Neutrophils to the ROScue: Mechanisms of NADPH oxidase activation and bacterial resistance

Nguyen, Giang T.; Green, Erin R.; Mecsas, Joan

doi:10.3389/fcimb.2017.00373

Cited by 741Neutrophil, Myeloperoxidase and Oxidative MechanismsRedox biology and oxidative stressImmune Response and Inflammation

Neutrophils to the ROScue: Mechanisms of NADPH oxidase activation and bacterial resistance

Open access

Nguyen, Giang T., Green, Erin R., Mecsas, Joan·2017·Frontiers in Cellular and Infection Microbiology

DOI 10.3389/fcimb.2017.00373PMC PMC5574878

Open this paper in CoChat — free account Open PDF

Abstract

Reactive oxygen species (ROS) generated by NADPH oxidase play an important role in antimicrobial host defense and inflammation. Their deficiency in humans results in recurrent and severe bacterial infections, while their unregulated release leads to pathology from excessive inflammation. The release of high concentrations of ROS aids in clearance of invading bacteria. Localization of ROS release to phagosomes containing pathogens limits tissue damage. Host immune cells, like neutrophils, also known as PMNs, will release large amounts of ROS at the site of infection following the activation of surface receptors. The binding of ligands to G-protein-coupled receptors (GPCRs), toll-like receptors, and cytokine receptors can prime PMNs for a more robust response if additional signals are encountered. Meanwhile, activation of Fc and integrin directly induces high levels of ROS production. Additionally, GPCRs that bind to the bacterial-peptide analog fMLP, a neutrophil chemoattractant, can both prime cells and trigger low levels of ROS production. Engagement of these receptors initiates intracellular signaling pathways, resulting in activation of downstream effector proteins, assembly of the NADPH oxidase complex, and ultimately, the production of ROS by this complex. Within PMNs, ROS released by the NADPH oxidase complex can activate granular proteases and induce the formation of neutrophil extracellular traps (NETs). Additionally, ROS can cross the membranes of bacterial pathogens and damage their nucleic acids, proteins, and cell membranes. Consequently, in order to establish infections, bacterial pathogens employ various strategies to prevent restriction by PMN-derived ROS or downstream consequences of ROS production. Some pathogens are able to directly prevent the oxidative burst of phagocytes using secreted effector proteins or toxins that interfere with translocation of the NADPH oxidase complex or signaling pathways needed for its activation. Nonetheless, these pathogens often rely on repair and detoxifying proteins in addition to these secreted effectors and toxins in order to resist mammalian sources of ROS. This suggests that pathogens have both intrinsic and extrinsic mechanisms to avoid restriction by PMN-derived ROS. Here, we review mechanisms of oxidative burst in PMNs in response to bacterial infections, as well as the mechanisms by which bacterial pathogens thwart restriction by ROS to survive under conditions of oxidative stress.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.3389/fcimb.2017.00373

