The C-terminal fragment of axon guidance molecule Slit3 binds heparin and neutralizes heparin's anticoagulant activity

Glycobiology

Volumn 22, Issue 9, 2012, Pages 1183-1192

  Condac, Eduard ^a   Strachan, Heather ^a   Gutierrez Sanchez, Gerardo ^a   Brainard, Benjamin ^a   Giese, Christina ^b   Heiss, Christian ^a   Johnson, Darryl ^a   Azadi, Parastoo ^a   Bergmann, Carl ^a   Orlando, Ron ^a   Esmon, Charles T ^c   Harenberg, Job ^b   Moremen, Kelley ^a   Wang, Lianchun ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

anticoagulation; antithrombin; heparin; neutralization; Slit3

Indexed keywords

ANTITHROMBIN; BLOOD CLOTTING FACTOR 10A; DRUG BINDING PROTEIN; FONDAPARINUX; HEPARAN SULFATE; PROTHROMBIN A; SLIT3 PROTEIN; UNCLASSIFIED DRUG;

ANTICOAGULATION; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; DRUG PROTEIN BINDING; HUMAN; PRIORITY JOURNAL; THROMBOELASTOGRAPHY;

AMINO ACID SEQUENCE; ANTICOAGULANTS; ANTITHROMBIN III; BINDING SITES; BLOOD COAGULATION; FACTOR XA; HEPARIN; HEPARIN ANTAGONISTS; HEPARIN, LOW-MOLECULAR-WEIGHT; HEPARITIN SULFATE; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTHROMBIN; RECOMBINANT PROTEINS; SOLUTIONS; THROMBELASTOGRAPHY;

EID: 84864472701     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws087     Document Type: Article

References (48)

