Molecular Mechanisms of IFN-γ to Up-Regulate MHC Class I Antigen Processing and Presentation

REFERENCES

• Boehm U., Klamp T., Groot M., Howard J. C. Cellular responses to interferon-gamma. Annu Rev Immunol 1997; 15: 749–795
   PubMed Web of Science ®Google Scholar
• Rosa F. M., Fellous M. Regulation of HLA-DR gene by IFN-gamma. Transcriptional and post-transcriptional control. J Immunol 1988; 140: 1660–1664
   PubMed Web of Science ®Google Scholar
• Foxwell B. M., Barrett K., Feldmann M. Cytokine receptors: Structure and signal transduction. Clin Exp Immunol 1992; 90: 161–169
   PubMed Web of Science ®Google Scholar
• Szente B. E., Soos J. M., Johnson H. W. The C-terminus of IFN gamma is sufficient for intracellular function. Biochem Biophys Res Commun 1994; 203: 1645–1654
   Google Scholar
• Briscoe J., Guschin D., Rogers N. C., Watling D., Muller M., Horn F., Heinrich P., Stark G. R., Kerr I. M. JAKs, STATs and signal transduction in response to the interferons and other cytokines. Philos Trans R Soc Lond B Biol Sci 1996; 351: 167–171
   Google Scholar
• Kohlhuber F., Rogers N. C., Watling D., Feng J., Guschin D., Briscoe J., Witthuhn B. A., Kotenko S. V., Pestka S., Stark G. R., Ihle J. N., Kerr I. M. A JAK1/JAK2 chimera can sustain alpha and gamma interferon responses. Mol Cell Biol 1997; 17: 695–706
   PubMed Web of Science ®Google Scholar
• Wu A. J., Chen Z. J., Kan E. C., Baum B. J. Interferon-gamma-induced JAK2 and STAT1 signalling in a human salivary gland cell line. J Cell Physiol 1997; 173: 110–114
   Google Scholar
• Svane I. M., Engel A. M., Nielsen M., Werdelin O. Interferon-gamma-induced MHC class I expression and defects in Jak/Stat signalling in methylcholanthrene-induced sarcomas. Scand J Immunol 1997; 46: 379–387
   Google Scholar
• Kerr I. M., Costa-Pereira A. P., Lillemeier B. F., Strobl B. Of JAKs, STATs, blind watchmakers, jeeps and trains. FEBS Lett 2003; 546: 1–5
   PubMedGoogle Scholar
• Miller D. M., Rahill B. M., Boss J. M., Lairmore M. D., Durbin J. E., Waldman J. W., Sedmak D. D. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J Exp Med 1998; 187: 675–683
   PubMed Web of Science ®Google Scholar
• Jouanguy E., Altare F., Lamhamedi-Cherradi S., Casanova J. L. Infections in IFNGR-1-deficient children. J Interferon Cytokine Res 1997; 17: 583–587
   Google Scholar
• Li S., Labrecque S., Gauzzi M. C., Cuddihy A. R., Wong A. H., Pellegrini S., Matlashewski G. J., Koromilas A. E. The human papilloma virus (HPV)-18 E6 oncoprotein physically associates with Tyk2 and impairs Jak-STAT activation by interferon-alpha. Oncogene 1999; 18: 5727–5737
   PubMed Web of Science ®Google Scholar
• Skrenta H., Yang Y., Pestka S., Fathman C. G. Ligand-independent down-regulation of IFN-gamma receptor 1 following TCR engagement. J Immunol 2000; 164: 3506–3511
   Google Scholar
• Jouanguy E., Dupuis S., Pallier A., Doffinger R., Fondaneche M. C., Fieschi C., Lamhamedi S., Cherradi Altare F., Emile J. F., Lutz P., Bordigoni P., Cokugras H., Akcakaya N., Landman-Parker J., Donnadieu J., Camcioglu Y., Casanova J. L. In a novel form of IFN-gamma receptor 1 deficiency, cell surface receptors fail to bind IFN-gamma. J Clin Invest 2000; 105: 1429–1436
   PubMed Web of Science ®Google Scholar
• Wei Y. P., Kita M., Shinmura K., Yan X. Q., Fukuyama R., Fushiki S., Imanishi J. Expression of IFN-gamma in cerebrovascular endothelial cells from aged mice. J Interferon Cytokine Res 2000; 20: 403–409
   PubMed Web of Science ®Google Scholar
• Takei Y., Sims T. N., Urmson J., Halloran P. F. Central role for interferon-gamma receptor in the regulation of renal MHC expression. J Am Soc Nephrol 2000; 11: 250–261
   Google Scholar
• Delgado M., Ganea D. Inhibition of IFN-gamma-induced janus kinase-1-STAT1 activation in macrophages by vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. J Immunol 2000; 165: 3051–3057
   PubMed Web of Science ®Google Scholar
• Allende L. M., Lopez-Goyanes A., Paz-Artal E., Corell A., Garcia-Perez M. A., Varela P., Scarpellini A., Negreira S., Palenque E., Arnaiz-Villena A. A point mutation in a domain of gamma interferon receptor 1 provokes severe immunodeficiency. Clin Diagn Lab Immunol 2001; 8: 133–137
   PubMedGoogle Scholar
• Koch O., Awomoyi A., Usen S., Jallow M., Richardson A., Hull J., Pinder M., Newport M., Kwiatkowski D. IFNGR1 gene promoter polymorphisms and susceptibility to cerebral malaria. J Infect Dis 2002; 185: 1684–1687
   PubMed Web of Science ®Google Scholar
• Fraser D. A., Loos B. G., Boman U., van Winkelhoff A. J., van der Velden U., Schenck K., Dembic Z. Polymorphisms in an interferon-gamma receptor-1 gene marker and susceptibility to periodontitis. Acta Odontol Scand 2003; 61: 297–302
   Web of Science ®Google Scholar
• Tiroch K., von Beckerath N., Koch W., Lengdobler J., Joost A., Schomig A., Kastrati A. Interferon-gamma and interferon-gamma receptor 1 and 2 gene polymorphisms and restenosis following coronary stenting. Atherosclerosis 2005; 182: 145–151
