Promiscuous processing of human α/β-protryptases by cathepsins L, B, and C

Journal of Immunology

Volumn 186, Issue 12, 2011, Pages 7136-7143

  Le, Quang T ^a   Min, Hae Ki ^a   Xia, Han Zhang ^a   Fukuoka, Yoshihiro ^a   Katunuma, Nobuhiko ^b   Schwartz, Lawrence B ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TOKUSHIMA BUNRI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA PROTRYPTASE ENZYME; CATHEPSIN B; CATHEPSIN L; DIPEPTIDYL PEPTIDASE I; ENZYME PRECURSOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL MATURATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME PURIFICATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING;

CATHEPSIN B; CATHEPSIN C; CATHEPSIN L; CATHEPSINS; CELL LINE; ENZYME PRECURSORS; HEPARIN; HUMANS; MASS SPECTROMETRY; MAST CELLS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRYPTASES;

EID: 79959564979     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001804     Document Type: Article

References (48)

1. Schwartz, L. B., R. A. Lewis, and K. F. Austen. 1981. Tryptase from human pulmonary mast cells. Purification and characterization. J. Biol. Chem. 256: 11939-11943.
2. Schwartz, L. B., R. A. Lewis, D. Seldin, and K. F. Austen. 1981. Acid hydrolases and tryptase from secretory granules of dispersed human lung mast cells. J. Immunol. 126: 1290-1294.
3. Sakai, K., S. Ren, and L. B. Schwartz. 1996. A novel heparin-dependent processing pathway for human tryptase. Autocatalysis followed by activation with dipeptidyl peptidase I. J. Clin. Invest. 97: 988-995.
4. Pereira, P. J., A. Bergner, S. Macedo-Ribeiro, R. Huber, G. Matschiner, H. Fritz, C. P. Sommerhoff, and W. Bode. 1998. Human b-tryptase is a ring-like tetramer with active sites facing a central pore. Nature 392: 306-311. (Pubitemid 28155107)
5. Trivedi, N. N., B. Tamraz, C. Chu, P. Y. Kwok, and G. H. Caughey. 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, e1-e4.
6. Wolters, P. J., C. T. N. Pham, D. J. Muilenburg, T. J. Ley, and G. H. Caughey. 2001. Dipeptidyl peptidase I is essential for activation of mast cell chymases, but not tryptases, in mice. J. Biol. Chem. 276: 18551-18556.
7. Guida, M., M. Riedy, D. Lee, and J. Hall. 2000. Characterization of two highly polymorphic human tryptase loci and comparison with a newly discovered monkey tryptase ortholog. Pharmacogenetics 10: 389-396. (Pubitemid 30433572)
8. Min, H. K., G. Moxley, M. C. Neale, and L. B. Schwartz. 2004. Effect of sex and haplotype on plasma tryptase levels in healthy adults. J. Allergy Clin. Immunol. 114: 48-51.
9. Soto, D., C. Malmsten, J. L. Blount, D. J. Muilenburg, and G. H. Caughey. 2002. Genetic deficiency of human mast cell a-tryptase. Clin. Exp. Allergy 32: 1000-1006.
10. Huang, C., L. Li, S. A. Krilis, K. Chanasyk, Y. Tang, Z. Li, J. E. Hunt, and R. L. Stevens. 1999. Human tryptases alpha and beta/II 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.
11. Marquardt, U., F. Zettl, R. Huber, W. Bode, and C. Sommerhoff. 2002. The crystal structure of human alpha1-tryptase reveals a blocked substrate-binding region. J. Mol. Biol. 321: 491-502.
12. Selwood, T., Z. M. Wang, D. R. McCaslin, and N. M. Schechter. 2002. Diverse stability and catalytic properties of human tryptase alpha and beta isoforms are mediated by residue differences at the S1 pocket. Biochemistry 41: 3329-3340.
13. Schwartz, L. B., H. K. Min, S. Ren, H. Z. Xia, J. Hu, W. Zhao, G. Moxley, and Y. Fukuoka. 2003. Tryptase precursors are preferentially and spontaneously released, whereas mature tryptase is retained by HMC-1 cells, Mono-Mac-6 cells, and human skin-derived mast cells. J. Immunol. 170: 5667-5673. (Pubitemid 36617859)
14. Kummer, J. A., A. M. Kamp, F. Citarella, A. J. Horrevoets, and C. E. Hack. 1996. Expression of human recombinant granzyme A zymogen and its activation by the cysteine proteinase cathepsin C. J. Biol. Chem. 271: 9281-9286.
