Diversity of structures and properties among catalases

More than 300 catalase sequences are now available, divided among monofunctional catalases (> 225), bifunctional catalase-peroxidases (> 50) and manganese-containing catalases (> 25). When combined with the recent appearance of crystal structures from at least two representatives from each of these groups (nine from the monofunctional catalases), valuable insights into the catalatic reaction mechanism in its various forms and into catalase evolution have been gained. The structures have revealed an unusually large number of modifications unique to catalases, a result of interacting with reactive oxygen species. Biochemical and physiological characterization of catalases from many different organisms has revealed a surprisingly wide range of catalatic efficiencies, despite similar sequences. Catalase gene expression in micro-organisms generally is controlled either by sensors of reactive oxygen species or by growth phase regulons, although the detailed mechanisms vary considerably.

[1]  Ignacio Fita,et al.  Characterization of the Catalase-Peroxidase KatG from Burkholderia pseudomallei by Mass Spectrometry* , 2003, Journal of Biological Chemistry.

[2]  J. Bravo,et al.  Truncation and heme pocket mutations reduce production of functional catalase HPII in Escherichia coli. , 1998, Protein engineering.

[3]  J. Roe,et al.  A developmentally regulated catalase required for proper differentiation and osmoprotection of Streptomyces coelicolor , 2000, Molecular microbiology.

[4]  R. Haas,et al.  Cloning and genetic characterization of Helicobacter pylori catalase and construction of a catalase-deficient mutant strain , 1996, Journal of bacteriology.

[5]  A. Anderson,et al.  Response of Plant-Colonizing Pseudomonads to Hydrogen Peroxide , 1989, Applied and environmental microbiology.

[6]  M. Jaquinod,et al.  High‐resolution structure and biochemical properties of a recombinant Proteus mirabilis catalase depleted in iron , 2002, Proteins.

[7]  M. Klotz,et al.  Multiple periplasmic catalases in phytopathogenic strains of Pseudomonas syringae , 1992, Applied and environmental microbiology.

[8]  C. Betzel,et al.  Crystal structure of catalase HPII from Escherichia coli. , 1995, Structure.

[9]  S. Mongkolsuk,et al.  Heterologous growth phase- and temperature-dependent expression and H2O2 toxicity protection of a superoxide-inducible monofunctional catalase gene from Xanthomonas oryzae pv. oryzae , 1996, Journal of bacteriology.

[10]  H. Atomi,et al.  Unique Presence of a Manganese Catalase in a Hyperthermophilic Archaeon, Pyrobaculum calidifontis VA1 , 2002, Journal of bacteriology.

[11]  S. Foster,et al.  PerR Controls Oxidative Stress Resistance and Iron Storage Proteins and Is Required for Virulence in Staphylococcus aureus , 2001, Infection and Immunity.

[12]  D. Touati,et al.  Cloning and characterization of the katA gene of Rhizobium meliloti encoding a hydrogen peroxide-inducible catalase , 1996, Journal of bacteriology.

[13]  A. Mauk,et al.  Modulation of the activities of catalase-peroxidase HPI of Escherichia coli by site-directed mutagenesis. , 2000, Biochemistry.

[14]  J. Sacchettini,et al.  Modification of the NADH of the isoniazid target (InhA) from Mycobacterium tuberculosis. , 1998, Science.

[15]  C. Obinger,et al.  Total Conversion of Bifunctional Catalase-Peroxidase (KatG) to Monofunctional Peroxidase by Exchange of a Conserved Distal Side Tyrosine* , 2003, Journal of Biological Chemistry.

[16]  B. Ames,et al.  Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium , 1985, Cell.

[17]  G. Hausner,et al.  Molecular evolutionary analysis based on the amino acid sequence of catalase , 1993, Journal of Molecular Evolution.

[18]  H. Schellhorn,et al.  Induction of resistance to hydrogen peroxide and radiation in Deinococcus radiodurans. , 1995, Canadian journal of microbiology.

[19]  P. Loewen,et al.  Diversity of properties among catalases. , 2002, Archives of biochemistry and biophysics.

[20]  P. Loewen,et al.  An Electrical Potential in the Access Channel of Catalases Enhances Catalysis* , 2003, Journal of Biological Chemistry.

