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Dynamic Interaction of HDAC1 with a Glucocorticoid Receptor-regulated Gene Is Modulated by the Activity State of the Promoter

Qiu, Yi, Stavreva, Diana A., Luo, Yi, Indrawan, Anindya, Chang, Myron, Hager, Gordon L.·2011·Journal of Biological Chemistry
DOI 10.1074/jbc.m110.185488
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FIGURE1 HDAC1mobilityontheMMTVarraychangesupongeneactivation. A , 3617 cells were transfected with HDAC1-GFP and ChFP-GR in the presence of tetracycline to suppress GFP-GR expression. Arrows indicate HDAC1-GFPandChFP-GRlocalizationontheMMTVarray.Fortranscriptioninduction,cellswere treated with 100 nM dexamethasone ( Dex ) ∼ 24 h after the transfection. B , localization of ChFP-NF1A1.1 to the array independently identified the MMTV promoter structures. C , schematic presentation of the kinetic profile of MMTV transcription rates (1, 9). D , FRAP recovery curves of GFP-tagged HDAC1 at the MMTV array before induction ( black diamonds ), 20-60 min after induction ( red diamonds ), and 2-3 h after induction ( green diamonds ). FRAP recovery for GFP-GR is also presented ( purple open diamonds ). Note that the mobility of GFP-tagged HDAC1 increased dramatically shortly (30-60 min) after dexamethasone treatment ( red diamonds ) compared with the mobility in uninduced cells ( black diamonds ) and then returned ( green diamonds ) to the initial slower mobility after prolonged dexamethasone treatment (120-180 min). The difference between the HDAC1-GFP FRAP recovery curves at the induced, uninduced, and repressed states is statistically highly significant (both p values < 0.001). The data represent means ± S.E. from three independent experiments (n ≥ 15 cells).
FIGURE1 HDAC1mobilityontheMMTVarraychangesupongeneactivation. A , 3617 cells were transfected with HDAC1-GFP and ChFP-GR in the presence of tetracycline to suppress GFP-GR expression. Arrows indicate HDAC1-GFPandChFP-GRlocalizationontheMMTVarray.Fortranscriptioninduction,cellswere treated with 100 nM dexamethasone ( Dex ) ∼ 24 h after the transfection. B , localization of ChFP-NF1A1.1 to the array independently identified the MMTV promoter structures. C , schematic presentation of the kinetic profile of MMTV transcription rates (1, 9). D , FRAP recovery curves of GFP-tagged HDAC1 at the MMTV array before induction ( black diamonds ), 20-60 min after induction ( red diamonds ), and 2-3 h after induction ( green diamonds ). FRAP recovery for GFP-GR is also presented ( purple open diamonds ). Note that the mobility of GFP-tagged HDAC1 increased dramatically shortly (30-60 min) after dexamethasone treatment ( red diamonds ) compared with the mobility in uninduced cells ( black diamonds ) and then returned ( green diamonds ) to the initial slower mobility after prolonged dexamethasone treatment (120-180 min). The difference between the HDAC1-GFP FRAP recovery curves at the induced, uninduced, and repressed states is statistically highly significant (both p values < 0.001). The data represent means ± S.E. from three independent experiments (n ≥ 15 cells).CC-BY · From the PDF
FIGURE2 HDAC1modificationssignificantly change HDAC1 mobility. A , FRAP analysis of the GFP-tagged HDAC1 6R mutant at the MMTV array before and after dexamethasone induction. The lysine-to-arginine mutant of HDAC1, which mimics unmodified HDAC1, exhibited accelerated mobility identical to the mobility of wild-type HDAC1 at early time points (30-60 min) upon dexamethasone treatment. The mobility did not change throughout the induction cycle. B , the GFP-tagged HDAC1 6R mutant was enriched at the MMTV locus marked by ChFP-NF1A1.1 in both induced and uninduced cells. Dex , dexamethasone. C , FRAP analysis of the GFP-tagged HDAC1 6Q mutant at the MMTV array before and after dexamethasone induction. The lysine-to-glutamine mutant of HDAC1,whichmimicsacetylatedHDAC1,exhibitedretardedmobilityidenticaltothemobilityofwild-typeHDAC1intheuninducedstateoratlatertimepoints (60-120min)upondexamethasonetreatment.Themobilitydidnotchangethroughouttheinductioncycle. D , the GFP-tagged HDAC1 6Q mutant colocalized with ChFP-NF1A1.1 at the array locus in both induced and uninduced cells. The data are means ± S.E. from three independent experiments (n ≥ 15 cells).
