Nuclear Magnetic Resonance Insight into the Multiple Glycosaminoglycan Binding Modes of the Link Module from Human TSG-6

Biochemistry

Volumn 55, Issue 2, 2016, Pages 262-276

  Park, Younghee ^a   Jowitt, Thomas A ^b   Day, Anthony J ^b   Prestegard, James H ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; CHEMICAL SHIFT; DIMERS; DISEASES; HYALURONIC ACID; MAGNETIC COUPLINGS; NUCLEAR MAGNETIC RESONANCE;

ANALYTICAL ULTRACENTRIFUGATION; CHEMICAL SHIFT PERTURBATIONS; INFLAMMATORY DISEASE PROCESS; NUCLEAR MAGNETIC RESONANCE TECHNIQUES; NUCLEAR OVERHAUSER EFFECTS; PARAMAGNETIC RELAXATION ENHANCEMENTS; RESIDUAL DIPOLAR COUPLING (RDCS); TUMOR NECROSIS FACTORS;

BINS;

CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; HEXASACCHARIDE; HYALURONIC ACID BINDING PROTEIN; TUMOR NECROSIS FACTOR STIMULATED GENE 6 PROTEIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; HERMES ANTIGEN; HYALURONIC ACID; PROTEIN BINDING; TNFAIP6 PROTEIN, HUMAN;

APPARENT DISSOCIATION CONSTANT; ARTICLE; BINDING AFFINITY; BINDING SITE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DIMERIZATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; IONIC STRENGTH; LIGAND BINDING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN POLYMERIZATION; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SPIN LABELING; ULTRACENTRIFUGATION; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN TERTIARY STRUCTURE;

ANTIGENS, CD44; CELL ADHESION MOLECULES; CHONDROITIN SULFATES; GLYCOSAMINOGLYCANS; HUMANS; HYALURONIC ACID; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84955296589     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b01148     Document Type: Article

References (85)

1. Day, A. J. and Prestwich, G. D. (2002) Hyaluronan-binding proteins: tying up the giant J. Biol. Chem. 277, 4585-4588 10.1074/jbc.R100036200
2. Day, A. J. and de la Motte, C. A. (2005) Hyaluronan cross-linking: a protective mechanism in inflammation? Trends Immunol. 26, 637-643 10.1016/j.it.2005.09.009
3. Tammi, M. I., Day, A. J., and Turley, E. A. (2002) Hyaluronan and homeostasis: A balancing act J. Biol. Chem. 277, 4581-4584 10.1074/jbc.R100037200
4. Monslow, J., Govindaraju, P., and Pure, E. (2015) Hyaluronan-a functional and structural sweet spot in the tissue microenvironment Front. Immunol. 6, 231 10.3389/fimmu.2015.00231
5. Petrey, A. C. and de la Motte, C. A. (2014) Hyaluronan, a crucial regulator of inflammation Front. Immunol. 5 (101) 1-13 10.3389/fimmu.2014.00101
6. Wells, J. M., Gaggar, A., and Blalock, J. E. (2015) MMP generated matrikines Matrix Biol. 44-46, 122-129 10.1016/j.matbio.2015.01.016
7. Kwok, J. C. F., Warren, P., and Fawcett, J. W. (2012) Chondroitin sulfate: A key molecule in the brain matrix Int. J. Biochem. Cell Biol. 44, 582-586 10.1016/j.biocel.2012.01.004
8. Ayerst, B. I., Day, A. J., Nurcombe, V., Cool, S. M., and Merry, C. L. R. (2014) New strategies for cartilage regeneration exploiting selected glycosaminoglycans to enhance cell fate determination Biochem. Soc. Trans. 42, 703-709 10.1042/BST20140031
9. Langford-Smith, A., Day, A. J., Bishop, P. N., and Clark, S. J. (2015) Complementing the sugar coce: role of GAGs and sialic acid in complement regulation Front. Immunol. 6 (25) 1-7 10.3389/fimmu.2015.00025
10. Xu, D. and Esko, J. D. (2014) Demystifying Heparan Sulfate-Protein Interactions. In Annual Review of Biochemistry (Kornberg, R. D., Ed.) Vol. 83, pp 129-157, Annual Reviews, Palo Alto, CA.
