216
Views
0
CrossRef citations to date
0
Altmetric
Special Report

Phenylbutyrate and β-cell function: contribution of histone deacetylases and ER stress Inhibition

, &
Pages 711-720 | Received 17 Nov 2016, Accepted 07 Feb 2017, Published online: 04 May 2017

References

  • American Diabetes Association . Diagnosis and classification of diabetes mellitus . Diabetes Care31 ( Suppl. 1 ), S55 – S60 ( 2008 ).
  • Idf . International Diabetes Federation Diabetes Atlas . 7th edition , ( 2015 ). www.diabetesatlas.org/
  • Khan S , JenaG . Sodium butyrate reduces insulin-resistance, fat accumulation and dyslipidemia in Type-2 diabetic rat: a comparative study with metformin . Chem. Biol. Interact.254 , 124 – 134 ( 2016 ).
  • Eizirik DL , CardozoAK , CnopM . The role for endoplasmic reticulum stress in diabetes mellitus . Endocr. Rev.29 ( 1 ), 42 – 61 ( 2008 ).
  • Chistiakov DA , SobeninIA , OrekhovAN , BobryshevYV . Role of endoplasmic reticulum stress in atherosclerosis and diabetic macrovascular complications . Biomed. Res. Int. 2014 , 610140 ( 2014 ).
  • Xiao C , GiaccaA , LewisGF . Sodium phenylbutyrate, a drug with known capacity to reduce endoplasmic reticulum stress, partially alleviates lipid-induced insulin resistance and beta-cell dysfunction in humans . Diabetes60 ( 3 ), 918 – 924 ( 2011 ).
  • Hotamisligil GS . Endoplasmic reticulum stress and the inflammatory basis of metabolic disease . Cell140 ( 6 ), 900 – 917 ( 2010 ).
  • Braakman I , BulleidNJ . Protein folding and modification in the mammalian endoplasmic reticulum . Annu. Rev. Biochem.80 , 71 – 99 ( 2011 ).
  • Skinner MK . Environmental epigenomics and disease susceptibility . EMBO Rep.12 ( 7 ), 620 – 622 ( 2011 ).
  • Choi S-W , FrisoS . Epigenetics: a new bridge between nutrition and health . Adv. Nutr.1 ( 1 ), 8 – 16 ( 2010 ).
  • Åkerblom HK , KnipM . Putative environmental factors in Type 1 diabetes . Diabetes Metab. Rev.14 ( 1 ), 31 – 68 ( 1998 ).
  • Martínez JA , MilagroFI , ClaycombeKJ , SchalinskeKL . Epigenetics in adipose tissue, obesity, weight loss, and diabetes . Adv. Nutr.5 ( 1 ), 71 – 81 ( 2014 ).
  • Khan S , KumarS , JenaG . Valproic acid reduces insulin-resistance, fat deposition and FOXO1-mediated gluconeogenesis in Type-2 diabetic rat . Biochimie125 , 42 – 52 ( 2016 ).
  • Khan S , JenaG . The role of butyrate, a histone deacetylase inhibitor in diabetes mellitus: experimental evidence for therapeutic intervention . Epigenomics7 ( 4 ), 669 – 680 ( 2015 ).
  • Kouzarides T . Histone acetylases and deacetylases in cell proliferation . Curr. Opin. Genet. Dev.9 ( 1 ), 40 – 48 ( 1999 ).
  • Kanika G , KhanS , JenaG . Sodium butyrate ameliorates l-arginine-induced pancreatitis and associated fibrosis in Wistar rat: role of inflammation and nitrosative stress . J. Biochem. Mol. Toxicol.29 ( 8 ), 349 – 359 ( 2015 ).
  • Khan S , JenaGB . Protective role of sodium butyrate, a HDAC inhibitor on beta-cell proliferation, function and glucose homeostasis through modulation of p38/ERK MAPK and apoptotic pathways: study in juvenile diabetic rat . Chem. Biol. Interact.213 , 1 – 12 ( 2014 ).
  • Christensen DP , GysemansC , LundhMet al. Lysine deacetylase inhibition prevents diabetes by chromatin-independent immunoregulation and beta-cell protection . Proc. Natl Acad. Sci. USA111 ( 3 ), 1055 – 1059 ( 2014 ).
