Multiple synergizing factors contribute to the strength of the CD8+ T cell response against listeriolysin O

International Immunology

Volumn 18, Issue 1, 2006, Pages 89-100

  Bruder, Dunja ^a   Nussbaum, Alexander K ^b   Gakamsky, Dimitry M ^c   Schirle, Markus ^b   Stevanovic, Stefan ^b   Singh Jasuja, Harpreet ^b   Darji, Ayub ^d   Chakraborty, Trinad ^d   Schild, Hansjörg ^b,e   Pecht, Israel ^c   Weiss, Siegfried ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Antigen presentation processing; Cytotoxic T cells; Epitopes; MHC class I

Indexed keywords

ALANINE; BACTERIAL TOXIN; EPITOPE; ISOLEUCINE; LISTERIOLYSIN; LYMPHOCYTE ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; PROTEASOME; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANTIGENICITY; ARTICLE; BACTERIAL IMMUNITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; FEMALE; GENE MUTATION; IN VITRO STUDY; LISTERIA MONOCYTOGENES; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PEPTIDE SYNTHESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN INTERACTION; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIGEN PRESENTATION; BACTERIAL TOXINS; CD8-POSITIVE T-LYMPHOCYTES; EPITOPES, T-LYMPHOCYTE; FEMALE; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; IMMUNODOMINANT EPITOPES; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MUTATION; PROTEIN TRANSPORT;

EID: 30344487585     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxh352     Document Type: Article

References (76)

