Phagocytic antigen processing and effects of microbial products on antigen processing and T-cell responses

Immunological Reviews

Volumn 168, Issue , 1999, Pages 217-239

  Ramachandra, Lakshmi ^a   Chu, Rose S ^a   Askew, David ^a   Noss, Erika H ^a   Canaday, David H ^a   Potter, N Stevenson ^a   Johnsen, Alyssa ^a   Krieg, Arthur M ^b,c   Nedrud, John G ^a   Boom, W Henry ^a   Harding, Clifford V ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c CpG ImmunoPharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; IMMUNOGLOBULIN G2A; INTERLEUKIN 5; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RIBONUCLEASE;

ANIMAL CELL; ANTIGEN PRESENTATION; ENDOCYTOSIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNITY; IMMUNIZATION; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; REVIEW; SPLEEN CELL; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; BACTERIAL TOXINS; CHOLERA TOXIN; CPG ISLANDS; ENTEROTOXINS; ESCHERICHIA COLI PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; MYCOBACTERIUM TUBERCULOSIS; PHAGOCYTOSIS; T-LYMPHOCYTES;

EID: 0032993283     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-065X.1999.tb01295.x     Document Type: Review

References (188)

1. 1. Levitskaya J, et al. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 1995;375:685-688.
2. 2. Ahn K, Angulo A, Ghazal P, Peterson PA, Yang Y, Fruh K. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc Natl Acad Sci USA 1996;93:10990-10995.
3. 3. Hill AB. Mechanisms of interference with the MHC class I-restricted pathway of antigen presentation by herpesviruses. Immunol Cell Biol 1996;74:523-526.
4. 4. Früh K, Ahn K, Peterson PA. Inhibition of MHC class I antigen presentation by viral proteins. J Mol Med 1997;75:18-27.
5. 5. Hengel H, Koszinowski UH. Interference with antigen processing by viruses. Curr Opin Immunol 1997;9:470-476.
6. 6. Oldstone MB. How viruses escape from cytotoxic T lymphocytes: molecular parameters and players. Virology 1997;234:179-185.
7. 7. Wiertz E, Hill A, Tortorella D, Ploegh H. Cytomegaloviruses use multiple mechanisms to elude the host immune response. Immunol Lett 1997;57:213-216.
8. 8. Heise MT, Connick M, Virgin HW. Murine cytomegalovirus inhibits interferon γ-induced antigen presentation to CD4 T cells by macrophages via regulation of expression of major histocompatibility complex class II-associated genes. J Exp Med 1998;187:1037-1046.
9. 9. Miller DM, et al. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J Exp Med 1998;187:675-683.
10. 10. Sparer TE, Gooding LR. Suppression of MHC class I antigen presentation by human adenoviruses. Curr Top Microbiol Immunol 1998;232:135-47.
11. 11. Cresswell P. Assembly, transport and function of MHC class II molecules. Annu Rev Immunol 1994;12:259-293.
12. 12. Bakke O, Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 1990;63:707-716.
13. 13. Lotteau V, et al. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 1990;348:600-605.
14. 14. Cresswell P. Invariant chain structure and MHC class II function. Cell 1996;84:505-507.
15. 15. Nakagawa T, et al. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 1998;280:450-453.
16. 16. Pierre P, Mellman I. Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 1998;93:1135-1145.
17. 17. Riese RJ, et al. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 1996;4:357-366.
18. 18. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. Cell 1995;82:155-165.
19. 19. Roche PA. HLA-DM: an in vivo facilitator of MHC class II peptide loading. Immunity 1995;3:259-262.
20. 20. Sloan VS, et al. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 1995;375:802-806.
21. 21. Sherman MA, Weber DA, Jensen PE. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptides. Immunity 1995;3:197-205.
22. 22. Denzin LK, Hammond C, Cresswell P. HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J Exp Med 1996;184:2153-2165.
23. 23. Weber DA, Evavold BD, Jensen PE. Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 1996;274:618-620.
24. 24. Katz JF, Stebbins C, Appella E, Sant AJ. Invariant chain and DM edit self-peptide presentation by major histocompatibility complex (MHC) class II molecules. J Exp Med 1996;184:1747-1753.
25. 25. Kropshofer H, Hammerling GJ, Vogt AB. How HLA-DM edits the MHC class II peptide repertoire: survival of the fittest? Immunol Today 1997;18:77-82.
26. 26. Liljedahl M, Kuwana T, Fung-Leung W-P, Jackson MR, Peterson PA, Karlsson L. HLA-DO is a lysosomal resident which requires association with HLA-DM for efficient intracellular transport. EMBO J 1996;15:4817-4824.
27. 27. Liljedahl M, et al. Altered antigen presentation in mice lacking H2-O. Immunity 1998;8:233-243.
28. 28. Denzin LK, Sant'Angelo DB, Hammond C, Surman MJ, Cresswell P. Negative regulation by HLA-DO of MHC class II-restricted antigen processing. Science 1997;278:106-109.
29. 29. Harding CV. Protein catabolism and antigen processing. In: Schwartz AL, Ciechanover A, eds. Cellular proteolytic systems. New York: Wiley-Liss; 1994. p. 163-180.
30. 30. Jensen PE. Reduction of disulfide bonds during antigen processing: evidence from a thiol-dependent insulin determinant. J Exp Med 1991;174:1121-1130.
31. 31. Jensen PE. Antigen unfolding and disulfide reduction in antigen presenting cells. Semin Immunol 1995;7:347-353.
32. 32. Merkel BJ, Mandel R, Ryser HJ-P, McCoy KL. Characterization of fibroblasts with a unique defect in processing antigens with disulfide bonds. J Immunol 1995;154:128-136.
33. 33. Collins DS, Unanue ER, Harding CV. Reduction of disulfide bonds within lysosomes is a key step in antigen processing. J Immunol 1991;147:4054-4059.
34. 34. Hampl J, Gradehandt G, Kalbacher H, Rude E. In vitro processing of insulin for recognition by murine T cells results in the generation of A chains with free CysSH. J Immunol 1992;148:2664-2671.
35. 35. Peters PJ, Neefjes JJ, Oorschot V, Ploegh HL, Geuze HJ. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments. Nature 1991;349:669-676.
36. 36. Harding CV, Geuze HJ. Immunogenic peptides bind to class II MHC molecules in an early lysosomal compartment. J Immunol 1993;151:3988-3998.
37. 37. Qiu Y, Xu X, Wandinger-Ness A, Dalke DP, Pierce SK. Separation of subcellular compartments containing distinct functional forms of MHC class II. J Cell Biol 1994;125:595-605.
38. 38. Rudensky AY, Maric M, Eastmen S, Shoemaker L, DeRoos PC, Blum JS. Intracellular assembly and transport of endogenous peptide-MHC class II complexes. Immunity 1994;1:585-594.
39. 39. Tulp A, Verwoerd D, Dobberstein B, Ploegh HL, Pieters J. Isolation and characterization of the intracellular MHC class II compartment. Nature 1994;369:120-126.
40. 40. West MA, Lucocq JM, Watts C. Antigen processing and class II MHC peptide loading compartments in human B-lymphoblastoid cells. Nature 1994;369:147-151.
41. 41. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 1997;139:639-649.
42. 41. Glickman JN, Morton PA, Slot JW, Kornfeld S, Geuze HJ. The biogenesis of the MHC class II compartment in human I-cell disease B lymphoblasts. J Cell Biol 1996;132:769-785.
43. 43. Amigorena S, Drake JR, Webster P, Mellman I. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 1994;369:113-120.
44. 44. Amigorena S, Webster P, Drake J, Newcomb J, Cresswell P, Mellman I. Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles. J Exp Med 1995;181:1729-1741.
45. 45. Pierre P, Mellman I. Exploring the mechanisms of antigen processing by cell fractionation. Curr Opin Immunol 1998;10:145-153.
46. 46. Castellino F, Germain RN. Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity 1995;2:73-88.
47. 47. Griffìn JP, Chu R, Harding CV. Early endosomes and a late endocytic compartment generate different peptide-class II MHC complexes via distinct processing mechanisms. J Immunol 1997;158:1523-1532.
48. 48. Peters PJ, et al. Major histocompatibility complex class II compartments in human B lymphoblastoid cells are distinct from early endosomes. J Exp Med 1995;182:325-334.
49. 49. Davidson HW, Reid PA, Lanzavecchia A, Watts C. Processed antigen binds to newly synthesized MHC class II molecules in antigen-specific B lymphocytes. Cell 1991;67:105-116.
50. 50. Neefjes JJ, Stollorz V, Peters PJ, Geuze HJ, Ploegh HL. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 1990;61:171-183.
51. 51. Romagnoli P, Layet C, Yewdell J, Bakke O, Germain RN. Relationship between invariant chain expression and major histocompatability complex class II transport into early and late endocytic compartments. J Exp Med 1993;177:583-596.
52. 52. Pieters J, Horstmann H, Bakke O, Griffiths G, Lipp J. Intracellular transport and localization of major histocompatability complex class II molecules and associated invariant chain. J Cell Biol 1991;115:1213-1223.
53. 53. Bénaroch P, et al. How MHC class II molecules reach the endocytic pathway. EMBO J 1995;14:37-49.
54. 54. Harding CV, Unanue ER. Antigen processing and intracellular Ia. Possible roles of endocytosis and protein synthesis in Ia function. J Immunol 1989;142:12-19.
55. 55. Salamero J, Humbert M, Cosson P, Davoust J. Mouse B lymphocyte specifìc endocytosis and recycling of MHC class II molecules. EMBO J 1990;9:3489-3496.
56. 56. Reid PA, Watts C. Cycling of cell-surface MHC glycoproteins through primaquine-sensitive intracellular compartments. Nature 1990;346:655-657.
57. 57. Pinet V, Malnati MS, Long EO. Two processing pathways for the MHC class II-restricted presentation of exogenous influenza virus antigen. J Immunol 1994;152:4852-4860.
58. 58. Pinet V, Vergelli M, Martin R, Bakke O, Long EO. Antigen presentation mediated by recycling of surface HLA-DR molecules. Nature 1995;375:603-606.
59. 59. Demotz S, Peleraux A. Processing of DR1-restricted determinants from the fusion protein of measles virus following two distinct pathways. Molec Immunol 1996;33:387-397.
60. 60. Briken V, Lankar D, Bonnerot C. New evidence for two MHC class II-restricted antigen presentation pathways by overexpression of a small G protein. J Immunol 1997;159:4653-4658.
61. 61. Pinet VM, Long EO. Peptide loading onto recycling HLA-DR molecules occurs in early endosomes. Eur J Immunol 1998;28:799-804.
62. 62. Delvig AA, Robinson JH. Two T cell epitopes from the M5 protein of viable Streptococcus pyogenes engage different pathways of bacterial antigen processing in mouse macrophages. J Immunol 1998;160:5267-5272.
63. 63. Zhong G, Romagnoli P, Germain RN. Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control endocytic presentation of distinct determinants in a single protein. J Exp Med 1997;185:429-438.
64. 64. Chianese-Bullock KA, Russell HI, Moller C, Gerhard W, Monaco JJ, Eisenlohr LC. Antigen processing of two H2 IEd-restricted epitopes is differentially influenced by the structural changes in a viral glycoprotein. J Immunol 1998;161:1599-1607.
65. 65. Harding CV, Unanue ER. Low-temperature inhibition of antigen processing and iron uptake from transferrin: deficits in endosome functions at 18°C. Eur J Immunol 1990;20:323-329.
66. 66. Antoine JC, Jouanne C, Lang T, Prina E, de Chastellier C, Frehel C. Localization of major histocompatibility complex class II molecules in phagolysosomes of murine macrophages infected with Leishmania amazonensis. Infect Immun 1991;59:764-775.
67. 67. Lang T, Kaye P. Presentation of Leishmania donovani promastigotes occurs via a brefeldin A-sensitive pathway. Eur J Immunol 1991;21:2407-2413.
68. 68. Harding CV, Geuze HJ. Class II MHC molecules are present in macrophage lysosomes and phagolysosomes that function in the phagocytic processing of Listeria monocytogenes for presentation to T cells. J Cell Biol 1992;119:531-542.
69. 69. Clemens DL, Horwitz MA. Membrane sorting during phagocytosis: selective exclusion of major histocompatibility complex molecules but not complement receptor CR3 during conventional and coiling phagocytosis. J Exp Med 1992;175:1317-1326.
70. 70. Clemens DL, Horwitz MA. Hypoexpression of major histocompatibility complex molecules on Legionella pneumophila phagosomes and phagolysosomes. Infect Immun 1993;61:2803-2812.
71. 71. Ziegler K, Unanue ER. Identification of a macrophage antigen-processing event required for I-region-restricted antigen presentation to T lymphocytes. J Immunol 1981;127:1869-1875.
72. 72. Pfeifer J, Wick MJ, Russell D, Normark S, Harding CV. Recombinant Escherichia coli express a defined, cytoplasmic epitope that is efficiently processed in macrophage phagolysosomes for class II MHC presentation to T lymphocytes. J Immunol 1992;149:2576-2584.
73. 73. Wick MJ, Pfeifer JD, Findlay KA, Harding CV, Normark SJ. Compartmentalization of defined epitopes expressed in Escherichia coli has only a minor influence on efficiency of phagocytic processing for presentation by class I and class II major histocompatibility complex molecules to T cells. Infect Immun 1993;61:4848-4856.
74. 74. Wick MJ, Harding CV, Normark SJ, Pfeifer JD. Parameters that influence the processing efficiency of antigenic epitopes expressed in Salmonella typhimurium. Infect Immun 1994;62:4542-4548.
75. 75. Ramachandra L, Song R, Harding CV. Phagosomes are fully competent antigen processing organelles that mediate the formation of peptide: class II MHC complexes. J Immunol 1999;161:3263-3272.
76. 76. Ramachandra L, Sramkoski RM, Canaday DH, Boom WH, Harding CV. Flow analysis of MHC molecules and other membrane proteins in isolated phagosomes. J Immunol Methods 1998;213:53-71.
77. 77. Sturgill-Koszycki S, et al. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994;263:678-681.
78. 78. Clemens DL, Horwitz MA. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 1995;181:257-270.
79. 79. Bevan MJ. Cross-priming for a secondary response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J Exp Med 1976;143:1283-1288.
80. 80. Gooding LR, Edwards CB. H-2 antigen requirements in the in vitro induction of SV40-specific cytotoxic T lymphocytes. J Immunol 1980;124:1258-1262.
81. 81. Carbone FR, Bevan MJ. Class I-restricted processing and presentation of exogenous cell-associated antigen in vivo. J Exp Med 1990;171:377-387.
82. 82. Debrick JE, Campbell PA, Staerz UD. Macrophages as accessory cells for class I MHC-restricted immune responses. J Immunol 1991;147:2846-2851.
83. 83. Collins DS, Findlay K, Harding CV. Processing of exogenous liposome-encapsulated antigens in vivo generates class I MHC-restricted T cell responses. J Immunol 1992;148:3336-3341.
84. 84. Pfeifer JD, Wick MJ, Roberts RL, Findlay KF, Normark SJ, Harding CV. Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature 1993;361:359-362.
85. 85. Harding CV, Pfeifer JD. Antigen expressed by Salmonella typhimurium is processed for class I major histocompatibility complex presentation by macrophages but not infected epithelial cells. Immunology 1994;83:670-674.
86. 86. Harding CV, Song R. Phagocytic processing of exogenous particulate antigens by macrophages for presentation by class I MHC molecules. J Immunol 1994;53:4925-4933.
87. 87. Kovacsovics-Bankowski M, Clark K, Benacerraf B, Rock KL. Efficient major histocompalibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci USA 1993;90:4942-4946.
88. 88. Schirmbeck R, Bohm W, Melber K, Reimann J. Processing of exogenous heat-aggregated (denatured) and particulate (native) hepatitis B surface antigen for class I-restricted epitope presentation. J Immunol 1995;155:4676-4684.
89. 89. Schirmbeck R, Melber K, Reimann J. 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 1995;25:1063-70.
90. 90. Lui T, Zhou X, Orvell C, Lederer E, Ljunggren HG, Jondal M. Heat-inactivated Sendai virus can enter multiple MHC class I processing pathways and generate cytotoxic T lymphocyte responses in vivo. J Immunol 1995;154:3147-3155.
91. 91. Albert ML, Sauter B, Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 1998;392:86-89.
92. 5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 1998;188:1359-1368.
93. 93. Bellone M, et al. Processing of engulfed apoptotic bodies yields T cell epitopes. J Immunol 1997;159:5391-5399.
94. 2-microglobulin in the processing of bacterial or particulate antigens via an alternate class I MHC processing pathway. J Immunol 1996;156:4182-4190.
95. + T cells by by M. tuberculosis via an alternate class I MHC antigen processing pathway. J Immunol 1999;162:372-379.
96. - T cells reactive with Mycobacterium tubuerculosis-infected antigen-presenting cells. J Exp Med 1998;187:1633-1640.
97. + cytotoxic T lymphocytes. Scand J Immunol 1995;42:66-75.
98. 2-microglobulin. Proc Natl Acad Sci USA 1992;89:7767-7781.
99. 99. Ojcius DM, Abastado J-P, Casrouge A, Mottez E, Cabanie L, Kourilsky P. Dissociation of the peptide-MHC class I complex limits the binding rate of exogenous peptide. J Immunol 1993;151:6020-6026.
100. b molecules are noncooperative. J Immunol 1996;157:2256-2261.
101. 101. Day PM, Esquivel F, Lukszo J, Bennink JR, Yewdell JW. Effect of TAP on the generation and intracellular trafficking of peptide-receptive major histocompatibility complex class I molecules. Immunity 1995;2:137-147.
102. 102. Song R, Harding CV. Peptide-receptive class I MHC molecules on TAP-deficient and wild type cells and their roles in the processing of exogenous antigens. Immunology (In press).
103. 103. Motal UMA, et al. Major histocompatibility complex class I-binding peptides are recycled to the cell surface after internalization. Eur J Immunol 1993;23:3224-3229.
104. 104. Bachmann MF, et al. TAP1-independent loading of class I molecules by exogenous viral proteins. Eur J Immunol 1995;25:1739-1743.
105. 105. Kovacsovics-Bankowski M, Rock KL. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 1995;267:243-246.
106. + T cells requires secretion of hemolysin and intracellular bacterial growth. J Immunol 1990;145:3540-3546.
107. 107. Reis e Sousa C, Germain R. Major histocompatibility complex class I presentation of peptides derived from soluble exogenous antigen by a subset of cells engaged in phagocytosis. J Exp Med 1995;182:841-851.
108. 108. Clements JD, Hartzog MM, Lyon FL. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine 1988;6:269-275.
109. 109. Lycke N, Tsuji T, Holmgren J. The adjuvant effect of Vibrio cholerae and E.coli heat-labile enterotoxins is linked to their ADP ribosyltransferase activity. Eur J Immunol 1992;22:2277-2281.
110. 110. Takahashi I, et al. Mechanisms for mucosal immunogenicity and adjuvancy of Escherichia coli labile enterotoxin. J Infect Dis 1996;173:627-635.
111. 111. Tamura S-I, et al. Synergistic action of cholera toxin B subunit (and Escherichia coli heat-labile toxin B subunit) and a trace amount of cholera whole toxin as an adjuvant for nasal influenza vaccine. Vaccine 1994;12:419-426.
112. 112. Tamura S-I, et al. Acceleration of influenza virus clearance by Th1 cells in the nasal site of mice immunized intranasally with adjuvant-combined recombinant nucleoprotein. J Immunol 1996;156:3892-3900.
113. 113. Liang X, Lamm ME, Nedrud JG. Oral administration of cholera toxin-Sendai virus conjugate potentiates gut and respiratory immunity against Sendai virus. J Immunol 1988;141:1495-1501.
114. 114. Rollwagen FM, Pacheco ND, Clements JD, Pavlovskis O, Rollins DM, Walker RI. Killed Campylobacter elicits immune response and protection when administered with an oral adjuvant. Vaccine 1993;11:1316-1320.
115. 115. Czinn SJ, Cai A, Nedrud JG. Protection of germ-free mice from infection by Helicobacter felis after active oral or passive IgA immunization. Vaccine 1993;11:637-642.
116. 116. Elson CO, Ealding W. Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. J Immunol 1984;132:2736-2741.
117. 117. Lycke N, Holmgren J. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 1986;59:301-308.
118. 118. Blanchard TG, Lycke N, Czinn SJ, Nedrud JG. Recombinant cholera toxin B subunit is not an effective mucosal adjuvant for oral immunization of mice against H. felis. Immunology 1998;94:22-27.
119. 119. Di Tommaso A, et al. Induction of antigen-specific antibodies in vaginal secretions by using a nontoxic mutant of heat-labile enterotoxin as a mucosal adjuvant. Infect Immun 1996;64:974-979.
120. 120. Partidos CD, Pizza M, Rappuoli R, Steward MW. The adjuvant effect of a nontoxic mutant of heat-labile enterotoxin of Escherichia coli for the induction of measles virus-specific CTL responses after intranasal co-immunization with a synthetic peptide. Immunology 1996;89:483-487.
121. 121. Lobet Y, Cluff CW, Cieplak W Jr. Effect of site-directed mutagenic alterations on ADP-ribosyltransferase activity of the A subunit of Escherichia coli heat-labile enterotoxin. Infect Immun 1991;59:2870-2879.
122. 122. Tsuji T, Inoue T, Miyama A, Okamoto K, Honda T, Miwatani T. A single amino acid substitution in the A subunit of Escherichia coli enterotoxin results in a loss of its toxicity. J Biol Chem 1990;265:22520-22525.
123. 123. Harford S, Dykes CW, Hobdin AN, Read MJ, Halliday IJ. Inactivation of the Escherichia coli heat-labile enterotoxin by in vitro mutagenesis of the A subunit gene. Eur J Immunol 1989;183:311-316.
124. 124. Cieplak W Jr, Mead DJ, Messer RJ, Grant CCR. Site directed mutagenic alteration of potential active site residues of the A subunit of Escherichia coli heat-labile enterotoxin. J Biol Chem 1995;270:1-6.
125. 125. Dickinson BL, Clements JD. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect Immun 1995;63:1617-1623.
126. 126. Grant CCR, Messer RJ, Cieplak W Jr. Role of trypsin-like cleavage at arginine 192 in the enzymatic and cytotonic activities of Escherichia coli heat labile enterotoxin. Infect Immun 1994;62:4270-4278.
127. 127. Douce G, et al. Mutants of Escherichia coli heat-labile toxin lacking ADP-ribosyltransferase activity act as non-toxic, mucosal adjuvants. Proc Natl Acad Sci USA 1995;92:1644-1648.
128. 128. Yamamoto S, et al. Mutants in the ADP-ribosyltransferase cleft of cholera toxin lack diarrheagenicity but retain adjuvanticity. J Exp Med 1997;185:1203-1210.
129. 129. Burnette WN, et al. Site-specific mutagenesis of the catalytic subunit of cholera toxin: substituting lysine for arginine 7 causes loss of activity. Infect Immun 1991;59:4266-4270.
130. 130. Nedrud JG, Czinn SJ, Cieplak W Jr. Mutant E. coli heat labile toxin molecules with reduced ADP-ribosylation activity act as oral mucosal adjuvants and can promote protective immune responses versus Helicobacter felis. Immunol Cell Biol 1997;75 (Suppl 1):A91.
131. 131. Ghiara P, et al. Therapeutic intragastric vaccination against Helicobacter pylori in mice eradicates an otherwise chronic infection and confers protection against reinfection. Infect Immun 1997;65:4996-5002.
132. 132. Pizza M, et al. Probing the structure activity relationship of Escherichia coli LT-A by site-directed mutagenesis. Mol Microbiol 1994;14:51-60.
133. 133. Matousek MP, Nedrud JN, Cieplak W, Harding CV. Inhibition of class II MHC antigen processing and presentation by Escherichia coli heat labile enterotoxin requires an enzymatically active A subunit. Infect Immun 1998;66:3480-3484.
134. 134. Matousek MP, Nedrud JG, Harding CV. Distinct effects of recombinant cholera toxin B subunit and holotoxin on different stages of class II MHC antigen processing and presentation by macrophages. J Immunol 1996;156:4137-4145.
135. 135. Bromander A, Holmgren J, Lycke N. Cholera toxin stimulates IL-1 production and enhances antigen presentation by macrophages in vitro. J Immunol 1991;146:2908-2914.
136. 136. Bromander AK, Kjerrulf M, Holmgren J, Lycke N. Cholera toxin enhances alloantigen presentation by cultured intestinal epithelial cells. Scand J Immunol 1993;37:452-458.
137. 137. Hörnquist E, Lycke N. Cholera toxin adjuvant greatly promotes antigen priming of T cells. Eur J Immunol 1993;23:2136-2143.
138. 138. Fenton MJ, Vermeulen MW. Immunopathology of tuberculosis: roles of macrophages and monocytes. Infect Immun 1996;64:683-690.
139. 139. Gercken J, Pryjma J, Ernst M, Flad HD. Defective antigen presentation by Mycobacterium tuberculosis infected monocytes. Infect Immun 1994;62:3472-3478.
140. 140. VanHeyningen TK, Collins HL, Russell DG. IL-6 produced by macrophages infected with Mycobacterium species suppresses T cell responses. J Immunol 1997;158:330-337.
141. 141. Mazzaccaro RJ, et al. Major histocompatibility class I presentation of soluble antigen facilitated by Mycobacterium tuberculosis infection. Proc Natl Acad Sci USA 1996;93:11786-11791.
142. 142. Hmama Z, Gabathuler R, Jefferies WA, de Jong G, Reiner NE. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J Immunol 1998;161:4882-93.
143. 143. Hussain S, Zwilling BS, Lafuse WP. Mycobacterium avium infected macrophages show unresponsiveness to IFN-γ and defective JAK-STAT cell signaling pathway. FASEB J 1998;12: A297.
144. + T cells of mycobacteria growing in human macrophages. Science 1993;260:984-986.
145. 145. Holsti MA, Allen PM. Processing and presentation of an antigen of Mycobacterium avium require access to an acidified compartment with active proteases. Infect Immun 1996;64:4091-4098.
146. 146. Havlir DV, Wallis RS, Boom WH, Daniel TM, Chervenak K, Ellner JJ. Human immune responses to Mycobacterium tuberculosis antigens. Infect Immun 1991;59:665-670.
147. 147. Ladel CH, Daugelat S, Kaufmann SHE. Immune response to Mycobacterium bovis bacille Calmette Guérin infection in major histocompatibility complex class I-and II-deficient knock-out mice: contribution of CD4 and CD8 T cells to acquired resistance. Eur J Immunol 1995;25:377-384.
148. 148. Orme IM, Collins FM. Protection against Mycobacterium tuberculosis infection by adoptive transfer. J Exp Med 1983;158:74-83.
149. 149. Orme IM, Furney SK, Roberts AD. Dissemination of enteric Mycobacterium avium infections in mice rendered immunodeficient by thymectomy and CD4 depletion or by prior infection with murine AIDS retrovirus. Infect Immun 1992;60:4747-4753.
150. + αβ T cell and γδ T cell responses to Mycobacterium tuberculosis: similarities and differences in anitgen recogition, cytotoxic effector function, and cytokine production. J Immunol 1995;154:1786-1796.
151. + T cells in vitro. Immunology 1996;87:339-342.
152. 152. Krieg AM, et al. CpG motifs in bacterial DNA trigger direct B cell activation. Nature 1995;374:546-549.
153. 153. Sun S, Beard C, Jaenisch R, Jones P, Sprent J. Mitogenicity of DNA from different organisms for murine B cells. J Immunol 1997;159:3119-3125.
154. 154. Stacey KJ, Sweet MJ, Hume DA. Macrophages ingest and are activated by bacterial DNA. J Immunol 1996;157:2116-2122.
155. 155. Sparwasser T, et al. Macrophage sense pathogens via DNA motifs: induction of tumor-necrosis factor-α-mediated shock. Eur J Immunol 1997;27(1671-1679).
156. 156. Jakob T, Walker PS, Krieg AM, Udey MC, Vogel JC. Activation of cutaneous dendritic cells by CpG-containing oligodeoxynucleotides: a role for dendritic cells in the augmentation of Th1 responses by immunostimulatory DNA. J Immunol 1998;161:3042-3049.
157. 157. Sparwasser T, et al. Bacterial DNA and immunostimulatory CpG oligonucleotides trigger maturation and activation of murine dendritic cells. Eur J Immunol 1998;28:2045-2054.
158. 158. Yamamoto S, et al. DNA from bacteria, but not from vertebrates, induces interferons, activates natural killer cells and inhibits tumor growth. Microbiol Immunol 1992;36:983-997.
159. 159. Ballas ZK, Rasmussen WL, Krieg AM. Induction of NK activity in murine and human cells by CpG motifs in oligodeoxynucleotides and bacterial DNA. J Immunol 1996;157:1840-1845.
160. 160. Sato Y, et al. Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 1996;273:352-354.
161. 161. Klinman DM, Yi A-K, Beaucage SL, Conover J, Krieg AM. CpG motifs present in bacterial DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon γ. Proc Natl Acad Sci USA 1996;93:2879-2883.
162. 162. Cowdery JS, Chace JH, Yi A-K, Krieg AM. Bacterial DNA induces NK cells to produce IFN-γ in vivo and increases the toxicity of lipopolysaccharides. J Immunol 1996;156:4570-4575.
