NLRC5: A key regulator of MHC class I-dependent immune responses

Nature Reviews Immunology

Volumn 12, Issue 12, 2012, Pages 813-820

  Kobayashi, Koichi S ^a,b,c   Van Den Elsen, Peter J ^d,e  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NOD LIKE RECEPTOR CARD CONTAINING 5; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; GENE ACTIVATION; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ADAPTIVE IMMUNITY; ANIMALS; GENE EXPRESSION REGULATION; GENES, MHC CLASS I; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; TRANS-ACTIVATORS;

EID: 84870212902     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3339     Document Type: Review

References (53)

1. Steimle, V., Otten, L. A., Zufferey, M. & Mach, B. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75, 135-146 (1993). (Pubitemid 23306027)
2. Chang, C. H., Guerder, S., Hong, S. C., van Ewijk, W. & Flavell, R. A. Mice lacking the MHC class II transactivator (CIITA) show tissue-specific impairment of MHC class II expression. Immunity 4, 167-178 (1996). (Pubitemid 26093162)
3. Ting, J. P. & Trowsdale, J. Genetic control of MHC class II expression. Cell 109, S21-S33 (2002). (Pubitemid 34457849)
4. Gobin, S. J., Peijnenburg, A., Keijsers, V. & van den Elsen, P. J. Site α is crucial for two routes of IFNγ-induced MHC class I transactivation: the ISRE-mediated route and a novel pathway involving CIITA. Immunity 6, 601-611 (1997). (Pubitemid 27239351)
5. Gobin, S. J. et al. The RFX complex is crucial for the constitutive and CIITA-mediated transactivation of MHC class I and β2-microglobulin genes. Immunity 9, 531-541 (1998). (Pubitemid 28499204)
6. Gobin, S. J., van Zutphen, M., Westerheide, S. D., Boss, J. M. & van den Elsen, P. J. The MHC-specific enhanceosome and its role in MHC class I and β2-microglobulin gene transactivation. J. Immunol. 167, 5175-5184 (2001). (Pubitemid 33009754)
7. Martin, B. K. et al. Induction of MHC class I expression by the MHC class II transactivator CIITA. Immunity 6, 591-600 (1997). (Pubitemid 27239350)
8. Williams, G. S. et al. Mice lacking the transcription factor CIITA - a second look. Int. Immunol. 10, 1957-1967 (1998). (Pubitemid 28566058)
9. Itoh-Lindstrom, Y. et al. Reduced IL-4-, lipopolysaccharide-, and IFN-γ-induced MHC class II expression in mice lacking class II transactivator due to targeted deletion of the GTP-binding domain. J. Immunol. 163, 2425-2431 (1999). (Pubitemid 29399161)
10. Robbins, G. R. et al. Regulation of class I major histocompatibility complex (MHC) by nucleotide-binding domain, leucine-rich repeat-containing (NLR) proteins. J. Biol. Chem. 287, 24294-24303 (2012).
11. Meissner, T. B. et al. NLR family member NLRC5 is a transcriptional regulator of MHC class I genes. Proc. Natl Acad. Sci. USA 107, 13794-13799 (2010).
12. Meissner, T. B. et al. NLRC5 cooperates with the RFX transcription factor complex to induce MHC class I gene expression. J. Immunol. 188, 4951-4958 (2012).
13. Staehli, F. et al. NLRC5 deficiency selectively impairs MHC class I-dependent lymphocyte killing by cytotoxic T cells. J. Immunol. 188, 3820-3828 (2012).
14. Neerincx, A., Rodriguez, G. M., Steimle, V. & Kufer, T. A. NLRC5 controls basal MHC class I gene expression in an MHC enhanceosome-dependent manner. J. Immunol. 188, 4940-4950 (2012).
15. Biswas, A., Meissner, T. B., Kawai, T. & Kobayashi, K. S. Cutting edge: impaired MHC class I expression in mice deficient for Nlrc5/class I transactivator. J. Immunol. 189, 516-520 (2012).
16. Tong, Y. et al. Enhanced TLR-induced NF-κB signaling and type I interferon responses in NLRC5 deficient mice. Cell Res. 22, 822-835 (2012).
17. Yao, Y. et al. NLRC5 regulates MHC class I antigen presentation in host defense against intracellular pathogens. Cell Res. 22, 836-847 (2012).
18. Choi, N. M., Majumder, P. & Boss, J. M. Regulation of major histocompatibility complex class II genes. Curr. Opin. Immunol. 23, 81-87 (2011).
19. van den Elsen, P. J. Expression regulation of major histocompatibility complex class I and class II encoding genes. Front. Immunol. 2, 48 (2011).
20. Reith, W. et al. Congenital immunodeficiency with a regulatory defect in MHC class II gene expression lacks a specific HLA-DR promoter binding protein, RF-X. Cell 53, 897-906 (1988).
21. Steimle, V. et al. A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). Genes Dev. 9, 1021-1032 (1995).
22. Masternak, K. et al. A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients. Nature Genet. 20, 273-277 (1998). (Pubitemid 28507672)
23. Nagarajan, U. M. et al. RFX-B is the gene responsible for the most common cause of the bare lymphocyte syndrome, an MHC class II immunodeficiency. Immunity 10, 153-162 (1999). (Pubitemid 29115621)
24. Durand, B. et al. RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency. EMBO J. 16, 1045-1055 (1997). (Pubitemid 27113183)
25. Masternak, K. et al. CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev. 14, 1156-1166 (2000). (Pubitemid 30324428)
26. Moreno, C. S. 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. 155, 4313-4321 (1995).
