Mast cell restricted mouse and human tryptase·heparin complexes hinder thrombin-induced coagulation of plasma and the generation of fibrin by proteolytically destroying fibrinogen

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 7834-7844

  Prieto García, Alicia ^a,e   Zheng, Dominick ^a   Adachi, Roberto ^b   Xing, Wei ^a   Lane, William S ^c   Chung, Kyungmee ^a   Anderson, Paul ^a   Hansbro, Philip M ^d   Castells, Mariana ^a   Stevens, Richard L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF NEWCASTLE   (Australia)

^e HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COAGULATION; DEPOSITS; ENCODING (SYMBOLS); GENES; GRANULATION; HISTOLOGY; MAMMALS; OLIGOMERS; PROTEINS; TISSUE;

BLOOD COAGULATION; CLEAVAGE SITES; FIBRIN DEPOSITION; PLASMA PROTEIN; PROTEASE INHIBITOR; PROTEOGLYCANS; SECRETORY GRANULES; SERINE PROTEASE;

POLYSACCHARIDES;

FIBRIN; FIBRINOGEN; HEPARIN; IMMUNOGLOBULIN E; LYSINE; MAST CELL PROTEASE 6; MAST CELL PROTEASE 7; PLASMA PROTEIN; PROTEINASE INHIBITOR; PROTEOGLYCAN; SERINE PROTEINASE; THROMBIN; TRYPTASE; UNCLASSIFIED DRUG;

ALPHA CHAIN; ANIMAL CELL; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; EDEMA; ENZYME DEGRADATION; ENZYME INACTIVATION; FIBRIN DEPOSITION; GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SECRETORY GRANULE; SKIN ANAPHYLAXIS; TPSAB1 GENE; TPSB2 GENE;

ANIMALIA; MAMMALIA; MUS;

EID: 84858049301     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.325712     Document Type: Article

References (45)