  • Gray SG , De MeytsP . Role of histone and transcription factor acetylation in diabetes pathogenesis . Diabetes Metab. Res. Rev.21 ( 5 ), 416 – 433 ( 2005 ).
  • Khan S , JenaG . Valproic acid improves glucose homeostasis by increasing beta-cell proliferation, function, and reducing its apoptosis through hdac inhibition in juvenile diabetic rat . J. Biochem. Mol. Toxicol.30 ( 9 ), 438 – 446 ( 2016 ).
  • Khan S , JenaG , TikooK , KumarV . Valproate attenuates the proteinuria, podocyte and renal injury by facilitating autophagy and inactivation of NF-kappaB/iNOS signaling in diabetic rat . Biochimie110 , 1 – 16 ( 2015 ).
  • Haumaitre C , LenoirO , ScharfmannR . Histone deacetylase inhibitors modify pancreatic cell fate determination and amplify endocrine progenitors . Mol. Cell. Biol.28 ( 20 ), 6373 – 6383 ( 2008 ).
  • Wang X , WeiX , PangQ , YiF . Histone deacetylases and their inhibitors: molecular mechanisms and therapeutic implications in diabetes mellitus . Acta Pharmaceutica Sinica B2 ( 4 ), 387 – 395 ( 2012 ).
  • Khan S , JenaG . Sodium butyrate, a HDAC inhibitor ameliorates eNOS, iNOS and TGF-beta1-induced fibrogenesis, apoptosis and DNA damage in the kidney of juvenile diabetic rats . Food Chem. Toxicol.73 , 127 – 139 ( 2014 ).
  • Iannitti T , PalmieriB . Clinical and experimental applications of sodium phenylbutyrate . Drugs R. D.11 ( 3 ), 227 – 249 ( 2011 ).
  • Khan S , AhirwarK , JenaG . Anti-fibrotic effects of valproic acid: role of HDAC inhibition and associated mechanisms . Epigenomics8 ( 8 ), 1087 – 1101 ( 2016 ).
  • Khan S , JenaG , TikooK . Sodium valproate ameliorates diabetes-induced fibrosis and renal damage by the inhibition of histone deacetylases in diabetic rat . Exp. Mol. Pathol.98 ( 2 ), 230 – 239 ( 2015 ).
  • Lichter-Konecki U , DiazG , MerrittJet al. Ammonia control in children with urea cycle disorders (UCDs); Phase II comparison of sodium phenylbutyrate and glycerol phenylbutyrate . Mol. Genet. Metab.103 ( 4 ), 323 – 329 ( 2011 ).
  • Kusaczuk M , KretowskiR , BartoszewiczM , Cechowska-PaskoM . Phenylbutyrate – a pan-HDAC inhibitor-suppresses proliferation of glioblastoma LN-229 cell line . Tumor Biol.37 ( 1 ), 931 – 942 ( 2016 ).
  • Haumaitre C , LenoirO , ScharfmannR . Histone deacetylase inhibitors modify pancreatic cell fate determination and amplify endocrine progenitors . Mol. Cell Biol.28 ( 20 ), 6373 – 6383 ( 2008 ).
  • Cadavez L , MontaneJ , Alcarraz-VizánGet al. Chaperones ameliorate beta cell dysfunction associated with human islet amyloid polypeptide overexpression . PLoS ONE9 ( 7 ), e101797 ( 2014 ).
  • Lenin R , MariaMS , AgrawalM , BalasubramanyamJ , MohanV , BalasubramanyamM . Amelioration of glucolipotoxicity-induced endoplasmic reticulum stress by a ‘chemical chaperone’ in human THP-1 monocytes . Exp. Diabetes Res. 2012 , 356487 ( 2012 ).
  • Iannitti MT , PalmieriB . Clinical and experimental applications of sodium phenylbutyrate . Drugs R. D.11 ( 3 ), 227 – 249 ( 2011 ).
  • Srinivasan K , SharmaSS . Sodium phenylbutyrate ameliorates focal cerebral ischemic/reperfusion injury associated with comorbid Type-2 diabetes by reducing endoplasmic reticulum stress and DNA fragmentation . Behav. Brain. Res.225 ( 1 ), 110 – 116 ( 2011 ).
  • Zeng W , GuoY-H , QiWet al. 4-Phenylbutyric acid suppresses inflammation through regulation of endoplasmic reticulum stress of endothelial cells stimulated by uremic serum . Life Sci.103 ( 1 ), 15 – 24 ( 2014 ).
