Oxidative Stress and Mitochondria Are Involved in Anaphylaxis and Mast Cell Degranulation: A Systematic Review
Anaphylaxis, an allergic reaction caused by the massive release of active mediators, can lead to anaphylactic shock (AS), the most severe and potentially life-threatening form of anaphylactic reaction. Nevertheless, understanding of its pathophysiology to support new therapies still needs to be impr...
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| Vydáno v: | Antioxidants Ročník 13; číslo 8; s. 920 |
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| Jazyk: | angličtina |
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29.07.2024
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| ISSN: | 2076-3921, 2076-3921 |
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| Abstract | Anaphylaxis, an allergic reaction caused by the massive release of active mediators, can lead to anaphylactic shock (AS), the most severe and potentially life-threatening form of anaphylactic reaction. Nevertheless, understanding of its pathophysiology to support new therapies still needs to be improved. We performed a systematic review, assessing the role and the complex cellular interplay of mitochondria and oxidative stress during anaphylaxis, mast cell metabolism and degranulation. After presenting the main characteristics of anaphylaxis, the oxidant/antioxidant balance and mitochondrial functions, we focused this review on the involvement of mitochondria and oxidative stress in anaphylaxis. Then, we discussed the role of oxidative stress and mitochondria following mast cell stimulation by allergens, leading to degranulation, in order to further elucidate mechanistic pathways. Finally, we considered potential therapeutic interventions implementing these findings for the treatment of anaphylaxis. Experimental studies evaluated mainly cardiomyocyte metabolism during AS. Cardiac dysfunction was associated with left ventricle mitochondrial impairment and lipid peroxidation. Studies evaluating in vitro mast cell degranulation, following Immunoglobulin E (IgE) or non-IgE stimulation, revealed that mitochondrial respiratory complex integrity and membrane potential are crucial for mast cell degranulation. Antigen stimulation raises reactive oxygen species (ROS) production from nicotinamide adenine dinucleotide phosphate (NADPH) oxidases and mitochondria, leading to mast cell degranulation. Moreover, mast cell activation involved mitochondrial morphological changes and mitochondrial translocation to the cell surface near exocytosis sites. Interestingly, antioxidant administration reduced degranulation by lowering ROS levels. Altogether, these results highlight the crucial role of oxidative stress and mitochondria during anaphylaxis and mast cell degranulation. New therapeutics against anaphylaxis should probably target oxidative stress and mitochondria, in order to decrease anaphylaxis-induced systemic and major organ deleterious effects. |
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| AbstractList | Anaphylaxis, an allergic reaction caused by the massive release of active mediators, can lead to anaphylactic shock (AS), the most severe and potentially life-threatening form of anaphylactic reaction. Nevertheless, understanding of its pathophysiology to support new therapies still needs to be improved. We performed a systematic review, assessing the role and the complex cellular interplay of mitochondria and oxidative stress during anaphylaxis, mast cell metabolism and degranulation. After presenting the main characteristics of anaphylaxis, the oxidant/antioxidant balance and mitochondrial functions, we focused this review on the involvement of mitochondria and oxidative stress in anaphylaxis. Then, we discussed the role of oxidative stress and mitochondria following mast cell stimulation by allergens, leading to degranulation, in order to further elucidate mechanistic pathways. Finally, we considered potential therapeutic interventions implementing these findings for the treatment of anaphylaxis. Experimental studies evaluated mainly cardiomyocyte metabolism during AS. Cardiac dysfunction was associated with left ventricle mitochondrial impairment and lipid peroxidation. Studies evaluating