1. Sercarz, E. E., Lehmann, P. V., Ametani, A., Benichou, G., Miller, A. and K. Moudgil. 1993. Dominance and crypticity of T cell antigenic determinants. Annu. Rev. Immunol. 11:729.
2. Braciale, T. J., Sweetser, M. T., Morrison, L. A., Kittlesen, D. J. and Braciale, V. L. 1989. Class I major histocompatibility complex-restricted cytolytic T lymphocytes recognize a limited number of sites on influenza hemagglutinin. Proc. Natl Acad. Sci. USA 86:277.
3. Berzofsky, J. A. 1988. Immunodominance in T lymphocyte recognition. Immunol. Lett. 18:83.
4. Pamer, E. G., Harty, J. T. and Bevan, M. J. 1991. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes. Nature 353:852.
5. Chen, W., Anton, L. C., Bennink, J. R. and Yewdell, J. W. 2000. Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 12:83.
6. Yewdell, J. W. and Bennink, J. R. 1999. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu. Rev. Immunol. 17:51.
7. Gellin, B. G. and Broome, C. V. 1989. Listeriosis. J. Am. Med. Assoc. 261:1313.
8. Kaufmann, S. H., Rodewald, H. R., Hug, E. and de Libero, G. 1988. Cloned Listeria monocytogenes specific non-MHC-restricted Lyt-cells with cytolytic and protective activity. J. Immunol. 140: 3173.
9. Pamer, E. G. 1994. Direct sequence identification and kinetic analysis of an MHC class I-restricted Listeria monocytogenes CTL epitope. J. Immunol. 152:686.
10. Sijts, A. J., Neisig, A., Neefjes, J. and Pamer, E. G. 1996. Two Listeria monocytogenes CTL eitopes are processed from the same antigen with different efficiencies. J. Immunol. 156:683.
11. Busch, D. H., Bouwer, H. G., Hinrichs, D. and Pamer, E. G. 1997. A nonamer peptide derived from Listeria monocytogenes metalloprotease is presented to cytolytic T lymphocytes. Infect. Immun. 65:5326.
12. d class I molecules. Eur. J. Immunol. 23:2005.
13. Vijh, S. and Pamer, E. G. 1997. Immunodominant and subdominant CTL responses to Listeria monocytogenes infection. J. Immunol. 158:3366.
14. Decatur, A. L. and Portnoy, D. A. 2000. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 290:992.
15. Darji, A., Chakraborty, T., Wehland, J. and Weiss, S. 1995. Listeriolysin generates a route for the presentation of exogenous antigens by major histocompatibility complex class I. Eur. J. Immunol. 25:2967.
16. Darji, A., Chakraborty, T., Wehland, J. and Weiss, S. 1997. TAP-dependent major histocompatibility complex class I presentation of soluble proteins using listeriolysin. Eur. J. Immunol. 27:1353.
17. Saledo, M., Momburg, F., Hämerling, G. J. and Ljunggren, H. G. 1994. Resistance to natural killer cell lysis conferred by TAP1/2 genes in human antigen-processing mutant cells. J. Immunol. 152:1702.
18. + T cells against exogenous proteins: Establishment and characterization of a T cell line specific for the membrane protein ActA of Listeria monocytogenes. Eur. J. Immunol. 28:2630.
19. Gakamsky, D. M., Bjorkman, P. J. and Pecht, I. 1996. Peptide interaction with a class I major histocompatibility complex-encoded molecule: allosteric control of the ternary complex stability. Biochemistry 35:14841.
20. b complex. Biochemistry 38:12165.
21. Gakamsky, D. M., Davis, D. M., Strominger, J. L. and Pecht, I. 2000. Assembly and dissociation of human leukocyte antigen (HLA)-A2 studied by real-time fluorescence resonance energy transfer. Biochemistry 39:11163.
22. Neefjes, J., Gottfried, E., Roelse, J. et al. 1995. Analysis of the fine specificity of rat, mouse and human TAP peptide transporters. Eur. J. Immunol. 25:1133.
23. Kuehn, L., Dahlmann, B., Gauthier, F. and Neubauer, H. P. 1989. High-molecular-mass proteinases in rabbit reticulocytes: The multicatalytic proteinase is an ATP-independent enzyme and ATP-activated proteolysis is in part associated with a cysteine proteinase complexed to alpha 1-macroglobulin. Biochim. Biophys. Acta 991:263.
24. Bouwer, H. G. A., Moors, M. and Hinrichs, D. J. 1996. Elimination of the listeriolysin O-directed immune response by conservative alteration of the immunodominant listeriolysin O amino acid 91 to 99 epitope. Infect. Immun. 64:3728.
25. Slifka, M. K., Blattmann, J. N., Sourdive, D. J. et al. 2003. Preferential escape of subdominant CD8+ T cells during negative selection results in an altered antiviral T cell hierarchy. J. Immunol. 170:1231.
26. Boes, B., Hengel, H., Ruppert, T., Multhaupt, G., Koszinowski, U. H. and Kloetzel, P. M. 1994. Interferon gamma stimulation modulates the proteolytic activity and cleavage site preference of 20S mouse proteasomes. J. Exp. Med. 179:901.