[21]  W. Bishai,et al.  A peroxide/ascorbate-inducible catalase from Haemophilus influenzae is homologous to the Escherichia coli katE gene product , 1994, Journal of bacteriology.

[22]  S V Evans,et al.  SETOR: hardware-lighted three-dimensional solid model representations of macromolecules. , 1993, Journal of molecular graphics.

[23]  N. Tanaka,et al.  Crystallization and preliminary X-ray analysis of catalase-peroxidase from the halophilic archaeon Haloarcula marismortui. , 2001, Acta crystallographica. Section D, Biological crystallography.

[24]  Takao Sato,et al.  The 2.0 Å crystal structure of catalase-peroxidase from Haloarcula marismortui , 2002, Nature Structural Biology.

[25]  T. J. Reid,et al.  Structure of beef liver catalase. , 1981, Journal of molecular biology.

[26]  S. Cole,et al.  The catalase—peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis , 1992, Nature.

[27]  S. Girotto,et al.  Conformational differences in Mycobacterium tuberculosis catalase-peroxidase KatG and its S315T mutant revealed by resonance Raman spectroscopy. , 2003, Biochemistry.

[28]  A. Hochman,et al.  Three different types of catalases in Klebsiella pneumoniae. , 1989, Archives of biochemistry and biophysics.

[29]  M. Klotz,et al.  Phylogenetic relationships among prokaryotic and eukaryotic catalases. , 1997, Molecular biology and evolution.

[30]  S. Mongkolsuk,et al.  Expression analysis and characterization of the mutant of a growth-phase- and starvation-regulated monofunctional catalase gene from Xanthomonas campestris pv. phaseoli. , 2000, Gene.

[31]  P. Nicholls,et al.  A mechanism for NADPH inhibition of catalase compound II formation , 1992, FEBS letters.

[32]  P. Fawcett,et al.  The Global Transcriptional Response of Bacillus subtilis to Peroxide Stress Is Coordinated by Three Transcription Factors , 2003, Journal of bacteriology.

[33]  G. Storz,et al.  OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[34]  G J Kleywegt,et al.  Detection, delineation, measurement and display of cavities in macromolecular structures. , 1994, Acta crystallographica. Section D, Biological crystallography.

[35]  P. Loewen,et al.  Catalase HPII from Escherichia coli exhibits enhanced resistance to denaturation. , 1999, Biochemistry.

[36]  Jeffrey D Laskin,et al.  UVB Light Stimulates Production of Reactive Oxygen Species , 2003, Journal of Biological Chemistry.

[37]  S. Encarnación,et al.  Only one catalase, katG, is detectable in Rhizobium etli, and is encoded along with the regulator OxyR on a plasmid replicon. , 2003, Microbiology.

[38]  P. Alzari,et al.  Crystallization and preliminary X-ray analysis of the hydroperoxidase I C-terminal domain from Escherichia coli. , 2002, Acta crystallographica. Section D, Biological crystallography.

[39]  D. Hicks Purification of three catalase isozymes from facultatively alkaliphilic Bacillus firmus OF4. , 1995, Biochimica et biophysica acta.

[40]  S. Girotto,et al.  Identification and Characterization of Tyrosyl Radical Formation in Mycobacterium tuberculosisCatalase-Peroxidase (KatG)* , 2002, The Journal of Biological Chemistry.

[41]  J. Aguirre,et al.  Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress , 1997, Journal of bacteriology.

[42]  H. E. Heath,et al.  Plasmid-encoded catalase of Staphylococcus simulans biovar staphylolyticus. , 1994, FEMS microbiology letters.

[43]  D. Hassett,et al.  Ferric uptake regulator (Fur) mutants of Pseudomonas aeruginosa demonstrate defective siderophore-mediated iron uptake, altered aerobic growth, and decreased superoxide dismutase and catalase activities , 1996, Journal of bacteriology.

[44]  T. Sato,et al.  Susceptibility to hydrogen peroxide and catalase activity of root nodule bacteria. , 1999, Bioscience, biotechnology, and biochemistry.

[45]  F. Fang,et al.  The alternative sigma factor katF (rpoS) regulates Salmonella virulence. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Murthy,et al.  The refined structure of beef liver catalase at 2·5 Å resolution , 1986 .