in vitro mast cell degranulation, following Immunoglobulin E (IgE) or non-IgE stimulation, revealed that mitochondrial respiratory complex integrity and membrane potential are crucial for mast cell degranulation. Antigen stimulation raises reactive oxygen species (ROS) production from nicotinamide adenine dinucleotide phosphate (NADPH) oxidases and mitochondria, leading to mast cell degranulation. Moreover, mast cell activation involved mitochondrial morphological changes and mitochondrial translocation to the cell surface near exocytosis sites. Interestingly, antioxidant administration reduced degranulation by lowering ROS levels. Altogether, these results highlight the crucial role of oxidative stress and mitochondria during anaphylaxis and mast cell degranulation. New therapeutics against anaphylaxis should probably target oxidative stress and mitochondria, in order to decrease anaphylaxis-induced systemic and major organ deleterious effects. Anaphylaxis, an allergic reaction caused by the massive release of active mediators, can lead to anaphylactic shock (AS), the most severe and potentially life-threatening form of anaphylactic reaction. Nevertheless, understanding of its pathophysiology to support new therapies still needs to be improved. We performed a systematic review, assessing the role and the complex cellular interplay of mitochondria and oxidative stress during anaphylaxis, mast cell metabolism and degranulation. After presenting the main characteristics of anaphylaxis, the oxidant/antioxidant balance and mitochondrial functions, we focused this review on the involvement of mitochondria and oxidative stress in anaphylaxis. Then, we discussed the role of oxidative stress and mitochondria following mast cell stimulation by allergens, leading to degranulation, in order to further elucidate mechanistic pathways. Finally, we considered potential therapeutic interventions implementing these findings for the treatment of anaphylaxis. Experimental studies evaluated mainly cardiomyocyte metabolism during AS. Cardiac dysfunction was associated with left ventricle mitochondrial impairment and lipid peroxidation. Studies evaluating in vitro mast cell degranulation, following Immunoglobulin E (IgE) or non-IgE stimulation, revealed that mitochondrial respiratory complex integrity and membrane potential are crucial for mast cell degranulation. Antigen stimulation raises reactive oxygen species (ROS) production from nicotinamide adenine dinucleotide phosphate (NADPH) oxidases and mitochondria, leading to mast cell degranulation. Moreover, mast cell activation involved mitochondrial morphological changes and mitochondrial translocation to the cell surface near exocytosis sites. Interestingly, antioxidant administration reduced degranulation by lowering ROS levels. Altogether, these results highlight the crucial role of oxidative stress and mitochondria during anaphylaxis and mast cell degranulation. New therapeutics against anaphylaxis should probably target oxidative stress and mitochondria, in order to decrease anaphylaxis-induced systemic and major organ deleterious effects.Anaphylaxis, an allergic reaction caused by the massive release of active mediators, can lead to anaphylactic shock (AS), the most severe and potentially life-threatening form of anaphylactic reaction. Nevertheless, understanding of its pathophysiology to support new therapies still needs to be improved. We performed a systematic review, assessing the role and the complex cellular interplay of mitochondria and oxidative stress during anaphylaxis, mast cell metabolism and degranulation. After presenting the main characteristics of anaphylaxis, the oxidant/antioxidant balance and mitochondrial functions, we focused this review on the involvement of mitochondria and oxidative stress in anaphylaxis. Then, we discussed the role of oxidative stress and mitochondria following mast cell stimulation by allergens, leading to degranulation, in order to further elucidate mechanistic pathways. Finally, we considered potential therapeutic interventions implementing these findings for the treatment of anaphylaxis. Experimental studies evaluated mainly cardiomyocyte metabolism during AS. Cardiac dysfunction was associated with left