FIGURE2 HDAC1modificationssignificantly change HDAC1 mobility. A , FRAP analysis of the GFP-tagged HDAC1 6R mutant at the MMTV array before and after dexamethasone induction. The lysine-to-arginine mutant of HDAC1, which mimics unmodified HDAC1, exhibited accelerated mobility identical to the mobility of wild-type HDAC1 at early time points (30-60 min) upon dexamethasone treatment. The mobility did not change throughout the induction cycle. B , the GFP-tagged HDAC1 6R mutant was enriched at the MMTV locus marked by ChFP-NF1A1.1 in both induced and uninduced cells. Dex , dexamethasone. C , FRAP analysis of the GFP-tagged HDAC1 6Q mutant at the MMTV array before and after dexamethasone induction. The lysine-to-glutamine mutant of HDAC1,whichmimicsacetylatedHDAC1,exhibitedretardedmobilityidenticaltothemobilityofwild-typeHDAC1intheuninducedstateoratlatertimepoints (60-120min)upondexamethasonetreatment.Themobilitydidnotchangethroughouttheinductioncycle. D , the GFP-tagged HDAC1 6Q mutant colocalized with ChFP-NF1A1.1 at the array locus in both induced and uninduced cells. The data are means ± S.E. from three independent experiments (n ≥ 15 cells).CC-BY · From the PDF
FIGURE 3 Loss of deacetylase activity does not affect the HDAC1 mobility profile during gene activation. A , deacetylase activity of GFP-tagged HDAC1 H141A. Cell extracts from HDAC1-GFP- and HDAC1 H141A-GFP-transfected 3134 cells were immunoprecipitated with anti-GFP or IgG (background control) antibody, and the deacetylation activity of the resulting immunoprecipitates was determined. The GFP-tagged HDAC1 H141A mutant, harboring a point mutation in the HDAC1 catalytic domain, had lost its deacetylase activity. B , FRAP analysis of GFP-tagged HD1 H141A on the MMTV array revealed mobility similar to the wild-type HDAC1 mobility. The data are means ± S.E. from three independent experiments (n ≥ 15 cells).
FIGURE 3 Loss of deacetylase activity does not affect the HDAC1 mobility profile during gene activation. A , deacetylase activity of GFP-tagged HDAC1 H141A. Cell extracts from HDAC1-GFP- and HDAC1 H141A-GFP-transfected 3134 cells were immunoprecipitated with anti-GFP or IgG (background control) antibody, and the deacetylation activity of the resulting immunoprecipitates was determined. The GFP-tagged HDAC1 H141A mutant, harboring a point mutation in the HDAC1 catalytic domain, had lost its deacetylase activity. B , FRAP analysis of GFP-tagged HD1 H141A on the MMTV array revealed mobility similar to the wild-type HDAC1 mobility. The data are means ± S.E. from three independent experiments (n ≥ 15 cells).CC-BY · From the PDF
FIGURE 4 HDAC1 and GR physically interact at the MMTV array. A , HDAC1-YFP/CFP-GR FRET pair and YFP-GR/CFP-GR FRET pair colocalized at the MMTV array site. Dex , dexamethasone. B , YFP-GR/HDAC1-CFPinteractionmeasuredbyFRET.TheFRETsignalbetweenYFP-GRandCFP-GRservedasapositivecontrol. C , schematic representation of GST-HDAC1 constructs. D , various GST-HDAC1fusionproteinswerepurifiedfrom Escherichia coli . The GST pulldown assays were performed in the presence of 35 S-labeled GR or HDAC1. The results demonstrate that amino acids 26-40 of HDAC1 are important for GR/HDAC1 and HDAC1/HDAC1 interactions.
