Generation of anaphylatoxins by human β-tryptase from C3, C4, and C51

Journal of Immunology

Volumn 180, Issue 9, 2008, Pages 6307-6316

  Fukuoka, Yoshihiro ^a   Xia, Han Zhang ^a   Sanchez Mun, Laura B ^b   Dellinger, Anthony L ^a   Escribano, Luis ^b   Schwartz, Lawrence B ^a,c  

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

^b HOSPITAL VIRGEN DE LA SALUD   (Spain)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHYLATOXIN; BETA TRYPTASE; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C4A; COMPLEMENT COMPONENT C5A; DEXTRAN; HEPARIN; POLYANION; TRYPTASE; UNCLASSIFIED DRUG; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C5; DEXTRAN SULFATE; MONOCLONAL ANTIBODY;

ARTICLE; COMPLEMENT SYSTEM; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MASS SPECTROMETRY; MAST CELL; MOLECULAR WEIGHT; PH; PRIORITY JOURNAL; ASTHMA; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; INNATE IMMUNITY; METABOLISM; PROTEIN QUATERNARY STRUCTURE; SKIN;

ANAPHYLATOXINS; ANTIBODIES, MONOCLONAL; ASTHMA; COMPLEMENT C3; COMPLEMENT C4; COMPLEMENT C5; DEXTRAN SULFATE; HEPARIN; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNITY, NATURAL; MAST CELLS; PROTEIN STRUCTURE, QUATERNARY; SKIN; TRYPTASES;

EID: 44449134781     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.9.6307     Document Type: Article

References (75)

