Inter-α-inhibitor impairs TSG-6-induced hyaluronan cross-linking

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29642-29653

  Baranova, Natalia S ^a   Foulcer, Simon J ^b   Briggs, David C ^b   Tilakaratna, Viranga ^b   Enghild, Jan J ^d   Milner, Caroline M ^c   Day, Anthony J ^b   Richter, Ralf P ^a,e,f  

^a CIC BIOMAGUNE   (Spain)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d AARHUS UNIVERSITY   (Denmark)

^e MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^f UNIVERSITÉ JOSEPH FOURIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSLINKER; EXTRACELLULAR MATRICES; FUNCTIONAL PROPERTIES; HEAVY CHAIN; INFLAMMATORY CONDITIONS; MOLECULAR SPECIES; TERNARY INTERACTIONS; TUMOR NECROSIS;

CHAINS; GLYCOPROTEINS;

HYALURONIC ACID;

CARBOHYDRATE BINDING PROTEIN; HERMES ANTIGEN; HYALURONIC ACID; INTER ALPHA TRYPSIN INHIBITOR; TUMOR NECROSIS FACTOR STIMULATED GENE 6 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; COMPLEX FORMATION; CONTROLLED STUDY; COVALENT BOND; EXTRACELLULAR MATRIX; HEAVY CHAIN; INCUBATION TIME; MOLECULAR STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

CARBOHYDRATE-BINDING PROTEIN; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; GLYCOSAMINOGLYCAN; HYALURONAN; MULTIFUNCTIONAL PROTEIN; PROTEIN COMPLEXES; PROTEIN SELF-ASSEMBLY; PROTEIN-PROTEIN INTERACTIONS; SUPRAMOLECULAR INTERACTIONS;

ALPHA-GLOBULINS; ANIMALS; ANTIGENS, CD44; BINDING SITES; BINDING, COMPETITIVE; BLOTTING, WESTERN; CELL ADHESION MOLECULES; CELL LINE; CELL LINE, TUMOR; CROSS-LINKING REAGENTS; HUMANS; HYALURONIC ACID; KINETICS; MICROSCOPY, INTERFERENCE; PROTEIN BINDING; SURFACE PLASMON RESONANCE;

EID: 84885635212     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.477422     Document Type: Article

References (64)

