Biochemical, structural, and kinetic characterization of PP
crystallography
enzyme
inhibition
kinetics
Journal
Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
revised:
27
04
2023
received:
03
10
2022
accepted:
04
05
2023
medline:
23
10
2023
pubmed:
25
5
2023
entrez:
25
5
2023
Statut:
ppublish
Résumé
Phosphoenolpyruvate carboxykinases (PEPCK) are a well-studied family of enzymes responsible for the regulation of TCA cycle flux, where they catalyze the interconversion of oxaloacetic acid (OAA) and phosphoenolpyruvate (PEP) using a phosphoryl donor/acceptor. These enzymes have typically been divided into two nucleotide-dependent classes, those that use ATP and those that use GTP. In the 1960's and early 1970's, a group of papers detailed biochemical properties of an enzyme named phosphoenolpyruvate carboxytransphosphorylase (later identified as a third PEPCK) from Propionibacterium freudenreichii (PP
Substances chimiques
Phosphoenolpyruvate
73-89-2
Phosphoenolpyruvate Carboxykinase (ATP)
EC 4.1.1.49
Oxaloacetic Acid
2F399MM81J
Guanosine Triphosphate
86-01-1
Nucleotides
0
Adenosine Triphosphate
8L70Q75FXE
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1261-1275Subventions
Organisme : Natural Sciences and Engineering Research Council of Canada
Informations de copyright
© 2023 The Authors. Proteins: Structure, Function, and Bioinformatics published by Wiley Periodicals LLC.
Références
Jeon JY, Lee H, Park J, et al. The regulation of glucose-6-phosphatase and phosphoenolpyruvate carboxykinase by autophagy in low-glycolytic hepatocellular carcinoma cells. Biochem Biophys Res Commun. 2015;463(3):440-446. doi:10.1016/j.bbrc.2015.05.103
Méndez-Lucas A, Hyroššová P, Novellasdemunt L, Viñals F, Perales JC. Mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M) is a pro-survival, endoplasmic reticulum (ER) stress response gene involved in tumor cell adaptation to nutrient availability. J Biol Chem. 2014;289(32):22090-22102. doi:10.1074/jbc.M114.566927
Montal ED, Dewi R, Bhalla K, et al. PEPCK coordinates the regulation of central carbon metabolism to promote cancer cell growth. Mol Cell. 2015;60(4):571-583. doi:10.1016/j.molcel.2015.09.025
Park JW, Kim SC, Kim WK, et al. Expression of phosphoenolpyruvate carboxykinase linked to chemoradiation susceptibility of human colon cancer cells. BMC Cancer. 2014;14(160):1-12. doi:10.1186/1471-2407-14-160
Marrero J, Rhee KY, Schnappinger D, Pethe K, Ehrt S. Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc Natl Acad Sci U S A. 2010;107(21):9819-9824. doi:10.1073/pnas.1000715107
Yuan Y, Hakimi P, Kao C, et al. Reciprocal changes in phosphoenolpyruvate carboxykinase and pyruvate kinase with age are a determinant of aging in Caenorhabditis elegans. J Biol Chem. 2016;291(3):1307-1319. doi:10.1074/jbc.M115.691766
Santra S, Cameron JM, Shyr C, et al. Cytosolic phosphoenolpyruvate carboxykinase deficiency presenting with acute liver failure following gastroenteritis. Mol Genet Metab. 2016;118(1):21-27. doi:10.1016/j.ymgme.2016.03.001
Yang J, Kalhan SC, Hanson RW. What is the metabolic role of phosphoenolpyruvate Carboxykinase? J Biol Chem. 2009;284(40):27025-27029. doi:10.1074/jbc.R109.040543
Sudom AM, Prasad L, Goldie H, Delbaere LTJ. The phosphoryl-transfer mechanism of Escherichia coli phosphoenolpyruvate carboxykinase from the use of AlF3. J Mol Biol. 2001;314:83-92. doi:10.1006/jmbi.2001.5120