1. Humbles, A. A., B. Lu, C. A. Nilsson, C. Lilly, E. Israel, Y. Fujiwara, N. P. Gerard, and C. Gerard. 2000. A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature 406: 998-1001.
2. Krug, N., T. Tschernig, V. J. Erpenbeck, J. M. Hohlfeld, and J. Kohl. 2001. Complement factors C3a and C5a are increased in bronchoalveolar lavage fluid after segmental allergen provocation in subjects with asthma. Am. J. Respir. Crit. Care Med. 164: 1841-1843. (Pubitemid 33152317)
3. Teran, L. M., M. G. Campos, B. T. Begishvilli, J. M. Schroder, R. Djukanovic, J. K. Shute, M. K. Church, S. T. Holgate, and D. E. Davies. 1997. Identification of neutrophil chemotactic factors in bronchoalveolar lavage fluid of asthmatic patients. Clin. Exp. Allergy 27: 396-405. (Pubitemid 27183362)
4. van de Graaf, E. A., H. M. Jansen, M. M. Bakker, C. Alberts, J. K. Eeftinck Schattenkerk, and T. A. Out. 1992. ELISA of complement C3a in bronchoalveolar lavage fluid. J. Immunol. Methods 147: 241-250.
5. Huber-Lang, M., E. M. Younkin, J. V. Sarma, N. Riedemann, S. R. McGuire, K. T. Lu, R. Kunkel, J. G. Younger, F. S. Zetoune, and P. A. Ward. 2002. Generation of C5a by phagocytic cells. Am. J. Pathol. 161: 1849-1859. (Pubitemid 35265542)
6. Huber-Lang, M., J. V. Sarma, F. S. Zetoune, D. Rittirsch, T. A. Neff, S. R. McGuire, J. D. Lambris, R. L. Warner, M. A. Flierl, L. M. Hoesel, et al. 2006. Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med. 12: 682-687. (Pubitemid 43865238)
7. Wetsel, R. A., and W. P. Kolb. 1983. Expression of C5a-like biological activities by the fifth component of human complement (C5) upon limited digestion with noncomplement enzymes without release of polypeptide fragments. J. Exp. Med. 157: 2029-2048.
8. Ward, P. A., and J. H. Hill. 1970. C5 chemotactic fragments produced by an enzyme in lysosomal granules of neutrophils. J. Immunol. 104: 535-543.
9. Wiggins, R. C., P. C. Giclas, and P. M. Henson. 1981. Chemotactic activity generated from the fifth component of complement by plasma kallikrein of the rabbit. J. Exp. Med. 153: 1391-1404. (Pubitemid 11067627)
10. Maruo, K., T. Akaike, T. Ono, T. Okamoto, and H. Maeda. 1997. Generation of anaphylatoxins through proteolytic processing of C3 and C5 by house dust mite protease. J. Allergy Clin. Immunol. 100: 253-260. (Pubitemid 27349869)
11. Wenzel, S. E., A. A. Fowler, III, and L. B. Schwartz. 1988. Activation of pulmonary mast cells by bronchoalveolar allergen challenge: in vivo release of histamine and tryptase in atopic subjects with and without asthma. Am. Rev. Respir. Dis. 137: 1002-1008. (Pubitemid 18151488)
12. 2, and other bronchoconstricting prostaglandins in the airways of subjects with mild asthma. Am. Rev. Respir. Dis. 142: 126-132.
13. Polosa, R., W. H. Ng, N. Crimi, C. Vancheri, S. T. Holgate, M. K. Church, and A. Mistretta. 1995. Release of mast-cell-derived mediators after endobronchial adenosine challenge in asthma. Am. J. Respir. Crit. Care Med. 151: 624-629.
14. Bradding, P., A. F. Walls, and S. T. Holgate. 2006. The role of the mast cell in the pathophysiology of asthma. J. Allergy Clin. Immunol. 117: 1277-1284. (Pubitemid 43795741)
15. Brightling, C. E., P. Bradding, F. A. Symon, S. T. Holgate, A. J. Wardlaw, and I. D. Pavord. 2002. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346: 1699-1705. (Pubitemid 34547483)
16. Carroll, N. G., S. Mutavdzic, and A. L. James. 2002. Increased mast cells and neutrophils in submucosal mucous glands and mucus plugging in patients with asthma. Thorax 57: 677-682.
17. Chen, F. H., K. T. Samson, K. Miura, K. Ueno, Y. Odajima, T. Shougo, Y. Yoshitsugu, and S. Shioda. 2004. Airway remodeling: a comparison between fatal and nonfatal asthma. J. Asthma 41: 631-638. (Pubitemid 39552485)
18. Schwartz, L. B. 2002. Mast cells and basophils. In Inflammatory Mechanisms in Allergic Diseases. B. Zweiman and L. B. Schwartz, eds. Marcel Dekker, Inc., New York, p. 3.
19. Caughey, G. H. 2007. Mast cell tryptases and chymases in inflammation and host defense. Immunol. Rev. 217: 141-154. (Pubitemid 46718143)