1. Tammi, M. I., Day, A. J., and Turley, E. A. (2002) Hyaluronan and homeostasis. A balancing act. J. Biol. Chem. 277, 4581-4584
2. Russell, D. L., and Salustri, A. (2006) Extracellular matrix of the cumulusoocyte complex. Semin. Reprod. Med. 24, 217-227
3. Day, A. J., and Sheehan, J. K. (2001) Hyaluronan. Polysaccharide chaos to protein organisation. Curr. Opin. Struct. Biol. 11, 617-622
4. Baranova, N. S., Nilebäck, 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
5. Day, A. J., and de la Motte, C. A. (2005) Hyaluronan cross-linking. A protective mechanism in inflammation? Trends Immunol. 26, 637-643
6. Zhao, M., Yoneda, M., Ohashi, Y., Kurono, S., Iwata, H., Ohnuki, Y., and Kimata, K. (1995) Evidence for the covalent binding of SHAP, heavy chains of inter-α-trypsin inhibitor, to hyaluronan. J. Biol. Chem. 270, 26657-26663
7. Yingsung, W., Zhuo, L., 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
8. Zhuo, L., Yoneda, M., Zhao, M., Yingsung, W., Yoshida, N., Kitagawa, Y., Kawamura, K., Suzuki, T., and Kimata, K. (2001) Defect in SHAP-hyaluronan complex causes severe female infertility.Astudy by inactivation of the bikunin gene in mice. J. Biol. Chem. 276, 7693-7696
9. Fülöp, C., Szántó, S., Mukhopadhyay, D., Bárdos, 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. Salustri, A., Garlanda, C., Hirsch, E., De Acetis, M., Maccagno, A., Bottazzi, B., Doni, A., Bastone, A., Mantovani, G., Beck Peccoz, P., Salvatori, G., Mahoney, D. J., Day, A. J., Siracusa, G., Romani, L., and Mantovani, A. (2004) PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131, 1577-1586
11. Scarchilli, L., Camaioni, A., Bottazzi, B., Negri, V., Doni, A., Deban, L., Bastone, A., Salvatori, G., Mantovani, A., Siracusa, G., and Salustri, A. (2007) PTX3 interacts with inter-α-trypsin inhibitor. Implications for hyaluronan organization and cumulus oophorus expansion. J. Biol. Chem. 282, 30161-30170
12. Inforzato, A., Rivieccio, V., Morreale, A. P., Bastone, A., Salustri, A., Scarchilli, L., Verdoliva, A., Vincenti, S., Gallo, G., Chiapparino, C., Pacello, L., Nucera, E., Serlupi-Crescenzi, O., Day, A. J., Bottazzi, B., Mantovani, A., De Santis, R., and Salvatori, G. (2008) Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. J. Biol. Chem. 283, 10147-10161
13. Ievoli, E., Lindstedt, R., Inforzato, A., Camaioni, A., Palone, F., Day, A. J., Mantovani, A., Salvatori, G., and Salustri, A. (2011) Implication of the oligomeric state of the N-terminal PTX3 domain in cumulus matrix assembly. Matrix Biol. 30, 330-337
14. Kida, D., Yoneda, M., Miyaura, S., Ishimaru, T., Yoshida, Y., Ito, T., Ishiguro, N., Iwata, H., and Kimata, K. (1999) The SHAP-HA complex in sera from patients with rheumatoid arthritis and osteoarthritis. J. Rheumatol. 26, 1230-1238
15. Hamerman, D., and Sandson, J. (1963) Unusual properties of hyaluronateprotein isolated from pathological synovial fluids. J. Clin. Invest. 42, 1882-1889
16. Zhuo, L., Kanamori, A., Kannagi, R., Itano, N., Wu, J., Hamaguchi, M., Ishiguro, N., and Kimata, K. (2006) SHAP potentiates the CD44-mediated leukocyte adhesion to the hyaluronan substratum. J. Biol. Chem. 281, 20303-20314
17. Lauer, M. E., Cheng, G., Swaidani, S., Aronica, M. A., Weigel, P. H., and Hascall, V. C. (2013) Tumor necrosis factor-stimulated gene-6 (TSG-6) amplifies hyaluronan synthesis by airway smooth muscle cells. J. Biol. Chem. 288, 423-431
18. Milner, C. M., Tongsoongnoen, W., Rugg, M. S., and Day, A. J. (2007) The molecular basis of inter-α-inhibitor heavy chain transfer on to hyaluronan. Biochem. Soc. Trans. 35, 672-676
19. Enghild, J. J., Thøgersen, I. B., Pizzo, S. V., and Salvesen, G. (1989) Analysis of inter-α-trypsin inhibitor and a novel trypsin inhibitor, pre-α-trypsin inhibitor, from human plasma. Polypeptide chain stoichiometry and assembly by glycan. J. Biol. Chem. 264, 15975-15981
20. Enghild, J. J., Salvesen, G., Thøgersen, I. B., Valnickova, Z., Pizzo, S. V., and Hefta, S. A. (1993) Presence of the protein-glycosaminoglycan- protein covalent cross-link in the inter-α-inhibitor-related proteinase inhibitor heavy chain 2/bikunin. J. Biol. Chem. 268, 8711-8716
