Serine Protease Inhibitor 6 Protects Cytotoxic T Cells from Self-Inflicted Injury by Ensuring the Integrity of Cytotoxic Granules

Immunity

Volumn 24, Issue 4, 2006, Pages 451-461

  Zhang, Manling ^a   Park, Sun Mi ^a   Wang, Yue ^a   Shah, Ramila ^a   Liu, Ni ^a   Murmann, Andrea E ^a   Wang, Chyung Ru ^a   Peter, Marcus E ^a   Ashton Rickardt, Philip G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

GRANZYME B; SERINE PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; LISTERIA MONOCYTOGENES; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ARENAVIRIDAE INFECTIONS; BLOTTING, WESTERN; CYTOPLASMIC GRANULES; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; GRANZYMES; LISTERIA INFECTIONS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERINE ENDOPEPTIDASES; SERPINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 33645973995     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2006.02.002     Document Type: Article

References (61)

1. Ahmed R., Salmi A., Butler L.D., Chiller J.M., and Oldstone M.B.A. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. J. Exp. Med. 160 (1984) 521-540
2. Badovinac V.P., Tvinnereim A.R., and Harty J.T. Regulation of antigen-specific T cell homeostasis by perforin and interferon-γ. Science 290 (2000) 1354-1357
3. + T cell expansion and mortality in vaccinated perforin-deficient mice. Immunity 18 (2003) 463-474
4. Baetz K., Isaaz S., and Griffiths G.M. Loss of cytotoxic T lymphocyte function in Chediak-Higashi syndrome arises from a secretory defect that prevents lytic granule exocytosis. J. Immunol. 154 (1995) 6122-6131
5. Balaji K.N., Schaschke N., Machleidt W., Catalfamo M., and Henkart P.A. Surface cathepsin B protects cytotoxic lymphocytes from self-destruction after degranulation. J. Exp. Med. 196 (2002) 493-503
6. Barbosa M.D., Nguyen Q.A., Tchernev V.T., Ashley J.A., Detter J.C., Blaydes S.M., Brandt S.J., Chotai D., Hodgman C., Solari R.C., and Kingsmore S.F. Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 382 (1996) 262-265
7. Bladergroen B.A., Strik M.C.M., Bovenschen N., van Berkum O., Scheffer G.L., Meijer C.J.L.M., Hack C.E., and Kummer J.A. The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J. Immunol. 166 (2001) 3218-3225
8. Budihardjo I., Oliver H., Lutter M., Luo X., and Wang X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15 (1999) 269-290
9. Coligan J.E., Kruisbeek A.M., Margulis D.H., Shevach E.M., and Strober W. Current Protocols in Immunology Vol 1 (1995), John Wiley and Sons, New York
10. Gong B., Chen Q., Endlich B., Mazumder S., and Almasan A. Ionizing radiation-induced, Bax-mediated cell death is dependent on activation of cysteine and serine proteases. Cell Growth Differ. 10 (1999) 491-502
11. Hanon E., Stinchcombe J.C., Saito M., Asquith B.E., Taylor G.P., Tanaka Y., Weber J.N., Griffiths G.M., and Bangham C.R. Fratricide among CD8(+) T lymphocytes naturally infected with human T cell lymphotropic virus type I. Immunity 13 (2000) 657-664
12. Heusel J.W., Wesselschmidt R.L., Shresta S., Russell J.H., and Ley T.J. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76 (1994) 977-987
13. Hirst C.E., Buzza M.S., Bird C.H., Warren H.S., Cameron P.U., Zhang M., Ashton-Rickardt P.G., and Bird P.I. The intracellular granzyme B inhibitor, proteinase inhibitor 9, is up-regulated during accessory cell maturation and effector cell degranulation, and its overexpression enhances CTL potency. J. Immunol. 170 (2003) 805-815
14. Huang J.-F., Yang Y., Sepulveda H., Shi W., Hwang I., Peterson P.A., Jackson M.R., Sprent J., and Cai Z. TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science 286 (1999) 952-954
15. Ida H., Nakashima T., Kedersha N.L., Yamasaki S., Huang M., Izumi Y., Miyashita T., Origuchi T., Kawakami A., Migita K., et al. Granzyme B leakage-induced cell death: a new type of activation-induced natural killer cell death. Eur. J. Immunol. 33 (2003) 3284-3292
16. Idziorek T., Estaquier J., DeBels F., and Ameisen J.-C. YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J. Immunol. Methods 185 (1995) 249-258
17. Jameson S.C. Maintaining the norm: T-cell homeostasis. Nat. Rev. Immunol. 2 (2002) 547-556
