Heparan sulfate 6-O-sulfotransferase isoform-dependent regulatory effects of heparin on the activities of various proteases in mast cells and the biosynthesis of 6-O-sulfated heparin

Journal of Biological Chemistry

Volumn 288, Issue 6, 2013, Pages 3705-3717

  Anower E Khuda, Md Ferdous ^a   Habuchi, Hiroko ^a   Nagai, Naoko ^a   Habuchi, Osami ^a   Yokochi, Takashi ^a   Kimata, Koji ^a  

^a AICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; CELLS; CYTOLOGY; ELECTROPHORESIS; ENZYMES; MUSCULOSKELETAL SYSTEM; POLYSACCHARIDES; SULFUR COMPOUNDS;

CONNECTIVE TISSUES; HEPARAN SULPHATE; ISOFORMS; MAST CELLS; MRNA EXPRESSION; PROTEASE ACTIVITIES; REGULATORY EFFECTS; SULPHATION; WESTERN-BLOT ANALYSIS; WILD TYPES;

COLLAGEN;

CARBOXYPEPTIDASE A; CHYMASE; HEPARAN SULFATE 6 O SULFOTRANSFERASE; HEPARAN SULFATE 6 O SULFOTRANSFERASE 1; HEPARAN SULFATE 6 O SULFOTRANSFERASE 2; HEPARIN; MESSENGER RNA; SULFOTRANSFERASE; TRYPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CELL CULTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME RELEASE; FETUS; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SULFATION;

EID: 84873635679     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.416651     Document Type: Article

References (69)

