Peptide methionine sulfoxide reductase contributes to the maintenance of adhesins in three major pathogens.

Pathogenic bacteria rely on adhesins to bind to host tissues. Therefore, the maintenance of the functional properties of these extracellular macromolecules is essential for the pathogenicity of these microorganisms. We report that peptide methionine sulfoxide reductase (MsrA), a repair enzyme, contributes to the maintenance of adhesins in Streptococcus pneumoniae, Neisseria gonorrhoeae, and Escherichia coli. A screen of a library of pneumococcal mutants for loss of adherence uncovered a MsrA mutant with 75% reduced binding to GalNAcbeta1-4Gal containing eukaryotic cell receptors that are present on type II lung cells and vascular endothelial cells. Subsequently, it was shown that an E. coli msrA mutant displayed decreased type I fimbriae-mediated, mannose-dependent, agglutination of erythrocytes. Previous work [Taha, M. K., So, M., Seifert, H. S., Billyard, E. & Marchal, C. (1988) EMBO J. 7, 4367-4378] has shown that mutants with defects in the pilA-pilB locus from N. gonorrhoeae were altered in their production of type IV pili. We show that pneumococcal MsrA and gonococcal PilB expressed in E. coli have MsrA activity. Together these data suggest that MsrA is required for the proper expression or maintenance of functional adhesins on the surfaces of these three major pathogenic bacteria.

[1]  C. Rosenow,et al.  Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae , 1996, Molecular microbiology.

[2]  Magdalene So,et al.  The Neisseria Transcriptional Regulator PilA Has a GTPase Activity (*) , 1995, The Journal of Biological Chemistry.

[3]  R. Fleischmann,et al.  The Minimal Gene Complement of Mycoplasma genitalium , 1995, Science.

[4]  E. Tuomanen,et al.  Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor , 1995, Nature.

[5]  R. Fleischmann,et al.  Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. , 1995, Science.

[6]  H. Masure,et al.  Peptide permeases from Streptococcus pneumoniae affect adherence to eucaryotic cells , 1995, Infection and immunity.

[7]  C. Arvidson,et al.  Interaction of the Neisseria gonorrhoeae PilA protein with the pilE promoter involves multiple sites on the DNA , 1995, Journal of bacteriology.

[8]  J. Pinkner,et al.  FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Tuomanen,et al.  Relationship between colonial morphology and adherence of Streptococcus pneumoniae , 1995, Infection and immunity.

[10]  M. Taha,et al.  Phosphorylation and functional analysis of PilA, a protein involved in the transcriptional regulation of the pilin gene in Neisseria gonorrhoeae , 1995, Molecular microbiology.

[11]  N. Brot,et al.  Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage , 1995, Journal of bacteriology.

[12]  E. Campbell,et al.  The rec locus, a competence-induced operon in Streptococcus pneumoniae , 1995, Journal of bacteriology.

[13]  E. Tuomanen,et al.  Receptor specificity of adherence of Streptococcus pneumoniae to human type-II pneumocytes and vascular endothelial cells in vitro. , 1994, Microbial pathogenesis.

[14]  A. Merz,et al.  The opaH locus of Neisseria gonorrhoeae MS11A is involved in epithelial cell invasion , 1994, Molecular microbiology.

[15]  M. Tuite,et al.  Protein disulphide isomerase: building bridges in protein folding. , 1994, Trends in biochemical sciences.

[16]  C. Vargas,et al.  Identification of a gene encoding a thioredoxin-like product necessary for cytochrome c biosynthesis and symbiotic nitrogen fixation in Rhizobium leguminosarum , 1994, Journal of bacteriology.

[17]  H. Masure,et al.  Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization , 1994, Infection and immunity.

[18]  H. Masure,et al.  Peptide permeases modulate transformation in Streptococcus pneumoniae , 1994, Molecular microbiology.

[19]  C. Georgopoulos,et al.  The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation. , 1994, The EMBO journal.

[20]  R. Durbin,et al.  2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans , 1994, Nature.

[21]  K. Schulze-Osthoff,et al.  Distinct effects of thioredoxin and antioxidants on the activation of transcription factors NF-kappa B and AP-1. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[22]  I. Ofek,et al.  Bacterial Adhesion to Cells and Tissues , 1994, Springer US.

[23]  H. Masure,et al.  Genetic identification of exported proteins in Streptococcus pneumoniae , 1993, Molecular microbiology.

[24]  C. Georgopoulos,et al.  Identification and characterization of the Escherichia coli gene dsbB, whose product is involved in the formation of disulfide bonds in vivo. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. Baeuerle,et al.  H2O2 and antioxidants have opposite effects on activation of NF‐kappa B and AP‐1 in intact cells: AP‐1 as secondary antioxidant‐responsive factor. , 1993, The EMBO journal.

