770
Views
0
CrossRef citations to date
0
Altmetric
Review

HDAC4: Mechanism of Regulation and Biological Functions

, &
Pages 139-150 | Published online: 28 Feb 2014

References

  • Thiagalingam S , ChengKH , LeeHJet al. Histone deacetylases: unique players in shaping the epigenetic histone code . Ann. NY Acad. Sci.983 , 84 – 100 ( 2003 ).
  • Grozinger CM , SchreiberSL . Deacetylase enzymes: biological functions and the use of small-molecule inhibitors . Chem. Biol.9 , 3 – 16 ( 2002 ).
  • Chen HP , DenicolaM , QinXet al. HDAC inhibition promotes cardiogenesis and the survival of embryonic stem cells through proteasome-dependent pathway . J. Cell Biochem.112 , 3246 – 3255 ( 2011 ).
  • Vaquero A , SternglanzR , ReinbergD . NAD+-dependent deacetylation of H4 lysine 16 by class III HDACs . Oncogene26 , 5505 – 5520 ( 2007 ).
  • Fischle W , KiermerV , DequiedtFet al. The emerging role of class II histone deacetylases . Biochem. Cell Biol.79 , 337 – 348 ( 2001 ).
  • Martin M , KettmannR , DequiedtF . Class IIa histone deacetylases: regulating the regulators . Oncogene26 , 5450 – 5467 ( 2007 ).
  • Yang XJ , SetoE . The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men . Nat. Rev. Mol. Cell Biol.9 , 206 – 218 ( 2008 ).
  • Barneda-Zahonero B , ParraM . Histone deacetylases and cancer . Mol. Oncol.6 , 579 – 589 ( 2012 ).
  • Wang AH , BertosNR , VezmarMet al. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor . Mol. Cell. Biol.19 , 7816 – 7827 ( 1999 ).
  • Vega RB , MatsudaK , OhJet al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis . Cell119 , 555 – 566 ( 2004 ).
  • Stark M , HaywardN . Genome-wide loss of heterozygosity and copy number analysis in melanoma using high-density single-nucleotide polymorphism arrays . Cancer Res.67 , 2632 – 2642 ( 2007 ).
  • Liu F , PoreN , KimMet al. Regulation of histone deacetylase 4 expression by the SP family of transcription factors . Mol. Biol. Cell17 , 585 – 597 ( 2006 ).
  • Addis RC , PrasadMK , YochemRLet al. OCT3/4 regulates transcription of histone deacetylase 4 (Hdac4) in mouse embryonic stem cells . J. Cell. Biochem.111 , 391 – 401 ( 2010 ).
  • Yuan JH , YangF , ChenBFet al. The histone deacetylase 4/SP1/microrna-200a regulatory network contributes to aberrant histone acetylation in hepatocellular carcinoma . Hepatology54 , 2025 – 2035 ( 2011 ).
  • Chen JF , MandelEM , ThomsonJMet al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation . Nat. Genet.38 , 228 – 233 ( 2006 ).
  • Sun Y , GeY , DrnevichJet al. Mammalian target of rapamycin regulates miRNA-1 and follistatin in skeletal myogenesis . J. Cell Biol.189 , 1157 – 1169 ( 2010 ).
  • Sluijter JP , van MilA , van VlietPet al. MicroRNA-1 and -499 regulate differentiation and proliferation in human-derived cardiomyocyte progenitor cells . Arterioscler. Thromb. Vasc. Biol.30 , 859 – 868 ( 2010 ).
  • Zhang J , YangY , YangTet al. microRNA-22, downregulated in hepatocellular carcinoma and correlated with prognosis, suppresses cell proliferation and tumourigenicity . Br. J. Cancer103 , 1215 – 1220 ( 2010 ).
  • Winbanks CE , WangB , BeyerCet al. TGF-beta regulates miR-206 and miR-29 to control myogenic differentiation through regulation of HDAC4 . J. Biol. Chem.286 , 13805 – 13814 ( 2011 ).