Cites

276 of 276 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Some cell surface receptors (TLR, GPCR and TNFR) can prime NOX2 activation.
“Some cell surface receptors (Toll-like receptors (TLR), G-protein-coupled receptors (GPCR) and TNF receptors (TNFR)), can prime the NOX2 activation [175].”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [175]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The NOX Family of ROS-Generating NADPH Oxidases: Physiology and Pathophysiology
Bedard, K., & Krause, K.-H. (2007) · Physiological Reviews · doi:10.1152/physrev.00044.2005 · Cited by 6,989 · see citing works
ROS function in redox signaling and oxidative stress
Schieber, M., & Chandel, N. S. (2014) · Current Biology · doi:10.1016/j.cub.2014.03.034 · Cited by 6,931 · see citing works
Neutrophil recruitment and function in health and inflammation
Kolaczkowska, E., & Kubes, P. (2013) · Nature Reviews Immunology · doi:10.1038/nri3399 · Cited by 5,472 · see citing works
Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling
Ray, P. D., Huang, B.-W., & Tsuji, Y. (2012) · Cellular Signalling · doi:10.1016/j.cellsig.2012.01.008 · Cited by 4,373 · see citing works
Integrins: A family of cell surface receptors
HYNES, R. (1987) · Cell · doi:10.1016/0092-8674(87)90233-9 · Cited by 4,294 · see citing works
Toll-Like Receptor Signaling Pathways
Kawasaki, T., & Kawai, T. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00461 · Cited by 3,250 · see citing works
Novel cell death program leads to neutrophil extracellular traps
Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V., & Zychlinsky, A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200606027 · Cited by 3,197 · see citing works
RGD AND OTHER RECOGNITION SEQUENCES FOR INTEGRINS
Ruoslahti, E. (1996) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.12.1.697 · Cited by 3,191 · cited 2× · see citing works
“…signaling to integrin activation, the inside-out step can be bypassed by using an “engineered” multivalent peptide poly-RGD (Arg-Gly-Asp), a ligand that is of sufficient valency to directly aggregate integrins and initiate “outside-in” signaling from all three βfamilies (Ruoslahti, 1996).”
Background
NOX enzymes and the biology of reactive oxygen
Lambeth, J. D. (2004) · Nature Reviews Immunology · doi:10.1038/nri1312 · Cited by 3,125 · see citing works
The G-Protein-Coupled Receptors in the Human Genome Form Five Main Families. Phylogenetic Analysis, Paralogon Groups, and Fingerprints
Fredriksson, R., Lagerström, M. C., Lundin, L.-G., & Schiöth, H. B. (2003) · Molecular Pharmacology · doi:10.1124/mol.63.6.1256 · Cited by 2,941 · see citing works
Redox regulation of cell survival
Trachootham, D., Lu, W., Ogasawara, M. A., Valle, N. R.-D., & Huang, P. (2008) · Antioxidants & Redox Signaling · doi:10.1089/ars.2007.1957 · Cited by 1,781 · see citing works
Beyond oxidative stress: an immunologist's guide to reactive oxygen species
Nathan, C., & Cunningham-Bussel, A. (2013) · Nature Reviews Immunology · doi:10.1038/nri3423 · Cited by 1,619 · see citing works
Cellular Defenses against Superoxide and Hydrogen Peroxide
Imlay, J. A. (2008) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.061606.161055 · Cited by 1,563 · see citing works
Calcium and ROS: A mutual interplay
Görlach, A., Bertram, K., Hudecova, S., & Krizanova, O. (2015) · Redox Biology · doi:10.1016/j.redox.2015.08.010 · Cited by 1,546 · see citing works
The SYK tyrosine kinase: A crucial player in diverse biological functions
Mócsai, A., Ruland, J., & Tybulewicz, V. L. J. (2010) · Nature Reviews Immunology · doi:10.1038/nri2765 · Cited by 1,368 · see citing works
Central Role for G Protein-Coupled Phosphoinositide 3-Kinase γ in Inflammation
Hirsch, E., Katanaev, V. L., Garlanda, C., Azzolino, O., Pirola, L., Silengo, L., Sozzani, S., Mantovani, A., Altruda, F., & Wymann, M. P. (2000) · Science · doi:10.1126/science.287.5455.1049 · Cited by 1,209 · see citing works
Activation of the OxyR Transcription Factor by Reversible Disulfide Bond Formation
Zheng, M., Åslund, F., & Storz, G. (1998) · Science · doi:10.1126/science.279.5357.1718 · Cited by 1,197 · see citing works
Integrin Structure, Activation, and InteractionsPreprint
Campbell, I. D., & Humphries, M. J. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004994 · Cited by 1,192 · see citing works
Killing activity of neutrophils is mediated through activation of proteases by K+ flux
Reeves, E. P., Lu, H., Jacobs, H. L., Messina, C. G. M., Bolsover, S., Gabella, G., Potma, E. O., Warley, A., Roes, J., & Segal, A. W. (2002) · Nature · doi:10.1038/416291a · Cited by 1,153 · see citing works
Structure-Function of the G Protein–Coupled Receptor Superfamily
Katritch, V., Cherezov, V., & Stevens, R. C. (2012) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-032112-135923 · Cited by 1,051 · see citing works
NADPH oxidases: An overview from structure to innate immunity-associated pathologies
Panday, A., Sahoo, M. K., Osorio, D., & Batra, S. (2015) · Cellular & Molecular Immunology · doi:10.1038/cmi.2014.89 · Cited by 944 · see citing works
Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: translocation during activation.
Borregaard, N., Heiple, J. M., Simons, E. R., & Clark, R. A. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.97.1.52 · Cited by 911 · see citing works
In Vitro Bactericidal Capacity of Human Polymorphonuclear Leukocytes: Diminished Activity in Chronic Granulomatous Disease of Childhood *
Quie, P. G., White, J. G., Holmes, B. M., & Good, R. A. (1967) · Journal of Clinical Investigation · doi:10.1172/jci105568 · Cited by 906 · see citing works
Regulating Rho GTPases and their regulators
Hodge, R. G., & Ridley, A. J. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.67 · Cited by 903 · see citing works
Integrin signalling at a glance
Harburger, D. S., & Calderwood, D. (2008) · Journal of Cell Science · doi:10.1242/jcs.018093 · Cited by 902 · see citing works
Reactive Oxygen Species and Neutrophil Function
Winterbourn, C. C., Kettle, A. J., & Hampton, M. B. (2016) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060815-014442 · Cited by 885 · see citing works
Properties of mouse and human IgG receptors and their contribution to disease models
Bruhns, P. (2012) · Blood · doi:10.1182/blood-2012-01-380121 · Cited by 869 · see citing works
ROS-dependent signal transduction
Reczek, C. R., & Chandel, N. S. (2014) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.09.010 · Cited by 850 · see citing works
Superoxide accelerates DNA damage by elevating free-iron levels
Keyer, K., & Imlay, J. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13635 · Cited by 841 · see citing works
Cloning the gene for an inherited human disorder—chronic granulomatous disease—On the basis of its chromosomal location
Royer-Pokora, B., Kunkel, L. M., Monaco, A. P., Goff, S. C., Newburger, P. E., Baehner, R. L., Cole, F. S., Curnutte, J. T., & Orkin, S. H. (1986) · Nature · doi:10.1038/322032a0 · Cited by 833 · see citing works
Roles of PLC-β2 and -β3 and PI3Kγ in Chemoattractant-Mediated Signal Transduction
Li, Z., Jiang, H., Xie, W., Zhang, Z., Smrcka, A. V., & Wu, D. (2000) · Science · doi:10.1126/science.287.5455.1046 · Cited by 807 · see citing works
DNA Microarray-Mediated Transcriptional Profiling of the Escherichia coli Response to Hydrogen Peroxide
Zheng, M., Wang, X., Templeton, L. J., Smulski, D. R., LaRossa, R. A., & Storz, G. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.15.4562-4570.2001 · Cited by 802 · see citing works
Alkyl Hydroperoxide Reductase Is the Primary Scavenger of Endogenous Hydrogen Peroxide in Escherichia coli
Seaver, L. C., & Imlay, J. A. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.24.7173-7181.2001 · Cited by 797 · see citing works
Mitochondrial reactive oxygen species drive proinflammatory cytokine production
Naik, E., & Dixit, V. M. (2011) · Journal of Experimental Medicine · doi:10.1084/jem.20110367 · Cited by 783 · see citing works
Iron‐sulphur clusters and the problem with oxygen
Imlay, J. A. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05028.x · Cited by 717 · see citing works
Studies of the Metabolic Activity of Leukocytes from Patients with a Genetic Abnormality of Phagocytic Function*
Holmes, B. M., Page, A. R., & Good, R. A. (1967) · Journal of Clinical Investigation · doi:10.1172/jci105634 · Cited by 687 · see citing works