15. Smyth, M. J., M. J. McGuire, and K. Y. Thia. 1995. Expression of recombinant human granzyme B. A processing and activation role for dipeptidyl peptidase I. J. Immunol. 154: 6299-6305.
16. Wilharm, E., M. A. Parry, R. Friebel, H. Tschesche, G. Matschiner, C. P. Sommerhoff, and D. E. Jenne. 1999. Generation of catalytically active granzyme K from Escherichia coli inclusion bodies and identification of efficient granzyme K inhibitors in human plasma. J. Biol. Chem. 274: 27331-27337.
17. Pham, C. T., and T. J. Ley. 1999. Dipeptidyl peptidase I is required for the processing and activation of granzymes A and B in vivo. Proc. Natl. Acad. Sci. USA 96: 8627-8632.
18. McGuire, M. J., P. E. Lipsky, and D. L. Thiele. 1993. Generation of active myeloid and lymphoid granule serine proteases requires processing by the granule thiol protease dipeptidyl peptidase I. J. Biol. Chem. 268: 2458-2467.
19. Adkison, A. M., S. Z. Raptis, D. G. Kelley, and C. T. Pham. 2002. Dipeptidyl peptidase I activates neutrophil-derived serine proteases and regulates the development of acute experimental arthritis. J. Clin. Invest. 109: 363-371.
20. Henningsson, F., K. Yamamoto, P. Saftig, T. Reinheckel, C. Peters, S. D. Knight, and G. Pejler. 2005. A role for cathepsin E in the processing of mast-cell carboxy-peptidase A. J. Cell Sci. 118: 2035-2042. (Pubitemid 40723846)
21. Butterfield, J. H., D.Weiler, G. Dewald, and G. J. Gleich. 1988. Establishment of an immature mast cell line from a patient with mast cell leukemia. Leuk. Res. 12: 345-355.
22. Katunuma, N., H. Tsuge, M. Nukatsuka, T. Asao, and M. Fukushima. 2002. Structure-based design of specific cathepsin inhibitors and their application to protection of bone metastases of cancer cells. Arch. Biochem. Biophys. 397: 305-311.
23. Murata, M., S. Miyashita, C. Yokoo, M. Tamai, K. Hanada, K. Hatayama, T. Towatari, T. Nikawa, and N. Katunuma. 1991. Novel epoxysuccinyl peptides. Selective inhibitors of cathepsin B, in vitro. FEBS Lett. 280: 307-310.
24. Schwartz, L. B., and T. R. Bradford. 1986. Regulation of tryptase from human lung mast cells by heparin. Stabilization of the active tetramer. J. Biol. Chem. 261: 7372-7379.
25. Sakai, K., S. D. Long, D. A. Pettit, G. A. Cabral, and L. B. Schwartz. 1996. Expression and purification of recombinant human tryptase in a baculovirus system. Protein Expr. Purif. 7: 67-73.
26. Schwartz, L. B., T. R. Bradford, D. C. Lee, and J. F. Chlebowski. 1990. Immunologic and physicochemical evidence for conformational changes occurring on conversion of human mast cell tryptase from active tetramer to inactive monomer. Production of monoclonal antibodies recognizing active tryptase. J. Immunol. 144: 2304-2311.
27. McGuire, M. J., P. E. Lipsky, and D. L. Thiele. 1992. Purification and characterization of dipeptidyl peptidase I from human spleen. Arch. Biochem. Biophys. 295: 280-288.
28. Barrett, A. J., and H. Kirschke. 1981. Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol. 80(Pt C): 535-561.
29. Le, T. Q., M. Kawachi, H. Yamada, M. Shiota, Y. Okumura, and H. Kido. 2006. Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain. Biol. Chem. 387: 467-475.
30. Heussen, C., and E. B. Dowdle. 1980. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal. Biochem. 102: 196-202.
31. Ren, S., K. Sakai, and L. B. Schwartz. 1998. Regulation of human mast cell betatryptase: conversion of inactive monomer to active tetramer at acid pH. J. Immunol. 160: 4561-4569.
32. Lindkvist, B., I. Fajardo, G. Pejler, and A. Borgström. 2006. Cathepsin B activates human trypsinogen 1 but not proelastase 2 or procarboxypeptidase B. Pancreatology 6: 224-231. (Pubitemid 44114492)
33. Henningsson, F., J. Ledin, C. Lunderius, M. Wilén, L. Hellman, and G. Pejler. 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.