[47]  D. Hassett,et al.  Bacterioferritin A Modulates Catalase A (KatA) Activity and Resistance to Hydrogen Peroxide in Pseudomonas aeruginosa , 1999, Journal of bacteriology.

[48]  B. Doble,et al.  Nucleotide sequence of katG, encoding catalase HPI of Escherichia coli , 1988, Journal of bacteriology.

[49]  G. Peschek,et al.  Effect of Distal Cavity Mutations on the Formation of Compound I in Catalase-Peroxidases* , 2000, The Journal of Biological Chemistry.

[50]  Markus Auer,et al.  Distal site aspartate is essential in the catalase activity of catalase-peroxidases. , 2003, Biochemistry.

[51]  J. Helmann,et al.  Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors , 1998, Molecular microbiology.

[52]  D. Ortiz de Orué Lucana,et al.  The mycelium-associated Streptomyces reticuli catalase-peroxidase, its gene and regulation by FurS. , 1999, Microbiology.

[53]  T. C. Bruice,et al.  Electron tunneling and ab initio calculations related to the one-electron oxidation of NAD(P)H bound to catalase. , 1995, Biochemistry.

[54]  J. Aguirre,et al.  Posttranscriptional Control Mediates Cell Type-Specific Localization of Catalase A during Aspergillus nidulans Development , 1998, Journal of bacteriology.

[55]  J. Mayfield,et al.  Identification of Brucella abortus OxyR and Its Role in Control of Catalase Expression , 2000, Journal of bacteriology.

[56]  E. Ruby,et al.  The Periplasmic, Group III Catalase of Vibrio fischeriIs Required for Normal Symbiotic Competence and Is Induced Both by Oxidative Stress and by Approach to Stationary Phase , 1998, Journal of bacteriology.

[57]  P. Nicholls,et al.  Enzymology and structure of catalases , 2000 .

[58]  S. Foster,et al.  In Staphylococcus aureus, Fur Is an Interactive Regulator with PerR, Contributes to Virulence, and Is Necessary for Oxidative Stress Resistance through Positive Regulation of Catalase and Iron Homeostasis , 2001, Journal of bacteriology.

[59]  O. Dideberg,et al.  Crystal structure of Proteus mirabilis PR catalase with and without bound NADPH. , 1995, Journal of molecular biology.

[60]  C. Obinger,et al.  The catalytic role of the distal site asparagine-histidine couple in catalase-peroxidases. , 2003, European journal of biochemistry.

[61]  B. Vainshtein,et al.  Three-dimensional structure of the enzyme catalase , 1981, Nature.

[62]  M. Field,et al.  Ligand diffusion in the catalase from Proteus mirabilis: A molecular dynamics study , 2001, Protein science : a publication of the Protein Society.

[63]  V. Deretic,et al.  Mycobacterial FurA is a negative regulator of catalase–peroxidase gene katG , 2001, Molecular microbiology.

[64]  Wilming,et al.  Spontaneous Formation of the Bioactive Form of the Tuberculosis Drug Isoniazid. , 1999, Angewandte Chemie.

[65]  G. Stauffer,et al.  Nucleotide sequence of katG of Salmonella typhimurium LT2 and characterization of its product, hydroperoxidase I , 1990, Molecular and General Genetics MGG.

[66]  B. Vainshtein,et al.  Three‐dimensional structure of catalase from Micrococcus lysodeikticus at 1.5 Å resolution , 1992, FEBS letters.

[67]  I. Kim,et al.  Transcription of ahpC, katG, and katE genes in Escherichia coli is regulated by polyamines: polyamine-deficient mutant sensitive to H2O2-induced oxidative damage. , 2003, Biochemical and biophysical research communications.

[68]  H. Duckworth,et al.  Hydroperoxidase II of Escherichia coli exhibits enhanced resistance to proteolytic cleavage compared to other catalases. , 2003, Biochemistry.

[69]  G. Allgood,et al.  Characterization of a manganese-containing catalase from the obligate thermophile Thermoleophilum album , 1986, Journal of bacteriology.