1. Esko, J. D., and Lindahl, U. (2001) Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173
2. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lince-cum, J., and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777
3. Perrimon, N., and Bernfield, M. (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725-728
4. Grobe, K., Ledin, J., Ringvall, M., Holmborn, K., Forsberg, E., Esko, J. D., and Kjellén, L. (2002) Heparan sulfate and development: differential roles of the N-acetylglucosamine N-deacetylase/N-sulfotransferase isozymes. Biochim. Biophys. Acta 1573, 209-215
5. Esko, J. D., and Selleck, S. B. (2002) Order out of chaos. Assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471
6. Habuchi, H., Habuchi, O., and Kimata, K. (2004) Sulfation pattern in gly-cosaminoglycan. Does it have a code? Glycoconj. J. 21, 47-52
7. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate pro-teoglycans fine-tune mammalian physiology. Nature 446, 1030-1037
8. Habuchi, H., Tanaka, M., Habuchi, O., Yoshida, K., Suzuki, H., Ban, K., and Kimata, K. (2000) The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J. Biol. Chem. 275, 2859-2868
9. Habuchi, H., and Kimata, K. (2010) Mice deficient in heparan sulfate 6-O-sulfotransferase-1. Prog. Mol. Biol. Transl. Sci. 93, 79-111
10. Habuchi, H., Miyake, G., Nogami, K., Kuroiwa, A., Matsuda, Y., Kusche-Gullberg, M., Habuchi, O., Tanaka, M., and Kimata, K. (2003) Biosynthesis of heparan sulphate with diverse structures and functions. Two alternatively spliced forms of human heparan sulphate 6-O-sulphotransferase-2 having different expression patterns and properties. Biochem. J. 371, 131-142
11. Habuchi, H., Nagai, N., Sugaya, N., Atsumi, F., Stevens, R. L., and Kimata, K. (2007) Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J. Biol. Chem. 282, 15578-15588
12. Izvolsky, K.I., Lu, J., Martin, G., Albrecht, K.H., and Cardoso, W. V. (2008) Systemic inactivation of Hs6st1 in mice is associated with late postnatal mortality without major defects in organogenesis. Genesis 46, 8-18
13. Pratt, T., Conway, C. D., Tian, N. M., Price, D. J., and Mason, J. O. (2006) Heparan sulphation patterns generated by specific heparan sulfotrans-ferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm. J. Neurosci. 26, 6911-6923
14. Tornberg, J., Sykiotis, G. P., Keefe, K., Plummer, L., Hoang, X., Hall, J. E., Quinton, R., Seminara, S. B., Hughes, V., Van Vliet, G., Van Uum, S., Crowley, W. F., Habuchi, H., Kimata, K., Pitteloud, N., and Bülow, H. E. (2011) Heparan sulfate 6-O-sulfotransferase 1, a gene involved in extracellular sugar modifications, is mutated in patients with idiopathic hy-pogonadotrophic hypogonadism. Proc. Natl. Acad. Sci. U.S.A. 108, 11524-11529
15. Bink, R. J., Habuchi, H., Lele, Z., Dolk, E., Joore, J., Rauch, G. J., Geisler, R., Wilson, S. W., den Hertog, J., Kimata, K., and Zivkovic, D. (2003) Heparan sulfate 6-O-sulfotransferase is essential for muscle development in ze-brafish. J. Biol. Chem. 278, 31118-31127
16. Chen, E., Stringer, S. E., Rusch, M. A., Selleck, S. B., and Ekker, S. C. (2005) A unique role for 6-O-sulfation modification in zebrafish vascular development. Dev. Biol. 284, 364-376
17. Bülow, H. E., and Hobert, O. (2004) Differential sulfations and epimeriza-tion define heparan sulfate specificity in nervous system development. Neuron 41, 723-736
18. Kamimura, K., Fujise, M., Villa, F., Izumi, S., Habuchi, H., Kimata, K., and Nakato, H. (2001) Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST) gene. Structure, expression, and function in the formation of the tracheal system. J. Biol. Chem. 276, 17014-17021
19. Kamimura, K., Koyama, T., Habuchi, H., Ueda, R., Masu, M., Kimata, K., and Nakato, H. (2006) Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J. Cell Biol. 174, 773-778
20. Kobayashi, T., Habuchi, H., Nogami, K., Ashikari-Hada, S., Tamura, K., Ide, H., and Kimata, K. (2010) Functional analysis of chick heparan sulfate 6-O-sulfotransferases in limb bud development. Dev. Growth Differ. 52, 146-156
21. Sugaya, N., Habuchi, H., Nagai, N., Ashikari-Hada, S., and Kimata, K. (2008) 6-O-Sulfation of heparan sulfate differentially regulates various fibroblast growth factor-dependent signalings in culture. J. Biol. Chem. 283, 10366-10376
22. Xing, W., Austen, K. F., Gurish, M. F., and Jones, T. G. (2011) Protease phenotype of constitutive connective tissue and of induced mucosal mast cells in mice is regulated by the tissue. Proc. Natl. Acad. Sci. U.S.A. 108, 14210-14215
23. Metcalfe, D. D., Baram, D., and Mekori, Y. A. (1997) Mast cells. Physiol. Rev. 77, 1033-1079
24. Pejler, G., Rönnberg, E., Waern, I., and Wernersson, S. (2010) Mast cell proteases. Multifaceted regulators of inflammatory disease. Blood 115, 4981-4990
25. Welle, M. (1997) Development, significance, and heterogeneity of mast cells with particular regardto the mast cell-specific proteases chymase and tryptase. J. Leukocyte Biol. 61, 233-245
