Serglycin proteoglycan: Regulating the storage and activities of hematopoietic proteases

BioFactors

Volumn 35, Issue 1, 2009, Pages 61-68

  Pejler, Gunnar ^a   Åbrink, Magnus ^b   Wernersson, Sara ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Hematopoietic cells; Mast cells; Proteases; Proteoglycans; Serglycin

Indexed keywords

PROTEINASE; PROTEOGLYCAN; SERGLYCIN; TRYPTASE; UNCLASSIFIED DRUG; PEPTIDE HYDROLASE; VESICULAR TRANSPORT PROTEIN;

ANIMAL EXPERIMENT; BIOGENESIS; BLOOD CLOTTING; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME ACTIVITY; ENZYME REGULATION; HEMATOPOIETIC CELL; IMMUNOREGULATION; MACROPHAGE; MAST CELL; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SECRETORY GRANULE; THROMBOCYTE; ANIMAL; BLOOD CELL; ENZYMOLOGY; METABOLISM; MOUSE;

MUS;

ANIMALS; BLOOD CELLS; MAST CELLS; MICE; PEPTIDE HYDROLASES; PROTEOGLYCANS; VESICULAR TRANSPORT PROTEINS;

EID: 65549115455     PISSN: 09516433     EISSN: None     Source Type: Journal    
DOI: 10.1002/biof.11     Document Type: Review

References (58)

