Intracellular growth and survival of Salmonella enterica serovar Typhimurium carrying truncated hemoglobins of Mycobacterium tuberculosis

Pawaria, Sudesh; Rajamohan, Govindan; Gambhir, Vandana; Lama, Amrita; Varshney, Grish C.; Dikshit, Kanak L.

doi:10.1016/j.micpath.2006.12.001

Cited by 28 publications

(29 citation statements)

References 34 publications

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“…This observation can be correlated to the previously observed function of trHbN to detoxify NO and therefore should be available to the mycobacteria whenever toxic levels of RNI are present. Studies on transcriptional regulation of M. tuberculosis trHbN have shown a significant level of trHbN synthesis during macrophage infection (27), and its NOD activity is sustained under low oxygen (28). In order to combat the rising levels of RNI shortly after infection, myco- bacteria have to respond immediately, and our finding of the highest response at 24 h for the glbN promoter supports this.…”

Section: Discussionsupporting

confidence: 69%

“…Since 30 mM NaNO 2 followed by 5 mM H 2 O 2 induced maximal glbO expression, this can be correlated with the poor protection against . NO toxicity by mycobacterial trHbO compared to that by trHbN (28), indicating that the primary role of trHbO is not in . NO oxidation.…”

Section: Discussionmentioning

confidence: 89%

“…The oxygenated form of trHbN can very efficiently convert NO to harmless nitrate (25,28). The inactivation of the glbN gene of M. bovis BCG impaired the ability of stationary-phase cells of the organism to protect aerobic respiration from NO (24).…”

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confidence: 99%

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Comparative Analysis of Mycobacterial Truncated Hemoglobin Promoters and thegroEL2Promoter in Free-Living and Intracellular Mycobacteria

Joseph

Madhavilatha

Kumar

et al. 2012

Appl Environ Microbiol

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ABSTRACTThe success ofMycobacterium tuberculosisdepends on its ability to withstand and survive the hazardous environment inside the macrophages that are created by reactive oxygen intermediates, reactive nitrogen intermediates, severe hypoxia, low pH, and high CO2levels. Therefore, an effective detoxification system is required for the pathogen to persistin vivo. The genome ofM. tuberculosiscontains a new family of hemoproteins named truncated hemoglobin O (trHbO) and truncated hemoglobin N (trHbN), encoded by theglbOandglbNgenes, respectively, important in the survival ofM. tuberculosisin macrophages. Mycobacterial heat shock proteins are known to undergo rapid upregulation under stress conditions. The expression profiles of the promoters of these genes were studied by constructing transcriptional fusions with green fluorescent protein and monitoring the promoter activity in both free-living and intracellular milieus at different time points. WhereasglbNshowed an early response to the oxidative and nitrosative stresses tested,glbOgave a lasting response to lower concentrations of both stresses. At all time points and under all stress conditions tested,groEL2showed higher expression than both trHb promoters and expression of both promoters showed an increase while inside the macrophages. Real-time PCR analysis of trHb andgroEL2mRNAs showed an initial upregulation at 24 h postinfection. The presence of theglbOprotein imparted an increased survival toM. smegmatisin THP-1 differentiated macrophages compared to that imparted by theglbNandhsp65proteins. The comparative upregulation shown by both trHb promoters while grown inside macrophages indicates the importance of these promoters for the survival ofM. tuberculosisin the hostile environment of the host.

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Section: Discussionsupporting

confidence: 69%

Section: Discussionmentioning

confidence: 89%

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Comparative Analysis of Mycobacterial Truncated Hemoglobin Promoters and thegroEL2Promoter in Free-Living and Intracellular Mycobacteria

Joseph

Madhavilatha

Kumar

et al. 2012

Appl Environ Microbiol

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“…The high rate of NO oxidation catalyzed by oxygenated trHbN suggests that this may be one of the vital defense systems in M. tuberculosis (41,42) for coping with the toxic effects of NO and nitrosative stress that may be important for allowing the intracellular survival of the bacterium in macrophages. This hypothesis is supported by the observation that expression of trHbN in an NO-sensitive mutant of Salmonella enhances the survival of the mutant both in vitro under nitrosative stress conditions and in vivo during macrophage infection (44).…”

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confidence: 82%

Responses ofMycobacterium tuberculosisHemoglobin Promoters to In Vitro and In Vivo Growth Conditions

