An interaction network in Bacillus subtilis coproporphyrinogen oxidase is essential for the oxidation of protoporphyrinogen IX.
coproporphyrinogen oxidase
kinetics
molecular dynamics simulation
protoporphyrinogen oxidase
site-directed mutagenesis
Journal
Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
20
02
2023
received:
21
12
2022
accepted:
01
04
2023
medline:
13
7
2023
pubmed:
27
4
2023
entrez:
27
4
2023
Statut:
ppublish
Résumé
Coproporphyrinogen oxidase (CPO) plays important role in the biosynthesis of heme by catalyzing the coproporphyrinogen III to coproporphyrin III. However, in earlier research, it was regarded as the protoporphyrinogen oxidase (PPO) because it can also catalyze the oxidation of protoporphyrinogen IX to protoporphyrin IX. Identification of the commonalities in CPO and PPO would help us to get a further understanding of the enzyme function. In this work, we explored the role of a non-conserved residue, Asp65 in Bacillus subtilis CPO (bsCPO), whose corresponding residues in PPO from various species are neutral or positive residue (arginine in human PPO or asparagine in tobacco PPO, etc.). We found that Asp65 performs its function by forming a polar interaction network with its surrounding residues in bsCPO, which is important for enzymatic activity. This polar network maintains the substrate binding chamber and stabilizes the micro-environment of the isoalloxazine ring of FAD for the substrate-FAD interaction. Both the comparison of the crystal structures of bsCPO with PPO and our previous work showed that a similar polar interaction network is also present in PPOs. The results confirmed our conjecture that non-conserved residues can form a conserved element to maintain the function of CPO or PPO.
Substances chimiques
Coproporphyrinogen Oxidase
EC 1.3.3.3
protoporphyrinogen
7412-77-3
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1163-1172Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Dailey HA, Gerdes S, Dailey TA, Burch JS, Phillips JD. Noncanonical coproporphyrin-dependent bacterial heme biosynthesis pathway that does not use protoporphyrin. Proc Natl Acad Sci U S A. 2015;112(7):2210-2215.
Hamza I, Dailey HA. One ring to rule them all: trafficking of heme and heme synthesis intermediates in the metazoans. Biochim Biophys Acta. 2012;1823(9):1617-1632.
Poulson R. The enzymic conversion of protoporphyrinogen IX to protoporphyrin IX in mammalian mitochondria. J Biol Chem. 1976;251(12):3730-3733.
Layer G, Reichelt J, Jahn D, Heinz DW. Structure and function of enzymes in heme biosynthesis. Protein Sci. 2010;19(6):1137-1161.
Dailey HA, Dailey TA, Gerdes S, et al. Prokaryotic heme biosynthesis: multiple pathways to a common essential product. Microbiol Mol Biol Rev. 2017;81(1):e00048-16.
Duke SO, Lydon J, Becerril JM, Sherman TD, Lehnen LP Jr, Matsumoto H. Protoporphyrinogen oxidase-inhibiting herbicides. Weed Sci. 1991;39:465-473.
Wang D-W, Zhang R-B, Yu S-Y, et al. Discovery of novel N-Isoxazolinylphenyltriazinones as promising protoporphyrinogen IX oxidase inhibitors. J Agric Food Chem. 2019;67(45):12382-12392.
Zuo Y, Wu Q, Su S-w, Niu C-w, Xi Z, Yang G-F. Synthesis, herbicidal activity, and QSAR of novel N-benzothiazolyl- pyrimidine-2,4-diones as protoporphyrinogen oxidase inhibitors. J Agric Food Chem. 2016;64(3):552-562.
Liang L, Yu S, Li Q, Wang X, Wang D, Xi Z. Design, synthesis, and molecular simulation studies of N-phenyltetrahydroquinazolinones as protoporphyrinogen IX oxidase inhibitors. Bioorg Med Chem. 2021;39:116165.
Wang D-W, Li Q, Wen K, et al. Synthesis and herbicidal activity of pyrido[2,3-d]pyrimidine-2,4-dione-benzoxazinone hybrids as protoporphyrinogen oxidase inhibitors. J Agric Food Chem. 2017;65(26):5278-5286.
Deybach JC, de Verneuil H, Nordmann Y. The inherited enzymatic defect in porphyria variegata. Hum Genet. 1981;58(4):425-428.
Meissner PN, Corrigall AV, Hift RJ. Fifty years of porphyria at the University of Cape Town. S Afr Med J. 2012;102(6):422-426.
Zhang F, Tang WJ, Hedtke B, et al. Tetrapyrrole biosynthetic enzyme protoporphyrinogen IX oxidase 1 is required for plastid RNA editing. Proc Natl Acad Sci U S A. 2014;111(5):2023-2028.
Li J, Zhang F, Li Y, Yang W, Lin R. Chloroplast-localized protoporphyrinogen IX Oxidase1 is involved in the mitotic cell cycle in Arabidopsis. Plant Cell Physiol. 2019;60(11):2436-2448.
Sun L, Wen X, Tan Y, et al. Site-directed mutagenesis and computational study of the Y366 active site in Bacillus subtilis protoporphyrinogen oxidase. Amino Acids. 2009;37(3):523-530.
Qin X, Tan Y, Wang L, et al. Structural insight into human variegate porphyria disease. FASEB J. 2011;25(2):653-664.
Qin X, Sun L, Wen X, et al. Structural insight into unique properties of protoporphyrinogen oxidase from Bacillus subtilis. J Struct Biol. 2010;170(1):76-82.
Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R, Messerschmidt A. Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J. 2004;23(8):1720-1728.
Corradi HR, Corrigall AV, Boix E, et al. Crystal structure of protoporphyrinogen oxidase from Myxococcus xanthus and its complex with the inhibitor acifluorfen. J Biol Chem. 2006;281(50):38625-38633.
