Delayed contraction of the CD8+ T cell response toward lymphocytic choriomeningitis virus infection in mice lacking serglycin

Journal of Immunology

Volumn 181, Issue 2, 2008, Pages 1043-1051

  Grujic, Mirjana ^a   Christensen, Jan P ^a   Sørensen, Maria R ^a   Abrink, Magnus ^b   Pejler, Gunnar ^c   Thomsen, Allan R ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UPPSALA UNIVERSITY   (Sweden)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANZYME B; PERFORIN; PHENFORMIN; TUMOR NECROSIS FACTOR ALPHA; GRANZYME; GZMB PROTEIN, MOUSE; PROTEOGLYCAN; SERGLYCIN; VESICULAR TRANSPORT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; EXPERIMENTAL MOUSE; IN VIVO STUDY; KINETICS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; VESICULAR STOMATITIS VIRUS; VIRUS INFECTION; VIRUS MENINGITIS; VIRUS STRAIN; WILD TYPE; ANIMAL; C57BL MOUSE; CYTOTOXICITY; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; NATURAL KILLER CELL; PHYSIOLOGY; VESICULAR STOMATITIS; VIROLOGY;

ANIMALS; ARENAVIRIDAE INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; GRANZYMES; INTERFERON TYPE II; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PERFORIN; PROTEOGLYCANS; TUMOR NECROSIS FACTOR-ALPHA; VESICULAR STOMATITIS; VESICULAR STOMATITIS INDIANA VIRUS; VESICULAR TRANSPORT PROTEINS;

EID: 49049090422     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.2.1043     Document Type: Article

References (57)