Chronic Granulomatous Disease: The European Experience
van den Berg, J. M., van Koppen, E., Åhlin, A., Belohradsky, B. H., Bernatowska, E. A., Corbeel, L., Español, T., Fischer, A., Kurenko-Deptuch, M., Mouy, R., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005234 · Cited by 685 · see citing works
Diverse novel functions of neutrophils in immunity, inflammation, and beyond
Mócsai, A. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20122220 · Cited by 679 · see citing works
Myeloperoxidase: a front-line defender against phagocytosed microorganisms
Klebanoff, S. J., Kettle, A. J., Rosen, H., Winterbourn, C. C., & Nauseef, W. M. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.0712349 · Cited by 679 · see citing works
Neutrophils: Between Host Defence, Immune Modulation, and Tissue Injury
Krüger, P., Saffarzadeh, M., Weber, A. N. R., Rieber, N. P., Radsak, M. P., von Bernuth, H., Benarafa, C., Roos, D., Skokowa, J., & Hartl, D. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004651 · Cited by 663 · see citing works
Regulation of Reactive Oxygen Species Generation in Cell Signaling
Bae, Y. S., Oh, H., Rhee, S. G., & Yoo, Y. D. (2011) · Molecules and Cells · doi:10.1007/s10059-011-0276-3 · Cited by 660 · see citing works
Janeway’s Immunobiology
Soesatyo, M. H. (2012) · Jurnal Teknosains · doi:10.22146/teknosains.5992 · Cited by 655 · see citing works
Neutrophil cell surface receptors and their intracellular signal transduction pathways
Futosi, K., Fodor, S., & Mócsai, A. (2013) · International Immunopharmacology · doi:10.1016/j.intimp.2013.06.034 · Cited by 642 · see citing works
Modeling the Reactions of Superoxide and Myeloperoxidase in the Neutrophil Phagosome
Winterbourn, C. C., Hampton, M. B., Livesey, J. H., & Kettle, A. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605898200 · Cited by 633 · see citing works
Isozyme-selective stimulation of phospholipase C-β2 by G protein βγ-subunits
Camps, M., Carozzi, A., Schnabel, P., Scheer, A., Parker, P. J., & Gierschik, P. (1992) · Nature · doi:10.1038/360684a0 · Cited by 629 · see citing works
The Role of Reactive Oxygen Species in Antibiotic-Mediated Killing of Bacteria
Acker, H. V., & Coenye, T. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2016.12.008 · Cited by 615 · see citing works
The PX domains of p47phox and p40phox bind to lipid products of PI(3)K
Kanai, F., Liu, H., Field, S. J., Akbary, H., Matsuo, T., Brown, G. E., Cantley, L. C., & Yaffe, M. B. (2001) · Nature Cell Biology · doi:10.1038/35083070 · Cited by 611 · see citing works
The integrin adhesome: from genes and proteins to human disease
Winograd-Katz, S. E., Fässler, R., Geiger, B., & Legate, K. R. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3769 · Cited by 608 · see citing works
A novel phosphoinositide 3 kinase activity in myeloid-derived cells is activated by G protein βγ subunits
Stephens, L., Smrcka, A. V., Cooke, F. T., Jackson, T., Sternweis, P. C., & Hawkins, P. T. (1994) · Cell · doi:10.1016/0092-8674(94)90237-2 · Cited by 595 · see citing works
Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli
Bagg, A., & Neilands, J. B. (1987) · Biochemistry · doi:10.1021/bi00391a039 · Cited by 593 · see citing works
Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol—disulfide status
Åslund, F., Zheng, M., Beckwith, J., & Storz, G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6161 · Cited by 586 · see citing works
Are Reactive Oxygen Species Always Detrimental to Pathogens?
Paiva, C. N., & Bozza, M. T. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5447 · Cited by 559 · see citing works
Activation and assembly of the NADPH oxidase: a structural perspective
Groemping, Y., & Rittinger, K. (2005) · Biochemical Journal · doi:10.1042/bj20041835 · Cited by 559 · see citing works
Salmonella Pathogenicity Island 2-Dependent Evasion of the Phagocyte NADPH Oxidase
Vázquez‐Torres, A., Xu, Y., Jones‐Carson, J., Holden, D. W., Lucia, S. M., Dinauer, M. C., Mastroeni, P., & Fang, F. C. (2000) · Science · doi:10.1126/science.287.5458.1655 · Cited by 557 · see citing works
Deficiency of the Hematopoietic Cell-Specific Rho Family GTPase Rac2 Is Characterized by Abnormalities in Neutrophil Function and Host Defense
Roberts, A. W., Kim, C., Zhen, L., Lowe, J. B., Kapur, R., Petryniak, B., Spaetti, A., Pollock, J. D., Borneo, J. B., Bradford, G. B., et al. (1999) · Immunity · doi:10.1016/s1074-7613(00)80019-9 · Cited by 556 · see citing works
The Ins and Outs of Leukocyte Integrin Signaling
Abram, C. L., & Lowell, C. A. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132554 · Cited by 535 · see citing works
A Small, Stable RNA Induced by Oxidative Stress: Role as a Pleiotropic Regulator and Antimutator
Altuvia, S., Weinstein‐Fischer, D., Zhang, A., Postow, L., & Storz, G. (1997) · Cell · doi:10.1016/s0092-8674(00)80312-8 · Cited by 510 · see citing works
Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria
Troxell, B., & Hassan, H. M. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00059 · Cited by 500 · see citing works
Hematopoietic Cell Regulation by Rac1 and Rac2 Guanosine Triphosphatases
Gu, Y., Filippi, M., Cancelas, J. A., Siefring, J. E., Williams, E. P., Jasti, A. C., Harris, C. E., Lee, A. W.-T., Prabhakar, R., Atkinson, S. J., et al. (2003) · Science · doi:10.1126/science.1088485 · Cited by 500 · see citing works
The NADPH oxidase of professional phagocytes—prototype of the NOX electron transport chain systems
Cross, A. R., & Segal, A. W. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.03.008 · Cited by 489 · see citing works
Priming of the neutrophil respiratory burst: role in host defense and inflammation
Benna, J. E., Hurtado-Nédelec, M., Marzaioli, V., Marie, J., Gougerot‐Pocidalo, M., & Dang, P. M. (2016) · Immunological Reviews · doi:10.1111/imr.12447 · Cited by 481 · see citing works
Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation
Ambruso, D. R., Knall, C., Abell, A. N., Panepinto, J. A., Kurkchubasche, A. G., Thurman, G. W., Gonzalez-Aller, C., Hiester, A. A., deBoer, M., Harbeck, R. J., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.080074897 · Cited by 480 · see citing works
ROS production in phagocytes: Why, when, and where?
Dupré-Crochet, S., Erard, M., & Nüβe, O. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.1012544 · Cited by 467 · see citing works
Formyl peptide receptors: A promiscuous subfamily of G protein-coupled receptors controlling immune responses
MIGEOTTE, I., COMMUNI, D., & PARMENTIER, M. (2006) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2006.09.009 · Cited by 457 · see citing works
Oxidative Stress, Redox Signaling, and Autophagy: Cell Death Versus Survival
Navarro-Yepes, J., Burns, M., Anandhan, A., Khalimonchuk, O., Razo, L. M. D., Quintanilla‐Vega, B., Pappa, A., Panayiotidis, M. I., & Franco, R. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5837 · Cited by 453 · see citing works
p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases
Benna, J. E., Dang, P. M., Gougerot‐Pocidalo, M., Marie, J., & Braut‐Boucher, F. (2009) · Experimental & Molecular Medicine · doi:10.3858/emm.2009.41.4.058 · Cited by 453 · see citing works
Leukocyte Oxidase: Defective Activity in Chronic Granulomatous Disease
Baehner, R. L., & Nathan, D. G. (1967) · Science · doi:10.1126/science.155.3764.835 · Cited by 436 · see citing works
The role of O2.− in the production of HO.: in vitro and in vivo
Liochev, S. I., & Fridovich, I. (1994) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(94)90239-9 · Cited by 423 · see citing works
Syk is required for integrin signaling in neutrophils
Mócsai, A., Zhou, M., Meng, F., Tybulewicz, V. L., & Lowell, C. A. (2002) · Immunity · doi:10.1016/s1074-7613(02)00303-5 · Cited by 421 · see citing works
Assay of metabolic superoxide production in Escherichia coli.
Imlay, J. A., & Fridovich, I. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)89596-9 · Cited by 420 · see citing works
A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40phox and selective defects in neutrophil NADPH oxidase activity
Matute, J. D., Arias, A. A., Wright, N. A. M., Wrobel, I. T., Waterhouse, C. C. M., Li, X. J., Marchal, C. C., Stull, N. D., Lewis, D. B., Steele, M., et al. (2009) · Blood · doi:10.1182/blood-2009-07-231498 · Cited by 417 · see citing works
Phosphorylation of p47 p hox Sites by PKC α, βΙΙ, δ, and ζ: Effect on Binding to p22 p hox and on NADPH Oxidase Activation
