Kinetics and thermodynamics of metal‐binding to histone deacetylase 8
dc.contributor.author | Kim, Byungchul | en_US |
dc.contributor.author | Pithadia, Amit S. | en_US |
dc.contributor.author | Fierke, Carol A. | en_US |
dc.date.accessioned | 2015-03-05T18:24:13Z | |
dc.date.available | 2016-05-10T20:26:27Z | en |
dc.date.issued | 2015-03 | en_US |
dc.identifier.citation | Kim, Byungchul; Pithadia, Amit S.; Fierke, Carol A. (2015). "Kinetics and thermodynamics of metal‐binding to histone deacetylase 8." Protein Science 24(3): 354-365. | en_US |
dc.identifier.issn | 0961-8368 | en_US |
dc.identifier.issn | 1469-896X | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/110703 | |
dc.description.abstract | Histone deacetylase 8 (HDAC8) was originally classified as a Zn(II)‐dependent deacetylase on the basis of Zn(II)‐dependent HDAC8 activity in vitro and illumination of a Zn(II) bound to the active site. However, in vitro measurements demonstrated that HDAC8 has higher activity with a bound Fe(II) than Zn(II), although Fe(II)‐HDAC8 rapidly loses activity under aerobic conditions. These data suggest that in the cell HDAC8 could be activated by either Zn(II) or Fe(II). Here we detail the kinetics, thermodynamics, and selectivity of Zn(II) and Fe(II) binding to HDAC8. To this end, we have developed a fluorescence anisotropy assay using fluorescein‐labeled suberoylanilide hydroxamic acid (fl‐SAHA). fl‐SAHA binds specifically to metal‐bound HDAC8 with affinities comparable to SAHA. To measure the metal affinity of HDAC, metal binding was coupled to fl‐SAHA and assayed from the observed change in anisotropy. The metal KD values for HDAC8 are significantly different, ranging from picomolar to micromolar for Zn(II) and Fe(II), respectively. Unexpectedly, the Fe(II) and Zn(II) dissociation rate constants from HDAC8 are comparable, koff ∼0.0006 s−1, suggesting that the apparent association rate constant for Fe(II) is slow (∼3 × 103 M−1 s−1). Furthermore, monovalent cations (K+ or Na+) that bind to HDAC8 decrease the dissociation rate constant of Zn(II) by ≥100‐fold for K+ and ≥10‐fold for Na+, suggesting a possible mechanism for regulating metal exchange in vivo. The HDAC8 metal affinities are comparable to the readily exchangeable Zn(II) and Fe(II) concentrations in cells, consistent with either or both metal cofactors activating HDAC8. | en_US |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.subject.other | monovalent cations | en_US |
dc.subject.other | metal‐binding mechanism | en_US |
dc.subject.other | fl‐SAHA | en_US |
dc.subject.other | histone deacetylase 8 | en_US |
dc.title | Kinetics and thermodynamics of metal‐binding to histone deacetylase 8 | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Biological Chemistry | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/110703/1/pro2623.pdf | |
dc.identifier.doi | 10.1002/pro.2623 | en_US |
dc.identifier.source | Protein Science | en_US |
dc.identifier.citedreference | Gantt SL, Joseph CG, Fierke CA ( 2010 ) Activation and inhibition of histone deacetylase 8 by monovalent cations. J Biol Chem 285: 6036 – 6043. | en_US |
dc.identifier.citedreference | Hurst TK, Wang D, Thompson RB, Fierke CA ( 2010 ) Carbonic anhydrase II‐based metal ion sensing: Advances and new perspectives. Biochim Biophys Acta 1804: 393 – 403. | en_US |
dc.identifier.citedreference | Kasner SE, Ganz MB ( 1992 ) Regulation of intracellular potassium in mesangial cells: a fluorescence analysis using the dye, PBFI. Am J Physiol 262: F462 – F467. | en_US |