20. Hunt, J. F., K. Fang, R. Malik, A. Snyder, N. Malhotra, T. A. Platts-Mills, and B. Gaston. 2000. Endogenous airway acidification: implications for asthma pathophysiology (see comments). Am. J. Respir. Crit. Care Med. 161: 694-699. (Pubitemid 30171718)
21. Ren, S., A. E. Lawson, M. Carr, C. M. Baumgarten, and L. B. Schwartz. 1997. Human tryptase fibrinogenolysis is optimal at acidic pH and generates anticoagulant fragments in the presence of the anti-tryptase monoclonal antibody B12. J. Immunol. 159: 3540-3548. (Pubitemid 127482113)
22. Fukuoka, Y., and L. B. Schwartz. 2004. Human β-tryptase: detection and characterization of the active monomer and prevention of tetramer reconstitution by protease inhibitors. Biochemistry 43: 10757-10764. (Pubitemid 39096718)
23. Fukuoka, Y., and L. B. Schwartz. 2006. The B12 anti-tryptase monoclonal antibody disrupts the tetrameric structure of heparin-stabilized β-tryptase to form monomers that are inactive at neutral pH and active at acidic pH. J. Immunol. 176: 3165-3172. (Pubitemid 43306979)
24. Kulka, M., L. Alexopoulou, R. A. Flavell, and D. D. Metcalfe. 2004. Activation of mast cells by double-stranded RNA: evidence for activation through Toll-like receptor 3. J. Allergy Clin. Immunol. 114: 174-182. (Pubitemid 39005135)
25. McCurdy, J. D., T. J. Olynych, L. H. Maher, and J. S. Marshall. 2003. Cutting edge: distinct Toll-like receptor 2 activators selectively induce different classes of mediator production from human mast cells. J. Immunol. 170: 1625-1629. (Pubitemid 36197374)
26. Varadaradjalou, S., F. Feger, N. Thieblemont, N. B. Hamouda, J. M. Pleau, M. Dy, and M. Arock. 2003. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human mast cells. Eur. J. Immunol. 33: 899-906. (Pubitemid 36546677)
27. Qiao, H., M. V. Andrade, F. A. Lisboa, K. Morgan, and M. A. Beaven. 2006. FcεR1 and toll-like receptors mediate synergistic signals to markedly augment production of inflammatory cytokines in murine mast cells. Blood 107: 610-618. (Pubitemid 43076385)
28. Okumura, S., J. I. Kashiwakura, H. Tomita, K. Matsumoto, T. Nakajima, H. Saito, and Y. Okayama. 2003. Identification of specific gene expression profile in human mast cells via Toll-like receptor 4 and FcεRI. Blood 102: 2547-2554. (Pubitemid 37193594)
29. Ember, J. A., and T. E. Hugli. 1997. Complement factors and their receptors. Immunopharmacology 38: 3-15. (Pubitemid 28049959)
30. Gerard, C., and N. P. Gerard. 1994. C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu. Rev. Immunol. 12: 775-808. (Pubitemid 24140431)
31. El-Lati, S. G., C. A. Dahinden, and M. K. Church. 1994. Complement peptides C3a- and C5a-induced mediator release from dissociated human skin mast cells. J. Invest. Dermatol. 102: 803-806. (Pubitemid 24144266)
32. Huey, R., Y. Fukuoka, P. D. Hoeprich, Jr., and T. E. Hugli. 1986. Cellular receptors to the anaphylatoxins C3a and C5a. Biochem. Soc. Symp. 51: 69-81.
33. Zhao, W., C. L. Kepley, P. A. Morel, L. M. Okumoto, Y. Fukuoka, and L. B. Schwartz. 2006. FcγRIIa, not FcγRIIb, is constitutively and functionally expressed on skin-derived human mast cells. J. Immunol. 177: 694-701. (Pubitemid 43939184)
34. T type of human lung mast cell. J. Allergy Clin. Immunol. 115: 1162-1168.
35. Caughey, G. H. 2006. Tryptase genetics and anaphylaxis. J. Allergy Clin. Immunol. 117: 1411-1414. (Pubitemid 43810215)
36. 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)
37. 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. (Pubitemid 26070579)
38. Pereira, P. J., A. Bergner, S. Macedo-Ribeiro, R. Huber, G. Matschiner, H. Fritz, C. P. Sommerhoff, and W. Bode. 1998. Human β-tryptase is a ring-like tetramer with active sites facing a central pore. Nature 392: 306-311. (Pubitemid 28155107)
39. Alter, S. C., J. A. Kramps, A. Janoff, and L. B. Schwartz. 1990. Interactions of human mast cell tryptase with biological protease inhibitors. Arch. Biochem. Biophys. 276: 26-31. (Pubitemid 20041812)