  • Harding HP , ZhangY , RonD . Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase . Nature397 ( 6716 ), 271 – 274 ( 1999 ).
  • Sidrauski C , ChapmanR , WalterP . The unfolded protein response: an intracellular signalling pathway with many surprising features . Trends Cell Biol.8 ( 6 ), 245 – 249 ( 1998 ).
  • Ellgaard L , HeleniusA . ER quality control: towards an understanding at the molecular level . Curr. Opin. Cell Biol.13 ( 4 ), 431 – 437 ( 2001 ).
  • Travers KJ , PatilCK , WodickaL , LockhartDJ , WeissmanJS , WalterP . Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation . Cell101 ( 3 ), 249 – 258 ( 2000 ).
  • Gardner BM , WalterP . Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response . Science333 ( 6051 ), 1891 – 1894 ( 2011 ).
  • Kimata Y , Ishiwata-KimataY , ItoTet al. Two regulatory steps of ER-stress sensor Ire1 involving its cluster formation and interaction with unfolded proteins . J. Cell Biol.179 ( 1 ), 75 – 86 ( 2007 ).
  • Jiang HY , WekSA , McgrathBCet al. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response . Mol. Cell Biol.24 ( 3 ), 1365 – 1377 ( 2004 ).
  • Bravo R , ParraV , GaticaDet al. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration . Int. Rev. Cell. Mol. Biol.301 , 215 – 290 ( 2013 ).
  • Urano F , WangX , BertolottiAet al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 . Science287 ( 5453 ), 664 – 666 ( 2000 ).
  • Tersey SA , NishikiY , TemplinATet al. Islet β-cell endoplasmic reticulum stress precedes the onset of Type-1 diabetes in the nonobese diabetic mouse model . Diabetes61 ( 4 ), 818 – 827 ( 2012 ).
  • Zhong J , RaoX , XuJ-F , YangP , WangC-Y . The role of endoplasmic reticulum stress in autoimmune-mediated beta-cell destruction in Type-1 diabetes . Exp. Diabetes Res. 2012 , 238980 ( 2012 ).
  • Chan J , BidenT , LaybuttD . Cross-talk between the unfolded protein response and nuclear factor-κB signalling pathways regulates cytokine-mediated beta cell death in MIN6 cells and isolated mouse islets . Diabetologia55 ( 11 ), 2999 – 3009 ( 2012 ).
  • Luo Z-F , FengB , MuJet al. Effects of 4-phenylbutyric acid on the process and development of diabetic nephropathy induced in rats by streptozotocin: regulation of endoplasmic reticulum stress-oxidative activation . Toxicol. Appl. Pharmacol.246 ( 1 ), 49 – 57 ( 2010 ).
  • Shang L , HuaH , FooKet al. β-cell dysfunction due to increased ER stress in a stem cell model of Wolfram syndrome . Diabetes63 ( 3 ), 923 – 933 ( 2014 ).
  • Yamada T , IshiharaH , TamuraAet al. WFS1-deficiency increases endoplasmic reticulum stress, impairs cell cycle progression and triggers the apoptotic pathway specifically in pancreatic beta-cells . Hum. Mol. Genet.15 ( 10 ), 1600 – 1609 ( 2006 ).
  • Lombardi A , UlianichL , TregliaASet al. Increased hexosamine biosynthetic pathway flux dedifferentiates INS-1E cells and murine islets by an extracellular signal-regulated kinase (ERK)1/2-mediated signal transmission pathway . Diabetologia55 ( 1 ), 141 – 153 ( 2012 ).
  • Laybutt DR , PrestonAM , AkerfeldtMCet al. Endoplasmic reticulum stress contributes to beta cell apoptosis in Type-2 diabetes . Diabetologia50 ( 4 ), 752 – 763 ( 2007 ).
  • Cnop M , LadriereL , HekermanPet al. Selective inhibition of eukaryotic translation initiation factor 2α dephosphorylation potentiates fatty acid-induced endoplasmic reticulum stress and causes pancreatic β-cell dysfunction and apoptosis . J. Biol. Chem.282 ( 6 ), 3989 – 3997 ( 2007 ).
  • Chan JY , LuzuriagaJ , BensellamM , BidenTJ , LaybuttDR . Failure of the adaptive unfolded protein response in islets of obese mice is linked with abnormalities in β-cell gene expression and progression to diabetes . Diabetes62 ( 5 ), 1557 – 1568 ( 2013 ).
