Antigen processing of two H2-IE(d)-restricted epitopes is differentially influenced by the structural changes in a viral glycoprotein

Journal of Immunology

Volumn 161, Issue 4, 1998, Pages 1599-1607

  Chianese Bullock, Kimberly A ^a   Russell, Helena I ^b   Moller, Christopher ^c   Gerhard, Walter ^c   Monaco, John J ^b   Eisenlohr, Laurence C ^a,d  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c WISTAR INSTITUTE   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; VIRUS GLYCOPROTEIN;

AMINO ACID ANALYSIS; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; ENDOCYTOSIS; EPITOPE MAPPING; FEMALE; INFLUENZA VIRUS; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

ANIMALS; ANTIGEN PRESENTATION; B-LYMPHOCYTES; CELL COMPARTMENTATION; ENDOCYTOSIS; EPITOPES; FEMALE; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-D ANTIGENS; LYMPHOMA, B-CELL; MICE; MICE, INBRED BALB C; PEPTIDE FRAGMENTS; TUMOR CELLS, CULTURED;

EID: 0032529386     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Unanue, E. R. 1984. Antigen-presenting function of the macrophage. Annu. Rev. Immunol. 2:395.
2. Germain, R. N., and D. H. Margulies. 1993. The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 11:403.
3. Cresswell, P. 1994. Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12:259.
4. Germain, R. N., F. Castellino, R. Han, C. Reis e Sousa, P. Romagnoli, S. Sadegh-Nasseri, and G.-M. Zhong. 1996. Processing and presentation of endocytically acquired protein antigens by MHC class Il and class I molecules. Immunol. Rev. 151:5.
5. Cresswell, P. 1992. Chemistry and functional role of the invariant chain. Curr. Opin. Immunol. 4:87.
6. Roche, P. A., M. S. Marks, and P. Cresswell. 1991. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 354:392.
7. Lotteau, V., L. Teyton, A. Peleraux, T. Nilsson, L. Karlsson, S. L. Schmid, V. Quaranta, and P. A. Peterson. 1990. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348:600.
8. Bakke, O., and B. Dobberstein. 1990. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63:707.
9. Lamb, C. A., J. W. Yewdell, J. R. Bennink, and P. Cresswell. 1991. Invariant chain targets HLA class II molecules to acidic endosomes containing internalized influenza virus. Proc. Natl. Acad. Sci. USA 88:5998.
10. Romagnoli, P., C. Layet, J. Yewdell, O. Bakke, and R. N. Germain. 1993. Relationship between invariant chain expression and major histocompatibility complex class II transport into early and late endocytic compartments. J. Exp. Med. 177:583.
11. Guagliardi, L. E., B. Koppelman, J. S. Blum, M. S. Marks, P. Cresswell, and F. M. Brodsky. 1990. Co-localization of molecules involved in antigen processing and presentation in an early endocytic compartment. Nature 343:133.
12. Roche, P. A., C. L. Teletski, E. Stang, O. Bakke, and E. O. Long. 1993. Cell surface HLA-DR-invariant chain complexes are targeted to endosomes by rapid internalization. Proc. Natl. Acad. Sci. USA 90:8581.
13. Maric, M. A., M. D. Taylor, and J. S. Blum. 1994. Endosomal aspartic proteinases are required for invariant chain processing. Proc. Natl. Acad. Sci. USA 91: 2171.
14. Blum, J. S., and P. Cresswell. 1988. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc. Natl. Acad. Sci. USA 85; 3975.
15. Riberdy, J. M., J. R. Newcomb, M. J. Surman, J. A. Barbosa, and P. Cresswell. 1992. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 360:474.
16. Sette, A., S. Ceman, R. T. Kubo, K. Sakaguchi, E. Apella, D. F. Hunt, T. A. Davis, H. Michel, J. Shabaniwitz, R, Rudersdorf, H. M. Grey, and R. DeMars. 1992. Invariant chain peptides in most HLA-DR molecules of an antigen-processing mutant. Science 258:1801.
17. Avva, R. R., and P. Cresswell. 1994. In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity 1:763.
18. Kropshofer, H., A. B. Vogt, L. J. Stern, and G. J. Hämmerling. 1995. Self-release of CLIP in peptide loading of HLA-DR molecules. Science 270:1357.
19. Sanderson, F., M. J. Kleijmeer, A. Kelly, D. Verwoerd, A. Tulp, J. J. Neefjes, H. J. Geuze, and J. Trowsdale. 1994. Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science 266:1566.
20. Pierre, P., L. K. Denzin, C. Hammond, J. R. Drake, S. Amigorena, P. Cresswell, and I. Mellman. 1996. HLA-DM is localized to conventional and unconventional MHC class II-containing endocytic compartments. Immunity 4:229.
21. Denzin, L. K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. Cell 82:155.
