Thromb Haemost 2020; 120(10): 1347-1350
DOI: 10.1055/s-0040-1716543
Invited Editorial Focus

The Multiple Faces of Heparin: Opportunities in COVID-19 Infection and Beyond

Ludovic Drouet
1   CREATIF (Centre de Référence et d'Éducation aux AntiThrombotiques d'Île de France), Cardiology Department, Hôpital Lariboisiere, Paris, France
2   Department of Vascular Medicine, Paris Saint Joseph Hospital, Paris, France
,
Job Harenberg
3   DOASENSE GmbH, Heidelberg, Germany
4   Medical Faculty Mannheim, Ruprecht-Karls-University, Heidelberg, Germany
,
Giangiacomo Torri
5   Istituto di Ricerche Chimiche e Biochimiche G. Ronzoni, Milan, Italy
› Author Affiliations

The Anticoagulant and Nonanticoagulant Properties of Heparin



Publication History

Received: 11 August 2020

Accepted: 11 August 2020

Article published online:
13 September 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Stuttgart · New York

 
  • References

  • 1 Lindahl U, Li J-P. Heparanase - discovery and targets. Adv Exp Med Biol 2020; 1221: 61-69
  • 2 Mulloy B, Hogwood J, Gray E, Lever R, Page CP. Pharmacology of heparin and related drugs. Pharmacol Rev 2016; 68 (01) 76-141
  • 3 Beurskens DMH, Huckriede JP, Schrijver R. et al The anticoagulant and nonanticoagulant properties of heparin. Thromb Haemost 2020; 120 (10) 1371-1383
  • 4 Rudd TR, Skidmore MA, Guimond SE. et al Glycosaminoglycan origin and structure revealed by multivariate analysis of NMR and CD spectra. Glycobiology 2009; 19 (01) 52-67
  • 5 Naggi A, Gardini C, Pedrinola G. et al Structural peculiarity and antithrombin binding region profile of mucosal bovine and porcine heparins. J Pharm Biomed Anal 2016; 118: 52-63
  • 6 Mourier PAJ, Guichard OY, Herman F. et al New insights in thrombin inhibition structure-activity relationships by characterization of octadecasaccharides from low molecular weight heparin. Molecules 2017; 22 (03) 428
  • 7 Cassinelli G, Torri G, Naggi A. Non-anticoagulant heparins as heparanase inhibitors. Adv Exp Med Biol 2020; 1221: 493-522
  • 8 Huang C, Wang Y, Li X. et al Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395 (10223): 497-506
  • 9 Guan W-J, Ni Z-Y, Hu Y. , et al; China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020; 382 (18) 1708-1720
  • 10 Bikdeli B, Madhavan MV, Gupta A. , et al; Global COVID-19 Thrombosis Collaborative Group. Pharmacological agents targeting thromboinflammation in COVID-19: review and implications for future research. Thromb Haemost 2020; 120 (07) 1004-1024
  • 11 Violi F, Pastori D, Cangemi R. et al Hypercoagulation and antithrombotic treatment in coronavirus 2019: a new challenge. Thromb Haemost 2020; 120 (06) 949-956
  • 12 Paolisso P, Bergamaschi L, D'Angelo EC. et al Preliminary experience with low molecular weight heparin strategy in COVID-19 patients. JACC Cardiovasc Imaging 2020; DOI: 10.1016/j.jcmg.2020.03.021.
  • 13 Clausen TM, Sandoval DR, Spliid CB. et al SARS-CoV-2 infection depends on cellular heparan sulfate and ACE2. bioRxiv 2020; DOI: 10.1101/2020.07.14.201616.
  • 14 Mycroft-West CJ, Su D, Elli S. et al The 2019 coronavirus (SARS-CoV-2) surface protein (Spike) S1 receptor binding domain undergoes conformational change upon heparin binding. bioRxiv 2020; DOI: 10.1101/2020.02.29.971093.
  • 15 Du L, He Y, Zhou Y. et al The spike protein of SARS-CoV--a target for vaccine and therapeutic development. Nat Rev Microbiol 2009; 7 (03) 226-236
  • 16 de Bont CM, Boelens WC, Pruijn GJM. NETosis, complement, and coagulation: a triangular relationship. Cell Mol Immunol 2019; 16 (01) 19-27
  • 17 Bal Dit Sollier C, Berge N, Drouet L. Enoxaparin chains stored during chronic treatment are mobilized by a bolus of unfractionated heparin: insights from the STACKENOX study. Blood Coagul Fibrinolysis 2016; 27 (07) 779-785
  • 18 Nelson A, Berkestedt I, Schmidtchen A. et al Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma. Shock 2008; 30 (06) 623-627
  • 19 Floer M, Götte M, Wild MK. et al Enoxaparin improves the course of dextran sodium sulfate-induced colitis in syndecan-1-deficient mice. Am J Pathol 2010; 176 (01) 146-157
  • 20 Lipowsky HH, Lescanic A. Inhibition of inflammation induced shedding of the endothelial glycocalyx with low molecular weight heparin. Microvasc Res 2017; 112: 72-78
  • 21 Varga Z, Flammer AJ, Steiger P. et al Endothelial cell infection and endotheliitis in COVID-19. Lancet 2020; 395 (10234): 1417-1418
  • 22 Lax SF, Skok K, Zechner P. et al Pulmonary arterial thrombosis in COVID-19 with fatal outcome: results from a prospective, single-center, clinicopathologic case series. Ann Intern Med 2020; M20-M2566 . Doi: 10.7326/M20-2566
  • 23 Harenberg J, Jonas JB, Trecca EMC. A liaison between sudden sensorineural hearing loss and SARS-CoV-2 infection. Thromb Haemost 2020; 120 (09) 1237-1239
  • 24 Harenberg J, Casu B. Heparin and its derivatives - present and future. Thromb Haemost 2009; 102 (05) 801-803
  • 25 Harenberg J, Casu B, Krämer R. et al Glycosaminoglycans: anticoagulant and nonanticoagulant actions: a short history of symposia held at villa vigoni. Semin Thromb Hemost 2014; 40 (08) 831-836
  • 26 Lip GYH, Collet JP, de Caterina R. et al Antithrombotic therapy in atrial fibrillation associated with valvular heart disease: executive summary of a joint consensus document from the European heart rhythm association (EHRA) and European Society of Cardiology Working Group on thrombosis, endorsed by the ESC Working Group on Valvular Heart Disease, Cardiac Arrhythmia Society of Southern Africa (CASSA), Heart Rhythm Society (HRS), Asia Pacific Heart Rhythm Society (APHRS), South African Heart (SA Heart) Association and Sociedad Latinoamericana de Estimulación Cardíaca y Electrofisiología (SOLEACE). Thromb Haemost 2017; 117 (12) 2215-2236
  • 27 Refaai MA, Shah V, Fernando R. Performance of the micro INR point-of-care system: a multicenter clinical trial. Thromb Haemost 2020; 120 (04) 687-691
  • 28 Harenberg J, Beyer-Westendorf J, Crowther M. , et al; Working Group Members. Accuracy of a rapid diagnostic test for the presence of direct oral factor Xa or thrombin inhibitors in urine - a multicenter trial. Thromb Haemost 2020; 120 (01) 132-140
  • 29 Testa S, Paoletti O, Giorgi-Pierfranceschi M. et al Switch from oral anticoagulants to parenteral heparin in SARS-CoV-2 hospitalized patients. Intern Emerg Med 2020; 15 (05) 751-753