  • Tang C , KoulajianK , SchuikiIet al. Glucose-induced beta cell dysfunction in vivo in rats: link between oxidative stress and endoplasmic reticulum stress . Diabetologia55 ( 5 ), 1366 – 1379 ( 2012 ).
  • Xiao C , GiaccaA , LewisGF . Sodium phenylbutyrate, a drug with known capacity to reduce endoplasmic reticulum stress, partially alleviates lipid-induced insulin resistance and β-cell dysfunction in humans . Diabetes60 ( 3 ), 918 – 924 ( 2011 ).
  • Basseri S , LhotakS , SharmaAM , AustinRC . The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response . J. Lipid Res.50 ( 12 ), 2486 – 2501 ( 2009 ).
  • Ozcan U , YilmazE , OzcanLet al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of Type-2 diabetes . Science313 ( 5790 ), 1137 – 1140 ( 2006 ).
  • Ma J , LuoT , ZengZet al. Histone deacetylase inhibitor phenylbutyrate exaggerates heart failure in pressure overloaded mice independently of HDAC inhibition . Sci. Rep.6 , 34036 ( 2016 ).
  • Haumaitre C , LenoirO , ScharfmannR . Directing cell differentiation with small-molecule histone deacetylase inhibitors . Cell Cycle8 ( 4 ), 536 – 544 ( 2009 ).
  • Khan S , BhatZR , JenaG . Role of autophagy and histone deacetylases in diabetic nephropathy: current status and future perspectives . Genes Dis.3 ( 3 ), 211 – 219 ( 2016 ).
  • Sampley ML , OzcanS . Regulation of insulin gene transcription by multiple histone acetyltransferases . DNA Cell. Biol.31 ( 1 ), 8 – 14 ( 2012 ).
  • Mosley AL , OzcanS . Glucose regulates insulin gene transcription by hyperacetylation of histone H4 . The J. Biol. Chem.278 ( 22 ), 19660 – 19666 ( 2003 ).
  • Lenoir O , FlosseauK , MaFXet al. Specific control of pancreatic endocrine β-and δ-cell mass by class IIa histone deacetylases HDAC4, HDAC5, and HDAC9 . Diabetes60 ( 11 ), 2861 – 2871 ( 2011 ).
  • Lundh M , ChristensenDP , Damgaard NielsenMet al. Histone deacetylases 1 and 3 but not 2 mediate cytokine-induced beta cell apoptosis in INS-1 cells and dispersed primary islets from rats and are differentially regulated in the islets of Type-1 diabetic children . Diabetologia55 ( 9 ), 2421 – 2431 ( 2012 ).
  • Hong YP , GuoWY , WangWXet al. 4-Phenylbutyric acid attenuates pancreatic beta-cell injury in rats with experimental severe acute pancreatitis . Int. J. Endocrinol. 2016 , 4592346 ( 2016 ).
  • Zhu M , GuoM , FeiL , PanXQ , LiuQQ . 4-Phenylbutyric acid attenuates endoplasmic reticulum stress-mediated pancreatic beta-cell apoptosis in rats with streptozotocin-induced diabetes . Endocrine47 ( 1 ), 129 – 137 ( 2014 ).
  • Fu SH , ChenST , HsuBR . Attenuation of primary nonfunction for syngeneic islet graft using sodium 4-phenylbutyrate . Transplant. Proc.37 ( 4 ), 1830 – 1831 ( 2005 ).
  • Hu H , LiL , WangCet al. 4-Phenylbutyric acid increases GLUT4 gene expression through suppression of HDAC5 but not endoplasmic reticulum stress . Cell. Physiol. Biochem.33 ( 6 ), 1899 – 1910 ( 2014 ).
  • True O , MatthiasP . Interplay between histone deacetylases and autophagy – from cancer therapy to neurodegeneration . Immunol. Cell. Biol.90 ( 1 ), 78 – 84 ( 2012 ).
  • Basseri S , AustinRC . Endoplasmic reticulum stress and lipid metabolism: mechanisms and therapeutic potential . Biochem. Res. Int. 2012 , 841362 ( 2012 ).
  • Ohoka N , HattoriT , KitagawaM , OnozakiK , HayashiH . Critical and functional regulation of CHOP (C/EBP homologous protein) through the N-terminal portion . J. Biol. Chem.282 ( 49 ), 35687 – 35694 ( 2007 ).