1. Iozzo, R. V. (1998) Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67, 609-652.
2. Bernfield, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J., and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777.
3. Kolset, S. O., Prydz, K., and Pejler, G. (2004) Intracellular proteoglycans. Biochem. J. 379, 217-227.
4. Bourdon, M. A., Oldberg, A., Pierschbacher, M., and Ruoslahti, E. (1985) Molecular cloning and sequence analysis of a chondroitin sulfate proteoglycan cDNA. Proc. Natl. Acad. Sci. USA 82, 1321-1325. (Pubitemid 15111044)
5. Kjellén, L., Pettersson, I., Lillhager, P., Steen, M. L., Pettersson, U., Lehtonen, P., Karlsson, T., Ruoslahti, E., and Hellman, L. (1989) Primary structure of a mouse mastocytoma proteoglycan core protein. Biochem. J. 263, 105-113.
6. Stevens, R. L., Fox, C. C., Lichtenstein, L. M., and Austen, K. F. (1988) Identification of chondroitin sulfate E proteoglycans and heparin proteoglycans in the secretory granules of human lung mast cells. Proc. Natl. Acad. Sci. USA 85, 2284-2287.
7. Kolset, S. O. and Tveit, H. (2008) Serglycin-structure and biology. Cell Mol. Life Sci. 65, 1073-1085.
8. Tantravahi, R. V., Stevens, R. L., Austen, K. F., and Weis, J. H. (1986) A single gene in mast cells encodes the core peptides of heparin and chondroitin sulfate proteoglycans. Proc. Natl. Acad. Sci. USA 83, 9207-9210.
9. Schmidt, R. E., MacDermott, R. P., Bartley, G., Bertovich, M., Amato, D. A., Austen, K. F., Schlossman, S. F., Stevens, R. L., and Ritz, J. (1985) Specific release of proteoglycans from human natural killer cells during target lysis. Nature 318, 289-291.
10. Niemann, C. U., Cowland, J. B., Klausen, P., Askaa, J., Calafat, J., and Borregaard, N. (2004) Localization of serglycin in human neutrophil granulocytes and their precursors. J. Leukoc. Biol. 76, 406-415.
11. Uhlin-Hansen, L., Wik, T., Kjellen, L., Berg, E., Forsdahl, F., and Kolset, S. O. (1993) Proteoglycan metabolism in normal and inflammatory human macrophages. Blood 82, 2880-2889.
12. Perin, J. P., Bonnet, F., Maillet, P., and Jolles, P. (1988) Characterization and N-terminal sequence of human platelet proteoglycan. Biochem. J. 255, 1007-1013. (Pubitemid 18263965)
13. Lemire, J. M., Chan, C. K., Bressler, S., Miller, J., LeBaron, R. G., and Wight, T. N. (2007) Interleukin-1beta selectively decreases the synthesis of versican by arterial smooth muscle cells. J. Cell. Biochem. 101, 753-766.
14. Schick, B. P., Gradowski, J. F., and San Antonio, J. D. (2001) Synthesis, secretion, and subcellular localization of serglycin proteoglycan in human endothelial cells. Blood 97, 449-458.
15. Maillet, P., Alliel, P. M., Mitjavila, M. T., Perin, J. P., Jolles, P., and Bonnet, F. (1992) Expression of the serglycin gene in human leukemic cell lines. Leukemia 6, 1143-1147.
16. Forsberg, E. and Kjellen, L. (2001) Heparan sulfate: lessons from knockout mice. J. Clin. Invest. 108, 175-180.
17. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037.
18. Å brink, M., Grujic, M., and Pejler, G. (2004) Serglycin is essential for maturation of mast cell secretory granule. J. Biol. Chem. 279, 40897-40905.
19. Braga, T., Grujic, M., Lukinius, A., Hellman, L., Abrink, M., and Pejler, G. (2007) Serglycin proteoglycan is required for secretory granule integrity in mucosal mast cells. Biochem. J. 403, 49-57.
20. Ringvall, M., Ronnberg, E., Wernersson, S., Duelli, A., Henningsson, F., Abrink, M., Garcia-Faroldi, G., Fajardo, I., and Pejler, G. (2008) Serotonin and histamine storage in mast cell secretory granules is dependent on serglycin proteoglycan. J. Allergy Clin. Immunol. 121, 1020-1026.
21. Henningsson, F., Hergeth, S., Cortelius, R., M.Å brink, 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.
22. 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.
23. Niemann, C. U., Abrink, M., Pejler, G., Fischer, R. L., Christensen, E. I., Knight, S. D., and Borregaard, N. (2007) Neutrophil elastase depends on serglycin proteoglycan for localization in granules. Blood 109, 4478-4486.
24. Woulfe, D. M., Lilliendahl, J. K., August, S., Rauova, L., Kowalska, A., Å brink, M., Pejler, G., White, J. G., and Schick, B. P. (2008) Serglycin proteoglycan deletion induces defects in platelet aggregation and thrombus formation in mice. Blood 111, 3458-3467.
25. Zernichow, 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-alpha secretion in response to lipopolysaccharide. J. Biol. Chem. 281, 26792-26801.
26. Grujic, M., Christensen, J. P., Sorensen, M. R., Abrink, M., Pejler, G., and Thomsen, A. R. (2008) Delayed contraction of the CD8+ T cell response toward lymphocytic choriomeningitis virus infection in mice lacking serglycin. J. Immunol. 181, 1043-1051.
27. Lundequist, A., Å brink, M., and Pejler, G. (2006) Mast cell-dependent activation of pro matrix metalloprotease 2: a role for serglycin proteoglycan-dependent mast cell proteases. Biol. Chem. 387, 1513-1519.
28. Pejler, G., Abrink, M., Ringvall, M., and Wernersson, S. (2007) Mast cell proteases. Adv. Immunol. 95, 167-255.
