Well-defined biomimetic surfaces to characterize glycosaminoglycan-mediated interactions on the molecular, supramolecular and cellular levels

Biomaterials

Volumn 35, Issue 32, 2014, Pages 8903-8915

  Migliorini, Elisa ^a,b   Thakar, Dhruv ^a,b   Sadir, Rabia ^a,c,d   Pleiner, Tino ^e   Baleux, Françoise ^f   Lortat Jacob, Hugues ^a,c,d   Coche Guerente, Liliane ^a,b   Richter, Ralf P ^a,b,g,h  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d CEA GRENOBLE   (France)

^e MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^f INSTITUT PASTEUR   (France)

^g CIC BIOMAGUNE   (Spain)

^h MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

Author keywords

Chemokine; Glycosaminoglycan; Quartz crystal microbalance; Spectroscopic ellipsometry; Surface plasmon resonance; T lymphocyte adhesion

Indexed keywords

CELL ADHESION; CELL MEMBRANES; MOLECULAR ORIENTATION; PROTEINS; QUARTZ CRYSTAL MICROBALANCES; SPECTROSCOPIC ELLIPSOMETRY; SUPRAMOLECULAR CHEMISTRY; SURFACE PLASMON RESONANCE; T-CELLS;

CELL MATRIX INTERACTIONS; CELLULAR INTERACTION; CHEMOKINES; EXTRACELLULAR MATRICES; GLYCOSAMINOGLYCANS; INTERCELLULAR ADHESION MOLECULE-1; NON-SPECIFIC BINDING; SURFACE BIOFUNCTIONALIZATION;

LIGANDS;

GLYCOSAMINOGLYCAN; HEPARAN SULFATE; INTERCELLULAR ADHESION MOLECULE 1; STREPTAVIDIN; STROMAL CELL DERIVED FACTOR 1; BOVINE SERUM ALBUMIN; FIBRONECTIN; LIGAND; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; BIOMIMETICS; CELL ADHESION; CELL INTERACTION; ELLIPSOMETRY; ENZYME IMMOBILIZATION; IN VITRO STUDY; JURKAT CELL LINE; LIPID BILAYER; PRIORITY JOURNAL; QUARTZ CRYSTAL MICROBALANCE; SURFACE PLASMON RESONANCE; T LYMPHOCYTE; BIOTINYLATION; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; EXTRACELLULAR MATRIX; HUMAN; PROCEDURES; SURFACE PROPERTY;

BIOMIMETICS; BIOTINYLATION; CELL ADHESION; CELL MEMBRANE; CHEMOKINE CXCL12; EXTRACELLULAR MATRIX; FIBRONECTINS; GLYCOSAMINOGLYCANS; HEPARITIN SULFATE; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; JURKAT CELLS; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; RECOMBINANT PROTEINS; SERUM ALBUMIN, BOVINE; STREPTAVIDIN; SURFACE PLASMON RESONANCE; SURFACE PROPERTIES; T-LYMPHOCYTES;

EID: 84905723835     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.07.017     Document Type: Article

References (69)

