Immunodominance of CD4 T cells to foreign antigens is peptide intrinsic and independent of molecular context: Implications for vaccine design

Journal of Immunology

Volumn 181, Issue 5, 2008, Pages 3039-3048

  Weaver, Jason M ^a   Lazarski, Christopher A ^a   Richards, Katherine A ^a   Chaves, Francisco A ^a   Jenks, Scott A ^a   Menges, Paula R ^a   Sant, Andrea J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE; VACCINE; ALLOANTIGEN; HLA ANTIGEN CLASS 2; PEPTIDE FRAGMENT; PROTEIN; T LYMPHOCYTE RECEPTOR;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; CELL SELECTION; CELL SPECIFICITY; CELL STIMULATION; DNA FLANKING REGION; IMMUNOGENICITY; LYMPH NODE; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; IMMUNOLOGY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS II; ISOANTIGENS; MICE; MICE, INBRED BALB C; PEPTIDE FRAGMENTS; PEPTIDES; PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; VACCINES;

EID: 51549100883     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.5.3039     Document Type: Article

References (111)

1. Sette, A., and B. Peters. 2007. Immune epitope mapping in the post-genomic era: lessons for vaccine development. Curr. Opin. Immunol. 19: 106-110. (Pubitemid 46073693)
2. Sant, A. J., F. A. Chaves, F. R. Krafcik, C. A. Lazarski, P. Menges, K. Richards, and J. M. Weaver. 2007. Immunodominance in CD4 T-cell responses: implications for immune responses to influenza virus and for vaccine design. Exp. Rev. Vaccines 6: 357-368.
3. Sant, A. J., F. A. Chaves, S. A. Jenks, K. A. Richards, P. Menges, J. M. Weaver, and C. A. Lazarski. 2005. The relationship between immunodominance, DM editing, and the kinetic stability of MHC class II:peptide complexes. Immunol. Rev. 207: 261-278. (Pubitemid 41415023)
4. Sercarz, E. E., P. V. Lehmann, A. Ametani, G. Benichou, A. Miller, and K. Moudgil. 1993. Dominance and crypticity of T cell antigenic determinants. Annu. Rev. Immunol. 11: 729-766.
5. Fairchild, P. J. 1999. Reversal of immunodominance among autoantigenic T-cell epitopes. Autoimmunity 30: 209-221.
6. Blum, J. S., C. Ma, and S. Kovats. 1997. Antigen-presenting cells and the selection of immunodominant epitopes. Crit. Rev. Immunol. 17: 411-417.
7. + T cell responses. Immunity 25: 533-543.
8. + T-cell-based cancer vaccines. Adv. Cancer Res. 95: 203-247.
9. Peters, B., and A. Sette. 2007. Integrating epitope data into the emerging web of biomedical knowledge resources. Nat. Rev. Immunol. 7: 485-490. (Pubitemid 46834847)
10. + responses to viruses: cell biology, cellular immunology, and mathematical models. Immunity 21: 149-153.
11. Liu, Z., K. P. Williams, Y. H. Chang, and J. A. Smith. 1993. Immunodominance: a single amino acid substitution within an antigenic site alters intramolecular selection of T cell determinants. J. Immunol. 151: 1852-1858. (Pubitemid 23235658)
12. Nikcevich, K. M., D. Kopielski, and A. Finnegan. 1994. Interference with the binding of a naturally processed peptide to class II alters the immunodominance of T cell epitopes in vivo. J. Immunol. 153: 1015-1026.
13. Adorini, L., S. Muller, F. Cardinaux, P. V. Lehmann, F. Falcioni, and Z. A. Nagy. 1988. In vivo competition between self peptides and foreign antigens in T-cell activation. Nature 334: 623-625. (Pubitemid 18205282)
14. Moudgil, K. D., H. Deng, N. K. Nanda, I. S. Grewal, A. Ametani, and E. E. Sercarz. 1996. Antigen processing and T cell repertoires as crucial aleatory features in induction of autoimmunity. J. Autoimmun. 9: 227-234.