  • Tuddenham L , WheelerG , Ntounia-FousaraSet al. The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells . FEBS Lett.580 , 4214 – 4217 ( 2006 ).
  • Miyaki S , SatoT , InoueAet al. MicroRNA-140 plays dual roles in both cartilage development and homeostasis . Genes Dev.24 , 1173 – 1185 ( 2010 ).
  • Guan YJ , YangX , WeiLet al. MiR-365: a mechanosensitive microRNA stimulates chondrocyte differentiation through targeting histone deacetylase 4 . FASEB J.25 , 4457 – 4466 ( 2011 ).
  • Sandhu SK , VoliniaS , CostineanSet al. miR-155 targets histone deacetylase 4 (HDAC4) and impairs transcriptional activity of B-cell lymphoma 6 (BCL6) in the Emu-miR-155 transgenic mouse model . Proc. Natl Acad. Sci. USA109 , 20047 – 20052 ( 2013 ).
  • Guo L , HanA , BatesDLet al. Crystal structure of a conserved N-terminal domain of histone deacetylase 4 reveals functional insights into glutamine-rich domains . Proc. Natl Acad. Sci. USA104 , 4297 – 4302 ( 2007 ).
  • Bottomley MJ , LoSurdo P , DiGiovine Pet al. Structural and functional analysis of the human HDAC4 catalytic domain reveals a regulatory structural zinc-binding domain . J. Biol. Chem.283 , 26694 – 26704 ( 2008 ).
  • Grozinger CM , SchreiberSL . Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization . Proc. Natl. Acad. Sci. USA97 , 7835 – 7840 ( 2000 ).
  • Wang AH , KruhlakMJ , WuJet al. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins . Mol. Cell Biol.20 , 6904 – 6912 ( 2000 ).
  • McKinsey TA , ZhangCL , LuJet al. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation . Nature408 , 106 – 111 ( 2000 ).
  • Backs J , SongK , BezprozvannayaSet al. CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy . J. Clin. Invest.116 , 1853 – 1864 ( 2006 ).
  • Nakagawa Y , KuwaharaK , HaradaMet al. Class II HDACs mediate CaMK-dependent signaling to NRSF in ventricular myocytes . J. Mol. Cell. Cardiol.41 , 1010 – 1022 ( 2006 ).
  • Backs J , BacksT , NeefSet al. The delta isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload . Proc. Natl Acad. Sci. USA106 , 2342 – 2347 ( 2009 ).
  • Zhang T , KohlhaasM , BacksJet al. CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses . J. Biol. Chem.282 , 35078 – 35087 ( 2007 ).
  • Backs J , WorstBC , LehmannLHet al. Selective repression of MEF2 activity by PKA-dependent proteolysis of HDAC4 . J. Cell Biol.195 , 403 – 415 ( 2011 ).
  • Zhou X , RichonVM , WangAHet al. Histone deacetylase 4 associates with extracellular signal-regulated kinases 1 and 2, and its cellular localization is regulated by oncogenic Ras . Proc. Natl Acad. Sci. USA97 , 14329 – 14333 ( 2000 ).
  • Cernotta N , ClocchiattiA , FloreanCet al. Ubiquitin-dependent degradation of HDAC4, a new regulator of random cell motility . Mol. Biol. Cell22 , 278 – 289 ( 2011 ).
  • Paroni G , CernottaN , DelloRusso Cet al. PP2A regulates HDAC4 nuclear import . Mol. Biol. Cell19 , 655 – 667 ( 2008 ).
  • Ago T , LiuT , ZhaiPet al. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy . Cell133 , 978 – 993 ( 2008 ).
  • Matsushima S , KurodaJ , AgoTet al. Increased oxidative stress in the nucleus caused by Nox4 mediates oxidation of HDAC4 and cardiac hypertrophy . Circ. Res.112 , 651 – 663 ( 2013 ).
  • Tatham MH , JaffrayE , VaughanOAet al. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9 . J. Biol. Chem.276 , 35368 – 35374 ( 2001 ).
  • Kirsh O , SeelerJS , PichlerAet al. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase . EMBO J.21 , 2682 – 2691 ( 2002 ).
