Bacterial proteins can be processed by macrophages in a transporter associated with antigen processing-independent, cysteine protease-dependent manner for presentation by MHC class I molecules

Journal of Immunology

Volumn 164, Issue 1, 2000, Pages 168-175

  Campbell, Daniel J ^a   Serwold, Thomas ^a   Shastri, Nilabh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; CD8 ANTIGEN; CYSTEINE PROTEINASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; ESCHERICHIA COLI; FEMALE; LIGAND BINDING; MACROPHAGE; MALE; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION;

EID: 0033976065     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.1.168     Document Type: Article

References (60)

1. Pamer, E. G., and P. Cresswell. 1998. Mechanisms of MHC class 1-restricted antigen processing. Annu. Rev. Immunol. 15:323.
2. York, I. A., and K. L. Rock. 1996. Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14:369.
3. Rock, K. L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A. L. Goldberg. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78:761.
4. Rock, K. L., and A. L. Goldberg. 1999. Degradation of cell proteins and the generation of MHC class I-presented peptides. Anna. Rev. Immunol. 17:739.
5. Monaco, J. J., and D. Nandi. 1995. The genetics of proteasomes and antigen processing. Annu. Rev. Genet. 29:729.
6. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature 351:456.
7. + cytotoxic T cells. J. Exp. Med. 172:1083.
8. Liu, T., X. Zhou, C. Orvell, E. Lederer, H. G. Ljunggren, and M. Jondal. 1995. Heat-inactivated Sendai virus can enter multiple MHC class I processing pathways and generate cytotoxic T lymphocyte responses in vivo. J. Immunol. 154: 3147.
9. Boehm, W., R. Schirmbeck, A. Elbe, K. Melber, D. Diminky, G. Kraal, N. Van Rooijen, Y. Barenholz, and J. Reitnann. 1995. Exogenous hepatitis B surface antigen particles processed by dendritic cells or macrophages prime murine MHC class I-restricted cytotoxic T lymphocytes in vivo. J. Immunol. 155: 3313.
10. Schirmbeck, R., W. Boehm, K. Melber, and J. Reimann. 1995. Processing of exogenous heat-aggregated (denatured) and particulate (native) hepatitis B surface antigen for class I-restricted epitope presentation. J. Immunol. 155:4676.
11. Sigal, L. J., S. Crotty, R. Andino, and K. L. Rock. 1999. Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398:77.
12. Bevan, M. J. 1976. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143:1283.
13. Pulaski, B. A., K.-Y. Yeh, N. Shastri, K. M. Maltby, D. P. Penny, E. M. Lord, and J. Frelinger. 1996. Interleukin 3 enhances CTL development and class I representation of exogenous antigen by tumor-infiltrating antigen presenting cells. Proc. Natl. Acad. Sci. USA 93:3669.
14. Carbone, F. R., C. Kurts, S. R. Bennett, J. F. Miller, and W. R. Heath. 1998. Cross-presentation: a general mechanism for CTL immunity and tolerance. Immunol. Today 19:368.
15. Schirmbeck, R., W. Böhm, and J. Reimann. 1994. Injection of detergent-denatured ovalbumin primes murine class I-restricted cytotoxic T cells in vivo. Eur. J. Immunol. 24:2068.
16. Schirmbeck, R., and J. Reimann. 1994. Peptide transporter-independent, stress protein-mediated endosomal processing of endogenous protein antigens for major histocompatibilily complex class I presentation. Eur. J. Immunol. 24:1478.
17. Schirmbeck, R., K. Melber, T. Mertens, and J. Reimann. 1994. Selective stimulation of murine cytotoxic T cell and antibody responses by particulate or monomeric hepatitis B virus surface (S) antigen. Eur. J. Immunol. 24:1088.
