Oxygen-dependent and oxygen-independent mechanisms of microbicidal activity of neutrophils
Abstract
The essential role of the phagocyte in host defense against the enormous variety of microbial predators in our environment requires the availability of a "universal" weapon effective against most microbes, or an arsenal of different agents with specificity for different classes and species of microorganisms. Both polymorphonuclear leukocytes (PMN) and mononuclear phagocytes possess, or can produce, a wide range of antimicrobial agents providing these cells with an "overkill" capacity [1] that will usually bypass microbial defenses against a given antimicrobial device of the phagocyte. In this brief review we focus on the PMN because its antimicrobial systems have been analyzed most extensively. However, the killing mechanisms of mononuclear phagocytes and PMN are sufficiently similar to permit the insights gained from the study of the PMN to be applied to all phagocytes, including macrophages.
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Neutrophils use both O2-dependent and O2-independent mechanisms to kill micro-organisms.
“Ultimately, neutrophils use both O2-dependent and O2-independent mechanisms to kill micro-organisms [85].”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [85]
Cites
Weiss, J. P., Elsbach, P., Olsson, I., & Odeberg, H. (1978) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)40872-6 · Cited by 451 · see citing works
Self-citationGrisham, M. B., Jefferson, M. M., Melton, D. F., & Thomas, E. L. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)90979-8 · Cited by 396 · see citing works
Long-Lived Oxidants Generated by Human Neutrophils: Characterization and Bioactivity
Weiss, S. J., Lampert, M. B., & Test, S. T. (1983) · Science · doi:10.1126/science.6635660 · Cited by 390 · see citing works
The Reticuloendothelial System
Friedman, H. P., Escobar, M., Reichard, S. M., & Filkins, J. P. (1985) · Springer eBooks · doi:10.1007/978-1-4613-2353-2 · Cited by 314 · see citing works
Purification and antibacterial activity of antimicrobial peptides of rabbit granulocytes
Selsted, M. E., Szklarek, D., & Lehrer, R. I. (1984) · Infection and Immunity · doi:10.1128/iai.45.1.150-154.1984 · Cited by 306 · see citing works
Elsbach, P., Weiss, J. P., Franson, R. C., Beckerdite-Quagliata, S., Schneider, A., & Harris, L. (1979) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)86622-x · Cited by 235 · see citing works
Self-citationPrimary structures of six antimicrobial peptides of rabbit peritoneal neutrophils.
Selsted, M. E., Brown, D. M., DeLange, R. J., Harwig, S. S. L., & Lehrer, R. I. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)89110-4 · Cited by 230 · see citing works
Weiss, S. J., & Slivka, A. (1982) · Journal of Clinical Investigation · doi:10.1172/jci110447 · Cited by 158 · see citing works
Elsbach, P., & Weiss, J. P. (1983) · Clinical Infectious Diseases · doi:10.1093/clinids/5.5.843 · Cited by 143 · see citing works
Self-citationWeiss, J. P., Franson, R. C., Beckerdite-Quagliata, S., Schmeidler, K., & Elsbach, P. (1975) · Journal of Clinical Investigation · doi:10.1172/jci107915 · Cited by 121 · see citing works
Self-citationResistance of Gram-negative Bacteria to Purified Bactericidal Leukocyte Proteins
Weiss, J. P., Beckerdite-Quagliata, S., & Elsbach, P. (1980) · Journal of Clinical Investigation · doi:10.1172/jci109707 · Cited by 117 · see citing works
Self-citationWeiss, J. P., Victor, M., STENDHAL, O., & Elsbach, P. (1982) · Journal of Clinical Investigation · doi:10.1172/jci110535 · Cited by 106 · see citing works
Self-citationThe Killing of Pathogens by Phagocytes
Gabig, T. G., & Babior, B. (1981) · Annual Review of Medicine · doi:10.1146/annurev.me.32.020181.001525 · Cited by 101 · see citing works
Weiss, J. P., Muello, K., Victor, M., & Elsbach, P. (1984) · The Journal of Immunology · doi:10.4049/jimmunol.132.6.3109 · Cited by 90 · see citing works
Self-citationWeiss, J. P., Victor, M., & Elsbach, P. (1983) · Journal of Clinical Investigation · doi:10.1172/jci110798 · Cited by 84 · see citing works
Self-citationWeiss, J. P., Kao, L., Victor, M., & Elsbach, P. (1985) · Journal of Clinical Investigation · doi:10.1172/jci111947 · Cited by 82 · see citing works
Self-citationBeckerdite-Quagliata, S., Mooney, C. L., Weiss, J. P., Franson, R., & Elsbach, P. (1974) · The Journal of Experimental Medicine · doi:10.1084/jem.140.2.396 · Cited by 71 · see citing works
