γ-interferon-regulated chaperone governs human lymphocyte antigen class II expression

FASEB Journal

Volumn 26, Issue 1, 2012, Pages 104-116

  Kämper, Nadine ^a   Franken, Sebastian ^a   Temme, Sebastian ^a   Koch, Susanne ^a   Bieber, Thomas ^a   Koch, Norbert ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

BAG6; CIITA; Class II transactivator; HLA class II; HLA class III encoded BAT3

Indexed keywords

B ASSOCIATED TRANSCRIPT 3; CHAPERONE; GAMMA INTERFERON; HLA ANTIGEN CLASS 2; HLA DM ANTIGEN; LYMPHOCYTE ANTIGEN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; CLASS 2 TRANSACTIVATOR GENE; CONTROLLED STUDY; GENE; GENE ACTIVATION; GENE TRANSLOCATION; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; TUMOR CELL LINE;

ANTIGEN-PRESENTING CELLS; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; FIBROBLASTS; GENE EXPRESSION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTERFERON-GAMMA; LUNG; LYMPHOCYTES; MACROPHAGES; MELANOMA; MOLECULAR CHAPERONES; NUCLEAR PROTEINS; PRIMARY CELL CULTURE; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TRANS-ACTIVATORS;

EID: 84855367971     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-189670     Document Type: Article

References (45)

1. Horton, R., Wilming, L., Rand, V., Rand, V., Lovering, R. C., Bruford, E. A., Khodiyar, V. K., Lush, M. J., Povey, S., Talbot, C. C., Wright, M. W., Wain, H. M., Trowsdale, J., Ziegler, A., and Beck, S. (2004) Gene map of the extended human MHC. Nat. Rev. Genet. 5, 889-899 (Pubitemid 39564252)
2. Pai, R. K., Askew, D., Boom, W. H., and Harding, C. V. (2002) Regulation of class II MHC expression in APCs: roles of types I, III and IV class II transactivator. J. Immunol. 169, 1326-1333 (Pubitemid 34809175)
3. Reith, W., LeibundGut-Landmann, S., and Waldburger, J.-M. (2005) Regulation of MHC class II gene expression by the class II transactivator. Nat. Rev. Immunol. 5, 793-806
4. Wright, K. L., and Ting, J. P.-Y. (2006) Epigenetic regulation of HLA class II and CIITA genes. Trends Immunol. 27, 405-412 (Pubitemid 44216195)
5. Beck, S., and Trowsdale, J. (1999) Sequence organization of the class II region of the human MHC. Immunol. Rev. 167, 201-210 (Pubitemid 29178982)
6. Thress, K., Henzel, W., Shillinglaw, W., and Kornbluth, S. (1998) Scythe: a novel reaper-binding apoptotic regulator. EMBO J. 17, 6135-6143 (Pubitemid 28497787)
7. Lehner, B., Semple, J. I., Brown, S. E., Counsell, R., Campbell, R. D., and Sanderson, C. M. (2003) Analysis of a high-throughput yeast two-hybrid system and its use to predict the function of intracellular proteins encoded within the human MHC class III region. Genomics 83, 153-167 (Pubitemid 37518270)
8. Kikukawa, Y., Minami, R., Shimada, M., Kobayashi, M., Tanaka, K., Yokosawa, H., and Kawahara, H. (2005) Unique proteasome subunit Xrpn10c is a specific receptor for the antiapoptotic ubiquitin-like protein Scythe. FEBS J. 272, 6373-6386 (Pubitemid 41815625)
9. Minami, R., Shimada, M., Yokosawa, H., and Kawahara, H. (2007) Scythe regulates apoptosis through modulating ubiquitin-mediated proteolysis of the Xenopus elongation factor XEF1AO. Biochem. J. 405, 495-501 (Pubitemid 47172047)
10. Pogge von Strandmann, E., Simhadri, V. R., von Treskow, B., Sasse, S., Reiners, K. S., Hansen, H. P., Rothe, A., BöB., Simhadri, V. L., Borchmann, McKinnon, P., P.J., Hallek, M., and Engert, A. (2007) Human leukocyte antigen-B-associates transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 27, 965-974 (Pubitemid 350251218)
11. Sasaki, T., Gan, E. C., Wakeham, A., Kornbluth, S., Mak, T. W., and Okada, H. (2007) HLA-B associated transcript 3 (BAG6)/Scythe is essential for p300-mediated acetylation of p53. Genes Dev. 21, 848-861 (Pubitemid 46572363)
12. Kabbage, M., and Dickam, M. B. (2008) The BAG proteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci. 65, 1390-1402
13. Corduan, A., Lecomte, S., Martin, C., Michel, D., and Desmots, F. (2009) Sequential interplay between BAG6 and HSP70 upon heat shock. Cell. Mol. Life Sci. 66, 1998-2004
14. Leznicki, P., Clancy, A., Schwappach, B., and High, S. (2010) Bat3 promotes the membrane integration of tail-anchored proteins. J. Cell Sci. 123, 2170-2178
15. Mariappan, M., Li, X., Stefanovic, A., Sharma, A., Matweja, A., Keenan, R. J., and Hedge, R. S. (2010) A ribosome-associated factor chaperones tail-anchored membrane proteins. Nature 466, 1120-1125
16. Minami, R., Hayakawa, A., Kagawa, H., Yanagi, Y., Yokosawa, H., and Kawahara, H. (2010) BAG6 is essential for selective elimination of defective proteasomal substrates. J. Cell Biol. 190, 637-650
17. Desmots, F., Russel, H. R., Lee, Y., Boyd, K., and McKinnon, P. J. (2005) The reaper-binding protein scythe modulates apoptosis and proliferation during mammalian development. Mol. Cell. Biol. 25, 10329-10337 (Pubitemid 41681958)
18. Watanabe, M., Suzuki, T., Taniguchi, M., and Shinohara, N. (1983) Monoclonal anti-Ia murine alloantibodies crossreactive with the Ia-homologues of other mammalian species including humans. Transplantation 36, 712-718 (Pubitemid 14216288)
19. Lampson, L. A., and Levy, R. (1980) Two populations of la-like molecules on a human B cell line. J. Immunol. 125, 293-299 (Pubitemid 10040437)
20. Barnstable, C. J., Bodmer. W. F., Brown, G., Galfre, G., Milstein, C., Williams, A. F., and Ziegler, A. (1978) Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tool for genetic analysis. Cell 14, 9-20 (Pubitemid 8340429)
21. Wraight, C. J., van Endert, P., Mö, P., Lipp, J., Ling, N. R., MacLennan, I. C., Koch, N., and Moldenhauer, G. (1990) Human major histocompatibility complex class II invariant chain is expressed on the cell surface. J. Biol. Chem. 265, 5787-5792
22. Sanderson, F., Thomas, C., Neefjes, J., and Trowsdale, J. (1996) Association between HLA-DM and HLA-DR in vivo. Immunity. 4, 87-96 (Pubitemid 26054938)
23. Schnappauf, F., Hake, S. B., Camacho Carvajal, M. M., Bontron, S., Lisowska-Grospierre, B., and Steimle, V. (2003) N-terminal destruction signals lead to rapid degradation of the major histocompatibility complex class II transactivator CIITA. Eur. J. Immunol. 33, 2337-2347 (Pubitemid 37010051)
24. Pessara, U., and Koch, N. (1990) Tumor necrosis factor alpha regulates expression of the MHC class II-associated invariant chain by binding of NF-κB-like factor to a promoter element. Mol. Cell. Biol. 10, 4146-4154
25. Temme, S., Eis-Hüer, A.-M., McLellan, A. D., and Koch, N. (2010) The herpes simplex virus-I encoded glycoprotein B diverts HLA-DR into the exosome pathway. J. Immunol. 184, 236-243
26. Neumann, J., Schach, N., and Koch, N. (2001) Glycosylation signals that separate the trimerization from the MHC class II-binding domain control intracellular degradation of invariant chain. J. Biol. Chem. 267, 13469-13475
27. Muhlethaler-Mottet, A., Di, Barardino, W., Otten, L.A., Mach, B. (1998) Activation of the MHC class II transactivator CIITA by interferon γ requires cooperative interaction between Stat1 and USF-1. Immunity 8, 157-166
28. Steimle, V., Siegrist, C., Mottet, A., Lisowska-Grospierre, B., and Mach, B. (1994) Regulation of MHC class II expression by interferon-gamma-mediated by the transactivator gene CIITA. Science 265, 106-109 (Pubitemid 24253184)
29. Cressman, D. E., Chin, K.-C., Taxman, D. J., and Ting, J. P.-Y. (1999) A defect in the nuclear translocation of CIITA causes a form of type II B are lymphocyte syndrome. Immunity 10, 163-171 (Pubitemid 29115622)
30. Krawczyk, M., Seguin-Esteves, Q., Leimgruber, E., Sperisen, P., Schmid, C., Bucher, P., and Reith, W. (2008) Identification of CIITA regulated genetic module dedicated for antigen presentation. PLoS Genet. 4, 1-16
31. Nguyen, P., Bar-Sela, G., Sun, L., Bisht, K.S., Cui, H., Kohn, E., Feinberg, A. P., and Gius, D. (2008) BAT3 and SET1A form a complex with CTCFL/BORIS to modulate H3K4 histone dimethylation and gene expression. Mol. Cell. Biol. 28, 6720-6729
32. Bhat, K. K., Truax, A. D., and Greer, S. F. (2010a) Phosphorylation of degron proximal residues are essential for class II transactivator (CIITA) transactivation and major histocompatibility class II expression. J. Biol. Chem. 285, 25893-25903
33. Cressman, D. E., O'Connor, W. J., Greer, S. F., Zhu, X.-S., and Ting, J.P.-Y. (2001) Mechanisms of nuclear import and export that control the subcellular localization of class II transactivator. J. Immunol. 167, 3626-3634 (Pubitemid 32910804)
34. Camacho-Carvajal, M. M., Klingler, S., Schnappauf, F., Hake, S. B., and Steimle, V. (2004) Importance of class II transactivator leucine-rich repeats for dominant-negative function and nucleo-cytoplasmic transport. Int. Immunol. 16, 65-75 (Pubitemid 38054628)
35. Strambio-De-Castillia, C., Niepel, M., and Rout, M. P. (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat. Rev. Mol. Cell. Biol. 11, 490-498
36. Wagstaff, K. M., and Jans, D. A. (2009) Importins and beyond: nonconventional nuclear transport mechanisms. Traffic 10, 1188-1198
37. Bhat, K. P., Truax, A. D., Brooks, J. K., and Greer, S. F. (2010) Association of the 19S proteosomal ATPases with the ATPase-binding domain of CIITA is essential for CIITA stability and MHC class II expression. Immunol. Cell Biol. 88, 807-816
38. Ensminger, A. W., and Isberg, R. R. (2010) E3 ubiquitin ligase activity and targeting of BAT3 by multiple Legionella pneumophilatranslocated substrates. Infect. Immun. 78, 3905-3919
39. Degli-Esposti, M. A., Abraham, L.J., McCann, V., Spies, T., Christiansen, F. T., and Dawkins, R. L. (1992) Ancestral haplotypes reveal the role of the central MHC in the immunogenetics of IDDM. Immunogenetics 36, 345-356
40. Vandiedonck, C., Beaurain, G., Giraud, M., Hue-Beauvais, C., Eymard, B., Tranchant, C., Gajdos, P., Dausset, J., and Garchon, H. J. (2004) Pleiotropic effects of the 8.1 HLA haplotype in patients with autoimmune myasthenia gravis and thymus hyperplasia. Proc. Natl. Acad. Sci. U. S. A. 101, 15464-15469 (Pubitemid 39441564)
41. Desmots, F., Russel, H. R., Michel, D., and McKinnon, P. J. (2008) Scythe regulates apoptosis inducing factor stability during endoplasmic reticulum stress induced apoptosis. J. Biol. Chem. 283, 3264-3271
42. Wang, Q., Liu, Y., Soetandyo, N., Baek, K., Hedge, R., and Ye, Y. (2011) A ubiquitin ligase-associated chaperone holdase maintains polypeptides in soluble states for proteasome degradation. Mol. Cell 42, 758-770.
43. Hessa, T., Sharma, A., Mariappan, M., Eshleman, H.D., Gutierrez, E., and Hedge, R. (2011) Protein targeting and degradation are coupled for elimination of mislocalized proteins. Nature 475, 394-399.
44. Favaloro, V., Vilardi, F., Schlecht, R., Mayer, M. P., and Dobberstein, B. (2010) Asna1/TRC40-mediated membrane insertion of tail-anchored proteins. J. Cell Sci. 123, 1522-1530
45. Manchen, S. T., and Hubberstey, A. V. (2001) Human scythe contains a functional nuclear localization sequence and remains in the nucleus during staurosporine-induced apoptosis. Biochem. Biophys. Res. Commun. 287, 1075-1082 (Pubitemid 32980561)