  • Liu F , DowlingM , YangXJet al. Caspase-mediated specific cleavage of human histone deacetylase 4 . J. Biol. Chem.279 , 34537 – 34546 ( 2004 ).
  • Paroni G , FontaniniA , CernottaNet al. Dephosphorylation and caspase processing generate distinct nuclear pools of histone deacetylase 4 . Mol. Cell. Biol.27 , 6718 – 6732 ( 2007 ).
  • Paroni G , MizzauM , HendersonCet al. Caspase-dependent regulation of histone deacetylase 4 nuclear-cytoplasmic shuttling promotes apoptosis . Mol. Biol. Cell.15 , 2804 – 2818 ( 2004 ).
  • Kozhemyakina E , CohenT , YaoTPet al. Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/MEF2 pathway . Mol. Cell. Biol.29 , 5751 – 5762 ( 2009 ).
  • McKinsey TA , ZhangCL , OlsonEN . Identification of a signal-responsive nuclear export sequence in class II histone deacetylases . Mol. Cell. Biol.21 , 6312 – 6321 ( 2001 ).
  • McKinsey TA , KuwaharaK , BezprozvannayaSet al. Class II histone deacetylases confer signal responsiveness to the ankyrin-repeat proteins ANKRA2 and RFXANK . Mol. Biol. Cell.17 , 438 – 447 ( 2006 ).
  • Wang AH , YangXJ . Histone deacetylase 4 possesses intrinsic nuclear import and export signals . Mol. Cell. Biol.21 , 5992 – 6005 ( 2001 ).
  • Kehat I , AccorneroF , AronowBJet al. Modulation of chromatin position and gene expression by HDAC4 interaction with nucleoporins . J. Cell. Biol.193 , 21 – 29 ( 2011 ).
  • Qian DZ , KachhapSK , CollisSJet al. Class II histone deacetylases are associated with VHL-independent regulation of hypoxia-inducible factor 1 alpha . Cancer Res.66 , 8814 – 8821 ( 2006 ).
  • Seo HW , KimEJ , NaHet al. Transcriptional activation of hypoxia-inducible factor-1alpha by HDAC4 and HDAC5 involves differential recruitment of p300 and FIH-1 . FEBS Lett.583 , 55 – 60 ( 2009 ).
  • Geng H , HarveyCT , PittsenbargerJet al. HDAC4 protein regulates HIF1alpha protein lysine acetylation and cancer cell response to hypoxia . J. Biol. Chem.286 , 38095 – 38102 ( 2011 ).
  • Choi MC , CohenTJ , BarrientosTet al. A direct HDAC4-MAP kinase crosstalk activates muscle atrophy program . Mol. Cell47 , 122 – 132 ( 2012 ).
  • Stronach EA , AlfraidiA , RamaNet al. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer . Cancer Res.71 , 4412 – 4422 ( 2011 ).
  • Fischle W , DequiedtF , HendzelMJet al. Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR . Mol. Cell9 , 45 – 57 ( 2002 ).
  • Guenther MG , BarakO , LazarMA . The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3 . Mol. Cell Biol.21 , 6091 – 6101 ( 2001 ).
  • Jeon EJ , LeeKY , ChoiNSet al. Bone morphogenetic protein-2 stimulates Runx2 acetylation . J. Biol. Chem.281 , 16502 – 16511 ( 2006 ).
  • Shinkai Y . Regulation and function of H3K9 methylation . Subcell. Biochem.41 , 337 – 350 ( 2007 ).
  • Zhang CL , McKinseyTA , OlsonEN . Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation . Mol. Cell. Biol.22 , 7302 – 7312 ( 2002 ).
  • Raychaudhuri N , RaychaudhuriS , ThamotharanMet al. Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring . J. Biol. Chem.283 , 13611 – 13626 ( 2008 ).
  • Hohl M , WagnerM , ReilJC , TauchnitzM , ZimmerAM , LehmannLH , ThielG , BohmM , BacksJ , MaackCet al. HDAC4 controls histone methylation in response to elevated cardiac load . J. Clin. Invest.123 , 1359 – 1370 ( 2013 ).