Hansson M, Hederstedt L. Bacillus subtilis HemY is a peripheral membrane protein essential for protoheme IX synthesis which can oxidize coproporphyrinogen III and protoporphyrinogen IX. J Bacteriol. 1994;176(19):5962-5970.
Corrigall AV, Siziba KB, Maneli MH, et al. Purification of and kinetic studies on a cloned protoporphyrinogen oxidase from the aerobic bacterium Bacillus subtilis. Arch Biochem Biophys. 1998;358(2):251-256.
Lee HJ, Lee SB, Chung JS, et al. Transgenic rice plants expressing a Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. Plant Cell Physiol. 2000;41(6):743-749.
Wang B, Zhang Z, Zhu H, Niu C, Wen X, Xi Z. The hydrogen bonding network involved Arg59 in human protoporphyrinogen IX oxidase is essential for enzyme activity. Biochem Biophys Res Commun. 2021;557:20-25.
Meissner PN, Day RS, Moore MR, Disler PB, Harley E. Protoporphyrinogen oxidase and porphobilinogen deaminase in variegate porphyria. Eur J Clin Invest. 1986;16(3):257-261.
Maneli MH, Corrigall AV, Klump HH, Davids LM, Kirsch RE, Meissner PN. Kinetic and physical characterisation of recombinant wild-type and mutant human protoporphyrinogen oxidases. Biochim Biophys Acta Proteins Proteom. 2003;1650(1-2):10-21.
Meissner PN, Dailey TA, Hift RJ, et al. A R59W mutation in human protoporphyrinogen oxidase results in decreased enzyme activity and is prevalent in South Africans with variegate porphyria. Nat Genet. 1996;13(1):95-97.
Wang B, Wen X, Qin X, et al. Quantitative structural insight into human variegate porphyria disease. J Biol Chem. 2013;288(17):11731-11740.
Brenner DA, Bloomer JR. A fluorometric assay for measurement of protoporphyrinogen oxidase activity in mammalian tissue. Clin Chim Acta. 1980;100(3):259-266.
Retzlaff K, Böger P. An endoplasmic reticulum plant enzyme has protoporphyrinogen IX oxidase activity. Pest Biochem Physiol. 1996;54(2):105-114.
Wang JM, Wang W, Kollman PA, Case DA. Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model. 2006;25(2):247-260.
Darden T, York D, Pedersen L. Particle Mesh Ewald - an N.Log(N) method for Ewald sums in large systems. J Chem Phys. 1993;98(12):10089-10092.
Ryckaert JP, Ciccotti G, Berendsen HJC. Numerical-integration of cartesian equations of motion of a system with constraints - molecular-dynamics of N-alkanes. J Comput Phys. 1977;23(3):327-341.
Berendsen HJC, Postma JPM, Vangunsteren WF, Dinola A, Haak JR. Molecular-dynamics with coupling to an external bath. J Chem Phys. 1984;81(8):3684-3690.
Binda C, Coda A, Angelini R, Federico R, Ascenzi P, Mattevi A. A 30-angstrom-long U-shaped catalytic tunnel in the crystal structure of polyamine oxidase. Structure. 1999;7(3):265-276.
Neeli R, Roitel O, Scrutton NS, Munro AW. Switching pyridine nucleotide specificity in P450 BM3: mechanistic analysis of the W1046H and W1046A enzymes. J Biol Chem. 2005;280(18):17634-17644.
Boateng MO, Corrigall AV, Sturrock E, Meissner PN. Characterisation of the flavin adenine dinucleotide binding region of Myxococcus xanthus protoporphyrinogen oxidase. Biochem Biophys Rep. 2015;4:306-311.
Warshel A. Computer Modelling of Chemical Reactions in Enzymes and Solutions. Wiley; 1991.
Warshel A, Levitt M. Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol. 1976;103(2):227-249.
Oanca G, Asadi M, Saha A, Ramachandran B, Warshel A. Exploring the catalytic reaction of cysteine proteases. J Phys Chem B. 2020;124(50):11349-11356.
Prah A, Purg M, Stare J, Vianello R, Mavri J. How monoamine oxidase a decomposes serotonin: an empirical valence bond simulation of the reactive step. J Phys Chem B. 2020;124(38):8259-8265.
Bauer P, Barrozo A, Purg M, et al. Q6: a comprehensive toolkit for empirical valence bond and related free energy calculations. SoftwareX. 2018;7:388-395.
Zhao LN, Mondal D, Warshel A. Exploring alternative catalytic mechanisms of the Cas9 HNH domain. Proteins Struct Funct Genet. 2020;88(2):260-264.
Warshel A, Weiss RM. An empirical valence bond approach for comparing reactions in solutions and in enzymes. J Am Chem Soc. 1980;102(20):6218-6226.
Kamerlin SC, Warshel A. The EVB as a quantitative tool for formulating simulations and analyzing biological and chemical reactions. Faraday Discuss. 2010;145:71-106.
Bonk BM, Weis JW, Tidor B. Machine learning identifies chemical characteristics that promote enzyme catalysis. J Am Chem Soc. 2019;141(9):4108-4118.
Blomberg R, Kries H, Pinkas DM, et al. Precision is essential for efficient catalysis in an evolved Kemp eliminase. Nature. 2013;503(7476):418-421.
Kiss G, Röthlisberger D, Baker D, Houk KN. Evaluation and ranking of enzyme designs. Prot Sci. 2010;19(9):1760-1773.
Heinemann I, Diekmann N, Masoumi A, et al. Functional definition of the tobacco protoporphyrinogen IX oxidase substrate-binding site. Biochem J. 2007;402:575-580.