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

Trends in Molecular Medicine

Volumn 15, Issue 12, 2009, Pages 571-579

  Allaoui, Abdelmounaaïm ^a   Botteaux, Anne ^a   Dumont, Jacques E ^a   Hoste, Candice ^a   De Deken, Xavier ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DUAL OXIDASE 1; DUAL OXIDASE 2; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 5; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLORA; BACTERICIDAL ACTIVITY; BACTERIUM; BIOCHEMISTRY; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; ENZYME SYNTHESIS; HOMEOSTASIS; HOST; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; LEUKOCYTE; MACROPHAGE; MICROFLORA; MUCOSA; NONHUMAN; PATHOGENICITY; PHAGOCYTOSIS; RESPIRATORY BURST; SALMONELLA; SIGNAL TRANSDUCTION;

BACTERIA; BACTERIAL INFECTIONS; GENE EXPRESSION REGULATION; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDROGEN PEROXIDE; INTESTINAL MUCOSA; NADPH OXIDASE; PEROXIDASES; THIOCYANATES;

EID: 70749093445     PISSN: 14714914     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molmed.2009.10.003     Document Type: Article

References (95)

1. Brown S.A., et al. Revisiting the host as a growth medium. Nat. Rev. Microbiol. 6 (2008) 657-666
2. Hsiao W.W., et al. The microbes of the intestine: an introduction to their metabolic and signaling capabilities. Endocrinol. Metab. Clin. North Am. 37 (2008) 857-871
3. Pedron T., and Sansonetti P. Commensals, bacterial pathogens and intestinal inflammation: an intriguing menage a trois. Cell Host. Microbe 3 (2008) 344-347
4. Wikoff W.R., et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 3698-3703
5. Backhed F., et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15718-15723
6. Gribar S.C., et al. No longer an innocent bystander: epithelial Toll-like receptor signaling in the development of mucosal inflammation. Mol. Med. 14 (2008) 645-659
7. Lambeth J.D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4 (2004) 181-189
8. Babior B.M. NADPH oxidase: an update. Blood 93 (1999) 1464-1476
9. Bedard K., and Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87 (2007) 245-313
10. Geiszt M., et al. Dual oxidases represent novel hydrogen peroxide sources supporting mucosal surface host defense. FASEB J. 17 (2003) 1502-1504
11. De Deken X., et al. Cloning of two human thyroid cDNAs encoding new members of the NADPH oxidase family. J. Biol. Chem. 275 (2000) 23227-23233
12. Dupuy C., et al. Purification of a novel flavoprotein involved in the thyroid NADPH oxidase. Cloning of the porcine and human cdnas. J. Biol. Chem. 274 (1999) 37265-37269
13. Ris-Stalpers C. Physiology and pathophysiology of the DUOXes. Antioxid. Redox. Signal. 8 (2006) 1563-1572
14. De Deken X., et al. Characterization of ThOX proteins as components of the thyroid H(2)O(2)-generating system. Exp. Cell Res. 273 (2002) 187-196
15. Grasberger H., et al. Missense mutations of dual oxidase 2 (DUOX2) implicated in congenital hypothyroidism have impaired trafficking in cells reconstituted with DUOX2 maturation factor. Mol. Endocrinol. 21 (2007) 1408-1421
16. Morand S., et al. DUOX maturation factors form cell surface complexes with DUOX affecting the specificity of reactive oxygen species generation. FASEB J. 23 (2009) 1205-1218
17. Luxen S., et al. Heterodimerization controls localization of DUOX-DUOXA NADPH oxidases in airway cells. J. Cell Sci. 122 (2009) 1238-1247
18. Fischer H. Mechanism and function of DUOX in epithelia of the lung. Antioxid. Redox. Signal 11 (2009) 2453-2465
19. Shao M.X., and Nadel J.A. Dual oxidase 1-dependent MUC5AC mucin expression in cultured human airway epithelial cells. Proc. Natl. Acad. Sci. U. S. A 102 (2005) 767-772
20. Boots A.W., et al. ATP-mediated activation of the NADPH oxidase DUOX1 mediates airway epithelial responses to bacterial stimuli. J. Biol. Chem 284 (2009) 17858-17867
