NLRC5, at the heart of antigen presentation

Frontiers in Immunology

Volumn 4, Issue NOV, 2013, Pages

  Neerincx, Andreas ^a   Castro, Wilson ^b   Guarda, Greta ^b   Kufer, Thomas A ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Antigen presentation; Innate signaling; MHC class I; NLR; NLRC5; Transcription

Indexed keywords

EID: 84890325874     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00397     Document Type: Article

References (75)

1. Schroder K, Tschopp J. The inflammasomes. Cell (2010) 140:821-32. doi: 10.1016/j.cell.2010.01.040
2. Rathinam VA, Vanaja SK, Fitzgerald KA. Regulation of inflammasome signaling. Nat Immunol (2012) 13:333-332. doi:10.1038/ni.2237
3. Kufer TA, Sansonetti PJ. NLR functions beyond pathogen recognition. Nat Immunol (2011) 12:121-8. doi:10.1038/ni.1985
4. Ting JP, Kastner DL, Hoffman HM. CATERPILLERs, pyrin and hereditary immunological disorders. Nat Rev Immunol (2006) 6:183-95. doi:10.1038/nri1788
5. Koonin EV, Aravind L. The NACHT family-a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci (2000) 25:223-4. doi:10.1016/S0968-0004(00)01577-2
6. Fritz JH, Ferrero RL, Philpott DJ, Girardin SE. Nod-like proteins in immunity, inflammation and disease. Nat Immunol (2006) 7:1250-7. doi:10.1038/ni1412
7. Kufer TA, Kremmer E, Adam AC, Philpott DJ, Sansonetti PJ. The pattern-recognition molecule Nod1 is localized at the plasma membrane at sites of bacterial interaction. Cell Microbiol (2008) 10:477-86. doi:10.1111/j.1462-5822.2007.01062.x
8. Krawczyk M, Reith W. Regulation of MHC class II expression, a unique regulatory system identified by the study of a primary immunodeficiency disease. Tissue Antigens (2006) 67:183-97. doi:10.1111/j.1399-0039.2006.00557.x
9. Accolla RS. Human B cell variants immunoselected against a single Ia antigen subset have lost expression of several Ia antigen subsets. J Exp Med (1983) 157:1053-8. doi:10.1084/jem.157.3.1053
10. Long EO, Mach B, Accolla RS. Ia-negative B-cell variants reveal a coordinate regulation in the transcription of the HLA class II gene family. Immunogenetics (1984) 19:349-53. doi:10.1007/BF00345408
11. Hume CR, Lee JS. Congenital immunodeficiencies associated with absence of HLA class II antigens on lymphocytes result from distinct mutations in trans-acting factors. Hum Immunol (1989) 26:288-309. doi:10.1016/0198-8859(89)90007-4
12. 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) 75:135-46. doi:10.1016/0092-8674(93)90685-J
13. Neefjes J, Jongsma ML, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol (2011) 11:823-36. doi:10.1038/nri3084
14. Muhlethaler-Mottet A, Otten LA, Steimle V, Mach B. Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO J (1997) 16:2851-60. doi:10.1093/emboj/16.10.2851
15. Nickerson K, Sisk TJ, Inohara N, Yee CS, Kennell J, Cho MC, et al. Dendritic cell-specific MHC class II transactivator contains a caspase recruitment domain that confers potent transactivation activity. J Biol Chem (2001) 276:19089-93. doi:10.1074/jbc.M101295200
16. Zinzow-Kramer WM, Long AB, Youngblood BA, Rosenthal KM, Butler R, Mohammed AU, et al. CIITA promoter I CARD-deficient mice express functional MHC class II genes in myeloid and lymphoid compartments. Genes Immun (2012) 13:299-310. doi:10.1038/gene.2011.86
17. Reith W, Mach B. The bare lymphocyte syndrome and the regulation of MHC expression. Annu Rev Immunol (2001) 19:331-73. doi:10.1146/annurev.immunol.19.1.331
18. Steimle V, Mach B. Complementation cloning of mammalian transcriptional regulators: the example of MHC class II gene regulators. Curr Opin Genet Dev (1995) 5:646-51. doi:10.1016/0959-437X(95)80034-4
19. Durand B, Sperisen P, Emery P, Barras E, Zufferey M, Mach B, et al. RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency. EMBO J (1997) 16:1045-55. doi:10.1093/emboj/16.5.1045