26. Coussens, L. M., Raymond, W. W., Bergers, G., Laig-Webster, M., Beh-rendtsen, O., Werb, Z., Caughey, G. H., and Hanahan, D. (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 13, 1382-1397
27. Miller, H. R., and Pemberton, A. D. (2002) Tissue-specific expression of mast cell granule serine proteinases and their role in inflammation in the lung and gut. Immunology 105, 375-390
28. Kolset, S. O., Prydz, K., and Pejler, G. (2004) Intracellular proteoglycans. BiochemJ. 379, 217-227
29. Prieto-García, A., Zheng, D., Adachi, R., Xing, W., Lane, W. S., Chung, K., Anderson, P., Hansbro, P. M., Castells, M., and Stevens, R. L. (2012) Mast cell-restricted mouse and human tryptase-heparin complexes hinder thrombin-induced coagulation of plasma and the generation of fibrin by proteolytically destroying fibrinogen. J. Biol. Chem. 287, 7834-7844
30. McNeil, H. P., Adachi, R., and Stevens, R. L. (2007) Mast cell-restricted tryptases. Structure and function in inflammation and pathogen defense. J. Biol. Chem. 282, 20785-20789
31. Enerbäck, L., Kolset, S. O., Kusche, M., Hjerpe, A., and Lindahl, U. (1985) Glycosaminoglycans in rat mucosal mast cells. Biochem. J. 227, 661-668
32. Kolset, S. O., and Tveit, H. (2008) Serglycin-structure and biology. Cell. Mol. Life Sci. 65, 1073-1085
33. Forsberg, E., Pejler, G., Ringvall, M., Lunderius, C., Tomasini-Johansson, B., Kusche-Gullberg, M., Eriksson, I., Ledin, J., Hellman, L., and Kjellén, L. (1999) Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400, 773-776
34. Humphries, D. E., Wong, G. W., Friend, D. S., Gurish, M. F., Qiu, W.-T., Huang, C., Sharpe, A. H, and Stevens, R. L. (1999) Heparin is essential for the storage of specific granule proteases in mast cells. Nature 400, 769-772
35. Feyerabend, T. B., Li, J. P., Lindahl, U., and Rodewald, H. R. (2006) Heparan sulfate C5-epimerase is essential for heparin biosynthesis in mast cells. Nat. Chem. Biol. 2, 195-196
36. HajMohammadi, S., Enjyoji, K., Princivalle, M., Christi, P., Lech, M., Beeler, D., Rayburn, H, Schwartz, J. J., Barzegar, S., de Agostini, A. I., Post, M. J., Rosenberg, R. D., and Shworak, N. W. (2003) Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. J. Clin. Invest. 111, 989-999
37. Yamada, N, Matsushima, H., Tagaya, Y., Shimada, S., and Katz, S. I. (2003) Generation of a large number of connective tissue type mast cells by culture of murine fetal skin cells. J. Invest. Dermatol. 121, 1425-1432
38. Toyoda, H., Kinoshita-Toyoda, A., and Selleck, S. B. (2000) Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo. J. Biol. Chem. 275, 2269-2275
39. Stevens, R. L., and Adachi, R. (2007) Protease-proteoglycan complexes of mouse and human mast cells and importance of their β-tryptase-heparin complexes in inflammation and innate immunity. Immunol. Rev. 217, 155-167
40. Ohtake-Niimi, S., Kondo, S., Ito, T., Kakehi, S., Ohta, T., Habuchi, H., Kimata, K., and Habuchi, O. (2010) Mice deficient in N-acetylgalac-tosamine 4-sulfate 6-O-sulfotransferase are unable to synthesize chon-droitin/dermatan sulfate containing N-acetylgalactosamine 4, 6-bissulfate residues and exhibit decreased protease activity in bone marrow-derived mast cells. J. Biol. Chem. 285, 20793-20805
41. Hunt, J. E., Stevens, R. L., Austen, K. F., Zhang, J., Xia, Z., and Ghildyal, N. (1996) Natural disruption of the mouse mast cell protease 7 gene in the C57BL/6 mouse. J. Biol. Chem. 271, 2851-2855
42. Abrink, M., Grujic, M., and Pejler, G. (2004) Serglycin is essential for maturation of mast cell secretory granule. J. Biol. Chem. 279, 40897-40905
43. Hallgren, J., Karlson, U., Poorafshar, M., Hellman, L., and Pejler, G. (2000) Mechanism for activation of mouse mast cell tryptase. Dependence on heparin and acidic pH for formation of active tetramers of mouse mast cell protease 6. Biochemistry 39, 13068-13077
44. Hallgren, J., Spillmann, D., and Pejler, G. (2001) Structural requirements and mechanism for heparin-induced activation of a recombinant mouse mast cell tryptase, mouse mast cell protease-6. Formation of active tryp-tase monomers in the presence of low molecular weight heparin. J. Biol. Chem. 276, 42774-42781
45. Razin, E., Stevens, R. L., Akiyama, F., Schmid, K., and Austen, K. F. (1982) Culture from mouse bone marrow of a subclass of mast cells possessing a distinct chondroitin sulfate proteoglycan with glycosaminoglycans rich in N-acetylgalactosamine-4, 6-disulfate. J. Biol. Chem. 257, 7229-7236
46. Henningsson, F., Ledin, J., Lunderius, C., Wilén, M., Hellman, L., and Pejler, G. (2002) Altered storage of proteases in mast cells from mice lacking heparin. A possible role for heparin in carboxypeptidase A processing. Biol. Chem. 383, 793-801
47. Pejler, G., Abrink, M., Ringvall, M., and Wernersson, S. (2007) Mast cell proteases. Adv. Immunol. 95, 167-255
48. Thompson, H. L., Schulman, E. S., and Metcalfe, D. D. (1988) Identification of chondroitin sulfate E in human lung mast cells. J. Immunol. 140, 2708-2713
