Current structural biology of the heparin interactome

Current Opinion in Structural Biology

Volumn 34, Issue , 2015, Pages 17-25

  Pomin, Vitor H ^a   Mulloy, Barbara ^b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITHROMBIN; BACTERIAL PROTEIN; CELL PENETRATING PEPTIDE; CHEMOKINE; CYTOKINE; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; GLYCOSAMINOGLYCAN; HEMAGGLUTININ; HEPARIN; HEPARIN BINDING HEMAGGLUTININ; HEPARIN BINDING PROTEIN; MORPHOGEN; OLIGOSACCHARIDE; SERINE PROTEINASE; UNCLASSIFIED DRUG; BLOOD CLOTTING FACTOR; IMMUNOLOGIC FACTOR; LIGAND; PROTEIN AGGREGATE; PROTEIN BINDING;

ALLOSTERISM; BINDING SITE; BLOOD CLOTTING; CELL PROLIFERATION; COMPLEX FORMATION; HEPARIN INTERACTOME; HUMAN; IMMUNE RESPONSE; INFLAMMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN MOTIF; REVIEW; STRUCTURE ANALYSIS; WOUND; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; IMMUNOLOGY; METABOLISM; MOLECULAR MODEL; STRUCTURE ACTIVITY RELATION;

ANIMALS; BLOOD COAGULATION FACTORS; CELL PROLIFERATION; CELL-PENETRATING PEPTIDES; CHEMOKINES; CYTOKINES; HEPARIN; HUMANS; IMMUNOLOGIC FACTORS; INFLAMMATION; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR STRUCTURE; PROTEIN AGGREGATES; PROTEIN BINDING; RECEPTORS, FIBROBLAST GROWTH FACTOR; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84930677017     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.05.007     Document Type: Review

References (60)