Delbaere LTJ, Sudom AM, Prasad L, Leduc Y, Goldie H. Structure/function studies of phosphoryl transfer by phosphoenolpyruvate carboxykinase. Biochim Biophys Acta. 2004;1697(1):271-278. doi:10.1016/j.bbapap.2003.11.030
Matte A, Goldie H, Sweet RM, Delbaere LTJ. Crystal structure of Escherichia coli phosphoenolpyruvate carboxykinase: a new structural family with the P-loop nucleoside triphosphate hydrolase fold. J Mol Biol. 1996;256(1):126-143. doi:10.1006/jmbi.1996.0072
McLeod MJ, Holyoak T. Phosphoenolpyruvate carboxykinases. Encycloped Biol Chem. 2021;III(3):400-412. doi:10.1016/b978-0-12-819460-7.00226-7
Johnson TA, Holyoak T. Increasing the conformational entropy of the Ω-loop lid domain in phosphoenolpyruvate carboxykinase impairs catalysis and decreases catalytic Fidelity. Biochemistry. 2010;49(25):5176-5187. doi:10.1021/bi100399e
Carlson GM, Holyoak T. Structural insights into the mechanism of phosphoenolpyruvate carboxykinase catalysis. J Biol Chem. 2009;284(40):27037-27041. doi:10.1074/jbc.R109.040568
Sullivan SM, Holyoak T. Enzymes with lid-gated active sites must operate by an induced fit mechanism instead of conformational selection. Proc Natl Acad Sci U S A. 2008;105(37):13829-13834. doi:10.1073/pnas.0805364105
Johnson TA, Mcleod MJ, Holyoak T. Utilization of substrate intrinsic binding energy for conformational change and catalytic function in phosphoenolpyruvate carboxykinase. Biochemistry. 2016;55(3):575-587. doi:10.1021/acs.biochem.5b01215
Johnson TA, Holyoak T. The Ω-loop lid domain of phosphoenolpyruvate carboxykinase is essential for catalytic function. Biochemistry. 2012;51(47):9547-9559. doi:10.1021/bi301278t
Das B, Tandon V, Saxena JK, Joshi S, Singh AR. Purification and characterization of phosphoenolpyruvate carboxykinase from Raillietina echinobothrida, a cestode parasite of the domestic fowl. Parasitology. 2013;140:136-146. doi:10.1017/S0031182012001254
Machová I, Snášel J, Dostál J, et al. Structural and functional studies of phosphoenolpyruvate carboxykinase from mycobacterium tuberculosis. PLoS One. 2015;10(3):1-21. doi:10.1371/journal.pone.0120682
Hebda CA, Nowak T. Phosphoenolpyruvate carboxykinase. Mn2+ and Mn2+ substrate complexes. J Biol Chem. 1982;257(10):5515-5522. doi:10.1016/S0021-9258(19)83807-3
Hidalgo J, Latorre P, Carrodeguas JA, Velázquez-Campoy A, Sancho J, López-Buesa P. Inhibition of pig phosphoenolpyruvate carboxykinase isoenzymes by 3-mercaptopicolinic acid and novel inhibitors. PLoS One. 2016;11(7):1-17. doi:10.1371/journal.pone.0159002
Sokaribo A, Novakovski BAA, Cotelesage J, White AP, Sanders D, Goldie H. Kinetic and structural analysis of Escherichia coli phosphoenolpyruvate carboxykinase mutants. Biochim Biophys Acta Gen Subj. 2020;1864(4):1-7. doi:10.1016/j.bbagen.2020.129517
Escós M, Latorre P, Hidalgo J, Hurtado-Guerrero R, Carrodeguas JA, López-Buesa P. Kinetic and functional properties of human mitochondrial phosphoenolpyruvate carboxykinase. Biochem Biophys Rep. 2016;7:124-129. doi:10.1016/j.bbrep.2016.06.007
Wilkes J, Cornish RA, Mettrick DF. Purification and properties of phosphoenolpyruvate carboxykinase from Ascaris suum. Int J Parasitol. 1982;12(2/3):163-171. doi:10.1016/0020-7519(82)90012-1
Cooper TG, Tchen TT, Wood HG, Benedict CR. The carboxylation of phosphoenolpyruvate and pyruvate: I. The active species of “CO2” utilized by phosphoenolpyruvate carboxykinase, carboxytransphosphorylase, and pyruvate carboxylase. J Biol Chem. 1968;243(14):3857-3863. doi:10.1016/S0021-9258(18)92022-3