1. 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 (Pubitemid 29399538)
2. 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 (Pubitemid 29399539)
3. 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
4. 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 (Pubitemid 21909287)
5. McNeil, H. P., Reynolds, D. S., Schiller, V., Ghildyal, N., Gurley, D. S., Austen, K. F., and Stevens, R. L. (1992) Isolation, characterization, and transcription of the gene encoding mouse mast cell protease 7. Proc. Natl. Acad. Sci. U.S.A. 89, 11174-11178
6. Wong, G. W., Yasuda, S., Morokawa, N., Li, L., and Stevens, R. L. (2004) Mouse chromosome 17A3.3 contains 13 genes that encode functional tryptic-like serine proteases with distinct tissue and cell expression patterns. J. Biol. Chem. 279, 2438-2452 (Pubitemid 38114227)
7. Harris, J. L., Niles, A., Burdick, K., Maffitt, M., Backes, B. J., Ellman, J. A., Kuntz, I., Haak-Frendscho, M., and Craik, C. S. (2001) Definition of the extended substrate specificity determinants for β-tryptases I and II. J. Biol. Chem. 276, 34941-34947
8. Huang, C., Li, L., Krilis, S. A., Chanasyk, K., Tang, Y., Li, Z., Hunt, J. E., and Stevens, R. L. (1999) Human tryptases α and βII are functionally distinct due in part to a single amino acid difference in one of the surface loops that forms the substrate binding cleft. J. Biol. Chem. 274, 19670-19676
9. Huang, C., De Sanctis, G. T., O'Brien, P. J., Mizgerd, J. P., Friend, D. S., Drazen, J. M., Brass, L. F., and Stevens, R. L. (2001) Evaluation of the substrate specificity of human mast cell tryptase βI and demonstration of its importance in bacterial infections of the lung. J. Biol. Chem. 276, 26276-26284
10. Vanderslice, P., Ballinger, S. M., Tam, E. K., Goldstein, S. M., Craik, C. S., and Caughey, G. H. (1990) Human mast cell tryptase. Multiple cDNAs and genes reveal a multigene serine protease family. Proc. Natl. Acad. Sci. U.S.A. 87, 3811-3815
11. Miller, J. S., Moxley, G., and Schwartz, L. B. (1990) Cloning and characterization of a second complementary DNA for human tryptase. J. Clin. Invest. 86, 864-870 (Pubitemid 20327377)
12. Schwartz, L. B., Lewis, R. A., and Austen, K. F. (1981) Tryptase from human pulmonary mast cells. Purification and characterization. J. Biol. Chem. 256, 11939-11943
13. Ghildyal, N., Friend, D. S., Freelund, R., Austen, K. F., McNeil, H. P., Schiller, V., and Stevens, R. L. (1994) Lack of expression of the tryptase mouse mast cell protease 7 in mast cells of the C57BL/6J mouse. J. Immunol. 153, 2624-2630 (Pubitemid 24278132)
14. 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 (Pubitemid 26047907)
15. 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 (Pubitemid 47099914)
16. 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
17. McNeil, H. P., Shin, K., Campbell, I. K., Wicks, I. P., Adachi, R., Lee, D. M., and Stevens, R. L. (2008) The mouse mast cell-restricted tetramer-forming tryptases mouse mast cell protease 6 and mouse mast cell protease 7 are critical mediators in inflammatory arthritis. Arthritis Rheum. 58, 2338-2346
18. 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
19. Tremaine, W. J., Brzezinski, A., Katz, J. A., Wolf, D. C., Fleming, T. J., Mordenti, J., Strenkoski-Nix, L. C., and Kurth, M. C. (2002) Treatment of mildly to moderately active ulcerative colitis with a tryptase inhibitor (APC 2059). An open-label pilot study. Aliment. Pharmacol. Ther. 16, 407-413 (Pubitemid 34214519)
20. Isozaki, Y., Yoshida, N., Kuroda, M., Handa, O., Takagi, T., Kokura, S., Ichikawa, H., Naito, Y., Okanoue, T., and Yoshikawa, T. (2006) Anti-tryptase treatment using nafamostat mesilate has a therapeutic effect on experimental colitis. Scand. J. Gastroenterol. 41, 944-953 (Pubitemid 43995470)
21. Hamilton, M. J., Sinnamon, M. J., Lyng, G. D., Glickman, J. N., Wang, X., Xing, W., Krilis, S. A., Blumberg, R. S., Adachi, R., Lee, D. M., and Stevens, R. L. (2011) Essential role for mast cell tryptase in acute experimental colitis. Proc. Natl. Acad. Sci. U.S.A. 108, 290-295
22. Zhang, J., Sun, J., Lindholt, J. S., Sukhova, G. K., Sinnamon, M., Stevens, R. L., Adachi, R., Libby, P., Thompson, R. W., and Shi, G. P. (2011) Mast cell tryptase deficiency attenuates mouse abdominal aortic aneurysm formation. Circ. Res. 108, 1316-1327
23. Oh, S. W., Pae, C. I., Lee, D. K., Jones, F., Chiang, G. K., Kim, H. O., Moon, S. H., Cao, B., Ogbu, C., Jeong, K. W., Kozu, G., Nakanishi, H., Kahn, M., Chi, E. Y., and Henderson, W. R., Jr. (2002) Tryptase inhibition blocks airway inflammation in a mouse asthma model. J. Immunol. 168, 1992-2000 (Pubitemid 34135803)
24. Jackson, N. E., Wang, H. W., Bryant, K. J., McNeil, H. P., Husain, A., Liu, K., Tedla, N., Thomas, P. S., King, G. C., Hettiaratchi, A., Cairns, J., and Hunt, J. E. (2008) Alternate mRNA splicing in multiple human tryptase genes is predicted to regulate tetramer formation. J. Biol. Chem. 283, 34178-34187