   PubMedGoogle Scholar
• Hindinger C., Gonzalez J. M., Bergmann C. C., Fuss B., Hinton D. R., Atkinson R. D., Macklin W. B., Stohlman S. A. Astrocyte expression of a dominant-negative interferon-gamma receptor. J Neurosci Res 2005; 82: 20–31
   Google Scholar
• Fruh K., Yang Y. Antigen presentation by MHC class I and its regulation by interferon gamma. Curr Opin Immunol 1999; 11: 76–81
   PubMed Web of Science ®Google Scholar
• Rouyez M. C., Lestingi M., Charon M., Fichelson S., Buzyn A., Dusanter-Fourt I. IFN regulatory factor-2 cooperates with STAT1 to regulate transporter associated with antigen processing-1 promoter activity. J Immunol 2005; 174: 3948–3958
   Google Scholar
• Mahboubi K., Pober J. S. Activation of signal transducer and activator of transcription 1 (STAT1) is not sufficient for the induction of STAT1-dependent genes in endothelial cells. Comparison of interferon-gamma and oncostatin M. J Biol Chem 2002; 277: 8012–8021
   Google Scholar
• Marques L., Brucet M., Lloberas J., Celada A. STAT1 regulates lipopolysaccharide- and TNF-alpha-dependent expression of transporter associated with antigen processing 1 and low molecular mass polypeptide 2 genes in macrophages by distinct mechanisms. J Immunol 2004; 173: 1103–1110
   Google Scholar
• Mori K., Stone S., Khaodhiar L., Braverman L. E., DeVito W. J. Induction of transcription factor interferon regulatory factor-1 by interferon-gamma (IFN gamma) and tumor necrosis factor-alpha (TNF alpha) in FRTL-5 cells. J Cell Biochem 1999; 74: 211–219
   Google Scholar
• Rein T., Muller M., Zorbas H. In vivo footprinting of the IRF-1 promoter: Inducible occupation of a GAS element next to a persistent structural alteration of the DNA. Nucleic Acids Res 1994; 22: 3033–3037
   PubMedGoogle Scholar
• Saura M., Zaragoza C., Bao C., McMillan A., Lowenstein C. J. Interaction of interferon regulatory factor-1 and nuclear factor kappaB during activation of inducible nitric oxide synthase transcription. J Mol Biol 1999; 289: 459–471
   PubMedGoogle Scholar
• Storm van's Gravesande K., Layne M. D., Ye Q., Le L., Baron R. M., Perrella M. A., Santambrogio L., Silverman E. S., Riese R. J. IFN regulatory factor-1 regulates IFN-gamma-dependent cathepsin S expression. J Immunol 2002; 168: 4488–4494
   PubMed Web of Science ®Google Scholar
• Giroux M., Schmidt M., Descoteaux A. IFN-gamma-induced MHC class II expression: Transactivation of class II transactivator promoter IV by IFN regulatory factor-1 is regulated by protein kinase C-alpha. J Immunol 2003; 171: 4187–4194
   PubMedGoogle Scholar
• Guo Y., Yang T., Liu X., Lu S., Wen J., Durbin J. E., Liu Y., Zheng P. Cis elements for transporter associated with antigen-processing-2 transcription: Two new promoters and an essential role of the IFN response factor binding element in IFN-gamma-mediated activation of the transcription initiator. Int Immunol 2002; 14: 189–200
   Google Scholar
• Lee A. H., Hong J. H., Seo Y. S. Tumour necrosis factor-alpha and interferon-gamma synergistically activate the RANTES promoter through nuclear factor kappaB and interferon regulatory factor 1 (IRF-1) transcription factors. Biochem J 2000; 350: 131–138
   PubMedGoogle Scholar
• Liu Q. P., Fruit K., Ward J., Correll P. H. Negative regulation of macrophage activation in response to IFN-gamma and lipopolysaccharide by the STK/RON receptor tyrosine kinase. J Immunol 1999; 163: 6606–6613
   Google Scholar
• Ossendorp F., Fu N., Camps M., Granucci F., Gobin S. J., van den Elsen P. J., Schuurhuis D., Adema G. J., Lipford G. B., Chiba T., Sijts A., Kloetzel P. M., Ricciardi-Castagnoli P., Melief C. J. Differential expression regulation of the alpha and beta subunits of the PA28 proteasome activator in mature dendritic cells. J Immunol 2005; 174: 7815–1722
   PubMed Web of Science ®Google Scholar
• Drew P. D., Franzoso G., Becker K. G., Bours V., Carlson L. M., Siebenlist U., Ozato K. NF kappa B and interferon regulatory factor 1 physically interact and synergistically induce major histocompatibility class I gene expression. J Interferon Cytokine Res 1995; 15: 1037–1045
   PubMed Web of Science ®Google Scholar
• Lehtonen A., Matikainen S., Julkunen I. Interferons up-regulate STAT1, STAT2, and IRF family transcription factor gene expression in human peripheral blood mononuclear cells and macrophages. J Immunol 1997; 159: 794–803
   PubMed Web of Science ®Google Scholar
• Morris K. R., Lutz R. D., Choi H. S., Kamitani T., Chmura K., Chan E. D. Role of the NF-kappaB signaling pathway and kappaB cis-regulatory elements on the IRF-1 and iNOS promoter regions in mycobacterial lipoarabinomannan induction of nitric oxide. Infect Immun 2003; 71: 1442–1452
   Google Scholar
• Paludan S. R., Ellermann-Eriksen S., Mogensen S. C. NF-kappaB activation is responsible for the synergistic effect of herpes simplex virus type 2 infection on interferon-gamma-induced nitric oxide production in macrophages. J Gen Virol 1998; 79: 2785–2793
