jones, 2011, Heparin characterization: challenges and solutions, Annu Rev Anal Chem (Palo Alto Calif), 4, 439, 10.1146/annurev-anchem-061010-113911 Rosenberg, 1975, Actions and interactions of antithrombin and heparin, N Engl J Med, 292, 146, 10.1056/NEJM197501162920307 Rosenberg, 1979, Highly active heparin species with multiple binding sites for antithrombin, Biochem Biophys Res Commun, 86, 1319, 10.1016/0006-291X(79)90260-2 Rosenberg, 1980, The interaction of heparin with thrombin and antithrombin, Biochem Biophys Res Commun, 96, 1200, 10.1016/0006-291X(80)90079-0 Rosenberg, 1985, Protease inhibitors of human plasma. Antithrombin-III. “The heparin-antithrombin system”, J Med, 16, 351 Rosenberg, 1973, The purification and mechanism of action of human antithrombin-heparin cofactor, J Biol Chem, 248, 6490, 10.1016/S0021-9258(19)43472-8 Lindahl, 1980, Evidence for a 3-O-sulfated D-glucosamine residue in the antithrombin-binding sequence of heparin, Proc Natl Acad Sci U S A, 77, 6551, 10.1073/pnas.77.11.6551 Onishi, 2016, Heparin and anticoagulation, Front Biosci (Landmark Ed), 21, 1372, 10.2741/4462 Yi, 2010, Oversulfated heparin by-products induce thrombin generation in human plasmas through contact system activation, Clin Appl Thromb Hemost, 16, 244, 10.1177/1076029610362071 Yi, 2010, Heparin and oversulfated heparin byproduct induce thrombin generation through contact system activation in plasma of patients with HIT, Clin Appl Thromb Hemost, 16, 251, 10.1177/1076029610362072 Gordts, 2018, The heparan sulfate proteoglycan grip on hyperlipidemia and atherosclerosis, Matrix Biol, 71–72, 262, 10.1016/j.matbio.2018.05.010 Esko, 1996, Influence of core protein sequence on glycosaminoglycan assembly, Curr Opin Struct Biol, 6, 663, 10.1016/S0959-440X(96)80034-0 Zhang, 1995, Repetitive Ser-Gly sequences enhance heparan sulfate assembly in proteoglycans, J Biol Chem, 270, 27127, 10.1074/jbc.270.45.27127 Zhang, 1994, Amino acid determinants that drive heparan sulfate assembly in a proteoglycan, J Biol Chem, 269, 19295, 10.1016/S0021-9258(17)32166-X Tollefsen, 2010, Vascular dermatan sulfate and heparin cofactor II, Prog Mol Biol Transl Sci, 93, 351, 10.1016/S1877-1173(10)93015-9 He, 2008, Vascular dermatan sulfate regulates the antithrombotic activity of heparin cofactor II, Blood, 111, 4118, 10.1182/blood-2007-12-127928 Giri, 2006, Placental dermatan sulfate: isolation, anticoagulant activity, and association with heparin cofactor II, Blood, 107, 2753, 10.1182/blood-2005-09-3755 Tollefsen, 1983, Activation of heparin cofactor II by dermatan sulfate, J Biol Chem, 258, 6713, 10.1016/S0021-9258(18)32276-2 Tollefsen, 1992, The interaction of glycosaminoglycans with heparin cofactor II: structure and activity of a high-affinity dermatan sulfate hexasaccharide, Adv Exp Med Biol, 313, 167, 10.1007/978-1-4899-2444-5_17 Tollefsen, 1984, Activation of heparin cofactor II by heparin and dermatan sulfate, Nouv Rev Fr Hematol, 26, 233 Maimone, 1991, Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity, J Biol Chem, 266, 14830, 10.1016/S0021-9258(18)98760-0 Vicente, 2004, Antithrombotic activity of dermatan sulfate in heparin cofactor II-deficient mice, Blood, 104, 3965, 10.1182/blood-2004-02-0598 Penc, 1998, Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function, J Biol Chem, 273, 28116, 10.1074/jbc.273.43.28116 Penc, 1999, Dermatan sulfate activates nuclear factor-kappab and induces endothelial and circulating intercellular adhesion molecule-1, J Clin Invest, 103, 1329, 10.1172/JCI4742 Margolis, 1997, Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding, Cell Tissue Res, 290, 343, 