[70]  D. Bol,et al.  Analysis of the dual regulatory mechanisms controlling expression of the vegetative catalase gene of Bacillus subtilis , 1994, Journal of bacteriology.

[71]  P. Harrison,et al.  Three-dimensional structure of the enzyme dimanganese catalase from Thermus Thermophilus at 1 Å resolution , 2000 .

[72]  I. von Ossowski,et al.  Catalase HPII of Escherichia coli catalyzes the conversion of protoheme to cis-heme d. , 1993, Biochemistry.

[73]  P. Loewen,et al.  Catalase-peroxidase KatG of Burkholderia pseudomallei at 1.7A resolution. , 2003, Journal of molecular biology.

[74]  B. Lei,et al.  Action Mechanism of Antitubercular Isoniazid , 2000, The Journal of Biological Chemistry.

[75]  J. W. Whittaker,et al.  Crystal structure of manganese catalase from Lactobacillus plantarum. , 2001, Structure.

[76]  P. Setlow,et al.  The katX Gene, Which Codes for the Catalase in Spores of Bacillus subtilis, Is a Forespore-Specific Gene Controlled by ςF, and KatX Is Essential for Hydrogen Peroxide Resistance of the Germinating Spore , 1998, Journal of bacteriology.

[77]  D. Rouse,et al.  Site‐directed mutagenesis of the katG gene of Mycobacterium tuberculosis: effects on catalase–peroxidase activities and isoniazid resistance , 1996, Molecular microbiology.

[78]  A. Ferraris,et al.  Mechanisms of Protection of Catalase by NADPH , 1999, The Journal of Biological Chemistry.

[79]  S. Cole,et al.  Regulation of catalase–peroxidase (KatG) expression, isoniazid sensitivity and virulence by furA of Mycobacterium tuberculosis , 2001, Molecular microbiology.

[80]  M. Klotz,et al.  The molecular evolution of catalatic hydroperoxidases: evidence for multiple lateral transfer of genes between prokaryota and from bacteria into eukaryota. , 2003, Molecular biology and evolution.

[81]  I. Fridovich,et al.  Purification of the o-dianisidine peroxidase from Escherichia coli B. Physicochemical characterization and analysis of its dual catalatic and peroxidatic activities. , 1979, The Journal of biological chemistry.

[82]  J. Hahn,et al.  H2O2-sensitive Fur-like Repressor CatR Regulating the Major Catalase Gene in Streptomyces coelicolor* , 2000, The Journal of Biological Chemistry.

[83]  Stefania Girotto,et al.  Reduced Affinity for Isoniazid in the S315T Mutant ofMycobacterium tuberculosis KatG Is a Key Factor in Antibiotic Resistance* , 2003, The Journal of Biological Chemistry.

[84]  J. Bravo,et al.  Crystallization and preliminary structural analysis of catalase A from Saccharomyces cerevisiae , 1997, Protein science : a publication of the Protein Society.

[85]  J. Tainer,et al.  Active and inhibited human catalase structures: ligand and NADPH binding and catalytic mechanism. , 2000, Journal of molecular biology.

[86]  Huijun Wei,et al.  Aspergillus nidulans Catalase-Peroxidase Gene (cpeA) Is Transcriptionally Induced during Sexual Development through the Transcription Factor StuA , 2002, Eukaryotic Cell.

[87]  C. Obinger,et al.  The role of distal tryptophan in the bifunctional activity of catalase-peroxidases. , 2001, Biochemical Society transactions.

[88]  E. Meir,et al.  Catalase-negative mutants ofEscherichia coli , 2005, Current Microbiology.

[89]  S. Cole,et al.  Use of site-directed mutagenesis to probe the structure, function and isoniazid activation of the catalase/peroxidase, KatG, from Mycobacterium tuberculosis. , 1999, The Biochemical journal.

[90]  O. Almarsson,et al.  Mechanism of one-electron oxidation of NAD(P)H and function of NADPH bound to catalase , 1993 .

[91]  C. Betzel,et al.  Structure of catalase-A from Saccharomyces cerevisiae. , 1999, Journal of molecular biology.

[92]  J. Hahn,et al.  Regulation of the furA and catC Operon, Encoding a Ferric Uptake Regulator Homologue and Catalase-Peroxidase, Respectively, in Streptomyces coelicolor A3(2) , 2000, Journal of bacteriology.