1. Monks, C. R., B. A. Freiberg, H. Kupfer, N. Sciaky, and A. Kupfer. 1998. Threedimensional segregation of supramolecular activation clusters in T cells. Nature 395: 82-86.
2. Stinchcombe, J. C., G. Bossi, S. Booth, and G. M. Griffiths. 2001. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761.
3. Bossi, G., and G. M. Griffiths. 2005. CTL secretory lysosomes: biogenesis and secretion of a harmful organelle. Semin. Immunol. 17: 87-94. (Pubitemid 39575984)
4. Curtsinger, J. M., D. C. Lins, and M. F. Mescher. 2003. Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J. Exp. Med. 197: 1141-1151.
5. Russell, J. H., and T. J. Ley. 2002. Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20: 323-370.
6. Lieberman, J. 2003. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3: 361-370. (Pubitemid 37323196)
7. Lieberman, J., and Z. Fan. 2003. Nuclear war: the granzyme A-bomb. Curr. Opin. Immunol. 15: 553-559.
8. Lord, S. J., R. V. Rajotte, G. S. Korbutt, and R. C. Bleackley. 2003. Granzyme B: a natural born killer. Immunol. Rev. 193: 31-38.
9. Wagner, L., O. O. Yang, E. A. Garcia-Zepeda, Y. Ge, S. A. Kalams, B. D. Walker, M. S. Pasternack, and A. D. Luster. 1998. Beta-chemokines are released from HIV-1-specific cytolytic T-cell granules complexed to proteoglycans. Nature 391: 908-911. (Pubitemid 28157670)
10. 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. (Pubitemid 23057866)
11. Smyth, M. J., J. M. Kelly, V. R. Sutton, J. E. Davis, K. A. Browne, T. J. Sayers, and J. A. Trapani. 2001. Unlocking the secrets of cytotoxic granule proteins. J. Leukocyte Biol. 70: 18-29.
12. Schmidt, R. E., R. P. MacDermott, G. Bartley, M. Bertovich, D. A. Amato, K. F. Austen, S. F. Schlossman, R. L. Stevens, and J. Ritz. 1985. Specific release of proteoglycans from human natural killer cells during target lysis. Nature 318: 289-291.
13. MacDermott, R. P., R. E. Schmidt, J. P. Caulfield, A. Hein, G. T. Bartley, J. Ritz, S. F. Schlossman, K. F. Austen, and R. L. Stevens. 1985. Proteoglycans in cellmediated cytotoxicity. Identification, localization, and exocytosis of a chondroitin sulfate proteoglycan from human cloned natural killer cells during target cell lysis. J. Exp. Med. 162: 1771-1787.
14. Kjellen, L., and U. Lindahl. 1991. Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60: 443-475.
15. Ruoslahti, E. 1988. Structure and biology of proteoglycans. Annu. Rev. Cell Biol. 4: 229-255.
16. Elliott, J. F., C. L. Miller, B. Pohajdak, D. Talbot, C. D. Helgason, R. C. Bleackley, and V. Paetkau. 1993. Induction of a proteoglycan core protein mRNA in mouse T lymphocytes. Mol. Immunol. 30: 749-754. (Pubitemid 23162779)
17. Kjellen, L., I. Pettersson, P. Lillhager, M. L. Steen, U. Pettersson, P. Lehtonen, T. Karlsson, E. Ruoslahti, and L. Hellman. 1989. Primary structure of a mouse mastocytoma proteoglycan core protein. Biochem. J. 263: 105-113. (Pubitemid 19243821)
18. Stevens, R. L., S. Avraham, M. C. Gartner, G. A. Bruns, K. F. Austen, and J. H. Weis. 1988. Isolation and characterization of a cDNA that encodes the peptide core of the secretory granule proteoglycan of human promyelocytic leukemia HL-60 cells. J. Biol. Chem. 263: 7287-7291. (Pubitemid 18155755)
19. Toyama-Sorimachi, N., F. Kitamura, H. Habuchi, Y. Tobita, K. Kimata, and M. Miyasaka. 1997. Widespread expression of chondroitin sulfate-type serglycins with CD44 binding ability in hematopoietic cells. J. Biol. Chem. 272: 26714-26719. (Pubitemid 27458898)
20. Masson, D., P. J. Peters, H. J. Geuze, J. Borst, and J. Tschopp. 1990. Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry 29: 11229-11235.
21. Galvin, J. P., L. H. Spaeny-Dekking, B. Wang, P. Seth, C. E. Hack, and C. J. Froelich. 1999. Apoptosis induced by granzyme B-glycosaminoglycan complexes: implications for granule-mediated apoptosis in vivo. J. Immunol. 162: 5345-5350.
22. Metkar, S. S., B. Wang, M. Aguilar-Santelises, S. M. Raja, L. Uhlin-Hansen, E. Podack, J. A. Trapani, and C. J. Froelich. 2002. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity 16: 417-428.
23. Raja, S. M., B. Wang, M. Dantuluri, U. R. Desai, B. Demeler, K. Spiegel, S. S. Metkar, and C. J. Froelich. 2002. Cytotoxic cell granule-mediated apoptosis: characterization of the macromolecular complex of granzyme B with serglycin. J. Biol. Chem. 277: 49523-49530. (Pubitemid 36014390)
24. Grujic, M., T. Braga, A. Lukinius, M. L. Eloranta, S. D. Knight, G. Pejler, and M. Abrink. 2005. Serglycin-deficient cytotoxic T lymphocytes display defective secretory granule maturation and granzyme B storage. J. Biol. Chem. 280: 33411-33418. (Pubitemid 41397139)
25. Nansen, A., T. Jensen, J. P. Christensen, S. O. Andreasen, C. Ropke, O. Marker, and A. R. Thomsen. 1999. Compromised virus control and augmented perforinmediated immunopathology in IFN-γ-deficient mice infected with lymphocytic choriomeningitis virus. J. Immunol. 163: 6114-6122.