15. Yewdell, J. W., and J. R. Bennink. 1999. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu. Rev. Immunol. 17: 51-88. (Pubitemid 29241119)
16. Safley, S. A., P. E. Jensen, P. A. Reay, and H. K. Ziegler. 1995. Mechanisms of T cell epitope immunodominance analyzed in murine listeriosis. J. Immunol. 155: 4355-4366.
17. Gapin, L., J. P. Cabaniols, R. Cibotti, D. M. Ojcius, P. Kourilsky, and J. M. Kanellopoulos. 1997. Determinant selection for T-cell tolerance in HEL-transgenic mice: dissociation between immunogenicity and tolerogenicity. Cell. Immunol. 177: 77-85. (Pubitemid 27192325)
18. Ma, C., P. E. Whiteley, P. M. Cameron, D. C. Freed, A. Pressey, S. L. Chen, B. Garni-Wagner, C. Fang, D. M. Zaller, L. S. Wicker, and J. S. Blum. 1999. Role of APC in the selection of immunodominant T cell epitopes. J. Immunol. 163: 6413-6423.
19. Thayer, W. P., J. R. Kraft, S. M. Tompkins, J. C. Moore, and P. E. Jensen. 1999. Assessment of the role of determinant selection in genetic control of the immune response to insulin in H-2b mice. J. Immunol. 163: 2549-2554.
20. 1 mice: implications for autoimmunity and infection. J. Immunol. 161: 6046-6053.
21. Manoury, B., E. W. Hewitt, N. Morrice, P. M. Dando, A. J. Barrett, and C. Watts. 1998. An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396: 695-699. (Pubitemid 29003950)
22. Watts, C., S. P. Matthews, D. Mazzeo, B. Manoury, and C. X. Moss. 2005. Asparaginyl endopeptidase: case history of a class II MHC compartment protease. Immunol. Rev. 207: 218-228. (Pubitemid 41415020)
23. Vidard, L., K. L. Rock, and B. Benacerraf. 1991. The generation of immunogenic peptides can be selectively increased or decreased by proteolytic enzyme inhibitors. J. Immunol. 147: 1786-1791.
24. Musson, J. A., N. Walker, H. Flick-Smith, E. D. Williamson, and J. H. Robinson. 2003. Differential processing of CD4 T-cell epitopes from the protective antigen of Bacillus anthracis. J. Biol. Chem. 278: 52425-52431.
25. Hsieh, C. S., P. deRoos, K. Honey, C. Beers, and A. Y. Rudensky. 2002. A role for cathepsin L and cathepsin S in peptide generation for MHC class II presentation. J. Immunol. 168: 2618-2625.
26. Moss, C. X., J. A. Villadangos, and C. Watts. 2005. Destructive potential of the aspartyl protease cathepsin D in MHC class II-restricted antigen processing. Eur. J. Immunol. 35: 3442-3451.
27. Schneider, S. C., J. Ohmen, L. Fosdick, B. Gladstone, J. Guo, A. Ametani, E. E. Sercarz, and H. Deng. 2000. Cutting edge: introduction of an endopeptidase cleavage motif into a determinant flanking region of hen egg lysozyme results in enhanced T cell determinant display. J. Immunol. 165: 20-23.
28. Zhu, H., K. Liu, J. Cerny, T. Imoto, and K. D. Moudgil. 2005. Insertion of the dibasic motif in the flanking region of a cryptic self-determinant leads to activation of the epitope-specific T cells. J. Immunol. 175: 2252-2260. (Pubitemid 41113832)
29. Phan, U. T., B. Arunachalam, and P. Cresswell. 2000. γ-Interferon- inducible lysosomal thiol reductase (GILT): maturation, activity, and mechanism of action. J. Biol. Chem. 275: 25907-25914.
