Author for correspondence: Clayton H. Johnson or Joan E. McEwen. Tel: +1 501 257 5559. Fax: +1 501 257 4820. e-mail: johnsonclaytonh@uams.edu or mcewenjoane@uams.edu
Histoplasma capsulatum produces an extracellular catalase termed M antigen, which is similar to catalase B of Aspergillus and Emericella species. Evidence is presented here for two additional catalase isozymes in H. capsulatum. Catalase A is highly similar to a large-subunit catalase in Aspergillus and Emericella species, while catalase P is a small-subunit catalase protein with greatest similarity to known peroxisomal catalases of animals and Saccharomycotina yeasts. Complete cDNAs for the CATA and CATP genes (encoding catalases A and P, respectively) were isolated. The transcriptional expression of the H. capsulatum CATA, CATB (M antigen) and CATP genes was assessed by Northern blot hybridizations on total RNA. Results at the transcript levels for these genes are shown for three conditions: cell morphology (mycelial versus yeast phase cells), oxidative stress (in response to a challenge with H2O2) and carbon source (glucose vs glycerol). Collectively, these results demonstrated regulation of CATA by both cell morphology and oxidative stress, but not by carbon source, and regulation of CATB and CATP by carbon source but not cell morphology or oxidative stress. A phylogenetic analysis of presently available catalase sequences and intron residences was done. The results support a model for evolution of eukaryotic monofunctional catalase genes from prokaryotic genes.
BeamanB. L.,
ScatesS. M.,
MoringS. E.,
DeemR.,
MisraH. P.
1983; Purification and properties of a unique superoxide dismutase from Nocardia asteroides
. J Biol Chem 258:91–96
BullockW. E.,
WrightS. D.
1987; Role of the adherence-promoting receptors, CR3, LFA-1, and p150,95, in binding of Histoplasma capsulatum by human macrophages. J Exp Med 165:195–210[CrossRef]
CaleraJ. A.,
ParisS.,
MonodM.,
HamiltonA. J.,
DebeaupuisJ. P.,
DiaquinM.,
Lopez-MedranoR.,
LealF.,
LatgéJ. P.
1997; Cloning and disruption of the antigenic catalase gene of Aspergillus fumigatus
. Infect Immun 65:4718–4724
CarpenaX.,
PerezR.,
OchoaW. F.,
VerdaguerN.,
KlotzM. G.,
SwitalaJ.,
Melik-AdamyanW.,
FitaI.,
LoewenP. C.
2001; Crystallization and preliminary X-ray analysis of clade I catalases from Pseudomonas syringae and Listeria seeligeri
. Acta Crystallogr D Biol Crystallogr 57:1184–1186[CrossRef]
CastroK. G.,
WardJ. W.,
SlutskerL.,
BuehlerJ. W.,
JaffeH. W.,
BerkelmanR. L.
1992). ; 1993 Revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. Morb Mortal Wkly Rep 41:1–14
ChangY. C.,
SegalB. H.,
HollandS. M.,
MillerG. F.,
Kwon-ChungK. J.
1998; Virulence of catalase-deficient A spergillus nidulans in p47(phox)–/– mice. Implications for fungal pathogenicity and host defense in chronic granulomatous disease. J Clin Invest 101:1843–1850[CrossRef]
CharyP.,
NatvigD. O.
1989; Evidence for three differentially regulated catalase genes in Neurospora crassa : effects of oxidative stress, heat shock, and development. J Bacteriol 171:2646–2652
DavidsonJ. F.,
WhyteB.,
BissingerP. H.,
SchiestlR. H.
1996; Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae
. Proc Natl Acad Sci USA 93:5116–5121[CrossRef]
DaviesS. F.,
KhanM.,
SarosiG. A.
1978; Disseminated histoplasmosis in immunologically suppressed patients: occurrence in a nonendemic area. Am J Med 64:94–100[CrossRef]
De GrooteM. A.,
OchsnerU. A.,
ShilohM. U.7 other authors1997; Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA 94:13997–14001[CrossRef]
Del SalG.,
ManfiolettiG.,
SchneiderC.
1989; The CTAB-DNA precipitation method: a common mini-scale preparation of template DNA from phagemids, phages or plasmids suitable for sequencing. Biotechniques 7:514–520
EissenbergL. G.,
GoldmanW. E.
1994; The interplay between Histoplasma capsulatum and its host cells. In Baillière’s Clinical Infectious Diseases pp 411–421 Edited by
RussellD.
London: W. B. Saunders;
FangF. C.,
DeGrooteM. A.,
FosterJ. W.8 other authors1999; Virulent Salmonella typhimurium has two periplasmic Cu,Zn-superoxide dismutases. Proc Natl Acad Sci USA 96:7502–7507[CrossRef]
FrugoliJ. A.,
ZhongH. H.,
NuccioM. L.,
McCourtP.,
McPeekM. A.,
ThomasT. L.,
McClungC. R.
1996; Catalase is encoded by a multigene family in Arabidopsis thaliana (L.) Heynh. Plant Physiol 112:327–336[CrossRef]
FrugoliJ. A.,
McPeekM. A.,
ThomasT. L.,
McClungC. R.
1998; Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics 149:355–365
GuanL.,
ScandaliosJ. G.
1996; Molecular evolution of maize catalases and their relationship to other eukaryotic and prokaryotic catalases. J Mol Evol 42:570–579[CrossRef]
HamiltonA. J.,
BartholomewM. A.,
FigueroaJ.,
FenelonL. E.,
HayR. J.
