The effect of iron starvation on the outer membrane protein composition of Neisseria gonorrhoeae

Norqvist, Astrid

doi:10.1016/0378-1097(78)90090-3

Cited by 26 publications

(41 citation statements)

References 7 publications

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“…Apparently, iron acquisition from transferrin and lactoferrin requires direct contact between the organisms and the proteins (Archibald & DeVoe, 1979;Simonson et al, 1982;McKenna et al, 1988;Morton & Williams, 1990), and involves iron-regulated receptors that exhibit specific recognition properties (Lee & Schryvers, 1988 ;Schryvers, 1988;Schryvers & Morris, 1988a, b ;Tsai et al, 1988;Morton & Williams, 1990;Ogunnariwo & Schryvers, 1990); indeed, the specificities of these receptors for transferrin or lactoferrin from particular animal species afford possible explanations for the host specificities of the organisms and also for the capacities of human transferrin and lactoferrin to enhance meningococcal infections in mice (Schryvers & Gonzalez, 1989). Such receptors are probably IRMPs, and in keeping with this suggestion, IRMPs are known to be produced in vitro by all of the above organisms (Norqvist et al, 1978;Brener et al, 1981 ;Mietzner et al 1984;Herrington & Sparling, 1985;Williams & Brown, 1986;Pidcock et al, 1988;Morton & Williams, 1989;Deneer & Potter, 1989a) and also in vivo, by at least N . meningitidis (Black et al, 1986).…”

Section: Introductionmentioning

confidence: 96%

Isolation and identification of a putative porcine transferrin receptor from Actinobacillus pleuropneumoniae biotype 1

Ricard

Archibald²,

Niven

1991

Journal of General Microbiology

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~ ~ ~~~Each of two affinity isolation methods, the first based on biotinylated porcine transferrin plus streptavidinagarose, and the second on Sepharose-coupled porcine transferrin, followed by SDS-PAGE, allowed the isolation and identification of two potential porcine-transferrin-binding polypeptides ( -64 kDa and 99 kDa) from total membranes of Actinobaciflus pfeuropneumoniae grown under iron-restricted conditions. Both polypeptides were iron-repressible and were identified as potential receptor candidates as they were not isolated when biotinylated human transferrin was used instead of biotinylated porcine transferrin. The 64 kDa polypeptide was the more easily removed from Sepharose-coupled porcine transferrin and only the 99 kDa polypeptide appeared to be an outer-membrane protein. While these results suggest that the 99 kDa polypeptide represents the porcine transferrin receptor of A. pfeuropneumoniae, and that the 64 kDa polypeptide represents an associated protein serving an accessory role, other interpretations are also possible.

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Section: Introductionmentioning

confidence: 96%

Isolation and identification of a putative porcine transferrin receptor from Actinobacillus pleuropneumoniae biotype 1

Ricard

Archibald²,

Niven

1991

Journal of General Microbiology

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“…which have been reported to be introduced during conditions of iron restriction are believed to be concerned with uptake of sequestered iron. However, with the notable exception of continuous culture studies of Neisseriu meningitidis (Archibald & DeVoe, 1978;DeVoe, 1982), these experiments were performed in batch culture with no control over the available iron, oxygen and carbon concentrations nor, indeed, the growth rate, which was greatly reduced (Norqvist et al, 1978;Mietzner et al, 1984;West & Sparling, 1985). We have therefore conducted an in vitro study of the influence of a fluctuating iron supply on the physiology and the regulation of the OMPs of N. gonorrhoeae using the unique advantages of continuous culture (see Keevil et al, 1986).…”

Section: Influence Of Iron-limited and Replete Continuousmentioning

confidence: 99%

Influence of Iron-limited and Replete Continuous Culture on the Physiology and Virulence of Neisseria gonorrhoeae