1. Amara A, Lorthioir O, Valenzuela A, Magerus A, Thelen M, Montes M, Virelizier JL, Delepierre M, Baleux F, Lortat-Jacob H, et al. 1999. Stromal cell-derived factor-1alpha associates with heparan sulfates through the first beta-strand of the chemokine. J Biol Chem. 274:23916-23925.
2. Bishop JR, Schuksz M, Esko JD. 2007. Heparan sulphate proteoglycans finetune mammalian physiology. Nature. 446:1030-1037.
3. Björk I, Lindahl U. 1982. Mechanism of the anticoagulant action of heparin. Mol Cell Biochem. 48:161-182.
4. Bolliger D, Seeberger MD, Tanaka KA. 2012. Principles and practice of thromboelastography in clinical coagulation management and transfusion practice. Transfus Med Rev. 26:1-13.
5. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T. 1999. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell. 96:795-806.
6. Capila I, Linhardt RJ. 2002. Heparin-protein interactions. Angew Chem Int Ed Engl. 41:391-412.
7. Conrad HE. 1998. Heparin-Binding Proteins. San Diego: Academic Press.
8. Crowther MA, Warkentin TE. 2008. Bleeding risk and the management of bleeding complications in patients undergoing anticoagulant therapy: Focus on new anticoagulant agents. Blood. 111:4871-4879.
9. Esko JD, Kimata K, Lindahl U. 2009. Proteoglycans and sulfated glycosaminoglycans. In: Varki A, Cummings RD, et al. editors. Essentials of Glycobiology, 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press. P. 229-248.
10. Fuster MM, Wang L. 2010. Endothelial heparan sulfate in angiogenesis. Prog Mol Biol Transl Sci. 93:179-212.
11. Geutskens SB, Hordijk PL, van Hennik PB. 2010. The chemorepellent Slit3 promotes monocyte migration. J Immunol. 185:7691-7698.
12. Hohenester E. 2008. Structural insight into Slit-Robo signalling. Biochem Soc Trans. 36:251-256.
13. Howitt JA, Clout NJ, Hohenester E. 2004. Binding site for Robo receptors revealed by dissection of the leucine-rich repeat region of Slit. EMBO J. 23:4406-4412.
14. Hu H. 2001. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat Neurosci. 4:695-701.
15. Hussain SA, Piper M, Fukuhara N, Strochlic L, Cho G, Howitt JA, Ahmed Y, Powell AK, Turnbull JE, Holt CE, et al. 2006. A molecular mechanism for the heparan sulfate dependence of Slit-robo signaling. J Biol Chem. 281:39693-39698.
16. Itoh A, Miyabayashi T, Ohno M, Sakano S. 1998. Cloning and expressions of three mammalian homologues of Drosophila Slit suggest possible roles for Slit in the formation and maintenance of the nervous system. Brain Res Mol Brain Res. 62:175-186.
17. Jones CA, London NR, Chen H, Park KW, Sauvaget D, Stockton RA, Wythe JD, Suh W, Larrieu-Lahargue F, Mukouyama YS, et al. 2008. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med. 14:448-453.
18. Kessler CM. 2004. Current and future challenges of antithrombotic agents and anticoagulants: Strategies for reversal of hemorrhagic complications. Semin Hematol. 41:44-50.
19. Lane DA, Denton J, Flynn AM, Thunberg L, Lindahl U. 1984. Anticoagulant activities of heparin oligosaccharides and their neutralization by platelet factor 4. Biochem J. 218:725-732.
20. Li XA, Hatanaka K, Guo L, Kitamura Y, Yamamoto A. 1994. Binding of serum amyloid P component to heparin in human serum. Biochim Biophys Acta. 1201:143-148.
21. Lindahl U, Backstrom G, Hook M, Thunberg L, Fransson LA, Linker A. 1979. Structure of the antithrombin-binding site in heparin. Proc Natl Acad Sci USA. 76:3198-3202.
22. Liu Z, Patel K, Schmidt H, Andrews W, Pini A, Sundaresan V. 2004. Extracellular Ig domains 1 and 2 of Robo are important for ligand (Slit) binding. Mol Cell Neurosci. 26:232-240.
23. Liu J, Zhang L, Wang D, Shen H, Jiang M, Mei P, Hayden PS, Sedor JR, Hu H. 2003. Congenital diaphragmatic hernia, kidney agenesis and cardiac defects associated with Slit3-deficiency in mice. Mech Dev. 120:1059-1070.
24. Maccarana M, Casu B, Lindahl U. 1993. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J Biol Chem. 268:23898-23905.
25. Maccarana M, Lindahl U. 1993. Mode of interaction between platelet factor 4 and heparin. Glycobiology. 3:271-277.
26. Morlot C, Thielens NM, Ravelli RB, Hemrika W, Romijn RA, Gros P, Cusack S, McCarthy AA. 2007. Structural insights into the Slit-Robo complex. Proc Natl Acad Sci USA. 104:14923-14928.
27. Nybo M, Madsen JS. 2008. Serious anaphylactic reactions due to protamine sulfate: A systematic literature review. Basic Clin Pharmacol Toxicol. 103:192-196.
28. Ogamo A, Nagai A, Nagasawa K. 1985. Binding of heparin fractions and other polysulfated polysaccharides to plasma fibronectin: Effects of molecular size and degree of sulfation of polysaccharides. Biochim Biophys Acta Gen Subj. 841:30-41.
29. Osmond RI, Kett WC, Skett SE, Coombe DR. 2002. Protein-heparin interactions measured by BIAcore 2000 are affected by the method of heparin immobilization. Anal Biochem. 310:199-207.
30. Patel K, Nash JA, Itoh A, Liu Z, Sundaresan V, Pini A. 2001. Slit proteins are not dominant chemorepellents for olfactory tract and spinal motor axons. Development. 128:5031-5037.
31. Petitou M, Casu B, Lindahl U. 2003. 1976-1983, a critical period in the history of heparin: The discovery of the antithrombin binding site. Biochimie. 85:83-89.
32. Pittman JR, Koenig A, Brainard BM. 2010. The effect of unfractionated heparin on thromboelastographic analysis in healthy dogs. J Vet Emerg Crit Care. 20:216-223.
33. Rezaie AR, Esmon CT. 1992. The function of calcium in protein-C activation by thrombin and the thrombin-thrombomodulin complex can be distinguished by mutational analysis of protein-C derivatives. J Biol Chem. 267:26104-26109.
34. Rice KG, Kim YS, Grant AC, Merchant ZM, Linhardt RJ. 1985. High-performance liquid chromatographic separation of heparin-derived oligosaccharides. Anal Biochem. 150:325-331.
35. Robinson CJ, Mulloy B, Gallagher JT, Stringer SE. 2006. VEGF165-binding sites within heparan sulfate encompass two highly sulfated domains and can be liberated by K5 lyase. J Biol Chem. 281:1731-1740.
36. Ronca F, Andersen JS, Paech V, Margolis RU. 2001. Characterization of Slit protein interactions with glypican-1. J Biol Chem. 276: 29141-29147.
37. Rosenberg RD, Damus PS. 1973. The purification and mechanism of action of human antithrombin-heparin cofactor. J Biol Chem. 248:6490-6505.
38. Rosenberg RD, Rosenberg JS. 1984. Natural anticoagulant mechanisms. J Clin Invest. 74:1-6.
39. Rothberg JM, Artavanis-Tsakonas S. 1992. Modularity of the Slit protein: Characterization of a conserved carboxy-terminal sequence in secreted proteins and a motif implicated in extracellular protein interactions. J Mol Biol. 227:367-370.
40. Rothberg JM, Jacobs JR, Goodman CS, Artavanis-Tsakonas S. 1990. Slit: An extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4:2169-2187.
41. Schuksz M, Fuster MM, Brown JR, Crawford BE, Ditto DP, Lawrence R, Glass CA, Wang L, Tor Y, Esko JD. 2008. Surfen, a small molecule antagonist of heparan sulfate. Proc Natl Acad Sci USA. 105: 13075-13080.
42. van Geffen M, van Heerde WL. 2012. Global haemostasis assays, from bench to bedside. Thromb Res. 129:681-687.
43. Wang L, Brown JR, Varki A, Esko JD. 2002. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L-and P-selectins. J Clin Invest. 110:127-136.
44. Williams EC, Huppert BJ, Asakura S. 1992. Neutralization of the anticoagulant effects of glycosaminoglycans by serum amyloid P component: Comparison with other plasma and platelet proteins. J Lab Clin Med. 120:159-167.
45. Yuan W, Rao Y, Babiuk RP, Greer JJ, Wu JY, Ornitz DM. 2003. A genetic model for a central (septum transversum) congenital diaphragmatic hernia in mice lacking Slit3. Proc Natl Acad Sci USA. 100:5217-5222.
46. Zhang S, Condac E, Geng JG, Bicknell R, Esko JD, Wang L. Heparin-induced leukocytosis requires 6-O-sulfation and is caused by blockade of selectin-and CXCL12-mediated leukocyte trafficking in mice. J Biol Chem.
47. Zhang B, Dietrich UM, Linhardt RJ, Margolis RU. 2009. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood. 114:4300-4309.
48. Zhang F, Ronca F, Qiu H, Jiang J, Gutierrez-Sanchez G, Bergmann C, Handel T, Wang L. 2004. Structural determinants of heparan sulfate interactions with Slit proteins. Biochem Biophys Res Commun. 317:352-357.