1. Bernfield M., Götte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 1999, 68:729-777.
2. Cain S.A., Baldock C., Gallagher J., Morgan A., Bax D.V., Weiss A.S., et al. Fibrillin-1 interactions with heparin. Implications for microfibril and elastic fiber assembly. JBiol Chem 2005, 280:30526-30537.
3. Cain S.A., Baldwin A.K., Mahalingam Y., Raynal B., Jowitt T.A., Shuttleworth C.A., et al. Heparan sulfate regulates fibrillin-1 N- and C-terminal interactions. JBiol Chem 2008, 283:27017-27027.
4. Baranova N.S., Nilebäck E., Haller F.M., Briggs D.C., Svedhem S., Day A.J., et al. The inflammation-associated protein TSG-6 cross-links hyaluronan via hyaluronan-induced TSG-6 oligomers. JBiol Chem 2011, 286:25675-25686.
5. Day A.J., De la Motte C.A. Hyaluronan cross-linking: a protective mechanism in inflammation?. Trends Immunol 2005, 26:637-643.
6. Attili S., Richter R.P. Self-assembly and elasticity of hierarchical proteoglycan-hyaluronan brushes. Soft Matter 2013, 9:10473-10483.
7. Lee G.M., Johnstone B., Jacobson K., Caterson B. The dynamic structure of the pericellular matrix on living cells. JCell Biol 1993, 123:1899-1907.
8. Knudson W., Knudson C.B. Assembly of a chondrocyte-like pericellular matrix on non-chondrogenic cells. Role of the cell surface hyaluronan receptors in the assembly of a pericellular matrix. JCell Sci 1991, 99(Pt 2):227-235.
9. Laguri C., Sadir R., Rueda P., Baleux F., Gans P., Arenzana-Seisdedos F., et al. The novel CXCL12γ isoform encodes an unstructured cationic domain which regulates bioactivity and interaction with both glycosaminoglycans and CXCR4. PLoS One 2007, 2:e1110.
10. Johnson Z., Proudfoot A.E., Handel T.M. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev 2005, 16:625-636.
11. Duchesne L., Octeau V., Bearon R.N., Beckett A., Prior I.A., Lounis B., et al. Transport of fibroblast growth factor 2 in the pericellular matrix is controlled by the spatial distribution of its binding sites in heparan sulfate. PLoS Biol 2012, 10:e1001361.
12. Rueda P., Balabanian K., Lagane B., Staropoli I., Chow K., Levoye A., et al. The CXCL12gamma chemokine displays unprecedented structural and functional properties that make it a paradigm of chemoattractant proteins. PLoS One 2008, 3:e2543.
13. Hesselgesser J., Liang M., Hoxie J., Greenberg M., Brass L.F., Orsini M.J., et al. Identification and characterization of the CXCR4 chemokine receptor in human T cell lines: ligand binding, biological activity, and HIV-1 infectivity. JImmunol 1998, 160:877-883.
14. Weber M., Hauschild R., Schwarz J., Moussion C., De Vries I., Legler D.F., et al. Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 2013, 339:328-332.
15. Altgärde N., Nilebäck E., De Battice L., Pashkuleva I., Reis R.L., Becher J., et al. Probing the biofunctionality of biotinylated hyaluronan and chondroitin sulfate by hyaluronidase degradation and aggrecan interaction. Acta Biomater 2013, 9:8158-8166.
16. Baranova N.S., Foulcer S.J., Briggs D.C., Tilakaratna V., Enghild J.J., Milner C.M., et al. Inter-α-inhibitor impairs TSG-6-induced hyaluronan cross-linking. JBiol Chem 2013, 288:29642-29653.
17. Richter R.P., Hock K.K., Burkhartsmeyer J., Boehm H., Bingen P., Wang G., et al. Membrane-grafted hyaluronan films: a well-defined model system of glycoconjugate cell coats. JAm Chem Soc 2007, 129:5306-5307.
18. Wolny P.M., Banerji S., Gounou C., Brisson A.R., Day A.J., Jackson D.G., et al. Analysis of CD44-hyaluronan interactions in an artificial membrane system: insights into the distinct binding properties of high and low molecular weight hyaluronan. JBiol Chem 2010, 285:30170-30180.
19. Reviakine I., Johannsmann D., Richter R.P. Hearing what you cannot see and visualizing what you hear: interpreting quartz crystal microbalance data from solvated interfaces. Anal Chem 2011, 83:8838-8848.
20. Richter R., Rodenhausen K., Eisele N.B., Schubert M. Coupling spectroscopic ellipsometry and quartz crystal microbalance to study organic films at the solid-liquid interface. Ellipsometry of functional organic surfaces and films 2014, 223-248. Springer, Berlin. K. Hinrichs, K.-J. Eichhorn (Eds.).
21. Laguri C., Sapay N., Simorre J.-P., Brutscher B., Imberty A., Gans P., et al. 13C-labeled heparan sulfate analogue as a tool to study protein/heparan sulfate interactions by NMR spectroscopy: application to the CXCL12α chemokine. JAm Chem Soc 2011, 133:9642-9645.