10.1007/s004410050939 Inatani, 2001, Inhibitory effects of neurocan and phosphacan on neurite outgrowth from retinal ganglion cells in culture, Invest Ophthalmol Vis Sci, 42, 1930 Renne, 2001, Cell surface-associated chondroitin sulfate proteoglycans bind contact phase factor H-kininogen, FEBS Lett, 500, 36, 10.1016/S0014-5793(01)02570-4 Kaplan, 2000, Macrophage plasma membrane chondroitin sulfate proteoglycan binds oxidized low-density lipoprotein, Atherosclerosis, 149, 5, 10.1016/S0021-9150(99)00287-7 Liu, 2009, Lessons learned from the contamination of heparin, Nat Prod Rep, 26, 313, 10.1039/b819896a Pan, 2010, Oversulfated chondroitin sulfate is not the sole contaminant in heparin, Nat Biotechnol, 28, 203, 10.1038/nbt0310-203 Pan, 2010, Identification of chemically sulfated/desulfated glycosaminoglycans in contaminated heparins and development of a simple assay for the detection of most contaminants in heparin, Glycobiol Insights, 2010, 1 Pan, 2010, Chemically oversulfated glycosaminoglycans are potent modulators of contact system activation and different cell signaling pathways, J Biol Chem, 285, 22966, 10.1074/jbc.M109.063735 van der Meer, 2017, From farm to pharma: an overview of industrial heparin manufacturing methods, Molecules, 22, 1025, 10.3390/molecules22061025 Guerrini, 2009, Orthogonal analytical approaches to detect potential contaminants in heparin, Proc Natl Acad Sci U S A, 106, 16956, 10.1073/pnas.0906861106 Yu, 2017, Surprising absence of heparin in the intestinal mucosa of baby pigs, Glycobiology, 27, 57, 10.1093/glycob/cww104 Schindewolf, 2007, Danaparoid in pregnancy in cases of heparin intolerance—use in 59 cases, Hamostaseologie, 27, 89 Meuleman, 1992, Orgaran (org 10172): its pharmacological profile in experimental models, Pathophysiol Haemost Thromb, 22, 58, 10.1159/000216296 Meuleman, 1982, A novel anti-thrombotic heparinoid (ORG 10172) devoid of bleeding inducing capacity: a survey of its pharmacological properties in experimental animal models, Thromb Res, 27, 353, 10.1016/0049-3848(82)90082-2 Nurmohamed, 1991, Pharmacological and clinical studies with lomoparan, a low molecular weight glycosaminoglycan, Semin Thromb Hemost, 17 Suppl 2, 205 de Valk, 1995, Comparing subcutaneous danaparoid with intravenous unfractionated heparin for the treatment of venous thromboembolism. a randomized controlled trial, Ann Intern Med, 123, 1, 10.7326/0003-4819-123-1-199507010-00001 Magnani, 2006, Heparin-induced thrombocytopenia (HIT)—a report of 1,478 clinical outcomes of patients treated with danaparoid (orgaran) from 1982 to mid-2004, Thromb Haemost, 95, 967, 10.1160/TH05-07-0489 Lauver, 2006, Sulodexide: a renewed interest in this glycosaminoglycan, Cardiovasc Drug Rev, 24, 214, 10.1111/j.1527-3466.2006.00214.x Ciszewicz, 2009, Sulodexide suppresses inflammation in human endothelial cells and prevents glucose cytotoxicity, Transl Res, 153, 118, 10.1016/j.trsl.2008.12.007 Lauver, 2005, Sulodexide attenuates myocardial ischemia/reperfusion injury and the deposition of C-reactive protein in areas of infarction without affecting hemostasis, J Pharmacol Exp Ther, 312, 794, 10.1124/jpet.104.075283 Ferdinando, 2014, Sulodexide down-regulates the release of cytokines, chemokines, and leukocyte colony stimulating factors from human macrophages: role of glycosaminoglycans in inflammatory pathways of chronic venous disease, Curr Vasc Pharmacol, 12, 173, 10.2174/1570161111666131126144025 Ahmed, 2007, Heparin induced thrombocytopenia: diagnosis and management update, Postgrad Med J, 83, 575, 10.1136/pgmj.2007.059188 Bakchoul, 2012, Recent advances in the diagnosis and treatment