25. Samoszuk, M., and Corwin, M. A. (2003) Mast cell inhibitor cromolyn increases blood clotting and hypoxia in murine breast cancer. Int. J. Cancer 107, 159-163 (Pubitemid 37100102)
26. Huang, C., Wong, G. W., Ghildyal, N., Gurish, M. F., Sali, A., Matsumoto, R., Qiu, W. T., and Stevens, R. L. (1997) The tryptase, mouse mast cell protease 7, exhibits anticoagulant activity in vivo and in vitro due to its ability to degrade fibrinogen in the presence of the diverse array of protease inhibitors in plasma. J. Biol. Chem. 272, 31885-31893 (Pubitemid 28013341)
27. Thomas, V. A., Wheeless, C. J., Stack, M. S., and Johnson, D. A. (1998) Human mast cell tryptase fibrinogenolysis. Kinetics, anticoagulation mechanism, and cell adhesion disruption. Biochemistry 37, 2291-2298 (Pubitemid 28119302)
28. Schwartz, L. B., Bradford, T. R., Littman, B. H., and Wintroub, B. U. (1985) The fibrinogenolytic activity of purified tryptase from human lung mast cells. J. Immunol. 135, 2762-2767 (Pubitemid 16217148)
29. Huang, C., Friend, D. S., Qiu, W. T., Wong, G. W., Morales, G., Hunt, J., and Stevens, R. L. (1998) Induction of a selective and persistent extravasation of neutrophils into the peritoneal cavity by tryptase mouse mast cell protease 6. J. Immunol. 160, 1910-1919 (Pubitemid 28106480)
30. Niles, A. L., Maffitt, M., Haak-Frendscho, M., Wheeless, C. J., and Johnson, D. A. (1998) Recombinant human mast cell tryptase β. Stable expression in Pichia pastoris and purification of fully active enzyme. Biotechnol. Appl. Biochem. 28, 125-131 (Pubitemid 28470097)
31. Razin, E., Ihle, J. N., Seldin, D., Mencia-Huerta, J. M., Katz, H. R., LeBlanc, P. A., Hein, A., Caulfield, J. P., Austen, K. F., and Stevens, R. L. (1984) Interleukin 3. A differentiation and growth factor for the mouse mast cell that contains chondroitin sulfate E proteoglycan. J. Immunol. 132, 1479-1486 (Pubitemid 14156069)
32. Kaieda, S., Shin, K., Nigrovic, P. A., Seki, K., Lee, R. T., Stevens, R. L., and Lee, D. M. (2010) Synovial fibroblasts promote the expression and granule accumulation of tryptase via interleukin-33 and its receptor ST-2 (IL1RL1). J. Biol. Chem. 285, 21478-21486
33. Svendsen, L., Blombäck, B., Blombäck, M., and Olsson, P. I. (1972) Substrates for determination of trypsin, thrombin, and thrombin-like enzymes. Folia Haematol. Int. Mag. Klin. Morphol. Blutforsch. 98, 446-454
34. Alter, S. C., Kramps, J. A., Janoff, A., and Schwartz, L. B. (1990) Interactions of human mast cell tryptase with biological protease inhibitors. Arch. Biochem. Biophys. 276, 26-31 (Pubitemid 20041812)
35. McNeil, H. P., Austen, K. F., Somerville, L. L., Gurish, M. F., and Stevens, R. L. (1991) Molecular cloning of the mouse mast cell protease-5 gene. A novel secretory granule protease expressed early in the differentiation of serosal mast cells. J. Biol. Chem. 266, 20316-20322 (Pubitemid 21908461)
36. Kollman, J. M., Pandi, L., Sawaya, M. R., Riley, M., and Doolittle, R. F. (2009) Crystal structure of human fibrinogen. Biochemistry 48, 3877-3886
37. Pereira, P. J., Bergner, A., Macedo-Ribeiro, S., Huber, R., Matschiner, G., Fritz, H., Sommerhoff, C. P., and Bode, W. (1998) Human β-tryptase is a ring-like tetramer with active sites facing a central pore. Nature 392, 306-311 (Pubitemid 28155107)
38. Shworak, N. W., Kojima, T., and Rosenberg, R. D. (1993) Isolation and characterization of ryudocan and syndecan heparan sulfate proteoglycans, core proteins, and cDNAs from a rat endothelial cell line. Haemostasis 23, 161-176 (Pubitemid 23116289)
39. 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
40. Fabian, I., Bleiberg, I., and Aronson, M. (1978) Increased uptake and desulphation of heparin by mouse macrophages in the presence of polycations. Biochim. Biophys. Acta 544, 69-76 (Pubitemid 9056763)
41. Atkins, F. M., and Metcalfe, D. D. (1983) Degradation of the heparin matrix of mast cell granules by cultured fibroblasts. J. Immunol. 131, 1420-1425 (Pubitemid 13042397)
42. Atkins, F. M., Friedman, M. M., and Metcalfe, D. D. (1985) Biochemical and microscopic evidence for the internalization and degradation of heparin- containing mast cell granules by bovine endothelial cells. Lab. Invest. 52, 278-286 (Pubitemid 15144083)
43. Pejler, G., and Karlström, A. (1993) Thrombin is inactivated by mast cell secretory granule chymase. J. Biol. Chem. 268, 11817-11822 (Pubitemid 23168136)
44. Trivedi, N. N., Tamraz, B., Chu, C., Kwok, P. Y., and Caughey, G. H. (2009) Human subjects are protected from mast cell tryptase deficiency despite frequent inheritance of loss-of-function mutations. J. Allergy Clin. Immunol. 124, 1099-1105
45. Kettelhut, B. V., and Metcalfe, D. D. (1991) Pediatric mastocytosis J. Invest. Dermatol. 96, Supplemental 15S-18S