Fontayne, A., Dang, P. M., Gougerot‐Pocidalo, M., & Benna, J. E. (2002) · Biochemistry · doi:10.1021/bi011953s · Cited by 412 · see citing works
OxyR and SoxRS Regulation of fur
Zheng, M., Doan, B., Schneider, T. D., & Storz, G. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.15.4639-4643.1999 · Cited by 402 · see citing works
Mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide
Imlay, J. A., & Linn, S. (1987) · Journal of Bacteriology · doi:10.1128/jb.169.7.2967-2976.1987 · Cited by 398 · see citing works
Regulation of the synthesis of superoxide dismutase in Escherichia coli. Induction by methyl viologen.
Hassan, H. M., & Fridovich, I. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)41019-2 · Cited by 390 · see citing works
Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase
Groote, M. A. D., Ochsner, U. A., Shiloh, M. U., Nathan, C., McCord, J. M., Dinauer, M. C., Libby, S. J., Vázquez‐Torres, A., Xu, Y., & Fang, F. C. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.13997 · Cited by 389 · see citing works
Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation
Sheppard, F. R., Kelher, M. R., Moore, E. E., McLaughlin, N. J. D., Banerjee, A. M., & Silliman, C. C. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.0804442 · Cited by 374 · see citing works
Neutrophil nicotinamide adenine dinucleotide phosphate oxidase assembly. Translocation of p47-phox and p67-phox requires interaction between p47-phox and cytochrome b558.
Heyworth, P. G., Curnutte, J. T., Nauseef, W. M., Volpp, B. D., Pearson, D. W., Rosen, H., & Clark, R. A. (1991) · Journal of Clinical Investigation · doi:10.1172/jci114993 · Cited by 373 · see citing works
Integrin signaling in neutrophils and macrophages uses adaptors containing immunoreceptor tyrosine-based activation motifs
Mócsai, A., Abram, C. L., Jakus, Z., Hu, Y., Lanier, L. L., & Lowell, C. A. (2006) · Nature Immunology · doi:10.1038/ni1407 · Cited by 369 · see citing works
Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane
Benna, J. E., Dang, P. M., & Gougerot‐Pocidalo, M. (2008) · Seminars in Immunopathology · doi:10.1007/s00281-008-0118-3 · Cited by 361 · see citing works
Deficiency of Src family kinases p59/61hck and p58c-fgr results in defective adhesion-dependent neutrophil functions.
Lowell, C. A., Fumagalli, L., & Berton, G. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.133.4.895 · Cited by 360 · see citing works
Novel cytochrome b system in phagocytic vacuoles of human granulocytes
Segal, A. W., & Jones, O. T. G. (1978) · Nature · doi:10.1038/276515a0 · Cited by 357 · see citing works
Myeloperoxidase: Contribution to the Microbicidal Activity of Intact Leukocytes
Klebanoff, S. J. (1970) · Science · doi:10.1126/science.169.3950.1095 · Cited by 347 · see citing works
Chronic Granulomatous Disease
Holland, S. M. (2012) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2012.11.002 · Cited by 345 · see citing works
Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils
Kobayashi, S. D., Braughton, K. R., Whitney, A. R., Voyich, J. M., Schwan, T. G., Musser, J. M., & DeLeo, F. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1833375100 · Cited by 336 · see citing works
CR3 (Mac-1, alpha M beta 2, CD11b/CD18) and Fc gamma RIII cooperate in generation of a neutrophil respiratory burst: requirement for Fc gamma RIII and tyrosine phosphorylation.
Zhou, M., & Brown, E. J. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.6.1407 · Cited by 324 · see citing works
Binding of the PX domain of p47phox to phosphatidylinositol 3,4‐bisphosphate and phosphatidic acid is masked by an intramolecular interaction
Karathanassis, D., Stahelin, R. V., Bravo, J., Perišić, O., Pacold, C. M., Cho, W., & Williams, R. L. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf519 · Cited by 321 · see citing works
A specific p47phox -serine phosphorylated by convergent MAPKs mediates neutrophil NADPH oxidase priming at inflammatory sites
Dang, P. M. (2006) · Journal of Clinical Investigation · doi:10.1172/jci27544 · Cited by 319 · see citing works
Molecular basis for Rac2 regulation of phagocyte NADPH oxidase
Diebold, B. A., & Bokoch, G. M. (2001) · Nature Immunology · doi:10.1038/85259 · Cited by 318 · see citing works
NADPH Oxidase Activation and Assembly During Phagocytosis
DeLeo, F. R., Allen, L. H., Apicella, M. A., & Nauseef, W. M. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.12.6732 · Cited by 313 · see citing works
Neutrophils exposed to bacterial lipopolysaccharide upregulate NADPH oxidase assembly.
DeLeo, F. R., Renee, J., McCormick, S. J., Nakamura, M., Apicella, M. A., Weiss, J. P., & Nauseef, W. M. (1998) · Journal of Clinical Investigation · doi:10.1172/jci949 · Cited by 312 · see citing works
Structure of the TPR Domain of p67phox in Complex with Rac·GTP
Lapouge, K., Smith, S. J. M., Walker, P. A., Gamblin, S. J., Smerdon, S. J., & Rittinger, K. (2000) · Molecular Cell · doi:10.1016/s1097-2765(05)00091-2 · Cited by 311 · see citing works
Neutrophil Extracellular Traps: How to Generate and Visualize Them
Brinkmann, V., Laube, B., Abed, U. A., Goosmann, C., & Zychlinsky, A. (2010) · Journal of Visualized Experiments · doi:10.3791/1724 · Cited by 301 · see citing works
The Comparative Toxicity of Nitric Oxide and Peroxynitrite to Escherichia coli
Brunelli, L., Crow, J. P., & Beckman, J. S. (1995) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1995.1044 · Cited by 284 · see citing works
Assessment of chlorination by human neutrophils
Foote, C. S., Goyne, T. E., & Lehrer, R. I. (1983) · Nature · doi:10.1038/301715a0 · Cited by 281 · see citing works
Regulation and termination of NADPH oxidase activity
DeCoursey, T. E., & Ligeti, E. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-5177-1 · Cited by 268 · see citing works
Src-family and Syk Kinases in Activating and Inhibitory Pathways in Innate Immune Cells: Signaling Cross TalkPreprint
Lowell, C. A. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002352 · Cited by 264 · see citing works
Rac translocates independently of the neutrophil NADPH oxidase components p47phox and p67phox. Evidence for its interaction with flavocytochrome b558.
Heyworth, P. G., Bohl, B. P., Bokoch, G., & Curnutte, J. T. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47341-3 · Cited by 263 · see citing works
Signal transduction during Fc receptor-mediated phagocytosis
García-García, E., & Rosales, C. (2002) · Journal of Leukocyte Biology · doi:10.1189/jlb.72.6.1092 · Cited by 249 · see citing works
Granule protein processing and regulated secretion in neutrophils
Sheshachalam, A., Srivastava, N., Mitchell, T., Lacy, P., & Eitzen, G. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00448 · Cited by 247 · see citing works
Tetratricopeptide Repeat (TPR) Motifs of p67 Participate in Interaction with the Small GTPase Rac and Activation of the Phagocyte NADPH Oxidase
Koga, H., Terasawa, H., Nunoi, H., Takeshige, K., Inagaki, F., & Sumimoto, H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.35.25051 · Cited by 244 · see citing works
Bactericidal activity of a superoxide anion-generating system. A model for the polymorphonuclear leukocyte.
Rosen, H., & Klebanoff, S. J. (1979) · The Journal of Experimental Medicine · doi:10.1084/jem.149.1.27 · Cited by 244 · see citing works
Arachidonic Acid and Phosphorylation Synergistically Induce a Conformational Change of p47 to Activate the Phagocyte NADPH Oxidase
Shiose, A., & Sumimoto, H. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.18.13793 · Cited by 243 · see citing works
Neutrophil priming: the cellular signals that say ‘amber’ but not ‘green’
Hallett, M. B., & LLOYDS, D. (1995) · Immunology Today · doi:10.1016/0167-5699(95)80178-2 · Cited by 240 · see citing works
Phosphorylation of the Respiratory Burst Oxidase Subunit p47 as Determined by Two-dimensional Phosphopeptide Mapping
Benna, J. E., Faust, L. R., Johnson, J. L., & BABIOR, B. M. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.11.6374 · Cited by 239 · see citing works
Mechanism for Phosphorylation-induced Activation of the Phagocyte NADPH Oxidase Protein p47
Ago, T., Nunoi, H., Ito, T., & Sumimoto, H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.47.33644 · Cited by 232 · see citing works
Protein Kinase C ζ Phosphorylates a Subset of Selective Sites of the NADPH Oxidase Component p47 phox and Participates in Formyl Peptide-Mediated Neutrophil Respiratory Burst
