Serglycin proteoglycan is required for secretory granule integrity in mucosal mast cells

Biochemical Journal

Volumn 403, Issue 1, 2007, Pages 49-57

  Braga, Tiago ^a   Grujic, Mirjana ^a   Lukinius, Agneta ^b   Hellman, Lars ^c   Åbrink, Magnus ^a   Pejler, Gunnar ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

Chymase; Mast cell; Protease; Proteoglycan; Serglycin; Tryptase

Indexed keywords

CHYMASE; MAST CELLS; PROTEASE; PROTEOGLYCAN; SERGLYCIN; TRYPTASE;

BIOMARKERS; BIOSYNTHESIS; GENES; PROTEINS; RATS; TISSUE;

CELLS;

CARBOXYPEPTIDASE A; PROTEOGLYCAN; SERGLYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; IN VITRO STUDY; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECRETORY GRANULE;

ANIMALS; BONE MARROW CELLS; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; INTESTINAL MUCOSA; MAST CELLS; MICE; MICE, INBRED C57BL; MUCOUS MEMBRANE; PROTEOGLYCANS; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SECRETORY VESICLES; VESICULAR TRANSPORT PROTEINS;

MUS;

EID: 34147144149     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061257     Document Type: Article

References (46)

1. Ha, T. Y., Reed, N. D. and Crowle, P. K. (1983) Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice. Infect. Immun. 41, 445-447
2. Oku, Y., Itayama, H. and Kamiya, M. (1984) Expulsion of Trichinella spiralis from the intestine of W/Wv mice reconstituted with haematopoietic and lymphopoietic cells and origin of mucosal mast cells. Immunology 53, 337-344
3. Nawa, Y., Kiyota, M., Korenaga, M. and Kotani, M. (1985) Defective protective capacity of W/Wv mice against Strongyloides ratti infection and its reconstitution with bone marrow cells. Parasite Immunol. 7, 429-438
4. Malaviya, R., Ikeda, T., Ross, E. and Abraham, S. N. (1996) Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-α. Nature 381, 77-80
5. Echtenacher, B., Mannel, D. N. and Hultner, L. (1996) Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381, 75-77
6. Galli, S. J., Nakae, S. and Tsai, M. (2005) Mast cells in the development of adaptive immune responses. Nat. Immunol. 6, 135-142
7. Metcalfe, D. D., Baram, D. and Mekori, Y. A. (1997) Mast cells. Physiol. Rev. 77, 1033-1079
8. Lutzelschwab, C., Lunderius, C., Enerback, L. and Hellman, L. (1998) A kinetic analysis of the expression of mast cell protease mRNA in the intestines of Nippostrongylus brasiliensis-infected rats. Eur. J. Immunol. 28, 3730-3737
9. Miller, H. R. (1996) Mucosal mast cells and the allergic response against nematode parasites. Vet. Immunol. Immunopathol. 54, 331-336
10. Mayrhofer, G. and Fisher, R. (1979) Mast cells in severely T-cell depleted rats and the response to infestation with Nippostrongylus brasiliensis. Immunology 37, 145-155
11. Ruitenberg, E. J. and Elgersma, A. (1976) Absence of intestinal mast cell response in congenitally athymic mice during Trichinella spiralis infection. Nature 264, 258-260
12. Aldenborg, F. and Enerback, L. (1985) Thymus dependence of connective tissue mast cells: a quantitative cytofluorometric study of the growth of peritoneal mast cells in normal and athymic rats. Int. Arch. Allergy Appl. Immunol. 78, 277-282
13. Welle, M. (1997) Development, significance, and heterogeneity of mast cells with particular regard to the mast cell-specific proteases chymase and tryptase. J. Leukocyte Biol. 61, 233-245
14. 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
15. Caughey, G. (2001) New developments in the genetics and activation of mast cell proteases. Mol. Immunol. 38, 1353-1357
16. Reynolds, D. S., Stevens, R. L., Lane, W. S., Carr, M. H., Austen, K. F. and Serafin, W. E. (1990) Different mouse mast cell populations express various combinations of at least six distinct mast cell serine proteases. Proc. Natl. Acad. Sci. U.S.A. 87, 3230-3234
17. Serafin, W. E., Dayton, E. T., Gravallese, P. M., Austen, K. F. and Stevens, R. L. (1987) Carboxypeptidase A in mouse mast cells: identification, characterization, and use as a differentiation marker. J. Immunol. 139, 3771-3776
18. 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
19. Trong, H. L., Newlands, G. F., Miller, H. R., Charbonneau, H., Neurath, H. and Woodbury, R. G. (1989) Amino acid sequence of a mouse mucosal mast cell protease. Biochemistry 28, 391-395
20. 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
21. Friend, D. S., Ghildyal, N., Gurish, M. F., Hunt, J., Hu, X., Austen, K. F. and Stevens, R. L. (1998) Reversible expression of tryptases and chymases in the jejunal mast cells of mice infected with Trichinella spiralis. J. Immunol. 160, 5537-5545
22. Friend, D. S., Ghildyal, N., Austen, K. F., Gurish, M. F., Matsumoto, R. and Stevens, R. L. (1996) Mast cells that reside at different locations in the jejunum of mice infected with Trichinella spiralis exhibit sequential changes in their granule ultrastructure and chymase phenotype. J. Cell Biol. 135, 279-290