Self-citationElsbach, P., Pettis, P. K., Beckerdite-Quagliata, S., & Franson, R. (1973) · Journal of Bacteriology · doi:10.1128/jb.115.2.490-497.1973 · Cited by 60 · see citing works
Self-citationWeiss, J. P., & Elsbach, P. (1977) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(77)90205-x · Cited by 40 · see citing works
Self-citationElsbach, P., Weiss, J. P., & Kao, L. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)89639-9 · Cited by 30 · see citing works
Self-citationvan Houte, A. J., Elsbach, P., Verkleij, A. J., & Weiss, J. P. (1977) · Infection and Immunity · doi:10.1128/iai.15.2.556-559.1977 · Cited by 12 · see citing works
Self-citation
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Protective effects of C5a blockade in sepsis
Czermak, B. J., Sarma, V. J., Pierson, C. L., Warner, R. L., Huber-Lang, M. S., Bless, N. M., Schmal, H., Friedl, H. P., & Ward, P. A. (1999) · Nature Medicine · doi:10.1038/10512 · Cited by 399 · see citing works
Rothe, G., Oser, A., & Valet, G. (1988) · Die Naturwissenschaften · doi:10.1007/bf00368326 · Cited by 282 · see citing works
Seiler, P. J., Aichele, P., Bandermann, S., Hauser, A. E., Lu, B., Gerard, N. P., Gerard, C. J., Ehlers, S., Mollenkopf, H., & Kaufmann, S. H. E. (2003) · European Journal of Immunology · doi:10.1002/eji.200323956 · Cited by 237 · see citing works
Lehrer, R. I., Ganz, T., Szklarek, D., & Selsted, M. E. (1988) · Journal of Clinical Investigation · doi:10.1172/jci113527 · Cited by 229 · see citing works
Role of C5a in Multiorgan Failure During Sepsis
Huber-Lang, M. S., Sarma, V. J., Lu, K. T., McGuire, S. R., Padgaonkar, V. A., Guo, R., Younkin, E. M., Kunkel, R. G., Ding, J., Erickson, R. W., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.1193 · Cited by 224 · see citing works
Activation of neutrophils by recombinant interleukin 6
Borish, L., Rosenbaum, R., Albury, L., & Clark, S. (1989) · Cellular Immunology · doi:10.1016/0008-8749(89)90026-9 · Cited by 211 · see citing works
Complement-Induced Impairment of Innate Immunity During Sepsis
Huber-Lang, M. S., Younkin, E. M., Sarma, J. V., McGuire, S. R., Lu, K. T., Guo, R. F., Padgaonkar, V. A., Curnutte, J. T., Erickson, R. W., & Ward, P. A. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.6.3223 · Cited by 200 · see citing works
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Elsbach, P., & Weiss, J. P. (1993) · Immunobiology · doi:10.1016/s0171-2985(11)80354-2 · Cited by 146 · see citing works
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A Noninvasive Fluorimetric Procedure for Measurement of Membrane Potential
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Zhao, C., Zhang, H., Wong, W., Sem, X., Han, H., Ong, S., Tan, Y., Yeap, W., Gan, C. S., Ng, K.-Q., et al. (2009) · Journal of Proteome Research · doi:10.1021/pr900364p · Cited by 99 · see citing works
Interleukin-4 is a neutrophil activator
Boey, H., Rosenbaum, R., Castracane, J. M., & Borish, L. (1989) · Journal of Allergy and Clinical Immunology · doi:10.1016/0091-6749(89)90115-2 · Cited by 80 · see citing works
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Mt, S., Appelberg, R., Silva, M. N., & Macedo, P. M. (1987) · Infection and Immunity · doi:10.1128/iai.55.9.2006-2016.1987 · Cited by 57 · see citing works
Ginsburg, I. (1987) · Inflammation · doi:10.1007/bf00915991 · Cited by 53 · see citing works
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Phagocytic Cell-Derived Inflammatory Mediators and Lung Disease
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Wiese, M., Gerlach, R. G., Popp, I., Matuszak, J., Mahapatro, M., Castiglione, K., Chakravortty, D., Willam, C., Hensel, M., Bogdan, C., et al. (2012) · Infection and Immunity · doi:10.1128/iai.05972-11 · Cited by 39 · see citing works
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Inzana, T. J., Siddaramppa, S., & Inzana, T. J. (2004) · Animal Health Research Reviews · doi:10.1079/ahr200466 · Cited by 30 · see citing works
Retention of phagocytic functions in cryopreserved human monocytes
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Briheim, G., Follin, P., Sandstedt, S., & Dahlgren, C. (1989) · Inflammation · doi:10.1007/bf00914928 · Cited by 26 · see citing works
Neutrophil and Eosinophil Granules as Stores of “Defense” Proteins
Gennaro, R., Romeo, D., Skerlavaj, B., & Zanetti, M. (1991) · Blood cell biochemistry · doi:10.1007/978-1-4615-3796-0_12 · Cited by 26 · see citing works