40. Fajardo, I., and G. Pejler. 2003. Formation of active monomers from tetrameric human β-tryptase. Biochem. J. 369: 603-610. (Pubitemid 36246243)
41. Schwartz, L. B., M. S. Kawahara, T. E. Hugli, D. Vik, D. T. Fearon, and K. F. Austen. 1983. Generation of C3a anaphylatoxin from human C3 by human mast cell tryptase. J. Immunol. 130: 1891-1895.
42. Isenman, D. E., D. I. Kells, N. R. Cooper, H. J. Muller-Eberhard, and M. K. Pangburn. 1981. Nucleophilic modification of human complement protein C3: correlation of conformational changes with acquisition of C3b-like functional properties. Biochemistry 20: 4458-4467. (Pubitemid 11013600)
43. 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.
44. Schwartz, L. B., T. R. Bradford, C. Rouse, A.-M. Irani, G. Rasp, J. K. Van der Zwan, and P.-W. G. Van Der Linden. 1994. Development of a new, more sensitive immunoassay for human tryptase: use in systemic anaphylaxis. J. Clin. Immunol. 14: 190-204. (Pubitemid 24182179)
45. Kambe, N., M. Kambe, J. P. Kochan, and L. B. Schwartz. 2001. Human skin-derived mast cells can proliferate while retaining their characteristic functional and protease phenotypes. Blood 97: 2045-2052. (Pubitemid 32239085)
46. Schwartz, L. B., K. F. Austen, and S. I. Wasserman. 1979. Immunologic release of β-hexosaminidase and β-glucuronidase from purified rat serosal mast cells. J. Immunol. 123: 1445-1450. (Pubitemid 10220721)
47. 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. (Pubitemid 11149212)
48. Hugli, T. E. 1977. Complement factors and inflammation: Effects of α-thrombin on components C3 and C5. In Chemistry and Biology of Thrombin. R. L. Lunblad, J. W. Fenton, and K. G. Mann, eds. Ann Arbor Science Publishers, Inc., Ann Arbor, p. 346.
49. Tsiftsoglou, S. A., and R. B. Sim. 2004. Human complement factor I does not require cofactors for cleavage of synthetic substrates. J. Immunol. 173: 367-375. (Pubitemid 38797362)
50. Tsiftsoglou, S. A., A. C. Willis, P. Li, X. Chen, D. A. Mitchell, Z. Rao, and R. B. Sim. 2005. The catalytically active serine protease domain of human complement factor I. Biochemistry 44: 6239-6249. (Pubitemid 40570717)
51. T types by labeling with antithrombin III-gold. Lab. Invest. 69: 552-561.
52. Metcalfe, D. D., N. A. Soter, S. I. Wasserman, and K. F. Austen. 1980. Identification of sulfated mucopolysaccharides including heparin in the lesional skin of a patient with mastocytosis. J. Invest. Dermatol. 74: 210-215. (Pubitemid 10039864)
53. Metcalfe, D. D., R. A. Lewis, J. E. Silbert, R. D. Rosenberg, S. I. Wasserman, and K. F. Austen. 1979. Isolation and characterization of heparin from human lung. J. Clin. Invest. 64: 1537-1543. (Pubitemid 10181293)
54. Thompson, H. L., E. S. Schulman, and D. D. Metcalfe. 1988. Identification of chondroitin sulfate E in human lung mast cells. J. Immunol. 140: 2708-2713.
55. Gillies, R. J., N. Raghunand, G. S. Karczmar, and Z. M. Bhujwalla. 2002. MRI of the tumor microenvironment. J. Magn. Reson. Imaging 16: 430-450. (Pubitemid 35167878)
56. Artuc, M., B. Hermes, U. M. Steckelings, A. Grutzkau, and B. M. Henz. 1999. Mast cells and their mediators in cutaneous wound healing-active participants or innocent bystanders? Exp. Dermatol. 8: 1-16. (Pubitemid 29038037)
57. Hermes, B., I. Feldmann-Boddeker, P. Welker, B. Algermissen, M. U. Steckelings, J. Grabbe, and B. M. Henz. 2000. Altered expression of mast cell chymase and tryptase and of c-Kit in human cutaneous scar tissue. J. Invest. Dermatol. 114: 51-55. (Pubitemid 30195972)
58. Humphreys, T. R., M. R. Monteiro, and G. F. Murphy. 2000. Mast cells and dendritic cells in basal cell carcinoma stroma. Dermatologic Surgery 26: 200-203.
59. Huttunen, M., M. L. Aalto, R. J. Harvima, M. Horsmanheimo, and I. T. Harvima. 2000. Alterations in mast cells showing tryptase and chymase activity in epithelializating and chronic wounds. Exp. Dermatol. 9: 258-265. (Pubitemid 30458508)
