Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro
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The contribution of the NADPH phagocyte oxidase (phox) and inducible nitric oxide (NO) synthase (iNOS) to the antimicrobial activity of macrophages for Salmonella typhimurium was studied by using peritoneal phagocytes from C57BL/6, congenic gp91phox(-/)-, iNOS(-/)-, and doubly immunodeficient phox(-/)-iNOS(-/)- mice. The respiratory burst and NO radical (NO.) made distinct contributions to the anti-Salmonella activity of macrophages. NADPH oxidase-dependent killing is confined to the first few hours after phagocytosis, whereas iNOS contributes to both early and late phases of antibacterial activity. NO-derived species initially synergize with oxyradicals to kill S. typhimurium, and subsequently exert prolonged oxidase-independent bacteriostatic effects. Biochemical analyses show that early killing of Salmonella by macrophages coincides with an oxidative chemistry characterized by superoxide anion (O(2).(-)), hydrogen peroxide (H(2)O(2)), and peroxynitrite (ONOO(-)) production. However, immunofluorescence microscopy and killing assays using the scavenger uric acid suggest that peroxynitrite is not responsible for macrophage killing of wild-type S. typhimurium. Rapid oxidative bacterial killing is followed by a sustained period of nitrosative chemistry that limits bacterial growth. Interferon gamma appears to augment antibacterial activity predominantly by enhancing NO. production, although a small iNOS-independent effect was also observed. These findings demonstrate that macrophages kill Salmonella in a dynamic process that changes over time and requires the generation of both reactive oxidative and nitrosative species.
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Distinct amounts of iron are a prerequisite for sufficient translation of TNF and other cytokine messenger RNAs and for promotion of antimicrobial oxidative stress responses.
“In contrast, distinct amounts of iron are a prerequisite for sufficient translation of TNF and other cytokine messenger RNAs (Wang et al., 2008) and promotion of antimicrobial oxidative stress responses (Vazquez-Torres et al., 2000;Weiss and Schaible, 2015).”
From Iron in infection and immunity (2020) · cites this paper as Vazquez-Torres et al., 2000
The Discussion (page unavailable in our copy) reports that macrophages use an early oxidative phase to kill Salmonella and describes a possible role for metal ions in potentiating that killing. It does not identify iron, establish that particular amounts of iron are required, or address cytokine mRNA translation; the latter part is attached to Wang et al. in the citing sentence. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe NADPH oxidase (NOX)-2 complex at the plasma or phagolysosomal membranes channels electrons from NADPH in the cytosol to oxygen, generating superoxide (O2−) radicals within the phagosome.
“The enzyme complex responsible for the oxygen burst is the NADPH oxidase (NOX)-2 complex at the plasma or phagolysomal membranes which channels electrons from NADPH in the cytosol to oxygen, generating superoxide (O2−) radicals within the phagosome (Vazquez-Torres et al., 2000).”
From The Role of Iron Regulation in Immunometabolism and Immune-Related Disease (2019) · cites this paper as Vazquez-Torres et al., 2000
The microbicidal activity of activated macrophages depends critically on the phagocytic NADPH oxidase (NOX2/gp91phox) and the inducible form of nitric oxide synthase (iNOS/NOS2).
“The microbicidal activity of activated Mø depends critically on the phagocytic nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (NOX2/gp91 phox ) and the inducible form of nitric oxide (NO) synthase (iNOS/NOS2) [74,75].”
From The Iron age of host–microbe interactions (2015) · cites this paper as [74]
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Toyonaga, T., Matsuura, M., Mori, K., Honzawa, Y., Minami, N., Yamada, S., Kobayashi, T., Hibi, T., & Nakase, H. (2016) · Scientific Reports · doi:10.1038/srep35014 · Cited by 75 · see citing works
Collins, H. L., Kaufmann, S. H. E., & Schaible, U. E. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.7.3458 · Cited by 69 · see citing works
Mitterstiller, A.-M., Haschka, D., Dichtl, S., Nairz, M., Demetz, E., Talasz, H., Soares, M. P., Einwallner, E., Esterbauer, H., Fang, F. C., et al. (2016) · Cellular Microbiology · doi:10.1111/cmi.12578 · Cited by 62 · see citing works
Self-citationNairz, M., Schroll, A., Haschka, D., Dichtl, S., Tymoszuk, P., Demetz, E., Moser, P., Haas, H., Fang, F. C., Theurl, I., et al. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00110 · Cited by 46 · see citing works
Self-citationSalmonella enterica Infection Stimulates Macrophages to Hemophagocytose
Pilonieta, M. C., Moreland, S. M., English, C. N., & Detweiler, C. S. (2014) · mBio · doi:10.1128/mbio.02211-14 · Cited by 35 · see citing works
Brown, D. E., Nick, H. J., McCoy, M. W., Moreland, S. M., Stepanek, A. M., Benik, R., O'Connell, K. E., Pilonieta, M. C., Nagy, T. A., & Detweiler, C. S. (2015) · Infection and Immunity · doi:10.1128/iai.02863-14 · Cited by 31 · see citing works
Enhanced Virulence of <i>Salmonella enterica</i> Serovar Typhimurium after Passage through Mice
Mastroeni, P., Morgan, F. J. E., McKinley, T. J., Shawcroft, E., Clare, S., Maskell, D. J., & Grant, A. J. (2011) · Infection and Immunity · doi:10.1128/iai.00954-10 · Cited by 30 · see citing works
Self-citation
- Authors
- Vazquez-Torres, A., Jones-Carson, J., Mastroeni, P., Ischiropoulos, H., & Fang, F. C.
- Affiliations
- aDepartment of Medicine, University of Colorado Health Sciences Center, Denver, Colorado 80262
- University of Cambridge (GB)
- Children's Hospital of Philadelphia (US)
- University of Colorado Health (US)
- Venue
- The Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 2000-07-17
- Volume
- 192
- Issue
- 2
- Pages
- 227-236
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC2193262
- OpenAlex
- W2135004245
- Cited by
- 530
- References
- 63
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 10 · 2023: 14 · 2022: 11 · 2021: 9 · 2020: 21 · 2019: 17 · 2018: 11 · 2017: 17 · 2016: 24 · 2015: 17 · 2014: 21 · 2013: 23 · 2012: 30
- FWCI
- 8.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Experimental Medicine (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust
- National Institutes of Health (AI39557)
- Directorate for Biological Sciences
- National Institute of Allergy and Infectious Diseases (AI 39557, R01AI039557, F32AI010181, AI44486, AI-10181, R01AI044486)
- 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, inducible nitric oxide synthase, Salmonella typhimurium, salmonellosis, peritoneal macrophages, respiratory burst, nitric oxide, peroxynitrite, superoxide, hydrogen peroxide, nitrosative stress, interferon-gamma, gp91phox, bactericidal mechanism
- MeSH terms
- NADPH Oxidase 2, Animals, Macrophage Activation, Membrane Glycoproteins, Mice, Inbred C57BL, Phagocytosis, Salmonella typhimurium, Superoxides, Tyrosine, Reactive Oxygen Species, Macrophages, Peritoneal, Nitric Oxide Synthase, NADPH Oxidases, Mice, Nitric Oxide Synthase Type II
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