27. Jabrane-Ferrat, N., Nekrep, N., Tosi, G., Esserman, L. & Peterlin, B. M. MHC class II enhanceosome: how is the class II transactivator recruited to DNA-bound activators? Int. Immunol. 15, 467-475 (2003). (Pubitemid 36432399)
28. Clausen, B. E. et al. Residual MHC class II expression on mature dendritic cells and activated B cells in RFX5-deficient mice. Immunity 8, 143-155 (1998). (Pubitemid 28123742)
29. Krawczyk, M. et al. Identification of CIITA regulated genetic module dedicated for antigen presentation. PLoS Genet. 4, e1000058 (2008).
30. O'Keefe, G. M., Nguyen, V. T. & Benveniste, E. N. Class II transactivator and class II MHC gene expression in microglia: modulation by the cytokines TGF-β, IL-4, IL-13 and IL-10. Eur. J. Immunol. 29, 1275-1285 (1999). (Pubitemid 29164174)
31. Muhlethaler-Mottet, A., Otten, L. A., 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. 16, 2851-2860 (1997). (Pubitemid 27226221)
32. Kuenzel, S. et al. The nucleotide-binding oligomerization domain-like receptor NLRC5 is involved in IFN-dependent antiviral immune responses. J. Immunol. 184, 1990-2000 (2010).
33. Neerincx, A. et al. A role for the human nucleotide-binding domain, leucine-rich repeat-containing family member NLRC5 in antiviral responses. J. Biol. Chem. 285, 26223-26232 (2010).
34. Benko, S., Magalhaes, J. G., Philpott, D. J. & Girardin, S. E. NLRC5 limits the activation of inflammatory pathways. J. Immunol. 185, 1681-1691 (2010).
35. Martinon, F. & Tschopp, J. NLRs join TLRs as innate sensors of pathogens. Trends Immunol. 26, 447-454 (2005). (Pubitemid 41008082)
36. Cressman, D. E., Chin, K. C., Taxman, D. J. & Ting, J. P. A defect in the nuclear translocation of CIITA causes a form of type II bare lymphocyte syndrome. Immunity 10, 163-171 (1999). (Pubitemid 29115622)
37. Spilianakis, C., Papamatheakis, J. & Kretsovali, A. Acetylation by PCAF enhances CIITA nuclear accumulation and transactivation of major histocompatibility complex class II genes. Mol. Cell. Biol. 20, 8489-8498 (2000).
38. Cressman, D. E., O'Connor, W. J., Greer, S. F., Zhu, X. S. & Ting, J. P. Mechanisms of nuclear import and export that control the subcellular localization of class II transactivator. J. Immunol. 167, 3626-3634 (2001). (Pubitemid 32910804)
39. Meissner, T. B., Li, A., Liu, Y. J., Gagnon, E. & Kobayashi, K. S. The nucleotide-binding domain of NLRC5 is critical for nuclear import and transactivation activity. Biochem. Biophys. Res. Commun. 418, 786-791 (2012).
40. Muhlethaler-Mottet, A. 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. 279, 40529-40535 (2004). (Pubitemid 39287644)
41. Zhu, X. S. et al. 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. 20, 6051-6061 (2000).
42. Peijnenburg, A. et al. Discoordinate expression of invariant chain and MHC class II genes in class II transactivator-transfected fibroblasts defective for RFX5. J. Immunol. 163, 794-801 (1999). (Pubitemid 29328087)
43. Cui, J. et al. NLRC5 negatively regulates the NF-κB and type I interferon signaling pathways. Cell 141, 483-496 (2010).
44. Davis, B. K. et al. Cutting edge: NLRC5-dependent ctivation of the inflammasome. J. Immunol. 186, 1333-1337 (2011).
45. Kumar, H. et al. NLRC5 deficiency does not influence cytokine induction by virus and bacteria infections. J. Immunol. 186, 994-1000 (2011).
46. Meissner, T. B., Li, A. & Kobayashi, K. S. NLRC5: a newly discovered MHC class I transactivator (CITA). Microbes Infect. 14, 477-484 (2012).
47. Nickerson, K. et al. Dendritic cell-specific MHC class II transactivator contains a caspase recruitment domain that confers potent transactivation activity. J. Biol. Chem. 276, 19089-19093 (2001).
48. Steimle, V., Siegrist, C. A., Mottet, A., Lisowska-Grospierre, B. & Mach, B. Regulation of MHC class II expression by interferon-γ mediated by the transactivator gene CIITA. Science 265, 106-109 (1994). (Pubitemid 24253184)
49. Chang, C. H., Fontes, J. D., Peterlin, M. & Flavell, R. A. Class II transactivator (CIITA) is sufficient for the inducible expression of major histocompatibility complex class II genes. J. Exp. Med. 180, 1367-1374 (1994). (Pubitemid 24289610)
50. Muhlethaler-Mottet, A., Di Berardino, W., Otten, L. A. & Mach, B. Activation of the MHC class II transactivator CIITA by interferon-γ requires cooperative interaction between Stat1 and USF-1. Immunity 8, 157-166 (1998). (Pubitemid 28123743)
51. Piskurich, J. F., Wang, Y., Linhoff, M. W., White, L. C. & Ting, J. P. Identification of distinct regions of 5Ŷ flanking DNA that mediate constitutive, IFN-γ, STAT1, and TGF-β-regulated expression of the class II transactivator gene. J. Immunol. 160, 233-240 (1998). (Pubitemid 28116734)
52. Wright, K. L. et al. CIITA stimulation of transcription factor binding to major histocompatibility complex class II and associated promoters in vivo. Proc. Natl Acad. Sci. USA 95, 6267-6272 (1998). (Pubitemid 28249001)
53. Bewry, N. N., Bolick, S. C., Wright, K. L. & Harton, J. A. GTP-dependent recruitment of CIITA to the class II major histocompatibility complex promoter. J. Biol. Chem. 282, 26178-26184 (2007). (Pubitemid 47443762)