NADPH oxidase-derived H2O 2 subverts pathogen signaling by oxidative phosphotyrosine conversion to PB-DOPA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 37, 2016, Pages 10406-10411

  Alvarez, Luis A ^a   Kovačič, Lidija ^b,g   Rodríguez, Javier ^c,e   Gosemann, Jan Hendrik ^a,h   Kubica, Malgorzata ^b   Pircalabioru, Gratiela G ^b,i   Friedmacher, Florian ^a   Cean, Ada ^d   Ghişe, Alina ^d   SǍrǍndan, Mihai B ^d   Puri, Prem ^a   Daff, Simon ^e   Plettner, Erika ^f   Von Kriegsheim, Alex ^c,e   Bourke, Billy ^a,b   Knaus, Ulla G ^a,b  

^a OUR LADY S CHILDREN S HOSPITAL   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

^d BANAT S UNIVERSITY OF AGRICULTURAL SCIENCES AND VETERINARY MEDICINE   (Romania)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f SIMON FRASER UNIVERSITY   (Canada)

^g Novartis Ireland Ltd   (Ireland)

^h UNIVERSITY OF LEIPZIG   (Germany)

ⁱ UNIVERSITY OF BUCHAREST   (Romania)

Author keywords

Bacterial tyrosine phosphorylation; DOPA; Mucosal immunity; Nadph oxidase; Reactive oxygen species (ros)

Indexed keywords

DOPA; HYDROGEN PEROXIDE; PEROXIDASE; PHOSPHOTYROSINE; POLYSACCHARIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; HEME; OXYGEN; REACTIVE OXYGEN METABOLITE; TYROSINE;

ANIMAL TISSUE; BACTERIAL COUNT; BACTERIAL VIABILITY; CAMPYLOBACTER JEJUNI; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CARBONYLATION; CELL MEMBRANE; CONFERENCE PAPER; DISULFIDE BOND; ENZYME ACTIVITY; FETUS; GENE EXPRESSION; HUMAN; HUMAN TISSUE; KLEBSIELLA PNEUMONIAE; LISTERIA MONOCYTOGENES; MICROENVIRONMENT; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; RAT; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SIGNAL TRANSDUCTION; UPREGULATION; ANTIBIOTIC RESISTANCE; CELL LINE; CHEMISTRY; DRUG EFFECTS; HOST PATHOGEN INTERACTION; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PATHOGENICITY; SALMONELLA ENTERICA;

CAMPYLOBACTER JEJUNI; CELL LINE; DIHYDROXYPHENYLALANINE; DRUG RESISTANCE, BACTERIAL; HEME; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDROGEN PEROXIDE; IMMUNE SYSTEM; KLEBSIELLA PNEUMONIAE; LISTERIA MONOCYTOGENES; NADPH OXIDASES; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; OXYGEN; PEROXIDASE; PHOSPHOTYROSINE; REACTIVE OXYGEN SPECIES; SALMONELLA ENTERICA; TYROSINE;

EID: 84987678831     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1605443113     Document Type: Article

References (39)