20. Masternak K, Barras E, Zufferey M, Conrad B, Corthals G, Aebersold R, et al. A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients. Nat Genet (1998) 20:273-7. doi:10.1038/3081
21. Nagarajan UM, Louis-Plence P, Desandro A, Nilsen R, Bushey A, Boss JM. RFX-B is the gene responsible for the most common cause of the bare lymphocyte syndrome, an MHC class II immunodeficiency. Immunity (1999) 10:153-62. doi:10.1016/S1074-7613(00)80016-3
22. Steimle V, Durand B, Barras E, Zufferey M, Hadam MR, Mach B, et al. A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). Genes Dev (1995) 9:1021-32. doi:10.1101/gad.9.9.1021
23. Moreno CS, Emery P, West JE, Durand B, Reith W, Mach B, et al. Purified X2 binding protein (X2BP) cooperatively binds the class II MHC X box region in the presence of purified RFX, the X box factor deficient in the bare lymphocyte syndrome. J Immunol (1995) 155:4313-21.
24. Moreno CS, Beresford GW, Louis-Plence P, Morris AC, Boss JM. CREB regulates MHC class II expression in a CIITA-dependent manner. Immunity (1999) 10:143-51. doi:10.1016/S1074-7613(00)80015-1
25. Villard J, Muhlethaler-Mottet A, Bontron S, Mach B, Reith W. CIITA-induced occupation of MHC class II promoters is independent of the cooperative stabilization of the promoter-bound multi-protein complexes. Int Immunol (1999) 11:461-9. doi:10.1093/intimm/11.3.461
26. Zhu XS, Linhoff MW, Li G, Chin KC, Maity SN, Ting JP. Transcriptional scaffold: CIITA interacts with NF-Y, RFX, and CREB to cause stereospecific regulation of the class II major histocompatibility complex promoter. Mol Cell Biol (2000) 20:6051-61. doi:10.1128/MCB.20.16.6051-6061.2000
27. Reith W, Leibundgut-Landmann S, Waldburger JM. Regulation of MHC class II gene expression by the class II transactivator. Nat Rev Immunol (2005) 5:793-806. doi:10.1038/nri1708
28. Wright KL, Ting JP. Epigenetic regulation of MHC-II and CIITA genes. Trends Immunol (2006) 27:405-12. doi:10.1016/j.it.2006.07.007
29. LeibundGut-Landmann S, Waldburger JM, Krawczyk M, Otten LA, Suter T, Fontana A, et al. Mini-review: specificity and expression of CIITA, the master regulator of MHC class II genes. Eur J Immunol (2004) 34:1513-25. doi:10.1002/eji.200424964
30. Gobin SJ, Keijsers V, Van Zutphen M, Van Den Elsen PJ. The role of enhancer A in the locus-specific transactivation of classical and nonclassical HLA class I genes by nuclear factor kappa B. J Immunol (1998) 161: 2276-83.
31. Gobin SJ, Van Zutphen M, Woltman AM, Van Den Elsen PJ. Transactivation of classical and nonclassical HLA class I genes through the IFN-stimulated response element. J Immunol (1999) 163:1428-34.
32. Johnson DR. Locus-specific constitutive and cytokine-induced HLA class I gene expression. J Immunol (2003) 170:1894-902.
33. van den Elsen PJ, Holling TM, Kuipers HF, Van Der Stoep N. Transcriptional regulation of antigen presentation. Curr Opin Immunol (2004) 16:67-75. doi:10.1016/j.coi.2003.11.015
34. Gobin SJ, Peijnenburg A, Keijsers V, Van Den Elsen PJ. Site 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) 6:601-11. doi:10.1016/S1074-7613(00)80348-9
35. Martin BK, Chin KC, Olsen JC, Skinner CA, Dey A, Ozato K, et al. Induction of MHC class I expression by the MHC class II transactivator CIITA. Immunity (1997) 6:591-600. doi:10.1016/S1074-7613(00)80347-7
36. Gobin SJ, Peijnenburg A, Van Eggermond M, Van Zutphen M, Van Den Berg R, Van Den Elsen PJ. The RFX complex is crucial for the constitutive and CIITA-mediated transactivation of MHC class I and beta2-microglobulin genes. Immunity (1998) 9:531-41. doi:10.1016/S1074-7613(00)80636-6
37. Gobin SJ, Van Zutphen M, Westerheide SD, Boss JM, Van Den Elsen PJ. The MHC-specific enhanceosome and its role in MHC class I and beta(2)-microglobulin gene transactivation. J Immunol (2001) 167:5175-84.
38. Itoh-Lindstrom Y, Piskurich JF, Felix NJ, Wang Y, Brickey WJ, Platt JL, et al. Reduced IL-4-, lipopolysaccharide-, and IFN-gamma-induced MHC class II expression in mice lacking class II transactivator due to targeted deletion of the GTP-binding domain. J Immunol (1999) 163:2425-31.