dc.identifier.citedreference | Borin ML, Goldman WF, Blaustein MP ( 1993 ) Intracellular free Na+ in resting and activated A7r5 vascular smooth muscle cells. Am J Physiol 264: C1513 – C1524. | en_US |
dc.identifier.citedreference | Tripp BC, Bell CB, 3rd, Cruz F, Krebs C, Ferry JG ( 2004 ) A role for iron in an ancient carbonic anhydrase. J Biol Chem 279: 6683 – 6687. | en_US |
dc.identifier.citedreference | D'Souza V M, Holz RC ( 1999 ) The methionyl aminopeptidase from Escherichia coli can function as an iron(II) enzyme. Biochemistry 38: 11079 – 11085. | en_US |
dc.identifier.citedreference | Porter DJ, Austin EA ( 1993 ) Cytosine deaminase. The roles of divalent metal ions in catalysis. J Biol Chem 268: 24005 – 24011. | en_US |
dc.identifier.citedreference | Seffernick JL, McTavish H, Osborne JP, de Souza ML, Sadowsky MJ, Wackett LP ( 2002 ) Atrazine chlorohydrolase from Pseudomonas sp. strain ADP is a metalloenzyme. Biochemistry 41: 14430 – 14437. | en_US |
dc.identifier.citedreference | Gattis SG ( 2010 ) Mechanism and metal specificity of zinc‐dependent deacetylases. PhD. Thesis. University of Michigan, pp 143 – 145. | en_US |
dc.identifier.citedreference | Waldron KJ, Rutherford JC, Ford D, Robinson NJ ( 2009 ) Metalloproteins and metal sensing. Nature 460: 823 – 830. | en_US |
dc.identifier.citedreference | Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV ( 1999 ) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284: 805 – 808. | en_US |
dc.identifier.citedreference | O'Halloran TV, Culotta VC ( 2000 ) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275: 25057 – 25060. | en_US |
dc.identifier.citedreference | Shi H, Bencze KZ, Stemmler TL, Philpott CC ( 2008 ) A cytosolic iron chaperone that delivers iron to ferritin. Science 320: 1207 – 1210. | en_US |
dc.identifier.citedreference | Nandal A, Ruiz JC, Subramanian P, Ghimire‐Rijal S, Sinnamon RA, Stemmler TL, Bruick RK, Philpott CC ( 2011 ) Activation of the HIF prolyl hydroxylase by the iron chaperones PCBP1 and PCBP2. Cell Metab 14: 647 – 657. | en_US |
dc.identifier.citedreference | Frey AG, Nandal A, Park JH, Smith PM, Yabe T, Ryu MS, Ghosh MC, Lee J, Rouault TA, Park MH, Philpott CC ( 2014 ) Iron chaperones PCBP1 and PCBP2 mediate the metallation of the dinuclear iron enzyme deoxyhypusine hydroxylase. Proc Natl Acad Sci USA 111: 8031 – 8036. | en_US |
dc.identifier.citedreference | Joshi P, Greco TM, Guise AJ, Luo Y, Yu F, Nesvizhskii AI, Cristea IM ( 2013 ) The functional interactome landscape of the human histone deacetylase family. Mol Syst Biol 9: 1 – 21. | en_US |
dc.identifier.citedreference | Thompson RB, Maliwal BP, Fierke CA ( 1998 ) Determination of metal ions by fluorescence anisotropy exhibits a broad dynamic range. Adv Opt Biophys 3256: 51 – 59. | en_US |
dc.identifier.citedreference | Suhling K, Siegel J, Lanigan PM, Leveque‐Fort S, Webb SE, Phillips D, Davis DM, French PM ( 2004 ) Time‐resolved fluorescence anisotropy imaging applied to live cells. Opt Lett 29: 584 – 586. | en_US |
dc.identifier.citedreference | Levitt JA, Matthews DR, Ameer‐Beg SM, Suhling K ( 2009 ) Fluorescence lifetime and polarization‐resolved imaging in cell biology. Curr Opin Biotechnol 20: 28 – 36. | en_US |
dc.identifier.citedreference | Wang D, Hurst TK, Thompson RB, Fierke CA ( 2011 ) Genetically encoded ratiometric biosensors to measure intracellular exchangeable zinc in Escherichia coli. J Biomed Opt 16: 1 – 11. | en_US |