1. Cameron EA, Sperandio V (2015) Frenemies: Signaling and nutritional integration in pathogen-microbiota-host interactions. Cell Host Microbe 18(3):275-284.
2. Kamada N, et al. (2012) Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336(6086):1325-1329.
3. Imlay JA (2013) The molecular mechanisms and physiological consequences of oxidative stress: Lessons from a model bacterium. Nat Rev Microbiol 11(7):443-454.
4. Holmström KM, Finkel T (2014) Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 15(6):411-421.
5. Winterbourn CC, Kettle AJ (2013) Redox reactions and microbial killing in the neutrophil phagosome. Antioxid Redox Signal 18(6):642-660.
6. Wright CJ, et al. (2014) Characterization of a bacterial tyrosine kinase in Porphyromonas gingivalis involved in polymicrobial synergy. MicrobiologyOpen 3(3):383-394.
7. Chao JD, Wong D, Av-Gay Y (2014) Microbial protein-tyrosine kinases. J Biol Chem 289(14):9463-9472.
8. Corcionivoschi N, et al. (2012) Mucosal reactive oxygen species decrease virulence by disrupting Campylobacter jejuni phosphotyrosine signaling. Cell Host Microbe 12(1):47-59.
9. Lin MH, et al. (2009) Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 reveals a tight link between tyrosine phosphorylation and virulence. Mol Cell Proteomics 8(12): 2613-2623.
10. Mancini S, Imlay JA (2015) The induction of two biosynthetic enzymes helps Escherichia coli sustain heme synthesis and activate catalase during hydrogen peroxide stress. Mol Microbiol 96(4):744-763.
11. (2) probe with improved performance for ratiometric and fluorescence lifetime imaging. ACS Chem Biol 8(3):535-542.
12. Hansen AM, et al. (2013) The Escherichia coli phosphotyrosine proteome relates to core pathways and virulence. PLoS Pathog 9(6):e1003403.
13. Marteyn B, Scorza FB, Sansonetti PJ, Tang C (2011) Breathing life into pathogens: The influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract. Cell Microbiol 13(2):171-176.
14. Kröger C, et al. (2013) An infection-relevant transcriptomic compendium for Salmonella enterica Serovar Typhimurium. Cell Host Microbe 14(6):683-695.
15. Guengerich FP, Munro AW (2013) Unusual cytochrome p450 enzymes and reactions. J Biol Chem 288(24):17065-17073.
16. Alvarez LA, et al. (2013) Cj1411c encodes for a cytochrome P450 involved in Campylobacter jejuni 81-176 pathogenicity. PLoS One 8(9):e75534.
17. Prasad B, Mah DJ, Lewis AR, Plettner E (2013) Water oxidation by a cytochrome p450: Mechanism and function of the reaction. PLoS One 8(4):e61897.
18. Reuter M, van Vliet AH (2013) Signal balancing by the CetABC and CetZ chemoreceptors controls energy taxis in Campylobacter jejuni. PLoS One 8(1):e54390.
19. Shi L, et al. (2014) Evolution of bacterial protein-tyrosine kinases and their relaxed specificity toward substrates. Genome Biol Evol 6(4):800-817.
20. Lacour S, Bechet E, Cozzone AJ, Mijakovic I, Grangeasse C (2008) Tyrosine phosphorylation of the UDP-glucose dehydrogenase of Escherichia coli is at the crossroads of colanic acid synthesis and polymyxin resistance. PLoS One 3(8):e3053.
21. Chen YY, Ko TP, Lin CH, Chen WH, Wang AH (2011) Conformational change upon product binding to Klebsiella pneumoniae UDP-glucose dehydrogenase: A possible inhibition mechanism for the key enzyme in polymyxin resistance. J Struct Biol 175(3): 300-310.
22. Houée-Lévin C, et al. (2015) Exploring oxidative modifications of tyrosine: An update on mechanisms of formation, advances in analysis and biological consequences. Free Radic Res 49(4):347-373.
23. Nagy P, Lechte TP, Das AB, Winterbourn CC (2012) Conjugation of glutathione to oxidized tyrosine residues in peptides and proteins. J Biol Chem 287(31):26068-26076.
24. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG (2006) Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18(1):69-82.
25. Mishra S, Imlay J (2012) Why do bacteria use so many enzymes to scavenge hydrogen peroxide? Arch Biochem Biophys 525(2):145-160.
26. Parsonage D, Karplus PA, Poole LB (2008) Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci USA 105(24):8209-8214.
27. Lee S, et al. (2010) The first global screening of protein substrates bearing proteinbound 3,4-Dihydroxyphenylalanine in Escherichia coli and human mitochondria. J Proteome Res 9(11):5705-5714.
28. Pancholi V, Chhatwal GS (2003) Housekeeping enzymes as virulence factors for pathogens. Int J Med Microbiol 293(6):391-401.
29. Peralta D, et al. (2015) A proton relay enhances H2O2 sensitivity of GAPDH to facilitate metabolic adaptation. Nat Chem Biol 11(2):156-163.
30. Guo A, et al. (2008) Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci USA 105(2):692-697.
31. Bergt C, Fu X, Huq NP, Kao J, Heinecke JW (2004) Lysine residues direct the chlorination of tyrosines in YXXK motifs of apolipoprotein A-I when hypochlorous acid oxidizes high density lipoprotein. J Biol Chem 279(9):7856-7866.
32. Albenberg L, et al. (2014) Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology 147(5):1055-1063.e8.
33. Zhang X, et al. (2010) Endogenous 3,4-dihydroxyphenylalanine and dopaquinone modifications on protein tyrosine: Links to mitochondrially derived oxidative stress via hydroxyl radical. Mol Cell Proteomics 9(6):1199-1208.
34. Renault M, et al. (2012) Cellular solid-state nuclear magnetic resonance spectroscopy. Proc Natl Acad Sci USA 109(13):4863-4868.
35. Turriziani B, et al. (2014) On-beads digestion in conjunction with data-dependent mass spectrometry: A shortcut to quantitative and dynamic interaction proteomics. Biology (Basel) 3(2):320-332.
36. Phillips JC, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26(16):1781-1802.
37. de Vries SJ, van Dijk M, Bonvin AM (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5(5):883-897.
38. van Dijk AD, Bonvin AM (2006) Solvated docking: Introducing water into the modelling of biomolecular complexes. Bioinformatics 22(19):2340-2347.
39. Oh E, Jeon B (2014) Role of alkyl hydroperoxide reductase (AhpC) in the biofilm formation of Campylobacter jejuni. PLoS One 9(1):e87312.