39. Proell M, Riedl SJ, Fritz JH, Rojas AM, Schwarzenbacher R. The Nod-like receptor (NLR) family: a tale of similarities and differences. PLoS One (2008) 3:e2119. doi:10.1371/journal.pone.0002119
40. Istomin AY, Godzik A. Understanding diversity of human innate immunity receptors: analysis of surface features of leucine-rich repeat domains in NLRs and TLRs. BMC Immunol (2009) 10:48. doi:10.1186/1471-2172-10-48
41. Benko S, Magalhaes JG, Philpott DJ, Girardin SE. NLRC5 limits the activation of inflammatory pathways. J Immunol (2010) 185:1681-91. doi:10.4049/jimmunol.0903900
42. Meissner TB, Li A, Biswas A, Lee KH, Liu YJ, Bayir E, et al. NLR family member NLRC5 is a transcriptional regulator of MHC class I genes. Proc Natl Acad Sci U S A (2010) 107:13794-9. doi:10.1073/pnas.1008684107
43. Neerincx A, Lautz K, Menning M, Kremmer E, Zigrino P, Hosel M, et al. A role for the human nucleotide-binding domain, leucine-rich repeat-containing family member NLRC5 in antiviral responses. J Biol Chem (2010) 285:26223-32. doi:10.1074/jbc.M110.109736
44. Kobayashi KS, van den Elsen PJ. NLRC5: a key regulator of MHC class I-dependent immune responses. Nat Rev Immunol (2012) 12:813-20. doi:10.1038/nri3339
45. Cui J, Zhu L, Xia X, Wang HY, Legras X, Hong J, et al. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell (2010) 141:483-96. doi:10.1016/j.cell.2010.03.040
46. Staehli F, Ludigs K, Heinz LX, Seguin-Estevez Q, Ferrero I, Braun M, et al. NLRC5 deficiency selectively impairs MHC class I-dependent lymphocyte killing by cytotoxic T cells. J Immunol (2012) 188:3820-8. doi:10.4049/jimmunol.1102671
47. Kuenzel S, Till A, Winkler M, Hasler R, Lipinski S, Jung S, et al. The nucleotide-binding oligomerization domain-like receptor NLRC5 is involved in IFN-dependent antiviral immune responses. J Immunol (2010) 184:1990-2000. doi:10.4049/jimmunol.0900557
48. Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics (2005) 21:2933-42. doi:10.1093/bioinformatics/bti473
49. Tanabe T, Chamaillard M, Ogura Y, Zhu L, Qiu S, Masumoto J, et al. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J (2004) 23:1587-97. doi:10.1038/sj.emboj.7600175
50. Girardin SE, Jehanno M, Mengin-Lecreulx D, Sansonetti PJ, Alzari PM, Philpott DJ. Identification of the critical residues involved in peptidoglycan detection by Nod1. J Biol Chem (2005) 280:38648-56. doi:10.1074/jbc.M509537200
51. Biswas A, Meissner TB, Kawai T, Kobayashi KS. Cutting edge: impaired MHC class I expression in mice deficient for Nlrc5/class I transactivator. J Immunol (2012) 189:516-20. doi:10.4049/jimmunol.1200064
52. Meissner TB, Li A, Liu YJ, Gagnon E, Kobayashi KS. The nucleotide-binding domain of NLRC5 is critical for nuclear import and transactivation activity. Biochem Biophys Res Commun (2012) 418:786-91. doi:10.1016/j.bbrc.2012.01.104
53. Neerincx A, Rodriguez GM, Steimle V, Kufer TA. NLRC5 controls basal MHC class I gene expression in an MHC enhanceosome-dependent manner. J Immunol (2012) 188:4940-50. doi:10.4049/jimmunol.1103136
54. Robbins GR, Truax AD, Davis BK, Zhang L, Brickey WJ, Ting JP. Regulation of class I major histocompatibility complex (MHC) by nucleotide-binding domain, leucine-rich repeat-containing (NLR) proteins. J Biol Chem (2012) 287:24294-303. doi:10.1074/jbc.M112.364604
55. Tong Y, Cui J, Li Q, Zou J, Wang HY, Wang RF. Enhanced TLR-induced NF-kappaB signaling and type I interferon responses in NLRC5 deficient mice. Cell Res (2012) 22:822-35. doi:10.1038/cr.2012.53
56. Yao Y, Wang Y, Chen F, Huang Y, Zhu S, Leng Q, et al. NLRC5 regulates MHC class I antigen presentation in host defense against intracellular pathogens. Cell Res (2012) 22:836-47. doi:10.1038/cr.2012.56
57. Sijts EJ, Kloetzel PM. The role of the proteasome in the generation of MHC class I ligands and immune responses. Cell Mol Life Sci (2011) 68:1491-502. doi:10.1007/s00018-011-0657-y