et al. 1989

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Neisseria gonorrhoeae strains P9-2 (Pens) and KW2 (PenR) were grown in chemostats of nonferrous design at constant growth rate, pH and dissolved oxygen tension. Iron limitation (pmax 0.1 h-l) was imposed by omitting iron salts from the defined medium and titrating increasing concentrations of the non-metabolizable iron chelators ovotransferrin and Desferal, to progressively decrease the growth yield. Metabolic activity during iron limitation was very high, with a qGlc which was 2-or 11-fold greater than during cystine-or glucose-limited growth, respectively. More aspartate and isoleucine were metabolized during cystine-limited growth, while more glutamate, proline and serine were metabolized during glucose-or iron-limited growth. Significant concentrations of alanine or valine were excreted during cystine-or glucoselimited growth, respectively. Iron-limited growth of an initial inoculum of non-piliated, transparent colony-forming (P-0-) gonococci resulted in the selection of 100% piliated bacteria. Initial inocula of P+ 0-gonococci retained this phenotype for over 100 generations. Iron-limited gonococci were extremely virulent in the guinea-pig subcutaneous chamber model and inocula of even 12 bacteria grew rapidly and persisted. By contrast, cystine-limited (ironreplete) gonococci retained piliation but did not survive in the chambers. Transition from ironlimited to glucose-limited growth resulted in marked loss of piliation but the bacteria remained virulent. Loss of virulence did not correlate with susceptibility to killing by normal human serum, nor with changes in the content or composition of lipooligosaccharide, which contained 2.9,3.7,4.3 and 4-8 kDa moieties. Additional proteins were detectable in Sarkosyl-purified outer membranes of iron-limited gonococci but several proteins with molecular masses similar to those described in the literature for iron-restricted gonococci were detectable in cystine-or glucose-limited bacteria. I N T R O D U C T I O NA versatile physiology (Keevil et al., 1986) or rapid antigenic variation in pili (P+), proteins I1 (O+), or other outer-membrane proteins (OMPs) (Heckels, 1984) might explain the ability of Neisseria gonorrhoeae to colonize and persist at anatomically distinct sites despite the host immune response. One important environmental factor which pathogens frequently encounter in Man is iron deprivation. Iron is an essential nutrient for the majority of bacteria, particularly aerobes. Potential pathogens must therefore acquire this nutrient in competition with the host, since many body fluids contain iron-binding proteins (Weinberg, 1978 ;Griffiths, 1983 ;Brown & Williams, 1985). For example, the mucosal surfaces invaded by N. gonorrhoeae secrete t Present address: Department of Microbiology, University of Bristol, Bristol BS8 ITD, UK.$ Present address: Department of Applied Biology, UWIST, Cardiff CF1 3NU, UK.Abbreviations: KDO, 2-keto-3-deoxyoctonate (3-deoxy-~-rnanno-2-otulosonate); MIRP, major iron-regulated protein; OMP, outer-membrane protein. 0001-4838 0 19...

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“…Thus, in establishing infection, the gonococcus must have the ability to adapt readily to a changing host environment. In this study, we investigated this topic by analyzing the protein profiles of conventionally grown, nonstressed, and nutrient-or oxygen-limited, stressed gonococci and found The existence of nutrient-specific regulation of protein synthesis in N. gonorrhoeae has been recognized previously by several investigators (12,28,32,36,62). The availability of iron, for instance, has been found to regulate the synthesis of various cytosolic and membrane proteins, including a number of proteins involved in iron acquisition, probably via the presence of iron-responsive elements adjacent to the genes involved (53).…”

Section: Discussionmentioning

confidence: 99%

“…Likewise, meningococci grown under iron limitation at a low pH are up to 1,200-fold more virulent than meningococci that are grown in conventional complex media (5). The altered virulence has been correlated with various changes in the surface properties of the bacteria (39), including the expression of iron-and oxygen-regulated outer membrane proteins that are not expressed when the bacteria are maintained in complex media (12,32,36,62). The presence of antibodies reactive with such environmentally regulated proteins in the sera of patients with gonorrhea (13,35) indicates that these antigens are expressed during natural infection.…”

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confidence: 99%

Identification and molecular analysis of a 63-kilodalton stress protein from Neisseria gonorrhoeae

1992

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Iron limitation, glucose deprivation, and growth under low oxygen supply (environmental stress) increased the expression of several proteins of Neisseria gonorrhoeae, including a 63-kilodalton protein identified by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. This gonococcal stress protein (GSP63) was detected in the cytosol and copurified with lithium acetate-derived outer membranes. Successful purification of the protein was achieved by sucrose density gradient centrifugation and by chromatography on phenylSepharose. Gel filtration of the purified protein revealed a molecular weight of approximately 450,000, suggesting that in its native state, the protein consists of a multimer of six to eight subunits. Isoelectric focusing indicated a pl of 5.2. Immunoblotting experiments using a polyclonal antiserum raised against the purified protein demonstrated cross-reactivity with a protein of the same electrophoretic mobility as GSP63 in all eight gonococcal isolates tested. N-terminal amino acid sequencing of the protein revealed up to 65% homology with members of the Hsp60 heat shock protein family, suggesting that GSP63 is related to this group of proteins. This relationship was further substantiated by the immunological cross-reactivity of GSP63 with mycobacterial Hsp60 and the ATP-binding activity of the gonococcal stress protein.

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The effect of iron starvation on the outer membrane protein composition of Neisseria gonorrhoeae

Cited by 26 publications

References 7 publications

Isolation and identification of a putative porcine transferrin receptor from Actinobacillus pleuropneumoniae biotype 1

Isolation and identification of a putative porcine transferrin receptor from Actinobacillus pleuropneumoniae biotype 1

Influence of Iron-limited and Replete Continuous Culture on the Physiology and Virulence of Neisseria gonorrhoeae

Identification and molecular analysis of a 63-kilodalton stress protein from Neisseria gonorrhoeae

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