Dang, P. M., Fontayne, A., Hakim, J., Benna, J. E., & Périanin, A. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.1206 · Cited by 225 · see citing works
Salmonella Pathogenicity Island 2-Encoded Type III Secretion System Mediates Exclusion of NADPH Oxidase Assembly from the Phagosomal Membrane
Gallois, A., Klein, J. R., Allen, L. H., Jones, B. D., & Nauseef, W. M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.9.5741 · Cited by 222 · see citing works
Vav GEFs are required for β2 integrin-dependent functions of neutrophils
Gakidis, M. A. M., Culleré, X., Olson, T. S., Wilsbacher, J. L., Zhang, B., Moores, S. L., Ley, K. F., Swat, W., Mayadas, T. N., & Brugge, J. S. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200404166 · Cited by 222 · see citing works
Escherichia coli xth mutants are hypersensitive to hydrogen peroxide
Demple, B., Halbrook, J., & Linn, S. (1983) · Journal of Bacteriology · doi:10.1128/jb.153.2.1079-1082.1983 · Cited by 221 · see citing works
Reactive oxygen species in phagocytic leukocytes
Robinson, J. M. (2008) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0461-4 · Cited by 216 · see citing works
Akt Phosphorylates p47 phox and Mediates Respiratory Burst Activity in Human Neutrophils
Chen, Q., Powell, D. W., Rane, M. J., Singh, S. P., Butt, W., Klein, J. B., & McLeish, K. R. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.10.5302 · Cited by 214 · see citing works
Cross-regulation of signaling by ITAM-associated receptors
Ivashkiv, L. B. (2009) · Nature Immunology · doi:10.1038/ni.1706 · Cited by 212 · see citing works
Rac2 Is an Essential Regulator of Neutrophil Nicotinamide Adenine Dinucleotide Phosphate Oxidase Activation in Response to Specific Signaling Pathways
Kim, C., & Dinauer, M. C. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.1223 · Cited by 207 · see citing works
Hydrogen peroxide inactivates the Escherichia coli Isc iron‐sulphur assembly system, and OxyR induces the Suf system to compensate
Jang, S., & Imlay, J. A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07418.x · Cited by 205 · see citing works
X-Linked Chronic Granulomatous Disease: Mutations in the CYBB Gene Encoding the gp91-phox Component of Respiratory-Burst Oxidase
Rae, J., Newburger, P. E., Dinauer, M. C., Noack, D., Hopkins, P. J., Kuruto, R., & Curnutte, J. T. (1998) · The American Journal of Human Genetics · doi:10.1086/301874 · Cited by 204 · see citing works
Regulation of the NADPH Oxidase and Associated Ion Fluxes During Phagocytosis
Nunes, P., Demaurex, N., & Dinauer, M. C. (2013) · Traffic · doi:10.1111/tra.12115 · Cited by 204 · see citing works
Methodological advances: the unsung heroes of the GPCR structural revolution
Ghosh, E., Kumari, P., Jaiman, D., & Shukla, A. K. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3933 · Cited by 201 · see citing works
Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils
Selvatici, R., Falzarano, M. S., Mollica, A., & Spisani, S. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.01.034 · Cited by 200 · see citing works
Regulation of the phagocyte NADPH oxidase activity: phosphorylation of gp91 phox /NOX2 by protein kinase C enhances its diaphorase activity and binding to Rac2, p67 phox , and p47 phox
Raad, H., Paciet, M.-H., Boussetta, T., Kroviarski, Y., Morel, F., Quinn, M. T., Gougerot‐Pocidalo, M., Dang, P. M., & Benna, J. E. (2008) · The FASEB Journal · doi:10.1096/fj.08-114553 · Cited by 198 · see citing works
ITAM-mediated Signaling by the T-Cell Antigen ReceptorPreprint
Love, P. E., & Hayes, S. M. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a002485 · Cited by 197 · see citing works
The Mitogen-Activated Protein Kinase Extracellular Signal-Regulated Kinase 1/2 Pathway Is Involved in formyl-Methionyl-Leucyl-Phenylalanine-Induced p47phox Phosphorylation in Human Neutrophils
Dewas, C., Fay, M., Gougerot‐Pocidalo, M., & Benna, J. E. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.9.5238 · Cited by 195 · see citing works
Redundant Hydrogen Peroxide Scavengers Contribute to Salmonella Virulence and Oxidative Stress Resistance
Hébrard, M., Viala, J. P. M., Méresse, S., Barras, F., & Aussel, L. (2009) · Journal of Bacteriology · doi:10.1128/jb.00144-09 · Cited by 190 · see citing works
Multiple Phenotypic Changes Define Neutrophil Priming
Miralda, I., Uriarte, S. M., & McLeish, K. R. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00217 · Cited by 189 · see citing works
Pivotal Advance: Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape
McCaffrey, R. L., & Allen, L. H. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0406287 · Cited by 188 · see citing works
Generation of signals activating neutrophil functions by leukocyte integrins: LFA-1 and gp150/95, but not CR3, are able to stimulate the respiratory burst of human neutrophils.
Berton, G., Laudanna, C., Sorio, C., et al. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.116.4.1007 · Cited by 187 · see citing works
Neutrophils from p40phox−/− mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing
Ellson, C. D., Davidson, K., Ferguson, G., O'Connor, R. P., Stephens, L., & Hawkins, P. T. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20052069 · Cited by 182 · see citing works
A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram‐negative bacteria
Korshunov, S., & Imlay, J. A. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.02719.x · Cited by 178 · see citing works
Protein kinase C-β contributes to NADPH oxidase activation in neutrophils
Dekker, L. V., Leitges, M., Altschuler, G. M., MISTRY, N., MCDERMOTT, A., Roes, J., & Segal, A. W. (2000) · Biochemical Journal · doi:10.1042/bj3470285 · Cited by 176 · see citing works
Disparate Impact of Oxidative Host Defenses Determines the Fate of Salmonella during Systemic Infection in Mice
Burton, N. A., Schürmann, N., Casse, O., Steeb, A. K., Claudi, B., Zankl, J., Schmidt, A., & Bumann, D. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2013.12.006 · Cited by 175 · see citing works
Human Neutrophils Kill Streptococcus pneumoniae via Serine Proteases
Standish, A. J., & Weiser, J. N. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900688 · Cited by 174 · see citing works
Biallelic neutrophil Na-antigen system is associated with a polymorphism on the phospho-inositol-linked Fc gamma receptor III (CD16)
Huizinga, T. W. J., Kleijer, M., Tetteroo, P. A. T., Roos, D., & Borne, A. E. G. K. V. D. (1990) · Blood · doi:10.1182/blood.v75.1.213.213 · Cited by 169 · see citing works
The N-formyl peptide receptors and the anaphylatoxin C5a receptors: An overview
Rabiet, M., HUET, E., & Boulay, F. (2007) · Biochimie · doi:10.1016/j.biochi.2007.02.015 · Cited by 166 · see citing works
Genetic disorders coupled to ROS deficiency
O’Neill, S., Brault, J., Stasia, M.-J., & Knaus, U. G. (2015) · Redox Biology · doi:10.1016/j.redox.2015.07.009 · Cited by 164 · see citing works
Dual role of phagocytic NADPH oxidase in bacterial killing
Rada, B., Geiszt, M., Káldi, K., Tímár, C. I., & Ligeti, E. (2004) · Blood · doi:10.1182/blood-2004-03-1005 · Cited by 161 · see citing works
Activation of mitogen-activated protein kinase cascades during priming of human neutrophils by TNF-α and GM-CSF
McLeish, K. R., Knall, C., Ward, R. A., Gerwins, P., Coxon, P. Y., Klein, J. B., & Johnson, G. L. (1998) · Journal of Leukocyte Biology · doi:10.1002/jlb.64.4.537 · Cited by 160 · see citing works
DNA repair is more important than catalase for Salmonella virulence in mice.
Buchmeier, N. A., Libby, S. J., Xu, Y., Loewen, P. C., Switala, J., Guiney, D. G., & Fang, F. C. (1995) · Journal of Clinical Investigation · doi:10.1172/jci117750 · Cited by 158 · see citing works
Priming of the Neutrophil Respiratory Burst Involves p38 Mitogen-activated Protein Kinase-dependent Exocytosis of Flavocytochrome b 558-containing Granules
Ward, R. A., Nakamura, M., & McLeish, K. R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003017200 · Cited by 158 · see citing works
The Ferritin-Like Dps Protein Is Required for <i>Salmonella enterica</i> Serovar Typhimurium Oxidative Stress Resistance and Virulence
Halsey, T. A., Vazquez-Torres, A., Gravdahl, D. J., Fang, F. C., & Libby, S. J. (2004) · Infection and Immunity · doi:10.1128/iai.72.2.1155-1158.2004 · Cited by 155 · see citing works