   PubMed Web of Science ®Google Scholar
• Paludan S. R., Malmgaard L., Ellermann-Eriksen S., Bosca L., Mogensen S. C. Interferon (IFN)-gamma and Herpes simplex virus/tumor necrosis factor-alpha synergistically induce nitric oxide synthase 2 in macrophages through cooperative action of nuclear factor-kappa B and IFN regulatory factor-1. Eur Cytokine Netw 2001; 12: 297–308
   PubMedGoogle Scholar
• Chon S. Y., Hassanain H. H., Gupta S. L. Cooperative role of interferon regulatory factor 1 and p91 (STAT1) response elements in interferon-gamma-inducible expression of human indoleamine 2,3-dioxygenase gene. J Biol Chem 1996; 271: 17247–17252
   PubMed Web of Science ®Google Scholar
• Haan C., Kreis S., Margue C., Behrmann I. Jaks and cytokine receptors—an intimate relationship. Biochem Pharmacol 2006; 72: 1538–1546
   PubMed Web of Science ®Google Scholar
• Rawlings J. S., Rosler K. M., Harrison D. A. The JAK/STAT signaling pathway. J Cell Sci 2004; 117: 1281–1283
   PubMed Web of Science ®Google Scholar
• Murray P. J. The JAK-STAT signaling pathway: Input and output integration. J Immunol 2007; 178: 2623–2629
   PubMed Web of Science ®Google Scholar
• Shuai K., Liu B. Regulation of JAK-STAT signalling in the immune system. Nat Rev Immunol 2003; 3: 900–911
   PubMed Web of Science ®Google Scholar
• Ilangumaran S., Rottapel R. Regulation of cytokine receptor signaling by SOCS1. Immunol Rev 2003; 192: 196–211
   PubMedGoogle Scholar
• Larsen L., Ropke C. Suppressors of cytokine signalling: SOCS. Apmis 2002; 110: 833–844
   PubMed Web of Science ®Google Scholar
• Vuong B. Q., Arenzana T. L., Showalter B. M., Losman J., Chen X. P., Mostecki J., Banks A. S., Limnander A., Fernandez N., Rothman P. B. SOCS-1 localizes to the microtubule organizing complex-associated 20S proteasome. Mol Cell Biol 2004; 24: 9092–9101
   PubMedGoogle Scholar
• Hebenstreit D., Horejs-Hoeck J., Duschl A. JAK/STAT-dependent gene regulation by cytokines. Drug News Perspect 2005; 18: 243–249
   PubMed Web of Science ®Google Scholar
• Ingley E., Klinken S. P. Cross-regulation of JAK and Src kinases. Growth Factors 2006; 24: 89–95
   PubMed Web of Science ®Google Scholar
• Baldeon M. E., Neece D. J., Nandi D., Monaco J. J., Gaskins H. R. Interferon-gamma independently activates the MHC class I antigen processing pathway and diminishes glucose responsiveness in pancreatic beta-cell lines. Diabetes 1997; 46: 770–778
   Google Scholar
• Fujimaki H., Hikawa N., Nagoya M., Nagata T., Minami M. IFN-gamma induces expression of MHC class I molecules in adult mouse dorsal root ganglion neurones. Neuroreport 1996; 7: 2951–2955
   PubMed Web of Science ®Google Scholar
• Leggatt G. R., Dunn L. A., De Kluyver R. L., Stewart T., Frazer I. H. Interferon-gamma enhances cytotoxic T lymphocyte recognition of endogenous peptide in keratinocytes without lowering the requirement for surface peptide. Immunol Cell Biol 2002; 80: 415–424
   Google Scholar
• Gobin S. J., van Zutphen M., Woltman A. M., van den Elsen P. J. Transactivation of classical and nonclassical HLA class I genes through the IFN-stimulated response element. J Immunol 1999; 163: 1428–1434
   PubMedGoogle Scholar
• Gobin S. J., Peijnenburg A., Keijsers V., van den Elsen P. J. alpha is crucial for two routes of IFN gamma-induced MHC class I transactivation: The ISRE-mediated route and a novel pathway involving CIITA. Immunity 1997; 6: 601–611
   PubMed Web of Science ®Google Scholar
• De Caterina R., Bourcier T., Laufs U., La Fata V., Lazzerini G., Neish A. S., Libby P., Liao J. K. Induction of endothelial-leukocyte interaction by interferon-gamma requires coactivation of nuclear factor-kappaB. Arterioscler Thromb Vasc Biol 2001; 21: 227–232
   PubMedGoogle Scholar
• Beppu K., Morisaki T., Matsunaga H., Uchiyama A., Ihara E., Hirano K., Kanaide H., Tanaka M., Katano M. Inhibition of interferon-gamma-activated nuclear factor-kappa B by cyclosporin A: A possible mechanism for synergistic induction of apoptosis by interferon-gamma and cyclosporin A in gastric carcinoma cells. Biochem Biophys Res Commun 2003; 305: 797–805
   Google Scholar
• Drew P. D., Lonergan M., Goldstein M. E., Lampson L. A., Ozato K., McFarlin D. E. Regulation of MHC class I and beta 2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes. J Immunol 1993; 150: 3300–3310
   PubMedGoogle Scholar
• Gobin S. J., van den Elsen P. J. Transcriptional regulation of the MHC class Ib genes HLA-E, HLA-F, and HLA-G. Hum Immunol 2000; 61: 1102–1107
   PubMed Web of Science ®Google Scholar
• Bluyssen A. R., Durbin J. E., Levy D. E. ISGF3 gamma p48, a specificity switch for interferon activated transcription factors. Cytokine Growth Factor Rev 1996; 7: 11–17
   PubMedGoogle Scholar
• Majumder S., Zhou L. Z., Chaturvedi P., Babcock G., Aras S., Ransohoff R. M. p48/STAT-1alpha-containing complexes play a predominant role in induction of IFN-gamma-inducible protein, 10 kDa (IP-10) by IFN-gamma alone or in synergy with TNF-alpha. J Immunol 1998; 161: 4736–4744