11. Milner, C. M. and Day, A. J. (2003) TSG-6: a multifunctional protein associated with inflammation J. Cell Sci. 116, 1863-1873 10.1242/jcs.00407
12. Milner, C. M., Higman, V. A., and Day, A. J. (2006) TSG-6: a pluripotent inflammatory mediator? Biochem. Soc. Trans. 34, 446-450 10.1042/BST0340446
13. Baranova, N. S., Nileback, E., Haller, F. M., Briggs, D. C., Svedhem, S., Day, A. J., and Richter, R. P. (2011) The inflammation-associated protein TSG-6 cross-links hyaluronan via hyaluronan-induced TSG-6 oligomers J. Biol. Chem. 286, 25675-25686 10.1074/jbc.M111.247395
14. Marson, A., Robinson, D. E., Brookes, P. N., Mulloy, B., Wiles, M., Clark, S. J., Fielder, H. L., Collinson, L. J., Cain, S. A., Kielty, C. M., McArthur, S., Buttle, D. J., Short, R. D., Whittle, J. D., and Day, A. J. (2009) Development of a microtiter plate-based glycosaminoglycan array for the investigation of glycosaminoglycan-protein interactions Glycobiology 19, 1537-1546 10.1093/glycob/cwp132
15. Mahoney, D. J., Mulloy, B., Forster, M. J., Blundell, C. D., Fries, E., Milner, C. M., and Day, A. J. (2005) Characterization of the interaction between tumor necrosis factor-stimulated gene-6 and heparin: implications for the inhibition of plasmin in extracellular matrix microenvironments J. Biol. Chem. 280, 27044-27055 10.1074/jbc.M502068200
16. Baranova, N. S., Inforzato, A., Briggs, D. C., Tilakaratna, V., Enghild, J. J., Thakar, D., Milner, C. M., Day, A. J., and Richter, R. P. (2014) Incorporation of pentraxin 3 into hyaluronan matrices is tightly regulated and promotes matrix cross-linking J. Biol. Chem. 289, 30481-30498 10.1074/jbc.M114.568154
17. Wisniewski, H. G., Hua, J. C., Poppers, D. M., Naime, D., Vilcek, J., and Cronstein, B. N. (1996) TNF/IL-1-inducible protein TSG-6 potentiates plasmin inhibition by inter-alpha-inhibitor and exerts a strong anti-inflammatory effect in vivo J. Immunol 156, 1609-1615
18. Fulop, C., Kamath, R. V., Li, Y., Otto, J. M., Salustri, A., Olsen, B. R., Glant, T. T., and Hascall, V. C. (1997) Coding sequence, exon-intron structure and chromosomal localization of murine TNF-stimulated gene 6 that is specifically expressed by expanding cumulus cell-oocyte complexes Gene 202, 95-102 10.1016/S0378-1119(97)00459-9
19. Carrette, O., Nemade, R. V., Day, A. J., Brickner, A., and Larsen, W. J. (2001) TSG-6 is concentrated in the extracellular matrix of mouse cumulus oocyte complexes through hyaluronan and inter-alpha-inhibitor binding Biol. Reprod. 65, 301-308 10.1095/biolreprod65.1.301
20. Mukhopadhyay, D., Hascall, V. C., Day, A. J., Salustri, A., and Fulop, C. (2001) Two distinct populations of tumor necrosis factor-stimulated gene-6 protein in the extracellular matrix of expanded mouse cumulus cell-oocyte complexes Arch. Biochem. Biophys. 394, 173-181 10.1006/abbi.2001.2552
21. Rugg, M. S., Willis, A. C., Mukhopadhyay, D., Hascall, V. C., Fries, E., Fulop, C., Milner, C. M., and Day, A. J. (2005) Characterization of complexes formed between TSG-6 and inter-alpha-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan J. Biol. Chem. 280, 25674-25686 10.1074/jbc.M501332200
22. Briggs, D. C., Birchenough, H. L., Ali, T., Rugg, M., Waltho, J. P., Ievoli, E., Jowitt, T. A., Enghild, J. J., Richter, R. P., Salustri, A., Milner, C. M., and Day, A. J. (2015) Metal Ion-Dependent Heavy Chain Transfer Activity of TSG-6 Mediates Assembly of the Cumulus-Oocyte Matrix J. Biol. Chem. 290, 28708-28723 10.1074/jbc.M115.669838
23. Enghild, J. J., Thogersen, I. B., Cheng, F., Fransson, L. A., Roepstorff, P., and Rahbek-Nielsen, H. (1999) Organization of the inter-alpha-inhibitor heavy chains on the chondroitin sulfate originating from Ser(10) of bikunin: posttranslational modification of IalphaI-derived bikunin Biochemistry 38, 11804-11813 10.1021/bi9908540
