DNA-PK contributes to the phosphorylation of AIRE: Importance in transcriptional activity

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 1, 2008, Pages 74-83

  Liiv, Ingrid ^a   Rebane, Ana ^a   Org, Tõnis ^a   Saare, Mario ^a   Maslovskaja, Julia ^a   Kisand, Kai ^a   Juronen, Erkki ^a   Valmu, Leena ^b   Bottomley, Matthew James ^c   Kalkkinen, Nisse ^b   Peterson, Pärt ^a,d  

^a UNIVERSITY OF TARTU   (Estonia)

^b UNIVERSITY OF HELSINKI   (Finland)

^c IRBM   (Italy)

^d UNIVERSITY OF TAMPERE   (Finland)

Author keywords

APECED; HSR domain; PHD finger; Phosphorylation

Indexed keywords

AUTOIMMUNE REGULATOR PROTEIN; DNA DEPENDENT PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ASSAY; CELL POPULATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME SUBUNIT; IMMUNOPRECIPITATION; IN VITRO STUDY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; TRANSACTIVATION; TRANSCRIPTION INITIATION;

AMINO ACID MOTIFS; ANTIGENS, NUCLEAR; CELL LINE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; EPITHELIAL CELLS; HUMANS; MASS SPECTROMETRY; MUTATION; PHOSPHORYLATION; PHOSPHOSERINE; PHOSPHOTHREONINE; PROTEIN BINDING; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

EID: 38049026826     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.09.003     Document Type: Article

References (51)