   PubMed Web of Science ®Google Scholar
• Kimura T., Kadokawa Y., Harada H., Matsumoto M., Sato M., Kashiwazaki Y., Tarutani M., Tan R. S., Takasugi T., Matsuyama T., Mak T. W., Noguchi S., Taniguchi T. Essential and non-redundant roles of p48 (ISGF3 gamma) and IRF-1 in both type I and type II interferon responses, as revealed by gene targeting studies. Genes Cells 1996; 1: 115–124
   PubMed Web of Science ®Google Scholar
• Kadereit S., Galabru J., Robert N., Meurs E. F., Hovanessian A. G. Characterization of an interferon-induced 48-kD protein immunologically related to the double-stranded RNA-activated protein kinase PKR. J Interferon Res 1994; 14: 251–257
   Google Scholar
• Weihua X., Kolla V., Kalvakolanu D. V. Interferon gamma-induced transcription of the murine ISGF3gamma (p48) gene is mediated by novel factors. Proc Natl Acad Sci U S A 1997; 94: 103–108
   PubMedGoogle Scholar
• Bluyssen H. A., Levy D. E. Stat2 is a transcriptional activator that requires sequence-specific contacts provided by stat1 and p48 for stable interaction with DNA. J Biol Chem 1997; 272: 4600–4605
   PubMedGoogle Scholar
• Wong L. H., Hatzinisiriou I., Devenish R. J., Ralph S. J. IFN-gamma priming up-regulates IFN-stimulated gene factor 3 (ISGF3) components, augmenting responsiveness of IFN-resistant melanoma cells to type I IFNs. J Immunol 1998; 160: 5475–5484
   PubMed Web of Science ®Google Scholar
• Matsumoto M., Tanaka N., Harada H., Kimura T., Yokochi T., Kitagawa M., Schindler C., Taniguchi T. Activation of the transcription factor ISGF3 by interferon-gamma. Biol Chem 1999; 380: 699–703
   Google Scholar
• Xiao W., Wang L., Yang X., Chen T., Hodge D., Johnson P. F., Farrar W. CCAAT/enhancer-binding protein beta mediates interferon-gamma-induced p48 (ISGF3-gamma) gene transcription in human monocytic cells. J Biol Chem 2001; 276: 23275–23281
   PubMedGoogle Scholar
• Matin S. F., Rackley R. R., Sadhukhan P. C., Kim M. S., Novick A. C., Bandyopadhyay S. K. Impaired alpha-interferon signaling in transitional cell carcinoma: Lack of p48 expression in 5637 cells. Cancer Res 2001; 61: 2261–2266
   Google Scholar
• Ma W., Lehner P. J., Cresswell P., Pober J. S., Johnson D. R. Interferon-gamma rapidly increases peptide transporter (TAP) subunit expression and peptide transport capacity in endothelial cells. J Biol Chem 1997; 272: 16585–16590
   PubMed Web of Science ®Google Scholar
• Seliger B., Hammers S., Hohne A., Zeidler R., Knuth A., Gerharz C. D., Huber C. IFN-gamma-mediated coordinated transcriptional regulation of the human TAP-1 and LMP-2 genes in human renal cell carcinoma. Clin Cancer Res 1997; 3: 573–578
   Google Scholar
• Tatake R. J., Ferrone S., Zeff R. A. The role of beta-2 microglobulin in temperature-sensitive and interferon-gamma-induced exocytosis of HLA class I molecules. Transplantation 1992; 54: 395–403
   Google Scholar
• Zugel U., Schoel B., Kaufmann S. H. Beta 2-microglobulin independent presentation of exogenously added foreign peptide and endogenous self-epitope by MHC class I alpha-chain to a cross-reactive CD8+ CTL clone. J Immunol 1994; 153: 4070–4080
   Google Scholar
• Romero J. M., Jimenez P., Cabrera T., Cozar J. M., Pedrinaci S., Tallada M., Garrido F., Ruiz-Cabello F. Coordinated downregulation of the antigen presentation machinery and HLA class I/beta2-microglobulin complex is responsible for HLA-ABC loss in bladder cancer. Int J Cancer 2005; 113: 605–610
   PubMed Web of Science ®Google Scholar
• Schiffer R., Baron J., Dagtekin G., Jahnen-Dechent W., Zwadlo-Klarwasser G. Differential regulation of the expression of transporters associated with antigen processing, TAP1 and TAP2, by cytokines and lipopolysaccharide in primary human macrophages. Inflamm Res 2002; 51: 403–408
   Google Scholar
• Garbi N., Tan P., Diehl A. D., Chambers B. J., Ljunggren H. G., Momburg F., Hammerling G. J. Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Nat Immunol 2000; 1: 234–238
   PubMed Web of Science ®Google Scholar
• Chefalo P. J., Grandea A. G., 3rd, Van Kaer L., Harding C. V. Tapasin-/- and TAP1-/- macrophages are deficient in vacuolar alternate class I MHC (MHC-I) processing due to decreased MHC-I stability at phagolysosomal pH. J Immunol 2003; 170: 5825–5833
   Google Scholar
• Grandea A. G., 3rd, Van Kaer L. Tapasin: An ER chaperone that controls MHC class I assembly with peptide. Trends Immunol 2001; 22: 194–199
   PubMedGoogle Scholar
• Grandea A. G., 3rd, Golovina T. N., Hamilton S. E., Sriram V., Spies T., Brutkiewicz R. R., Harty J. T., Eisenlohr L. C., Van Kaer L. Impaired assembly yet normal trafficking of MHC class I molecules in Tapasin mutant mice. Immunity 2000; 13: 213–222
   PubMed Web of Science ®Google Scholar
• Howarth M., Williams A., Tolstrup A. B., Elliott T. Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc Natl Acad Sci U S A 2004; 101: 11737–11742
