Granzyme B is expressed in mouse mast cells in vivo and in vitro and causes delayed cell death independent of perforin

Cell Death and Differentiation

Volumn 14, Issue 10, 2007, Pages 1768-1779

  Pardo, J ^a   Wallich, R ^b   Ebnet, K ^c   Iden, S ^c   Zentgraf, H ^d   Martin, P ^a   Ekiciler, A ^a   Prins, A ^e   Mullbacher A ^e   Huber, M ^f   Simon, M M ^a  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e Biology and Environment   (Australia)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FC EPSILON RECEPTOR; FC RECEPTOR; GRANZYME B; PERFORIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BONE MARROW; CELL ACTIVATION; CELL ADHESION; CELL COMMUNICATION; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME RELEASE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE DISORDER; MAST CELL; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN CELL; TARGET CELL; WILD TYPE;

ANIMALS; ANOIKIS; APOPTOSIS; CELL ADHESION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; GRANZYMES; LUNG; MAST CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PERFORIN; RECEPTORS, IGG; SKIN;

MUS;

EID: 34548724545     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4402183     Document Type: Article

References (50)

1. Metz M, Maurer M (2007) Mast cells - Key effector cells in immune responses. Trends Immunol 28: 234-241.
2. Marshall JS (2004) Mast-cell responses to pathogens. Nat Rev Immunol 4: 787-799.
3. Gall SJ, Nakae S, Tsai M (2005) Mast cells in the development of adaptive immune responses. Nat Immunol 6: 135-142.
4. Kataoka TR, Morii E, Oboki K, Kitamura Y (2004) Strain-dependent inhibitory effect of mutant mi-MITF on cytotoxic activities of cultured mast cells and natural killer cells of mice. Lab Invest 84: 376-384.
5. Russell JH, Ley TJ (2002) Lymphocyte-mediated cytotoxicity. Annu Rev Immunol 20: 323-370.
6. Stinchcombe JC, Bossi G, Booth S, Griffiths GM (2001) The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761.
7. Pardo J, Bosque A, Brehm R, Wallich R, Naval J, Mullbacher A et al. (2004) Apoptotic pathways are selectively activated by granzyme A and/or granzyme B in CTL-mediated target cell lysis. J Cell Biol 167: 457-468.
8. Simon MM, Ebnet K, Kramer MD (1993) Molecular analysis and possible pleiotropic function(s) of the T cell-specific serine proteinase 1 In: Sitkovsky MV, Henkart PA (eds). Cytotoxix Cells: Recognition, Effector Function, Generation, and Methods. Birkhäuser: Boston, Basel, Berlin pp 278-294.
9. Suidan HS, Bouvier J, Schaerer E, Stone SR, Monard D, Tschopp J (1994) Granzyme A released upon stimulation of cytotoxic T lymphocytes activates the thrombin receptor on neuronal cells and astrocytes. Proc Natl Acad Sci USA 91: 8112-8116.
10. Buzza MS, Zamurs L, Sun J, Bird CH, Smith AI, Trapani JA et al. (2005) Extracellular matrix remodeling by human granzyme B via cleavage of vitronectin, fibronectin, and laminin. J Biol Chem 280: 23549-23558.
11. Choy JC, Hung VH, Hunter AL, Cheung PK, Motyka B, Goping IS et al. (2004) Granzyme B induces smooth muscle cell apoptosis in the absence of perforin: Involvement of extracellular matrix degradation. Arterioscler Thromb Vasc Biol 24: 2245-2250.
12. Simon MM, Simon HG, Fruth U, Epplen J, Muller-Hermelink HK, Kramer MD (1987) Cloned cytolytic T-effector cells and their malignant variants produce an extracellular matrix degrading trypsin-like serine proteinase. Immunology 60: 219-230.
13. Tak PP, Spaeny-Dekking L, Kraan MG, Breedveld FC, Froelich CJ, Hack CE (1999) The levels of soluble granzyme A and B are elevated in plasma and synovial fluid of patients with rheumatoid arthritis (RA). Clin Exp Immunol 116: 366-370.
14. Froelich CJ, Zhang X, Turbov J, Hudig D, Winkler U, Hanna WL (1993) Human granzyme B degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J Immunol 151: 7161-7171.
15. Stevens RL, Rothenberg ME, Levi-Schaffer F, Austen KF (1987) Ontogeny of in vitro-differentiated mouse mast cells. Fed Proc 46: 1915-1919.
16. Gimborn K, Lessmann E, Kuppig S, Krystal G, Huber M (2005) SHIP down-regulates FcepsilonR1-induced degranulation at supraoptimal IgE or antigen levels. J Immunol 174: 507-516.
17. Martin P, Wallich R, Pardo J, Mullbacher A, Munder M, Modolell M et al. (2005) Quiescent and activated mouse granulocytes do not express granzyme A and B or perforin: Similarities or differences with human polymorphonuclear leukocytes? Blood 106: 2871-2878.
18. Chen JW, Pan W, D'Souza MP, August JT (1985) Lysosome-associated membrane proteins: Characterization of LAMP-1 of macrophage P388 and mouse embryo 3T3 cultured cells. Arch Biochem Biophys 239: 574-586.
19. Tschopp J, Nabholz M (1990) Perforin-mediated target cell lysis by cytolytic T lymphocytes. Annu Rev Immunol 8: 279-302.
20. Schwartz LB, Austen KF (1980) Enzymes of the mast cell granule. J Invest Dermatol 74: 349-353.
21. Huber M, Helgason CD, Scheid MP, Duronio V, Humphries RK, Krystal G (1998) Targeted disruption of SHIP leads to Steel factor-inducad degranulation of mast cells. EMBO J 17: 7311-7319.
