A role for cathepsin E in the processing of mast-cell carboxypeptidase A

Journal of Cell Science

Volumn 118, Issue 9, 2005, Pages 2035-2042

  Henningsson, Frida ^a   Yamamoto, Kenji ^b   Saftig, Paul ^c   Reinheckel, Thomas ^d   Peters, Christoph ^d   Knight, Stefan D ^a   Pejler, Gunnar ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF KIEL   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Carboxypeptidase A; Cathepsin E; Heparin; Mast cells; Proteoglycan

Indexed keywords

ASPARTIC PROTEINASE; CARBOXYPEPTIDASE A; CATHEPSIN B; CATHEPSIN D; CATHEPSIN E; CATHEPSIN L; HEPARIN; PROTEOGLYCAN; RECOMBINANT PROTEIN;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; CELL GRANULE; CELL PH; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SECRETION; SECRETORY GRANULE;

ANIMALS; BLOTTING, WESTERN; CARBOXYPEPTIDASES A; CATHEPSIN B; CATHEPSIN D; CATHEPSIN E; CATHEPSINS; CELL LINE; CELLS, CULTURED; CLONING, MOLECULAR; CYSTEINE ENDOPEPTIDASES; ENZYME ACTIVATION; FEMALE; HEPARIN; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MAST CELLS; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PEPTIDE HYDROLASES; PROTEOGLYCANS; RECOMBINANT PROTEINS; SECRETORY VESICLES; TIME FACTORS;

ANIMALIA;

EID: 19444388210     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02333     Document Type: Article

References (45)