  • Sailaja BS , Cohen-CarmonD , ZimmermanGet al. Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4 . Proc. Natl Acad. Sci. USA109 , E3687 – E3695 ( 2012 ).
  • Huang SK , ScruggsAM , DonaghyJet al. Histone modifications are responsible for decreased Fas expression and apoptosis resistance in fibrotic lung fibroblasts . Cell Death Dis.4 , e621 ( 2013 ).
  • Gregoire S , TremblayAM , XiaoLet al. Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation . J. Biol. Chem.281 , 4423 – 4433 ( 2006 ).
  • Zhao X , SternsdorfT , BolgerTAet al. Regulation of MEF2 by histone deacetylase 4- and SIRT1 deacetylase-mediated lysine modifications . Mol. Cell Biol.25 , 8456 – 8464 ( 2005 ).
  • Gregoire S , YangXJ . Association with class IIa histone deacetylases upregulates the sumoylation of MEF2 transcription factors . Mol. Cell Biol.25 , 2273 – 2287 ( 2005 ).
  • Kang JS , AllistonT , DelstonRet al. Repression of Runx2 function by TGF-beta through recruitment of class II histone deacetylases by Smad3 . EMBO J.24 , 2543 – 2555 ( 2005 ).
  • Pei M , ChenD , LiJet al. Histone deacetylase 4 promotes TGF-beta1-induced synovium-derived stem cell chondrogenesis but inhibits chondrogenically differentiated stem cell hypertrophy . Differentiation78 , 260 – 268 ( 2009 ).
  • Lin Q , SchwarzJ , BucanaCet al. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C . Science276 , 1404 – 1407 ( 1997 ).
  • Karamboulas C , SwedaniA , WardCet al. HDAC activity regulates entry of mesoderm cells into the cardiac muscle lineage . J. Cell. Sci.119 , 4305 – 4314 ( 2006 ).
  • McKinsey TA , ZhangCL , OlsonEN . Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5 . Proc. Natl Acad. Sci. USA97 , 14400 – 14405 ( 2000 ).
  • Miska EA , LangleyE , WolfDet al. Differential localization of HDAC4 orchestrates muscle differentiation . Nucleic Acids Res.29 , 3439 – 3447 ( 2001 ).
  • Liu Y , RandallWR , SchneiderMF . Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle . J. Cell Biol.168 , 887 – 897 ( 2005 ).
  • Passier R , ZengH , FreyNet al. CaM kinase signaling induces cardiac hypertrophy and activates the MEF2 transcription factor in vivo . J. Clin. Invest.105 , 1395 – 1406 ( 2000 ).
  • Huang ZP , ChenJ , SeokHYet al. MicroRNA-22 regulates cardiac hypertrophy and remodeling in response to stress . Circ. Res.112 , 1234 – 1243 ( 2013 ).
  • Gupta MP , SamantSA , SmithSHet al. HDAC4 and PCAF bind to cardiac sarcomeres and play a role in regulating myofilament contractile activity . J. Biol. Chem.283 , 10135 – 10146 ( 2008 ).
  • Cohen TJ , BarrientosT , HartmanZCet al. The deacetylase HDAC4 controls myocyte enhancing factor-2-dependent structural gene expression in response to neural activity . FASEB J.23 , 99 – 106 ( 2009 ).
  • Cohen TJ , WaddellDS , BarrientosTet al. The histone deacetylase HDAC4 connects neural activity to muscle transcriptional reprogramming . J. Biol. Chem.282 , 33752 – 33759 ( 2007 )
  • Tang H , MacphersonP , MarvinMet al. A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression . Mol. Biol. Cell20 , 1120 – 1131 ( 2009 ).
  • Darcy MJ , CalvinK , CavnarKet al. Regional and subcellular distribution of HDAC4 in mouse brain . J. Comp. Neurol.518 , 722 – 740 ( 2010 ).