1990; Evidence that the M antigen of Histoplasma capsulatum var. capsulatum is a catalase which exhibits cross-reactivity with other dimorphic fungi. J Med Vet Mycol 28:479–485[CrossRef]
HaymanG. T.,
BolenP. L.
1993; Movement of shuttle plasmids from Escherichia coli into yeasts other than Saccharomyces cerevisiae using trans-kingdom conjugation. Plasmid 30:251–257[CrossRef]
JeavonsL.,
HamiltonA. J.,
VanittanakomN.,
UngpakornR.,
EvansE. G.,
SirisanthanaT.,
HayR. J.
1998; Identification and purification of specific Penicillium marneffei antigens and their recognition by human immune sera. J Clin Microbiol 36:949–954
JohnsonC. H.,
McEwenJ. E.
1999; Isolation of a Histoplasma capsulatum cDNA that complements a mitochondrial NAD(+)-isocitrate dehydrogenase subunit I-deficient mutant of Saccharomyces cerevisiae
. Yeast 15:799–804[CrossRef]
JohnsonC. H.,
SchmidtG. W.
1993; The psbB gene cluster of the Chlamydomonas reinhardtii chloroplast: sequence and transcriptional analyses of psbN and psbH
. Plant Mol Biol 22:645–658[CrossRef]
KameiK.,
BrummerE.,
ClemonsK. V.,
StevensD. A.
1992; Induction of stress protein synthesis in Histoplasma capsulatum by heat, low pH and hydrogen peroxide. J Med Vet Mycol 30:385–393[CrossRef]
KawasakiL.,
WysongD.,
DiamondR.,
AguirreJ.
1997; Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J Bacteriol 179:3284–3292
Lopez-MedranoR.,
OvejeroM. C.,
CaleraJ. A.,
PuenteP.,
LealF.
1995; An immunodominant 90-kilodalton Aspergillus fumigatus antigen is the subunit of a catalase. Infect Immun 63:4774–4780
MarchlerG.,
SchüllerC.,
AdamG.,
RuisH.
1993; A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. EMBO J 12:1997–2003
MarescaB.,
LambowitzA. M.,
KobayashiG. S.,
MedoffG.
1979; Respiration in the yeast and mycelial phases of Histoplasma capsulatum
. J Bacteriol 138:647–649
MarescaB.,
CarratuL.,
KobayashiG. S.
1994; Morphological transition in the human fungal pathogen Histoplasma capsulatum
. Trends Microbiol 2:110–114[CrossRef]
OrrW. C.,
SohalR. S.
1994; Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster
. Science 263:1128–1130[CrossRef]
RambukkanaA.,
DasP. K.,
KolkA. H.,
BurggraafJ. D.,
KuijperS.,
HarboeM.
1993; Identification of a novel 27-kDa protein from Mycobacterium tuberculosis culture fluid by a monoclonal antibody specific for the Mycobacterium tuberculosis complex. Scand J Immunol 37:471–478[CrossRef]
SonnenbergM. G.,
BelisleJ. T.
1997; Definition of Mycobacterium tuberculosis culture filtrate proteins by two-dimensional polyacrylamide gel electrophoresis, N-terminal amino acid sequencing, and electrospray mass spectrometry. Infect Immun 65:4515–4524
SpiegelhalderC.,
GersteneckerB.,
KerstenA.,
SchiltzE.,
KistM.
1993; Purification of Helicobacter pylori superoxide dismutase and cloning and sequencing of the gene. Infect Immun 61:5315–5325
TakasukaT.,
SayersN. M.,
AndersonM. J.,
BenbowE. W.,
DenningD. W.
1999; Aspergillus fumigatus catalases: cloning of an Aspergillus nidulans catalase B homologue and evidence for at least three catalases. FEMS Immunol Med Microbiol 23:125–133[CrossRef]
ThompsonJ. D.,
HigginsD. G.,
GibsonT. J.
1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680[CrossRef]
Vera-CabreraL.,
JohnsonW. M.,
WelshO.,
Resendiz-UrestiF. L.,
Salinas-CarmonaM. C.
1999; Distribution of a Nocardia brasiliensis catalase gene fragment in members of the genera Nocardia, Gordona , and Rhodococcus
. J Clin Microbiol 37:1971–1976
WheatL. J.,
SlamaT. G.,
NortonJ. A.,
KohlerR. B.,
EitzenH. E.,
FrenchM. L.,
SathapatayavongsB.
1982; Risk factors for disseminated or fatal histoplasmosis. Analysis of a large urban outbreak. Ann Intern Med 96:159–163[CrossRef]
WoodsJ. P.,
GoldmanW. E.
1992; In vivo generation of linear plasmids with addition of telomeric sequences by Histoplasma capsulatum
. Mol Microbiol 6:3603–3610[CrossRef]
WorshamP. L.,
GoldmanW. E.
1988; Quantitative plating of Histoplasma capsulatum without addition of conditioned medium or siderophores. J Med Vet Mycol 26:137–143[CrossRef]
Zancope-OliveiraR. M.,
ReissE.,
LottT. J.,
MayerL. W.,
DeepeG. S.Jr1999; Molecular cloning, characterization, and expression of the M antigen of Histoplasma capsulatum
. Infect Immun 67:1947–1953
Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalasesThe GenBank accession numbers for the cDNA sequences reported in this paper are AF139985 (CATB), AF189368 (CATA) and AF189369 (CATP).