27. Dick, T. P., Ruppert, T., Groettrupp, M. et al. 1996. Coordinated dual cleavages induced by the proteasome regulator PA28 lead to dominant MHC ligands. Cell 88:253.
28. Driscoll, J., Brown, M. G., Finley, D. and Monaco, J. J. 1993. MHC-linked LMP gene products specifically alter peptidase activities of the proteasome. Nature 365:262.
29. Gaczynska, M., Rock, K. L. and Goldberg, A. L. 1993. γ-interferon and expression of MHC genes regulate peptide hydrolysis by proteasomes. Nature 365:264.
30. Groettrup, M., Soza, A., Eggers, M. et al. 1996. A role for the proteasome regulator P28a in antigen presentation. Nature 381:166.
31. Gileadi, U., MoinsTeisserenc, H. T., Correa, I. et al. 1999. Generation of an immunodominant CTL epitope is affected by proteasome subunit composition and stability of the antigenic protein. J. Immunol. 163:6045.
32. Schwarz, K., van den Broek, M., Kostka, S. et al. 2000. Overexpression of the proteasome subunits LMP2, LMP7, and MECL-1 but not PA28α/β enhances the presentation of an immunodominant lymphocytic choreomeningitis virus T cell epitope. J. Immunol. 165:768.
33. Sijts, A. J. A. M., Standera, S., Toes, R. E. M. et al. 2000. MHC class I antigen processing of an adenovirus CTL epitope is linked to the levels of immunoproteasomes in infected cells. J. Immunol. 164: 4500.
34. Darji, A., Bruder, D., zur Lage, S. et al. 1998. The role of the bacterial membrane protein ActA in immunity and protection against Listeria monocytogenes. J. Immunol. 161:2414.
35. Momburg, F., Roelse, J., Hämmerling, G. J. and Neefjes, J. J. 1994. Peptide size selection by the major histocompatibility complex-encoded peptide transporter. J. Exp. Med. 179:1613.
36. Momburg, F., Neefjes, J. J. and Hammerling, G. J. 1994. Peptide selection by MHC encoded TAP transporters. Curr. Opin. Immunol. 6:32.
37. Lauveau, G., Kakimi, K., Niedermann, G. et al. 1999. Human transporters associated with antigen processing (TAP) select epitope precursor peptides for processing in the endoplasmic reticulum and presentation to T cells. J. Exp. Med. 190:1227.
38. d epitope is generated and translocated into the endoplasmic reticulum as an 11-mer peptide precursor. J. Immunol. 167:1515.
39. Villanueva, M. S., Sijts, A. J. A. M. and Pamer, E. G. 1995. Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells. J. Immunol. 155:5227.
40. Yellen-Shaw, A. and Eisenlohr, L. C. 1997. Regulation of class I-restricted epitope processing by local or distal flanking sequence. J. Immunol. 158:1727.
41. Yellen-Shaw, A. J., Wherry, E. J., Dubois, G. C. and Eisenlohr, L. C. 1997. Point mutation flanking a CTL epitope ablates in vitro and in vivo recognition of a full-length viral protein. J. Immunol. 158:3227.
42. + T cell recognition of an endogenously processed epitope is regulated primarily by residues within the epitope. J. Exp. Med. 176:1335.
43. Eisenlohr, L. C., Yewdell, J. W. and Bennink, J. R. 1992. Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes. J. Exp. Med. 175:481.
44. Seifert, U., Liermann, H., Racanelli, V. et al. 2004. Hepatitis C virus mutation affects proteasomal epitope processing. J. Clin. Invest. 114:250.
45. Sette, A., Vitiello, A., Reherman, B. et al. 1994. The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J. Immunol. 153:5586.
46. b cells. J. Immunol. 152:4843.
47. Basler, M., Youhnovski, N., van den Broek, M., Przybylski, M. and Groettrup, M. 2004. Immunoproteasomes down-regulate presentation of a subdominant T cell epitope from lymphocytic choriomeningitis virus. J. Immunol. 173:3925.
48. Niedermann, G., Butz, S., Ihlenfeldt, H. G. et al. 1995. Contribution of proteasome-mediated proteolysis to the hierarchy of epitopes presented by major histocompatibility complex class I molecules. Immunity 2:289.
49. Deng, Y., Yewdell, J. W., Eisenlohr, L. C. and Bennink, J. R. 1997. MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J. Immunol. 158:1507.
50. Meier, U. C., Kleneman, P., Griffin, P. et al. 1995. Cytotoxic T lymphocyte lysis inhibited by viable HIV mutants. Science 270:1360.
51. Probst-Kepper, M., Hecht, H. J., Herrmann, H. et al. 2004. Conformational restraints and flexibility of 14-meric peptides in complex with HLA-B*3501. J. Immunol. 173:5610.
52. Davenport, M. P., Smith, K. J., Barouch, D. et al. 1997. HLA class I binding motifs derived from random peptide libraries differ at the COOH terminus from those of eluted peptides. J. Exp. Med. 185:367.