Ngeleka, M., Martineau‐Doizé, B., & Fairbrother, J. M. (1994) · Infection and Immunity · doi:10.1128/iai.62.2.398-404.1994 · Cited by 21 · see citing works
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Lerche, C. J., Schwartz, F. A., Pries‐Heje, M. M., Fosbøl, E. L., Iversen, K. K., Jensen, P. Ø., Høiby, N., Hyldegaard, O., Bundgaard, H., & Moser, C. E. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.805964 · Cited by 14 · see citing works
França, T. T., Al-Sbiei, A., Bashir, G. H., Mohamed, Y. A., Salgado, R. C., Barreiros, L. A., Napoleão, S. M. D. S., Weber, C. W., Ferreira, J. F. S., Aranda, C. S., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.148652 · Cited by 11 · see citing works
Primary Immunodeficiency Syndromes and Their Manifestations in Lymph Nodes
Cottier, H., Kraft, R., & Meister, F. (1991) · Current topics in pathology · doi:10.1007/978-3-642-75522-4_4 · Cited by 11 · see citing works
Xue, L., Ainsworth, A. J., Hanson, L. A., Qian, Y., & Noya, M. (1999) · Developmental & Comparative Immunology · doi:10.1016/s0145-305x(98)00048-2 · Cited by 8 · see citing works
The role of neutrophils in the mechanisms of sepsis
Kosyreva, A. M., Miroshnichenko, E. A., & Makarova, O. V. (2024) · Russian Journal of Archive of Pathology · doi:10.17116/patol20248606182 · Cited by 7 · see citing works
Immunopharmacology of Oral Betalactams
Periti, P. (1998) · Journal of Chemotherapy · doi:10.1179/joc.1998.10.2.91 · Cited by 7 · see citing works
Nunes, A. P., dos Santos-Destro, Y. M., Rodrigues, A. C. J., Detoni, M. B., Cruz, E. M. S., Berbert, G. S., Park, B., Pires, M. F. M. K., Pavanelli, W. R., & Providello, M. V. (2025) · Life Sciences · doi:10.1016/j.lfs.2025.123779 · Cited by 5 · see citing works
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Prajsnar, T. K., Michno, B. J., Pooranachandran, N., Fenton, A. K., Mitchell, T. J., Dockrell, D. H., & Renshaw, S. A. (2022) · Cellular Microbiology · doi:10.1155/2022/9429516 · Cited by 4 · see citing works
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Rojas-Espinosa, O., Arce‐Paredes, P., Islas-Trujillo, S., Becerril-Villanueva, L. E., & Ponce-Regalado, M. D. (2024) · Modern Research in Inflammation · doi:10.4236/mri.2024.132002 · Cited by 2 · see citing works
Role of Complement in Multi-Organ Dysfunction Syndrome
Huber-Lang, M. S., Sarma, J. V., Zetoune, F. S., & Ward, P. A. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/1-4020-8056-5_22 · Cited by 1 · see citing works
Polymorphonuclear leukocytes in acute inflammation
Jones, O. T. G., & Cross, A. R. (1988) · Springer eBooks · doi:10.1007/978-94-009-1293-9_1 · Cited by 1 · see citing works
Neonatal Neutrophil Normal and Abnormal Physiology
Parravicini, E., van de Ven, C., & Cairo, M. S. (2004) · Elsevier eBooks · doi:10.1016/b978-0-7216-9654-6.50160-0
Neonatal Neutrophil Normal and Abnormal Physiology
Bhatia, M., Parravicini, E., van de Ven, C., & Cairo, M. S. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-3479-7.10154-5
Shephard, M. T., Merkhan, M. M., Dale, T. P., & Forsyth, N. R. (2023) · Research Square · doi:10.21203/rs.3.rs-3006436/v1
- Authors
- Elsbach, P., & Weiss, J.
- Affiliations
- NYU Langone Health (US)
- ORCID
- Weiss, Jerrold
- Venue
- Immunology Letters
- Publisher
- Elsevier BV
- Published
- 1985-01
- Volume
- 11
- Issue
- 3-4
- Pages
- 159-163
- ISSN
- 0165-2478 (ISSN-L)
- OpenAlex
- W1991397191
- Cited by
- 52
- References
- 21
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 2 · 2022: 3 · 2021: 2 · 2020: 2 · 2016: 1 · 2012: 1
- FWCI
- 1.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Immunology Letters (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01am005472-24)
- U.S. Public Health Service
- National Institute of Allergy and Infectious Diseases (AI-18571)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Life Sciences › Immunology and Microbiology › Microbiology › Antimicrobial Peptides and Activities
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- neutrophils, microbicidal activity, oxygen-dependent killing, polymorphonuclear leukocytes, phagocytes, antimicrobial mechanisms, mononuclear phagocytes, macrophages, host defense
- MeSH terms
- Animals, Blood Bactericidal Activity, Blood Proteins, Calcium, Cytotoxicity, Immunologic, Escherichia coli, Humans, Magnesium, Membrane Proteins, Neutrophils, Oxygen, Phagocytes, Rabbits, Antimicrobial Cationic Peptides, In Vitro Techniques
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