of heparin-induced thrombocytopenia, Ther Adv Hematol, 3, 237, 10.1177/2040620712443537 Qian, 2010, Molecular mechanism underlines heparin-induced thrombocytopenia and thrombosis, Prog Mol Biol Transl Sci, 93, 395, 10.1016/S1877-1173(10)93017-2 Weiser, 2010, Activated contact system and abnormal glycosaminoglycans in lupus and other auto- and non-autoimmune diseases, Prog Mol Biol Transl Sci, 93, 443, 10.1016/S1877-1173(10)93019-6 Amiral, 1992, Platelet factor 4 complexed to heparin is the target for antibodies generated in heparin-induced thrombocytopenia, Thromb Haemost, 68, 095, 10.1055/s-0038-1656329 Ibbotson, 2002, Danaparoid: a review of its use in thromboembolic and coagulation disorders, Drugs, 62, 2283, 10.2165/00003495-200262150-00016 Norbert, 2006, Results of a systematic evaluation of treatment outcomes for heparin-induced thrombocytopenia in patients receiving danaparoid, ancrod, and/or coumarin explain the rapid shift in clinical practice during the 1990s, Thromb Res, 117, 507, 10.1016/j.thromres.2005.04.011 Magnani, 1993, Heparin-induced thrombocytopenia (HIT): an overview of 230 patients treated with orgaran (org 10172), Thromb Haemost, 69, 554, 10.1055/s-0038-1649626 Chong, 1989, Heparin-induced thrombocytopenia: studies with a new low molecular weight heparinoid, org 10172, Blood, 73, 1592, 10.1182/blood.V73.6.1592.1592 Henny, 1985, The effectiveness of a low molecular weight heparinoid in chronic intermittent haemodialysis, Thromb Haemost, 53, 460, 10.1055/s-0038-1657872 Ireland, 1986, The anticoagulant effect of heparinoid org 10172 during haemodialysis: an objective assessment, Thromb Haemost, 55, 271, 10.1055/s-0038-1661535 Krystin, 2012, Heparin-induced thrombocytopenia: in vitro studies on the interaction of dabigatran, rivaroxaban, and low-sulfated heparin, with platelet factor 4 and anti-PF4/heparin antibodies, Blood, 119, 1248, 10.1182/blood-2011-05-353391 Kesieme, 2011, Deep vein thrombosis: a clinical review, J Blood Med, 2, 59, 10.2147/JBM.S19009 Ferri, 2017 A.D.A.M. Medical Encyclopedia, 2012 Boneu, 1985, Effects of heparin, its low molecular weight fractions and other glycosaminoglycans on thrombus growth in vivo, Thromb Res, 40, 81, 10.1016/0049-3848(85)90352-4 Gallus, 1993, Orgaran (org 10172) or heparin for preventing venous thrombosis after elective surgery for malignant disease? A double-blind, randomised, multicentre comparison. ANZ-Organon Investigators' Group, Thromb Haemost, 70, 562, 10.1055/s-0038-1649627 Bergqvist, 1991, Thromboprophylaxis in patients with hip fractures: a prospective, randomized, comparative study between org 10172 and dextran 70, Surgery, 109, 617 Hoek, 1992, Prevention of deep vein thrombosis following total hip replacement by low molecular weight heparinoid, Thromb Haemost, 67, 028, 10.1055/s-0038-1648374 Turpie, 1987, Double-blind randomised trial of org 10172 low-molecular-weight heparinoid in prevention of deep-vein thrombosis in thrombotic stroke, Lancet, 329, 523, 10.1016/S0140-6736(87)90173-5 Ten Cate, 2010, Use of a heparinoid in patients with hemorrhagic stroke and thromboembolic disease, Ann Neurol, 15, 268 Bratt, 1990, Two daily subcutaneous injections of fragmin as compared with intravenous standard heparin in the treatment of deep venous thrombosis (DVT), Thromb Haemost, 64, 506, 10.1055/s-0038-1647348 Lopaciuk, 1992, Subcutaneous low molecular weight heparin versus subcutaneous unfractionated heparin in the treatment of deep vein thrombosis: a Polish multicenter trial, Thromb Haemost, 68, 014, 10.1055/s-0038-1656309 Albada, 1989, Treatment of acute venous thromboembolism with low molecular weight