   Google Scholar
• Fromm S. V., Duady-Ben Yaakov S., Schechter C., Ehrlich R. Assembly and cell surface expression of TAP-independent, chloroquine-sensitive and interferon-gamma-inducible class I MHC complexes in transformed fibroblast cell lines are regulated by tapasin. Cell Immunol 2002; 215: 207–218
   Google Scholar
• Seliger B., Schreiber K., Delp K., Meissner M., Hammers S., Reichert T., Pawlischko K., Tampe R., Huber C. Downregulation of the constitutive tapasin expression in human tumor cells of distinct origin and its transcriptional upregulation by cytokines. Tissue Antigens 2001; 57: 39–45
   PubMed Web of Science ®Google Scholar
• Demine R., Walden P. Testing the role of gp96 as peptide chaperone in antigen processing. J Biol Chem 2005; 280: 17573–17578
   PubMed Web of Science ®Google Scholar
• Heikema A., Agsteribbe E., Wilschut J., Huckriede A. Generation of heat shock protein-based vaccines by intracellular loading of gp96 with antigenic peptides. Immunol Lett 1997; 57: 69–74
   PubMed Web of Science ®Google Scholar
• Menoret A., Peng P., Srivastava P. K. Association of peptides with heat shock protein gp96 occurs in vivo and not after cell lysis. Biochem Biophys Res Commun 1999; 262: 813–818
   PubMed Web of Science ®Google Scholar
• Robert J., Ramanayake T., Maniero G. D., Morales H., Chida A. S. Phylogenetic conservation of glycoprotein 96 ability to interact with CD91 and facilitate antigen cross-presentation. J Immunol 2008; 180: 3176–3182
   Google Scholar
• Dahlmann B. Proteasomes. Essays Biochem 2005; 41: 31–48
   PubMedGoogle Scholar
• Goldberg A. L., Gaczynska M., Grant E., Michalek M., Rock K. L. Functions of the proteasome in antigen presentation. Cold Spring Harb Symp Quant Biol 1995; 60: 479–490
   Google Scholar
• Heink S., Ludwig D., Kloetzel P. M., Kruger E. IFN-gamma-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc Natl Acad Sci U S A 2005; 102: 9241–9246
   PubMed Web of Science ®Google Scholar
• Monaco J. J., Nandi D. The genetics of proteasomes and antigen processing. Annu Rev Genet 1995; 29: 729–754
   PubMed Web of Science ®Google Scholar
• Tanaka K. Role of proteasomes modified by interferon-gamma in antigen processing. J Leukoc Biol 1994; 56: 571–575
   PubMedGoogle Scholar
• Bose S., Stratford F. L., Broadfoot K. I., Mason G. G., Rivett A. J. Phosphorylation of 20S proteasome alpha subunit C8 (alpha7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by gamma-interferon. Biochem J 2004; 378: 177–184
   PubMed Web of Science ®Google Scholar
• Bose S., Brooks P., Mason G. G., Rivett A. J. gamma-Interferon decreases the level of 26 S proteasomes and changes the pattern of phosphorylation. Biochem J 2001; 353: 291–297
   PubMed Web of Science ®Google Scholar
• Ortiz-Navarrete V., Seelig A., Gernold M., Frentzel S., Kloetzel P. M., Hammerling G. J. Subunit of the ‘20S’ proteasome (multicatalytic proteinase) encoded by the major histocompatibility complex. Nature 1991; 353: 662–664
   PubMed Web of Science ®Google Scholar
• Boes B., Hengel H., Ruppert T., Multhaup G., Koszinowski U. H., Kloetzel P. M. Interferon gamma stimulation modulates the proteolytic activity and cleavage site preference of 20S mouse proteasomes. J Exp Med 1994; 179: 901–909
   Google Scholar
• Groettrup M., Kraft R., Kostka S., Standera S., Stohwasser R., Kloetzel P. M. A third interferon-gamma-induced subunit exchange in the 20S proteasome. Eur J Immunol 1996; 26: 863–869
   PubMed Web of Science ®Google Scholar
• Nandi D., Woodward E., Ginsburg D. B., Monaco J. J. Intermediates in the formation of mouse 20S proteasomes: implications for the assembly of precursor beta subunits. Embo J 1997; 16: 5363–5375
   Google Scholar
• Groettrup M., Khan S., Schwarz K., Schmidtke G. Interferon-gamma inducible exchanges of 20S proteasome active site subunits: Why?. Biochimie 2001; 83: 367–372
   PubMed Web of Science ®Google Scholar
• Unno M., Mizushima T., Morimoto Y., Tomisugi Y., Tanaka K., Yasuoka N., Tsukihara T. The structure of the mammalian 20S proteasome at 2.75 A resolution. Structure (Camb) 2002; 10: 609–618
   PubMed Web of Science ®Google Scholar
• Aki M., et al. Interferon-gamma induces different subunit organizations and functional diversity of proteasomes. J Biochem (Tokyo) 1994; 115: 257–269
   PubMed Web of Science ®Google Scholar
• Groettrup M., Standera S., Stohwasser R., Kloetzel P. M. The subunits MECL-1 and LMP2 are mutually required for incorporation into the 20S proteasome. Proc Natl Acad Sci U S A 1997; 94: 8970–8975
   PubMed Web of Science ®Google Scholar
• Cascio P., Goldberg A. L. Preparation of hybrid (19S-20S-PA28) proteasome complexes and analysis of peptides generated during protein degradation. Methods Enzymol 2005; 398: 336–352
   PubMed Web of Science ®Google Scholar
• Goldberg A. L., Cascio P., Saric T., Rock K. L. The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol 2002; 39: 147–164