[93]  D. Hassett,et al.  Role of the Pseudomonas aeruginosa oxyR-recG Operon in Oxidative Stress Defense and DNA Repair: OxyR-Dependent Regulation of katB-ankB, ahpB, andahpC-ahpF , 2000, Journal of bacteriology.

[94]  A. Beckhouse,et al.  Resistance to hydrogen peroxide in Helicobacter pylori: role of catalase (KatA) and Fur, and functional analysis of a novel gene product designated 'KatA-associated protein', KapA (HP0874). , 2002, Microbiology.

[95]  M. Tamoi,et al.  Crystallization and preliminary X-ray diffraction studies of catalase-peroxidase from Synechococcus PCC 7942. , 2002, Acta crystallographica. Section D, Biological crystallography.

[96]  J. Visser,et al.  Induction of glucose oxidase, catalase, and lactonase in Aspergillus niger , 1993, Current Genetics.

[97]  P. Loewen,et al.  Catalases HPI and HPII in Escherichia coli are induced independently. , 1985, Archives of biochemistry and biophysics.

[98]  S. Engelmann,et al.  Cloning, nucleotide sequence, and regulation of katE encoding a sigma B-dependent catalase in Bacillus subtilis , 1995, Journal of bacteriology.

[99]  G. Owens,et al.  The Redox-Sensitive Transcriptional Activator OxyR Regulates the Peroxide Response Regulon in the Obligate AnaerobeBacteroides fragilis , 2000, Journal of bacteriology.

[100]  M. Klotz,et al.  Structure of the Clade 1 catalase, CatF of Pseudomonas syringae, at 1.8 Å resolution , 2003, Proteins.

[101]  J. Musser,et al.  Molecular genetic basis of antimicrobial agent resistance in Mycobacterium tuberculosis: 1998 update. , 1998, Tubercle and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[102]  J. Aguirre,et al.  Multiple Catalase Genes Are Differentially Regulated in Aspergillus nidulans , 2001, Journal of bacteriology.

[103]  M. Klotz,et al.  Crystallization and preliminary X-ray analysis of clade I catalases from Pseudomonas syringae and Listeria seeligeri. , 2001, Acta crystallographica. Section D, Biological crystallography.

[104]  H N Kirkman,et al.  Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[105]  M. Ibañez-Ruiz,et al.  Identification of a non‐haem catalase in Salmonella and its regulation by RpoS (σS) , 2001, Molecular microbiology.

[106]  M. Orozco,et al.  Theoretical study of the mechanisms of substrate recognition by catalase. , 2001, Journal of the American Chemical Society.

[107]  Kaewkanya Nakjarung,et al.  The oxyR from Agrobacterium tumefaciens: evaluation of its role in the regulation of catalase and peroxide responses. , 2003, Biochemical and biophysical research communications.

[108]  K. Wilson,et al.  Structure of catalase HPII from Escherichia coli at 1.9 Å resolution , 1999, Proteins.

[109]  K. Welinder Bacterial catalase-peroxidases are gene duplicated members of the plant peroxidase superfamily. , 1991, Biochimica et biophysica acta.

[110]  M. Ueda,et al.  Structure-function study of the amino-terminal stretch of the catalase subunit molecule in oligomerization, heme binding, and activity expression , 2003, Applied Microbiology and Biotechnology.

[111]  W. Doolittle,et al.  Horizontal transfer of catalase-peroxidase genes between archaea and pathogenic bacteria. , 2000, Trends in genetics : TIG.

[112]  A. Puppo,et al.  Differential Regulation of Two Divergent Sinorhizobium meliloti Genes for HPII-Like Catalases during Free-Living Growth and Protective Role of Both Catalases during Symbiosis , 1999, Journal of bacteriology.

[113]  A. McEwan,et al.  OxyR Acts as a Repressor of Catalase Expression in Neisseria gonorrhoeae , 2003, Infection and Immunity.

[114]  P. Loewen,et al.  Crystallization and preliminary X-ray analysis of the catalase-peroxidase KatG from Burkholderia pseudomallei. , 2002, Acta crystallographica. Section D, Biological crystallography.