heparin (Fragmin). results of a double-blind randomized study, Circulation, 80, 935, 10.1161/01.CIR.80.4.935 Prandoni, 1992, Comparison of subcutaneous low-molecular-weight heparin with intravenous standard heparin in proximal deep-vein thrombosis, Lancet, 339, 441, 10.1016/0140-6736(92)91054-C Hull, 1992, Subcutaneous low-molecular-weight heparin compared with continuous intravenous heparin in the treatment of proximal-vein thrombosis, J Vasc Surg, 18, 975 Levi, 1983, Disseminated intravascular coagulation, Ned Tijdschr Geneeskd, 22, 10 Levi, 2000, Disseminated intravascular coagulation, Ned Tijdschr Geneeskd, 144, 470 NHLBI/NIH Moake, 2017, Disseminated intravascular coagulation (DIC), The Merck Manual Kilgore, 1998, The semisynthetic polysaccharide pentosan polysulfate prevents complement-mediated myocardial injury in the rabbit perfused heart, J Pharmacol Exp Ther, 285, 987 Ontachi, 2005, Effect of combined therapy of danaparoid sodium and tranexamic acid on chronic disseminated intravascular coagulation associated with abdominal aortic aneurysm, Circ J, 69, 1150, 10.1253/circj.69.1150 Nieuwenhuis, 1986, Treatment of disseminated intravascular coagulation in acute promyelocytic leukemia with low molecular weight heparinoid org 10172, Cancer, 58, 761, 10.1002/1097-0142(19860801)58:3<761::AID-CNCR2820580325>3.0.CO;2-6 Coccheri, 2013, Development and use of sulodexide in vascular diseases: implications for treatment, Drug Des Devel Ther, 8, 49, 10.2147/DDDT.S6762 Baglin, 2002, Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism, Proc Natl Acad Sci U S A, 99, 11079, 10.1073/pnas.162232399 Corral, 2004, Homozygous deficiency of heparin cofactor II relevance of P17 glutamate residue in serpins, relationship with conformational diseases, and role in thrombosis, Circulation, 110, 1303, 10.1161/01.CIR.0000140763.51679.D9 Harper, 1991, Screening for heparin binding variants of antithrombin, J Clin Pathol, 44, 477, 10.1136/jcp.44.6.477 Huntington, 2001, The serpins: nature's molecular mousetraps, Sci Prog, 84, 125, 10.3184/003685001783239032 Silverman, 2001, The serpins are an expanding superfamily of structurally similar but functionally diverse proteins evolution, mechanism of inhibition, novel functions, and a revised nomenclature, J Biol Chem, 276, 33293, 10.1074/jbc.R100016200 Olson, 1992, Role of protein conformational changes, surface approximation and protein cofactors in heparin-accelerated antithrombin-proteinase reactions, Adv Exp Med Biol, 313, 155, 10.1007/978-1-4899-2444-5_16 Olson, 1992, Role of the antithrombin-binding pentasaccharide in heparin acceleration of antithrombin-proteinase reactions. Resolution of the antithrombin conformational change contribution to heparin rate enhancement, J Biol Chem, 267, 12528, 10.1016/S0021-9258(18)42309-5 Casu, 1991, Structural features and binding properties of chondroitin sulfates, dermatan sulfate, and heparan sulfate, Semin Thromb Hemost, 17 suppl 1, 9 Linhardt, 1991, Structural features of dermatan sulfates and their relationship to anticoagulant and antithrombotic activities, Biochem Pharmacol, 42, 1609, 10.1016/0006-2952(91)90431-4 Furie, 1992, Molecular and cellular biology of blood coagulation, N Engl J Med, 326, 800, 10.1056/NEJM199203193261205 Hoppensteadt, 2014, Pharmacological profile of sulodexide, Int Angiol, 33, 229 Roberto, 2009, Current management of intermittent claudication: the role of pharmacological and nonpharmacological symptom-directed therapies, Curr Vasc Pharmacol, 7, 394, 10.2174/157016109788340668 Karino, 1984, Flow through a venous valve and its implication for thrombus formation, Thromb Res, 36, 