Contribution of Glutathione Peroxidase to the Virulence of Streptococcus pyogenes
Brenot, A., King, K. Y., Janowiak, B. E., Griffith, O. W., & Caparon, M. G. (2003) · Infection and Immunity · doi:10.1128/iai.72.1.408-413.2004 · Cited by 148 · see citing works
Integrin-mediated signaling in human neutrophil functioning
Williams, M. A., & Solomkin, J. S. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.65.6.725 · Cited by 148 · see citing works
Crystal Structure of the Rac1−RhoGDI Complex Involved in NADPH Oxidase Activation,
Grizot, S., Fauré, J., Fieschi, F., et al. (2001) · Biochemistry · doi:10.1021/bi010288k · Cited by 146 · see citing works
The Src family kinases Hck, Fgr, and Lyn are critical for the generation of the in vivo inflammatory environment without a direct role in leukocyte recruitment
Kovács, M., Németh, T., Jakus, Z., Sitaru, C., Simon, E., Futosi, K., Botz, B., Helyes, Z., Lowell, C. A., & Mócsai, A. (2014) · The Journal of Experimental Medicine · doi:10.1084/jem.20132496 · Cited by 146 · see citing works
Inhibition of the Fc receptor-mediated oxidative burst in macrophages by the Yersinia pseudotuberculosis tyrosine phosphatase
Bliska, J. B., & Black, D. S. (1995) · Infection and Immunity · doi:10.1128/iai.63.2.681-685.1995 · Cited by 146 · see citing works
Redox Signal Transduction: Mutations Shifting [2Fe-2S] Centers of the SoxR Sensor-Regulator to the Oxidized Form
Hidalgo, E., Ding, H., & Demple, B. (1997) · Cell · doi:10.1016/s0092-8674(00)81864-4 · Cited by 143 · see citing works
Regulation of the Phagocyte NADPH Oxidase by Rac GTPase
Bokoch, G., & Zhao, T. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.1533 · Cited by 142 · see citing works
Ultrastructural localization of cytochrome b in the membranes of resting and phagocytosing human granulocytes.
Jesaitis, A. J., Buescher, E. S., Harrison, D. J., Quinn, M. T., Parkos, C. A., Livesey, S. A., & Linner, J. G. (1990) · Journal of Clinical Investigation · doi:10.1172/jci114509 · Cited by 142 · see citing works
PI3Kβ Plays a Critical Role in Neutrophil Activation by Immune Complexes
Kulkarni, S., Sitaru, C., Jakus, Z., Anderson, K. E., Damoulakis, G., Davidson, K., Hirose, M., Juss, J. K., Oxley, D., Chessa, T. A. M., et al. (2011) · Science Signaling · doi:10.1126/scisignal.2001617 · Cited by 141 · see citing works
The role of ferritins in the physiology of <i>Salmonella enterica</i> sv. Typhimurium: a unique role for ferritin B in iron‐sulphur cluster repair and virulence
Velayudhan, J., Castor, M., Richardson, A., Main‐Hester, K. L., & Fang, F. C. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05600.x · Cited by 140 · see citing works
Dual Role of Rac in the Assembly of NADPH Oxidase, Tethering to the Membrane and Activation of p67
Sarfstein, R., Gorzalczany, Y., Mizrahi, A., Berdichevsky, Y., Molshanski-Mor, S., Weinbaum, C., Hirshberg, M., Dagher, M., & Pick, E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m312394200 · Cited by 138 · see citing works
Community Behavior and Spatial Regulation within a Bacterial Microcolony in Deep Tissue Sites Serves to Protect against Host Attack
Davis, K. M., Mohammadi, S., & Isberg, R. R. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.11.008 · Cited by 135 · see citing works
P-Rex1 Is a Primary Rac2 Guanine Nucleotide Exchange Factor in Mouse Neutrophils
Dong, X., Mo, Z., Bokoch, G., Guo, C., Li, Z., & Wu, D. (2005) · Current Biology · doi:10.1016/j.cub.2005.09.014 · Cited by 135 · see citing works
Localization of Rac2 via the C terminus and aspartic acid 150 specifies superoxide generation, actin polarity and chemotaxis in neutrophils
Filippi, M., Harris, C. E., Meller, J., et al. (2004) · Nature Immunology · doi:10.1038/ni1081 · Cited by 134 · see citing works
Helicobacter pylori Disrupts NADPH Oxidase Targeting in Human Neutrophils to Induce Extracellular Superoxide Release
Allen, L. H., Beecher, B. R., Lynch, J. T., Rohner, O. V., & Wittine, L. M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3658 · Cited by 129 · see citing works
Phosphorylation of the NADPH Oxidase Component p67PHOX by ERK2 and P38MAPK: Selectivity of Phosphorylated Sites and Existence of an Intramolecular Regulatory Domain in the Tetratricopeptide-Rich Region
Dang, P. M., Morel, F., Gougerot‐Pocidalo, M., & Benna, J. E. (2003) · Biochemistry · doi:10.1021/bi0205754 · Cited by 128 · see citing works
Neutrophil-mediated oxidative burst and host defense are controlled by a Vav-PLCγ2 signaling axis in mice
Graham, D. B., Robertson, C. M., Bautista, J., Mascarenhas, F., Diacovo, M. J., Montgrain, V., Lam, S. K., Cremasco, V., Dunne, W. M., Faccio, R., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci32729 · Cited by 124 · see citing works
Innate Immune Responses to Tuberculosis
Schorey, J. S., & Schlesinger, L. S. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.tbtb2-0010-2016 · Cited by 124 · see citing works
Antagonists of Phosphatidylinositol 3-Kinase Block Activation of Several Novel Protein Kinases in Neutrophils
Ding, J., Vlahos, C. J., Liu, R., Brown, R. F., & Badweyt, J. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.19.11684 · Cited by 123 · see citing works
Maternal genomic neutrophil FcRIII deficiency leading to neonatal isoimmune neutropenia [see comments]
Huizinga, T. W. J., Kuijpers, R. W. A. M., Kleijer, M., et al. (1990) · Blood · doi:10.1182/blood.v76.10.1927.1927 · Cited by 123 · see citing works
How did life survive Earth's great oxygenation?
Fischer, W. W., Hemp, J., & Valentine, J. S. (2016) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2016.03.013 · Cited by 121 · see citing works
Pseudomonas aeruginosa Effector ExoS Inhibits ROS Production in Human Neutrophils
Vareechon, C., Zmina, S. E., Karmakar, M., et al. (2017) · Cell Host & Microbe · doi:10.1016/j.chom.2017.04.001 · Cited by 121 · see citing works
Critical role of phospholipase Cγ2 in integrin and Fc receptor-mediated neutrophil functions and the effector phase of autoimmune arthritis
Jakus, Z., Simon, E., Frommhold, D., Sperandio, M., & Mócsai, A. (2009) · Journal of Experimental Medicine · doi:10.1084/jem.20081859 · Cited by 119 · see citing works
The Src Family Kinases Hck and Fgr Are Dispensable for Inside-Out, Chemoattractant-Induced Signaling Regulating β2 Integrin Affinity and Valency in Neutrophils, but Are Required for β2 Integrin-Mediated Outside-In Signaling Involved in Sustained Adhesion
Giagulli, C., Ottoboni, L., Caveggion, E., Rossi, B., Lowell, C. A., Constantin, G., Laudanna, C., & Berton, G. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.1.604 · Cited by 118 · see citing works
Immunoreceptor-like signaling by β2 and β3 integrins
Jakus, Z., Fodor, S., Abram, C. L., Lowell, C. A., & Mócsai, A. (2007) · Trends in Cell Biology · doi:10.1016/j.tcb.2007.09.001 · Cited by 117 · see citing works
Interleukin-8-induced Priming of Neutrophil Oxidative Burst Requires Sequential Recruitment of NADPH Oxidase Components into Lipid Rafts
Guichard, C., Pédruzzi, E., Dewas, C., Fay, M., Pouzet, C., Bens, M., Vandewalle, A., Ogier‐Denis, É., Gougerot‐Pocidalo, M., & Elbim, C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m506594200 · Cited by 116 · see citing works
Chronic granulomatous disease: Clinical, functional, molecular, and genetic studies. The Israeli experience with 84 patients
Wolach, B., Gavrieli, R., de Boer, M., van Leeuwen, K., Berger‐Achituv, S., Stauber, T., Ben‐Ari, J., Rottem, M., Schlesinger, Y., Grisaru‐Soen, G., et al. (2016) · American Journal of Hematology · doi:10.1002/ajh.24573 · Cited by 116 · see citing works
The p40 and p47 PX Domains of NADPH Oxidase Target Cell Membranes via Direct and Indirect Recruitment by Phosphoinositides
Zhan, Y., Virbasius, J. V., Song, X., Pomerleau, D. P., & Zhou, G. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109520200 · Cited by 115 · see citing works
Distinct Ligand-dependent Roles for p38 MAPK in Priming and Activation of the Neutrophil NADPH Oxidase
Brown, G. E., Stewart, M. Q., Bissonnette, S. A., Elia, A. E. H., Wilker, E., & Yaffe, M. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314258200 · Cited by 115 · see citing works
Granule Exocytosis Contributes to Priming and Activation of the Human Neutrophil Respiratory Burst
Uriarte, S. M., Rane, M. J., Luerman, G. C., Barati, M. T., Ward, R. A., Nauseef, W. M., & McLeish, K. R. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003112 · Cited by 115 · see citing works