21. Moskwa P., et al. A novel host defense system of airways is defective in cystic fibrosis. Am. J. Respir. Crit Care Med. 175 (2007) 174-183
22. El Hassani R.A., et al. Dual oxidase2 is expressed all along the digestive tract. Am. J. Physiol. Gastrointest. Liver Physiol. 288 (2005) G933-G942
23. Ha E.M., et al. A direct role for dual oxidase in Drosophila gut immunity. Science 310 (2005) 847-850
24. Ha E.M., et al. Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in Drosophila gut. Nat. Immunol. 10 (2009) 949-957
25. Moreno J.C., et al. Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism. N. Engl. J. Med. 347 (2002) 95-102
26. Maruo Y., et al. Transient congenital hypothyroidism caused by biallelic mutations of the dual oxidase 2 gene in Japanese patients detected by a neonatal screening program. J. Clin. Endocrinol. Metab. 93 (2008) 4261-4267
27. Ohye H., et al. A novel homozygous missense mutation of the dual oxidase 2 (DUOX2) gene in an adult patient with large goiter. Thyroid 18 (2008) 561-566
28. Pfarr N., et al. Congenital hypothyroidism caused by new mutations in the thyroid oxidase 2 (THOX2) gene. Clin. Endocrinol. (Oxf) 65 (2006) 810-815
29. Varela V., et al. Three mutations (p.Q36H, p.G418fsX482 and g.IVS19-2A>C) in the dual oxidase 2 gene responsible for congenital goiter and iodide organification defect. Clin. Chem. 52 (2006) 182-191
30. Vigone M.C., et al. Persistent mild hypothyroidism associated with novel sequence variants of the DUOX2 gene in two siblings. Hum. Mutat. 26 (2005) 395
31. Fischer H., et al. Developmental regulation of DUOX1 expression and function in human fetal lung epithelial cells. Am. J. Physiol. Lung Cell Mol. Physiol 292 (2007) L1506-L1514
32. Milenkovic M., et al. Duox expression and related H2O2 measurement in mouse thyroid: onset in embryonic development and regulation by TSH in adult. J. Endocrinol. 192 (2007) 615-626
33. Luxen S., et al. Silencing of DUOX NADPH oxidases by promoter hypermethylation in lung cancer. Cancer Res. 68 (2008) 1037-1045
34. Ostrakhovitch, E.A. and Li, S.S. (2009) NIP1/DUOXA1 expression in epithelial breast cancer cells: regulation of cell adhesion and actin dynamics. Breast Cancer Res. Treat, in press
35. Harper R.W., et al. Differential regulation of dual NADPH oxidases/peroxidases, DUOX1 and DUOX2, by Th1 and Th2 cytokines in respiratory tract epithelium. FEBS Lett. 579 (2005) 4911-4917
36. Nagai K., et al. Dual oxidase 1 and 2 expression in airway epithelium of smokers and patients with mild/moderate chronic obstructive pulmonary disease. Antioxid. Redox. Signal. 10 (2008) 705-714
37. Wright J.M., et al. Respiratory epithelial gene expression in patients with mild and severe cystic fibrosis lung disease. Am. J. Respir. Cell Mol. Biol. 35 (2006) 327-336
38. Rigutto S., et al. Activation of dual oxidases DUOX1 and DUOX2: differential regulation mediated by camp-dependent protein kinase and protein kinase C-dependent phosphorylation. J. Biol. Chem. 284 (2009) 6725-6734
39. Ha E.M., et al. Regulation of DUOX by the Galphaq-phospholipase Cbeta-Ca2+ pathway in Drosophila gut immunity. Dev. Cell 16 (2009) 386-397
40. Rada B., et al. The Pseudomonas toxin pyocyanin inhibits the dual oxidase-based antimicrobial system as it imposes oxidative stress on airway epithelial cells. J. Immunol. 181 (2008) 4883-4893
41. Gattas M.V., et al. Oxidative epithelial host defense is regulated by infectious and inflammatory stimuli. Free Radic. Biol. Med 47 (2009) 1450-1458
42. Reeves E.P., et al. Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416 (2002) 291-297
43. Swillens S., et al. Consequences of the intracellular distribution of cyclic 3′,5′-nucleotides phosphodiesterases. FEBS Lett. 49 (1974) 92-95