26. + T lymphocytes mediate clearance of virus and regulate the antiviral antibody response. J. Virol. 61: 1867-1874.
27. Abrink, M., M. Grujic, and G. Pejler. 2004. Serglycin is essential for maturation of mast cell secretory granule. J. Biol. Chem. 279: 40897-40905. (Pubitemid 39287689)
28. Ahmed, R., and M. B. Oldstone. 1988. Organ-specific selection of viral variants during chronic infection. J. Exp. Med. 167: 1719-1724. (Pubitemid 18128750)
29. Thomsen, A. R., A. Nansen, C. Andersen, J. Johansen, O. Marker, and J. P. Christensen. 1997. Cooperation of B cells and T cells is required for survival of mice infected with vesicular stomatitis virus. Int. Immunol. 9: 1757-1766. (Pubitemid 27494138)
30. + T cells but do not induce cell differentiation. Int. Immunol. 11: 1463-1473.
31. Tough, D. F., P. Borrow, and J. Sprent. 1996. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 272: 1947-1950. (Pubitemid 26234507)
32. Battegay, M., S. Cooper, A. Althage, J. Banziger, H. Hengartner, and R. M. Zinkernagel. 1991. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33: 191-198.
33. + effector T cell responses. J. Immunol. 164: 3689-3697.
34. Wherry, E. J., and R. Ahmed. 2004. Memory CD8 T-cell differentiation during viral infection. J. Virol. 78: 5535-5545.
35. Braga, T., M. Grujic, A. Lukinius, L. Hellman, M. Abrink, and G. Pejler. 2007. Serglycin proteoglycan is required for secretory granule integrity in mucosal mast cells. Biochem. J. 403: 49-57. (Pubitemid 46569866)
36. + T cells during viral infection: correlation with stable memory development. J. Gen. Virol. 83: 2123-2133.
37. Shin, H., and E. J. Wherry. 2007. CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19: 408-415. (Pubitemid 47284857)
38. + T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
39. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188: 2205-2213.
40. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
41. Niemann, C. U., M. Abrink, G. Pejler, R. L. Fischer, E. I. Christensen, S. D. Knight, and N. Borregaard. 2007. Neutrophil elastase depends on serglycin proteoglycan for localization in granules. Blood 109: 4478-4486.
42. Woulfe, D. S., J. K. Lilliendahl, S. August, L. Rauova, M. A. Kowalska, M. Abrink, G. Pejler, J. G. White, and B. P. Schick. 2008. Serglycin proteoglycan deletion induces defects in platelet aggregation and thrombus formation in mice. Blood 111: 3458-3467.
43. Kagi, D., B. Ledermann, K. Burki, P. Seiler, B. Odermatt, K. J. Olsen, E. R. Podack, R. M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369: 31-37. (Pubitemid 24144352)
44. Zajac, A. J., J. M. Dye, and D. G. Quinn. 2003. Control of lymphocytic choriomeningitis virus infection in granzyme B deficient mice. Virology 305: 1-9. (Pubitemid 36062806)
45. Griffiths, G. M., and S. Isaaz. 1993. Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 120: 885-896. (Pubitemid 23056295)
46. Lemansky, P., E. Smolenova, C. Wrocklage, and A. Hasilik. 2007. Neutrophil elastase is associated with serglycin on its way to lysosomes in U937 cells. Cell Immunol. 246: 1-7. (Pubitemid 47087771)
47. Hallgren, J., U. Karlson, M. Poorafshar, L. Hellman, and G. Pejler. 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. (Pubitemid 30825911)
48. Pejler, G., and L. Berg. 1995. Regulation of rat mast cell protease 1 activity: protease inhibition is prevented by heparin proteoglycan. Eur. J. Biochem. 233: 192-199.
49. Mercado, R., S. Vijh, S. E. Allen, K. Kerksiek, I. M. Pilip, and E. G. Pamer. 2000. Early programming of T cell populations responding to bacterial infection. J. Immunol. 165: 6833-6839. (Pubitemid 32001151)
50. + T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol. 2: 415-422.
51. van Stipdonk, M. J., E. E. Lemmens, and S. P. Schoenberger. 2001. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2: 423-429.
52. Busch, D. H., K. M. Kerksiek, and E. G. Pamer. 2000. Differing roles of inflammation and antigen in T cell proliferation and memory generation. J. Immunol. 164: 4063-4070.
53. Vella, A. T., T. Mitchell, B. Groth, P. S. Linsley, J. M. Green, C. B. Thompson, J. W. Kappler, and P. Marrack. 1997. CD28 engagement and proinflammatory cytokines contribute to T cell expansion and long-term survival in vivo. J. Immunol. 158: 4714-4720.
54. Roberts, R., J. Gallagher, E. Spooncer, T. D. Allen, F. Bloomfield, and T. M. Dexter. 1988. Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis. Nature 332: 376-378. (Pubitemid 18091081)
55. Tufvesson, E., and G. Westergren-Thorsson. 2002. Tumour necrosis factor-α interacts with biglycan and decorin. FEBS Lett. 530: 124-128. (Pubitemid 35248197)
56. Wrenshall, L. E., J. L. Platt, E. T. Stevens, T. N. Wight, and J. D. Miller. 2003. Propagation and control of T cell responses by heparan sulfate-bound IL-2. J. Immunol. 170: 5470-5474.
57. Lander, A. D. 1998. Proteoglycans: master regulators of molecular encounter? Matrix Biol. 17: 465-472.