24. Ochsner, S. A., Day, A. J., Rugg, M. S., Breyer, R. M., Gomer, R. H., and Richards, J. S. (2003) Disrupted function of tumor necrosis factor-alpha-stimulated gene 6 blocks cumulus cell-oocyte complex expansion Endocrinology 144, 4376-4384 10.1210/en.2003-0487
25. Ochsner, S. A., Russell, D. L., Day, A. J., Breyer, R. M., and Richards, J. S. (2003) Decreased expression of tumor necrosis factor-alpha-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice Endocrinology 144, 1008-1019 10.1210/en.2002-220435
26. Fulop, C., Szanto, S., Mukhopadhyay, D., Bardos, T., Kamath, R. V., Rugg, M. S., Day, A. J., Salustri, A., Hascall, V. C., Glant, T. T., and Mikecz, K. (2003) Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice Development 130, 2253-2261 10.1242/dev.00422
27. Yingsung, W., Zhuo, L. S., Morgelin, M., Yoneda, M., Kida, D., Watanabe, H., Ishiguro, N., Iwata, H., and Kimata, K. (2003) Molecular heterogeneity of the SHAP-hyaluronan complex-Isolation and characterization of the complex in synovial fluid from patients with rheumatoid arthritis J. Biol. Chem. 278, 32710-32718 10.1074/jbc.M303658200
28. Wisniewski, H. G., Colon, E., Liublinska, V., Karia, R. J., Stabler, T. V., Attur, M., Abramson, S. B., Band, P. A., and Kraus, V. B. (2014) TSG-6 activity as a novel biomarker of progression in knee osteoarthritis Osteoarthritis and Cartilage 22, 235-241 10.1016/j.joca.2013.12.004
29. Lord, M. S., Day, A. J., Youssef, P., Zhuo, L., Watanabe, H., Caterson, B., and Whitelock, J. M. (2013) Sulfation of the Bikunin Chondroitin Sulfate Chain Determines Heavy Chain center dot Hyaluronan Complex Formation J. Biol. Chem. 288, 22930-22941 10.1074/jbc.M112.404186
30. Kahmann, J. D., O'Brien, R., Werner, J. M., Heinegard, D., Ladbury, J. E., Campbell, I. D., and Day, A. J. (2000) Localization and characterization of the hyaluronan-binding site on the link module from human TSG-6 Structure 8, 763-774 10.1016/S0969-2126(00)00163-5
31. Mahoney, D. J., Blundell, C. D., and Day, A. J. (2001) Mapping the hyaluronan-binding site on the link module from human tumor necrosis factor-stimulated gene-6 by site-directed mutagenesis J. Biol. Chem. 276, 22764-22771 10.1074/jbc.M100666200
32. Blundell, C. D., Almond, A., Mahoney, D. J., DeAngelis, P. L., Campbell, I. D., and Day, A. J. (2005) Towards a structure for a TSG-6.hyaluronan complex by modeling and NMR spectroscopy: insights into other members of the link module superfamily J. Biol. Chem. 280, 18189-18201 10.1074/jbc.M414343200
33. Higman, V. A., Blundell, C. D., Mahoney, D. J., Redfield, C., Noble, M. E., and Day, A. J. (2007) Plasticity of the TSG-6 HA-binding loop and mobility in the TSG-6-HA complex revealed by NMR and X-ray crystallography J. Mol. Biol. 371, 669-684 10.1016/j.jmb.2007.05.073
34. Higman, V. A., Briggs, D. C., Mahoney, D. J., Blundell, C. D., Sattelle, B. M., Dyer, D. P., Green, D. E., DeAngelis, P. L., Almond, A., Milner, C. M., and Day, A. J. (2014) A refined model for the TSG-6 link module in complex with hyaluronan: use of defined oligosaccharides to probe structure and function J. Biol. Chem. 289, 5619-5634 10.1074/jbc.M113.542357
35. Kohda, D., Morton, C. J., Parkar, A. A., Hatanaka, H., Inagaki, F. M., Campbell, I. D., and Day, A. J. (1996) Solution structure of the link module: a hyaluronan-binding domain involved in extracellular matrix stability and cell migration Cell 86, 767-775 10.1016/S0092-8674(00)80151-8