22. Bleul C.C., Wu L., Hoxie J.A., Springer T.A., Mackay C.R. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc Natl Acad Sci U S A 1997, 94:1925-1930.
23. Nagasawa T., Hirota S., Tachibana K., Takakura N., Nishikawa S., Kitamura Y., et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996, 382:635-638.
24. Massena S., Christoffersson G., Hjertstrom E., Zcharia E., Vlodavsky I., Ausmees N., et al. Achemotactic gradient sequestered on endothelial heparan sulfate induces directional intraluminal crawling of neutrophils. Blood 2010, 116:1924-1931.
25. Lortat-Jacob H. The molecular basis and functional implications of chemokine interactions with heparan sulphate. Curr Opin Struct Biol 2009, 19:543-548.
26. Mulloy B., Gee C., Wheeler S.F., Wait R., Gray E., Barrowcliffe T.W. Molecular weight measurements of low molecular weight heparins by gel permeation chromatography. Thromb Haemost 1997, 77:668-674.
27. Richter R., Mukhopadhyay A., Brisson A. Pathways of lipid vesicle deposition on solid surfaces: a combined QCM-D and AFM study. Biophys J 2003, 85:3035-3047.
28. Eisele N.B., Frey S., Piehler J., Görlich D., Richter R.P. Ultrathin nucleoporin phenylalanine-glycine repeat films and their interaction with nuclear transport receptors. EMBO Rep 2010, 11:366-372.
29. Domack A., Prucker O., Ruhe J., Johannsmann D. Swelling of a polymer brush probed with a quartz crystal resonator. Phys Rev E 1997, 56:680-689.
30. Johannsmann D., Reviakine I., Rojas E., Gallego M. Effect of sample heterogeneity on the interpretation of QCM(-D) data: comparison of combined quartz crystal microbalance/atomic force microscopy measurements with finite element method modeling. Anal Chem 2008, 80:8891-8899.
31. D. Johannsmann. n.d. http://www2.pc.tu-clausthal.de/dj/software_en.shtml.
32. Eisele N.B., Andersson F.I., Frey S., Richter R.P. Viscoelasticity of thin biomolecular films: a case study on nucleoporin phenylalanine-glycine repeats grafted to a histidine-tag capturing QCM-D sensor. Biomacromolecules 2012, 13:2322-2332.
33. Dubacheva G.V., Curk T., Mognetti B.M., Auzély-Velty R., Frenkel D., Richter R.P. Superselective targeting using multivalent polymers. JAm Chem Soc 2014, 136:1722-1725.
34. Mobley J.L., Ennis E., Shimizu Y. Differential activation-dependent regulation of integrin function in cultured human T-leukemic cell lines. Blood 1994, 83:1039-1050.
35. Wolny P.M., Spatz J.P., Richter R.P. On the adsorption behavior of biotin-binding proteins on gold and silica. Langmuir 2010, 26:1029-1034.
36. Sarrazin S., Lamanna W.C., Esko J.D. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol 2011, 3:a004952.
37. Richter R.P., Brisson A. Characterization of lipid bilayers and protein assemblies supported on rough surfaces by atomic force microscopy. Langmuir 2003, 19:1632-1640.
38. Horton M.R., Manley S., Arevalo S.R., Lobkovsky A.E., Gast A.P. Crystalline protein domains and lipid bilayer vesicle shape transformations. JPhys Chem B 2007, 111:880-885.
39. Frey W., Schief W.R., Vogel V. Two-dimensional crystallization of streptavidin studied by quantitative Brewster angle microscopy. Langmuir 1996, 12:1312-1320.
40. Richter R.P., Bérat R., Brisson A.R. Formation of solid-supported lipid bilayers: an integrated view. Langmuir 2006, 22:3497-3505.
41. Bingen P., Wang G., Steinmetz N.F., Rodahl M., Richter R.P. Solvation effects in the quartz crystal microbalance with dissipation monitoring response to biomolecular adsorption. A phenomenological approach. Anal Chem 2008, 80:8880-8890.
42. Hermens W.T., Benes M., Richter R., Speijer H. Effects of flow on solute exchange between fluids and supported biosurfaces. Biotechnol Appl Biochem 2004, 39:277-284.
43. Zhang Z., Xie J., Liu H., Liu J., Linhardt R.J. Quantification of heparan sulfate disaccharides using ion-pairing reversed-phase microflow high-performance liquid chromatography with electrospray ionization trap mass spectrometry. Anal Chem 2009, 81:4349-4355.
44. Roussille L., Brotons G., Ballut L., Louarn G., Ausserré D., Ricard-Blum S. Surface characterization and efficiency of a matrix-free and flat carboxylated gold sensor chip for surface plasmon resonance (SPR). Anal Bioanal Chem 2011, 401:1601-1617.
45. Fermas S., Gonnet F., Sutton A., Charnaux N., Mulloy B., Du Y., et al. Sulfated oligosaccharides (heparin and fucoidan) binding and dimerization of stromal cell-derived factor-1 (SDF-1/CXCL 12) are coupled as evidenced by affinity CE-MS analysis. Glycobiology 2008, 18:1054-1064.