29. Metkar, S. S., Wang, B., Aguilar-Santelises, M., Raja, S. M., Uhlin-Hansen, L., Podack, E., Trapani, J. A., and Froelich, C. J. (2002) Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity 16, 417-428.
30. Raja, S. M., Wang, B., Dantuluri, M., Desai, U. R., Demeler, B., Spiegel, K., Metkar, S. S., and Froelich, C. J. (2002) Cytotoxic cell granule-mediated apoptosis. Characterization of the macromolecular complex of granzyme B with serglycin. J. Biol. Chem. 277, 49523-49530.
31. Kim, T., Gondre-Lewis, M. C., Arnaoutova, I., and Loh, Y. P. (2006) Dense-core secretory granule biogenesis. Physiology (Bethesda, MD) 21, 124-133.
32. Hallgren, J., Backstrom, 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.
33. 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 [see comments]. 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 [see comments]. Nature 400, 769-772.
35. 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.
36. Schwartz, L. B., Riedel, C., Caulfield, J. P., Wasserman, S. I., and Austen, K. F. (1981) Cell association of complexes of chymase, heparin proteoglycan, and protein after degranulation by rat mast cells. J. Immunol. 126, 2071-2078.
37. 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.
38. Kreuger, J., Spillmann, D., Li, J. P., and Lindahl, U. (2006) Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell. Biol. 174, 323-327.
39. Pereira, P. J., Bergner, A., Macedo-Ribeiro, S., Huber, R., Matschiner, G., Fritz, H., Sommerhoff, C. P., and Bode, W. (1998) Human beta-tryptase is a ring-like tetramer with active sites facing a central pore. Nature 392, 306-311.
40. Alter, S. C., Metcalfe, D. D., Bradford, T. R., and Schwartz, L. B. (1987) Regulation of human mast cell tryptase. Effects of enzyme concentration, ionic strength and the structure and negative charge density of polysaccharides. Biochem. J. 248, 821-827.
41. Schwartz, L. B. and Bradford, T. R. (1986) Regulation of tryptase from human lung mast cells by heparin. Stabilization of the active tetramer. J. Biol. Chem. 261, 7372-7379.
42. Elrod, K. C., Moore, W. R., Abraham, W. M., and Tanaka, R. D. (1997) Lactoferrin, a potent tryptase inhibitor, abolishes late-phase airway responses in allergic sheep. Am. J. Respir. Crit. Care. Med. 156, 375-381.
43. Hallgren, J., Estrada, S., Karlson, U., Alving, K., and Pejler, G. (2001) Heparin antagonists are potent inhibitors of mast cell tryptase. Biochemistry 40, 7342-7349.
44. 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.
45. 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 tryptase monomers in the presence of low molecular weight heparin. J. Biol. Chem. 276, 42774-42781.
46. Schwartz, L. B., Riedel, C., Schratz, J. J., and Austen, K. F. (1982) Localization of carboxypeptidase A to the macromolecular heparin proteoglycan-protein complex in secretory granules of rat serosal mast cells. J. Immunol. 128, 1128-1133.
47. Serafin, W. E., Katz, H. R., Austen, K. F., and Stevens, R. L. (1986) Complexes of heparin proteoglycans, chondroitin sulfate E proteoglycans, and [3H]diisopropyl fluorophosphate-binding proteins are exocytosed from activated mouse bone marrow-derived mast cells. J. Biol. Chem. 261, 15017-15021.
48. Pejler, G. and Maccarana, M. (1994) Interaction of heparin with rat mast cell protease 1. J. Biol. Chem. 269, 14451-14456. (Pubitemid 24193997)
49. Pejler, G. and Berg, L. (1995) Regulation of rat mast cell protease 1 activity. Protease inhibition is prevented by heparin proteoglycan. Eur. J. Biochem. 233, 192-199.
50. Sommerhoff, C. P., Ruoss, S. J., and Caughey, G. H. (1992) Mast cell proteoglycans modulate the secretagogue, proteoglycanase, and amidolytic activities of dog mast cell chymase. J. Immunol. 148, 2859-2866.
51. Pejler, G., Soderstrom, K., and Karlstrom, A. (1994) Inactivation of thrombin by a complex between rat mast-cell protease 1 and heparin proteoglycan. Biochem. J. 299 (Part 2), 507-513.
52. Tchougounova, E. and Pejler, G. (2001) Regulation of extravascular coagulation and fibrinolysis by heparin-dependent mast cell chymase. FASEB J. 15, 2763-2765.
53. Pejler, G. and Sadler, J. E. (1999) Mechanism by which heparin proteoglycan modulates mast cell chymase activity. Biochemistry 38, 12187-12195.
54. Pejler, G. (1996) Lactoferrin regulates the activity of heparin proteoglycan- bound mast cell chymase: characterization of the binding of heparin to lactoferrin. Biochem. J. 320, 897-903.
55. Schiemann, F., Grimm, T. A., Hoch, J., Gross, R., Lindner, B., Petersen, F., Bulfone-Paus, S., and Brandt, E. (2006) Mast cells and neutrophils proteolytically activate chemokine precursor CTAP-III and are subject to counterregulation by PF-4 through inhibition of chymase and cathepsin G. Blood 107, 2234-2242.
56. 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.
57. 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.
58. White, J. G. (2004) Medich giant platelet disorder: a unique alpha granule deficiency I. Structural abnormalities. Platelets 15, 345-353.