30. Dai, G., S. Carmicle, N. K. Steede, and S. J. Landry. 2002. Structural basis for helper T-cell and antibody epitope immunodominance in bacteriophage T4 Hsp10: role of disordered loops. J. Biol. Chem. 277: 161-168. (Pubitemid 34952041)
31. Carmicle, S., N. K. Steede, and S. J. Landry. 2007. Antigen three-dimensional structure guides the processing and presentation of helper T-cell epitopes. Mol. Immunol. 44: 1159-1168. (Pubitemid 44415976)
32. Landry, S. J. 2000. Helper T-cell epitope immunodominance associated with structurally stable segments of hen egg lysozyme and HIV gp120. J. Theor. Biol. 203: 189-201.
33. Lazarski, C. L., F. Chaves, S. Jenks, S. Wu, K. Richards, J. M. Weaver, and A. Sant. 2005. The kinetic stability of MHC class II:peptide complexes is a key parameter that dictates immunodominance. Immunity 23: 29-40. (Pubitemid 41019655)
34. Busch, R., C. H. Rinderknecht, S. Roh, A. W. Lee, J. J. Harding, T. Burster, T. M. Hornell, and E. D. Mellins. 2005. Achieving stability through editing and chaperoning: regulation of MHC class II peptide binding and expression. Immunol. Rev. 207: 242-260. (Pubitemid 41415022)
35. Lich, J. D., J. A. Jayne, D. Zhou, J. F. Elliott, and J. S. Blum. 2003. Editing of an immunodominant epitope of glutamate decarboxylase by HLA-DM. J. Immunol. 171: 853-859.
36. Lovitch, S. B., S. J. Petzold, and E. R. Unanue. 2003. Cutting edge: H-2DM is responsible for the large differences in presentation among peptides selected by I-Ak during antigen processing. J. Immunol. 171: 2183-2186.
37. Nanda, N. K., and E. K. Bikoff. 2005. DM peptide-editing function leads to immunodominance in CD4 T cell responses in vivo. J. Immunol. 175: 6473-6480. (Pubitemid 41598889)
38. Nanda, N., and A. J. Sant. 2000. DM determines the cryptic and immunodominant fate of T cell epitopes. J. Exp. Med. 192: 781-788. (Pubitemid 30737585)
39. Davies, M. N., and D. R. Flower. 2007. Harnessing bioinformatics to discover new vaccines. Drug Discov. Today 12: 389-395.
40. Sundaresh, S., A. Randall, B. Unal, J. M. Petersen, J. T. Belisle, M. G. Hartley, M. Duffield, R. W. Titball, D. H. Davies, P. L. Felgner, and P. Baldi. 2007. From protein microarrays to diagnostic antigen discovery: a study of the pathogen Francisella tularensis. Bioinformatics 23: i508-i518. (Pubitemid 47244438)
41. + T cell responses to newly identified HLA-A*0201-restricted T cell epitopes conserved among vaccinia and variola (smallpox) viruses. J. Exp. Med. 197: 927-932.
42. Wahl, A., J. Weidanz, and W. Hildebrand. 2006. Direct class I HLA antigen discovery to distinguish virus-infected and cancerous cells. Exp. Rev. Proteomics 3: 641-652. (Pubitemid 46021200)
43. Sette, A., and J. Fikes. 2003. Epitope-based vaccines: an update on epitope identification, vaccine design and delivery. Curr. Opin. Immunol. 15: 461-470. (Pubitemid 36934509)
44. Qin, H., C. Zhou, D. Wang, W. Ma, X. Liang, C. Lin, Y. Zhang, and S. Zhang. 2005. Specific antitumor immune response induced by a novel DNA vaccine composed of multiple CTL and T helper cell epitopes of prostate cancer associated antigens. Immunol. Lett. 99: 85-93. (Pubitemid 40718938)
45. Chen, L., T. Gao, N. Yang, J. Huang, Y. Chen, T. Gao, Q. Li, and D. Ren. 2007. Immunization with a synthetic multiepitope antigen induces humoral and cellular immune responses to hepatitis C virus in mice. Viral Immunol. 20: 170-179. (Pubitemid 46608962)
46. Fournillier, A., P. Dupeyrot, P. Martin, P. Parroche, A. Pajot, L. Chatel, A. Fatmi, E. Gerossier, C. Bain, Y. C. Lone, et al. 2006. Primary and memory T cell responses induced by hepatitis C virus multiepitope long peptides. Vaccine 24: 3153-3164.