36. Blundell, C. D., Mahoney, D. J., Almond, A., DeAngelis, P. L., Kahmann, J. D., Teriete, P., Pickford, A. R., Campbell, I. D., and Day, A. J. (2003) The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding J. Biol. Chem. 278, 49261-49270 10.1074/jbc.M309623200
37. Parkar, A. A. and Day, A. J. (1997) Overlapping sites on the Link module of human TSG-6 mediate binding to hyaluronan and chrondroitin-4-sulphate FEBS Lett. 410, 413-417 10.1016/S0014-5793(97)00621-2
38. Wisniewski, H. G., Snitkin, E. S., Mindrescu, C., Sweet, M. H., and Vilcek, J. (2005) TSG-6 protein binding to glycosaminoglycans: formation of stable complexes with hyaluronan and binding to chondroitin sulfates J. Biol. Chem. 280, 14476-14484 10.1074/jbc.M411734200
39. Heng, B. C., Gribbon, P. M., Day, A. J., and Hardingham, T. E. (2008) Hyaluronan Binding to Link Module of TSG-6 and to G1 Domain of Aggrecan Is Differently Regulated by pH J. Biol. Chem. 283, 32294-32301 10.1074/jbc.M804155200
40. Williamson, M. P. (2013) Using chemical shift perturbation to characterise ligand binding Prog. Nucl. Magn. Reson. Spectrosc. 73, 1-16 10.1016/j.pnmrs.2013.02.001
41. Losonczi, J. A., Andrec, M., Fischer, M. W., and Prestegard, J. H. (1999) Order matrix analysis of residual dipolar couplings using singular value decomposition J. Magn. Reson. 138, 334-342 10.1006/jmre.1999.1754
42. Prestegard, J. H., Bougault, C. M., and Kishore, A. I. (2004) Residual dipolar couplings in structure determination of biomolecules Chem. Rev. 104, 3519-3540 10.1021/cr030419i
43. Dominguez, C., Boelens, R., and Bonvin, A. M. (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information J. Am. Chem. Soc. 125, 1731-1737 10.1021/ja026939x
44. de Vries, S. J., van Dijk, A. D., Krzeminski, M., van Dijk, M., Thureau, A., Hsu, V., Wassenaar, T., and Bonvin, A. M. (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets Proteins: Struct., Funct., Genet. 69, 726-733 10.1002/prot.21723
45. Day, A. J., Aplin, R. T., and Willis, A. C. (1996) Overexpression, purification, and refolding of link module from human TSG-6 in Escherichia coli: effect of temperature, media, and mutagenesis on lysine misincorporation at arginine AGA codons Protein Expression Purif. 8, 1-16 10.1006/prep.1996.0068
46. Kahmann, J. D., Koruth, R., and Day, A. J. (1997) Method for quantitative refolding of the link module from human TSG-6 Protein Expression Purif. 9, 315-318 10.1006/prep.1996.0694
47. Pomin, V. H., Park, Y., Huang, R. R., Heiss, C., Sharp, J. S., Azadi, P., and Prestegard, J. H. (2012) Exploiting enzyme specificities in digestions of chondroitin sulfates A and C: Production of well-defined hexasaccharides Glycobiology 22, 826-838 10.1093/glycob/cws055
48. Kneller, D. G. and Kuntz, I. D. (1993) UCSF Sparky-and NMR display, annotation and assignment tool Journal of Cellular Biochemistry 254
49. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293 10.1007/BF00197809
50. Farmer, B. T., 2nd, Constantine, K. L., Goldfarb, V., Friedrichs, M. S., Wittekind, M., Yanchunas, J., Jr., Robertson, J. G., and Mueller, L. (1996) Localizing the NADP+ binding site on the MurB enzyme by NMR Nat. Struct. Biol. 3, 995-997 10.1038/nsb1296-995
51. Liu, Y. and Prestegard, J. H. (2010) A device for the measurement of residual chemical shift anisotropy and residual dipolar coupling in soluble and membrane-associated proteins J. Biomol. NMR 47, 249-258 10.1007/s10858-010-9427-7
52. Yao, L., Ying, J., and Bax, A. (2009) Improved accuracy of 15N-1H scalar and residual dipolar couplings from gradient-enhanced IPAP-HSQC experiments on protonated proteins J. Biomol. NMR 43, 161-170 10.1007/s10858-009-9299-x
53. Kay, L. E., Ikura, M., Tschudin, R., and Bax, A. (1990) 3-Dimensional Triple-Resonance Nmr-Spectroscopy of Isotopically Enriched Proteins J. Magn. Reson. 89, 496-514 10.1016/0022-2364(90)90333-5
