The DOI matches its Crossref record; 258 of the 259 references it cites were found in a registry or an index.
Nitric oxide and redox mechanisms in the immune response
Open accessAbstract
The role of redox molecules, such as NO and ROS, as key mediators of immunity has recently garnered renewed interest and appreciation. To regulate immune responses, these species trigger the eradication of pathogens on the one hand and modulate immunosuppression during tissue-restoration and wound-healing processes on the other. In the acidic environment of the phagosome, a variety of RNS and ROS is produced, thereby providing a cauldron of redox chemistry, which is the first line in fighting infection. Interestingly, fluctuations in the levels of these same reactive intermediates orchestrate other phases of the immune response. NO activates specific signal transduction pathways in tumor cells, endothelial cells, and monocytes in a concentration-dependent manner. As ROS can react directly with NO-forming RNS, NO bioavailability and therefore, NO response(s) are changed. The NO/ROS balance is also important during Th1 to Th2 transition. In this review, we discuss the chemistry of NO and ROS in the context of antipathogen activity and immune regulation and also discuss similarities and differences between murine and human production of these intermediates.
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In the citing paper
“nNOS and eNOS, which are expressed constitutively, produce a low level of NO for short periods (seconds to minutes).447”
From Role of neuroinflammation in neurodegeneration development (2023) · cites this paper as [447]
In the citing paper
“At present, three types of NOS have been identified, including neuronal NOS (nNOS, also named as NOS1), endothelial NOS (eNOS, also named as NOS3), and inducible NOS (iNOS, also named as NOS2).447”
From Role of neuroinflammation in neurodegeneration development (2023) · cites this paper as [447]
In the citing paper
“Intracellular communication and immune response are mediated by at least five classes of endogenously generated reactive small molecules (Figure 1): nitric oxide (NO) and reactive nitrogen oxide species (RNS), reactive oxygen species (ROS), eicosanoids and reactive lipid species (formed by oxidation of fatty acids), a variety of sulfur-based species such as hydrogen sulfide (H2S), thiols and disul”
From Signaling and stress: The redox landscape in NOS2 biology (2015) · cites this paper as [3]
In the citing paper
“An additional mechanism for IL-10 production is through NO-dependent increases of COX2 [3, 57]].”
From Signaling and stress: The redox landscape in NOS2 biology (2015) · cites this paper as [3]
In the citing paper
“In chronic disease, involving extended exposure to pathogens or particulates such as plaques in the brain or following a critical mutation, wound healing processes persist and can lead to fibrosis or tumor growth [3].”
From Signaling and stress: The redox landscape in NOS2 biology (2015) · cites this paper as [3]
In the citing paper
“These molecules can act as sensors to steer signaling cascades during inflammation, for example from a T helper (Th) 1 to a Th2 cytokine response [3, 87].”
From Signaling and stress: The redox landscape in NOS2 biology (2015) · cites this paper as [3]
In the citing paper
“In the phagosome, iron deposition facilitates the sterilization process in conjunction with ROS and nitrite [3].”
From Signaling and stress: The redox landscape in NOS2 biology (2015) · cites this paper as [3]
In the citing paper
“Lysis of Staphylococcus bacteria involves the sequential exposure to respiratory burst followed by •NO exposure [126].”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [126]
In the citing paper
“•NO and RNS eradicate bacteria by nitrosylation and oxidation of bacterial macromolecules [126].”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [126]
In the citing paper
“The •NO/ROS balance is also important during the transition from Th1 to Th2 [125,126].”
From The Role of Reactive Species on Innate Immunity (2022) · cites this paper as [126]
In the citing paper
“Recognition of bacteria by macrophages leads to ROS production in different cellular compartments, where they fulfill different antibacterial functions.”