FIGURE 4 HDAC1 and GR physically interact at the MMTV array. A , HDAC1-YFP/CFP-GR FRET pair and YFP-GR/CFP-GR FRET pair colocalized at the MMTV array site. Dex , dexamethasone. B , YFP-GR/HDAC1-CFPinteractionmeasuredbyFRET.TheFRETsignalbetweenYFP-GRandCFP-GRservedasapositivecontrol. C , schematic representation of GST-HDAC1 constructs. D , various GST-HDAC1fusionproteinswerepurifiedfrom Escherichia coli . The GST pulldown assays were performed in the presence of 35 S-labeled GR or HDAC1. The results demonstrate that amino acids 26-40 of HDAC1 are important for GR/HDAC1 and HDAC1/HDAC1 interactions.CC-BY · From the PDF
FIGURE5 GFP-GRFRAPrecoveryattheMMTVarrayisHDAC1-independent. A , GR mobility did not changethroughouttheinductioncycle. B , FRAPanalysisofGR mobilityattheMMTVarrayincellscoexpressingHDAC1ortheHDAC16RorHDAC16QmutantdemonstratedthatGRmobilitywasnotinfluencedbyHDAC1mobility. C , the GFP-tagged HDAC1 del 40 mutant was not enriched at the MMTV array locus. Dex , dexamethasone. D , FRAP analysis of the GFP-tagged HDAC1 del 40 mutant during the dexamethasone induction cycle. The FRAP recovery curves of wild-type HDAC1-GFP are also shown as references. The GFP-tagged HDAC1 del 40 mutant, which was unable to bind to GR and HDAC1, was highly mobile. The data are means ± S.E. from three independent experiments (n ≥ 15 cells).
FIGURE5 GFP-GRFRAPrecoveryattheMMTVarrayisHDAC1-independent. A , GR mobility did not changethroughouttheinductioncycle. B , FRAPanalysisofGR mobilityattheMMTVarrayincellscoexpressingHDAC1ortheHDAC16RorHDAC16QmutantdemonstratedthatGRmobilitywasnotinfluencedbyHDAC1mobility. C , the GFP-tagged HDAC1 del 40 mutant was not enriched at the MMTV array locus. Dex , dexamethasone. D , FRAP analysis of the GFP-tagged HDAC1 del 40 mutant during the dexamethasone induction cycle. The FRAP recovery curves of wild-type HDAC1-GFP are also shown as references. The GFP-tagged HDAC1 del 40 mutant, which was unable to bind to GR and HDAC1, was highly mobile. The data are means ± S.E. from three independent experiments (n ≥ 15 cells).CC-BY · From the PDF
FIGURE 6 HDAC1exchange dynamics vary with promoter activity state. Shown is a model for the HDAC1 interactions during MMTV promoter activation and down-regulation. A , uninduced promoter; B , MMTV promoter at the peak of GR-induced transcription; C , refractory transcription state. Dex , dexamethasone; Pol II , polymerase II.
FIGURE 6 HDAC1exchange dynamics vary with promoter activity state. Shown is a model for the HDAC1 interactions during MMTV promoter activation and down-regulation. A , uninduced promoter; B , MMTV promoter at the peak of GR-induced transcription; C , refractory transcription state. Dex , dexamethasone; Pol II , polymerase II.CC-BY · From the PDF

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Metadata

Authors
Qiu, Y., Stavreva, D. A., Luo, Y., Indrawan, A., Chang, M., & Hager, G. L.
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2011-03
Volume
286
Issue
9
Pages
7641-7647
ISSN
0021-9258
DOI
10.1074/jbc.m110.185488
Cited by
24
References
2
Language
en
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