23. Haig, D. M., Huntley, J. F., MacKellar, A., Newlands, G. F., Inglis, L., Sangha, R., Cohen, D., Hapel, A., Galli, S. J. and Miller, H. R. (1994) Effects of stem cell factor (kit-ligand) and interleukin-3 on the growth and serine proteinase expression of rat bone-marrow-derived or serosal mast cells. Blood 83, 72-83
24. Gurish, M. F., Ghildyal, N., McNeil, H. P., Austen, K. F., Gillis, S. and Stevens, R. L. (1992) Differential expression of secretory granule proteases in mouse mast cells exposed to interleukin 3 and c-kit ligand. J. Exp. Med. 175, 1003-1012
25. Yurt, R. W., Leid, Jr, R. W. and Austen, K. F. (1977) Native heparin from rat peritoneal mast cells. J. Biol. Chem. 252, 518-521
26. Enerback, L., Kolset, S. O., Kusche, M., Hjerpe, A. and Lindahl, U. (1985) Glycosaminoglycans in rat mucosal mast cells. Biochem. J. 227, 661-668
27. Forsberg, E., Pejler, G., Ringvall, M., Lunderius, C., Tomasini-Johansson, B., Kusche-Gullberg, M., Eriksson, I., Ledin, J., Hellman, L. and Kjellen, L. (1999) Abnormal mast cells in mice deficient in a heparin-synthesizing enzyme. Nature 400, 773-776
28. 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
29. Henningsson, F., Ledin, J., Lunderius, C., Wilen, 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
30. Abrink, M., Grujic, M. and Pejler, G. (2004) Serglycin is essential for maturation of mast cell secretory granule. J. Biol. Chem. 279, 40897-40905
31. Miller, H. R., Wright, S. H., Knight, P. A. and Thornton, E. M. (1999) A novel function for transforming growth factor-β1: upregulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific β-chymase, mouse mast cell protease-1. Blood 93, 3473-3486
32. Fajardo, I. and Pejler, G. (2003) Human mast cell β-tryptase is a gelatinase. J. Immunol. 171, 1493-1499
33. Skokos, D., Botros, H. G., Demeure, C., Morin, J., Peronet, R., Birkenmeier, G., Boudaly, S. and Mecheri, S. (2003) Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J. Immunol. 170, 3037-3045
34. Raposo, G., Tenza, D., Mecheri, S., Peronet, R., Bonnerot, C. and Desaymard, C. (1997) Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol. Biol. Cell 8, 2631-2645
35. Lukinius, A. and Korsgren, O. (2001) The transplanted fetal endocrine pancreas undergoes an inherent sequential differentiation similar to that in the native pancreas: an ultrastructural study in the pig-to-mouse model. Diabetes 50, 962-971
36. Zemichow, L., Abrink, M., Hallgren, J., Grujic, M., Pejler, G. and Kolset, S. O. (2006) Serglycin is the major secreted proteoglycan in macrophages and has a role in the regulation of macrophage tumor necrosis factor-α secretion in response to lipopolysaccharide. J. Biol. Chem. 281, 26792-26801
37. Huntley, J. F., Newlands, G. F., Gibson, S., Ferguson, A. and Miller, H. R. (1985) Histochemical demonstration of chymotrypsin like serine esterases in mucosal mast cells in four species including man. J. Clin. Pathol. 38, 375-384
38. 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
39. Fang, K. C., Raymond, W. W., Lazarus, S. C. and Caughey, G. H. (1996) Dog mastocytoma cells secrete a 92-kD gelatinase activated extracellularly by mast cell chymase. J. Clin. Invest. 97, 1589-1596
40. Sali, A., Matsumoto, R., McNeil, H. P., Karplus, M. and Stevens, R. L. (1993) Three-dimensional models of four mouse mast cell chymases: identification of proteoglycan binding regions and protease-specific antigenic epitopes. J. Biol. Chem. 268, 9023-9034
41. Grujic, M., Braga, T., Lukinius, A., Eloranta, M. L., Knight, S. D., Pejler, G. and Abrink, M. (2005) Serglycin-deficient cytotoxic T lymphocytes display defective secretory granule maturation and granzyme B storage. J. Biol. Chem. 280, 33411-33418
42. Hallgren, J., Bäckström, S., Estrada, S., Thuveson, M. and Pejler, G. (2004) Histidines are critical for heparin-dependent activation of mast cell tryptase. J. Immunol. 173, 1868-1875
43. Ghildyal, N., Friend, D. S., Stevens, R. L., Austen, K. F., Huang, C., Penrose, J. F., Sali, A. and Gurish, M. F. (1996) Fate of two mast cell tryptases in V3 mastocytosis and normal BALB/c mice undergoing passive systemic anaphylaxis: prolonged retention of exocytosed mMCP-6 in connective tissues, and rapid accumulation of enzymatically active mMCP-7 in the blood. J. Exp. Med. 184, 1061-1073
44. Wastling, J. M., Scudamore, C. L., Thornton, E. M., Newlands, G. F. and Miller, H. R. (1997) Constitutive expression of mouse mast cell protease-1 in normal BALB/c mice and its up-regulation during intestinal nematode infection. Immunology 90, 308-313
45. Brown, J. K., Knight, P. A., Wright, S. H., Thornton, E. M. and Miller, H. R. (2003) Constitutive secretion of the granule chymase mouse mast cell protease-1 and the chemokine, CCL2, by mucosal mast cell homologues. Clin. Exp. Allergy 33, 132-146
46. Henningsson, F., Hergeth, S., Cortelius, R., Abrink, M. and Pejler, G. (2006) A role for serglycin proteoglycan in granular retention and processing of mast cell secretory granule components. FEBS J. 273, 4901-4912