1. Finnish-German Consortium. An autoimmune disease, APECED, caused by mutations in a novel gene featuring two PHD-type zinc-finger domains. Nat. Genet. 17 (1997) 399-403
2. Nagamine K., Peterson P., Scott H.S., Kudoh J., Minoshima S., Heino M., Krohn K.J., Lalioti M.D., Mullis P.E., Antonarakis S.E., Kawasaki K., Asakawa S., Ito F., and Shimizu N. Positional cloning of the APECED gene. Nat. Genet. 17 (1997) 393-398
3. Heino M., Peterson P., Kudoh J., Nagamine K., Lagerstedt A., Ovod V., Ranki A., Rantala I., Nieminen M., Tuukkanen J., Scott H.S., Antonarakis S.E., Shimizu N., and Krohn K. Autoimmune regulator is expressed in the cells regulating immune tolerance in thymus medulla. Biochem. Biophys. Res. Commun. 257 (1999) 821-825
4. Kumar P.G., Laloraya M., Wang C.Y., Ruan Q.G., Davoodi-Semiromi A., Kao K.J., and She J.X. The autoimmune regulator (AIRE) is a DNA-binding protein. J. Biol. Chem. 276 (2001) 41357-41364
5. Pitkanen J., Doucas V., Sternsdorf T., Nakajima T., Aratani S., Jensen K., Will H., Vahamurto P., Ollila J., Vihinen M., Scott H.S., Antonarakis S.E., Kudoh J., Shimizu N., Krohn K., and Peterson P. The autoimmune regulator protein has transcriptional transactivating properties and interacts with the common coactivator CREB-binding protein. J. Biol. Chem. 275 (2000) 16802-16809
6. Bottomley M.J., Collard M.W., Huggenvik J.I., Liu Z., Gibson T.J., and Sattler M. The SAND domain structure defines a novel DNA-binding fold in transcriptional regulation. Nat. Struct. Biol. 8 (2001) 626-633
7. Bienz M. The PHD finger, a nuclear protein-interaction domain. Trends Biochem. Sci. 31 (2006) 35-40
8. Gozani O., Karuman P., Jones D.R., Ivanov D., Cha J., Lugovskoy A.A., Baird C.L., Zhu H., Field S.J., Lessnick S.L., Villasenor J., Mehrotra B., Chen J., Rao V.R., Brugge J.S., Ferguson C.G., Payrastre B., Myszka D.G., Cantley L.C., Wagner G., Divecha N., Prestwich G.D., and Yuan J. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114 (2003) 99-111
9. Schultz D.C., Friedman J.R., and Rauscher III F.J. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2alpha subunit of NuRD. Genes Dev. 15 (2001) 428-443
10. Shi X., Hong T., Walter K.L., Ewalt M., Michishita E., Hung T., Carney D., Pena P., Lan F., Kaadige M.R., Lacoste N., Cayrou C., Davrazou F., Saha A., Cairns B.R., Ayer D.E., Kutateladze T.G., Shi Y., Cote J., Chua K.F., and Gozani O. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442 (2006) 96-99
11. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., Wu C., and Allis C.D. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442 (2006) 86-90
12. Bottomley M.J., Stier G., Pennacchini D., Legube G., Simon B., Akhtar A., Sattler M., and Musco G. NMR structure of the first PHD finger of autoimmune regulator protein (AIRE1). Insights into autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy (APECED) disease. J. Biol. Chem. 280 (2005) 11505-11512
13. Björses P., Halonen M., Palvimo J.J., Kolmer M., Aaltonen J., Ellonen P., Perheentupa J., Ulmanen I., and Peltonen L. Mutations in the AIRE gene: effects on subcellular location and transactivation function of the autoimmune polyendocrinopathy-candidiasis-ectodermal dystrophy protein. Am. J. Hum. Genet. 66 (2000) 378-392
14. Pitkanen J., Vahamurto P., Krohn K., and Peterson P. Subcellular localization of the autoimmune regulator protein. Characterization of nuclear targeting and transcriptional activation domain. J. Biol. Chem. 276 (2001) 19597-19602
15. Halonen M., Kangas H., Ruppell T., Ilmarinen T., Ollila J., Kolmer M., Vihinen M., Palvimo J., Saarela J., Ulmanen I., and Eskelin P. APECED-causing mutations in AIRE reveal the functional domains of the protein. Human Mutat. 23 (2004) 245-257
16. Pitkanen J., Rebane A., Rowell J., Murumagi A., Strobel P., Moll K., Saare M., Heikkila J., Doucas V., Marx A., and Peterson P. Cooperative activation of transcription by autoimmune regulator AIRE and CBP. Biochem. Biophys. Res. Commun. 333 (2005) 944-953
17. Smith G.C., and Jackson S.P. The DNA-dependent protein kinase. Genes Dev. 13 (1999) 916-934
18. Zhang S., Schlott B., Gorlach M., and Grosse F. DNA-dependent protein kinase (DNA-PK) phosphorylates nuclear DNA helicase II/RNA helicase A and hnRNP proteins in an RNA-dependent manner. Nucleic Acids Res. 32 (2004) 1-10
19. Koike M. Dimerization, translocation and localization of Ku70 and Ku80 proteins. J. Radiat. Res. 43 (2002) 223-236
20. Giffin W., Kwast-Welfeld J., Rodda D.J., Prefontaine G.G., Traykova-Andonova M., Zhang Y., Weigel N.L., Lefebvre Y.A., and Hache R.J. Sequence-specific DNA binding and transcription factor phosphorylation by Ku Autoantigen/DNA-dependent protein kinase. Phosphorylation of Ser-527 of the rat glucocorticoid receptor. J. Biol. Chem. 272 (1997) 5647-5658
21. Sartorius C.A., Takimoto G.S., Richer J.K., Tung L., and Horwitz K.B. Association of the Ku autoantigen/DNA-dependent protein kinase holoenzyme and poly(ADP-ribose) polymerase with the DNA binding domain of progesterone receptors. J. Mol. Endocrinol. 24 (2000) 165-182
22. Mayeur G.L., Kung W.J., Martinez A., Izumiya C., Chen D.J., and Kung H.J. Ku is a novel transcriptional recycling coactivator of the androgen receptor in prostate cancer cells. J. Biol. Chem. 280 (2005) 10827-10833