   PubMed Web of Science ®Google Scholar
• Rivett A. J., Bose S., Brooks P., Broadfoot K. I. Regulation of proteasome complexes by gamma-interferon and phosphorylation. Biochimie 2001; 83: 363–366
   PubMed Web of Science ®Google Scholar
• Brooks P., Fuertes G., Murray R. Z., Bose S., Knecht E., Rechsteiner M. C., Hendil K. B., Tanaka K., Dyson J., Rivett J. Subcellular localization of proteasomes and their regulatory complexes in mammalian cells. Biochem J 2000; 346: 155–161
   PubMed Web of Science ®Google Scholar
• Berezutskaya E., Bagchi S. The human papillomavirus E7 oncoprotein functionally interacts with the S4 subunit of the 26 S proteasome. J Biol Chem 1997; 272: 30135–30140
   PubMedGoogle Scholar
• Eichten A., Westfall M., Pietenpol J. A., Munger K. Stabilization and functional impairment of the tumor suppressor p53 by the human papillomavirus type 16 E7 oncoprotein. Virology 2002; 295: 74–85
   Google Scholar
• Smahel M., Sima P., Ludvikova V., Marinov I., Pokorna D., Vonka V. Immunisation with modified HPV16 E7 genes against mouse oncogenic TC-1 cell sublines with downregulated expression of MHC class I molecules. Vaccine 2003; 21: 1125–1136
   PubMedGoogle Scholar
• Kao W. H., Beaudenon S. L., Talis A. L., Huibregtse J. M., Howley P. M. Human papillomavirus type 16 E6 induces self-ubiquitination of the E6AP ubiquitin-protein ligase. J Virol 2000; 74: 6408–6417
   PubMedGoogle Scholar
• Gao Q., Kumar A., Singh L., Huibregtse J. M., Beaudenon S., Srinivasan S., Wazer D. E., Band H., Band V. Human papillomavirus E6-induced degradation of E6TP1 is mediated by E6AP ubiquitin ligase. Cancer Res 2002; 62: 3315–3321
   PubMedGoogle Scholar
• Lagrange M., Charbonnier S., Orfanoudakis G., Robinson P., Zanier K., Masson M., Lutz Y., Trave G., Weiss E., Deryckere F. Binding of human papillomavirus 16 E6 to p53 and E6AP is impaired by monoclonal antibodies directed against the second zinc-binding domain of E6. J Gen Virol 2005; 86: 1001–1007
   Google Scholar
• Thomas M. C., Chiang C. M. E6 oncoprotein represses p53-dependent gene activation via inhibition of protein acetylation independently of inducing p53 degradation. Mol Cell 2005; 17: 251–264
   PubMed Web of Science ®Google Scholar
• Groettrup M., Ruppert T., Kuehn L., Seeger M., Standera S., Koszinowski U., Kloetzel P. M. The interferon-gamma-inducible 11 S regulator (PA28) and the LMP2/LMP7 subunits govern the peptide production by the 20 S proteasome in vitro. J Biol Chem 1995; 270: 23808–23815
   PubMed Web of Science ®Google Scholar
• Nandi D., Jiang H., Monaco J. J. Identification of MECL-1 (LMP-10) as the third IFN-gamma-inducible proteasome subunit. J Immunol 1996; 156: 2361–2364
   PubMed Web of Science ®Google Scholar
• Akiyama K., Kagawa S., Tamura T., Shimbara N., Takashina M., Kristensen P., Hendil K. B., Tanaka K., Ichihara A. Replacement of proteasome subunits X and Y by LMP7 and LMP2 induced by interferon-gamma for acquirement of the functional diversity responsible for antigen processing. FEBS Lett 1994; 343: 85–88
   PubMed Web of Science ®Google Scholar
• Sijts A. J., Ruppert T., Rehermann B., Schmidt M., Koszinowski U., Kloetzel P. M. Efficient generation of a hepatitis B virus cytotoxic T lymphocyte epitope requires the structural features of immunoproteasomes. J Exp Med 2000; 191: 503–514
   PubMed Web of Science ®Google Scholar
• Bocher W. O., Dekel B., Schwerin W., Geissler M., Hoffmann S., Rohwer A., Arditti F., Cooper A., Bernhard H., Berrebi A., Rose-John S., Shaul Y., Galle P. R., Lohr H. F., Reisner Y. Induction of strong hepatitis B virus (HBV) specific T helper cell and cytotoxic T lymphocyte responses by therapeutic vaccination in the trimera mouse model of chronic HBV infection. Eur J Immunol 2001; 31: 2071–2079
   Google Scholar
• Xu W., Chu Y., Zhang R., Xu H., Wang Y., Xiong S. Endoplasmic reticulum targeting sequence enhances HBV-specific cytotoxic T lymphocytes induced by a CTL epitope-based DNA vaccine. Virology 2005; 334: 255–263
   Google Scholar
• Witt E., Zantopf D., Schmidt M., Kraft R., Kloetzel P. M., Kruger E. Characterisation of the newly identified human Ump1 homologue POMP and analysis of LMP7(beta 5i) incorporation into 20 S proteasomes. J Mol Biol 2000; 301: 1–9
   PubMedGoogle Scholar
• York I. A., Goldberg A. L., Mo X. Y., Rock K. L. Proteolysis and class I major histocompatibility complex antigen presentation. Immunol Rev 1999; 172: 49–66
   PubMed Web of Science ®Google Scholar
• McCutchen-Maloney S. L., Matsuda K., Shimbara N., Binns D. D., Tanaka K., Slaughter C. A., DeMartino G. N. cDNA cloning, expression, and functional characterization of PI31, a proline-rich inhibitor of the proteasome. J Biol Chem 2000; 275: 18557–18565
   PubMed Web of Science ®Google Scholar
• Zaiss D. M., Standera S., Holzhutter H., Kloetzel P., Sijts A. J. The proteasome inhibitor PI31 competes with PA28 for binding to 20S proteasomes. FEBS Lett 1999; 457: 333–338