Davis JJ, Willard JM, Wood HG. Phosphoenolpyruvate carboxytransphosphorylase. III. Comparison of the fixation of carbon dioxide and the conversion of phosphoenolpyruvate and phosphate into pyruvate and pyrophosphate. Biochemistry. 1969;8(8):3127-3136. doi:10.1021/bi00836a001
Lochmuller H, Wood HG, Davis JJ. Phosphoenolpyruvate Carboxytransphosphorylase: II. Crystallization and Properties J Biol Chem. 1966;241(23):5678-5691. doi:10.1016/S0021-9258(18)96398-2
Willard JM, Rose IA. Formation of Enolpyruvate in the phosphoenolpyruvate Carboxytransphosphorylase reaction. Biochemistry. 1973;12(26):5241-5246. doi:10.1021/bi00750a003
O'Brien WE, Singleton R, Wood HG. Phosphoenolpyruvate carboxytransphosphorylase. An investigation of the mechanism with 18O. Biochemistry. 1973;12(26):5247-5253. doi:10.1021/bi00750a004
O'Brien WE, Wood HG, Carboxytransphosphorylase: VIII. Ligand-mediated interaction of subunits as a possible control mechanism in Propionibacteria. J Biol Chem. 1974;249(15):4917-4925. doi:10.1016/S0021-9258(19)42409-5
Willard JM, Davis JJ, Wood HG. Phosphoenolpyruvate carboxytransphosphorylase. IV. requirement for metal cations. Biochemistry. 1969;8(8):3137-3144. doi:10.1021/bi00836a002
Wood HG, Davis JJ, Willard JM. Phosphoenolpyruvate carboxytransphosphorylase. V. Mechanism of the reaction and the role of metal ions. Biochemistry. 1969;8(8):3145-3155. doi:10.1021/bi00836a003
Hunt M, Kohler P. Purification and characterization of phosphoenolpyruvate carboxykinase from Trypanosma brucei. Biochim Biophys Acta. 1995;1(1249):15-22. doi:10.1016/1067-4838(95)00061-X
Trapani S, Linss J, Goldenberg S, Fischer H, Craievich AF, Oliva G. Crystal structure of the dimeric phosphoenolpyruvate carboxykinase (PEPCK) from Trypanosoma cruzi at 2 Å resolution. J Mol Biol. 2001;313:1059-1072. doi:10.1006/jmbi.2001.5093
Burnell JN. Purification and properties of phosphoenolpyruvate carboxykinase from C4 plants. Aust J Plant Physiol. 1986;13(5):577. doi:10.1071/pp9860577
Tortora P, Hanozet GM, Guerritore A. Purification of phosphoenolpyruvate carboxykinase from Saccharomyces cerevisiae and its use for bicarbonate assay. Anal Biochem. 1985;144(1):179-185. doi:10.1016/0003-2697(85)90101-0
Chiba Y, Kamikawa R, Nakada-Tsukui K, Saito-Nakano Y, Nozaki T. Discovery of PPi-type phosphoenolpyruvate carboxykinase genes in eukaryotes and bacteria. J Biol Chem. 2015;290(39):23960-23970. doi:10.1074/jbc.M115.672907
Chiba Y, Miyakawa T, Shimane Y, Takai K, Tanokura M, Nozaki T. Structural comparisons of phosphoenolpyruvate carboxykinases reveal the evolutionary trajectories of these phosphodiester energy conversion enzymes. J Biol Chem. 2019;294(50):19269-19278. doi:10.1074/jbc.RA119.010920
Studier FW. Protein production by auto-induction in high-density shaking cultures. Protein Expr Purif. 2005;41(1):207-234. doi:10.1016/j.pep.2005.01.016
Gasteiger E, Hoogland C, Gattiker A, et al. Protein identification and analysis tools on the ExPASy server. In: Walker JM, ed. The proteomics protocols handbook. Springer Protocols Handbooks. Humana Press; 2005:571-608. doi:10.1385/1-59259-890-0:571
Otwinowski Z, Minor W. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997;276:307-326. doi:10.1016/S0076-6879(97)76066-X
Stein N. CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. J Appl Cryst. 2008;41(3):641-643. doi:10.1107/S0021889808006985
Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J Appl Cryst. 1997;30(6):1022-1025. doi:10.1107/S0021889897006766