dc.identifier.citedreference | Huang CC, Lesburg CA, Kiefer LL, Fierke CA, Christianson DW ( 1996 ) Reversal of the hydrogen bond to zinc ligand histidine‐119 dramatically diminishes catalysis and enhances metal equilibration kinetics in carbonic anhydrase II. Biochemistry 35: 3439 – 3446. | en_US |
dc.identifier.citedreference | Kiefer LL, Paterno SA, Fierke CA ( 1995 ) Hydrogen‐bond network in the metal‐binding site of carbonic‐anhydrase enhances zinc affinity and catalytic efficiency. J Am Chem Soc 117: 6831 – 6837. | en_US |
dc.identifier.citedreference | Strahl BD, Allis CD ( 2000 ) The language of covalent histone modifications. Nature 403: 41 – 45. | en_US |
dc.identifier.citedreference | Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M ( 2009 ) Lysine acetylation targets protein complexes and co‐regulates major cellular functions. Science 325: 834 – 840. | en_US |
dc.identifier.citedreference | Wolfson NA, Pitcairn CA, Fierke CA ( 2013 ) HDAC8 substrates: histones and beyond. Biopolymers 99: 112 – 126. | en_US |
dc.identifier.citedreference | Khochbin S, Verdel A, Lemercier C, Seigneurin‐Berny D ( 2001 ) Functional significance of histone deacetylase diversity. Curr Opin Genet Dev 11: 162 – 166. | en_US |
dc.identifier.citedreference | Gregoretti IV, Lee YM, Goodson HV ( 2004 ) Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol 338: 17 – 31. | en_US |
dc.identifier.citedreference | Blander G, Guarente L ( 2004 ) The Sir2 family of protein deacetylases. Annu Rev Biochem 73: 417 – 435. | en_US |
dc.identifier.citedreference | Finnin MS, Donigian JR, Cohen A, Richon VM, Rifkind RA, Marks PA, Breslow R, Pavletich NP ( 1999 ) Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401: 188 – 193. | en_US |
dc.identifier.citedreference | Marek M, Kannan S, Hauser AT, Moraes Mourão M, Caby S, Cura V, Stolfa DA, Schmidtkunz K, Lancelot J, Andrade L, Renaud JP, Oliveira G, Sippl W, Jung M, Cavarelli J, Pierce RJ, Romier C ( 2013 ) Structural basis for the inhibition of histone deacetylase 8 (HDAC8), a key epigenetic player in the blood fluke Schistosoma mansoni. PLoS Pathog 9: 1 – 15. | en_US |
dc.identifier.citedreference | Dowling DP, Gattis SG, Fierke CA, Christianson DW ( 2010 ) Structures of metal‐substituted human histone deacetylase 8 provide mechanistic inferences on biological function. Biochemistry 49: 5048 – 5056. | en_US |
dc.identifier.citedreference | Lohman TM, Mascotti DP ( 1992 ) Thermodynamics of ligand‐nucleic acid interactions. Methods Enzymol 212: 400 – 424. | en_US |
dc.identifier.citedreference | Dowling DP, Gantt SL, Gattis SG, Fierke CA, Christianson DW ( 2008 ) Structural studies of human histone deacetylase 8 and its site‐specific variants complexed with substrate and inhibitors. Biochemistry 47: 13554 – 13563. | en_US |
dc.identifier.citedreference | Vannini A, Volpari C, Gallinari P, Jones P, Mattu M, Carfi A, De Francesco R, Steinkuhler C, Di Marco S ( 2007 ) Substrate binding to histone deacetylases as shown by the crystal structure of the HDAC8‐substrate complex. EMBO Rep 8: 879 – 884. | en_US |
dc.identifier.citedreference | McCall KA, Fierke CA ( 2004 ) Probing determinants of the metal ion selectivity in carbonic anhydrase using mutagenesis. Biochemistry 43: 3979 – 3986. | en_US |
dc.identifier.citedreference | Gantt SL, Gattis SG, Fierke CA ( 2006 ) Catalytic activity and inhibition of human histone deacetylase 8 is dependent on the identity of the active site metal ion. Biochemistry 45: 6170 – 6178. | en_US |