1. Xu D., Esko J.D. Demystifying heparan sulfate-protein interactions. Annu Rev Biochem 2014, 83:129-157.
2. Ori A., Wilkinson M.C., Fernig D.G. A systems biology approach for the investigation of the heparin/heparan sulfate interactome. J Biol Chem 2011, 286:19892-19904.
3. Casu B., Naggi A., Torri G. Re-visiting the structure of heparin. Carbohydr Res 2014, 403C:60-68.
4. Santos G.R., Tovar A.M., Capillé N.V., Pereira M.S., Pomin V.H., Mourão P.A. Structural and functional analyses of bovine and porcine intestinal heparins confirm they are different drugs. Drug Discov Today 2014, 19:1801-1807.
5. Rivera C.G., Bader J.S., Popel A.S. Angiogenesis-associated crosstalk between collagens, CXC chemokines, and thrombosponding domain-containing proteins. Ann Biomed Eng 2011, 39:2213-2222.
6. Roper J.A., Williamson R.C., Bass M.D. Syndecan and integrin interactomes: large complexes in small spaces. Curr Opin Struct Biol 2012, 22:583-590.
7. Peyssel F., Ricard-Blum S. Heparin-protein interactions: from affinity and kinetics tobiological roles, Application to an interaction network regulating angiogenesis. Matrix Biol 2014, 35:73-81.
8. Spiller K.L., Nassiri S., Witherel C.E., Anfang R.R., Ng J., Nakazawa K.R., Yu T., Vunjak-Novakovic G. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds. Biomaterials 2015, 37:194-207.
9. Kufareva I., Salanga C.L., Handel T.M. Chemokine and chemokine receptor structure and interactions: implications for therapeutic strategies. Immunol Cell Biol 2015, 93:372-383.
10. Schlorke D., Thomas L., Samsonov A.S., Huster D., Arnhold J. The influence of glycosaminoglycans on IL-8-mediated functions of neutrophils. Carbohydr Res 2012, 356:196-203.
11. Möbius K., Nordsieck K., Pichert A., Samsonov S.A., Thomas L., Schiller J., Kalkhof S., Teresa Pisabarro M., Beck-Sickinger A.G., Huster D. Investigation of lysine side chain interactions of interleukin-8 with heparin and other glycosaminoglycans studied by a methylation-NMR approach. Glycobiology 2013, 23:1260-1269.
12. Seo Y., Andaya A., Bleiholder C., Leary J.A. Differentiation of CC vs CXC chemokine dimers with GAG octasaccharide binding partners: an ion mobility mass spectrometry approach. J Am Chem Soc 2013, 135:4325-4332.
13. Laguri C., Sapay N., Simorre J.P., Brutscher B., Imberty A., Gans P., Lortat-Jacob H. 13C-labeled heparan sulfate analogue as a tool to study protein/heparan sulfate interactions by NMR spectroscopy: application to the CXCL12α chemokine. J Am Chem Soc 2011, 133:9642-9645.
14. Ziarek J.J., Veldkamp C.T., Zhang F., Murray N.J., Kartz G.A., Liang X., Su J., Baker J.E., Linhardt R.J., Volkman B.F. Heparin oligosaccharides inhibit chemokine (CXC motif) ligand 12 (CXCL12) cardioprotection by binding orthogonal to the dimerization interface, promoting oligomerization, and competing with the chemokine (CXC motif) receptor 4 (CXCR4) N terminus. J Biol Chem 2013, 288:737-746.
15. Poluri K.M., Joseph P.R., Sawant K.V., Rajarathnam K. Molecular basis of glycosaminoglycan heparin binding to the chemokine CXCL1 dimer. J Biol Chem 2013, 288:25143-25153.
16. Severin I.C., Gaudry J.P., Johnson Z., Kungl A., Jansma A., Gesslbauer B., Mulloy B., Power C., Proudfoot A.E., Handel T. Characterization of the chemokine CXCL11-heparin interaction suggests two different affinities for glycosaminoglycans. J Biol Chem 2010, 285:17713-17724.
17. Saesen E., Sarrazin S., Laguri C., Sadir R., Maurin D., Thomas A., Imberty A., Lortat-Jacob H. Insights into the mechanism by which interferon-γ basic amino acid clusters mediate protein binding to heparan sulfate. J Am Chem Soc 2013, 135:9384-9390.
18. Künze G., Gehrcke J.P., Pisabarro M.T., Huster D. NMR characterization of the binding properties and conformation of glycosaminoglycans interacting with interleukin-10. Glycobiology 2014, 24:1036-1049.
19. Zhao B., LiWang P.J. Characterization of the interactions of vMIP-II, and a dimeric variant of vMIP-II, with glycosaminoglycans. Biochemistry 2010, 49:7012-7022.
20. Sadir R., Baleux F., Grosdiedier A., Imberty A., Lortat-Jacob H. Characterization of the stromal cell-derived factor-1α-heparin complex. J Biol Chem 2001, 276:8288-8296.
21. Amara A., Lorthioir O., Valenzuela A., Magerus A., Thelen M., Montes M., Virelizier J.L., Delepierre M., Baleux F., Lortat-Jacob H. Stromal cell-derived factor-1α associates with heparan sulfates though the first β-strand of the chemokine. J Biol Chem 1999, 274:23916-23925.