22. Rival Y, Del Maschio A, Rabiet MJ, Dejana E, Duperray A (1996) Inhibition of platelet endothelial cell adhesion molecule-1 synthesis and leukocyte transmigration in endothelial cells by the combined action of TNF-alpha and IFN-gamma. J Immunol 157: 1233-1241.
23. Dejana E (2004) Endothelial cell-cell junctions: Happy together. Nat Rev Mol Cell Biol 5: 261-270.
24. Raja SM, Metkar SS, Froelich CJ (2003) Cytotoxic granule-mediated apoptosis: Unraveling the complex mechanism. Curr Opin Immumol 15: 528-532.
25. Dikov MM, Springman EB, Yeola S, Serafin WE (1994) Processing of procarboxypeptidase A and other zymogens in murine mast cells. J Biol Chem 269: 25897-25904.
26. Salvesen G, Enghild JJ (1990) An unusual specificity in the activation of neutrophil serine proteinase zymogens. Biochemistry 29: 5304-5308.
27. Huang C, Friend DS, Qiu WT, Wong GW, Morales G, Hunt J et al. (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.
28. Hallgren J, Spillmann D, 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.
29. Stepp SE, Dufourcq-Lagelouse R, Le Deist F, Bhawan S, Certain S, Mathew PA et al. (1999) Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science 286: 1957-1954.
30. Marshall JS, Jawdat DM (2004) Mast cells in innate immunity. J Allergy Clin Immunol 114: 21-27.
31. Echtenacher B, Mannell DN, Hultner L (1996) Critical protective role of mast cells in a model of acute septic peritonitis. Nature 381 75-77.
32. Malaviya R, Ikeda T, Ross E, Abraham SN (1996) Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 381: 77-80.
33. Nourshargh S, Marelli-Berg FM (2005) Transmigration through venular walls: A key regulator of leukocyte phenotype and function. Trends Immunol 26: 157-165.
34. Meredith, Jr JE, Fazeli B, Schwartz MA (1993) The extracellular matrix as a cell survival factor. Mol Biol Cell 4: 953-961.
35. Wang Y, Jin G, Miao H, Li JY, Usami S, Chien S (2006) Integrins regulate VE-cadherin and catenins: Dependence of this regulation on Src, but not on Ras. Proc Natl Acad Sci USA 103: 1774-1779.
36. Choy JC, Cruz RP, Kerjner A, Geisbrecht J, Sawchuk T, Fraser SA et al. (2005) Granzyme B induces endothelial cell apoptosis and contributes to the development of transplant vascular disease. Am J Transplant 5: 494-499.
37. Hansson GK, Libby P (2006) The immune response in atherosclerosis: A double-edged sword. Nat Rev Immunol 6: 508-519.
38. Kaartinen M, Penttila A, Kovanen PT (1994) Accumulation of activated mast cells in the shoulder region of human coronary atheroma, the predilection site of atheromatous rupture. Circulation 90: 1669-1678.
39. Choy JC, McDonald PC, Suarez AC, Hung VH, Wilson JE, McManus BM et al. (2003) Granzyme B in atherosclerosis and transplant vascular disease: Association with cell death and atherosclerotic disease severity. Mod Pathol 16: 460-470.
40. Lu LF, Lind EF, Gondek DC, Bennett KA, Gleeson MW, Pino-Lagos K et al. (2006) Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442: 997-1002.
41. Kummer JA, Tak PP, Brinkman BM, van Tilborg AA, Kamp AM, Verweij CL et al. (1994) Expression of granzymes A and B in synovial tissue from patients with rheumatoid arthritis and osteoarthritis. Clin Immunol Immunopathol 73: 88-95.
42. Kiener HP, Baghestanian M, Dominkus M, Walchshofer S, Ghannadan M, Willheim M et al. (1998) Expression of the C5a receptor (CD88) on synovial mast cells in-patients with rheumatoid arthritis. Arthitis Rheum 41: 233-245.
43. Lee DM, Friend DS, Gurish MF, Benoist C, Mathis D, Brenner MB (2002) Mast cells: A cellular link between autoantibodies and inflammatory arthritis. Science 297: 1689-1692.
44. Johnston B, Bums AR, Kubes P (1998) A role for mast cells in the development of adjuvant-induced vasculitis and arthritis. Am J Pathol 152: 555-563.
45. Nishizumi H, Yamamoto T (1997) Impaired tyrosine phosphorylation and Ca2+ mobilization, but not degranulation, in lyn-deficient bone marrow-derived mast cells. J Immunol 158: 2350-2355.
46. Bhakdi S, Bayley H, Valeva A, Walev I, Walker B, Kehoe M et al. (1996) Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: Prototypes of pore-forming bacterial cytolysins. Arch Microbiol 165: 73-79.
47. Pardo J, Balkow S, Anel A, Simon MM (2002) Granzymes are essential for natural killer cell-mediated and perf-facilitated tumor control. Eur J Immunol 32: 2881-2887.
48. Pardo J, Perez-Galan P, Gamen S, Marzo I, Morrison I, Kaspar AA et al. (2001) A role of the mitochondrial apoptosis-inducing factor in granulysin-induced apoptosis. J Immunol 167: 1222-1229.
49. Ebnet K, Suzuki A, Horikoshi Y, Hirose T, Meyer Zu Brickwedde MK, Ohno S et al. (2001) The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J 20 3738-3748.
50. Strik MCM, de Koning PJA, Kleijmeer MJ, Bladergroen BA, Wolbink AM, Griffith JM et al. Human mast cells produce and release the cytotoxic lymphocyte-associated protease gzanzyme B upon activation. Mol Immunol 2007; 44: 3462-3472.