Effect of hemoglobin and of ferric ammonium citrate on the virulence of periodontopathic bacteria

Mukherjee, Sabyasachi; Murphy, Richard A.; Wawszkiewcz, Edward J.

doi:10.1111/j.1399-302x.1988.tb00009.x

Cited by 9 publications

(7 citation statements)

References 34 publications

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“…It has been proposed that free haemin compounds could be available to bacteria of dental plaque after the haemolysis of erythrocytes present in the crevicular fluid (Mukherjee, 1985). Such a possibility is consistent with the recently reported haemolytic activity associated with the LtxA toxin produced by this pathogen (Balashova et al, 2006) and the observation that haemoglobin but not inorganic iron enhances the virulence of A. actinomycetemcomitans when tested in guinea pigs (Mukherjee et al, 1988). It is not known whether this pathogen uses haemin and haemoglobin by direct binding or by the production of a haemophore, which could scavenge haemin from haemoglobin, as described for other bacteria, such as Serratia marcescens (Wandersman & Delepelaire, 2004).…”

Section: Resultssupporting

confidence: 81%

Evaluation of different iron sources and their influence in biofilm formation by the dental pathogen Actinobacillus actinomycetemcomitans

Rhodes

Shoemaker

Menke

et al. 2007

Journal of Medical Microbiology

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Actinobacillus actinomycetemcomitans, a pathogen associated with oral and extra-oral infections, requires iron to grow under limiting conditions. Although incapable of producing siderophores, this pathogen could acquire iron by direct interaction with compounds such as haemin, haemoglobin, lactoferrin and transferrin. In this work the ability of different A. actinomycetemcomitans strains to bind and use different iron sources was tested. None of the strains tested used haemoglobin, lactoferrin or transferrin as sole sources of iron. However, all of them used FeCl3 and haemin as iron sources under chelated conditions. Dot-blot binding assays showed that all strains bind lactoferrin, haemoglobin and haemin, but not transferrin. Insertion inactivation of hmsF, which encodes a predicted cell-envelope protein related to haemin-storage proteins produced by other pathogens, reduced haemin and Congo red binding drastically without affecting haemin utilization as an iron source under chelated conditions. Biofilm assays showed that all strains tested attached to and formed biofilms on plastic under iron-rich and iron-chelated conditions. However, scanning electron microscopy showed that smooth strains formed simpler biofilms than rough isolates. Furthermore, the incubation of rough cells in the presence of FeCl3 or haemin resulted in the formation of more aggregates and microcolonies compared with the fewer cell aggregates formed when cells were grown in the presence of the synthetic iron chelator dipyridyl. These cell responses to changes in extracellular iron concentrations may reflect those that this pathogen expresses under the conditions it encounters in the human oral cavity.

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Section: Resultssupporting

confidence: 81%

Evaluation of different iron sources and their influence in biofilm formation by the dental pathogen Actinobacillus actinomycetemcomitans

Rhodes

Shoemaker

Menke

et al. 2007

Journal of Medical Microbiology

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“…A large number of studies have convincingly demonstrated that the availability of iron plays a critical role in both the emergence and virulence of a large number of pathogenic species (7, 14-16, 20, 27, 38, 52, 53). We (5,10,21) and several others (9,22,25,30,31,34,41,44) have demonstrated that iron is an important regulatory factor both in P. gingivalis growth and in its expression of virulence. Therefore, an understanding of the role of iron in the growth and virulence of this pathogen in the subgingival environment is of paramount importance in comprehending the possible control of the progression of the periodontal disease process.…”

Section: Discussionmentioning

confidence: 81%

Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50

1991

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Porphyromonas gingivalis (Bacteroides gingivalis) requires iron in the form of hemin for growth and virulence in vitro, but the contributions of the porphyrin ring structure, porphyrin-associated iron, host hemin-sequestering molecules, and host iron-withholding proteins to its survival are unknown. Therefore, the effects of various porphyrins, host iron transport proteins, and inorganic iron sources on the growth of P. gingivalis W50 were examined to delineate the various types of iron molecules used for cellular metabolism. Cell envelope-associated hemin and iron stores contributed to the growth of P. gingivalis in hemin-free culture, and depletion of these endogenous reserves required eight serial transfers into hemin-free medium for total suppression of growth. Comparable growth of P. gingivalis was observed with 7.7 microM equivalents of hemin as hemoglobin (HGB), methemoglobin, myoglobin, hemin-saturated serum albumin, lactoperoxidase, cytochrome c, and catalase. Unrestricted growth was recorded in the presence of haptoglobin-HGB and hemopexin-hemin complexes, indicating that these host defense proteins do not sequester HGB and hemin from P. gingivalis. The iron chelator 2,2'-bipyridyl functionally chelated hemin-associated iron, resulting in dose-dependent inhibition of growth in hemin-restricted cultures at 1 to 25 microM 2,2'-bipyridyl concentrations. In the absence of an exogenous iron source, protoporphyrin IX did not support P. gingivalis growth. These findings suggest that the iron atom in the hemin molecule is the critical constituent for growth and that the tetrapyrrole porphyrin ring structure may represent an important vehicle for delivery of iron into the P. gingivalis cell. P. gingivalis does not have a strict requirement for porphyrins, since growth occurred with nonhemin iron sources, including high concentrations (200 muM) of ferric, ferrous, and nitrogenous inorganic iron, and P. gingivalis exhibited unrestricted growth in the presence of host transferrin, lactoferrin, and serum albumin. The diversity of iron substrates utilized by P. gingivalis and the observation that growth was not affected by the bacteriostatic effects of host iron-withholding proteins, which it may encounter in the periodontal pocket, may explain why P. gingivalis is such a formidable pathogen in the periodontal disease process.

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“…The hemoiytic activity of T. denticola may then favor the growth and establishment of hemin-dependent bacteria such as the black-pigmented bacterial species. Interestingly, a recent study by Mukherjee et al (17) indicated that addition of hemoglobin to a P. gingivalis cell suspension had an enhancing effect on the virulence of this bacteria when injected in an experimental animal model.…”

Section: Discussionmentioning

confidence: 99%

Characteristics of hemolytic and hemagglutinating activities of Treponema denticola

Grenier

1991

Oral Microbiology and Immunology

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Treponema denticola, a suspected periodontal pathogen, was shown to agglutinate and lyse human red blood cells. Both activities were cell-associated, heat-labile, and produced during the exponential growth phase. Hemolytic activity was time-dependent and required incubation at 37 degrees C; further incubation at 4 degrees C increased the hemolysis. Hemagglutination was reduced in the presence of D-glucosamine, EDTA or sodium salicylate, whereas hemolytic activity was affected by calcium chloride, magnesium chloride, EDTA or sodium salicylate. These biological activities may favor a higher concentration of hemin-containing compounds in periodontal sites, and therefore represent additional potential virulence mechanisms.

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Effect of hemoglobin and of ferric ammonium citrate on the virulence of periodontopathic bacteria

Cited by 9 publications

References 34 publications

Evaluation of different iron sources and their influence in biofilm formation by the dental pathogen Actinobacillus actinomycetemcomitans

Evaluation of different iron sources and their influence in biofilm formation by the dental pathogen Actinobacillus actinomycetemcomitans

Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50

Characteristics of hemolytic and hemagglutinating activities of Treponema denticola

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