22. Sadir R., Imberty A., Baleux F., Lortat-Jacob H. Heparan sulfate/heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. J Biol Chem 2004, 279:43854-43860.
23. Murphy J.W., Cho Y., Sachpatzidis A., Fan C., Hodsdon M.E., Lolis E. Structural and functional basis of CXCL12 (stromal cell-derived factor-1α) binding to heparin. J Biol Chem 2007, 282:10018-10027.
24. Kurzbach D., Schwarz T.C., Platzer G., Höfler S., Hinderberger D., Konrat R. Compensatory adaptations of structural dynamics in an intriscially disordered protein complex. Angew Chem Int Ed 2014, 53:3840-3843.
25. Cress B.F., Englaender J.A., He W., Kasper D., Linhardt R.J., Koffas M.A. Masquerading microbial pathogens: capsular polysaccharides mimic host-tissue molecules. FEMS Microbiol Rev 2014, 38:660-697.
26. Blaum B.S., Deakin J.A., Johansson C.M., Herbert A.P., Barlow P.N., Lyon M., Uhrín D. Lysine and arginine side chains in glycosaminoglycan-protein complexes investigated by NMR, cross-linking, and mass spectrometry: a case study of the factor H-heparin interaction. J Am Chem Soc 2010, 132:6374-6381.
27. García-Mayoral M.F., Moussaoui M., de la Torre B.G., Andreu D., Boix E., Nogués M.V., Rico M., Laurents D.V., Bruix M. NMR structural determinants of eosinophil cationic protein binding to membrane and heparin mimetics. Biophys J 2010, 98:2702-2711.
28. García-Mayoral M.F., Canales A., Díaz D., López-Prados J., Moussaoui M., de Paz J.L., Angulo J., Nieto P.M., Jiménez-Barbero J., Boix E., Brunx M. Insights into the glycosaminoglycan-mediated cytotoxic mechanism of eosinophil cationic protein revealed by NMR. ACS Chem Biol 2013, 18:144-151.
29. Seo E.S., Blaum B.S., Vargues T., De Cecco M., Deakin J.A., Lyon M., Barran P.E., Campopiano D.J., Uhrín D. Interaction of human β-defensin 2 (HBD2) with glycosaminoglycans. Biochemistry 2010, 49:10486-10495.
30. de Paula V.S., Pomin V.H., Valente A.P. Unique properties of human β-defensin 6 (hBD6) and glycosaminoglycan complex: sandwich-like dimerization and competition with the chemokine receptor 2 (CCR2) binding site. J Biol Chem 2014, 289:22969-22979.
31. Chabrol E., Nurisso A., Daina A., Vassal-Stermann E., Thepaut M., Girard E., Vivès R.R., Fieschi F. Glycosaminoglycans are interactants of Langerin: comparison with gp120 highlights an unexpected calcium-independent binding mode. PLoS One 2012, 7:e50722.
32. Munoz-Garcia J.C., Chabrol E., Vives R.R., Thomas A., de Paz J.L., Rojo J., Imberty A., Fieschi F., Nieto P.M., Angulo J: Langerin-heparin interaction: two binding sites for small and large ligands as revealed by a combination of NMR spectroscopy and cross-linking mapping experiments. J Am Chem Soc 2015, 137:4100-4110.
33. Huntington J.A. Thrombin inhibition by the serpins. J Thromb Haemost 2013, 11:254-264.
34. Guerrini M., Elli S., Mourier P., Rudd T.R., Gaudesi D., Casu B., Boudier C., Torri G., Viskov C. An unusual antithrombin-binding heparin octasaccharide with an additional 3-O-sulfated glucosamine in the active pentasaccharide sequence. Biochem J 2013, 449:343-351.
35. Viskov C., Elli S., Urso E., Gaudesi D., Mourier P., Herman F., Boudier C., Casu B., Torri G., Guerrini M. Heparin dodecasaccharide containing two antithrombin-binding pentasaccharides: structural features and biological properties. J Biol Chem 2013, 288:25895-25907.
36. Dementiev A., Swanson R., Roth R., Isetti G., Izaguirre G., Olson S.T., Gettins P.G. The allosteric mechanism of activation of antithrombin as an inhibitor of factor IXa and factor Xa: heparin-independent full activation through mutations adjacent to helix D. J Biol Chem 2013, 288:33611-33619.
37. Brown A., Robinson C.J., Gallagher J.T., Blundell T.L. Cooperative heparin-mediated oligomerization of fibroblast growth factor-1 (FGF1) precedes recruitment of FGFR2 to ternary complexes. Biophys J 2013, 104:1720-1730.
38. Mohammadi M., Olsen S.K., Goetz R. A protein canyon in the FGF-FGF receptor dimer selects from an à la carte menu of heparan sulfate motifs. Curr Opin Struct Biol 2005, 15:506-516.
39. Xu Y., Cai C., Chandarajoti K., Hsieh P.H., Li L., Pham T.Q., Sparkenbaugh E.M., Sheng J., Key N.S., Pawlinski R., et al. Homogeneous low-molecular-weight heparins with reversible anticoagulant activity. Nat Chem Biol 2014, 10:248-250.
40. Liu J., Linhardt R.J. Chemoenzymatic synthesis of heparan sulfate and heparin. Nat Prod Rep 2014, 31:1676-1685.
