Sulfation of the bikunin chondroitin sulfate chain determines heavy chain-hyaluronan complex formation

Journal of Biological Chemistry

Volumn 288, Issue 32, 2013, Pages 22930-22941

  Lord, Megan S ^a   Day, Anthony J ^b   Youssef, Peter ^c   Zhuo, Lisheng ^d   Watanabe, Hideto ^d   Caterson, Bruce ^e   Whitelock, John M ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d AICHI MEDICAL UNIVERSITY   (Japan)

^e CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIKUNIN; CHONDROITIN SULFATES; COMPLEX FORMATIONS;

BIOCHEMISTRY; BIOLOGY;

HYALURONIC ACID;

CHONDROITIN SULFATE; DISACCHARIDE; HYALURONIC ACID; MONOCLONAL ANTIBODY; SODIUM CHLORIDE; ULINASTATIN;

AMINO ACID SEQUENCE; ANION EXCHANGE CHROMATOGRAPHY; ANTIGEN ANTIBODY REACTION; ARTICLE; CARBOHYDRATE ANALYSIS; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GLYCOSYLATION; HEAVY CHAIN; HUMAN; MOLECULAR INTERACTION; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN TRANSPORT; PROTEIN URINE LEVEL; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; SULFATION; TRANSESTERIFICATION;

BIKUNIN; CHONDROITIN SULFATE; EXTRACELLULAR MATRIX PROTEINS; GLYCOSAMINOGLYCAN; HYALURONAN; INTER-Α-TRYPSIN INHIBITOR; PROTEOGLYCAN; PROTEOGLYCAN STRUCTURE;

ALPHA-GLOBULINS; CARBOHYDRATE CONFORMATION; CHONDROITIN SULFATES; EXTRACELLULAR MATRIX; FEMALE; HUMANS; HYALURONIC ACID; MALE; OVULATION;

EID: 84881415083     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.404186     Document Type: Article

References (57)

