Differential regulation of MHCII genes by PRMT6, via an AT-hook motif of RFX5

Molecular Immunology

Volumn 56, Issue 4, 2013, Pages 390-398

  Stavride, Phoebe ^a,b   Arampatzi, Panagiota ^a,b   Papamatheakis, Joseph ^a,b  

^a INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

Author keywords

AT hook; MHCII expression; MHCII transcription; PRMT6; RFX5

Indexed keywords

HLA DQ ANTIGEN; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PRMT6 PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; REGULATOR PROTEIN; RFX5 PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HLA ANTIGEN CLASS 2; NUCLEAR PROTEIN; PRMT6 PROTEIN, HUMAN; PROTEIN BINDING; RFX5 PROTEIN, HUMAN;

ARTICLE; AT HOOK MOTIF; CONTROLLED STUDY; GENE CONTROL; GENETIC TRANSCRIPTION; METHYLATION; PRIORITY JOURNAL; AMINO ACID SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; TUMOR CELL LINE; WESTERN BLOTTING;

AMINO ACID SEQUENCE; AT-HOOK MOTIFS; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DQ ANTIGENS; HLA-DR ANTIGENS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN-ARGININE N-METHYLTRANSFERASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84881097302     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.05.235     Document Type: Article

References (50)

1. Accolla R.S. Human B cell variants immunoselected against a single Ia antigen subset have lost expression of several Ia antigen subsets. Journal of Experimental Medicine 1983, 157:1053-1058.
2. Arampatzi P., Gialitakis M., Makatounakis T., Papamatheakis J. Gene-specific factors determine mitotic expression and bookmarking via alternate regulatory elements. Nucleic Acids Research 2013, 41:2202-2215.
3. Aravind L., Landsman D. AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Research 1998, 26:4413-4421.
4. Boulanger M.C., Liang C., Russell R.S., Lin R., Bedford M.T., Wainberg M.A., Richard S. Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. Journal of Virology 2005, 79:124-131.
5. Brickey W.J., Wright K.L., Zhu X.S., Ting J.P. Analysis of the defect in IFN-gamma induction of MHC class II genes in G1B cells: identification of a novel and functionally critical leucine-rich motif (62-LYLYLQL-68) in the regulatory factor X 5 transcription factor. Journal of Immunology 1999, 163:6622-6630.
6. Bull M., van Hoef A., Gorski J. Transcription analysis of class II human leukocyte antigen genes from normal and immunodeficient B lymphocytes, using polymerase chain reaction. Molecular and Cellular Biology 1990, 10:3792-3796.
7. Casper J.T., Ash R.A., Kirchner P., Hunter J.B., Havens P.L., Chusid M.J. Successful treatment with an unrelated-donor bone marrow transplant in an HLA-deficient patient with severe combined immune deficiency ("bare lymphocyte syndrome"). Journal of Pediatrics 1990, 116:262-265.
8. Durand B., Sperisen P., Emery P., Barras E., Zufferey M., Mach B., Reith W. RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency. EMBO Journal 1997, 16:1045-1055.
9. El-Andaloussi N., Valovka T., Toueille M., Steinacher R., Focke F., Gehrig P., Covic M., Hassa P.O., Schar P., Hubscher U., Hottiger M.O. Arginine methylation regulates DNA polymerase beta. Molecular Cell 2006, 22:51-62.
10. Emery P., Durand B., Mach B., Reith W. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Research 1996, 24:803-807.
11. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., Pollington J.E., Gavin O.L., Gunasekaran P., Ceric G., Forslund K., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A. The Pfam protein families database. Nucleic Acids Research 2010, 38:D211-D222.
12. Gialitakis M., Arampatzi P., Makatounakis T., Papamatheakis J. Gamma interferon-dependent transcriptional memory via relocalization of a gene locus to PML nuclear bodies. Molecular and Cellular Biology 2010, 30:2046-2056.