Pawaria

Lama

Raje

et al. 2008

Appl Environ Microbiol

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The success of Mycobacterium tuberculosis as one of the dreaded human pathogens lies in its ability to utilize different defense mechanisms in response to the varied environmental challenges during the course of its intracellular infection, latency, and reactivation cycle. Truncated hemoglobins trHbN and trHbO are thought to play pivotal roles in the cellular metabolism of this organism during stress and hypoxia. To delineate the genetic regulation of the M. tuberculosis hemoglobins, transcriptional fusions of the promoters of the glbN and glbO genes with green fluorescent protein were constructed, and their responses were monitored in Mycobacterium smegmatis and M. tuberculosis H37Ra exposed to environmental stresses in vitro and in M. tuberculosis H37Ra after in vivo growth inside macrophages. The glbN promoter activity increased substantially during stationary phase and was nearly 3-to 3.5-fold higher than the activity of the glbO promoter, which remained more or less constant during different growth phases in M. smegmatis, as well as in M. tuberculosis H37Ra. In both mycobacterial hosts, the glbN promoter activity was induced 1.5-to 2-fold by the general nitrosative stress inducer, nitrite, as well as the NO releaser, sodium nitroprusside (SNP). The glbO promoter was more responsive to nitrite than to SNP, although the overall increase in its activity was much less than that of the glbN promoter. Additionally, the glbN promoter remained insensitive to the oxidative stress generated by H 2 O 2 , but the glbO promoter activity increased nearly 1.5-fold under similar conditions, suggesting that the trHb gene promoters are regulated differently under nitrosative and oxidative stress conditions. In contrast, transition metal-induced hypoxia enhanced the activity of both the glbN and glbO promoters at all growth phases; the glbO promoter was induced ϳ2.3-fold, which was found to be the highest value for this promoter under all the conditions evaluated. Addition of iron along with nickel reversed the induction in both cases. Interestingly, a concentration-dependent decrease in the activity of both trHb gene promoters was observed when the levels of iron in the growth media were depleted by addition of an iron chelator. These results suggested that an iron/heme-containing oxygen sensor is involved in the modulation of the trHb gene promoter activities directly or indirectly in conjunction with other cellular factors. The modes of promoter regulation under different physiological conditions were found to be similar for the trHbs in both M. smegmatis and M. tuberculosis H37Ra, indicating that the promoters might be regulated by components that are common to the two systems. Confocal microscopy of THP-1 macrophages infected with M. tuberculosis carrying the trHb gene promoter fusions showed that there was a significant level of promoter activity during intracellular growth in macrophages. Time course evaluation of the promoter activity after various times up to 48 h by fluorescence-activated cell sorting analysis of th...

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“…The relationship between V. parahaemolyticus and fish has been widely recognized (Woo et al, 2006). Pathogens that can survive and persist, express a broad array of virulence that functions to circumvent the host immune system (Pawaria et al, 2007;Li et al, 2008;Roop et al, 2009). Macrophages and neutrophil granulocytes are the primary host cells for Vibrio species.…”

Section: Introductionmentioning

confidence: 99%

Intracellular survival of virulence and low-virulence strains of Vibrio parahaemolyticus in Epinephelus awoara macrophages and peripheral leukocytes

Sang

Chen

et al. 2015

Genet. Mol. Res.

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ABSTRACT. In this study, we examined the virulence factors and pathogenesis of Vibrio parahaemolyticus in Epinephelus awoara. The chemotactic motility of V. parahaemolyticus for phagocytosis and intracellular survival in fish macrophages was determined using virulence strains and low-virulence strains of V. parahaemolyticus. We found that the intracellular mean number of virulence strains of V. parahaemolyticus ranged from 0-180 min after co-incubation with macrophages and peripheral leukocytes, was relatively low, and decreased steadily over the observation period. Low-virulence strains of V. parahaemolyticus were unable to survive in peripheral leukocytes and macrophages. Cell viability in response to V. parahaemolyticus was assessed using the MTT assay. Low-virulence V. parahaemolyticus strains exhibited lower cytotoxicity compared to virulent strains. The average percent of live macrophages and peripheral leukocytes infected by V. parahaemolyticus ranged from 13.50-79.20%. These results indicate that V. parahaemolyticus in E. awoara is a facultative intracellular bacterium that may be involved in virulence.

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Intracellular growth and survival of Salmonella enterica serovar Typhimurium carrying truncated hemoglobins of Mycobacterium tuberculosis

Cited by 28 publications

References 34 publications

Comparative Analysis of Mycobacterial Truncated Hemoglobin Promoters and thegroEL2Promoter in Free-Living and Intracellular Mycobacteria

Comparative Analysis of Mycobacterial Truncated Hemoglobin Promoters and thegroEL2Promoter in Free-Living and Intracellular Mycobacteria

Responses ofMycobacterium tuberculosisHemoglobin Promoters to In Vitro and In Vivo Growth Conditions

Intracellular survival of virulence and low-virulence strains of Vibrio parahaemolyticus in Epinephelus awoara macrophages and peripheral leukocytes

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