47. Vuola, J. M., S. Keating, D. P. Webster, T. Berthoud, S. Dunachie, S. C. Gilbert, and A. V. Hill. 2005. Differential immunogenicity of various heterologous prime-boost vaccine regimens using DNA and viral vectors in healthy volunteers. J. Immunol. 174: 449-455.
48. Kanto, T., and N. Hayashi. 2006. Immunopathogenesis of hepatitis C virus infection: multifaceted strategies subverting innate and adaptive immunity. Intern. Med. 45: 183-191.
49. Sette, A., M. Newman, B. Livingston, D. McKinney, J. Sidney, G. Ishioka, S. Tangri, J. Alexander, J. Fikes, and R. Chesnut. 2002. Optimizing vaccine design for cellular processing, MHC binding and TCR recognition. Tissue Antigens 59: 443-451. (Pubitemid 35034464)
50. Tacken, P. J., I. J. de Vries, K. Gijzen, B. Joosten, D. Wu, R. P. Rother, S. J. Faas, C. J. Punt, R. Torensma, G. J. Adema, and C. G. Figdor. 2005. Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 106: 1278-1285.
51. Sabado, R. L., E. Babcock, D. G. Kavanagh, V. Tjomsland, B. D. Walker, J. D. Lifson, N. Bhardwaj, and M. Larsson. 2007. Pathways utilized by dendritic cells for binding, uptake, processing and presentation of antigens derived from HIV-1. Eur. J. Immunol. 37: 1752-1763.
52. Steinman, R. M. 1996. Dendritic cells and immune-based therapies. Exp. Hematol. 24: 859-862.
53. + T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J. Exp. Med. 203: 607-617.
54. + T cells in a spectrum of human MHC I haplotypes. Proc. Natl. Acad. Sci. USA 104: 1289-1294.
55. Ferenci, T., and U. Klotz. 1978. Affinity chromatographic isolation of the periplasmic maltose binding protein of Escherichia coli. FEBS Lett. 94: 213-217. (Pubitemid 9038309)
56. Wang, X., and T. Mosmann. 2001. In vivo priming of CD4 T cells that produce interleukin (IL)-2 but not IL-4 or interferon (IFN)-γ, and can subsequently differentiate into IL-4- or IFN-γ-secreting cells. J. Exp. Med. 194: 1069-1080. (Pubitemid 32995778)
57. Kappler, J. W., B. Skidmore, J. White, and P. Marrack. 1981. Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas: lack of independent antigen and H-2 recognition. J. Exp. Med. 153: 1198-1214.
58. Bhattacharya, A., M. E. Dorf, and T. A. Springer. 1981. A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication. J. Immunol. 127: 2488-2495. (Pubitemid 12245847)
59. Sarmiento, M., A. L. Glasebrook, and F. W. Fitch. 1980. IgG or IgM monoclonal antibodies reactive with different determinants on the molecular complex bearing Lyt 2 antigen block T cell-mediated cytolysis in the absence of complement. J. Immunol. 125: 2665-2672. (Pubitemid 11204170)
60. Bruce, J., F. W. Symington, T. J. McKearn, and J. Sprent. 1981. A monoclonal antibody discriminating between subsets of T and B cells. J. Immunol. 127: 2496-2501. (Pubitemid 12245848)
61. Loss, G. E., Jr., C. G. Elias, P. E. Fields, R. K. Ribaudo, M. McKisic, and A. J. Sant. 1993. Major histocompatibility complex class II-restricted presentation of an internally synthesized antigen displays cell-type variability and segregates from the exogenous class II and endogenous class I presentation pathways. J. Exp. Med. 178: 73-85.
62. Martineau, P., C. Leclerc, and M. Hofnung. 1996. Modulating the immunological properties of a linear B-cell epitope by insertion into permissive sites of the MalE protein. Mol. Immunol. 33: 1345-1358. (Pubitemid 27196369)
63. Carson, R. T., K. M. Vignali, D. L. Woodland, and D. A. Vignali. 1997. T cell receptor recognition of MHC class II-bound peptide flanking residues enhances immunogenicity and results in altered TCR V region usage. Immunity 7: 387-399.