dc.identifier.citedreference | Christianson DW, Cox JD ( 1999 ) Catalysis by metal‐activated hydroxide in zinc and manganese metalloenzymes. Annu Rev Biochem 68: 33 – 57. | en_US |
dc.identifier.citedreference | Auld DS ( 2001 ) Zinc coordination sphere in biochemical zinc sites. Biometals 14: 271 – 313. | en_US |
dc.identifier.citedreference | Hernick M, Fierke CA ( 2005 ) Zinc hydrolases: the mechanisms of zinc‐dependent deacetylases. Arch Biochem Biophys 433: 71 – 84. | en_US |
dc.identifier.citedreference | Becker A, Schlichting I, Kabsch W, Groche D, Schultz S, Wagner AF ( 1998 ) Iron center, substrate recognition and mechanism of peptide deformylase. Nat Struct Biol 5: 1053 – 1058. | en_US |
dc.identifier.citedreference | Zhu J, Dizin E, Hu X, Wavreille AS, Park J, Pei D ( 2003 ) S ‐Ribosylhomocysteinase (LuxS) is a mononuclear iron protein. Biochemistry 42: 4717 – 4726. | en_US |
dc.identifier.citedreference | Gattis SG, Hernick M, Fierke CA ( 2010 ) Active site metal ion in UDP‐3‐O‐((R)−3‐Hydroxymyristoyl)‐ N ‐acetylglucosamine deacetylase (LpxC) switches between Fe(II) and Zn(II) depending on cellular conditions. J Biol Chem 285: 33788 – 33796. | en_US |
dc.identifier.citedreference | Hernick M, Gattis SG, Penner‐Hahn JE, Fierke CA ( 2010 ) Activation of Escherichia coli UDP‐3‐O‐[(R)−3‐hydroxymyristoyl]‐ N ‐acetylglucosamine deacetylase by Fe2+ yields a more efficient enzyme with altered ligand affinity. Biochemistry 49: 2246 – 2255. | en_US |
dc.identifier.citedreference | Wegener D, Wirsching F, Riester D, Schwienhorst A ( 2003 ) A fluorogenic histone deacetylase assay well suited for high‐throughput activity screening. Chem Biol 10: 61 – 68. | en_US |
dc.identifier.citedreference | Mazitschek R, Patel V, Wirth DF, Clardy J ( 2008 ) Development of a fluorescence polarization based assay for histone deacetylase ligand discovery. Bioorg Med Chem Lett 18: 2809 – 2812. | en_US |
dc.identifier.citedreference | Singh RK, Mandal T, Balasubramanian N, Cook G, Srivastava DK ( 2011 ) Coumarin‐suberoylanilide hydroxamic acid as a fluorescent probe for determining binding affinities and off‐rates of histone deacetylase inhibitors. Anal Biochem 408: 309 – 315. | en_US |
dc.identifier.citedreference | Kristoffersen AS, Erga SR, Hamre B, Frette O ( 2014 ) Testing fluorescence lifetime standards using two‐photon excitation and time‐domain instrumentation: rhodamine B, coumarin 6 and lucifer yellow. J Fluoresc 24: 1015 – 1024. | en_US |
dc.identifier.citedreference | Takagai Y, Nojiri Y, Takase T, Hinze WL, Butsugan M, Igarashi S ( 2010 ) "Turn‐on" fluorescent polymeric microparticle sensors for the determination of ammonia and amines in the vapor state. Analyst 135: 1417 – 1425. | en_US |
dc.identifier.citedreference | Zheng H, Zhan XQ, Bian QN, Zhang XJ ( 2013 ) Advances in modifying fluorescein and rhodamine fluorophores as fluorescent chemosensors. Chem Comm 49: 429 – 447. | en_US |
dc.identifier.citedreference | Martin MM, Lindqvist L ( 1975 ) pH‐dependence of fluorescein fluorescence. J Lumin 10: 381 – 390. | en_US |
dc.identifier.citedreference | Irving H, Williams RJP ( 1948 ) Order of stability of metal complexes. Nature 162: 746 – 747. | en_US |
dc.identifier.citedreference | Outten CE, O'Halloran TV ( 2001 ) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292: 2488 – 2492. | en_US |
dc.identifier.citedreference | Wang D, Hosteen O, Fierke CA ( 2012 ) ZntR‐mediated transcription of zntA responds to nanomolar intracellular free zinc. J Inorg Biochem 111: 173 – 181. | en_US |