Collaborative computational project 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. 1994;50(5):760-763. doi:10.1107/S0907444994003112
Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. 2004;60(12):2126-2132. doi:10.1107/S0907444904019158
Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. 1997;D53(3):240-255. doi:10.1107/S0907444996012255
Afonine PV, Grosse-Kunstleve RW, Echols N, et al. Towards automated crystallographic structure refinement with phenix.Refine. Acta Crystallogr D Biol Crystallogr. 2012;68(4):352-367. doi:10.1107/S0907444912001308
Chen VB, Arendall WB III, Headd JJ, et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. 2010;66(1):12-21. doi:10.1107/S0907444909042073
Evgeny K, Kim H. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007;372(3):774-797. doi:10.1016/j.jmb.2007.05.022
Tsai CS. Spontaneous decarboxylation of oxalacetic acid. Can J Chem. 1967;46(4):873-890. doi:10.1139/v68-111
Haberland ME, Willard JM, Wood HG. Phosphoenolpyruvate carboxytransphosphorylase. Study of the catalytic and physical structures. Biochemistry. 1972;11(5):712-722. doi:10.1021/bi00755a007
Cui DS, Broom A, McLeod MJ, Meiering EM, Holyoak T. Asymmetric anchoring is required for efficient Ω-loop opening and closing in cytosolic phosphoenolpyruvate Carboxykinase. Biochemistry. 2017;56(15):2106-2115. doi:10.1021/acs.biochem.7b00178
Sullivan SM, Holyoak T. Structures of rat cytosolic PEPCK: insight into the mechanism of phosphorylation and decarboxylation of oxaloacetic acid. Biochemistry. 2007;46(35):10078-10088. doi:10.1021/bi701038x
Wood HG, Stjernholm RL, Leaver-Fay A. The metabolism of labeled glucose by the propionic acid bacteria. J Bacteriol. 1955;70(5):510-520. doi:10.1128/jb.70.5.510-520.1955
Siu PML, Wood HG. Phosphoenolpyruvic carboxytransphosphorylase, a CO2 fixation enzyme from propionic acid bacteria. J Biol Chem. 1962;237(10):3044-3051. doi:10.1016/S0021-9258(18)50118-6
Siu PML, Wood HG, Stjernholm RL. Fixation of CO2 by phosphoenolpyruvic carboxytransphosphorylase. J Biol Chem. 1961;236(4):21-22. doi:10.1016/S0021-9258(18)64271-1
Van Eunen K, Bouwman J, Daran-Lapujade P, et al. Measuring enzyme activities under standardized in vivo-like conditions for systems biology. FEBS J. 2010;277(3):749-760. doi:10.1111/j.1742-4658.2009.07524.x
Greenfield NJ, Hussain M, Lenard J. Effects of growth state and amines on cytoplasmic and vacuolar pH, phosphate and polyphosphate levels in Saccharomyces cerevisiae: a 31P-nuclear magnetic resonance study. Biochim Biophys Acta. 1987;926:205-214. doi:10.1016/0304-4165(87)90205-4
den Hollander JA, Shulman RG, Ugurbil K, Brown TR. Phosphorus-31 nuclear magnetic resonance studies of the effect of oxygen upon glycolysis in yeast. Biochemistry. 1981;20(20):5871-5880. doi:10.1021/bi00523a034
Cornish RA, Wilkes J, Mettrick DF. A study of phosphoenolypyruvate carboxykinase from Moniliformis dubius (Acanthocephala). Mol Biochem Parasitol. 1980;2:151-166. doi:10.1016/0166-6851(81)90096-7
Hunt M, Köhler P. Purification and characterization of phosphoenolpyruvate carboxykinase from Trypanosoma brucei. Biochimica et Biophysica Acta (BBA). 1995;1249(1):15-22. doi:10.1016/0167-4838(95)00061-X
Cymeryng C, Cazzulo JJ, Cannata JBJ. Phosphoenolpyruvate carboxykinase from Trypanosoma cruzi. Purification and physicochemical and kinetic properties. Mol Biochem Parasitol. 1995;73:91-101. doi:10.1016/0166-6851(95)00099-m
