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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Veröffentlicht in:Antioxidants Jg. 13; H. 8; S. 920
Hauptverfasser: Piotin, Anays, Oulehri, Walid, Charles, Anne-Laure, Tacquard, Charles, Collange, Olivier, Mertes, Paul-Michel, Geny, Bernard
Format: Journal Article
Sprache:Englisch
Veröffentlicht: Switzerland MDPI AG 29.07.2024
MDPI
Schlagworte:
Allergens
Allergies
anaphylactic shock
Anaphylaxis
Antibiotics
Antigens
antioxidant
Antioxidants
Cardiomyocytes
Cell activation
Cell surface
Degranulation
Drug dosages
Epidemiology
Exocytosis
Health aspects
Immunoglobulin E
Immunoglobulins
Immunology
Life Sciences
Lipid metabolism
Lipid peroxidation
Mast cells
Medical research
Medicine, Experimental
Membrane potential
Metabolism
Mitochondria
Musculoskeletal system
NAD(P)H oxidase
NADP (coenzyme)
NADPH-diaphorase
Narcotics
Oxidants
Oxidative metabolism
Oxidative stress
oxidoreductases
Pathophysiology
Physiological aspects
Reactive oxygen species
reactive oxygen species (ROS)
Reviews
Systematic Review
Therapeutic applications
therapeutics
France
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
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.
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.)
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CitedBy_id crossref_primary_10_1007_s10787_025_01685_2
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crossref_primary_10_3390_microorganisms13081883
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Issue 8
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
Language English
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crossref_primary_10_3390_antiox13080920
PublicationCentury 2000
PublicationDate 20240729
PublicationDateYYYYMMDD 2024-07-29
PublicationDate_xml – month: 7
  year: 2024
  text: 20240729
  day: 29
PublicationDecade 2020
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
– name: Basel
PublicationTitle Antioxidants
PublicationTitleAlternate Antioxidants (Basel)
PublicationYear 2024
Publisher MDPI AG
MDPI
Publisher_xml – name: MDPI AG
– name: MDPI
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Snippet Anaphylaxis, an allergic reaction caused by the massive release of active mediators, can lead to anaphylactic shock (AS), the most severe and potentially...
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SubjectTerms Allergens
Allergies
anaphylactic shock
Anaphylaxis
Antibiotics
Antigens
antioxidant
Antioxidants
Cardiomyocytes
Cell activation
Cell surface
Degranulation
Drug dosages
Epidemiology
Exocytosis
Health aspects
Immunoglobulin E
Immunoglobulins
Immunology
Life Sciences
Lipid metabolism
Lipid peroxidation
Mast cells
Medical research
Medicine, Experimental
Membrane potential
Metabolism
Mitochondria
Musculoskeletal system
NAD(P)H oxidase
NADP (coenzyme)
NADPH-diaphorase
Narcotics
Oxidants
Oxidative metabolism
Oxidative stress
oxidoreductases
Pathophysiology
Physiological aspects
Reactive oxygen species
reactive oxygen species (ROS)
Reviews
Systematic Review
Therapeutic applications
therapeutics
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Title Oxidative Stress and Mitochondria Are Involved in Anaphylaxis and Mast Cell Degranulation: A Systematic Review
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