Modulation of the Activities of Catalase−Peroxidase HPI of Escherichia coli by Site-Directed Mutagenesis
Hillar, A., Peters, B., Pauls, R. J., Loboda, A., Zhang, H., Mauk, A. G., & Loewen, P. C. (2000) · Biochemistry · doi:10.1021/bi0000059 · Cited by 115 · see citing works
156Pro-->Gln substitution in the light chain of cytochrome b558 of the human NADPH oxidase (p22-phox) leads to defective translocation of the cytosolic proteins p47-phox and p67-phox.
Leusen, J. H. W., Bolscher, B. G. J. M., Hilarius, P. M., Weening, R. S., Kaulfersch, W., Seger, R. A., Roos, D., & Verhoeven, A. J. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.180.6.2329 · Cited by 111 · see citing works
A point mutation in gp91-phox of cytochrome b558 of the human NADPH oxidase leading to defective translocation of the cytosolic proteins p47-phox and p67-phox.
Leusen, J. H. W., de Boer, M., Bolscher, B. G. J. M., Hilarius, P. M., Weening, R. S., Ochs, H. D., Roos, D., & Verhoeven, A. J. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117207 · Cited by 108 · see citing works
The Src Family Kinases Hck and Fgr Regulate Neutrophil Responses to N -Formyl-Methionyl-Leucyl-Phenylalanine
Fumagalli, L., Zhang, H., Baruzzi, A., Lowell, C. A., & Berton, G. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.6.3874 · Cited by 108 · see citing works
Defective localization of the NADPH phagocyte oxidase to Salmonella -containing phagosomes in tumor necrosis factor p55 receptor-deficient macrophages
Vázquez‐Torres, A., Fantuzzi, G., Edwards, C. K., Dinarello, C. A., & Fang, F. C. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.041618998 · Cited by 107 · see citing works
Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst
Aussel, L., Zhao, W., Hébrard, M., Guilhon, A., Viala, J. P. M., Henri, S., Chasson, L., Gorvel, J., Barras, F., & Méresse, S. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07611.x · Cited by 107 · see citing works
Tumor necrosis factor as an activator of human granulocytes. Potentiation of the metabolisms triggered by the Ca2+-mobilizing agonists.
Yuo, A., Kitagawa, S., Suzuki, I., et al. (1989) · The Journal of Immunology · doi:10.4049/jimmunol.142.5.1678 · Cited by 106 · see citing works
Catalase (KatA) and KatA-associated protein (KapA) are essential to persistent colonization in the Helicobacter pylori SS1 mouse model
Harris, A. G., Wilson, J. E., Danon, S. J., Dixon, M. F., Donegan, K., & Hazell, S. L. (2003) · Microbiology · doi:10.1099/mic.0.26012-0 · Cited by 106 · see citing works
The prolyl isomerase Pin1 acts as a novel molecular switch for TNF-α–induced priming of the NADPH oxidase in human neutrophils
Boussetta, T., Gougerot‐Pocidalo, M., Hayem, G., et al. (2010) · Blood · doi:10.1182/blood-2010-03-273094 · Cited by 103 · see citing works
Gonococci possessing only certain P.II outer membrane proteins interact with human neutrophils
Fischer, S. H., & Rest, R. F. (1988) · Infection and Immunity · doi:10.1128/iai.56.6.1574-1579.1988 · Cited by 103 · see citing works
Activation of the Phagocyte NADPH Oxidase Protein p47
Huang, J., & Kleinberg, M. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.28.19731 · Cited by 102 · see citing works
Genetic redirection of T cells for cancer therapy
McCaffrey, R. L., Schwartz, J. T., Lindemann, S. R., et al. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.1209811 · Cited by 102 · see citing works
Differential Requirement for SLP-76 Domains in T Cell Development and Function
Myung, P. S., Derimanov, G. S., Jordan, M. S., et al. (2001) · Immunity · doi:10.1016/s1074-7613(01)00253-9 · Cited by 101 · see citing works
Rab27a and Rab27b Regulate Neutrophil Azurophilic Granule Exocytosis and NADPH oxidase Activity by Independent Mechanisms
Johnson, J. L., Brzezinska, A. A., Tolmachova, T., Munafó, D. B., Ellis, B. A., Seabra, M. C., Hong, H., & Catz, S. D. (2009) · Traffic · doi:10.1111/j.1600-0854.2009.01029.x · Cited by 98 · see citing works
The Neutrophil Btk Signalosome Regulates Integrin Activation during Sterile Inflammation
Volmering, S., Block, H., Boras, M., Lowell, C. A., & Zarbock, A. (2016) · Immunity · doi:10.1016/j.immuni.2015.11.011 · Cited by 98 · see citing works
PI3K Signaling in Neutrophils
Hawkins, P. T., Stephens, L., Suire, S., & Wilson, M. I. (2010) · Current topics in microbiology and immunology · doi:10.1007/82_2010_40 · Cited by 97 · see citing works
Streptolysin O Rapidly Impairs Neutrophil Oxidative Burst and Antibacterial Responses to Group A Streptococcus
Uchiyama, S., Döhrmann, S., Timmer, A. M., Dixit, N., Ghochani, M., Bhandari, T., Timmer, J. C., Sprague, K., Bubeck-Wardenburg, J., Simon, S. I., et al. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00581 · Cited by 97 · see citing works
Transient Association of the Nicotinamide Adenine Dinucleotide Phosphate Oxidase Subunits p47phox and p67phox With Phagosomes in Neutrophils From Patients With X-Linked Chronic Granulomatous Disease
Allen, L. H., DeLeo, F. R., Gallois, A., Toyoshima, S., Suzuki, K., & Nauseef, W. M. (1999) · Blood · doi:10.1182/blood.v93.10.3521.410k21_3521_3530 · Cited by 96 · see citing works
evasion of the NADPH phagocyte oxidase
Vázquez‐Torres, A., & Fang, F. C. (2001) · Microbes and Infection · doi:10.1016/s1286-4579(01)01492-7 · Cited by 95 · see citing works
Phosphorylation of p22 Is Mediated by Phospholipase D-dependent and -independent Mechanisms
Regier, D. S., Greene, D. G., Sergeant, S., Jesaitis, A. J., & McPhail, L. C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004703200 · Cited by 95 · see citing works
The Lyn Tyrosine Kinase Negatively Regulates Neutrophil Integrin Signaling
Pereira, S. E., & Lowell, C. A. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.3.1319 · Cited by 95 · see citing works
Maternal genomic neutrophil FcRIII deficiency leading to neonatal isoimmune neutropenia [see comments]
Huizinga, T. W. J., Kuijpers, R. W. A. M., Kleijer, M., et al. (1990) · Blood · doi:10.1182/blood.v76.10.1927.bloodjournal76101927 · Cited by 93 · see citing works
Direct measurement of oxidative and nitrosative stress dynamics in Salmonella inside macrophages
van der Heijden, J., Bosman, E. S., Reynolds, L. A., & Finlay, B. B. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1414569112 · Cited by 89 · see citing works
Staphylococcus aureus, phagocyte NADPH oxidase and chronic granulomatous disease
Buvelot, H., Posfay-Barbe, K. M., Linder, P., Schrenzel, J., & Krause, K. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw042 · Cited by 88 · see citing works
Neutrophil direction sensing and superoxide production linked by the GTPase-activating protein GIT2
Mazaki, Y., Hashimoto, S., Tsujimura, T., Morishige, M., Hashimoto, A., Aritake, K., Yamada, A., Nam, J.-M., Kiyonari, H., Nakao, K., et al. (2006) · Nature Immunology · doi:10.1038/ni1349 · Cited by 86 · see citing works
Vav Proteins in Neutrophils Are Required for FcγR-Mediated Signaling to Rac GTPases and Nicotinamide Adenine Dinucleotide Phosphate Oxidase Component p40(phox)
Utomo, A. R. H., Culleré, X., Glogauer, M., Swat, W., & Mayadas, T. N. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.9.6388 · Cited by 86 · see citing works
Interactions of Neisseria gonorrhoeae with Adherent Polymorphonuclear Leukocytes
Simons, M. P., Nauseef, W. M., & Apicella, M. A. (2005) · Infection and Immunity · doi:10.1128/iai.73.4.1971-1977.2005 · Cited by 86 · see citing works
Interleukin-8 primes human neutrophils for enhanced superoxide anion production.
Wozniak, A., Betts, W. H., Murphy, G. A., & Rokicinski, M. (1993) · PubMed Central · Cited by 85 · see citing works
Bacillus anthracis Toxins Inhibit Human Neutrophil NADPH Oxidase Activity
Crawford, M. A., Cv, A., Bourdeau, R. W., & Bokoch, G. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.12.7557 · Cited by 85 · see citing works
Regulation of In Vitro and In Vivo Immune Functions by the Cytosolic Adaptor Protein SKAP-HOM
Togni, M., Swanson, K. D., Reimann, S., Kliche, S., Pearce, A. C., Simeoni, L., Reinhold, D., Wienands, J., Neel, B. G., Schraven, B. L., et al. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.18.8052-8063.2005 · Cited by 85 · see citing works
Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes
Criss, A. K., & Seifert, H. S. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01205.x · Cited by 83 · see citing works