18. Schirmbeck, R., K. Melber, T. Mertens, and J. Reimann. 1994. Antibody and cytotoxic T-cell responses to soluble hepatitis B virus (HBV) S antigen in mice: implication for the pathogenesis of HBV-induced hepatitis. J. Virol. 68:1418.
19. + cytotoxic T lymphocyte responses in vivo. J. Immunol. 152:1110.
20. Rock, K. L. 1996. A new foreign policy: MHC class I molecules monitor the outside world. Immunol. Today 17:131.
21. Debrick, J. E., P. A. Campbell, and U. D. Staerz. 1991. Macrophages as accessory cells for class I MHC-restricted immune responses. J. Immunol. 147:2846.
22. Morein, B., B. Sundquist, S. Höglund, K. Dalsgaard, and A. Osterhaus. 1984. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature 308:457.
23. Norbury, C. C., L. J. Hewlett, A. R. Prescott, N. Shastri, and C. Watts. 1995. Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 3:783.
24. Kovacsovics-Bankowski, M., and K. L. Rock. 1994. Presentation of exogenous antigens by macrophages: analysis of major histocompatibility complex class I and II presentation and regulation by cytokines. Eur. J. Immunol. 24:2421.
25. Pfeifer, J. D., M. J. Wick, R. L. Roberts, K. Findlay, S. J. Normark, and C. V. Harding. 1993. Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature 361:359.
26. Reis e Sousa, C., and R. N. Germain. 1995. Major histocompatibility complex class I presentation of peptides derived from soluble exogenous antigen by a subset of cells engaged in phagocytosis. J. Exp. Med. 182:841.
27. Shen, Z., G. Reznikoff, G. Dranoff, and K. L. Rock. 1997. Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J. Immunol. 158:1273.
28. Svensson, M., B. Stockinger, and M. J. Wick. 1997. Bone marrow-derived dendritic cells can process bacteria for MHC-I and MHC-II presentation to T cells. J. Immunol. 158:4229.
29. Norbury, C. C., B. J. Chambers, A. R. Prescott, H. G. Ljunggren, and C. Watts. 1997. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur. J. Immunol. 27:280.
30. Albert, M. L., B. Sauter, and N. Bhardwaj. 1998. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392:86.
31. Rock, K. L., S. Gamble, and L. Rothstein. 1990. Presentation of exogenous antigen with class I major histocompatibility complex molecules. Science 249:918.
32. Allison, J. P. 1994. CD28-B7 interactions in T-cell activation. Curr. Opin. Immunol. 6:414.
33. Kovacsovics-Bankowski, M., and K. L. Rock. 1995. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 267:243.
34. Yeh, K.-Y., A. J. McAdam, B. A. Pulaski, N. Shastri, J. G. Frelinger, and E. M. Lord. 1998. IL-3 enhances both presentation of exogenous particulate antigen in association with class I major histocompatibility antigen and generation of primary tumor specific cytolytic T lymphocytes. J. Immunol. 160:5773.
35. Schirmbeck, R., K. Melber, and J. Reimann. 1995. Hepatitis B virus small surface antigen particles are processed in a novel endosomal pathway for major histocompatibility complex class I-restricted epitope presentation. Eur. J. Immunol. 25:1063.
36. 2 microglobulin in the processing of bacterial or particulate antigens via an alternate class I MHC processing pathway. J. Immunol. 156:4182.
37. Bachmann, M. F., A. Oxenius, H. Pircher, H. Hengartner, P. A. Ashton-Richardt, S. Tonegawa, and R. M. Zinkernagel. 1995. TAP1-independent loading of class I molecules by exogenous viral proteins. Eur. J. Immunol. 25:1739.
38. Karttunen, J., S. Sanderson, and N. Shastri. 1992. Detection of rare antigen presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc. Natl. Acad. Sci. USA 89:6020.
39. Mendoza, L., P. Paz, A. R. Zuberi, G. Christianson, D. C. Roopenian, and N. Shastri. 1997. Minors held by majors: the H13 minor histocompatibility locus defined as a peptide/MHC class I complex. Immunity 7:461.