  • Baumeister P , LuoS , SkarnesWCet al. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers . Mol. Cell. Biol.25 ( 11 ), 4529 – 4540 ( 2005 ).
  • Kahali S , SarcarB , PrabhuA , SetoE , ChinnaiyanP . Class I histone deacetylases localize to the endoplasmic reticulum and modulate the unfolded protein response . FASEB J.26 ( 6 ), 2437 – 2445 ( 2012 ).
  • Baumeister P , LuoS , SkarnesWCet al. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: activating mechanisms mediated by YY1 and its interactive chromatin modifiers . Mol. Cell Biol.25 ( 11 ), 4529 – 4540 ( 2005 ).
  • Pratt WB , ToftDO . Regulation of signaling protein function and trafficking by the HSP90/HSP70-based chaperone machinery . Exp. Biol. Med.228 ( 2 ), 111 – 133 ( 2003 ).
  • Yang X , ZhangY , XuWet al. Potential role of HSP90 in rat islet function under the condition of high glucose . Acta Diabetol53 ( 4 ), 621 – 628 ( 2016 ).
  • Lazaro I , OguizaA , RecioCet al. Targeting HSP90 ameliorates nephropathy and atherosclerosis through suppression of NF-κB and stat signaling pathways in diabetic mice . Diabetes64 ( 10 ), 3600 – 3613 ( 2015 ).
  • Kovacs JJ , MurphyPJ , GaillardSet al. HDAC6 regulates HSP90 acetylation and chaperone-dependent activation of glucocorticoid receptor . Mol. Cell18 ( 5 ), 601 – 607 ( 2005 ).
  • Galassetti P . Inflammation and oxidative stress in obesity, metabolic syndrome, and diabetes . Exp. Diabetes Res. 2012 , 943706 ( 2012 ).
  • Li B , LiuS , MiaoL , CaiL . Prevention of diabetic complications by activation of Nrf2: diabetic cardiomyopathy and nephropathy . Exp. Diabetes Res. 2012 , 216512 ( 2012 ).
  • Mozzini C , Fratta PasiniA , GarbinUet al. Increased endoplasmic reticulum stress and Nrf2 repression in peripheral blood mononuclear cells of patients with stable coronary artery disease . Free Rad. Biol. Med.68 ( 0 ), 178 – 185 ( 2014 ).
  • Cullinan SB , ZhangD , HanninkM , ArvisaisE , KaufmanRJ , DiehlJA . Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival . Mol. Cell. Biol.23 ( 20 ), 7198 – 7209 ( 2003 ).
  • Kawai Y , GardunoL , TheodoreM , YangJ , ArinzeIJ . Acetylation-deacetylation of the transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2) regulates its transcriptional activity and nucleocytoplasmic localization . The J. Biol. Chem.286 ( 9 ), 7629 – 7640 ( 2011 ).
  • Lee DY , LeeCI , LinTEet al. Role of histone deacetylases in transcription factor regulation and cell cycle modulation in endothelial cells in response to disturbed flow . Proc. Natl Acad. Sci. USA.109 ( 6 ), 1967 – 1972 ( 2012 ).
  • Clinical Trials Database: NCT00533559 . https://clinicaltrials.gov/ct2/show/NCT00533559
  • Wagner FF , LundhM , KayaTet al. An Isochemogenic set of inhibitors to define the therapeutic potential of histone deacetylases in β-cell protection . ACS Chem. Biol.11 ( 2 ), 363 – 374 ( 2016 ).
  • Lundh M , GalboT , PoulsenSS , Mandrup-PoulsenT . Histone deacetylase 3 inhibition improves glycaemia and insulin secretion in obese diabetic rats . Diabetes Obes. Metab.17 ( 7 ), 703 – 707 ( 2015 ).
  • Chou DH , HolsonEB , WagnerFFet al. Inhibition of histone deacetylase 3 protects beta cells from cytokine-induced apoptosis . Chem. Biol.19 ( 6 ), 669 – 673 ( 2012 ).
  • Li X , XuC , YangP . c-Jun NH2-terminal kinase 1/2 and endoplasmic reticulum stress as interdependent and reciprocal causation in diabetic embryopathy . Diabetes62 ( 2 ), 599 – 608 ( 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.