54. Muhandiram, D. R. and Kay, L. E. (1994) Gradient-Enhanced Triple-Resonance 3-Dimensional Nmr Experiments with Improved Sensitivity J. Magn. Reson., Ser. B 103, 203-216 10.1006/jmrb.1994.1032
55. Zuiderweg, E. R. and Fesik, S. W. (1989) Heteronuclear three-dimensional NMR spectroscopy of the inflammatory protein C5a Biochemistry 28, 2387-2391 10.1021/bi00432a008
56. Marion, D., Driscoll, P. C., Kay, L. E., Wingfield, P. T., Bax, A., Gronenborn, A. M., and Clore, G. M. (1989) Overcoming the overlap problem in the assignment of 1H NMR spectra of larger proteins by use of three-dimensional heteronuclear 1H-15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1 beta Biochemistry 28, 6150-6156 10.1021/bi00441a004
57. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R. A., Rouault, T. A., and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition Anal. Biochem. 326, 234-256 10.1016/j.ab.2003.12.014
58. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology J. Biomol. NMR 13, 289-302 10.1023/A:1008392405740
59. Guntert, P., Mumenthaler, C., and Wuthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273, 283-298 10.1006/jmbi.1997.1284
60. Herrmann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS J. Biomol. NMR 24, 171-189 10.1023/A:1021614115432
61. Valafar, H. and Prestegard, J. H. (2004) REDCAT: a residual dipolar coupling analysis tool J. Magn. Reson. 167, 228-241 10.1016/j.jmr.2003.12.012
62. Schwieters, C. D., Kuszewski, J. J., Tjandra, N., and Marius Clore, G. M. (2003) The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160, 65-73 10.1016/S1090-7807(02)00014-9
63. De Vries, S. J., van Dijk, M., and Bonvin, A. M. J. J. (2010) The HADDOCK web server for data-driven biomolecular docking Nat. Protoc. 5, 883-897 10.1038/nprot.2010.32
64. Kirschner, K. N., Yongye, A. B., Tschampel, S. M., Gonzalez-Outeirino, J., Daniels, C. R., Foley, B. L., and Woods, R. J. (2008) GLYCAM06: a generalizable biomolecular force field. Carbohydrates J. Comput. Chem. 29, 622-655 10.1002/jcc.20820
65. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-1612 10.1002/jcc.20084
66. Kveder, M., Pifat, G., Pecar, S., Schara, M., Ramos, P., and Esterbauer, H. (1997) Nitroxide reduction with ascorbic acid in spin labeled human plasma LDL and VLDL Chem. Phys. Lipids 85, 1-12 10.1016/S0009-3084(96)02636-9
67. Johnson, P. E., Brun, E., MacKenzie, L. F., Withers, S. G., and McIntosh, L. P. (1999) The cellulose-binding domains from Cellulomonas fimi beta-1, 4-glucanase CenC bind nitroxide spin-labeled cellooligosaccharides in multiple orientations J. Mol. Biol. 287, 609-625 10.1006/jmbi.1999.2627
68. Battiste, J. L. and Wagner, G. (2000) Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data Biochemistry 39, 5355-5365 10.1021/bi000060h
69. Jain, N. U., Venot, A., Umemoto, K., Leffler, H., and Prestegard, J. H. (2001) Distance mapping of protein-binding sites using spin-labeled oligosaccharide ligands Protein science: a publication of the Protein Society 10, 2393-2400 10.1110/ps.17401
70. Kay, L. E., Torchia, D. A., and Bax, A. (1989) BACKBONE DYNAMICS OF PROTEINS AS STUDIED BY N-15 INVERSE DETECTED HETERONUCLEAR NMR-SPECTROSCOPY-APPLICATION TO STAPHYLOCOCCAL NUCLEASE Biochemistry 28, 8972-8979 10.1021/bi00449a003
71. Blundell, C. D., Kahmann, J. D., Perczel, A., Mahoney, D. J., Cordell, M. R., Teriete, P., Campbell, I. D., and Day, A. J. (2002) Getting to grips with HA-protein interactions. In Hyaluronan (Kennedy, J. F., Phillips, G. O., Williams, P. A., and Hascall, V. C., Eds.) pp 161-172, Woodhead Publishing Ltd., Cambridge, U.K.