From Functions of ROS in Macrophages and Antimicrobial Immunity (2021) · cites this paper as [234]
Citations
Cites
Items 201–258 of 258
Kline, J. N., Hunninghake, G. M., He, B., Monick, M. M., & Hunninghake, G. W. (1998) · Experimental Lung Research · doi:10.3109/01902149809046050 · Cited by 62
Role of Nitric Oxide Synthase Type 2 in Acute Infection with Murine Cytomegalovirus
Noda, S., TANAKA, K. A., Sawamura, S., Sasaki, M., Matsumoto, T., Mikami, K., Aiba, Y., Hasegawa, H., Kawabe, N., & Koga, Y. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.5.3533 · Cited by 61
Kavoosi, G., Ardestani, S. K., & Kariminia, A. (2009) · Parasitology · doi:10.1017/s0031182009990473 · Cited by 61
Cytoprotective and Anti‐Inflammatory Actions of Carbon Monoxide in Organ Injury and Sepsis Models
Ryter, S. W., & Choi, A. M. K. (2006) · Novartis Foundation symposium · doi:10.1002/9780470059593.ch12 · Cited by 60
Yim, C., McGregor, J. R., Kwon, O. D., Bastian, N. R., Rees, M. R., Mori, M., Hibbs, J. B., & Samlowski, W. E. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.9.4382 · Cited by 60
Akaki, T., Tomioka, H., Shimizu, T., Dekio, S., & Sato, K. (2000) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.2000.01298.x · Cited by 57
Ohshima, H., Tsuda, M., Adachi, H., Ogura, T., Sügimura, T., & Esumi, H. (1991) · Carcinogenesis · doi:10.1093/carcin/12.7.1217 · Cited by 57
Zell, R., Markgraf, R., Schmidtke, M., G�rlach, M., Stelzner, A., Henke, A., Sigusch, H. H., & Gl�ck, B. (2004) · Medical Microbiology and Immunology · doi:10.1007/s00430-003-0198-6 · Cited by 54
Toxoplasma gondii: The role of IFN-gamma, TNFRp55 and iNOS in inflammatory changes during infection
Silva, N. M., Vieira, J. C. M., Carneiro, C. M., & Tafuri, W. L. (2009) · Experimental Parasitology · doi:10.1016/j.exppara.2009.05.011 · Cited by 54
Hardy, S. J., Ferrante, A., Poulos, A., Robinson, B. S., Johnson, D. W., & Murray, A. W. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.153.4.1754 · Cited by 53
Small‐conductance Cl– channels contribute to volume regulation and phagocytosis in microglia
Ducharme, G., Newell, E. W., Pinto, C., & Schlichter, L. C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05802.x · Cited by 52
Nitric Oxide and Intracellular Heme
Kim, Y.-M., Bergonia, H. A., Müller, C., Pitt, B. R., Watkins, W. D., & Lancaster, J. R. (1995) · Advances in pharmacology · doi:10.1016/s1054-3589(08)61092-3 · Cited by 51
Blanchette, J., Abu‐Dayyeh, I., Hassani, K., Whitcombe, L. A., & Olivier, M. (2008) · Immunology · doi:10.1111/j.1365-2567.2008.02929.x · Cited by 50
Kibbe, M. R., Billiar, T. R., & Tzeng, E. (2000) · Circulation Research · doi:10.1161/01.res.86.8.829 · Cited by 50
Chakrabarti, G. (1999) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/43.3.359 · Cited by 50
Crompton, T., Outram, S. V., Buckland, J., & Owen, M. J. (1998) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199806)28:06 · Cited by 49
Analysis of differentially expressed genes in nitric oxide-exposed human monocytic cells
Turpaev, K. T., Bouton, C., Diet, A., Glatigny, A., & Drapier, J. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.02.002 · Cited by 47
Hydrogen Sulfide: A Novel Mediator of Leukocyte Activation
Zhang, H., & Bhatia, M. (2008) · Immunopharmacology and Immunotoxicology · doi:10.1080/08923970802278045 · Cited by 45
Prostaglandin E2 inhibits replication of HIV-1 in macrophages through activation of protein kinase A
Hayes, M. M., Lane, B. R., King, S. R., Markovitz, D. M., & Coffey, M. (2002) · Cellular Immunology · doi:10.1016/s0008-8749(02)00017-5 · Cited by 43
Kreckler, L. M., Gizewski, E. T., Wan, T. C., & Auchampach, J. A. (2009) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.157651 · Cited by 42
Nitric oxide in dengue and dengue haemorrhagic fever: necessity or nuisance?
Chaturvedi, U. C., & Nagar, R. (2009) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2009.00544.x · Cited by 41
Kaku, Y., Nanri, H., 崎村, 知., 江島, 邦., Kuroiwa, A., & Ikeda, M. (1997) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(96)00156-5 · Cited by 41
Sciorati, C., Rovere, P. Q., Ferrarini, M., Paolucci, C., Heltai, S., Vaiani, R., Clementi, E., & Manfredi, A. A. (1999) · PubMed · Cited by 37
Cytokine interactions that determine the outcome of mycobacterial infection of macrophages
Reljić, R., Stylianou, E., Balu, S., & K‐C., J. (2010) · Cytokine · doi:10.1016/j.cyto.2010.04.005 · Cited by 37
Endogenous formation of N-nitroso compounds: a current perspective.