34. Waguri, S., N. Sato, T. Watanabe, K. Ishidoh, E. Kominami, K. Sato, and Y. Uchiyama. 1995. Cysteine proteinases in GH4C1 cells, a rat pituitary tumor cell line, are secreted by the constitutive and regulated secretory pathways. Eur. J. Cell Biol. 67: 308-318.
35. Kukor, Z., J. Mayerle, B. Krüger, M. Tóth, P. M. Steed, W. Halangk, M. M. Lerch, and M. Sahin-Tóth. 2002. Presence of cathepsin B in the human pancreatic secretory pathway and its role in trypsinogen activation during hereditary pancreatitis. J. Biol. Chem. 277: 21389-21396.
36. Yasothornsrikul, S., D. Greenbaum, K. F. Medzihradszky, T. Toneff, R. Bundey, R. Miller, B. Schilling, I. Petermann, J. Dehnert, A. Logvinova, et al. 2003. Cathepsin L in secretory vesicles functions as a prohormone-processing enzyme for production of the enkephalin peptide neurotransmitter. Proc. Natl. Acad. Sci. USA 100: 9590-9595.
37. Dahl, S. W., T. Halkier, C. Lauritzen, I. Dolenc, J. Pedersen, V. Turk, and B. Turk. 2001. Human recombinant pro-dipeptidyl peptidase I (cathepsin C) can be activated by cathepsins L and S but not by autocatalytic processing. Biochemistry 40: 1671-1678. (Pubitemid 32144036)
38. Nakagawa, T., W. Roth, P. Wong, A. Nelson, A. Farr, J. Deussing, J. A. Villadangos, H. Ploegh, C. Peters, and A. Y. Rudensky. 1998. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280: 450-453.
39. Guncar, G., G. Pungercic, I. Klemencic, V. Turk, and D. Turk. 1999. Crystal structure of MHC class II-associated p41 Ii fragment bound to cathepsin L reveals the structural basis for differentiation between cathepsins L and S. EMBO J. 18: 793-803. (Pubitemid 29082259)
40. Honey, K., T. Nakagawa, C. Peters, and A. Rudensky. 2002. Cathepsin L regulates CD4+ T cell selection independently of its effect on invariant chain: a role in the generation of positively selecting peptide ligands. J. Exp. Med. 195: 1349-1358.
41. Maehr, R., J. D. Mintern, A. E. Herman, A. M. Lennon-Duménil, D. Mathis, C. Benoist, and H. L. Ploegh. 2005. Cathepsin L is essential for onset of autoimmune diabetes in NOD mice. J. Clin. Invest. 115: 2934-2943.
42. Honey, K., K. Benlagha, C. Beers, K. Forbush, L. Teyton, M. J. Kleijmeer, A. Y. Rudensky, and A. Bendelac. 2002. Thymocyte expression of cathepsin L is essential for NKT cell development. Nat. Immunol. 3: 1069-1074.
43. Huang, C., G. Morales, A. Vagi, K. Chanasyk, M. Ferrazzi, C. Burklow, W. T. Qiu, E. Feyfant, A. Sali, and R. L. Stevens. 2000. Formation of enzymatically active, homotypic, and heterotypic tetramers of mouse mast cell tryptases. Dependence on a conserved Trp-rich domain on the surface. J. Biol. Chem. 275: 351-358.
44. Trivedi, N. N., Q. Tong, K. Raman, V. J. Bhagwandin, and G. H. Caughey. 2007. Mast cell alpha and beta tryptases changed rapidly during primate speciation and evolved from gamma-like transmembrane peptidases in ancestral vertebrates. J. Immunol. 179: 6072-6079.
45. Trivedi, N. N., W. W. Raymond, and G. H. Caughey. 2008. Chimerism, point mutation, and truncation dramatically transformed mast cell delta-tryptases during primate evolution. J. Allergy Clin. Immunol. 121: 1262-1268.
46. Murakumo, Y., H. Ide, H. Itoh, M. Tomita, T. Kobayashi, H. Maruyama, Y. Horii, and Y. Nawa. 1995. Cloning of the cDNA encoding mast cell tryptase of Mongolian gerbil, Meriones unguiculatus, and its preferential expression in the intestinal mucosa. Biochem. J. 309: 921-926.
47. Raymond, W. W., C. P. Sommerhoff, and G. H. Caughey. 2005. Mastin is a gelatinolytic mast cell peptidase resembling a mini-proteasome. Arch. Biochem. Biophys. 435: 311-322.
48. Schwartz, L. B., A. M. Irani, K. Roller, M. C. Castells, and N. M. Schechter. 1987. Quantitation of histamine, tryptase, and chymase in dispersed human T and TC mast cells. J. Immunol. 138: 2611-2615.