1. Barrett, A. J. (1992). Cellular proteolysis. An overview. Ann. New York Acad. Sci. 674, 1-15.
2. Chapman, H. A., Riese, R. J. and Shi, G. P. (1997). Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59, 63-88.
3. De Young, M. B., Nemeth, E. F. and Searpa, A. (1987). Measurement of the internal pH of mast cell granules using microvolumetric fluorescence and isotopic techniques. Arch. Biochem. Biophys. 254, 222-233.
4. Dikov, M. M., Springman, E. B., Yeola, S. and Seratin, W. E. (1994). Processing of procarboxypeptidase A and other zymogens in murine mast cells. J. Biol. Chem. 269, 25897-25904.
5. Dragonetti, A., Baldassarre, M., Castino, R., Demoz, M., Luini, A., Buccione, 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.
6. Everitt, M. T. and Neurath, H. (1980). Rat peritoneal mast cell carboxypeptidase: localization, purification, and enzymatic properties. FEBS Lett. 110, 292-296.
7. 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.
8. Guicciardi, M. E., Deussing, J., Miyoshi, H., Brunk, S. F., Svingen, P. A., Peters, C., Kaufmann, S. H. and Gores, G. J. (2000). Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J. Clin. Invest. 106, 1127-1137.
9. Halangk, W., Lerch, M. M., Brandt-Nedelev, B., Roth, W., Ruthenbuerger, M., Reinheckel, T., Domschke, W., Lippert, H., Peters, C. and Deussing, J. (2000). Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J. Clin. Invest. 106, 773-781.
10. 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.
11. 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.
12. 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.
13. Henningsson, F., Wolters, P., Chapman, H. A., Caughey, G. H. and Pejler, G. (2003). Mast cell cathepsins C and S control levels of carboxypeptidase A and the chymase, mouse mast cell protease 5. Biol. Chem. 384, 1527-1531.
14. 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.
15. Irani, A. M., Sampson, H. A. and Schwartz, L. B. (1989). Mast cells in atopic dermatitis. Allergy 44 (Suppl. 9), 31-34.
16. Jones, T. A., Zou, J. Y., Cowan, S. W. and Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta. Crystallogr. A 47, 110-119.
17. Kleywegt, G. J., Zou, J. Y., Kjeldgaard, M. and Jones, T. (2001). Crystallography of biological macromolecules. In International Tables for Crystallography, vol. F (ed. A. E. Rossmann M.), pp. 353-356. Dordrecht: Kluwer Academic Publishers.
18. Kokkonen, J. O., Vartiainen, M. and Kovanen, P. T. (1986). Low density lipoprotein degradation by secretory granules of rat mast cells. Sequential degradation of apolipoprotein B by granule chymase and carboxypeptidase A. J. Biol. Chem. 261, 16067-16072.
19. Lundequist, A., Tchougounova, E., Abrink, M. and Pejler, G. (2004). Cooperation between mast cell carboxypeptidase A and the chymase mouse mast cell protease 4 in the formation and degradation of angiotensin II. J. Biol. Chem. 279, 32339-32344.
20. Matsumoto, R., Sali, A., Ghildyal, N., Karplus, M. and Stevens, R. L. (1995). Packaging of proteases and proteoglycans in the granules of mast cells and other hematopoietic cells. A cluster of histidines on mouse mast cell protease 7 regulates its binding to heparin serglycin proteoglycans. J. Biol. Chem. 270, 19524-19531.
21. Metcalfe, D. D., Baram, D. and Mekori, Y. A. (1997). Mast cells. Physiol. Rev. 77, 1033-1079.
22. Murshudov, G. N. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D Biol. Crystallogr. 53, 240-255.
23. Muto, N., Yamamoto, M., Tani, S. and Yonezawa, S. (1988). Characteristic distribution of cathepsin E which immunologically cross-reacts with the 86-kDa acid proteinase from rat gastric mucosa. J. Biochem. 103, 629-632.
24. Nakagawa, T., Roth, W., Wong, P., Nelson, A., Farr, A., Deussing, J., Villadangos, J. A., Ploegh, H., Peters, C. and Rudensky, A. Y. (1998). Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280, 450-453.
25. Nakagawa, T. Y., Brissette, W. H., Lira, P, D., Griffiths, R. J., Petrushova, N., Stock, J., McNeish, J. D., Eastman, S. E., Howard, E. D., Clarke, S. R. et al. (1999). Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10, 207-217.
26. Ostermann, N., Gerhartz, B., Worpenberg, S., Trappe, J. and Eder, J. (2004). Crystal structure of an activation intermediate of cathepsin E. J. Mol. Biol. 342, 889-899.
27. Potts, W., Bowyer, J., Jones, H., Tucker, D., Freemont, A. J., Millest, A., Martin, C., Vernon, W., Neerunjun, D., Slynn, G. et al. (2004). Cathepsin L-deficient mice exhibit abnormal skin and bone development and show increased resistance to osteoporosis following ovariectomy. Int. J. Exp. Pathol. 85, 85-96.
28. Rath-Wolfson, L. (2001). An immunocytochemical approach to the demonstration of intracellular processing of mast cell carboxypeptidase. Appl. Immunohistochem. Mol. Morphol. 9, 81-85.
29. Reddanna, P., Prabhu, K. S., Whelan, J. and Reddy, C. C. (2003). Carboxypeptidase A-catalyzed direct conversion of leukotriene C4 to leukotriene F4. Arch. Biochem. Biophys. 413, 158-163.
30. Reinheckel, T., Deussing, J., Roth, W. and Peters, C. (2001). Towards specific functions of lysosomal cysteine peptidases: phenotypes of mice deficient for cathepsin B or cathepsin L. Biol. Chem. 382, 736-741.
31. Reynolds, D. S., Gurley, D. S., Stevens, R. L., Sugarbaker, D. J., Austen, K. F. and Serafin, W. E. (1989). Cloning of cDNAs that encode human mast cell carboxypeptidase A, and comparison of the protein with mouse mast cell carboxypeptidase A and rat pancreatic carboxypeptidases. Proc. Natl. Acad. Sci. USA 86, 9480-9484.
32. Roth, W., Deussing, J., Botchkarev, V. A., Pauly-Evers, M., Saftig, P., Hafner, A., Schmidt, P., Schmahl, W., Scherer, J., Anton-Lamprecht, I. et al. (2000). Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling. FASEB J. 14, 2075-2086.
33. Saftig, P., Hetman, M., Schmahl, W., Weber, K., Heine, L., Mossmann, H., Koster, A., Hess, B., Evers, M., von Figura, K. et al. (1995). Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells. EMBO J. 14, 3599-3608.
34. Saftig, P., Hunziker, E., Wehmeyer, O., Jones, S., Boyde, A., Rommerskirch, W., Moritz, J. D., Schu, P. and von Figura, K. (1998). Impaired osteoclastic bone resorption leads to osteopetrosis in cathepsin-K-deficient mice. Proc. Natl. Acad. Sci. USA 95, 13453-13458.
35. Sakai, H., Saku, T., Kato, Y. and Yamamoto, K. (1989). Quantitation and immunohistochemical localization of cathepsins E and D in rat tissues and blood cells. Biochim. Biophys. Acta 991, 367-375.
36. 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.
37. Springman, E. B., Dikov, M. M. and Serafin, W. E. (1995). Mast cell procarboxypeptidase A. J. Biol. Chem. 270, 1300-1307.
38. Stevens, R. L. and Austen, K. F. (1989). Recent advances in the cellular and molecular biology of mast cells. Immunol. Today 10, 381-386.
39. Tatnell, P. J., Lees, W. E. and Kay, J. (1997). Cloning, expression and characterisation of murine procathepsin E. FEBS Lett. 408, 62-66.
40. Tchougounova, E. and Pejler, G. (2001). Regulation of extravascular coagulation and fibrinolysis by heparin-dependent mast cell chymase. FASEB J. 15, 2763-2765.
41. Tsukuba, T., Okamoto, K., Yasuda, Y., Morikawa, W., Nakanishi, H. and Yamamoto, K. (2000). New functional aspects of cathepsin D and cathepsin E. Mol. Cell 10, 601-611.
42. Tsukuba, T., Okamoto, K., Okamoto, Y., Yanagawa, M., Kohmura, K., Yasuda, Y., Uchi, H., Nakabara, T., Furue, M., Nakayama, K. et al. (2003). association of cathepsin E deficiency with development of atopic dermatitis. J. Biochem. 134, 893-902.
43. Turk, B., Turk, D. and Turk, V. (2000). Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta 1477, 98-111.
44. Wedemeyer, J., Tsai, M. and Galli, S. J. (2000). Roles of mast cells and basophils in innate and acquired immunity. Curr. Opin. Immunol. 12, 624-631.
45. Wolters, P. J., Pham, C. T., Muilenburg, D. J., Ley, T. J. and Caughey, G. H. (2001). Dipeptidyl peptidase I is essential for activation of mast cell chymases, but not tryptases, in mice. J. Biol. Chem. 276, 18551-18556.