18. Kagi D., Ledermann B., Burki K., Seiler P., Odermatt B., Olsen K.J., Podack E.R., Zinkernagel R.M., and Hengartner H. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369 (1994) 31-37
19. Kagi D., Vignaux F., Ledermann B., Burki K., Depraetere V., Nagata S., Hengartner H., and Golstein P. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 265 (1994) 528-530
20. Kagi D., Ledermann B., Burki K., Zinkernagel R.M., and Hengartner H. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 14 (1996) 207-232
21. + T cells by perforin. Eur. J. Immunol. 29 (1999) 3262-3272
22. Kaiserman D., Knaggs S., Scarff K.L., Gillard A., Mirza G., Cadman M., McKeone R., Denny P., Cooley J., Benarafa C., et al. Comparison of human chromosome 6p25 with mouse chromosome 13 reveals a greatly expanded ov-serpin gene repertoire in the mouse. Genomics 79 (2002) 349-362
23. Kuhn R., Schwenk F., Aguet M., and Rajewsky K. Inducible gene targeting in mice. Science 269 (1995) 1427-1429
24. Kupfer A., Singer S.J., and Dennert G. On the mechanism of unidirectional killing in mixtures of two cytotoxic T lymphocytes. Unidirectional polarization of cytoplasmic organelles and the membrane-associated cytoskeleton in the effector cell. J. Exp. Med. 163 (1986) 489-498
25. Lieberman J. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3 (2003) 361-370
26. Liu N., Raja S.M., Zazzeroni F., Metkar S.S., Shah R., Zhang M., Wang Y., Bromme D., Russin W.A., Lee J.C., et al. NF-kappa B protects from the lysosomal pathway of cell death. EMBO J. 22 (2003) 5313-5322
27. Liu N., Phillips T., Zhang M., Wang Y., Opferman J.T., Shah R., and Ashton-Rickardt P.G. Serine protease inhibitor 2A is a protective factor for memory T cell development. Nat. Immunol. 5 (2004) 919-926
28. Lopez-Boado Y.S., Espinola M., Bahr S., and Belaaouaj A. Neutrophil serine proteinases cleave bacterial flagellin, abrogating its host response-inducing activity. J. Immunol. 172 (2004) 509-515
29. Lutz M.B., Kukutsch N., Ogilvie A.L.J., Robner S., Koch F., Romani N., and Schuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223 (1999) 77-92
30. Matloubian M., Suresh M., Glass A., Galvan M., Chow K., Whitmire J.K., Walsh C.M., Clark W.R., and Ahmed R. A role for perforin in downregulating T-cell responses during chronic viral infection. J. Virol. 73 (1999) 2527-2536
31. McMichael A. Preparing for HIV vaccines that induce cytotoxic T lymphocytes. Curr. Opin. Immunol. 10 (1998) 379-381
32. Medema J.P., Schuurhuis D.H., Rea D., van Tongeren J., de Jong J., Bres S.A., Laban S., Toes R.E.M., Toebes M., Schumacher T.N.M., et al. Expression of the serpin serine protease inhibitor 6 protects dendritic cells from cytotoxic T lymphocyte-induced apoptosis: differential modulation by T helper type 1 and type 2 cells. J. Exp. Med. 194 (2001) 657-667
33. Medema J.P., de Jong J., Peltenburg L.T.C., Verdegaal E.M.E., Gorter A., Bres S.A., Franken K.L.M.C., Hahne M., Albar J.P., Melief C.J.M., and Offringa R. Blockade of the granzyme B/perforin pathway through over-expression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors. Proc. Natl. Acad. Sci. USA 98 (2001) 11515-11520
34. Medhurst A., Harrison D.C., Read S.J., Campbell C.A., Robbins M.J., and Pangalos M.N. The use of TaqMan RT-PCR assays for semiquantitative analysis of gene expression in CNS tissues and disease models. J. Neurosci. Methods 98 (2000) 9-20
35. Menasche G., Pastural E., Feldmann J., Certain S., Ersoy F., Dupuis S., Wulffraat N., Bianchi D., Fischer A., Le Deist F., and de Saint Basile G. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 25 (2000) 173-176
36. Millard P.J., Henkart M.P., Reynolds C.W., and Henkart P.A. Purification and properties of cytoplasmic granules from cytotoxic rat LGL tumors. J. Immunol. 132 (1984) 3197-3204
37. Odake S., Kam C.M., Narasimhan L., Poe M., Blake J.T., Krahenbuhl O., Tschopp J., and Powers J.C. Human and murine cytotoxic T lymphocyte serine proteases: subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins. Biochemistry 30 (1991) 2217-2227
38. + T lymphocytes. Int. Immunol. 13 (2001) 411-419
