The basal transcription complex component TAF3 transduces changes in nuclear phosphoinositides into transcriptional output

Molecular Cell

Volumn 58, Issue 3, 2015, Pages 453-467

  Stijf Bultsma, Yvette ^a,b   Sommer, Lilly ^b   Tauber, Maria ^c   Baalbaki, Mai ^d   Giardoglou, Panagiota ^e   Jones, David R ^b   Gelato, Kathy A ^c   vanPelt, Jason ^e   Shah, Zahid ^a   Rahnamoun, Homa ^f   Toma, Clara ^f   Anderson, Karen E ^g   Hawkins, Philip ^g   Lauberth, Shannon M ^f   Haramis, Anna Pavlina G ^e   Hart, Daniel ^d   Fischle, Wolfgang ^c   Divecha, Nullin ^a,b  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e LEIDEN UNIVERSITY   (Netherlands)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE KINASE MM; MESSENGER RNA; MYOGENIC FACTOR; MYOSIN LIGHT CHAIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PIP4K2B PROTEIN; TAF3 PROTEIN; TATA BINDING PROTEIN ASSOCIATED FACTOR; UNCLASSIFIED DRUG; HISTONE; HOMEODOMAIN PROTEIN; LYSINE; PHOSPHATIDYLINOSITOL PHOSPHATE 4-KINASE; PHOSPHOTRANSFERASE; PROTEIN BINDING; TAF3 PROTEIN, MOUSE; TRANSCRIPTION FACTOR IID;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GENOTYPE; HEMATOPOIESIS; HISTONE METHYLATION; IMMUNOBLOTTING; IN VITRO STUDY; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NONHUMAN; OVERLAPPING GENE; PHENOTYPE; PROMOTER REGION; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; TRANSCRIPTION REGULATION; UPREGULATION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CYTOLOGY; DNA MICROARRAY; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; METHYLATION; MOLECULAR GENETICS; MOUSE; MUTATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; RNA INTERFERENCE; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION PROFILING; HISTONES; HOMEODOMAIN PROTEINS; LYSINE; METHYLATION; MICE; MOLECULAR SEQUENCE DATA; MUTATION; MYOBLASTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHATIDYLINOSITOLS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BINDING; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION FACTOR TFIID; TRANSCRIPTION, GENETIC; ZEBRAFISH;

EID: 84928925874     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.03.009     Document Type: Article

References (59)

1. Asp P., Blum R., Vethantham V., Parisi F., Micsinai M., Cheng J., Bowman C., Kluger Y., Dynlacht B.D. Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc. Natl. Acad. Sci. USA 2011, 108:E149-E158.
2. Bidlingmaier S., Liu B. Interrogating yeast surface-displayed human proteome to identify small molecule-binding proteins. Mol. Cell. Proteomics 2007, 6:2012-2020.
3. Bidlingmaier S., Wang Y., Liu Y., Zhang N., Liu B. Comprehensive analysis of yeast surface displayed cDNA library selection outputs by exon microarray to identify novel protein-ligand interactions. Mol. Cell. Proteomics 2011, 10:005116.
4. Bienz M. The PHD finger, a nuclear protein-interaction domain. Trends Biochem. Sci. 2006, 31:35-40.
5. Blind R.D., Suzawa M., Ingraham H.A. Direct modification and activation of a nuclear receptor-PIP[U+2082] complex by the inositol lipid kinase IPMK. Sci. Signal. 2012, 5:ra44.
6. Boronenkov I.V., Loijens J.C., Umeda M., Anderson R.A. Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing pre-mRNA processing factors. Mol. Biol. Cell 1998, 9:3547-3560.
7. Bultsma Y., Keune W.J., Divecha N. PIP4Kbeta interacts with and modulates nuclear localization of the high-activity PtdIns5P-4-kinase isoform PIP4Kalpha. Biochem. J. 2010, 430:223-235.
8. Burley S.K., Roeder R.G. Biochemistry and structural biology of transcription factor IID (TFIID). Annu. Rev. Biochem. 1996, 65:769-799.