dc.identifier.citedreference | Vinkenborg JL, Nicolson TJ, Bellomo EA, Koay MS, Rutter GA, Merkx M ( 2009 ) Genetically encoded FRET sensors to monitor intracellular Zn2+ homeostasis. Nat Methods 6: 737 – 740. | en_US |
dc.identifier.citedreference | Bozym RA, Thompson RB, Stoddard AK, Fierke CA ( 2006 ) Measuring picomolar intracellular exchangeable zinc in PC‐12 cells using a ratiometric fluorescence biosensor. ACS Chem Biol 1: 103 – 111. | en_US |
dc.identifier.citedreference | Qin Y, Dittmer PJ, Park JG, Jansen KB, Palmer AE ( 2011 ) Measuring steady‐state and dynamic endoplasmic reticulum and Golgi Zn2+ with genetically encoded sensors. Proc Natl Acad Sci USA 108: 7351 – 7356. | en_US |
dc.identifier.citedreference | Petrat F, de Groot H, Rauen U ( 2001 ) Subcellular distribution of chelatable iron: a laser scanning microscopic study in isolated hepatocytes and liver endothelial cells. Biochem J 356: 61 – 69. | en_US |
dc.identifier.citedreference | Meguro R, Asano Y, Odagiri S, Li C, Iwatsuki H, Shoumura K ( 2007 ) Nonheme‐iron histochemistry for light and electron microscopy: a historical, theoretical and technical review. Arch Histol Cytol 70: 1 – 19. | en_US |
dc.identifier.citedreference | Esposito BP, Epsztejn S, Breuer W, Cabantchik ZI ( 2002 ) A review of fluorescence methods for assessing labile iron in cells and biological fluids. Anal Biochem 304: 1 – 18. | en_US |
dc.identifier.citedreference | MacKenzie EL, Iwasaki K, Tsuji Y ( 2008 ) Intracellular iron transport and storage: from molecular mechanisms to health implications. Antioxid Redox Signal 10: 997 – 1030. | en_US |
dc.identifier.citedreference | Singh RK, Lall N, Leedahl TS, McGillivray A, Mandal T, Haldar M, Mallik S, Cook G, Srivastava DK ( 2013 ) Kinetic and thermodynamic rationale for suberoylanilide hydroxamic acid being a preferential human histone deacetylase 8 inhibitor as compared to the structurally similar ligand, trichostatin a. Biochemistry 52: 8139 – 8149. | en_US |
dc.identifier.citedreference | Pearson RG ( 1963 ) Hard and soft acids and bases. J Am Chem Soc 85: 3533 – 3539. | en_US |
dc.identifier.citedreference | Fersht AR ( 2000 ) Transition‐state structure as a unifying basis in protein‐folding mechanisms: contact order, chain topology, stability, and the extended nucleus mechanism. Proc Natl Acad Sci USA 97: 1525 – 1529. | en_US |
dc.identifier.citedreference | Vannini A, Volpari C, Filocamo G, Casavola EC, Brunetti M, Renzoni D, Chakravarty P, Paolini C, De Francesco R, Gallinari P, Steinkühler C, Di Marco S ( 2004 ) Crystal structure of a eukaryotic zinc‐dependent histone deacetylase, human HDAC8, complexed with a hydroxamic acid inhibitor. Proc Natl Acad Sci USA 101: 15064 – 15069. | en_US |
dc.identifier.citedreference | Somoza JR, Skene RJ, Katz BA, Mol C, Ho JD, Jennings AJ, Luong C, Arvai A, Buggy JJ, Chi E, Tang J, Sang BC, Verner E, Wynands R, Leahy EM, Dougan DR, Snell G, Navre M, Knuth MW, Swanson RV, McRee DE, Tari LW ( 2004 ) Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure 12: 1325 – 1334. | en_US |
dc.identifier.citedreference | Borin ML, Goldman WF, Blaustein MP ( 1993 ) Intracellular free Na+ in resting and activated A7r5 vascular smooth‐muscle cells. Am J Physiol 264: C1513 – C1524. | en_US |
dc.identifier.citedreference | Woehl EU, Dunn MF ( 1995 ) The roles of Na+ and K+ in pyridoxal‐phosphate enzyme catalysis. Coord Chem Rev 144: 147 – 197. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.