Tannenbaum, S. R. (1987) · PubMed · Cited by 37
Sciorati, C., Rovere, P. Q., Ferrarini, M., Paolucci, C., Heltai, S., Vaiani, R., Clementi, E., & Manfredi, A. A. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.3.1570 · Cited by 37
Inhibitors of 3C Cysteine Proteinases from Picornaviridae
Lall, M. S., Jain, R., & Vederas, J. C. (2004) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026043387836 · Cited by 36
Ogawa, R., Pacelli, R., Espey, M. G., Miranda, K. M., Friedman, N., Kim, S., Cox, G., Mitchell, J. B., Wink, D. A., & Russo, A. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00470-6 · Cited by 35
Self-citationSkorokhod, O. A., Schwarzer, E., Ceretto, M., & Arese, P. (2007) · Malaria Journal · doi:10.1186/1475-2875-6-73 · Cited by 35
Nussler, A. K. (1995) · Hepatology · doi:10.1016/0270-9139(95)90459-x · Cited by 35
Ali, M., Al-Olayan, E. M., Lewis, S., Matthews, H., & Hurd, H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012634 · Cited by 34
Lähde, Korhonen, R., & Moilanen (2000) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2000.00781.x · Cited by 33
Mendes-Ribeiro, A., Moss, M. B., Siqueira, M. A. S., Moraes, T. L., Ellory, J. C., Mann, G. E., & Brunini, T. M. C. (2008) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2008.04970.x · Cited by 32
Direct Covalent Modification as a Strategy to Inhibit Nuclear Factor-Kappa B
Pande, V., Sousa, S. F., & Ramos, M. J. (2009) · Current Medicinal Chemistry · doi:10.2174/092986709789578222 · Cited by 30
Nitric Oxide Is Protective in Listeric Meningoencephalitis of Rats
Remer, K. A., Jungi, T. W., Fatzer, R., Täuber, M. G., & Leib, S. L. (2001) · Infection and Immunity · doi:10.1128/iai.69.6.4086-4093.2001 · Cited by 30
Matthiesen, S., Lindemann, D., Warnken, M., Juergens, U. R., & Racké, K. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.10.043 · Cited by 29
Badger, A. M. (1986) · Journal of Leukocyte Biology · doi:10.1002/jlb.40.6.725 · Cited by 29
Jacobs, A. T., & Ignarro, L. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211642200 · Cited by 28
Devey, L. R., Mohr, E., Bellamy, C. O. C., Simpson, K. J., Henderson, N. C., Harrison, E. M., Ross, J. A., & Wigmore, S. J. (2009) · Transplantation · doi:10.1097/tp.0b013e3181ae3067 · Cited by 27
Dukes, C. S., Yu, Y., Rivadeneira, E., Sauls, D. L., Liao, H., Haynes, B. F., & Weinberg, J. B. (1995) · Journal of Virology · doi:10.1128/jvi.69.7.4000-4005.1995 · Cited by 26
Nitric Oxide in Mycobacterium tuberculosis Infection
Chan, J., & Jl, F. (2002) · Springer eBooks · doi:10.1007/0-306-46816-6_14 · Cited by 26
Lintas, C., Clark, A., Fox, J. G., Tannenbaum, S. R., & Newberne, P. M. (1982) · Carcinogenesis · doi:10.1093/carcin/3.2.161 · Cited by 25
Remote Tissue Injury Primes Hepatocytes for Nitric Oxide Synthesis
Freeswick, P. D., Wan, Y., Geller, D. A., Nussler, A. K., & Billiar, T. R. (1994) · Journal of Surgical Research · doi:10.1006/jsre.1994.1132 · Cited by 24
Reversible S-Nitrosation and Inhibition of HIV-1 Protease
Sehajpal, P. K., Basu, A., Ogiste, J. S., & Lander, H. M. (1999) · Biochemistry · doi:10.1021/bi9912995 · Cited by 23
Wu, F. Y., Cepinskas, G., Wilson, J. X., & Tyml, K. (2001) · Microcirculation · doi:10.1111/j.1549-8719.2001.tb00188.x · Cited by 23
Nitric Oxide-Derived Nitrosating Species and Gene Expression in Human Monocytic Cells
Turpaev, K. T., Bouton, C., & Drapier, J. (2004) · Biochemistry · doi:10.1021/bi049831y · Cited by 22
Disparities in the respiratory burst between human and rat neutrophils
Johnson, J. L., Moore, E. E., Hiester, A. A., Tamura, D. Y., Zallen, G. S., & Silliman, C. C. (1999) · Journal of Leukocyte Biology · doi:10.1002/jlb.65.2.211 · Cited by 21
Resistance to endotoxic shock in mice lacking natriuretic peptide receptor‐A
Panayiotou, C. M., Baliga, R. S., Stidwill, R. P., Taylor, V., Singer, M., & Hobbs, A. J. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00830.x · Cited by 19