21. Rugg, M. S., Willis, A. C., Mukhopadhyay, D., Hascall, V. C., Fries, E., Fülöp, C., Milner, C. M., and Day, A. J. (2005) Characterization of complexes formed between TSG-6 and inter-α-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J. Biol. Chem. 280, 25674-25686
22. Sanggaard, K. W., Karring, H., Valnickova, Z., Thøgersen, I. B., and Enghild, J. J. (2005) The TSG-6 and IαI interaction promotes a transesterification cleaving the protein-glycosaminoglycan-protein (PGP) cross-link. J. Biol. Chem. 280, 11936-11942
23. Sanggaard, K. W., Sonne-Schmidt, C. S., Krogager, T. P., Kristensen, T., Wisniewski, H. G., Thøgersen, I. B., and Enghild, J. J. (2008) TSG-6 transfers proteins between glycosaminoglycans via a Ser28-mediated covalent catalytic mechanism. J. Biol. Chem. 283, 33919-33926
24. Sanggaard, K. W., Sonne-Schmidt, C. S., Krogager, T. P., Lorentzen, K. A., Wisniewski, H. G., Thøgersen, I. B., and Enghild, J. J. (2008) The transfer of heavy chains from bikunin proteins to hyaluronan requires both TSG-6 and HC2. J. Biol. Chem. 283, 18530-18537
25. Sanggaard, K. W., Sonne-Schmidt, C. S., Jacobsen, C., Thøgersen, 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 × TSG-6 complexes. Biochemistry 45, 7661-7668
26. Sato, H., Kajikawa, S., Kuroda, S., Horisawa, Y., Nakamura, N., Kaga, N., Kakinuma, C., Kato, K., Morishita, H., Niwa, H., and Miyazaki, J. (2001) Impaired fertility in female mice lacking urinary trypsin inhibitor. Biochem. Biophys. Res. Commun. 281, 1154-1160
27. Jessen, T. E., and Ødum, L. (2004) TSG-6 and calcium ions are essential for the coupling of inter-α-trypsin inhibitor to hyaluronan in human synovial fluid. Osteoarthritis Cartilage 12, 142-148
28. Lee, T. H., Wisniewski, H. G., and Vilcek, J. (1992)Anovel secretory tumor necrosis factor-inducible protein (TSG-6) is a member of the family of hyaluronate binding proteins, closely related to the adhesion receptor CD44. J. Cell Biol. 116, 545-557
29. 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
30. Milner, C. M., and Day, A. J. (2003) TSG-6. A multifunctional protein associated with inflammation. J. Cell Sci. 116, 1863-1873
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
32. 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
33. 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
34. Kuznetsova, S. A., Mahoney, D. J., Martin-Manso, G., Ali, T., Nentwich, H. A., Sipes, J. M., Zeng, B., Vogel, T., Day, A. J., and Roberts, D. D. (2008) TSG-6 binds via its CUB-C domain to the cell-binding domain of fibronectin and increases fibronectin matrix assembly. Matrix Biol. 27, 201-210
35. Mukhopadhyay, D., Hascall, V. C., Day, A. J., Salustri, A., and Fülöp, 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
36. 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-α-inhibitor binding. Biol. Reprod. 65, 301-308
37. Salustri, A., Yanagishita, M., and Hascall, V. C. (1989) Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification. J. Biol. Chem. 264, 13840-13847
38. Powers, R. W., Chen, L., Russell, P. T., and Larsen, W. J. (1995) Gonadotropin- stimulated regulation of blood-follicle barrier is mediated by nitric oxide. Am. J. Physiol. 269, E290-298
39. Hess, K. A., Chen, L., and Larsen, W. J. (1998) The ovarian blood follicle barrier is both charge- and size-selective in mice. Biol Reprod 58, 705-711
40. Chen, L., Zhang, H., Powers, R. W., Russell, P. T., and Larsen, W. J. (1996) Covalent linkage between proteins of the inter-α-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells. J. Biol. Chem. 271, 19409-19414
41. Chen, L., Mao, S. J., and Larsen, W. J. (1992) Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-α-trypsin inhibitor family. J. Biol. Chem. 267, 12380-12386
42. Nentwich, H. A., Mustafa, Z., Rugg, M. S., Marsden, B. D., Cordell, M. R., Mahoney, D. J., Jenkins, S. C., Dowling, B., Fries, E., Milner, C. M., Loughlin, J., and Day, A. J. (2002)Anovel allelic variant of the human TSG-6 gene encoding an amino acid difference in the CUB module. Chromosomal localization, frequency analysis, modeling, and expression. J. Biol. Chem. 277, 15354-15362
43. Attili, S., and Richter, R. P. (2012) Combining colloidal probe atomic force and reflection interference contrast microscopy to study the compressive mechanics of hyaluronan brushes. Langmuir 28, 3206-3216