22. Sloan, V. S., P. Cameron, G. Porter, M. Gammon, M. Amaya, E. Mellins, and D. M. Zaller. 1995. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375:802.
23. Sherman, M. A., D. A. Weber, and P. E. Jensen. 1995. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity 3:197.
24. Katz, J. F., C. Stebbins, E. Apella, and A. J. Sant. 1996. Invariant chain and DM edit self-peptide presentation by major histocompatibility complex (MHC) class II molecules. J. Exp. Med. 184:1747.
25. Denzin, L. K., C. Hammond, and P. Cresswell. 1996. HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J. Exp. Med. 184:2153.
26. Kropshofer, H., S. O. Arndt, G. Moldenhauer, G. J. Hämmerling, and A. B. Vogt. 1997. HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH. Immunity 6:293.
27. Amigorena, S., J. R. Drake, P. Webster, and I. Mellman. 1994. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 369:113.
28. Escola, J.-M., F. Deleuil, E. Sung, J. Boretto, P. Chavrier, and J.-P. Gorvel. 1996. Characterization of a lysozyme-major histocompatibility complex class II molecule-loading compartment as a specialized recycling endosome in murine B lymphocytes. J. Biol. Chem. 271:27360.
29. Peters, P. J., J. J. Neefjes, V. Oorschot, H. L. Ploegh, and H. J. Geuze. 1991. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 349:669.
30. Qui, Y., X. Xu, A. Wandinger-Ness, D. P. Dalke, and S. K. Pierce. 1994. Separation of subcellular compartments containing distinct functional forms of MHC class n. J. Cell Biol. 125:595.
31. Tulp, A., D. Verwoerd, B. Dobberstein, H. L. Ploegh, and J. Pieters. 1994. Isolation and characterization of the intracellular MHC class II compartment. Nature 369:120.
32. West, M. A., J. M. Lucocq, and C. Watts. 1994. Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells. Nature 369:147.
33. Rudensky, A. Y., M. Marie, S. Eastman, L. Shoemaker, P. C. DeRoos, and J. S. Blum. 1994. Intracellular assembly and transport of endogenous peptide-MHC class II complexes. Immunity 1:585.
34. Castellino, F., and R. N. Germain. 1995. Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity 2:73.
35. Zhong, G., P. Romagnoli, and R. N. Germain. 1997. Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control presentation of distinct determinants in a single protein. J. Exp. Med. 185:429.
36. Pinet, V., M. S. Malnati, and E. O. Long. 1994. Two processing pathways for the MHC class II-restricted presentation of exogenous influenza virus antigen. J. Immunol. 152:4852.
37. Pinet, V., M. Vergelli, R. Martin, O. Bakke, and E. O. Long. 1995. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature 375: 603.
38. Robadey, C., W. Ammerlaan, C. Muller, I. Cloutier, R.-P. Sékaly, J.-A. Haefliger, and S. Demotz. 1997. The processing routes determined by negatively charged residues in DR1-restricted T cell determinants. J. Immunol. 159:3238.
39. Griffin, J. P., R. Chu, and C. V. Harding. 1997. Early endosomes and a late endocytic compartment generate different peptide-class II MHC complexes via distinct processing mechanisms. J. Immunol. 158:1523.
40. Lindner, R., and E. R. Unanue. 1996. Distinct antigen MHC class II complexes generated by separate processing pathways. EMBO J. 15:6910.
41. Wiley, D. C., and J. J Skehel. 1987. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu. Rev. Biochem. 56:365.
42. White, J. M., and I. A. Wilson. 1987. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J. Cell Biol. 105:2887.
43. Doms, R. W., A. Helenius, and J. White. 1985. Membrane fusion activity of the influenza virus hemagglutinin: the low pH-induced conformational change. J. Biol. Chem. 260:2973.
44. Skehel, J., P. M. Bayley, E. B. Brown, S. R. Martin, M. D. Waterfield, J. M. White, I. A. Wilson, and D. C. Wiley. 1982. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc. Natl. Acad. Sci. USA 79:968.
45. Bullough, P. A., F. M. Hughson, J. J. Skehel, and D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37.
46. Hurwitz, J. L., E. Heber-Katz, C. J. Hackett, and W. Gerhard. 1984. Characterization of the murine Th response to influenza virus hemagglutinin: evidence for three major specificities. J. Immunol. 133:3371.
47. Eisenlohr, L. C., W. Gerhard, and C. J. Hackett. 1988. Individual class II-restricted antigenic determinants of the same protein exhibit distinct kinetics of appearance and persistence on antigen-presenting cells. J. Immunol. 141:2581.
48. Eisenlohr, L. C., W. Gerhard, and C. J. Hackett. 1988. Acid-induced conformational modification of the hemagglutinin molecule alters interaction of influenza virus with antigen presenting cells. J. Immunol. 141:1870.
49. Gerhard, W., J. W. Yewdell, M. E. Frankel, and R. G. Webster. 1981. Antigenic structure of influenza virus hemagglutinin defined by hybridoma antibodies. Nature 290:713.
50. Kim, K. J., C. Kanellopoulos-Langevin, R. M. Merwin, D. H. Sachs, and R. Asofsky. 1979. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 122:549.
51. + CTL that utilizes a perforin-rather than a Fas ligand-dependent cytotoxic mechanism. J. Immunol. 156:15.
52. Dang, L. H., L. L. Lien, B. Benacerraf, and K. L. Rock. 1993. A mutant antigen-presenting cell defective in antigen presentation expresses class II MHC molecules with an altered conformation. J. Immunol. 150:4206.
53. Gerhard, W., C. J. Hackett, and F. Melchers. 1983. The recognition specificity of a murine helper T cell for hemagglutinin of influenza virus A/PR/8/34. J. Immunol. 130:2379.
54. Scherle, P. A., and W. Gerhard. 1988. Differential ability of B cells specific for external vs internal influenza virus proteins to respond to help from influenza virus-specific T-cell clones in vivo. Proc. Natl. Acad. Sci. USA 85:4446.
55. Eisenlohr, L. C., I. Bacik, J. R. Bennink, K. Bernstein, and J. W. Yewdell. 1992. Expression of a membrane protease enhances presentation of endogenous antigens to MHC class I-restricted T lymphocytes. Cell 71:963.
56. Caton, A. J., G. G. Brownlee, J. W. Yewdell, and W. Gerhard. 1982. The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31:417.
57. Brand, C. M., and J. J. Skehel. 1972. Crystalline antigen from the influenza virus envelope. Nat. New Biol. 238:145.
58. Sette, A., S. Southwood, J. Miller, and E. Apella. 1995. Binding of major histocompatibility complex class II to the invariant chain-derived peptide, CLIP, is regulated by allelic polymorphism in class II. J. Exp. Med. 181:677.
59. Hackett, C. J., J. W. Yewdell, J. R. Bennink, and M. Wysocka. 1991. Class II MHC-restricted T cell determinants processed from either endosomes or the cytosol show similar requirements for host protein transport but different kinetics of presentation. J. Immunol. 146:2944.
60. Yewdell, J. W., A. Taylor, A. Yellen, A. Caton, W. Gerhard, and T. Bächi. 1993. Mutations in or near the fusion peptide of the influenza virus hemagglutinin affect an antigenic site in the globular region. J. Virol. 67:933.
61. Eisenlohr, L. C., and C. J. Hackett. 1989. Class II major histocompatibility complex-restricted T cells specific for a virion structural protein that do not recognize exogenous influenza virus. J. Exp. Med. 169:921.
62. Lazarowitz, S. G., and P. W. Choppin. 1975. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 68:440.
63. Klenk, H.-D., R. Rott, M. Orlich, and J. Blödorn. 1975. Activation of influenza A viruses by trypsin treatment. Virology 68:426.
64. Wilson, I. A., J. J. Skehel, and D. C. Wiley. 1981. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289:366.
65. Skehel, J. J., T. Bizebard, P. A. Bullough, F. M. Hughson, M. Knossow, D. A. Steinhauer, S. A. Wharton, and D. C. Wiley. 1995. Membrane fusion by influenza hemagglutinin. Cold Spring Harb. Symp. Quant. Biol. 60:573.
66. Gerhard, W., A. M. Haberman, P. A. Scherle, A. H. Taylor, G. Palladino, and A. J. Caton. 1991. Identification of eight determinants in the hemagglutinin molecule of influenza virus A/PR/8/34 (H1N1) which are recognized by class II-restricted T cells from BALB/c mice. J. Virol. 65:364.
67. Germain, R. N., and L. R. Hendrix. 1991. MHC class II structure, occupancy, and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 353:134.
68. Schafer, P. H., J. M. Green, S. Malapati, L. Gu, and S. K. Pierce. 1996. HLA-DM is present in one-fifth the amount of HLA-DR in the class II peptide-loading compartment where it associates with leupeptin-induced peptide (LIP)-HLA-DR complexes. J. Immunol. 157:5487.
69. Ma, C., and J. S. Blum. 1997. Receptor-mediated endocytosis of antigens overcomes the requirement for HLA-DM in class II-restricted antigen presentation. J. Immunol. 158:1.
70. Matlin, K. S., H. Reggio, A. Helenius, and K. Simons. 1981. Infectious entry pathway of influenza virus in a canine kidney cell line. J. Cell Biol. 91:601.
71. Germain, R. N. 1994. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76:287.