245, 10.1016/0049-3848(84)90224-X Nenci, 2002, Dermatan sulphate as an antithrombotic drug, Pathophysiol Haemost Thromb, 32, 303, 10.1159/000073586 Ciuffetti, 1989, Effects of 3-glucosaminoglycan sulfate on hemorheologic parameters in hyperlipidemic peripheral vascular disease (PVD) patients: a preliminary double-blind crossover study, Angiology, 40, 255, 10.1177/0003319789040004032 Radhakrishnamurthy, 1986, Studies of chemical and biologic properties of a fraction of sulodexide, a heparin-like glycosaminoglycan, Atherosclerosis, 60, 141, 10.1016/0021-9150(86)90006-7 Cristofori, 1985, Pharmacokinetics and distribution of a fluoresceinated glycosaminoglycan, sulodexide, in rats Part I: pharmacokinetics in rats, Arztl Forsch, 35, 1513 Ram, 2007, The role of sulodexide in the treatment of diabetic nephropathy, Drugs, 67, 2681, 10.2165/00003495-200767180-00004 Coccheri, 2002, Randomised, double blind, multicentre, placebo controlled study of sulodexide in the treatment of venous leg ulcers, Thromb Haemost, 87, 947, 10.1055/s-0037-1613116 Kilgore, 1994, The complement system in myocardial ischaemia/reperfusion injury, Cardiovasc Res, 28, 437, 10.1093/cvr/28.4.437 Carden, 2000, Pathophysiology of ischaemia-reperfusion injury, J Pathol, 190, 255, 10.1002/(SICI)1096-9896(200002)190:3<255::AID-PATH526>3.0.CO;2-6 Friedrichs, 1994, Effects of heparin and N-acetyl heparin on ischemia/reperfusion-induced alterations in myocardial function in the rabbit isolated heart, Circ Res, 75, 701, 10.1161/01.RES.75.4.701 Gralinski, 1996, Selective inhibition of the alternative complement pathway by sCR1[desLHR-a]protects the rabbit isolated heart from human complement-mediated damage, Immunopharmacology, 34, 79, 10.1016/0162-3109(96)00105-1 Lauver, 2004, Sulodexide attenuates myocardial ischemia/reperfusion injury and the deposition of C-reactive protein in areas of infarction without affecting hemostasis, J Pharmacol Exp Ther, 312, 794, 10.1124/jpet.104.075283 Rajtar, 1993, Effects of glycosaminoglycans on platelet and leucocyte function: role of N-sulfation, Biochem Pharmacol, 46, 958, 10.1016/0006-2952(93)90507-S Achour, 2005, One year course of oral sulodexide in the management of diabetic nephropathy, J Nephrol, 18, 568 Gambaro, 1994, Treatment with a glycosaminoglycan formulation ameliorates experimental diabetic nephropathy, Kidney Int, 46, 797, 10.1038/ki.1994.335 Radbill, 2008, Rationale and strategies for early detection and management of diabetic kidney disease, Mayo Clin Proc, 83, 1373, 10.4065/83.12.1373 Khosla, 2006, Lessons learned from recent hypertension trials about kidney disease, Clin J Am Soc Nephrol, 1, 229, 10.2215/CJN.00840805 Lopez-Otin, 2013, The hallmarks of aging, Cell, 153, 1194, 10.1016/j.cell.2013.05.039 Kennedy, 2014, Geroscience: linking aging to chronic disease, Cell, 159, 709, 10.1016/j.cell.2014.10.039 Pan, 2010, Glycosaminoglycans and activated contact system in cancer patient plasmas, Prog Mol Biol Transl Sci, 93, 473, 10.1016/S1877-1173(10)93020-2 Yagmurdur, 2003, Antiinflammatory action of heparin via the complement system in renal ischemia-reperfusion, Transplant Proc, 35, 2566, 10.1016/j.transproceed.2003.08.076 Calabrese, 2001, An active fraction of unfractionated heparin from a natural source is recognized by the first component of the complement system, Cell Mol Biol, 47 Calabrese, 1997, The first component of the human complement system recognizes the active fraction of heparin, Cell Mol Biol, 43, 237 Sahu, 1993, Identification of multiple sites of interaction between heparin and the complement system, Mol Immunol., 30, 679, 10.1016/0161-5890(93)90079-Q