39. Perou C.M., Justice M.J., Pryor R.J., and Kaplan J. Complementation of the beige mutation in cultured cells by episomally replicating murine yeast artificial chromosomes. Proc. Natl. Acad. Sci. USA 93 (1996) 5905-5909
40. Perou C.M., Moore K.J., Nagle D.L., Misumi D.J., Woolf E.A., McGrail S.H., Holmgren L., Brody T.H., Dussault Jr. B.J., Monroe C.A., et al. Identification of the murine beige gene by YAC complementation and positional cloning. Nat. Genet. 13 (1996) 303-308
41. Peters P.J., Borst J., Oorschot V., Fukuda M., Krahenbuhl O., Tschopp J., Slot J.W., and Geuze H.J. Cytotoxic T lymphocyte granules are secretory lysosomes, containing perforin and granzymes. J. Exp. Med. 173 (1991) 1099-1109
42. + memory cell homeostasis. J. Immunol. 173 (2004) 3801-3809
43. Pircher H.-P., Moskophidis D., Rohrer U., Burki K., Hengartner H., and Zinkernagel R.M. Viral escape by selection of cytotoxic T cell-resistant virus varients in vivo. Nature 346 (1990) 624-632
44. Podack E.R., Young J.D., and Cohn Z.A. Isolation and biochemical and functional characterization of perforin 1 from cytolytic T-cell granules. Proc. Natl. Acad. Sci. USA 82 (1985) 8629-8633
45. Pope C., Kim S.K., Marzo A., Masopust D., Williams K., Jiang J., Shen H., and Lefrancois L. Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166 (2001) 3402-3409
46. Revell P.A., Grossman W.J., Thomas D.A., Cao X., Behl R., Ratner J.A., Lu Z.H., and Ley T.J. Granzyme B and the downstream granzymes C and/or F are important for cytotoxic lymphocyte functions. J. Immunol. 174 (2005) 2124-2131
47. Russell J.H., and Ley T.J. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20 (2002) 323-370
48. Shi L., Kraut R.P., Aebersold R., and Greenberg A.H. A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175 (1992) 553-566
49. Silverman G.A., Bird P.I., Carrell R.W., Church F.C., Coughlin P.B., Gettins P.G.W., Irving J.A., Lomas D.A., Luke C.J., Moyer R.W., et al. The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. J. Biol. Chem. 276 (2001) 33293-33296
50. Spaner D., Raju K., Rudvanyi L., Lin Y., and Miller R.G. A role for perforin in activation-induced cell death. J. Immunol. 160 (1998) 2655-2664
51. Spaner D., Raju K., Rabinovich B., and Miller R.G. A role for perforin in activation-induced T cell death in vivo: increased expansion of allogeneic perforin-deficient T cells in SCID mice. J. Immunol. 162 (1999) 1192-1199
52. Stinchcombe J.C., Page L.J., and Griffiths G.M. Secretory lysosome biogenesis in cytotoxic T lymphocytes from normal and Chediak Higashi syndrome patients. Traffic 1 (2000) 435-444
53. Sun J., Bird C.H., Sutton V., McDonald L., Coughlin P.B., De Jong T.A., Trapani J.A., and Bird P.I. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J. Biol. Chem. 271 (1996) 27802-27809
54. Sun J., Ooms L., Bird C.H., Sutton V.R., Trapani J.A., and Bird P.I. A new family of 10 murine ovalbumin serpins includes two homologs of proteinase inhibitor 8 and two homologs of the granzyme B inhibitor (proteinase inhibitor 9). J. Biol. Chem. 272 (1997) 15434-15441
55. Trambas C.M., and Griffiths G.M. Delivering the kiss of death. Nat. Immunol. 4 (2003) 399-403
56. + cytolytic T lymphocytes. Proc. Natl. Acad. Sci. USA 87 (1990) 9015-9019
57. Ward D.M., Griffiths G.M., Stinchcombe J.C., and Kaplan J. Analysis of the lysosomal storage disease Chediak-Higashi syndrome. Traffic 1 (2000) 816-822
58. Ware C.B., Siverts L.A., Nelson A.M., Morton J.F., and Ladiges W.C. Utility of a C57BL/6 ES line versus 129 ES lines for targeted mutations in mice. Transgenic Res. 12 (2003) 743-746
59. Wilson S.M., Yip R., Swing D.A., O'Sullivan T.N., Zhang Y., Novak E.K., Swank R.T., Russell L.B., Copeland N.G., and Jenkins N.A. A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc. Natl. Acad. Sci. USA 97 (2000) 7933-7938
60. Zagury D., Bernard J., Thierness N., Feldman M., and Berke G. Isolation and characterization of individual functionally reactive cytotoxic T lymphocytes. Conjugation, killing and recycling at the single cell level. Eur. J. Immunol. 5 (1975) 812-818
61. Zajac A.J., Dye J.M., and Quinn D.G. Control of lymphocytic choriomeningitis virus infection in granzyme B deficient mice. Virology 305 (2003) 1-9