Flagged first, then by citations

Sorted by citations

The Chemistry of Reactive Oxygen Species (ROS) Revisited: Outlining Their Role in Biological Macromolecules (DNA, Lipids and Proteins) and Induced Pathologies
Juan, C. A., Pérez de la Lastra, J. M., Plou, F. J., & Pérez-Lebeña, E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094642 · Cited by 2,810 · see citing works
Inflammation and aging: signaling pathways and intervention therapies
Li, X., Li, C., Zhang, W., Wang, Y., Qian, P., & Huang, H. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01502-8 · Cited by 1,443 · see citing works
Age and Age-Related Diseases: Role of Inflammation Triggers and Cytokines
Rea, I. M., Gibson, D. S., McGilligan, V., McNerlan, S. E., Alexander, H. D., & Ross, O. A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00586 · Cited by 1,267 · see citing works
NADPH Oxidases (NOX): An Overview from Discovery, Molecular Mechanisms to Physiology and Pathology
Vermot, A., Petit-Härtlein, I., Smith, S. M. E., & Fieschi, F. (2021) · Antioxidants · doi:10.3390/antiox10060890 · Cited by 766 · see citing works
Neutrophil chemoattractant receptors in health and disease: Double-edged swords
Metzemaekers, M., Gouwy, M., & Proost, P. (2020) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-0412-0 · Cited by 570 · see citing works
Beneficial and Detrimental Effects of Reactive Oxygen Species on Lifespan: A Comprehensive Review of Comparative and Experimental Studies
Shields, H. J., Traa, A., & Van Raamsdonk, J. M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.628157 · Cited by 478 · see citing works
Neutrophils at the crossroads of innate and adaptive immunity
Rosales, C. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.4mir0220-574rr · Cited by 372 · see citing works
Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity
Andrés, C. M. C., Pérez de la Lastra, J. M., Andrés Juan, C., Plou, F. J., & Pérez-Lebeña, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031841 · Cited by 342 · see citing works
Reactive oxygen species in pathogen clearance: The killing mechanisms, the adaption response, and the side effects
Li, H., Zhou, X., Huang, Y., Liao, B., Cheng, L., & Ren, B. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.622534 · Cited by 284 · see citing works
The Role of Reactive Species on Innate Immunity
Andrés, C., Pérez de la Lastra, J., Juan, C., Plou, F., & Pérez-Lebeña, E. (2022) · Vaccines · doi:10.3390/vaccines10101735 · Cited by 142 · see citing works
A multiple-hit hypothesis involving reactive oxygen species and myeloperoxidase explains clinical deterioration and fatality in COVID-19
Goud, P. T., Bai, D., & Abu-Soud, H. M. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.51811 · Cited by 88 · see citing works
Role of Neutrophils in the Pathogenesis of Nonalcoholic Steatohepatitis
Hwang, S., Yun, H., Moon, S., Cho, Y. E., & Gao, B. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.751802 · Cited by 84 · see citing works

Inhibition of NADPH oxidase promotes alternative and anti‐inflammatory microglial activation during neuroinflammation
Choi, S., Aïd, S., Kim, H., Jackson, S. H., & Bosetti, F. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07572.x · Cited by 222 · see citing works
Bioluminescence Imaging of NADPH Oxidase Activity in Different Animal Models
Han, W., Li, H., Segal, B. H., & Blackwell, T. S. (2012) · Journal of Visualized Experiments · doi:10.3791/3925 · Cited by 16 · see citing works
Class I phosphoinositide 3-kinases control sustained NADPH oxidase activation in adherent neutrophils
Song, Z., Hudik, E., Bars, R. L., Roux, B., Dang, P. M., Benna, J. E., Nüße, O., & Dupré‐Crochet, S. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114088 · Cited by 21 · see citing works
Effect of Metazoa on Proportion of Physiologically Active Bacteria.
Fujimoto, N., Asuka, I., Suzuki, M., et al. (1999) · Japanese Journal of Water Treatment Biology · doi:10.2521/jswtb.35.279 · Cited by 1 · see citing works
Src is an upstream regulator of NADPH oxidase in human vascular smooth muscle cells
Touyz, R. M. (2002) · American Journal of Hypertension · doi:10.1016/s0895-7061(02)02302-6

Authors: Nguyen, G. T., Green, E. R., & Mecsas, J.
Affiliations: Tufts University (US)
Corresponding author: Mecsas, Joan
ORCID: Nguyen, Giang T.
Green, Erin R.
Mecsas, Joan
Venue: Frontiers in Cellular and Infection Microbiology
Publisher: Frontiers Media SA
Published: 2017-08-25
Volume: 7
Pages: 373-373
ISSN: 2235-2988 (ISSN-L)
DOI: 10.3389/fcimb.2017.00373
PMC: PMC5574878
OpenAlex: W2747004888
Cited by: 741
References: 276
Citations by year: 2026: 73 · 2025: 71 · 2024: 101 · 2023: 100 · 2022: 117 · 2021: 118 · 2020: 93 · 2019: 53 · 2018: 14 · 2017: 1
FWCI: 4.52
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Cellular and Infection Microbiology (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institutes of Health (AI113166)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: NADPH oxidase, neutrophils, reactive oxygen species, respiratory burst, neutrophil extracellular traps, G protein-coupled receptors, Toll-like receptors, fMLP, integrin activation, Fc receptors, bacterial effector proteins, oxidative stress detoxification, phagosome, antimicrobial host defense
MeSH terms: Animals, Bacterial Infections, Bacterial Toxins, Enzyme Activation, Humans, Inflammation, Mice, Transgenic, Neutrophils, Phagosomes, Integrins, Respiratory Burst, Reactive Oxygen Species, Receptors, Cytokine, Oxidative Stress, NADPH Oxidases, Receptors, G-Protein-Coupled, Toll-Like Receptors, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Neutrophils to the ROScue: Mechanisms of NADPH oxidase activation and bacterial resistance

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks