The RNA-binding E3 ubiquitin ligase MEX-3C links ubiquitination with MHC-I mRNA degradation

EMBO Journal

Volumn 31, Issue 17, 2012, Pages 3596-3606

  Cano, Florencia ^a   Bye, Helen ^a   Duncan, Lidia M ^a   Buchet Poyau, Karine ^b   Billaud, Marc ^b   Wills, Mark R ^c   Lehner, Paul J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUT ALBERT BONNIOT   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

30UTR; antigen presentation; HLA A; MHC class I; mRNA decay; NK cells; ubiquitin E3 ligase

Indexed keywords

BETA ACTIN; IMMUNOGLOBULIN RECEPTOR; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; PROTEIN MEX 3C; RNA BINDING PROTEIN; SMALL INTERFERING RNA; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADAPTIVE IMMUNITY; ALLOTYPE; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; GENE; HLA A2 GENE; HUMAN; HUMAN CELL; INNATE IMMUNITY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; RNA DEGRADATION; TRANSCRIPTION REGULATION; UBIQUITINATION;

CELL LINE; HEK293 CELLS; HLA-A2 ANTIGEN; HUMANS; KILLER CELLS, NATURAL; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; UBIQUITINATION;

EID: 84866059126     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.218     Document Type: Article

References (30)

1. Buchet-Poyau K, Courchet J, Le Hir H, Séraphin B, Scoazec JY, Duret L, Domon-Dell C, Freund JN, Billaud M (2007) Identification and characterization of human Mex-3 proteins, a novel family of evolutionarily conserved RNA-binding proteins differentially localized to processing bodies. Nucleic Acids Res 35: 1289-1300
2. Cano F, Miranda-Saavedra D, Lehner PJ (2010) RNA-binding E3 ubiquitin ligases: novel players in nucleic acid regulation. Biochem Soc Trans 38: 1621-1626
3. Chalifour A, Scarpellino L, Back J, Brodin P, Devèvre E, Gros F, Lévy F, Leclercq G, Höglund P, Beermann F, Held W (2009) A Role for cis interaction between the inhibitory Ly49A receptor and MHC class I for natural killer cell education. Immunity 30: 337-347
4. Draper BW, Mello CC, Bowerman B, Hardin J, Priess JR (1996) MEX-3 is a KH domain protein that regulates blastomere identity in early C. elegans embryos. Cell 87: 205-216
5. Duncan LM, Nathan JA, Lehner PJ (2010) Stabilization of an E3 ligase-E2-ubiquitin complex increases cell surface MHC class I expression. J Immunol 184: 6978-6985
6. Ferrone S, Marincola FM (1995) Loss of HLA class I antigens by melanoma cells: molecular mechanisms, functional significance and clinical relevance. Immunol Today 16: 487-494
7. Glasmacher E, Hoefig KP, Vogel KU, Rath N, Du L, Wolf C, Kremmer E, Wang X, Heissmeyer V (2010) Roquin binds inducible costimulator mRNA and effectors of mRNA decay to induce microRNA-independent post-transcriptional repression. Nat Immunol 11: 725-733
8. Gobin SJ, van den Elsen PJ (2001) Locus-specific regulation of HLA-A and HLA-B expression is not determined by nucleotide variation in the X2 box promoter element. Blood 97: 1518-1521
9. Held W, Mariuzza RA (2008) Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat Rev Immunol 8: 269-278
10. Holmes TD, El-Sherbiny YM, Davison A, Clough SL, Blair GE, Cook GP (2011) A human NK cell activation/inhibition threshold allows small changes in the target cell surface phenotype to dramatically alter susceptibility to NK cells. J Immunol 186: 1538-1545
11. Hunter CP, Kenyon C (1996) Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87: 217-226
12. Kageshita T, Wang Z, Calorini L, Yoshii A, Kimura T, Ono T, Gattoni-Celli S, Ferrone S (1993) Selective loss of human leukocyte class I allospecificities and staining of melanoma cells by monoclonal antibodies recognizing monomorphic determinants of class I human leukocyte antigens. Cancer Res 53: 3349-3354
13. Kulkarni S, Savan R, Qi Y, Gao X, Yuki Y, Bass SE, Martin MP, Hunt P, Deeks SG, Telenti A, Pereyra F, Goldstein D, Wolinsky S, Walker B, Young HA, Carrington M (2011) Differential microRNA regulation of HLA-C expression and its association with HIV control. Nature 472: 495-498
14. Kurnick JT, Ramirez-Montagut T, Boyle LA, Andrews DM, Pandolfi F, Durda PJ, Butera D, Dunn IS, Benson EM, Gobin SJ, van den Elsen PJ (2001) A novel autocrine pathway of tumor escape from immune recognition: melanoma cell lines produce a soluble protein that diminishes expression of the gene encoding the melanocyte lineage melan-A/MART-1 antigen through down-modulation of its promoter. J Immunol 167: 1204-1211
15. Laroia G, Sarkar B, Schneider RJ (2002) Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs. Proc Nat Acad Sci USA 99: 1842-1846
16. McCutcheon JA, Gumperz J, Smith KD, Lutz CT, Parham P (1995) Low HLA-C expression at cell surfaces correlates with increased turnover of heavy chain mRNA. J Exp Med 181: 2085-2095
17. Mühlemann O, Lykke-Andersen J (2010) How and where are nonsense mRNAs degraded in mammalian cells? RNA Biol 7: 28-32
18. Nathan JA, Sengupta S, Wood SA, Admon A, Markson G, Sanderson C, Lehner PJ (2008) The ubiquitin E3 ligase MARCH7 is differentially regulated by the deubiquitylating enzymes USP7 and USP9X. Traffic 9: 1130-1145
19. Parham P (2005) MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5: 201-214
20. Randow F, Lehner PJ (2009) Viral avoidance and exploitation of the ubiquitin system. Nat Cell Biol 11: 527-534
21. Stagg HR, Thomas M, van den Boomen D, Wiertz EJ, Drabkin HA, Gemmill RM, Lehner PJ (2009) The TRC8 E3 ligase ubiquitinates MHC class I molecules before dislocation from the ER. J Cell Biol 186: 685-692
22. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, Hill KM, Yu D, Domaschenz H, Whittle B, Lambe T, Roberts IS, Copley RR, Bell JI, Cornall RJ, Goodnow CC (2005) A RING-type ubiqui-tin ligase family member required to repress follicular helper T cells and autoimmunity. Nature 435: 452-458
23. Wang Z, Marincola FM, Rivoltini L, Parmiani G, Ferrone S (1999) Selective histocompatibility leukocyte antigen (HLA)-A2 loss caused by aberrant pre-mRNA splicing in 624MEL28 melanoma cells. J Exp Med 190: 205-215
24. Wearsch PA, Cresswell P (2008) The quality control of MHC class I peptide loading. Curr Opin Cell Biol 20: 624-631
25. Weekes MP, Antrobus R, Lill JR, Duncan LM, Hör S, Lehner PJ (2010) Comparative analysis of techniques to purify plasma membrane proteins. J Biomol Tech 21: 108-115
26. Weinstock J, Wu J, Cao P, Kingsbury WD, McDermott JL, Kodrasov MP, McKelvey DM, Kumar KGS, Goldenberg SJ, Mattern MR, Nicholson B (2012) Selective dual inhibitors of the cancer-related deubiquitylating proteases USP7 and USP47. Med Chem Lett (In press)
27. Wills MR, Ashiru O, Reeves MB, Okecha G, Trowsdale J, Tomasec P, Wilkinson GW, Sinclair J, Sissons JG (2005) Human cytomegalo-virus encodes an MHC class I-like molecule (UL142) that functions to inhibit NK cell lysis. J Immunol 175: 7457-7465
28. Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362
29. Yu D, Tan AH, Hu X, Athanasopoulos V, Simpson N, Silva DG, Hutloff A, Giles KM, Leedman PJ, Lam KP, Goodnow CC, Vinuesa CG (2007) Roquin represses autoimmunity by limiting inducible T-cell co-stimulator messenger RNA. Nature 450: 299-303
30. Zamorano R, Suchindran S, Gainer JV (2006) 3'-Untranslated region of the type 2 bradykinin receptor is a potent regulator of gene expression. Am J Physiol Renal Physiol 290: F456-F464