49. Stevens, R. L., Fox, C. C., Lichtenstein, L. M., and Austen, K. F. (1988) Identification of chondroitin sulfate E proteoglycans and heparin pro-teoglycans in the secretory granules of human lung mast cells. Proc. Natl. Acad. Sci. U.S.A. 85, 2284-2287
50. Lidholt, K., Eriksson, I., and Kjellén, L. (1995) Heparin proteoglycans synthesized bymouse mastocytoma contain chondroitin sulphate. Biochem. J. 311, 233-238
51. Henningsson, F., Hergeth, S., Cortelius, R., Abrink, M., and Pejler, G. (2006) A role for serglycin proteoglycan in granular retention and proc-essingof mast cell secretory granule components. FEBS J.273, 4901-4912
52. Henningsson, F., Yamamoto, K., Saftig, P., Reinheckel, T., Peters, C., Knight, S. D., and Pejler, G. (2005) A role for cathepsin E in the processing of mast-cell carboxypeptidase A. J. Cell Sci. 118, 2035-2042
53. Dragonetti, A., Baldassarre, M., Castino, R., Démoz, M., Luini, A., Buc-cione, R., and Isidoro, C. (2000) The lysosomal protease cathepsin D is efficiently sorted to and secreted from regulated secretory compartments in the rat basophilic/mast cell line RBL. J. Cell Sci. 113, 3289-3298
54. Wolters, P. J., Laig-Webster, M., and Caughey, G. H. (2000) Dipeptidyl peptidase I cleaves matrix-associated proteins and is expressed mainly by mast cells innormal dog airways. Am. J. Respir. Cell Mol. Biol. 22, 183-190
55. von Heijne, G. (1984) How signal sequences maintain cleavage specificity. J. Mol. Biol. 173, 243-251
56. Reynolds, D. S., Gurley, D. S., Austen, K. F., and Serafin, W. E. (1991) Cloning of the cDNA and gene of mouse mast cell protease-6. Transcription by progenitor mast cells and mast cells of the connective tissue subclass. J. Biol. Chem. 266, 3847-3853
57. Sakai, K., Ren, S., and Schwartz, L. B. (1996) A novel heparin-dependent processing pathway for human tryptase. Autocatalysis followed by activation with dipeptidyl peptidase I. J. Clin. Invest. 97, 988-995
58. Huang, R. Y., Blom, T., and Hellman, L. (1991) Cloning and structural analysis of MMCP-1, MMCP-4, and MMCP-5, three mouse mast cell-specific serine proteases. Eur. J. Immunol. 21, 1611-1621
59. Serafin, W. E., Reynolds, D. S., Rogelj, S., Lane, W. S., Conder, G. A., Johnson, S. S., Austen, K. F., and Stevens, R. L. (1990) Identification and molecular cloning of a novel mouse mucosal mast cell serine protease. J. Biol. Chem. 265, 423-429
60. Pejler, G., Knight, S. D., Henningsson, F., and Wernersson, S.(2009) Novel insights into the biological function of mast cell carboxypeptidase A. Trends Immunol. 8, 401-408
61. Feyerabend, T. B., Hausser, H., Tietz, A., Blum, C., Hellman, L., Straus, A. H., Takahashi, H. K., Morgan, E. S., Dvorak, A. M., Fehling, H. J., and Rodewald, H. (2005) Loss of histochemical identity in mast cells lacking carboxypeptidase A. Mol. Cell Biol. 25, 6199-6210
62. Knight, P. A., Wright, S. H., Lawrence, C. E., Paterson, Y. Y., and Miller, H. R. (2000) Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. J. Exp. Med. 192, 1849-1856
63. Orinska, Z., Maurer, M., Mirghomizadeh, F., Bulanova, E., Metz, M., Nashkevich, N., Schiemann, F., Schulmistrat, J., Budagian, V., Giron-Michel, J., Brandt, E., Paus, R., and Bulfone-Paus, S. (2007) IL-15 constrains mast cell-dependent antibacterial defenses by suppressing chymase activities. Nat. Med. 13, 927-934
64. Sun, J., Zhang, J., Lindholt, J. S., Sukhova, G. K., Liu, J., He, A., Abrink, M., Pejler, G., Stevens, R. L., Thompson, R. W., Ennis, T. L., Gurish, M. F., Libby, P., and Shi, G. P. (2009) Critical role of mast cell chymase in mouse abdominal aortic aneurysm formation. Circulation 120, 973-982
65. Schneider, L. A., Schlenner, S. M., Feyerabend, T. B., Wunderlin, M., and Rodewald, H. R. (2007) Molecular mechanism of mast cell mediated innate defense against endothelin and snake venom sarafotoxin. J. Exp. Med. 204, 2629-2639
66. Metz, M., Piliponsky, A. M., Chen, C. C., Lammel, V., Abrink, M., Pejler, G., Tsai, M., and Galli, S. J. (2006) Mast cells can enhance resistance to snake and honeybee venoms. Science 313, 526-530
67. Shin, K., Watts, G. F., Oettgen, H. C., Friend, D. S., Pemberton, A. D., Gurish, M. F., and Lee, D. M. (2008) Mouse mast cell tryptase mMCP-6 is a critical link between adaptive and innate immunity in the chronic phase of Trichinella spiralis infection. J. Immunol. 180, 4885-4891
68. Thakurdas, S. M., Melicoff, E., Sansores-Garcia, L., Moreira, D. C., Petrova, Y., Stevens, R. L., and Adachi, R. (2007) The mast cell-restricted tryptase mMCP-6 has a critical immunoprotective role in bacterial infections. J. Biol. Chem. 282, 20809-20815
69. Shin, K., Nigrovic, P. A., Crish, J., Boilard, E., McNeil, H. P., Larabee, K. S., Adachi, R., Gurish, M. F., Gobezie, R., Stevens, R. L., and Lee, D. M. (2009) Mast cells contribute to autoimmune inflammatory arthritis via their tryptase/heparin complexes. J. Immunol. 182, 647-656