Jabalquinto AM, Laivenieks M, Zeikus JG, Cardemil E. Characterization of the oxaloacetate decarboxylase and pyruvate kinase-like activities of Saccharomyces cerevisiae and anaerobiospirillum succiniciproducens phosphoenolpyruvate carboxykinases. J Protein Chem. 1999;18(6):659-664. doi:10.1023/A:1020602222808
Cannata JJB, Stoppani AOM. Phosphopyruvate carboxylase from bakers' yeast. III. The mechanism of oxaloacetate decarboxylation. J Biol Chem. 1963;238(4):3356-3366. doi:10.1016/S0021-9258(18)67920-7
Case CL, Mukhopadhyay B. Kinetic characterization of recombinant human cytosolic phosphoenolpyruvate carboxykinase with and without a His10-tag. Biochim Biophys Acta Gen Subj. 2007;1770(11):1576-1584. doi:10.1016/j.bbagen.2007.07.012
Machová I, Snášel J, Zimmermann M, et al. Mycobacterium tuberculosis phosphoenolpyruvate carboxykinase is regulated by redox mechanisms and interaction with thioredoxin. J Biol Chem. 2014;289(19):13066-13078. doi:10.1074/jbc.M113.536748
Barwell S, Duman R, Wagner A, Holyoak T. Directional regulation of cytosolic PEPCK catalysis is mediated by competitive binding of anions. Biochem Biophys Res Commun. 2022;637:218-223. doi:10.1016/j.bbrc.2022.11.025
Stiffin RM, Sullivan SM, Carlson GM, Holyoak T. Differential inhibition of cytosolic PEPCK by substrate analogues. Kinetic and structural characterization of inhibitor recognition. Biochemistry. 2008;47(7):2099-2109. doi:10.1021/bi7020662
Ash D, Emig F, Chowdhury S, Satoh Y, Schramm V. Mammalian and avian liver phosphoenolpyruvate carboxykinase-alternate substrates and inhibition by analogs of oxaloacetate. J Biol Chem. 1990;265(13):7377-7384. doi:10.1016/S0021-9258(19)39124-0
Makinen AL, Nowak T. 3-Mercaptopicolinate. A reversible active site inhibitor of avian liver phosphoenolpyruvate carboxykinase. J Biol Chem. 1983;258(19):11654-111662. doi:10.1016/S0021-9258(17)44278-5
Balan MD, McLeod MJ, Lotosky WR, Ghaly M, Holyoak T. Inhibition and allosteric regulation of monomeric phosphoenolpyruvate carboxykinase by 3-mercaptopicolinic acid. Biochemistry. 2015;54(38):5878-5887. doi:10.1021/acs.biochem.5b00822
McLeod MJ, Krismanich AP, Assoud A, Dmitrienko GI, Holyoak T. Characterization of 3-[(carboxymethyl)thio]picolinic acid: a novel inhibitor of phosphoenolpyruvate carboxykinase. Biochemistry. 2019;58(37):3918-3926. doi:10.1021/acs.biochem.9b00583
Foley LH, Wang P, Dunten P, Ramsey G, Gubler ML, Wertheimer SJ. X-ray structures of two xanthine inhibitors bound to PEPCK and N-3 modifications of substituted 1,8-Dibenzylxanthines. Bioorg Med Chem Lett. 2003;13(21):3871-3874. doi:10.1016/s0960-894X(03)00723-6
Foley LH, Wang P, Dunten P, Ramsey G, Gubler ML, Wertheimer SJ. Modified 3-alkyl-1,8-dibenzylxanthines as GTP-competitive inhibitors of phosphoenolpyruvate Carboxykinase. Bioorg Med Chem Lett. 2003;13(20):3607-3610. doi:10.1016/s0960-894X(03)00722-4
Jomain-Baum M, Schramm VL. Kinetic mechanism of phosphoenolpyruvate Carboxykinase (GTP) from rat liver cytosol: product inhibition, isotope exchange at equilibrium, and partial reactions. J Biol Chem. 1978;253(10):3648-3659. doi:10.1016/S0021-9258(17)34850-0
Jomain-Baum M, Schramm VL, Hanson RW. Mechanism of 3-mercaptopicolinic acid inhibition of hepatic phosphoenolpyruvate Carboxykinase (GTP). J Biol Chem. 1976;251(1):37-44. doi:10.1016/S0021-9258(17)33923-6
Martell AE, Motekaitis RJ, Chen D, Hancock RD, McManus D. Selection of new Fe(lll)/Fe(ll) chelating agents as catalysts for the oxidation of hydrogen sulfide to sulfur by air. Can J Chem. 1996;74(10):1872-1879. doi:10.1139/v96-210