64. + T cells that are dependent on MHC class II-bound peptide-flanking residues. [Published erratum appears in 2002 J. Immunol. 169: 4674.] J. Immunol. 169: 739-749.
65. Berkower, I., L. A. Matis, G. K. Buckenmeyer, F. R. Gurd, D. L. Longo, and J. A. Berzofsky. 1984. Identification of distinct predominant epitopes recognized by myoglobin-specific T cells under the control of different Ir genes and characterization of representative T cell clones. J. Immunol. 132: 1370-1378. (Pubitemid 14154565)
66. Reiner, S. L., D. J. Fowell, N. H. Moskowitz, K. Swier, D. R. Brown, C. R. Brown, C. W. Turck, P. A. Scott, N. Killeen, and R. M. Locksley. 1998. Control of Leishmania major by a monoclonal αβ T cell repertoire. J. Immunol. 160: 884-889. (Pubitemid 28049331)
67. Shimonkevitz, R., S. Colon, J. W. Kappler, P. Marrack, and H. M. Grey. 1984. Antigen recognition by H-2-restricted T cells. II. A tryptic ovalbumin peptide that substitutes for processed antigen. J. Immunol. 133: 2067-2074. (Pubitemid 14035311)
68. Moudgil, K. D., D. Sekiguchi, S. Y. Kim, and E. E. Sercarz. 1997. Immunodominance is independent of structural constraints: each region within hen eggwhite lysozyme is potentially available upon processing of native antigen. J. Immunol. 159: 2574-2579.
69. Moudgil, K. D., E. E. Sercarz, and I. S. Grewal. 1998. Modulation of the immunogenicity of antigenic determinants by their flanking residues. Immunol. Today 19: 217-220.
70. d protein using two functionally distinct registers. Biochemistry 38: 16663-16670.
71. Stryer, L. 1965. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin: a fluorescent probe of non-polar binding sites. J. Mol. Biol. 13: 482-495.
72. Turner, D. C., and L. Brand. 1968. Quantitative estimation of protein binding site polarity: fluorescence of N-arylaminonaphthalenesulfonates. Biochemistry 7: 3381-3390.
73. Sundd, M., S. Kundu, and M. V. Jagannadham. 2002. Acid and chemical induced conformational changes of ervatamin B: presence of partially structured multiple intermediates. J. Biochem. Mol. Biol. 35: 143-154. (Pubitemid 34389482)
74. Dubey, V. K., and M. V. Jagannadham. 2003. Differences in the unfolding of procerain induced by pH, guanidine hydrochloride, urea, and temperature. Biochemistry 42: 12287-12297. (Pubitemid 37296505)
75. Coeffier, E., J. M. Clement, V. Cussac, N. Khodaei-Boorane, M. Jehanno, M. Rojas, A. Dridi, M. Latour, R. El Habib, F. Barre-Sinoussi, et al. 2000. Antigenicity and immunogenicity of the HIV-1 gp41 epitope ELDKWA inserted into permissive sites of the MalE protein. Vaccine 19: 684-693.
76. Rodseth, L. E., P. Martineau, P. Duplay, M. Hofnung, and F. A. Quiocho. 1990. Crystallization of genetically engineered active maltose-binding proteins, including an immunogenic viral epitope insertion. J. Mol. Biol. 213: 607-611.
77. Shimonkevitz, R., J. Kappler, P. Marrack, and H. Grey. 1983. Antigen recognition by H-2-restricted T cells. I. Cell-free antigen processing. J. Exp. Med. 158: 303-316.
78. Stein, P. E., A. G. Leslie, J. T. Finch, and R. W. Carrell. 1991. Crystal structure of uncleaved ovalbumin at 1.95 A resolution. J. Mol. Biol. 221: 941-959. (Pubitemid 121003429)
79. Robertson, J. M., P. E. Jensen, and B. D. Evavold. 2000. DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 164: 4706-4712.
