Dual oxidases and hydrogen peroxide in a complex dialogue between host mucosae and bacteria

Allaoui, Abdelmounaaïm; Botteaux, Anne; Dumont, Jacques Emile; Hoste, Candice; Deken, Xavier De

doi:10.1016/j.molmed.2009.10.003

Cited by 48 publications

(37 citation statements)

References 95 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Current literature suggests that DUOX expression in the respiratory tract correlates with cell differentiation (1,11,24). In this study, we have shown that ATRA is a key component for DUOX2 mRNA and protein expression as well as inducibility by rhinovirus.…”

Section: Discussionsupporting

confidence: 52%

All-trans retinoic acid mediates DUOX2 expression and function in respiratory tract epithelium

Linderholm

Onitsuka

et al. 2010

American Journal of Physiology-Lung Cellular and Molecular Phys

View full text Add to dashboard Cite

RW. All-trans retinoic acid mediates DUOX2 expression and function in respiratory tract epithelium. Am J Physiol Lung Cell Mol Physiol 299: L215-L221, 2010. First published May 28, 2010 doi:10.1152/ajplung.00015.2010.-DUOX1 and DUOX2 are members of the NADPH oxidase family that are specifically regulated to produce hydrogen peroxide in epithelia of the thyroid, gastrointestinal tract, and respiratory tract. The determinants of DUOX1 or DUOX2 expression in various tissues have not been established. Using respiratory tract epithelial cells as a model, we investigated changes in DUOX mRNA and protein expression during the first 10 days of differentiation. By comparing a respiratory tract cell line, HBE1, with primary tracheobronchial epithelial (TBE) cells, we determined that DUOX2 was significantly expressed only in cell conditions that included all-trans retinoic acid (ATRA). In HBE1 cells, DUOX2 mRNA increased 6-fold after ATRA treatment. Similarly, ATRA induced a 19-fold increase in DUOX2 mRNA expression in primary TBE cells with parallel increases in DUOX protein and DUOXmediated H2O2 production as well. In addition, DUOX2 induction by rhinovirus required the presence of ATRA. ATRA had no effect on DUOX1 expression for all the conditions studied. Our data indicate that for respiratory epithelial cells, ATRA is important in the regulation of DUOX2 expression, function, and rhinovirus-mediated DUOX2 inducibility. DUOX1; gene regulation DUOX ISOZYMES DUOX1 AND DUOX2 are dual NADPH oxidase (NOX)-putative heme peroxidases expressed predominantly in epithelial tissues including epithelia of the thyroid, gastrointestinal tract, and respiratory tract (19). They are members of the NOX family that specifically produce hydrogen peroxide (H 2 O 2 ) in a regulated fashion. The functional significance of DUOX-mediated H 2 O 2 production and the relative contribution of each isoform for functional activity appears to be tissue-specific. For example, DUOX2 is the essential isoform for thyroid hormone synthesis (21), whereas DUOX1 appears to be the major isoform required for wound healing and innate host defense in the respiratory tract (6,7,16,22,28). In addition, the 5-to 10-fold higher levels of DUOX1 mRNA compared with DUOX2 mRNA in respiratory tract epithelium (17, 27) suggest DUOX1 is the predominant isoform for DUOXmediated H 2 O 2 production in the airway. However, DUOX2 likely has a higher capacity for H 2 O 2 generation compared with DUOX1 (2, 25) and may have a larger contribution to basal H 2 O 2 production than previously appreciated (15). How the relative expression levels and functional roles of each DUOX isoform are established in tissues remains undetermined.To begin to address this issue, we investigated some potential factors necessary for DUOX isoform expression in differentiating respiratory tract epithelia. Recent data suggest that DUOX expression in respiratory tract epithelia increases with increasing differentiation (11, 24). Furthermore, it has been proposed that DUOX expression is specifically expr...

show abstract

Section: Discussionsupporting

confidence: 52%

All-trans retinoic acid mediates DUOX2 expression and function in respiratory tract epithelium

Linderholm

Onitsuka

et al. 2010

American Journal of Physiology-Lung Cellular and Molecular Phys

View full text Add to dashboard Cite

show abstract

“…Exposure to oxidative stress is likely to occur in both the aquatic (28) and human host (29,30) environments that this organism inhabits. Whether oxidant levels in these environments would be sufficient to activate H-NOX by the proposed mechanism remains uncertain.…”