1. Proksch, G. J., and Routh, J. I. (1972) The purification of the trypsin inhibitor from human pregnancy urine. J. Lab. Clin. Med. 79, 491-499
2. Enghild, J. J., Thøgersen, I. B., Pizzo, S. V., and Salvesen, G. (1989) Analysis of inter-trypsin inhibitor and a novel trypsin inhibitor, pre-trypsin inhibitor, from human plasma. Polypeptide chain stoichiometry and assembly by glycan. J. Biol. Chem. 264, 15975-15981
3. 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-inhibitor-related proteinase inhibitor heavy chain 2/bikunin. J. Biol. Chem. 268, 8711-8716
4. 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-inhibitor that act as intermediates in the covalent transfer of heavy chains onto hyaluronan. J. Biol. Chem. 280, 25674-25686
5. Blom, A., Pertoft, H., and Fries, E. (1995) Inter-inhibitor is required for the formation of the hyaluronan-containing coat on fibroblasts and mesothelial cells. J. Biol. Chem. 270, 9698-9701
6. 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-trypsin inhibitor family. J. Biol. Chem. 267, 12380-12386
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. 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
9. Enghild, J. J., Salvesen, G., Hefta, S. A., Thøgersen, I. B., Rutherfurd, S., and Pizzo, S. V. (1991) Chondroitin 4-sulfate covalently cross-links the chains of the human blood protein pre-inhibitor. J. Biol. Chem. 266, 747-751
10. Yoneda, M., Suzuki, S., and Kimata, K. (1990) Hyaluronic acid associated with the surfaces of cultured fibroblasts is linked to a serum-derived 85-kDa protein. J. Biol. Chem. 265, 5247-5257
11. Sandson, J., Hamerman, D., and Schwick, G. (1965) Altered properties of pathological hyaluronate due to a bound inter trypsin inhibitor. Trans. Assoc. Am. Physicians 78, 304-313
12. 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. A study by inactivation of the bikunin gene in mice. J. Biol. Chem. 276, 7693-7696
13. 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
14. Gerdin, B., and HAllgren, R. (1997) Dynamic role of hyaluronan (HYA) in connective tissue activation and inflammation. J. Intern. Med. 242, 49-55
15. Zhuo, L., Salustri, A., and Kimata, K. (2002) A physiological function of serum proteoglycan bikunin: the chondroitin sulfate moiety plays a central role. Glycoconj. J. 19, 241-247
16. 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
17. Day, A. J., and de la Motte, C. A. (2005) Hyaluronan cross-linking: a protective mechanism in inflammation? Trends Immunol. 26, 637-643
18. Sanggaard, K. W., Scavenius, C., Rasmussen, A. J., Wisniewski, H.-G., Thogersen, I. B., and Enghild, J. J. (2010) The TSG-6/HC2-mediated transfer is a dynamic process shuffling heavy chains between glycosaminoglycans. J. Biol. Chem. 285, 21988-21993
19. Hutadilok, N., Ghosh, P., and Brooks, P. M. (1988) Binding of haptoglobin, inter-trypsin inhibitor, and 1 proteinase inhibitor to synovial fluid hyaluronate and the influence of these proteins on its degradation by oxygen derived free radicals. Ann. Rheum. Dis. 47, 377-385
20. 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
21. Kanayama, S., Yamada, Y., Onogi, A., Shigetomi, H., Ueda, S., Tsuji, Y., Haruta, S., Kawaguchi, R., Yoshida, S., Sakata, M., Sado, T., Kitanaka, T., Oi, H., Yagyu, T., and Kobayashi, H. (2008) Molecular structure and function analysis of bikunin on down-regulation of tumor necrosis factor expression in activated neutrophils. Cytokine 42, 191-197
22. He, H., Li, W., Tseng, D. Y., Zhang, S., Chen, S.-Y., Day, A. J., and Tseng, S. C. (2009) Biochemical characterization and function of complexes formed by hyaluronan and the heavy chains of inter-inhibitor (HC*HA) purified from extracts of human amniotic membrane. J. Biol. Chem. 284, 20136-20146
23. Kakizaki, I., Takahashi, R., Ibori, N., Kojima, K., Takahashi, T., Yamaguchi, M., Kon, A., and Takagaki, K. (2007) Diversity in the degree of sulfation and chain length of the glycosaminoglycan moiety of urinary trypsin inhibitor isomers. Biochim. Biophys. Acta 1770, 171-177
24. Yamada, S., Oyama, M., Yuki, Y., Kato, K., and Sugahara, K. (1995) The uniform galactose 4-sulfate structure in the carbohydrate-protein linkage region of human urinary trypsin inhibitor. Eur. J. Biochem. 233, 687-693
25. Yamada, S., Oyama, M., Kinugasa, H., Nakagawa, T., Kawasaki, T., Nagasawa, S., Khoo, K. H., Morris, H. R., Dell, A., and Sugahara, K. (1995) The sulphated carbohydrate-protein linkage region isolated from chondroitin 4-sulphate chains of inter-trypsin inhibitor in human plasma. Glycobiology 5, 335-341
26. Enghild, J. J., Thøgersen, I. B., Cheng, F., Fransson, L. A., Roepstorff, P., and Rahbek-Nielsen, H. (1999) Organization of the inter-inhibitor heavy chains on the chondroitin sulfate originating from Ser10 of bikunin: posttranslational modification of I-I-derived bikunin. Biochemistry 38, 11804-11813
27. Chi, L., Wolff, J. J., Laremore, T. N., Restaino, O. F., Xie, J., Schiraldi, C., Toida, T., Amster, I. J., and Linhardt, R. J. (2008) Structural analysis of bikunin glycosaminoglycan. J. Am. Chem. Soc. 130, 2617-2625
28. Toyoda, H., Kobayashi, S., Sakamoto, S., Toida, T., and Imanari, T. (1993) Structural analysis of a low-sulfated chondroitin sulfate chain in human urinary trypsin inhibitor. Biol. Pharm. Bull. 16, 945-947