13. Guccione E., Bassi C., Casadio F., Martinato F., Cesaroni M., Schuchlautz H., Luscher B., Amati B. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 2007, 449:933-937.
14. Huth J.R., Bewley C.A., Nissen M.S., Evans J.N., Reeves R., Gronenborn A.M., Clore G.M. The solution structure of an HMG-I(Y)-DNA complex defines a new architectural minor groove binding motif. Natural Structural Biology 1997, 4:657-665.
15. Hyllus D., Stein C., Schnabel K., Schiltz E., Imhof A., Dou Y., Hsieh J., Bauer U.M. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes and Development 2007, 21:3369-3380.
16. Iberg A.N., Espejo A., Cheng D., Kim D., Michaud-Levesque J., Richard S., Bedford M.T. Arginine methylation of the histone H3 tail impedes effector binding. Journal of Biological Chemistry 2008, 283:3006-3010.
17. Invernizzi C.F., Xie B., Frankel F.A., Feldhammer M., Roy B.B., Richard S., Wainberg M.A. Arginine methylation of the HIV-1 nucleocapsid protein results in its diminished function. AIDS 2007, 21:795-805.
18. Invernizzi C.F., Xie B., Richard S., Wainberg M.A. PRMT6 diminishes HIV-1 Rev binding to and export of viral RNA. Retrovirology 2006, 3:93.
19. Kirmizis A., Santos-Rosa H., Penkett C.J., Singer M.A., Vermeulen M., Mann M., Bahler J., Green R.D., Kouzarides T. Arginine methylation at histone H3R2 controls deposition of H3K4 trimethylation. Nature 2007, 449:928-932.
20. Kretsovali A., Spilianakis C., Dimakopoulos A., Makatounakis T., Papamatheakis J. Self-association of class II transactivator correlates with its intracellular localization and transactivation. Journal of Biological Chemistry 2001, 276:32191-32197.
21. Lang P., Stolpa J.C., Freiberg B.A., Crawford F., Kappler J., Kupfer A., Cambier J.C. TCR-induced transmembrane signaling by peptide/MHC class II via associated Ig-alpha/beta dimers. Science 2001, 291:1537-1540.
22. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
23. Le Clerc S., Limou S., Coulonges C., Carpentier W., Dina C., Taing L., Delaneau O., Labib T., Sladek R., Deveau C., Guillemain H., Ratsimandresy R., Montes M., Spadoni J.L., Therwath A., Schachter F., Matsuda F., Gut I., Lelievre J.D., Levy Y., Froguel P., Delfraissy J.F., Hercberg S., Zagury J.F. Genomewide association study of a rapid progression cohort identifies new susceptibility alleles for AIDS (ANRS Genomewide Association Study 03). Journal of Infectious Diseases 2009, 200:1194-1201.
24. LeibundGut-Landmann S., Waldburger J.M., Krawczyk M., Otten L.A., Suter T., Fontana A., Acha-Orbea H., Reith W. Mini-review: specificity and expression of CIITA, the master regulator of MHC class II genes. European Journal of Immunology 2004, 34:1513-1525.
25. Leveille C., Castaigne J.G., Charron D., Al-Daccak R. MHC class II isotype-specific signaling complex on human B cells. European Journal of Immunology 2002, 32:2282-2291.
26. Long A.B., Ferguson A.M., Majumder P., Nagarajan U.M., Boss J.M. Conserved residues of the bare lymphocyte syndrome transcription factor RFXAP determine coordinate MHC class II expression. Molecular Immunology 2006, 43:395-409.
27. MacGregor G.R., Caskey C.T. Construction of plasmids that express E. coli beta-galactosidase in mammalian cells. Nucleic Acids Research 1989, 17:2365.
28. Mantovani R., Pessara U., Tronche F., Li X.Y., Knapp A.M., Pasquali J.L., Benoist C., Mathis D. Monoclonal antibodies to NF-Y define its function in MHC class II and albumin gene transcription. EMBO Journal 1992, 11:3315-3322.
29. Masternak K., Barras E., Zufferey M., Conrad B., Corthals G., Aebersold R., Sanchez J.C., Hochstrasser D.F., Mach B., Reith W. A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients. Nature Genetics 1998, 20:273-277.
30. Matsuoka T., Tabata H., Matsushita S. Monocytes are differentially activated through HLA-DR-DQ, and -DP molecules via mitogen-activated protein kinases. Journal of Immunology 2001, 166:2202-2208.
31. Miranda T.B., Webb K.J., Edberg D.D., Reeves R., Clarke S. Protein arginine methyltransferase 6 specifically methylates the nonhistone chromatin protein HMGA1a. Biochemical and Biophysical Research Communications 2005, 336:831-835.
32. Moreno C.S., Beresford G.W., Louis-Plence P., Morris A.C., Boss J.M. CREB regulates MHC class II expression in a CIITA-dependent manner. Immunity 1999, 10:143-151.
33. Nagarajan U.M., Long A.B., Harreman M.T., Corbett A.H., Boss J.M. A hierarchy of nuclear localization signals governs the import of the regulatory factor X complex subunits and MHC class II expression. Journal of Immunology 2004, 173:410-419.
34. Nagarajan U.M., Louis-Plence P., DeSandro A., Nilsen R., Bushey A., Boss J.M. RFX-B is the gene responsible for the most common cause of the bare lymphocyte syndrome, an MHC class II immunodeficiency. Immunity 1999, 10:153-162.
35. Parry R.V., Ward S.G. Protein arginine methylation: a new handle on T lymphocytes?. Trends in Immunology 2010, 31:164-169.
36. Peretti M., Villard J., Barras E., Zufferey M., Reith W. Expression of the three human major histocompatibility complex class II isotypes exhibits a differential dependence on the transcription factor RFXAP. Molecular and Cellular Biology 2001, 21:5699-5709.
37. Reeves R. Molecular biology of HMGA proteins: hubs of nuclear function. Gene 2001, 277:63-81.
38. Reith W., Mach B. The bare lymphocyte syndrome and the regulation of MHC expression. Annual Review of Immunology 2001, 19:331-373.
39. Schneider R., Bannister A.J. Protein N-methyltransferase assays in the study of gene transcription. Methods 2002, 26:226-232.
40. Sgarra R., Lee J., Tessari M.A., Altamura S., Spolaore B., Giancotti V., Bedford M.T., Manfioletti G. The AT-hook of the chromatin architectural transcription factor high mobility group A1a is arginine-methylated by protein arginine methyltransferase 6. Journal of Biological Chemistry 2006, 281:3764-3772.
41. Steimle V., Durand B., Barras E., Zufferey M., Hadam M.R., Mach B., Reith W. A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). Genes and Development 1995, 9:1021-1032.
42. 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 1993, 75:135-146.
43. Ting J.P., Trowsdale J. Genetic control of MHC class II expression. Cell 2002, 109(Suppl.):S21-S33.
44. Vilen B.J., Cogswell J.P., Ting J.P. Stereospecific alignment of the X and Y elements is required for major histocompatibility complex class II DRA promoter function. Molecular and Cellular Biology 1991, 11:2406-2415.
45. Vilen B.J., Penta J.F., Ting J.P. Structural constraints within a trimeric transcriptional regulatory region. Constitutive and interferon-gamma-inducible expression of the HLA-DRA gene. Journal of Biological Chemistry 1992, 267:23728-23734.
46. Xie B., Invernizzi C.F., Richard S., Wainberg M.A. Arginine methylation of the human immunodeficiency virus type 1 Tat protein by PRMT6 negatively affects Tat Interactions with both cyclin T1 and the Tat transactivation region. Journal of Virology 2007, 81:4226-4234.
47. Yoshimatsu M., Toyokawa G., Hayami S., Unoki M., Tsunoda T., Field H.I., Kelly J.D., Neal D.E., Maehara Y., Ponder B.A., Nakamura Y., Hamamoto R. Dysregulation of PRMT1 and PRMT6 Type I arginine methyltransferases, is involved in various types of human cancers. International Journal of Cancer 2011, 128:562-573.
48. Zhang Q., Wang Y. High mobility group proteins and their post-translational modifications. Biochimica et Biophysica Acta 2008, 1784:1159-1166.
49. Zhang Q., Wang Y. HMG modifications and nuclear function. Biochimica et Biophysica Acta 2010, 1799:28-36.
50. Zou Y., Webb K., Perna A.D., Zhang Q., Clarke S., Wang Y. A mass spectrometric study on the in vitro methylation of HMGA1a and HMGA1b proteins by PRMTs: methylation specificity, the effect of binding to AT-rich duplex DNA, and the effect of C-terminal phosphorylation. Biochemistry 2007, 46:7896-7906.