9. Ciruela A., Hinchliffe K.A., Divecha N., Irvine R.F. Nuclear targeting of the beta isoform of type II phosphatidylinositol phosphate kinase (phosphatidylinositol 5-phosphate 4-kinase) by its alpha-helix 7. Biochem. J. 2000, 346:587-591.
10. Clark J., Anderson K.E., Juvin V., Smith T.S., Karpe F., Wakelam M.J., Stephens L.R., Hawkins P.T. Quantification of PtdInsP3 molecular species in cells and tissues by mass spectrometry. Nat. Methods 2011, 8:267-272.
11. Clarke J.H., Letcher A.J., D'santos C.S., Halstead J.R., Irvine R.F., Divecha N. Inositol lipids are regulated during cell cycle progression in the nuclei of murine erythroleukaemia cells. Biochem. J. 2001, 357:905-910.
12. Clarke J.H., Richardson J.P., Hinchliffe K.A., Irvine R.F. Type II PtdInsP kinases: location, regulation and function. Biochem. Soc. Symp. 2007, 74:149-159.
13. Deato M.D., Tjian R. Switching of the core transcription machinery during myogenesis. Genes Dev. 2007, 21:2137-2149.
14. Deato M.D., Tjian R. An unexpected role of TAFs and TRFs in skeletal muscle differentiation: switching core promoter complexes. Cold Spring Harb. Symp. Quant. Biol. 2008, 73:217-225.
15. Deato M.D., Marr M.T., Sottero T., Inouye C., Hu P., Tjian R. MyoD targets TAF3/TRF3 to activate myogenin transcription. Mol. Cell 2008, 32:96-105.
16. Divecha N., Banfić H., Irvine R.F. The polyphosphoinositide cycle exists in the nuclei of Swiss 3T3 cells under the control of a receptor (for IGF-I) in the plasma membrane, and stimulation of the cycle increases nuclear diacylglycerol and apparently induces translocation of protein kinase C to the nucleus. EMBO J. 1991, 10:3207-3214.
17. Divecha N., Letcher A.J., Banfic H.H., Rhee S.G., Irvine R.F. Changes in the components of a nuclear inositide cycle during differentiation in murine erythroleukaemia cells. Biochem. J. 1995, 312:63-67.
18. Elouarrat D., van der Velden Y.U., Jones D.R., Moolenaar W.H., Divecha N., Haramis A.P. Role of phosphatidylinositol 5-phosphate 4-kinase α in zebrafish development. Int. J. Biochem. Cell Biol. 2013, 45:1293-1301.
19. Emerling B.M., Hurov J.B., Poulogiannis G., Tsukazawa K.S., Choo-Wing R., Wulf G.M., Bell E.L., Shim H.S., Lamia K.A., Rameh L.E., et al. Depletion of a putatively druggable class of phosphatidylinositol kinases inhibits growth of p53-null tumors. Cell 2013, 155:844-857.
20. Gelato K.A., Tauber M., Ong M.S., Winter S., Hiragami-Hamada K., Sindlinger J., Lemak A., Bultsma Y., Houliston S., Schwarzer D., et al. Accessibility of different histone H3-binding domains of UHRF1 is allosterically regulated by phosphatidylinositol 5-phosphate. Mol. Cell 2014, 54:905-919.
21. 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., et al. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 2003, 114:99-111.
22. Hart D.O., Santra M.K., Raha T., Green M.R. Selective interaction between Trf3 and Taf3 required for early development and hematopoiesis. Dev. Dyn. 2009, 238:2540-2549.
23. Hochheimer A., Tjian R. Diversified transcription initiation complexes expand promoter selectivity and tissue-specific gene expression. Genes Dev. 2003, 17:1309-1320.
24. Jones D.R., Bultsma Y., Keune W.J., Halstead J.R., Elouarrat D., Mohammed S., Heck A.J., D'Santos C.S., Divecha N. Nuclear PtdIns5P as a transducer of stress signaling: an invivo role for PIP4Kbeta. Mol. Cell 2006, 23:685-695.