Section: Discussionmentioning

confidence: 99%

Heme-independent Redox Sensing by the Heme-Nitric Oxide/Oxygen-binding Protein (H-NOX) from Vibrio cholerae

Mukhopadyay¹,

Sudasinghe

Schaub

et al. 2016

Journal of Biological Chemistry

View full text Add to dashboard Cite

Heme nitric oxide/oxygen (H-NOX)-binding proteins act as nitric oxide (NO) sensors among various bacterial species. In several cases, they act to mediate communal behavior such as biofilm formation, quorum sensing, and motility by influencing the activity of downstream signaling proteins such as histidine kinases (HisKa) in a NO-dependent manner. An H-NOX/HisKa regulatory circuit was recently identified in Vibrio cholerae, and the H-NOX protein has been spectroscopically characterized. However, the influence of the H-NOX protein on HisKa autophosphorylation has not been evaluated. This process may be important for persistence and pathogenicity in this organism. Here, we have expressed and purified the V. cholerae HisKa (HnoK) and H-NOX in its heme-bound (holo) and heme-free (apo) forms. Autophosphorylation assays of HnoK in the presence of H-NOX show that the holoprotein in the Fe(II)-NO and Fe(III) forms is a potent inhibitor of HnoK. Activity of the Fe(III) form and aerobic instability of the Fe(II) form suggested thatVibrio cholerae H-NOX may act as a sensor of the redox state as well as NO. Remarkably, the apoprotein also showed robust HnoK inhibition that was dependent on the oxidation of cysteine residues to form disulfide bonds at a highly conserved zinc site. The importance of cysteine in this process was confirmed by mutagenesis, which also showed that holo Fe(III), but not Fe(II)-NO, H-NOX relied heavily upon cysteine for activation. These results highlight a heme-independent mechanism for activation of V. cholerae H-NOX that implicates this protein as a dual redox/NO sensor.

show abstract

“…In the human genome, there are five NOX enzymes (NOX1 to NOX5) and two DUOX enzymes (DUOX1 and DUOX2). Interestingly, the diverse NOX and DUOX family enzymes are not only expressed in phagocytic cells, but also in various nonphagocytic cells, including mucosal epithelial cells (Ha et al, 2005;Allaoui et al, 2009;Fischer, 2009), indicating their potential biological roles in these cells. In addition, several recent studies have shown that ROS are microbicidal effector molecules in the gut epithelia (El Hassani et al, 2005;Ha et al, 2005Ha et al, , 2009a.…”

Section: Introductionmentioning

confidence: 99%

The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis

Yao¹,

Wang²,

Li³

et al. 2015

The ISME Journal

View full text Add to dashboard Cite

The guts of metazoans are in permanent contact with the microbial realm that includes beneficial symbionts, nonsymbionts, food-borne microbes and life-threatening pathogens. However, little is known concerning how host immunity affects gut bacterial community. Here, we analyze the role of a dual oxidase gene (BdDuox) in regulating the intestinal bacterial community homeostasis of the oriental fruit fly Bactrocera dorsalis. The results showed that knockdown of BdDuox led to an increased bacterial load, and to a decrease in the relative abundance of Enterobacteriaceae and Leuconostocaceae bacterial symbionts in the gut. The resulting dysbiosis, in turn, stimulates an immune response by activating BdDuox and promoting reactive oxygen species (ROS) production that regulates the composition and structure of the gut bacterial community to normal status by repressing the overgrowth of minor pathobionts. Our results suggest that BdDuox plays a pivotal role in regulating the homeostasis of the gut bacterial community in B. dorsalis.

show abstract

Dual oxidases and hydrogen peroxide in a complex dialogue between host mucosae and bacteria

Cited by 48 publications

References 95 publications

All-trans retinoic acid mediates DUOX2 expression and function in respiratory tract epithelium

All-trans retinoic acid mediates DUOX2 expression and function in respiratory tract epithelium

Heme-independent Redox Sensing by the Heme-Nitric Oxide/Oxygen-binding Protein (H-NOX) from Vibrio cholerae

The dual oxidase gene BdDuox regulates the intestinal bacterial community homeostasis of Bactrocera dorsalis

Contact Info

Product

Resources

About