80. Scott, C. A., P. A. Peterson, L. Teyton, and I. A. Wilson. 1998. Crystal structures of two I-Ad-peptide complexes reveal that high affinity can be achieved without large anchor residues. [Published erratum appears in 1998 Immunity 8: 531.] Immunity 8: 319-329.
81. Rholam, M., N. Brakch, D. Germain, D. Y. Thomas, C. Fahy, H. Boussetta, G. Boileau, and P. Cohen. 1995. Role of amino acid sequences flanking dibasic cleavage sites in precursor proteolytic processing: the importance of the first residue C-terminal of the cleavage site. Eur. J. Biochem. 227: 707-714.
82. Scamuffa, N., F. Calvo, M. Chretien, N. G. Seidah, and A. M. Khatib. 2006. Proprotein convertases: lessons from knockouts. FASEB J. 20: 1954-1963.
83. Steiner, D. F. 1998. The proprotein convertases. Curr. Opin. Chem. Biol. 2: 31-39.
84. Bachert, C., C. Fimmel, and A. D. Linstedt. 2007. Endosomal trafficking and proprotein convertase cleavage of cis Golgi protein GP73 produces marker for hepatocellular carcinoma. Traffic 8: 1415-1423. (Pubitemid 47394245)
85. Seidah, N. G., and M. Chretien. 1997. Eukaryotic protein processing: endoproteolysis of precursor proteins. Curr. Opin. Biotechnol. 8: 602-607. (Pubitemid 27455338)
86. Glandieres, J. M., M. Hertzog, N. Lazar, N. Brakch, P. Cohen, B. Alpert, and M. Rholam. 2002. Kinetics of precursor cleavage at the dibasic sites: involvement of peptide dynamics. FEBS Lett. 516: 75-79.
87. Mayer, G., G. Boileau, and M. Bendayan. 2004. Sorting of furin in polarized epithelial and endothelial cells: expression beyond the Golgi apparatus. J. Histochem. Cytochem. 52: 567-579. (Pubitemid 38658190)
88. Gammon, G., H. M. Geysen, R. J. Apple, E. Pickett, M. Palmer, A. Ametani, and E. E. Sercarz. 1991. T cell determinant structure: cores and determinant envelopes in three mouse major histocompatibility complex haplotypes. J. Exp. Med. 173: 609-617.
89. Belmares, M. P., R. Busch, K. W. Wucherpfennig, H. M. McConnell, and E. D. Mellins. 2002. Structural factors contributing to DM susceptibility of MHC class II/peptide complexes. J. Immunol. 169: 5109-5117.
90. Van Ham, S. M., U. Gruneberg, G. Malcherek, I. Broker, A. Melms, and J. Trowsdale. 1996. Human histocompatibility leukocyte antigen (HLA)-DM edits peptides presented by HLA-DR according to their ligand binding motifs. J. Exp. Med. 184: 2019-2024.
91. Weber, D. A., B. D. Evavold, and P. E. Jensen. 1996. Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 274: 618-620.
92. Katz, J. F., C. Stebbins, E. Appella, 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: 1747-1753. (Pubitemid 26404466)
93. 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: 802-806.
94. Kropshofer, H., A. B. Vogt, G. Moldenhauer, J. Hammer, J. S. Blum, and G. J. Hammerling. 1996. Editing of the HLA-DR-peptide repertoire by HLA-DM. EMBO J. 15: 6144-6154.
95. Raddrizzani, L., E. Bono, A. B. Vogt, H. Kropshofer, F. Gallazzi, T. Sturniolo, G. J. Hammerling, F. Sinigaglia, and J. Hammer. 1999. Identification of destabilizing residues in HLA class II-selected bacteriophage display libraries edited by HLA-DM. Eur. J. Immunol. 29: 660-668. (Pubitemid 29078528)
96. Lazarski, C. A., F. A. Chaves, and A. J. Sant. 2006. The impact of DM on MHC class II-restricted antigen presentation can be altered by manipulation of MHC-peptide kinetic stability. J. Exp. Med. 203: 1319-1328.