53. Van der Most, R. G., Murali-Krishna, K., Whitton, J. L. et al. 1998. Identification of D-b and K-b restricted subdominant cytotoxic T cell responses in lymphocytic choriomeningitis virus infected mice. Virology 240:158.
54. Gallimore, A., Dumrese, T., Hengartner, H., Zinkernagel, R. M. and Rammensee, H.-G. 1998. Protective immunity does not correlate with the hierarchy of virus specific cytotoxic T cell responses to naturally processed peptides. J. Exp. Med. 187:1647.
55. Momburg, F., Roelse, J., Howard, J. C., Butcher, G. W., Hämmerling, G. and Neefjes, J. J. 1994. Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367:648.
56. Fruci, D., Lauvau, G., Saveanu, L. et al. 2003. Quantifying recruitment of cytosolic peptides for HLA class I presentation: Impact of TAP transport. J. Immunol. 170:2977.
57. Chen, W., Khilko, S., Fecondo, J., Margulies, D. H. and McCluskey, J. 1994. Determinant selection of major histocompatibility complex class I-restricted antigenic peptides is explained by class I-peptide affinity and is strongly influenced by nondominant anchor residues. J. Exp. Med. 180:1471.
58. Nussbaum, A. K., Dick, T. P., Keilholz, W. et al. 1998. Cleavage motifs of the yeast 20S proteasome beta subunits deduced from digests of enolase 1. Proc. Natl Acad. Sci. USA 95:12504.
59. Del Val, M., Schlicht, H.-J., Ruppert, T., Reddehase, M. J. and Koszinowsky, U. H. 1991. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell 66:1145.
60. Eggers, M., Boes-Fabian, B., Ruppert, T., Kloetzel, P. M. and Koszinowski, U. H. 1995. The cleavage preference of the proteasome governs the yield of antigenic peptides. J. Exp. Med. 182:1865.
61. Shastri, N., Serwold, T. and Gonzalez, F. 1995. Presentation of endogenous peptide/MHC class I complexes is profoundly influenced by specific C-terminal flanking sequences. J. Immunol. 155:4339.
62. Kloetzel, P.-M. 2004. Generation of major histocompatibility complex class I antigens: Functional interplay between proteasomes and TPPII. Nat. Immunol. 5:661.
63. Kessler, J. H., Beekman, N. J. Bres-Vloemans, S. A. et al. 2001. Efficient identification of novel HLA-A*0201-presented cytotoxic T lymphocyte epitopes in the widely expressed tumor antigen PRAME by proteasome mediated digestion analysis. J. Exp. Med. 193:73.
64. Morel, S., Levy, F., Burlet-Schulz, O. et al. 2000. Processing of some antigens by the standard proteasome but not by the immunoproteasome results in poor presentation by dendritic cells. Immunity 12:107.
65. Cascio, P., Hilton, C., Kisselev, A. F., Rock, K. L. and Goldberg, A. L. 2001. 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J. 20:2357.
66. Kisselev, A. F., Akopian, T. N., Woo, K. M. and Goldberg, A. L. 1998. The size of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem. 274:3363.
67. Rock, K. L., York, I. A. and Goldberg, A. L. 2004. Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat. Immunol. 5:670.
68. Kloetzel, P.-M. and Ossendorp, F. 2004. Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr. Opin. Immunol. 16:76.
69. Saric, T., Beninga, J., Graef, C. I., Akopian, T. N., Rock, K. L. and Goldberg, A. L. 2001. Major histocompatibility complex class I-presented antigenic peptides are degraded in cytosolic extracts primarily by thimet oligopeptidase. J. Biol. Chem. 276:36474.
70. York, I. A., Mo, A. X., Lemerise, K. et al. 2003. The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 18:429.
71. Stoltze, L., Schirle, M., Schwarz, G. et al. 2000. Two new proteases in the MHC class I processing pathway. Nat. Immunol. 1:413.
72. Serwold, T., Gaw, S. and Shastri, N. 2001. ER aminopeptidases generate a unique pool of peptides for MHC class I molecules. Nat. Immunol. 2:644.
73. Saric, T., Chang, S. C., Hattori, A. et al. 2002. An IFN-gamma induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat. Immunol. 3:1169.
74. Serwold, T., Gonzalez, F., Kim, J., Jacob, R. and Shastri, N. 2002. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419:480.
75. York, I. A., Chang, S. C., Saric, T. et al. 2002. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat. Immunol. 3:1177.
76. Valmori, D., Gileadi, U., Servis, C. et al. 1999. Modulation of proteasomal activity required for the generation of a cytotoxic T lymphocyte-defined peptide derived from tumor antigen MAGE-3. J. Exp. Med. 189:895.