40. b complex to T-cells. J. Immunol. 150:2724.
41. Higgins, D. E., N. Shastri, and D. A. Portnoy. 1999. Delivery of protein to the cytosol of macrophages using Escherichia coli K-12. Mol. Microbiol. 31:1631.
42. Sanderson, S., and N. Shastri. 1994. LacZ inducible peptide/MHC specific T-hybrids. Int. Immunol. 6:369.
43. Serwold, T., and N. Shastri. 1999. Specific proteolytic cleavages limit the diversity of the pool of peptides available to MHC Class I molecules in living cells. J. Immunol. 162:4712.
44. + T cells. Cell 71:1205.
45. Wick, M. J., and J. D. Pfeifer. 1996. Major histocompatibility complex class I presentation of ovalbumin peptide 257-264 from exogenous sources: protein context influences the degree of TAP-independent presentation. Eur. J. Immunol. 26:2790.
46. Schirmbeck, R., and J. Reimann. 1996. "Empty" L-d molecules capture peptides from endocytosed hepatitis B surface antigen particles for major histocompatibility complex class I-restricted presentation. Eur. J. Immunol. 26:2812.
47. Hewitt, E. W., A. Treumann, N. Morrice, P. J. Tatnell, J. Kay, and C. Watts. 1997. Natural processing sites for human cathepsin E and cathepsin D in tetanus toxin: implications for T cell epitope generation. J. Immunol 159:4693.
48. Shi, G. P., J. A. Villadangos, G. Dranoff, C. Small, L. Gu, K. J. Haley, R. Riese, H. L. Ploegh, and H. A. Chapman. 1999. Cathepsin S required for normal MHC class II peptide loading and germinal center development. Immunity 10:197.
49. Nakagawa, T. Y., W. H. Brissette, P. D. Lira, R. J. Griffiths, N. Petrushova, J. Stock, J. D. McNeish, S. E. Eastman, E. D. Howard, S. R. Clarke, et al. 1999. Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice. Immunity 10:207.
50. Rodriguez, G. M., and S. Diment. 1995. Destructive proteolysis by cysteine proteases in antigen presentation of ovalbumin. Eur. J. Immunol. 25:1823.
51. Nakagawa, T., W. Roth, P. Wong, A. Nelson, A. Farr, J. Deussing, J. A. Villadangos, H. Ploegh, C. Peters, and A. Y. Rudensky. 1998. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 280:450.
52. Riese, R. J., P. R. Wolf, D. Bromme, L. R. Natkin, J. A. Villadangos, H. L. Ploegh, and H. A. Chapman. 1996. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity. 4:357.
53. Rotzschke, O., K. Falk, S. Stevanovic, G. Jung, P. Walden, and H.-G. Rammensee. 1991. Exact prediction of a natural T cell epitope. Eur. J. Immunol. 21:2891.
54. Malarkannan, S., S. Goth, D. R. Buchholz, and N. Shastri. 1995. The role of MHC class I molecules in the generation of endogenous peptide/MHC complexes. J. Immunol. 154:585.
55. Ho, M. K., and T. A. Springer. 1982. Mac-1 antigen: quantitative expression in macrophage populations and tissues, and immunofluorescent localization in spleen. J. Immunol. 128:2281.
56. Mettay, J. P., M. D. Witmer-Pack, R. Agger, M. T. Crowley, D. Lawless, and R. M. Steinman. 1990. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J. Exp. Med. 171: 1753.
57. Ploegh, H. L. 1998. Viral strategies of immune evasion. Science 280:248.
58. Levitskaya, J., M. Coram, V. Levitsky, S. Imreh, P. M. Steigerwald-Mullen, G. Klein, M. G. Kurilla, and M. G. Masucci. 1995. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375:685.
59. + T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity 7:791.
60. Stenger, S., R. J. Mazzaccaro, K. Uyemura, S. Cho, P. F. Barnes, J. P. Rosat, A. Sette, M. B. Brenner, S. A. Porcelli, B. R. Bloom, et al. 1997. Differential effects of cytolytic T cell subsets on intracellular infection. Science 276:1684.