   PubMed Web of Science ®Google Scholar
• Tanahashi N., Kawahara H., Murakami Y., Tanaka K. The proteasome-dependent proteolytic system. Mol Biol Rep 1999; 26: 3–9
   Google Scholar
• Zaiss D. M., Standera S., Kloetzel P. M., Sijts A. J. PI31 is a modulator of proteasome formation and antigen processing. Proc Natl Acad Sci U S A 2002; 99: 14344–14349
   PubMed Web of Science ®Google Scholar
• Azar G. A., Sekaly R. P., Thibodeau J. A defective viral superantigen-presenting phenotype in HLA-DR transfectants is corrected by CIITA. J Immunol 2005; 174: 7548–7557
   Google Scholar
• Tanahashi N., Yokota K., Ahn J. Y., Chung C. H., Fujiwara T., Takahashi E., DeMartino G. N., Slaughter C. A., Toyonaga T., Yamamura K., Shimbara N., Tanaka K. Molecular properties of the proteasome activator PA28 family proteins and gamma-interferon regulation. Genes Cells 1997; 2: 195–211
   PubMed Web of Science ®Google Scholar
• Ahn J. Y., Tanahashi N., Akiyama K., Hisamatsu H., Noda C., Tanaka K., Chung C. H., Shibmara N., Willy P. J., Mott J. D. Primary structures of two homologous subunits of PA28, a gamma-interferon-inducible protein activator of the 20S proteasome. FEBS Lett 1995; 366: 37–42
   PubMed Web of Science ®Google Scholar
• Groettrup M., Soza A., Eggers M., Kuehn L., Dick T. P., Schild H., Rammensee H. G., Koszinowski U. H., Kloetzel P. M. A role for the proteasome regulator PA28alpha in antigen presentation. Nature 1996; 381: 166–168
   PubMed Web of Science ®Google Scholar
• Schwarz K., Eggers M., Soza A., Koszinowski U. H., Kloetzel P. M., Groettrup M. The proteasome regulator PA28alpha/beta can enhance antigen presentation without affecting 20S proteasome subunit composition. Eur J Immunol 2000; 30: 3672–3679
   PubMed Web of Science ®Google Scholar
• Hendil K. B., Khan S., Tanaka K. Simultaneous binding of PA28 and PA700 activators to 20 S proteasomes. Biochem J 1998; 332: 749–754
   PubMed Web of Science ®Google Scholar
• Kim D. H., Lee S. M., Hong B. Y., Kim Y. T., Choi T. J. Cloning and sequence analysis of cDNA for the proteasome activator PA28-beta subunit of flounder (Paralichthys olivaceus). Mol Immunol 2003; 40: 611–616
   Google Scholar
• McCusker D., Wilson M., Trowsdale J. Organization of the genes encoding the human proteasome activators PA28alpha and beta. Immunogenetics 1999; 49: 438–445
   Google Scholar
• Sijts A., Sun Y., Janek K., Kral S., Paschen A., Schadendorf D., Kloetzel P. M. The role of the proteasome activator PA28 in MHC class I antigen processing. Mol Immunol 2002; 39: 165–169
   PubMed Web of Science ®Google Scholar
• Rechsteiner M., Realini C., Ustrell V. The proteasome activator 11 S REG (PA28) and class I antigen presentation. Biochem J 2000; 345: 1–15
   PubMedGoogle Scholar
• Yao Y., Huang L., Krutchinsky A., Wong M. L., Standing K. G., Burlingame A. L., Wang C. C. Structural and functional characterizations of the proteasome-activating protein PA26 from Trypanosoma brucei. J Biol Chem 1999; 274: 33921–33930
   Google Scholar
• van Hall T., Sijts A., Camps M., Offringa R., Melief C., Kloetzel P. M., Ossendorp F. Differential influence on cytotoxic T lymphocyte epitope presentation by controlled expression of either proteasome immunosubunits or PA28. J Exp Med 2000; 192: 483–494
   PubMed Web of Science ®Google Scholar
• Sijts A., Zaiss D., Kloetzel P. M. The role of the ubiquitin-proteasome pathway in MHC class I antigen processing: implications for vaccine design. Curr Mol Med 2001; 1: 665–676
   Google Scholar
• Murata S., Udono H., Tanahashi N., Hamada N., Watanabe K., Adachi K., Yamano T., Yui K., Kobayashi N., Kasahara M., Tanaka K., Chiba T. Immunoproteasome assembly and antigen presentation in mice lacking both PA28alpha and PA28beta. EMBO J 2001; 20: 5898–5907
   PubMed Web of Science ®Google Scholar
• Sun Y., Sijts A. J., Song M., Janek K., Nussbaum A. K., Kral S., Schirle M., Stevanovic S., Paschen A., Schild H., Kloetzel P. M., Schadendorf D. Expression of the proteasome activator PA28 rescues the presentation of a cytotoxic T lymphocyte epitope on melanoma cells. Cancer Res 2002; 62: 2875–2882
   PubMed Web of Science ®Google Scholar
• Yamano T., Murata S., Shimbara N., Tanaka N., Chiba T., Tanaka K., Yui K., Udono H. Two distinct pathways mediated by PA28 and hsp90 in major histocompatibility complex class I antigen processing. J Exp Med 2002; 196: 185–196
   PubMed Web of Science ®Google Scholar
• Yamano T., Sugahara H., Mizukami S., Murata S., Chiba T., Tanaka K., Yui K., Udono H. Allele-selective effect of PA28 in MHC class I antigen processing. J Immunol 2008; 181: 1655–1664
   PubMedGoogle Scholar
• Kloetzel P. M., Ossendorp F. Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr Opin Immunol 2004; 16: 76–81
   PubMed Web of Science ®Google Scholar
• Hammer G. E., Gonzalez F., Champsaur M., Cado D., Shastri N. The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat Immunol 2006; 7: 103–112
   PubMed Web of Science ®Google Scholar