72. Blundell, C. D., Mahoney, D. J., Cordell, M. R., Almond, A., Kahmann, J. D., Perczel, A., Taylor, J. D., Campbell, I. D., and Day, A. J. (2007) Determining the molecular basis for the pH-dependent interaction between the link module of human TSG-6 and hyaluronan J. Biol. Chem. 282, 12976-12988 10.1074/jbc.M611713200
73. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44, 213-223 10.1007/s10858-009-9333-z
74. Wang, X., Bansal, S., Jiang, M., and Prestegard, J. H. (2008) RDC-assisted modeling of symmetric protein homo-oligomers Protein science: a publication of the Protein Society 17, 899-907 10.1110/ps.073395108
75. Nivedha, A. K., Makeneni, S., Foley, B. L., Tessier, M. B., and Woods, R. J. (2014) Importance of Ligand Conformational Energies in Carbohydrate Docking: Sorting the Wheat from the Chaff J. Comput. Chem. 35, 526-539 10.1002/jcc.23517
76. Banerji, S., Wright, A. J., Noble, M., Mahoney, D. J., Campbell, I. D., Day, A. J., and Jackson, D. G. (2007) Structures of the Cd44-hyaluronan complex provide insight into a fundamental carbohydrate-protein interaction Nat. Struct. Mol. Biol. 14, 234-239 10.1038/nsmb1201
77. Bathe, M., Rutledge, G. C., Grodzinsky, A. J., and Tidor, B. (2005) A coarse-grained molecular model for glycosaminoglycans: Application to chondroitin, chondroitin sulfate, and hyaluronic acid Biophys. J. 88, 3870-3887 10.1529/biophysj.104.058800
78. Sattelle, B. M., Shakeri, J., and Almond, A. (2013) Does Microsecond Sugar Ring Flexing Encode 3D-Shape and Bioactivity in the Heparanome? Biomacromolecules 14, 1149-1159 10.1021/bm400067g
79. Briggs, D., Birchenough, H., Ali, T., Rugg, M., Waltho, J., Ievoli, E., Jowitt, T., Enghild, J., Richter, R., Salustri, A., Milner, C., and Day, A. (2015) Metal Ion-dependent Heavy Chain Transfer Activity of TSG-6 Mediates Assembly of the Cumulus-Oocyte Matrix J. Biol. Chem. 290, 28708-28723 10.1074/jbc.M115.669838
80. Discher, D. E., Janmey, P., and Wang, Y. L. (2005) Tissue cells feel and respond to the stiffness of their substrate Science 310, 1139-1143 10.1126/science.1116995
81. Discher, D. E., Mooney, D. J., and Zandstra, P. W. (2009) Growth Factors, Matrices, and Forces Combine and Control Stem Cells Science 324, 1673-1677 10.1126/science.1171643
82. Geiger, B., Spatz, J. P., and Bershadsky, A. D. (2009) Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 10, 21-33 10.1038/nrm2593
83. Deshauer, C., Morgan, A. M., Ryan, E. O., Handel, T. M., Prestegard, J. H., and Wang, X. (2015) Interactions of the Chemokine CCL5/RANTES with Medium-Sized Chondroitin Sulfate Ligands Structure 23, 1066-1077 10.1016/j.str.2015.03.024
84. Dyer, D. P., Thomson, J. M., Hermant, A., Jowitt, T. A., Handel, T. M., Proudfoot, A. E. I., Day, A. J., and Milner, C. M. (2014) TSG-6 Inhibits Neutrophil Migration via Direct Interaction with the Chemokine CXCL8 J. Immunol. 192, 2177-2185 10.4049/jimmunol.1300194
85. Sanggaard, K. W., Sonne-Schmidt, C. S., Jacobsen, C., Thogersen, I. B., Valnickova, Z., Wisniewski, H. G., and Enghild, J. J. (2006) Evidence for a two-step mechanism involved in the formation of covalent HC center dot TSG-6 complexes Biochemistry 45, 7661-7668 10.1021/bi060106s