25. Jones D.R., Ramirez I.B., Lowe M., Divecha N. Measurement of phosphoinositides in the zebrafish Danio rerio. Nat. Protoc. 2013, 8:1058-1072.
26. Jude J.G., Spencer G.J., Huang X., Somerville T.D., Jones D.R., Divecha N., Somervaille T.C. A targeted knockdown screen of genes coding for phosphoinositide modulators identifies PIP4K2A as required for acute myeloid leukemia cell proliferation and survival. Oncogene 2014.
27. Jungmichel S., Sylvestersen K.B., Choudhary C., Nguyen S., Mann M., Nielsen M.L. Specificity and commonality of the phosphoinositide-binding proteome analyzed by quantitative mass spectrometry. Cell Rep. 2014, 6:578-591.
28. Keune W.J., Sims A.H., Jones D.R., Bultsma Y., Lynch J.T., Jirström K., Landberg G., Divecha N. Low PIP4K2B expression in human breast tumors correlates with reduced patient survival: A role for PIP4K2B in the regulation of E-cadherin expression. Cancer Res. 2013, 73:6913-6925.
29. Lauberth S.M., Bilyeu A.C., Firulli B.A., Kroll K.L., Rauchman M. A phosphomimetic mutation in the Sall1 repression motif disrupts recruitment of the nucleosome remodeling and deacetylase complex and repression of Gbx2. J.Biol. Chem. 2007, 282:34858-34868.
30. Lauberth S.M., Nakayama T., Wu X., Ferris A.L., Tang Z., Hughes S.H., Roeder R.G. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013, 152:1021-1036.
31. Lessard J., Wu J.I., Ranish J.A., Wan M., Winslow M.M., Staahl B.T., Wu H., Aebersold R., Graef I.A., Crabtree G.R. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 2007, 55:201-215.
32. Lewis A.E., Sommer L., Arntzen M.O., Strahm Y., Morrice N.A., Divecha N., D'Santos C.S. Identification of nuclear phosphatidylinositol 4,5-bisphosphate-interactingproteins by neomycin extraction. Mol. Cell. Proteomics 2011, 10:003376.
33. Lindsay Y., McCoull D., Davidson L., Leslie N.R., Fairservice A., Gray A., Lucocq J., Downes C.P. Localization of agonist-sensitive PtdIns(3,4,5)P3 reveals a nuclear pool that is insensitive to PTEN expression. J.Cell Sci. 2006, 119:5160-5168.
34. Liu Z., Scannell D.R., Eisen M.B., Tjian R. Control of embryonic stem cell lineage commitment by core promoter factor, TAF3. Cell 2011, 146:720-731.
35. Lower K.M., Turner G., Kerr B.A., Mathews K.D., Shaw M.A., Gedeon A.K., Schelley S., Hoyme H.E., White S.M., Delatycki M.B., et al. Mutations in PHF6 are associated with Börjeson-Forssman-Lehmann syndrome. Nat. Genet. 2002, 32:661-665.
36. Maffucci T. An introduction to phosphoinositides. Curr. Top. Microbiol. Immunol. 2012, 362:1-42.
37. Maston G.A., Zhu L.J., Chamberlain L., Lin L., Fang M., Green M.R. Non-canonical TAF complexes regulate active promoters in human embryonic stem cells. eLife 2012, 1:e00068.
38. Meijer H.J., Berrie C.P., Iurisci C., Divecha N., Musgrave A., Munnik T. Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem. J. 2001, 360:491-498.
39. Mellman D.L., Gonzales M.L., Song C., Barlow C.A., Wang P., Kendziorski C., Anderson R.A. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 2008, 451:1013-1017.
40. Musselman C.A., Kutateladze T.G. PHD fingers: epigenetic effectors and potential drug targets. Mol. Interv. 2009, 9:314-323.
41. Ndamukong I., Jones D.R., Lapko H., Divecha N., Avramova Z. Phosphatidylinositol 5-phosphate links dehydration stress to the activity of arabidopsis trithorax-like factor ATX1. PLoS ONE 2010, 5:e13396.