• Serwold T., Gonzalez F., Kim J., Jacob R., Shastri N. ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 2002; 419: 480–483
   PubMed Web of Science ®Google Scholar
• Saric T., Chang S. C., Hattori A., York I. A., Markant S., Rock K. L., Tsujimoto M., Goldberg A. L. An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 2002; 3: 1169–1176
   PubMed Web of Science ®Google Scholar
• Maile R., Elsegood K. A., Harding T. C., Uney J. B., Stewart C. E., Banting G., Dayan C. M. Effective formation of major histocompatibility complex class II-peptide complexes from endogenous antigen by thyroid epithelial cells. Immunology 2000; 99: 367–374
   PubMed Web of Science ®Google Scholar
• Lu J., Wettstein P. J., Higashimoto Y., Appella E., Celis E. TAP-independent presentation of CTL epitopes by Trojan antigens. J Immunol 2001; 166: 7063–7071
   Google Scholar
• O'Donnell P. W., Haque A., Klemsz M. J., Kaplan M. H., Blum J. S. Cutting edge: Induction of the antigen-processing enzyme IFN-gamma-inducible lysosomal thiol reductase in melanoma cells. Is STAT1-dependent but CIITA-independent. J Immunol 2004; 173: 731–735
   Google Scholar
• Brooks P., Murray R. Z., Mason G. G., Hendil K. B., Rivett A. J. Association of immunoproteasomes with the endoplasmic reticulum. Biochem J 2000; 352: 611–615
   Google Scholar
• Bulik S., Peters B., Ebeling C., Holzhutter H. Cytosolic processing of proteasomal cleavage products can enhance the presentation efficiency of MHC-1 epitopes. Genome Inform 2004; 15: 24–34
   Google Scholar
• Book A. J., Yang P., Scalf M., Smith L. M., Vierstra R. D. Tripeptidyl peptidase II. An oligomeric protease complex from Arabidopsis. Plant Physiol 2005; 138: 1046–1057
   Google Scholar
• De Winter H., Breslin H., Miskowski T., Kavash R., Somers M. Inhibitor-based validation of a homology model of the active-site of tripeptidyl peptidase II. J Mol Graph Model 2005; 23: 409–418
   Google Scholar
• Malandrinos G., Louloudi M., Koukkou A. I., Sovago I., Drainas C., Hadjiliadis N. Zinc(II) and cadmium(II) metal complexes of thiamine pyrophosphate and 2-(alpha-hydroxyethyl)thiamine pyrophosphate: Models for activation of pyruvate decarboxylase. J Biol Inorg Chem 2000; 5: 218–226
   Google Scholar
• Reits E., Neijssen J., Herberts C., Benckhuijsen W., Janssen L., Drijfhout J. W., Neefjes J. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity 2004; 20: 495–506
   PubMed Web of Science ®Google Scholar
• York I. A., Bhutani N., Zendzian S., Goldberg A. L., Rock K. L. Tripeptidyl peptidase II is the major peptidase needed to trim long antigenic precursors, but is not required for most MHC class I antigen presentation. J Immunol 2006; 177: 1434–1443
   PubMedGoogle Scholar
• Luft T., Rizkalla M., Tai T. Y., Chen Q., MacFarlan R. I., Davis I. D., Maraskovsky E., Cebon J. Exogenous peptides presented by transporter associated with antigen processing (TAP)-deficient and TAP-competent cells: Intracellular loading and kinetics of presentation. J Immunol 2001; 167: 2529–2537
   PubMed Web of Science ®Google Scholar
• Ayalon O., Hughes E. A., Cresswell P., Lee J., O'Donnell L., Pardi R., Bender J. R. Induction of transporter associated with antigen processing by interferon gamma confers endothelial cell cytoprotection against natural killer-mediated lysis. Proc Natl Acad Sci U S A 1998; 95: 2435–2440
   PubMedGoogle Scholar
• Kuroda K., Yamashina K., Kitatani N., Kagishima A., Hamaoka T., Hosaka Y. Characterization of defectiveness in endogenous antigen presentation of novel murine cells established from methylcholanthrene-induced fibrosarcomas. Immunology 1995; 84: 153–158
   Google Scholar
• Gabathuler R., Reid G., Kolaitis G., Driscoll J., Jefferies W. A. Comparison of cell lines deficient in antigen presentation reveals a functional role for TAP-1 alone in antigen processing. J Exp Med 1994; 180: 1415–1425
   PubMed Web of Science ®Google Scholar
• Belich M. P., Glynne R. J., Senger G., Sheer D., Trowsdale J. Proteasome components with reciprocal expression to that of the MHC-encoded LMP proteins. Curr Biol 1994; 4: 769–776
   PubMedGoogle Scholar
• Kjerrulf M., Grdic D., Ekman L., Schon K., Vajdy M., Lycke N. Y. Interferon-gamma receptor-deficient mice exhibit impaired gut mucosal immune responses but intact oral tolerance. Immunology 1997; 92: 60–68
   Google Scholar
• Nagao M., Nakajima Y., Kanehiro H., Hisanaga M., Aomatsu Y., Ko S., Tatekawa Y., Ikeda N., Kanokogi H., Urizono Y., Kobayashi T., Shibaji T., Kanamura T., Ogawa S., Nakano H. The impact of interferon gamma receptor expression on the mechanism of escape from host immune surveillance in hepatocellular carcinoma. Hepatology 2000; 32: 491–500
   Google Scholar
• Khouw I. M., van Wachem P. B., Plantinga J. A., Haagmans B. L., de Leij L. F., van Luyn M. J. Foreign-body reaction to dermal sheep collagen in interferon-gamma-receptor knock-out mice. J Biomed Mater Res 2000; 50: 259–266
   Google Scholar