Kavoosi, G., Ardestani, S. K., Kariminia, A., Abolhassani, M., & Turco, S. J. (2006) · Experimental Parasitology · doi:10.1016/j.exppara.2006.04.006 · Cited by 19
Modulation of Monocyte Chemokine Production and Nuclear Factor Kappa B Activity by Oxidants
Lee, J. S., Kahlon, S. S., Culbreth, R., & Cooper, J. A. D. (1999) · Journal of Interferon & Cytokine Research · doi:10.1089/107999099313613 · Cited by 19
Bonaparte, K. L., Hudson, C. A., Wu, C. W., & Massa, P. T. (2006) · Glia · doi:10.1002/glia.20344 · Cited by 18
Induction of myocardial nitric oxide synthase by Coxsackie B3 virus in mice
Robinson, Zhang, Bevan, Belder, D., Moncada, S., Martin, & Archard (1999) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.1999.00505.x · Cited by 17
Turpaev, K. T., Glatigny, A., Bignon, J. S., Delacroix, H., & Drapier, J. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.10.054 · Cited by 16
Park, K. S., Guo, Z., Shao, L., Du, Q., & Geller, D. A. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.05.036 · Cited by 15
Turpaev, K. T., & Drapier, J. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2009.01.015 · Cited by 12
Sosroseno, W., Musa, M., Ravichandran, M., Ibrahim, M. F., Bird, P. S., & Seymour, G. J. (2006) · Oral Microbiology and Immunology · doi:10.1111/j.1399-302x.2006.00300.x · Cited by 7
Basu, A., Sehajpal, P. K., Ogiste, J. S., & Lander, H. M. (1999) · Antioxidants and Redox Signaling · doi:10.1089/ars.1999.1.1-105 · Cited by 5
Sciorati, C., Rovere, P. Q., Ferrarini, M., et al. (1999) · Cited by 5
Flagged first, then by citations
1 of the 259 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Williams, 1988, Nitrosation
- Rhee, 2000, Sci. STKE
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“At present, three types of NOS have been identified, including neuronal NOS (nNOS, also named as NOS1), endothelial NOS (eNOS, also named as NOS3), and inducible NOS (iNOS, also named as NOS2).(447) nNOS and eNOS, which are expressed constitutively, produce a low level of NO for short periods (seconds to minutes).”
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Blaser, H., Dostert, C., Mak, T. W., & Brenner, D. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.12.002 · Cited by 1,008
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Metadata
- Authors
- Wink, D. A., Hines, H. B., Cheng, R. Y. S., Switzer, C. H., Flores-Santana, W., Vitek, M. P., Ridnour, L. A., & Colton, C. A.
- Affiliations
- National Institutes of Health (US)
- United States Army Medical Research Institute of Infectious Diseases (US)
- Radiation Biology Branch, National Cancer Institute, National Institutes of Health , Bethesda, Maryland, USA
- Duke Medical Center (US)
- Corresponding author
- Wink, David A
- Colton, Carol A
- ORCID
- Venue
- Journal of Leukocyte Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-01-13
- Volume
- 89
- Issue
- 6
- Pages
- 873-891
- ISSN
- 0741-5400 (ISSN-L)
- 1938-3673
- PMC
- PMC3100761
- OpenAlex
- W2171480404
- Cited by
- 765
- References
- 259
- Citations by year
- 2026: 25 · 2025: 58 · 2024: 46 · 2023: 57 · 2022: 69 · 2021: 74 · 2020: 56 · 2019: 44 · 2018: 40 · 2017: 60 · 2016: 53 · 2015: 57 · 2014: 48 · 2013: 35 · 2012: 27
- FWCI
- 3.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Leukocyte Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (R01AG031845, R01AG031124)
- 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
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Keywords
- nitric oxide, reactive oxygen species, reactive nitrogen species, redox signaling, immune regulation, phagosome, immunosuppression, wound healing, Th1/Th2 balance, signal transduction, pathogen eradication
- MeSH terms
- Animals, Humans, Immunity, Cellular, Nitric Oxide, Oxidation-Reduction, Signal Transduction
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