42. Pena P.V., Davrazou F., Shi X., Walter K.L., Verkhusha V.V., Gozani O., Zhao R., Kutateladze T.G. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006, 442:100-103.
43. Peña P.V., Davrazou F., Shi X., Walter K.L., Verkhusha V.V., Gozani O., Zhao R., Kutateladze T.G. Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 2006, 442:100-103.
44. Rajakumara E., Wang Z., Ma H., Hu L., Chen H., Lin Y., Guo R., Wu F., Li H., Lan F., et al. PHD finger recognition of unmodified histone H3R2 links UHRF1 to regulation of euchromatic gene expression. Mol. Cell 2011, 43:275-284.
45. Rameh L.E., Tolias K.F., Duckworth B.C., Cantley L.C. A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate. Nature 1997, 390:192-196.
46. Richardson J.P., Wang M., Clarke J.H., Patel K.J., Irvine R.F. Genomic tagging of endogenous type IIbeta phosphatidylinositol 5-phosphate 4-kinase in DT40 cells reveals a nuclear localisation. Cell. Signal. 2007, 19:1309-1314.
47. Shah Z.H., Jones D.R., Sommer L., Foulger R., Bultsma Y., D'Santos C., Divecha N. Nuclear phosphoinositides and their impact on nuclear functions. FEBS J. 2013, 280:6295-6310.
48. Shi X., Hong T., Walter K.L., Ewalt M., Michishita E., Hung T., Carney D., Peña P., Lan F., Kaadige M.R., et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 2006, 442:96-99.
49. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
50. Thomas M.C., Chiang C.M. The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 2006, 41:105-178.
51. van den Bout I., Divecha N. PIP5K-driven PtdIns(4,5)P2 synthesis: regulation and cellular functions. J.Cell Sci. 2009, 122:3837-3850.
52. van Oevelen C., Bowman C., Pellegrino J., Asp P., Cheng J., Parisi F., Micsinai M., Kluger Y., Chu A., Blais A., et al. The mammalian Sin3 proteins are required for muscle development and sarcomere specification. Mol. Cell. Biol. 2010, 30:5686-5697.
53. Van Vlierberghe P., Palomero T., Khiabanian H., Van der Meulen J., Castillo M., Van Roy N., De Moerloose B., Philippé J., González-García S., Toribio M.L., et al. PHF6 mutations in T-cell acute lymphoblastic leukemia. Nat. Genet. 2010, 42:338-342.
54. Varier R.A., Outchkourov N.S., de Graaf P., van Schaik F.M., Ensing H.J., Wang F., Higgins J.M., Kops G.J., Timmers H.T. A phospho/methyl switch at histone H3 regulates TFIID association with mitotic chromosomes. EMBO J. 2010, 29:3967-3978.
55. Vermeulen M., Mulder K.W., Denissov S., Pijnappel W.W., van Schaik F.M., Varier R.A., Baltissen M.P., Stunnenberg H.G., Mann M., Timmers H.T. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007, 131:58-69.
56. Wang M., Bond N.J., Letcher A.J., Richardson J.P., Lilley K.S., Irvine R.F., Clarke J.H. Genomic tagging reveals a random association of endogenous PtdIns5P 4-kinases IIalpha and IIbeta and a partial nuclear localization of the IIalpha isoform. Biochem. J. 2010, 430:215-221.
57. Watt S.A., Kimber W.A., Fleming I.N., Leslie N.R., Downes C.P., Lucocq J.M. Detection of novel intracellular agonist responsive pools of phosphatidylinositol 3,4-bisphosphate using the TAPP1 pleckstrin homology domain in immunoelectron microscopy. Biochem. J. 2004, 377:653-663.
58. Wysocka J., Swigut T., Xiao H., Milne T.A., Kwon S.Y., Landry J., Kauer M., Tackett A.J., Chait B.T., Badenhorst P., et al. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006, 442:86-90.
59. Yoshida N., Yoshida S., Koishi K., Masuda K., Nabeshima Y. Cell heterogeneity upon myogenic differentiation: down-regulation of MyoD and Myf-5 generates 'reserve cells'. J.Cell Sci. 1998, 111:769-779.