Right place, right time, right peptide: DO keeps DM focused

Immunological Reviews

Volumn 207, Issue , 2005, Pages 279-292

  Denzin, Lisa K ^a,b   Fallas, Jennifer L ^a,b   Prendes, Maria ^a   Yi, Woelsung ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DM ANTIGEN; HLA DO ANTIGEN;

B LYMPHOCYTE DIFFERENTIATION; CELLULAR DISTRIBUTION; DOWN REGULATION; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW;

ANIMALS; ANTIGEN PRESENTATION; B-LYMPHOCYTES; CELL DIFFERENTIATION; HLA-D ANTIGENS; HUMANS; LYMPHOCYTE ACTIVATION; PEPTIDES;

EID: 26244441527     PISSN: 01052896     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0105-2896.2005.00302.x     Document Type: Review

References (120)

1. Boes M, Cuvillier A, Ploegh H. Membrane specializations and endosome maturation in dendritic cells and B cells. Trends Cell Biol 2004;14:175-183.
2. Hiltbold EM, Roche PA. Trafficking of MHC class II molecules in the late secretory pathway. Curr Opin Immunol 2002;14:30-35.
3. Pieters J. MHC class II-restricted antigen processing and presentation. Adv Immunol 2000;75:159-208.
4. Watts C. The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat Immunol 2004;5:685-692.
5. Jones PP, Murphy DB, Hewgill D, McDevitt HO. Detection of a common polypeptide chain in I - A and I - E sub-region immunoprecipitates. Mol Immunol 1979;16:51-60.
6. Machamer CE, Cresswell P. Biosynthesis and glycosylation of the invariant chain associated with HLA-DR antigens. J Immunol 1982;129:2564-2569.
7. Bakke O, Dobberstein B. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 1990;63:707-716.
8. 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.
9. 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.
10. 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.
11. 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.
12. Blum JS, Cresswell P. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc Natl Acad Sci USA 1988;85:3975-3979.
13. Maric MA, Taylor MD, Blum JS. Endosomal aspartic proteinases are required for invariant-chain processing. Proc Natl Acad Sci USA 1994;91:2171-2175.
14. 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.
15. Neefjes JJ, Ploegh HL. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistance alpha beta heterodimers in endosomes. EMBO J 1992;11:411-416.
16. Riberdy JM, Newcomb JR, Surman MJ, Barbosa JA, Cresswell P. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 1992;360:474-477.
17. Sette A, et al. Invariant chain peptides in most HLA-DR molecules of an antigen-processing mutant. Science 1992;258:1801-1804.
18. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 1995;82:155-165.
19. Sherman MA, Weber DA, Jensen PE. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity 1995;3:197-205.
20. Sloan VS, et al. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 1995;375:802-806.
21. Ceman S, Rudersdorf R, Long EO, Demars R. MHC class II deletion mutant expresses normal levels of transgene encoded class II molecules that have abnormal conformation and impaired antigen presentation ability. J Immunol 1992;149:754-761.
22. Mellins E, Smith L, Arp B, Cotner T, Celis E, Pious D. Defective processing and presentation of exogenous antigens in mutants with normal HLA class II genes. Nature 1990;343:71-74.
23. Riberdy JM, Cresswell P. The antigen-processing mutant T2 suggests a role for MHC-linked genes in class II antigen presentation. J Immunol 1992;148:2586-2590.
24. Avva RR, Cresswell P. In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity 1994;1:763-774.
25. Riberdy JM, Avva RR, Geuze HJ, Cresswell P. Transport and intracellular distribution of MHC class II molecules and associated invariant chain in normal and antigen-processing mutant cell lines. J Cell Biol 1994;125:1225-1237.
26. Chicz RM, Urban RG, Gorga JC, Vignali DA, Lane WS, Strominger JL. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J Exp Med 1993;178:27-47.
27. Chicz RM, et al. Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature 1992;358:764-768.
28. Fling SP, Arp B, Pious D. HLA-DMA and -DMB genes are both required for MHC class II/peptide complex formation in antigen-presenting cells. Nature 1994;368:554-558.
29. Morris P, et al. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 1994;368:551-554.
30. Fung-Leung WP, et al. Antigen presentation and T cell development in H2-M-deficient mice. Science 1996;271:1278-1281.
31. Martin WD, Hicks GG, Mendiratta SK, Leva HI, Ruley HE, Van Kaer L. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection. Cell 1996;84:543-550.
32. Miyazaki T, et al. Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway. Cell 1996;84:531-541.
33. Kelly AP, Monaco JJ, Cho SG, Trowsdale J. A new human HLA class II-related locus, DM. Nature 1991;353:571-573.
34. Cho SG, Attaya M, Monaco JJ. New class II-like genes in the murine MHC. Nature 1991;353:573-576.
35. Carrington M, Harding A. Sequence analysis of two novel HLA-DMA alleles. Immunogenetics 1994;40:165.
36. Carrington M, Yeager M, Mann D. Characterization of HLA DMB polymorphism. Immunogenetics 1993;38:446-449.
37. Sanderson F, Powis SH, Kelly AP, Trowsdale J. Limited polymorphism in HLA-DM does not involve the peptide binding groove. Immunogenetics 1994;39:56-58.
38. Denzin LK, Robbins NF, Carboy-Newcomb C, Cresswell P. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1994;1:595-606.
39. Sanderson F, et al. Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science 1994;266:1566-1569.
40. Karlsson L, Peleraux A, Lindstedt R, Liljedahl M, Peterson PA. Reconstitution of an operational MHC class II compartment in nonantigen-presenting cells. Science 1994;266:1569-1573.
41. Lindstedt R, Liljedahl M, Peleraux A, Peterson PA, Karlsson L. The MHC class II molecule H2-M is targeted to an endosomal compartment by a tyrosine-based targeting motif. Immunity 1995;3:561-572.
42. Mosyak L, Zaller DM, Wiley DC. The structure of HLA-DM, the peptide exchange catalyst that loads antigen onto class II MHC molecules during antigen presentation. Immunity 1998;9:377-383.
43. Fremont DH, Crawford F, Marrack P, Hendrickson WA, Kappler J. Crystal structure of mouse H2-M. Immunity 1998;9:385-393.
44. Ceman S, Rudersdorf RA, Petersen JM, DeMars R. DMA and DMB are the only genes in the class II region of the human MHC needed for class II-associated antigen processing. J Immunol 1995;154:2545-2556.
45. 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.
46. 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.
47. Pashine A, et al. Interaction of HLA-DR with an acidic face of HLA-DM disrupts sequence-dependent interactions with peptides. Immunity 2003;19:183-192.
48. Zarutskie JA, Busch R, Zavala-Ruiz Z, Rushe M, Mellins ED, Stern LJ. The kinetic basis of peptide exchange catalysis by HLA-DM. Proc Natl Acad Sci USA 2001;98:12450-12455.
49. Stern JF. Obesity: a crisis in Maryland. Md Med 2004;5:22-25.
50. Anderson MW, Gorski J. Cutting edge: TCR contacts as anchors: effects on affinity and HLA-DM stability. J Immunol 2003;171:5683-5687.
51. Weber DA, Evavold BD, Jensen PE. Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 1996;274:618-620.
52. Chou CL, Sadegh-Nasseri S. HLA-DM recognizes the flexible conformation of major histocompatibility complex class II. J Exp Med 2000;192:1697-1706.
53. Siklodi B, et al. Binding affinity independent contribution of peptide length to the stability of peptide-HLA-DR complexes in live antigen presenting cells. Hum Immunol 1998;59:463-471.
54. Raddrizzani L, et al. Identification of destabilizing residues in HLA class II-selected bacteriophage display libraries edited by HLA-DM. Eur J Immunol 1999;29:660-668.
55. Servenius B, Rask L, Peterson PA. Class II genes of the human major histocompatibility complex. The DO beta gene is a divergent member of the class II beta gene family. J Biol Chem 1987;262:8759-8766.
56. Tonnelle C, DeMars R, Long EO. Do beta: a new beta chain gene in HLA-D with a distinct regulation of expression. EMBO J 1985;4:2839-2847.
57. Trowsdale J, Kelly A. The human HLA class II alpha chain gene DZ alpha is distinct from genes in the DP, DQ and DR subregions. EMBO J 1985;4:2231-2237.
58. Inoko H, Ando A, Kimura M, Tsuji K. Isolation and characterization of the cDNA clone and genomic clones of a new HLA class II antigen heavy chain, DO alpha. J Immunol 1985;135:2156-2159.
59. Jonsson AK, Rask L. Human class II DNA and DOB genes display low sequence variability. Immunogenetics 1989;29:411-413.
60. van Lith M, van Ham M, Neefjes J. Novel polymorphisms in HLA-DOA and HLA-DOB in B-cell malignancies. Immunogenetics 2002;54:591-595.
61. Naruse TK, et al. Limited polymorphism in the HLA-DOA gene. Tissue Antigens 1999;53:359-365.
62. Naruse TK, et al. The HLA-DOB gene displays limited polymorphism with only one amino acid substitution. Tissue Antigens 2002;59:512-519.
63. Karlsson L, Peterson PA. The alpha chain gene of H-2O has an unexpected location in the major histocompatibility complex. J Exp Med 1992;176:477-483.
64. Karlsson L, Surh CD, Sprent J, Peterson PA. A novel class II MHC molecule with unusual tissue distribution. Nature 1991;351:485-488.
65. Karlsson L, Surh CD, Sprent J, Peterson PA. An unusual class II molecule. Immunol Today 1992;13:469-470.
66. Surh CD, et al. Two subsets of epithelial cells in the thymic medulla. J Exp Med 1992;176:495-505.
67. Liljedahl M, Kuwana T, Fung-Leung WP, 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.
68. Douek DC, Altmann DM. HLA-DO is an intracellular class II molecule with distinctive thymic expression. Int Immunol 1997;9:355-364.
69. Roucard C, et al. In vivo and in vitro modulation of HLA-DM and HLA-DO is induced by B lymphocyte activation. J Immunol 2001;167:6849-6858.
70. Liljedahl M, et al. Altered antigen presentation in mice lacking H2-O. Immunity 1998;8:233-243.
71. 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.
72. van Ham SM, et al. HLA-DO is a negative modulator of HLA-DM-mediated MHC class II peptide loading. Curr Biol 1997;7:950-957.
73. Kropshofer H, Vogt AB, Moldenhauer G, Hammer J, Blum JS, Hammerling GJ. Editing of the HLA-DR-peptide repertoire by HLA-DM. EMBO J 1996;15:6144-6154.
74. Chen X, et al. Regulated expression of human histocompatibility leukocyte antigen (HLA)-DO during antigen-dependent and antigen-independent phases of B cell development. J Exp Med 2002;195:1053-1062.
75. Deshaies F, Brunet A, Diallo D, Denzin LK, Samaan A, Thibodeau J. A point mutation in me groove of HLA-Do allows egress from the endoplasmic reticulm independently of HLA-DM. Proc Natl Acad Sci USA 2005;102:6443-6448.
76. Pallas JL, Tobin HM, Lou O, Guo D, Sant'Angelo DB, Denzin LK. Ectopic Expression of HLA-DO in mouse dendritic cells diminishes MHC class II antigen presentation. J Immunol 2004;173:1549-1560.
77. Kropshofer H, et al. A role for HLA-DO as a co-chaperone of HLA-DM in peptide loading of MHC class II molecules. EMBO J 1998;17:2971-2981.
78. van Lith M, et al. Regulation of MHC class II antigen presentation by sorting of recycling HLA-DM/DO and class II within the multivesicular body. J Immunol 2001;167:884-892.
79. Potter PK, et al. Accurate intracellular localization of HLA-DM requires correct spacing of a cytoplasmic YTPL targeting motif relative to the transmembrane domain. Eur J Immunol 1999;29:3936-3944.
80. Marks MS, Roche PA, van Donselaar E, Woodruff L, Peters PJ, Bonifacino JS. A lysosomal targeting signal in the cytoplasmic tail of the beta chain directs HLA-DM to MHC class II compartments. J Cell Biol 1995;131:351-369.
81. Brunet A, Samaan A, Deshaies F, Kindt TJ, Thibodeau J. Functional characterization of a lysosomal sorting motif in the cytoplasmic tail of HLA-DObeta. J Biol Chem 2000;275:37062-37071.
82. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 1998;273:20121-20127.
83. Kleijmeer M, et al. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J Cell Biol 2001;155:53-63.
84. Murk JL, Stoorvogel W, Kleijmeer MJ, Geuze HJ. The plasticity of multivesicular bodies and the regulation of antigen presentation. Semin Cell Dev Biol 2002;13:303-311.
85. Wake CT, Flavell RA. Multiple mechanisms regulate the expression of murine immune response genes. Cell 1985;42:623-628.
86. Bellemare-Pelletier A, et al. HLA-DO transduced in human monocyte-derived dendritic cells modulates MHC class II antigen processing. J Leukoc Biol 2005.
87. Kropshofer H, Hammerling GJ, Vogt AB. The impact of the non-classical MHC proteins HLA-DM and HLA-DO on loading of MHC class II molecules. Immunol Rev 1999;172:267-278.
88. Steinman RM, Inaba K. Myeloid dendritic cells. J Leukoc Biol 1999;66:205-208.
89. Steimle V, Otten LA, Zufferey M, Mach B. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 1993;75:135-146.
90. Steimle V, Siegrist CA, Mottet A, Lisowska-Grospierre B, Mach B. Regulation of MHC class II expression by interferon-gamma mediated by the transactivator gene CIITA. Science 1994;265:106-109.
91. Beresford GW, Boss JM. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nat Immunol 2001;2:652-657.
92. Masternak K, Muhlethaler-Mottet A, Villard J, Zufferey M, Steimle V, Reith W. CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev 2000;14:1156-1166.
93. Taxman DJ, Cressman DE, Ting JP. Identification of class II transcriptional activator-induced genes by representational difference analysis: discoordinate regulation of the DN alpha/DO beta heterodimer. J Immunol 2000;165:1410-1416.
94. Nagarajan UM, et al. Class II transactivator is required for maximal expression of HLA-DOB in B cells. J Immunol 2002;168:1780-1786.
95. Khalil H, et al. Class II transactivator-induced expression of HLA-DO (beta) in HeLa cells. Tissue Antigens 2002;60:372-382.
96. Hake SB, Tobin HM, Steimle V, Denzin LK. Comparison of the transcriptional regulation of classical and non-classical MHC class II genes. Eur J Immunol 2003;33:2361-2371.
97. Ponzoni M, Guarnaccia F, Corrias MV, Cornaglia-Ferraris P. Uncoordinate induction and differential regulation of HLA class-I and class-II expression by gamma-interferon in differentiating human neuroblastoma cells. Int J Cancer 1993;55:817-823.
98. Chang CH, Guerder S, Hong SC, van Ewijk W, Flavell RA. Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity 1996;4:167-178.
99. Chen Z, Koralov SB, Gendelman M, Carroll MC, Kelsoe G. Humoral immune responses in Cr2-/- mice: enhanced affinity maturation but impaired antibody persistence. J Immunol 2000;164:4522-4532.
100. Lam KP, Stall AM. Major histocompatibility complex class II expression distinguishes two distinct B cell developmental pathways during ontogeny. J Exp Med 1994;180:507-516.
101. Hardy RR, Li YS, Allman D, Asano M, Gui M, Hayakawa K. B-cell commitment, development and selection. Immunol Rev 2000;175:23-32.
102. Chalouni C, Banchereau J, Vogt AB, Pascual V, Davoust J. Human germinal center B cells differ from naive and memory B cells by their aggregated MHC class II-rich compartments lacking HLA-DO. Int Immunol 2003;15:457-466.
103. Glazier KS, Hake SB, Tobin HM, Chadburn A, Schattner EJ, Denzin LK. Germinal center B cells regulate their capability to present antigen by modulation of HLA-DO. J Exp Med 2002;195:1063-1069.
104. Lapointe R, Bellemare-Pelletier A, Housseau F, Thibodeau J, Hwu P. CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specific T cells. Cancer Res 2003;63:2836-2843.
105. van Ham M, et al. Modulation of the major histocompatibility complex class II-associated peptide repertoire by human histocompatibility leukocyte antigen (HLA)-DO. J Exp Med 2000;191:1127-1136.
106. Perraudeau M, et al. Altered major histocompatibility complex class II peptide loading in H2-O-deficient mice. Eur J Immunol 2000;30:2871-2880.
107. Brocke P, Armandola E, Garbi N, Hammerling GJ. Downmodulation of antigen presentation by H2-O in B cell lines and primary B lymphocytes. Eur J Immunol 2003;33:411-421.
108. Qi L, Ostrand-Rosenberg S. H2-O inhibits presentation of bacterial superantigens, but not endogenous self antigens. J Immunol 2001;167:1371-1378.
109. Alfonso C, Williams GS, Han JO, Westberg JA, Winqvist O, Karlsson L. Analysis of H2-O influence on antigen presentation by B cells. J Immunol 2003;171:2331-2337.
110. Alfonso C, Williams GS, Karlsson L. H2-O influence on antigen presentation in H2-E-expressing mice. Eur J Immunol 2003;33:2014-2021.
111. Murphy DB, et al. Monoclonal antibody detection of a major self peptide. MHC class II complex. J Immunol 1992;148:3483-3491.
112. Zhong G, Reis e Sousa C, Germain RN. Production, specificity, and functionality of monoclonal antibodies to specific peptide-major histocompatibility complex class II complexes formed by processing of exogenous protein. Proc Natl Acad Sci USA 1997;94:13856-13861.
113. Watts C. Capture and processing of exogenous antigens for presentation on MHC molecules. Annu Rev Immunol 1997;15:821-850.
114. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-252.
115. Metlay JP, Pure E, Steinman RM. Distinct features of dendritic cells and anti-Ig activated B cells as stimulators of the primary mixed leukocyte reaction. J Exp Med 1989;169:239-254.
116. Guery JC, Ria F, Adorini L. Dendritic cells but not B cells present antigenic complexes to class II-restricted T cells after administration of protein in adjuvant. J Exp Med 1996;183:751-757.
117. Sprent J. Features of cells controlling H-2-restricted presentation of antigen to T helper cells in vivo. J Immunol 1980;125:2089-2096.
118. MacLennan IC. Germinal centers. Annu Rev Immunol 1994;12:117-139.
119. Han S, Zheng B, Takahashi Y, Kelsoe G. Distinctive characteristics of germinal center B cells. Semin Immunol 1997;9:255-260.
120. Gray D, et al. B-T lymphocyte interactions in the generation and survival of memory cells. Immunol Rev 1996;150:45-61.