23. Giffin W., Gong W., Schild-Poulter C., and Hache R.J. Ku antigen-DNA conformation determines the activation of DNA-dependent protein kinase and DNA sequence-directed repression of mouse mammary tumor virus transcription. Mol. Cell. Biol. 19 (1999) 4065-4078
24. Xu P., LaVallee P.A., Lin J.J., and Hoidal J.R. Characterization of proteins binding to E-box/Ku86 sites and function of Ku86 in transcriptional regulation of the human xanthine oxidoreductase gene. J. Biol. Chem. 279 (2004) 16057-16063
25. Lee K.A.W., Zerivitz K., and Akusjärvi G. Cell Biology: A Laboratory Handbook, Academic Press. In: celis J.E. (Ed) (1994) 668-673
26. Lai J.S., and Herr W. Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 6958-6962
27. Obenauer J.C., Cantley L.C., and Yaffe M.B. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31 (2003) 3635-3641
28. Blom N., Gammeltoft S., and Brunak S. Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294 (1999) 1351-1362
29. Kont V., Laan M., Kisand K., Merits A., Scott H.S., and Peterson P. Modulation of Aire regulates the expression of tissue-restricted antigens. Mol. Immunol. 45 (2008) 25-33
30. Hsu H.L., Yannone S.M., and Chen D.J. Defining interactions between DNA-PK and ligase IV/XRCC4. DNA Repair (Amst) 1 (2002) 225-235
31. Nguyen T.N., and Goodrich J.A. Protein-protein interaction assays: eliminating false positive interactions. Nat. Methods 3 (2006) 135-139
32. Lees-Miller S.P., Sakaguchi K., Ullrich S.J., Appella E., and Anderson C.W. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12 (1992) 5041-5049
33. Ishida-Yamamoto A., Kartasova T., Matsuo S., Kuroki T., and Iizuka H. Involucrin and SPRR are synthesized sequentially in differentiating cultured epidermal cells. J. Invest. Dermatol. 108 (1997) 12-16
34. Derbinski J., Gabler J., Brors B., Tierling S., Jonnakuty S., Hergenhahn M., Peltonen L., Walter J., and Kyewski B. Promiscuous gene expression in thymic epithelial cells is regulated at multiple levels. J. Exp. Med. 202 (2005) 33-45
35. Ramsey C., Bukrinsky A., and Peltonen L. Systematic mutagenesis of the functional domains of AIRE reveals their role in intracellular targeting. Hum. Mol. Genet. 11 (2002) 3299-3308
36. Gottlieb T.M., and Jackson S.P. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72 (1993) 131-142
37. Hammarsten O., and Chu G. DNA-dependent protein kinase: DNA binding and activation in the absence of Ku. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 525-530
38. Torrance H., Giffin W., Rodda D.J., Pope L., and Hache R.J. Sequence-specific binding of Ku autoantigen to single-stranded DNA. J. Biol. Chem. 273 (1998) 20810-20819
39. Park E.J., Chan D.W., Park J.H., Oettinger M.A., and Kwon J. DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res. 31 (2003) 6819-6827
40. Galande S., and Kohwi-Shigematsu T. Poly(ADP-ribose) polymerase and Ku autoantigen form a complex and synergistically bind to matrix attachment sequences. J. Biol. Chem. 274 (1999) 20521-20528
41. Lomberk G., Bensi D., Fernandez-Zapico M.E., and Urrutia R. Evidence for the existence of an HP1-mediated subcode within the histone code. Nat. Cell Biol. 8 (2006) 407-415
42. Mo X., and Dynan W.S. Subnuclear localization of Ku protein: functional association with RNA polymerase II elongation sites. Mol. Cell. Biol. 22 (2002) 8088-8099
43. Akiyoshi H., Hatakeyama S., Pitkanen J., Mouri Y., Doucas V., Kudoh J., Tsurugaya K., Uchida D., Matsushima A., Oshikawa K., Nakayama K.I., Shimizu N., Peterson P., and Matsumoto M. Subcellular expression of autoimmune regulator is organized in a spatiotemporal manner. J. Biol. Chem. 279 (2004) 33984-33991
44. Johnnidis J.B., Venanzi E.S., Taxman D.J., Ting J.P., Benoist C.O., and Mathis D.J. Chromosomal clustering of genes controlled by the aire transcription factor. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 7233-7238
45. Karpova A.Y., Trost M., Murray J.M., Cantley L.C., and Howley P.M. Interferon regulatory factor-3 is an in vivo target of DNA-PK. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 2818-2823
46. Lebrun P., Montminy M.R., and Van Obberghen E. Regulation of the pancreatic duodenal homeobox-1 protein by DNA-dependent protein kinase. J. Biol. Chem. 280 (2005) 38203-38210
47. Schild-Poulter C., Shih A., Yarymowich N.C., and Hache R.J. Down-regulation of histone H2B by DNA-dependent protein kinase in response to DNA damage through modulation of octamer transcription factor 1. Cancer Res. 63 (2003) 7197-7205
48. Anderson M.S., Venanzi E.S., Klein L., Chen Z., Berzins S.P., Turley S.J., von Boehmer H., Bronson R., Dierich A., Benoist C., and Mathis D. Projection of an immunological self shadow within the thymus by the Aire protein. Science 298 (2002) 1395-1401
49. Liston A., Lesage S., Wilson J., Peltonen L., and Goodnow C.C. Aire regulates negative selection of organ-specific T cells. Nat. Immunol. 4 (2003) 350-354
50. Rossi S.W., Kim M.Y., Leibbrandt A., Parnell S.M., Jenkinson W.E., Glanville S.H., McConnell F.M., Scott H.S., Penninger J.M., Jenkinson E.J., Lane P.J., and Anderson G. RANK signals from CD4(+)3(-) inducer cells regulate development of Aire-expressing epithelial cells in the thymic medulla. J. Exp. Med. 204 (2007) 1267-1272
51. Wada T., Nakashima T., Hiroshi N., and Penninger J.M. RANKL-RANK signaling in osteoclastogenesis and bone disease. Trends Mol. Med. 12 (2006) 17-25