97. Tan, M. C., A. M. Mommaas, J. W. Drijfhout, R. Jordens, J. J. Onderwater, D. Verwoerd, A. A. Mulder, A. N. van der Heiden, D. Scheidegger, L. C. Oomen, et al. 1997. Mannose receptor-mediated uptake of antigens strongly enhances HLA class II-restricted antigen presentation by cultured dendritic cells. Eur. J. Immunol. 27: 2426-2435. (Pubitemid 27404330)
98. Mahnke, K., M. Guo, S. Lee, H. Sepulveda, S. L. Swain, M. Nussenzweig, and R. M. Steinman. 2000. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J. Cell Biol. 151: 673-684. (Pubitemid 30828145)
99. Engering, A. J., M. Cella, D. Fluitsma, M. Brockhaus, E. C. Hoefsmit, A. Lanzavecchia, and J. Pieters. 1997. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur. J. Immunol. 27: 2417-2425.
100. Prigozy, T. I., P. A. Sieling, D. Clemens, P. L. Stewart, S. M. Behar, S. A. Porcelli, M. B. Brenner, R. L. Modlin, and M. Kronenberg. 1997. The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity 6: 187-197.
101. Lanzavecchia, A. 1985. Antigen-specific interaction between T and B cells. Nature 314: 537-539.
102. Bonnerot, C., D. Lankar, D. Hanau, D. Spehner, J. Davoust, J. Salamero, and W. H. Fridman. 1995. Role of B cell receptor Igα and Igβ subunits in MHC class II-restricted antigen presentation. Immunity 3: 335-347.
103. Fikes, J. D., and A. Sette. 2003. Design of multi-epitope, analogue-based cancer vaccines. Exp. Opin. Biol. Ther. 3: 985-993.
104. Livingston, B., C. Crimi, M. Newman, Y. Higashimoto, E. Appella, J. Sidney, and A. Sette. 2002. A rational strategy to design multiepitope immunogens based on multiple Th lymphocyte epitopes. J. Immunol. 168: 5499-5506. (Pubitemid 34556128)
105. Wu, S., M. Beier, M. B. Sztein, J. Galen, T. Pickett, A. A. Holder, O. G. Gomez-Duarte, and M. M. Levine. 2000. Construction and immunogenicity in mice of attenuated Salmonella typhi expressing Plasmodium falciparum merozoite surface protein 1 (MSP-1) fused to tetanus toxin fragment C. J. Biotechnol. 83: 125-135. (Pubitemid 30734755)
106. Jiang, Y., C. Lin, B. Yin, X. He, Y. Mao, M. Dong, P. Xu, L. Zhang, B. Liu, and H. Wang. 1999. Effects of the configuration of a multi-epitope chimeric malaria DNA vaccine on its antigenicity to mice. Chin. Med. J. 112: 686-690. (Pubitemid 29374406)
107. Sette, A., R. Chesnut, B. Livingston, C. Wilson, and M. Newman. 2000. HLA-binding peptides as a therapeutic approach for chronic HIV infection. Drugs 3: 643-648.
108. Bull, T. J., S. C. Gilbert, S. Sridhar, R. Linedale, N. Dierkes, K. Sidi-Boumedine, and J. Hermon-Taylor. 2007. A novel multi-antigen virally vectored vaccine against Mycobacterium avium subspecies paratuberculosis. PLoS ONE 2: e1229.
109. Do, Y., C. G. Park, Y. S. Kang, S. H. Park, R. M. Lynch, H. Lee, B. S. Powell, and R. M. Steinman. 2008. Broad T cell immunity to the LcrV virulence protein is induced by targeted delivery to DEC-205/CD205-positive mouse dendritic cells. Eur. J. Immunol. 38: 20-29.
110. Nchinda, G., J. Kuroiwa, M. Oks, C. Trumpfheller, C. G. Park, Y. Huang, D. Hannaman, S. J. Schlesinger, O. Mizenina, M. C. Nussenzweig, et al. 2008. The efficacy of DNA vaccination is enhanced in mice by targeting the encoded protein to dendritic cells. J. Clin. Invest. 118: 1427-1436.
111. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.