44. Attili, S., Borisov, O. V., and Richter, R. P. (2012) Films of end-grafted hyaluronan are a prototype of a brush of a strongly charged, semiflexible polyelectrolyte with intrinsic excluded volume. Biomacromolecules 13, 1466-1477
45. de Gennes, P. G. (1987) Polymers at an interface; a simplified view. Adv. Colloid Interface Sci. 27, 189-209
46. Eisele, N. B., Frey, S., Piehler, J., Görlich, D., and Richter, R. P. (2010) Ultrathin nucleoporin phenylalanine-glycine repeat films and their interaction with nuclear transport receptors. EMBO Rep 11, 366-372
47. Richter, R. P., Hock, K. K., Burkhartsmeyer, J., Boehm, H., Bingen, P., Wang, G., Steinmetz, N. F., Evans, D. J., and Spatz, J. P. (2007) Recognition of single nucleotide polymorphisms using scanning potential hairpin denaturation. J. Am. Chem. Soc. 129, 5306-5307
48. Fujimoto, T., Savani, R. C., Watari, M., Day, A. J., and Strauss, J. F., 3rd (2002) Induction of the hyaluronic acid-binding protein, tumor necrosis factor-stimulated gene-6, in cervical smooth muscle cells by tumor necrosis factor-α and prostaglandin E2. Am. J. Pathol. 160, 1495-1502
49. de Belder, A. N., and Wik, K. O. (1975) Preparation and properties of fluorescein-labelled hyaluronate. Carbohydr. Res. 44, 251-257
50. Lesley, J., He, Q., Miyake, K., Hamann, A., Hyman, R., and Kincade, P. W. (1992) Requirements for hyaluronic acid binding by CD44. A role for the cytoplasmic domain and activation by antibody. J. Exp. Med. 175, 257-266
51. Gal, I., Lesley, J., Ko, W., Gonda, A., Stoop, R., Hyman, R., and Mikecz, K. (2003) Role of the extracellular and cytoplasmic domains of CD44 in the rolling interaction of lymphoid cells with hyaluronan under physiologic flow. J. Biol. Chem. 278, 11150-11158
52. Lesley, J., Gál, I., Mahoney, D. J., Cordell, M. R., Rugg, M. S., Hyman, R., Day, A. J., and Mikecz, K. (2004) TSG-6 modulates the interaction between hyaluronan and cell surface CD44. J. Biol. Chem. 279, 25745-25754
53. 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
54. 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
55. 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
56. 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
57. Getting, S. J., Mahoney, D. J., Cao, T., Rugg, M. S., Fries, E., Milner, C. M., Perretti, M., and Day, A. J. (2002) The link module from human TSG-6 inhibits neutrophil migration in a hyaluronan- and inter-α-inhibitor- independent manner. J. Biol. Chem. 277, 51068-51076
58. Colón, E., Shytuhina, A., Cowman, M. K., Band, P. A., Sanggaard, K. W., Enghild, J. J., and Wisniewski, H. G. (2009) Transfer of inter-α-inhibitor heavy chains to hyaluronan by surface-linked hyaluronan-TSG-6 complexes. J. Biol. Chem. 284, 2320-2331
59. 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
60. Fraser, J. R., Laurent, T. C., and Laurent, U. B. (1997) Hyaluronan. Its nature, distribution, functions and turnover. J. Intern. Med. 242, 27-33
61. Mahoney, D. J., Swales, C., Athanasou, N. A., Bombardieri, M., Pitzalis, C., Kliskey, K., Sharif, M., Day, A. J., Milner, C. M., and Sabokbar, A. (2011) TSG-6 inhibits osteoclast activity via an autocrine mechanism and is functionally synergistic with osteoprotegerin. Arthritis Rheum. 63, 1034-1043
62. Bayliss, M. T., Howat, S. L., Dudhia, J., Murphy, J. M., Barry, F. P., Edwards, J. C., and Day, A. J. (2001) Up-regulation and differential expression of the hyaluronan-binding protein TSG-6 in cartilage and synovium in rheumatoid arthritis and osteoarthritis. Osteoarthritis Cartilage 9, 42-48
63. Yoshihara, Y., Plaas, A., Osborn, B., Margulis, A., Nelson, F., Stewart, M., Rugg, M. S., Milner, C. M., Day, A. J., Nemoto, K., and Sandy, J. D. (2008) Superficial zone chondrocytes in normal and osteoarthritic human articular cartilages synthesize novel truncated forms of inter-α-trypsin inhibitor heavy chains which are attached to a chondroitin sulfate proteoglycan other than bikunin. Osteoarthritis Cartilage 16, 1343-1355
64. Luchetti, M. M., Piccinini, G., Mantovani, A., Peri, G., Matteucci, C., Pomponio, G., Fratini, M., Fraticelli, P., Sambo, P., Di Loreto, C., Doni, A., Introna, M., and Gabrielli, A. (2000) Expression and production of the long pentraxin PTX3 in rheumatoid arthritis (RA). Clin. Exp. Immunol. 119, 196-202