ventricle mitochondrial impairment and lipid peroxidation. Studies evaluating in vitro mast cell degranulation, following Immunoglobulin E (IgE) or non-IgE stimulation, revealed that mitochondrial respiratory complex integrity and membrane potential are crucial for mast cell degranulation. Antigen stimulation raises reactive oxygen species (ROS) production from nicotinamide adenine dinucleotide phosphate (NADPH) oxidases and mitochondria, leading to mast cell degranulation. Moreover, mast cell activation involved mitochondrial morphological changes and mitochondrial translocation to the cell surface near exocytosis sites. Interestingly, antioxidant administration reduced degranulation by lowering ROS levels. Altogether, these results highlight the crucial role of oxidative stress and mitochondria during anaphylaxis and mast cell degranulation. New therapeutics against anaphylaxis should probably target oxidative stress and mitochondria, in order to decrease anaphylaxis-induced systemic and major organ deleterious effects. |
| Audience | Academic |
| Author | Piotin, Anays Oulehri, Walid Charles, Anne-Laure Geny, Bernard Collange, Olivier Mertes, Paul-Michel Tacquard, Charles |
| AuthorAffiliation | 1 Physiology and Functional Exploration Service, Strasbourg University Hospital, 67000 Strasbourg, France; anays.piotin@chru-strasbourg.fr 3 Team 3072 “Mitochondria, Oxidative Stress and Muscle Protection”, Translational Medicine Federation of Strasbourg (FMTS), Faculty of Medicine, University of Strasbourg, 67000 Strasbourg, France; walid.oulehri@chru-strasbourg.fr (W.O.); anne.laure.charles@unistra.fr (A.-L.C.); olivier.collange@chru-strasbourg.fr (O.C.); paul.michel.mertes@chru-strasbourg.fr (P.-M.M.) 5 Établissement Français du Sang (EFS) Grand Est, French National Institute of Health and Medical Research), (INSERM) BPPS UMR_S1255, Fédération de Médecine Translationnelle de Strasbourg (FMTS), University of Strasbourg, 67000 Strasbourg, France 4 Department of Anesthesia and Intensive Care, Strasbourg University Hospital, 67000 Strasbourg, France; charlesambroise.tacquard@chru-strasbourg.fr 2 Division of Asthma and Allergy, Chest Diseases Department, Strasbourg University Hospital, 67000 |
| AuthorAffiliation_xml | – name: 5 Établissement Français du Sang (EFS) Grand Est, French National Institute of Health and Medical Research), (INSERM) BPPS UMR_S1255, Fédération de Médecine Translationnelle de Strasbourg (FMTS), University of Strasbourg, 67000 Strasbourg, France – name: 3 Team 3072 “Mitochondria, Oxidative Stress and Muscle Protection”, Translational Medicine Federation of Strasbourg (FMTS), Faculty of Medicine, University of Strasbourg, 67000 Strasbourg, France; walid.oulehri@chru-strasbourg.fr (W.O.); anne.laure.charles@unistra.fr (A.-L.C.); olivier.collange@chru-strasbourg.fr (O.C.); paul.michel.mertes@chru-strasbourg.fr (P.-M.M.) – name: 4 Department of Anesthesia and Intensive Care, Strasbourg University Hospital, 67000 Strasbourg, France; charlesambroise.tacquard@chru-strasbourg.fr – name: 1 Physiology and Functional Exploration Service, Strasbourg University Hospital, 67000 Strasbourg, France; anays.piotin@chru-strasbourg.fr – name: 2 Division of Asthma and Allergy, Chest Diseases Department, Strasbourg University Hospital, 67000 Strasbourg, France |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39199166$$D View this record in MEDLINE/PubMed https://hal.science/hal-04907501$$DView record in HAL |
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| CitedBy_id | crossref_primary_10_1007_s10787_025_01685_2 crossref_primary_10_3390_biom15091347 crossref_primary_10_3390_microorganisms13081883 |
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| Keywords | antioxidant mast cells degranulation mitochondria anaphylactic shock anaphylaxis reactive oxygen species (ROS) oxidative stress B. Oxidative oxidative stress B. Oxidative oxidative stress reactive oxygen species (ROS) antioxidant mitochondria anaphylaxis anaphylactic shock mast cells degranulation |
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| Title | Oxidative Stress and Mitochondria Are Involved in Anaphylaxis and Mast Cell Degranulation: A Systematic Review |
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