41. Zulueta M.M., Lin S.Y., Hu Y.P., Hung S.C. Synthetic heparin and heparan sulfate oligosaccharides and their protein interactions. Curr Opin Chem Biol 2013, 17:1023-1029.
42. Hu Y.P., Zhong Y.Q., Chen Z.G., Chen C.Y., Shi Z., Zulueta M.M., Ku C.C., Lee P.Y., Wang C.C., Hung S.C. Divergent synthesis of 48 heparan sulfate-based disaccharides and probing the specific sugar-fibroblast growth factor-1 interaction. J Am Chem Soc 2012, 134:20722-20727.
43. Li Y.C., Ho I.H., Ku C.C., Zhong Y.Q., Hu Y.P., Chen Z.G., Chen C.Y., Lin W.C., Zulueta M.M., Hung S.C., et al. Interactions that influence the binding of synthetic heparan sulfate based disaccharides to fibroblast growth factor-2. Chem Biol 2014, 9:1712-1717.
44. Yu F., Roy S., Arevalo E., Schaeck J., Wang J., Holte K., Duffner J., Gunay N.S., Capila I., Kaundinya G.V. Characterization of heparin-protein interaction by saturation transfer difference (STD) NMR. Anal Bioanal Chem 2014, 406:3079-3089.
45. Muñoz-García J.C., Solera C., Carrero P., de Paz J.L., Angulo J., Nieto P.M. 3D structure of a heparin mimetic analogue of a FGF-1 activator. A NMR and molecular modelling study. Org Biomol Chem 2013, 11:8269-8275.
46. Muñoz-García J.C., Garcia-Jimenez M.J., Carrero P., Canales A., Jiménez-Barbero J., Martin-Lomas M., Imberty A., De Paz J.L., Angulo J., Lortat-Jacob H., Nieto P.M. Importance of the polarity of the glycosaminoglycan chain on the interaction with FGF-1. Glycobiology 2014, 24:1004-1009.
47. Thacker B.E., Xu D., Lawrence R., Esko J.D. Heparan sulfate 3-O-sulfation: a rare modification in search of a function. Matrix Biol 2014, 35:60-72.
48. Nieto L., Canales Á., Giménez-Gallego G., Nieto P.M., Jiménez-Barbero J. Conformational selection of the AGA*IA(M) heparin pentasaccharide when bound to the fibroblast growth factor receptor. Chemistry 2011, 17:11204-11209.
49. Nieto L., Canales Á., Fernández I.S., Santillana E., González-Corrochano R., Redondo-Horcajo M., Cañada F.J., Nieto P., Martín-Lomas M., Giménez-Gallego G., Jiménez-Barbero J. Heparin modulates the mitogenic activity of fibroblast growth factor by inducing dimerization of its receptor. A 3D view by using NMR. Chembiochem 2013, 14. 1732-1444.
50. Platonova N., Miquel G., Chiu L.Y., Taouji S., Moroni E., Colombo G., Chevet E., Sue S.C., Bikfalvi A. Dimerization capacities of FGF2 purified with or without heparin-affinity chromatography. PLoS One 2014, 9:e110055.
51. Whalen D.M., Malinauskas T., Gilbert R.J.C., Siebold C. Structural insights into proteoglycan-shaped Hedgehog signalling. Proc Natl Acad Sci 2013, 110:16420-16425.
52. Lim J., Yao S., Graf M., Winkler C., Yang D. Structure-function analysis of full-length midkine reveals novel residues important for heparin binding and zebrafish embryogenesis. Biochem J 2013, 451:407-415.
53. Madine J., Pandya M.J., Hicks M.R., Rodger A., Yates E.A., Radford S.E., Middleton D.A. Site-specific identification of an aβ fibril-heparin interaction site by using solid-state NMR spectroscopy. Angew Chem Int Ed Engl 2012, 51:13140-13143.
54. Vieira T.C., Reynaldo D.P., Gomes M.P., Almeida M.S., Cordeiro Y., Silva J.L. Heparin binding by murine recombinant prion protein leads to transient aggregation and formation of RNA-resistant species. J Am Chem Soc 2011, 133:334-344.
55. Ellett LJ, Coleman BM, Shambrook MC, Johanssen VA, Collins SJ, Masters CL, Hill AF, Lawson VA: Glycosaminoglycan sulfation determines the biochemical properties of prion protein aggregates. Glycobiology 2015, in press.
56. Wang X. Solution structure of decorin-binding protein A from Borrelia burgdorferi. Biochemistry 2012, 51:8353-8362.
57. Morgan A., Wang X. The novel heparin-binding motif in decorin-binding protein A from strain B31 of Borrelia burgdorferi explains the higher binding affinity. Biochemistry 2013, 52:8237-8245.
58. Lebrun P., Raze D., Fritzinger B., Wieruszeski J.M., Biet F., Dose A., Carpentier M., Schwarzer D., Allain F., Lippens G., Locht C. Differential contribution of the repeats to heparin binding of HBHA, a major adhesin of Mycobacterium tuberculosis. PLoS One 2012, 7:e32421.
59. Bechara C., Pallerla M., Zaltsman Y., Burlina F., Alves I.D., Lequin O., Sagan S. Tryptophan within basic peptide sequences triggers glycosaminoglycan-dependent endocytosis. FASEB J 2013, 27:738-749.
60. 0 conformations of a bioactive heparin-like hexasaccharide. J Am Chem Soc 2005, 127:5778-5779.