44. Niethammer P., et al. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459 (2009) 996-999
45. Schutte B.C., and McCray Jr. P.B. [beta]-defensins in lung host defense. Annu. Rev. Physiol 64 (2002) 709-748
46. Nuding S., et al. Antibacterial activity of human defensins on anaerobic intestinal bacterial species: a major role of HBD-3. Microbes. Infect. 11 (2009) 384-393
47. Benov L., and Fridovich I. Escherichia coli exhibits negative chemotaxis in gradients of hydrogen peroxide, hypochlorite and N-chlorotaurine: products of the respiratory burst of phagocytic cells. Proc. Natl. Acad. Sci. U. S. A 93 (1996) 4999-5002
48. Botteaux A., et al. Potential role of Noxes in the protection of mucosae: H(2)O(2) as a bacterial repellent. Microbes. Infect. 11 (2009) 537-544
49. Roy K., et al. Enterotoxigenic Escherichia coli EtpA mediates adhesion between flagella and host cells. Nature 457 (2009) 594-598
50. Stebbins C.E., and Galan J.E. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414 (2001) 77-81
51. Flannagan R.S., et al. Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat. Rev. Microbiol. 7 (2009) 355-366
52. Gaillard J.L., et al. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from Gram-positive cocci. Cell 65 (1991) 1127-1141
53. Gruenheid S., and Finlay B.B. Microbial pathogenesis and cytoskeletal function. Nature 422 (2003) 775-781
54. Vazquez-Torres A., et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 287 (2000) 1655-1658
55. Philips J.A. Mycobacterial manipulation of vacuolar sorting. Cell Microbiol. 10 (2008) 2408-2415
56. Stevens D.L., et al. Effects of alpha and theta toxins from Clostridium perfringens on human polymorphonuclear leukocytes. J. Infect. Dis. 156 (1987) 324-333
57. Sierig G., et al. Cytotoxic effects of streptolysin o and streptolysin s enhance the virulence of poorly encapsulated group a streptococci. Infect. Immun. 71 (2003) 446-455
58. Tsolis R.M., et al. Role of Salmonella typhimurium Mn-superoxide dismutase (SodA) in protection against early killing by J774 macrophages. Infect. Immun. 63 (1995) 1739-1744
59. Canvin J., et al. Identification of sodC encoding periplasmic [Cu,Zn]-superoxide dismutase in Salmonella. FEMS Microbiol. Lett. 136 (1996) 215-220
60. Buchmeier N.A., et al. DNA repair is more important than catalase for Salmonella virulence in mice. J. Clin. Invest 95 (1995) 1047-1053
61. Hassett D.J., et al. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol. 17 (2009) 130-138
62. Monds R.D., and O'Toole G.A. The developmental model of microbial biofilms: 10 years of a paradigm up for review. Trends Microbiol. 17 (2009) 73-87
63. Fang F.C., et al. The transcriptional regulator SoxS is required for resistance of Salmonella typhimurium to paraquat but not for virulence in mice. Infect. Immun. 65 (1997) 5371-5375
64. Martchenko M., et al. Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol. Biol. Cell 15 (2004) 456-467
65. Lau G.W., et al. Pseudomonas aeruginosa OxyR is required for full virulence in rodent and insect models of infection and for resistance to human neutrophils. Infect. Immun. 73 (2005) 2550-2553
66. Chen P.R., et al. A new oxidative sensing and regulation pathway mediated by the MgrA homologue SarZ in Staphylococcus aureus. Mol. Microbiol. 71 (2009) 198-211
67. Filice G.A. Resistance of Nocardia asteroides to oxygen-dependent killing by neutrophils. J. Infect. Dis. 148 (1983) 861-867
68. Chavez V., et al. Ce-DUOX1/BLI-3 generates reactive oxygen species (ROS) as a protective innate immune mechanism in Caenorhabditis elegans. Infect. Immun 77 (2009) 4983-4989
69. Lipinski S., et al. DUOX2-derived reactive oxygen species are effectors of NOD2-mediated antibacterial responses. J. Cell Sci. 122 (2009) 3522-3530