60. Levi-Schaffer, F., and A. Kupietzky. 1990. Mast cells enhance migration and proliferation of fibroblasts into an in vitro wound. Exp. Cell Res. 188: 42-49. (Pubitemid 20147851)
61. Numata, Y., T. Terui, R. Okuyama, N. Hirasawa, Y. Sugiura, I. Miyoshi, T. Watanabe, A. Kuramasu, H. Tagami, and H. Ohtsu. 2006. The accelerating effect of histamine on the cutaneous wound-healing process through the action of basic fibroblast growth factor. J. Invest. Dermatol. 126: 1403-1409. (Pubitemid 43997925)
62. Reed, J. A., A. P. Albino, and N. S. McNutt. 1995. Human cutaneous mast cells express basic fibroblast growth factor. Lab. Invest. 72: 215-222.
63. Trautmann, A., A. Toksoy, E. Engelhard, E. B. Brocker, and R. Gillitzer. 2000. Mast cell involvement in normal human skin wound healing: expression of monocyte chemoattractant protein-I is correlated with recruitment of mast cells which synthesize interleukin-4 in vivo. J. Pathol. 190: 100-106. (Pubitemid 30053360)
64. Blair, R. J., H. Meng, M. J. Marchese, S. L. Ren, L. B. Schwartz, M. G. Tonnesen, and B. L. Gruber. 1997. Human mast cells stimulate vascular tube formation: tryptase is a novel, potent angiogenic factor. J. Clin. Invest. 99: 2691-2700. (Pubitemid 27259816)
65. Coussens, L. M., W. W. Raymond, G. Bergers, M. Laig-Webster, O. Behrendtsen, Z. Werb, G. H. Caughey, and D. Hanahan. 1999. Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 13: 1382-1397. (Pubitemid 29270244)
66. Dethlefsen, S. M., N. Matsuura, and B. R. Zetter. 1994. Mast cell accumulation at sites of murine tumor implantation: implications for angiogenesis and tumor metastasis. Invasion Metastasis 14: 395-408.
67. Imada, A., N. Shijubo, H. Kojima, and S. Abe. 2000. Mast cells correlate with angiogenesis and poor outcome in stage I lung adenocarcinoma. Eur. Respir. J. 15: 1087-1093. (Pubitemid 30399279)
68. Ribatti, D., A. Vacca, A. Marzullo, B. Nico, R. Ria, L. Roncali, and F. Dammacco. 2000. Angiogenesis and mast cell density with tryptase activity increase simultaneously with pathological progression in B-cell non-Hodgkin's lymphomas. Int. J. Cancer 85: 171-175. (Pubitemid 30023063)
69. Ribatti, D., S. Molica, A. Vacca, B. Nico, E. Crivellato, A. M. Roccaro, and F. Dammacco. 2003. Tryptase-positive mast cells correlate positively with bone marrow angiogenesis in B-cell chronic lymphocytic leukemia. Leukemia 17: 1428-1430. (Pubitemid 36857360)
70. Takanami, I., K. Takeuchi, and M. Naruke. 2000. Mast cell density is associated with angiogenesis and poor prognosis in pulmonary adenocarcinoma. Cancer 88: 2686-2692. (Pubitemid 30417928)
71. Karp, C. L., A. Grupe, E. Schadt, S. L. Ewart, M. Keane-Moore, P. J. Cuomo, J. Kohl, L. Wahl, D. Kuperman, S. Germer, et al. 2000. Identification of complement factor 5 as a susceptibility locus for experimental allergic asthma. Nat. Immunol. 1: 221-226.
72. Drouin, S. M., J. Kildsgaard, J. Haviland, J. Zabner, H. P. Jia, P. B. McCray, Jr., B. F. Tack, and R. A. Wetsel. 2001. Expression of the complement anaphylatoxin C3a and C5a receptors on bronchial epithelial and smooth muscle cells in models of sepsis and asthma. J. Immunol. 166: 2025-2032. (Pubitemid 32114691)
73. Taube, C., Y. H. Rha, K. Takeda, J. W. Park, A. Joetham, A. Balhorn, A. Dakhama, P. C. Giclas, V. M. Holers, and E. W. Gelfand. 2003. Inhibition of complement activation decreases airway inflammation and hyperresponsiveness. Am. J. Respir. Crit. Care Med. 168: 1333-1341. (Pubitemid 37487328)
74. Marc, M. M., P. Korosec, M. Kosnik, I. Kern, M. Flezar, S. Suskovic, and J. Sorli. 2004. Complement factors C3a, C4a, and C5a in chronic obstructive pulmonary disease and asthma. Am. J. Respir. Cell Mol. Biol. 31: 216-219. (Pubitemid 39095451)
75. Fregonese, L., F. J. Swan, S. A. van, M. Dolhnikoff, M. A. Santos, M. R. Daha, J. Stolk, T. Tschernig, P. J. Sterk, P. S. Hiemstra, K. F. Rabe, and T. Mauad. 2005. Expression of the anaphylatoxin receptors C3aR and C5aR is increased in fatal asthma. J. Allergy Clin. Immunol. 115: 1148-1154. (Pubitemid 40824582)