29. Mizon, C., Mairie, C., Balduyck, M., Hachulla, E., and Mizon, J. (2001) The chondroitin sulfate chain of bikunin-containing proteins in the inter-inhibitor family increases in size in inflammatory diseases. Eur. J. Biochem. 268, 2717-2724
30. Fujimoto, T., Savani, R. C., Watari, M., Day, A. J., and Strauss, J. F. (2002) Induction of the hyaluronic acid-binding protein, tumor necrosis factorstimulated gene-6, in cervical smooth muscle cells by tumor necrosis factor-and prostaglandin E2. Am. J. Pathol. 160, 1495-1502
31. 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
32. Melrose, J., Numata, Y., and Ghosh, P. (1996) Biotinylated hyaluronan: a versatile and highly sensitive probe capable of detecting nanogram levels of hyaluronan binding proteins (hyaladherins) on electroblots by a novel affinity detection procedure. Electrophoresis 17, 205-212
33. Lehrman, M. A., and Gao, N. (2003) Alternative and sources of reagents and supplies of fluorophore-assisted carbohydrate electrophoresis (FACE). Glycobiology 13, 1G-3G
34. Calabro, A., Benavides, M., Tammi, M., Hascall, V. C., and Midura, R. J. (2000) Microanalysis of enzyme digests of hyaluronan and chondroitin/ dermatan sulfate by fluorophore-assisted carbohydrate electrophoresis (FACE). Glycobiology 10, 273-281
35. Klock, J. C., and Starr, C. M. (1998) Polyacrylamide gel electrophoresis of fluorophore-labeled carbohydrates from glycoproteins. Methods Mol. Biol. 76, 115-129
36. Melrose, J. (2001) Cartilage and smooth muscle cell proteoglycans detected by affinity blotting using biotinylated hyaluronan. Methods Mol. Biol. 171, 53-66
37. 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
38. Pugia, M. J., and Lott, J. A. (2005) Pathophysiology and diagnostic value of urinary trypsin inhibitors. Clin. Chem. Lab. Med. 43, 1-16
39. Itoh, Y., and Kawai, T. (1990) Human 1-microglobulin: its measurement and clinical significance. J. Clin. Lab. Anal. 4, 376-384
40. 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-trypsin inhibitor heavy chains which are attached to a chondroitin sulfate proteoglycan other than bikunin. Osteoarthritis Cartilage 16, 1343-1355
41. Forteza, R., Casalino-Matsuda, S. M., Monzon, M. E., Fries, E., Rugg, M. S., Milner, C. M., and Day, A. J. (2007) TSG-6 potentiates the antitissue kallikrein activity of inter-inhibitor through bikunin release. Am. J. Respir. Cell Mol. Biol. 36, 20-31
42. Thomas, G. J., Yung, S., and Davies, M. (1998) Bikunin present in human peritoneal fluid is in part derived from the interaction of serum with peritoneal mesothelial cells. Am. J. Pathol. 153, 1267-1276
43. Ochiai, H., Toyoda, H., and Onodera, M. (1988) Analysis of chondroitin sulfates in human urinary trypsin inhibitor. Chem. Pharm. Bull. 36, 3726-3727
44. Ly, M., Leach, F. E., 3rd, Laremore, T. N., Toida, T., Amster, I. J., and Linhardt, R. J. (2011) The proteoglycan bikunin has a defined sequence. Nat. Chem. Biol. 7, 827-833
45. Laremore, T. N., Leach, F. E., 3rd, Amster, I. J., and Linhardt, R. J. (2011) Electrospray ionization Fourier transform mass spectrometric analysis of intact bikunin glycosaminoglycan from normal human plasma. Int. J. Mass Spectrom. 305, 109-115
46. Couchman, J. R., Caterson, B., Christner, J. E., and Baker, J. R. (1984) Mapping by monoclonal antibody detection of glycosaminoglycans in connective tissues. Nature 307, 650-652
47. Yuki, Y., Nomura, K., Kirihara, M., Shimomura, M., Hiratani, H., Nishimura, R., and Kato, K. (1993) Charge isomers of urinary bikunin (trypsin inhibitor). Biochim. Biophys. Acta 1203, 298-303
48. 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
49. Chen, L., Zhang, H., Powers, R. W., Russell, P. T., and Larsen, W. J. (1996) Covalent linkage between proteins of the inter-inhibitor family and hyaluronic acid is mediated by a factor produced by granulosa cells. J. Biol. Chem. 271, 19409-19414
50. 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 x TSG-6 complexes. Biochemistry 45, 7661-7668
51. Colón, E., Shytuhina, A., Cowman, M. K., Band, P. A., Sanggaard, K. W., Enghild, J. J., and Wisniewski, H. G. (2009) Transfer of inter-inhibitor heavy chains to hyaluronan by surface-linked hyaluronan-TSG-6 complexes. J. Biol. Chem. 284, 2320-2331
52. Mukhopadhyay, D., Asari, A., Rugg, M. S., Day, A. J., and Fülöp, C. (2004) Specificity of the tumor necrosis factor-induced protein 6-mediated heavy chain transfer from inter-trypsin inhibitor to hyaluronan: implications for the assembly of the cumulus extracellular matrix. J. Biol. Chem. 279, 11119-11128
53. Capon, C., Mizon, C., Lemoine, J., Rodié-Talbère, P., and Mizon, J. (2003) In acute inflammation, the chondroitin-4 sulphate carried by bikunin is not only longer, it is also undersulphated. Biochimie 85, 101-107
54. Sanggaard, K. W., Karring, H., Valnickova, Z., Thøgersen, I. B., and Enghild, J. J. (2005) The TSG-6 and I-I interaction promotes a transesterification cleaving the protein-glycosaminoglycan-protein (PGP) cross-link. J. Biol. Chem. 280, 11936-11942
55. Zhu, L., Zhuo, L., Watanabe, H., and Kimata, K. (2008) Equivalent involvement of inter-trypsin inhibitor heavy chain isoforms in forming covalent complexes with hyaluronan. Connect. Tissue Res. 49, 48-55
56. Bost, F., Diarra-Mehrpour, M., and Martin, J. P. (1998) Inter-trypsin inhibitor proteoglycan family-a group of proteins binding and stabilizing the extracellular matrix. Eur. J. Biochem. 252, 339-346
57. 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