46. 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. JBiol Chem 2006, 282:10018-10027.
47. Sadir R., Baleux F., Grosdidier A., Imberty A., Lortat-Jacob H. Characterization of the stromal cell-derived factor-1α-heparin complex. JBiol Chem 2001, 276:8288-8296.
48. Soriano A., Martínez C., García F., Plana M., Palou E., Lejeune M., et al. Plasma stromal cell-derived factor (SDF)-1 levels, SDF1-3'A genotype, and expression of CXCR4 on T lymphocytes: their impact on resistance to human immunodeficiency virus type 1 infection and its progression. JInfect Dis 2002, 186:922-931.
49. Ganju R.K., Brubaker S.A., Meyer J., Dutt P., Yang Y., Qin S., et al. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. JBiol Chem 1998, 273:23169-23175.
50. 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. JBiol Chem 2004, 279:43854-43860.
51. Hogg N., Laschinger M., Giles K., McDowall A. T-cell integrins: more than just sticking points. JCell Sci 2003, 116:4695-4705.
52. Yang Y., Jun C.D., Liu J.H., Zhang R., Joachimiak A., Springer T.A., et al. Structural basis for dimerization of ICAM-1 on the cell surface. Mol Cell 2003, 14:269-276.
53. Deisenhofer J. Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8 Å resolution. Biochemistry 1981, 20:2361-2370.
54. Semmrich M., Smith A., Feterowski C., Beer S., Engelhardt B., Busch D.H., et al. Importance of integrin LFA-1 deactivation for the generation of immune responses. JExp Med 2005, 201:1987-1998.
55. Azcutia V., Routledge M., Williams M.R., Newton G., Frazier W.A., Manica A., et al. CD47 plays a critical role in T-cell recruitment by regulation of LFA-1 and VLA-4 integrin adhesive functions. Mol Biol Cell 2013, 24:3358-3368.
56. Reichel A., Schaible D., Al Furoukh N., Cohen M., Schreiber G., Piehler J. Noncovalent, site-specific biotinylation of histidine-tagged proteins. Anal Chem 2007, 79:8590-8600.
57. Nisnevitch M., Firer M.A. The solid phase in affinity chromatography: strategies for antibody attachment. JBiochem Biophys Methods 2001, 49:467-480.
58. Cha T., Guo A., Zhu X.-Y. Enzymatic activity on a chip: the critical role of protein orientation. Proteomics 2005, 5:416-419.
59. Chevalier S., Cuestas-Ayllon C., Grazu V., Luna M., Feracci H., De la Fuente J.M. Creating biomimetic surfaces through covalent and oriented binding of proteins. Langmuir 2010, 26:14707-14715.
60. Murphy J.W., Yuan H., Kong Y., Xiong Y., Lolis E.J. Heterologous quaternary structure of CXCL12 and its relationship to the CC chemokine family. Proteins 2009, 78:1331-1337.
61. Schumann K., Lämmermann T., Bruckner M., Legler D.F., Polleux J., Spatz J.P., et al. Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 2010, 32:703-713.
62. Laguri C., Arenzana-Seisdedos F., Lortat-Jacob H. Relationships between glycosaminoglycan and receptor binding sites in chemokines-the CXCL12 example. Carbohydr Res 2008, 343:2018-2023.
63. Ray P., Lewin S.A., Mihalko L.A., Lesher-Perez S.-C., Takayama S., Luker K.E., et al. Secreted CXCL12 (SDF-1) forms dimers under physiological conditions. Biochem J 2012, 442:433-442.
64. Ziarek J.J., Getschman A.E., Butler S.J., Taleski D., Stephens B., Kufareva I., et al. Sulfopeptide probes of the CXCR4/CXCL12 interface reveal oligomer-specific contacts and chemokine allostery. ACS Chem Biol 2013, 8:1955-1963.
65. Veldkamp C.T., Seibert C., Peterson F.C., De la Cruz N.B., Haugner J.C., Basnet H., et al. Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci Signal 2008, 1:ra4.
66. Bargatze R.F., Butcher E.C. Rapid G protein-regulated activation event involved in lymphocyte binding to high endothelial venules. JExp Med 1993, 178:367-372.
67. Von Andrian U.H., Mackay C.R. T-cell function and migration. Two sides of the same coin. NEngl J Med 2000, 343:1020-1034.
68. Weber K.S., Ostermann G., Zernecke A., Schröder A., Klickstein L.B., Weber C. Dual role of H-Ras in regulation of lymphocyte function antigen-1 activity by stromal cell-derived factor-1alpha: implications for leukocyte transmigration. Mol Biol Cell 2001, 12:3074-3086.
69. Rueda P., Richart A., Récalde A., Gasse P., Vilar J., Guérin C., et al. Homeostatic and tissue reparation defaults in mice carrying selective genetic invalidation of CXCL12/proteoglycan interactions. Circulation 2012, 126:1882-1895.