58. Meissner TB, Liu YJ, Lee KH, Li A, Biswas A, Van Eggermond MC, et al. NLRC5 cooperates with the RFX transcription factor complex to induce MHC class I gene expression. J Immunol (2012) 188:4951-8. doi:10.4049/jimmunol.1103160
59. Muhlethaler-Mottet A, Krawczyk M, Masternak K, Spilianakis C, Kretsovali A, Papamatheakis J, et al. The S box of major histocompatibility complex class II promoters is a key determinant for recruitment of the transcriptional co-activator CIITA. J Biol Chem (2004) 279:40529-35. doi:10.1074/jbc.M406585200
60. Hake SB, Masternak K, Kammerbauer C, Janzen C, Reith W, Steimle V. CIITA leucine-rich repeats control nuclear localization, in vivo recruitment to the major histocompatibility complex (MHC) class II enhanceosome, and MHC class II gene transactivation. Mol Cell Biol (2000) 20:7716-25. doi:10.1128/MCB.20.20.7716-7725.2000
61. Camacho-Carvajal MM, Klingler S, Schnappauf F, Hake SB, Steimle V. Importance of class II transactivator leucine-rich repeats for dominant-negative function and nucleo-cytoplasmic transport. Int Immunol (2004) 16:65-75. doi:10.1093/intimm/dxh010
62. Bewry NN, Bolick SC, Wright KL, Harton JA. GTP-dependent recruitment of CIITA to the class II major histocompatibility complex promoter. J Biol Chem (2007) 282:26178-84. doi:10.1074/jbc.M611747200
63. Harton JA, Cressman DE, Chin KC, Der CJ, Ting JP. GTP binding by class II transactivator: role in nuclear import. Science (1999) 285:1402-5. doi:10.1126/science.285.5432.1402
64. Harton JA, O'Connor W Jr, Conti BJ, Linhoff MW, Ting JP. Leucine-rich repeats of the class II transactivator control its rate of nuclear accumulation. Hum Immunol (2002) 63:588-601. doi:10.1016/S0198-8859(02)00400-7
65. Zurek B, Bielig H, Kufer TA. Cell-based reporter assay to analyze activation of Nod1 and Nod2. Methods Mol Biol (2011) 748:107-19. doi:10.1007/978-1-61779-139-0_7
66. Ronald PC, Beutler B. Plant and animal sensors of conserved microbial signatures. Science (2010) 330:1061-4. doi:10.1126/science.1189468
67. Padmanabhan MS, Dinesh-Kumar SP. All hands on deck-the role of chloroplasts, endoplasmic reticulum, and the nucleus in driving plant innate immunity. Mol Plant Microbe Interact (2010) 23:1368-80. doi:10.1094/MPMI-05-10-0113
68. Chang C, Yu D, Jiao J, Jing S, Schulze-Lefert P, Shen QH. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signaling. Plant Cell (2013) 25:1158-73. doi:10.1105/tpc.113.109942
69. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathog (2013) 9:e1003235. doi:10.1371/journal.ppat.1003235
70. Garcia AV, Parker JE. Heaven's Gate: nuclear accessibility and activities of plant immune regulators. Trends Plant Sci (2009) 14:479-87. doi:10.1016/j.tplants.2009.07.004
71. Algarra I, Garcia-Lora A, Cabrera T, Ruiz-Cabello F, Garrido F. The selection of tumor variants with altered expression of classical and nonclassical MHC class I molecules: implications for tumor immune escape. Cancer Immunol Immunother (2004) 53:904-10. doi:10.1007/s00262-004-0517-9
72. Karre K. NK cells, MHC class I molecules and the missing self. Scand J Immunol (2002) 55:221-8. doi:10.1046/j.1365-3083.2002.01053.x
73. Ling A, Soares F, Croitoru DO, Tattoli I, Carneiro LA, Boniotto M, et al. Post-transcriptional inhibition of luciferase reporter assays by the nod-like receptor proteins NLRX1 and NLRC3. J Biol Chem (2012) 287:28705-16. doi:10.1074/jbc.M111.333146
74. Kumar H, Pandey S, Zou J, Kumagai Y, Takahashi K, Akira S, et al. NLRC5 deficiency does not influence cytokine induction by virus and bacteria infections. J Immunol (2011) 186:994-1000. doi:10.4049/jimmunol.1002094
75. Davis BK, Roberts RA, Huang MT, Willingham SB, Conti BJ, Brickey WJ, et al. Cutting edge: NLRC5-dependent activation of the inflammasome. J Immunol (2010) 186:1333-7. doi:10.4049/jimmunol.1003111