163. 163. Halpern MD, Kurlander RJ, Pisetsky DS. Bacterial DNA induces murine interferon-γ production by stimulation of interleukin-12 and tumor necrosis factor-α. Cell Immunol 1996;167:72-78.
164. 164. Chace JH, Hooker NA, Mildenstein KL, Krieg AM, Cowdery JS. Bacterial DNA-induced NK cell IFN-γ production is dependent on macrophage secretion of IL-12. Clin Immunol Immunopathol 1997;84:185-193.
165. H2 immunity in neonatal mice. Science 1996;271:1728-1730.
166. 166. Chu R, Targoni OS, Krieg AM, Lehmann PV, Harding CV. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J Exp Med 1997;186:1623-1631.
167. 167. Roman M, et al. Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat Med 1997;3:849-854.
168. 168. Sun S, Kishimoto H, Sprent J. DNA as an adjuvant: capacity of insect DNA and synthetic oligodeoxynucleotides to augment T cell responses to specific antigen. J Exp Med 1998;187:1145-1150.
169. 169. Lipford GB, Bauer M, Blank C, Reiter R, Wagner H, Heeg K. CpG-containing synthetic oligonucleotides promote B and cytotoxic T cell responses to protein antigen: a new class of vaccine adjuvants. Eur J Immunol 1997;27:2340-2344.
170. 170. Davis HL, Weeranta R, Waldschmidt TJ, Tygrett L, Schorr J, Krieg AM. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J Immunol 1998;160:870-6.
171. 171. Moldoveanu Z, Love-Homan L, Huang WQ, Krieg AM. CpG DNA, a novel immune enhancer for systemic and mucosal immunization with influenza virus. Vaccine 1998;16:1216-1224.
172. 172. Kline JN, et al. Modulation of airway inflammation by CpG oligodeoxynucleotides in a murine model of asthma. J Immunol 1998;160:2555-2559.
173. 173. Zimmermann S, et al. CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J Immunol 1998;160:3627-3630.
174. 174. Steeg PS, Johnson HM, Oppenheim JJ. Regulation of murine macrophage Ia antigen expression by an immune interferon-like lymphokine: inhibitory effect of endotoxin. J Immunol 1982;129:2402-2406.
175. 175. Koerner TJ, Hamilton TA, Adams DO. Suppressed expression of surface Ia on macrophages by lipopolysaccaride: evidence for regulation at the level of accumulation of mRNA. J Immunol 1987;139:239-243.
176. 176. Askew D, Burger CJ, Elgert KD. Tumor-induced modulation of macrophage class II MHC molecule mRNA expression. Mol Immunol 1993;30:911-920.
177. 177. Sicher SC, Vazquez MA, Lu CY. Inhibition of macrophage Ia expression by nitric oxide. J Immunol 1994;153:1293-1300.
178. 178. Cella M, Engering A, Pinet V, Pieters J, Lanzavecchia A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 1997;388:782-787.
179. 179. Cella M, Sallusto F, Lanzavecchia A. Origin, maturation and antigen presenting function of dendritic cells. Curr Opin Immunol 1997;9:10-16.
180. 180. Pierre P, et al. Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 1997;388:787-792.
181. 181. Bancherean J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392(6673):245-252.
182. 182. Sallusto F, Cella M, Danieli C, Lanzavecchia A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 1995;182:389-400.
183. 183. Winzler C, et al. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med 1997;185:317-328.
184. 184. Henderson RA, Watkins SC, Flynn JL. Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J Immunol 1997;159:635-643.
185. 185. Rescigno M, et al. Bacteria-induced neobiosynthesis, stabilization, and surface expression of functional class I molecules in mouse dendritic cells. Proc Natl Acad Sci USA 1998;95:5229-5234.
186. 186. Castellino F, Zappacosta F, Coligan JE, Germain RN. Large protein fragments as substrates for endocytic antigen capture by MHC class II molecules. J Immunol 1998;161:4048-4057.
187. 187. Lindner R, Unanue ER. Distinct antigen MHC class II complexes generated by separate processing pathways. EMBO J 1996;15:6910-6920.
188. 188. Harding CV. Phagocytic processing of antigens for presentation by MHC molecules. Trends Cell Biol 1995;5:105-109.