[26]  E. Tuomanen,et al.  The cell wall mediates pneumococcal attachment to and cytopathology in human endothelial cells , 1993, Infection and immunity.

[27]  J. Tomb A periplasmic protein disulfide oxidoreductase is required for transformation of Haemophilus influenzae Rd. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[28]  C. Higgins,et al.  ABC transporters: from microorganisms to man. , 1992, Annual review of cell biology.

[29]  B. Dupuy,et al.  Role of pilA, an essential regulatory gene of Neisseria gonorrhoeae, in the stress response , 1992, Journal of bacteriology.

[30]  J. Eaton,et al.  Multicellular oxidant defense in unicellular organisms. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Yodoi,et al.  Thiordoxin regulates the DNA binding activity of NF-χB by reduction of a disulphid bond involving cysteine 62 , 1992 .

[32]  N. Brot,et al.  Cloning, sequencing, and expression of the Escherichia coli peptide methionine sulfoxide reductase gene. , 1992, The Journal of biological chemistry.

[33]  N. Brot,et al.  High level expression and purification of peptide methionine sulfoxide reductase in Escherichia coli. , 1992, Cellular and molecular biology.

[34]  John Walker,et al.  A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae , 1992, Nucleic Acids Res..

[35]  R. Taylor,et al.  Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Koreaki Ito,et al.  Identification and characterization of an Escherichia coli gene required for the formation of correctly folded alkaline phosphatase, a periplasmic enzyme. , 1992, The EMBO journal.

[37]  J. Beckwith,et al.  Identification of a protein required for disulfide bond formation in vivo , 1991, Cell.

[38]  R. Ohayon,et al.  Mechanism of hydrogen peroxide formation catalyzed by NADPH oxidase in thyroid plasma membrane. , 1991, The Journal of biological chemistry.

[39]  W. Saurin,et al.  Control of pilus expression in Neisseria gonorrhoeae as an original system in the family of two‐component regulators , 1991, Molecular microbiology.

[40]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[41]  C. Deal,et al.  Lacto- and ganglio-series glycolipids are adhesion receptors for Neisseria gonorrhoeae. , 1990, The Journal of biological chemistry.

[42]  F. Galibert,et al.  Cloning, nucleotide sequence, and expression of the Rhodobacter sphaeroides Y thioredoxin gene , 1990, Journal of bacteriology.

[43]  A. Holmgren Thioredoxin and glutaredoxin systems , 1989 .

[44]  H. Sambrook Molecular cloning : a laboratory manual. Cold Spring Harbor, NY , 1989 .

[45]  H. Seifert,et al.  Pilin expression in Neisseria gonorrhoeae is under both positive and negative transcriptional control. , 1988, The EMBO journal.

[46]  D. Roberts,et al.  Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[47]  E. Beachey,et al.  Isolation and characterization of a receptor for type 1 fimbriae of Escherichia coli from guinea pig erythrocytes. , 1988, The Journal of biological chemistry.

[48]  C. Parsot Evolution of biosynthetic pathways: a common ancestor for threonine synthase, threonine dehydratase and D‐serine dehydratase. , 1986, The EMBO journal.

[49]  I. J. Evans,et al.  A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria , 1986, Nature.

[50]  B. Koellreutter,et al.  Oligomannoside-type glycopeptides inhibiting adhesion of Escherichia coli strains mediated by type 1 pili: preparation of potent inhibitors from plant glycoproteins , 1986, Infection and immunity.

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

[52]  T. Meyer,et al.  Role of chromosomal rearrangement in N. gonorrhoeae pilus phase variation , 1985, Cell.

[53]  J. Devereux,et al.  A comprehensive set of sequence analysis programs for the VAX , 1984, Nucleic Acids Res..

[54]  L. Beaman,et al.  The role of oxygen and its derivatives in microbial pathogenesis and host defense. , 1984, Annual review of microbiology.

[55]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[56]  G. Magnusson,et al.  Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells , 1983, The Journal of experimental medicine.

[57]  N. Brot,et al.  Biochemistry and physiological role of methionine sulfoxide residues in proteins. , 1983, Archives of biochemistry and biophysics.

[58]  N. Brot,et al.  Reduction of N-acetyl methionine sulfoxide: a simple assay for peptide methionine sulfoxide reductase. , 1982, Analytical biochemistry.

[59]  N. Brot,et al.  Enzymatic reduction of oxidized alpha-1-proteinase inhibitor restores biological activity. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[60]  N. Brot,et al.  Enzymatic reduction of protein-bound methionine sulfoxide. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. Fox,et al.  Marker discrimination in transformation and mutation of pneumococcus. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Douglas S. Kellogg,et al.  NEISSERIA GONORRHOEAE I , 1963, Journal of bacteriology.

[63]  S. Lacks,et al.  A study of the genetic material determining an enzyme activity in Pneumococcus , 1960 .