70. van Klaveren R.J., et al. Involvement of an NAD(P)H oxidase-like enzyme in superoxide anion and hydrogen peroxide generation by rat type II cells. Thorax 52 (1997) 465-471
71. Ogier-Denis E., et al. NOX enzymes and Toll-like receptor signaling. Semin. Immunopathol. 30 (2008) 291-300
72. Guillot L., et al. Response of human pulmonary epithelial cells to lipopolysaccharide involves Toll-like receptor 4 (TLR4)-dependent signaling pathways: evidence for an intracellular compartmentalization of TLR4. J. Biol. Chem. 279 (2004) 2712-2718
73. Kawahara T., et al. Role of nicotinamide adenine dinucleotide phosphate oxidase 1 in oxidative burst response to Toll-like receptor 5 signaling in large intestinal epithelial cells. J. Immunol. 172 (2004) 3051-3058
74. Park H.S., et al. Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J. Immunol. 173 (2004) 3589-3593
75. Rothfork J.M., et al. Inactivation of a bacterial virulence pheromone by phagocyte-derived oxidants: new role for the NADPH oxidase in host defense. Proc. Natl. Acad. Sci. U. S. A 101 (2004) 13867-13872
76. Yan F., et al. Reactive oxygen species regulate Pseudomonas aeruginosa lipopolysaccharide-induced MUC5AC mucin expression via PKC-NADPH oxidase-ROS-TGF-alpha signaling pathways in human airway epithelial cells. Biochem. Biophys. Res. Commun. 366 (2008) 513-519
77. Kesimer M., et al. Tracheobronchial air-liquid interface cell culture: a model for innate mucosal defense of the upper airways?. Am. J. Physiol. Lung Cell Mol. Physiol 296 (2009) L92-L100
78. Kunisawa J., et al. Immunological commonalities and distinctions between airway and digestive immunity. Trends Immunol. 29 (2008) 505-513
79. Cani P.D., et al. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58 (2009) 1091-1103
80. Wang X., et al. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res. 68 (2008) 9909-9917
81. Carlsson J., et al. Hydrogen peroxide excretion by oral streptococci and effect of lactoperoxidase-thiocyanate-hydrogen peroxide. Infect. Immun. 40 (1983) 70-80
82. Lainhart W., et al. Shiga toxin as a bacterial defense against a eukaryotic predator, Tetrahymena thermophila. J. Bacteriol. 191 (2009) 5116-5122
83. Cliffe L.J., et al. Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 308 (2005) 1463-1465
84. Kim M., et al. Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 459 (2009) 578-582
85. Stasia M.J., et al. Chronic-granulomatous disease. Rev. Med. Interne. 30 (2009) 221-232
86. Leto T.L., and Geiszt M. Role of NOX family NADPH oxidases in host defense. Antioxid. Redox. Signal. 8 (2006) 1549-1561
87. Lambeth J.D., et al. NOX enzymes as novel targets for drug development. Semin. Immunopathol. 30 (2008) 339-363
88. Mullard A. Microbiology: tinker, bacteria, eukaryote, spy. Nature 459 (2009) 159-161
89. Blaser M.J., and Kirschner D. The equilibria that allow bacterial persistence in human hosts. Nature 449 (2007) 843-849
90. Dethlefsen L., et al. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449 (2007) 811-818
91. Martin F.P., et al. Top-down systems biology integration of conditional prebiotic modulated transgenomic interactions in a humanized microbiome mouse model. Mol. Syst. Biol. 4 (2008) 205
92. Geiszt M., et al. NAD(P)H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J. Immunol. 171 (2003) 299-306
93. Kawahara T., et al. Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase NOX1 and its organizer NOXO1 in guinea pig gastric mucosal cells. Am. J. Physiol. Cell Physiol. 288 (2005) C450-C457
94. Zhang X., et al. Toll-like receptor 4 deficiency causes pulmonary emphysema. J. Clin. Invest 116 (2006) 3050-3059
95. Banfi B., et al. A Ca(2+)-activated NADPH oxidase in testis, spleen and lymph nodes. J. Biol. Chem. 276 (2001) 37594-37601