  • Bolger TA , YaoTP . Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death . J. Neurosci.25 , 9544 – 9553 ( 2005 ).
  • Bolger TA , ZhaoX , CohenTJet al. The neurodegenerative disease protein ataxin-1 antagonizes the neuronal survival function of myocyte enhancer factor-2 . J. Biol. Chem.282 , 29186 – 29192 ( 2007 ).
  • Chawla S , VanhoutteP , ArnoldFJet al. Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5 . J. Neurochem.85 , 151 – 159 ( 2003 ).
  • Jovicic A , ZaldivarJolissaint JFet al. MicroRNA-22 (miR-22) overexpression is neuroprotective via general anti-apoptotic effects and may also target specific Huntington’s disease-related mechanisms . PLoS ONE8 , e54222 ( 2013 ).
  • Chen B , CepkoCL . HDAC4 regulates neuronal survival in normal and diseased retinas . Science323 , 256 – 259 ( 2009 ).
  • Yang Y , QinX , LiuSet al. Peroxisome proliferator-activated receptor gamma is inhibited by histone deacetylase 4 in cortical neurons under oxidative stress . J. Neurochem.118 , 429 – 439 ( 2011 ).
  • Williams SR , AldredMA , DerKaloustian VMet al. Haploinsufficiency of HDAC4 causes brachydactyly mental retardation syndrome, with brachydactyly type E, developmental delays, and behavioral problems . Am. J. Hum. Genet.87 , 219 – 228 ( 2010 ).
  • Kim T , ParkJK , KimHJet al. Association of histone deacetylase genes with schizophrenia in Korean population . Psychiatry Res.178 , 266 – 269 ( 2012 ).
  • Li J , ChenJ , RicuperoCLet al. Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia . Nat. Med.18 , 783 – 790 ( 2013 ).
  • Lenoir O , FlosseauK , MaFXet al. Specific control of pancreatic endocrine beta- and delta-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9 . Diabetes60 , 2861 – 2871 ( 2011 ).
  • Chauchereau A , MathieuM , de SaintignonJet al. HDAC4 mediates transcriptional repression by the acute promyelocytic leukaemia-associated protein PLZF . Oncogene23 , 8777 – 8784 ( 2004 ).
  • Lemercier C , BrocardMP , Puvion-DutilleulFet al. Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor . J. Biol. Chem.277 , 22045 – 22052 ( 2002 ).
  • Wilson AJ , ByunDS , NasserSet al. HDAC4 promotes growth of colon cancer cells via repression of p21 . Mol. Biol. Cell19 , 4062 – 4075 ( 2008 ).
  • Mottet D , PirotteS , LamourVet al. HDAC4 represses p21(WAF1/Cip1) expression in human cancer cells through a Sp1-dependent, p53-independent mechanism . Oncogene28 , 243 – 256 ( 2009 ).
  • Liu R , WangL , ChenGet al. FOXP3 up-regulates p21 expression by site-specific inhibition of histone deacetylase 2/histone deacetylase 4 association to the locus . Cancer Res.69 , 2252 – 2259 ( 2009 ).
  • Barrett A , SantangeloS , TanKet al. Breast cancer associated transcriptional repressor PLU-1/JARID1B interacts directly with histone deacetylases . Int. J. Cancer121 , 265 – 275 ( 2007 ).
  • Xu XS , WangL , AbramsJet al. Histone deacetylases (HDACs) in XPC gene silencing and bladder cancer . J. Hematol. Oncol.4 , 17 ( 2011 ).
  • Geng H , HarveyCT , PittsenbargerJet al. HDAC4 protein regulates HIF1alpha protein lysine acetylation and cancer cell response to hypoxia . J. Biol. Chem.286 , 38095 – 38102 ( 2011 ).
  • Song B , WangY , XiYet al. Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells . Oncogene28 , 4065 – 4074 ( 2009 ).
  • Isaacs JT , AntonyL , DalrympleSLet al. Tasquinimod Is an allosteric modulator of HDAC4 survival signaling within the compromised cancer microenvironment . Cancer Res.73 , 1386 – 1399 ( 2013 ).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.