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The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock

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Harvard

Mendez-Barbero, N, Yuste-Montalvo, A, Nuñez-Borque, E, Jensen, BM, Gutiérrez-Muñoz, C, Tome-Amat, J, Garrido-Arandia, M, Díaz-Perales, A, Ballesteros-Martinez, C, Laguna, JJ, Beitia, JM, Poulsen, LK, Cuesta-Herranz, J, Blanco-Colio, LM & Esteban, V 2020, 'The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock', The Journal of allergy and clinical immunology, vol. 145, no. 2, pp. 583-596.e6. https://doi.org/10.1016/j.jaci.2019.09.019

APA

Mendez-Barbero, N., Yuste-Montalvo, A., Nuñez-Borque, E., Jensen, B. M., Gutiérrez-Muñoz, C., Tome-Amat, J., Garrido-Arandia, M., Díaz-Perales, A., Ballesteros-Martinez, C., Laguna, J. J., Beitia, J. M., Poulsen, L. K., Cuesta-Herranz, J., Blanco-Colio, L. M., & Esteban, V. (2020). The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock. The Journal of allergy and clinical immunology, 145(2), 583-596.e6. https://doi.org/10.1016/j.jaci.2019.09.019

CBE

Mendez-Barbero N, Yuste-Montalvo A, Nuñez-Borque E, Jensen BM, Gutiérrez-Muñoz C, Tome-Amat J, Garrido-Arandia M, Díaz-Perales A, Ballesteros-Martinez C, Laguna JJ, Beitia JM, Poulsen LK, Cuesta-Herranz J, Blanco-Colio LM, Esteban V. 2020. The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock. The Journal of allergy and clinical immunology. 145(2):583-596.e6. https://doi.org/10.1016/j.jaci.2019.09.019

MLA

Vancouver

Author

Mendez-Barbero, Nerea ; Yuste-Montalvo, Alma ; Nuñez-Borque, Emilio ; Jensen, Bettina M ; Gutiérrez-Muñoz, Carmen ; Tome-Amat, Jaime ; Garrido-Arandia, María ; Díaz-Perales, Araceli ; Ballesteros-Martinez, Contanza ; Laguna, Jose Julio ; Beitia, J M ; Poulsen, Lars K ; Cuesta-Herranz, Javier ; Blanco-Colio, Luis Miguel ; Esteban, Vanesa. / The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock. In: The Journal of allergy and clinical immunology. 2020 ; Vol. 145, No. 2. pp. 583-596.e6.

Bibtex

@article{ee72ccd6c1e5400aa3ade41824c750c1,
title = "The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock",
abstract = "BACKGROUND: Anaphylaxis includes mast cell (MC) activation, but less is known about downstream mechanisms (ie, vascular permeability controlled by endothelial cells [ECs]). The TNF-like weak inducer of apoptosis (TWEAK) and its sole receptor, fibroblast growth factor-inducible molecule 14 (Fn14), belong to the TNF superfamily and are involved in proinflammatory responses.OBJECTIVE: We sought to investigate the role of TWEAK/Fn14 axis in anaphylaxis.METHODS: In vivo vascular permeability and mouse models of passive systemic anaphylaxis (PSA) and active systemic anaphylaxis were applied to wild-type (WT), TWEAK- and Fn14-deficient mice (TWEAK-/- and Fn14-/-, respectively). Primary bone marrow-derived mast cells (BMMCs) and ECs from WT and Fn14-/- or TWEAK-/- mice were studied. The TWEAK/Fn14 axis was also investigated in human samples.RESULTS: Mice with PSA and active systemic anaphylaxis had increased Fn14 and TWEAK expression in lung tissues and increased serum soluble TWEAK concentrations. TWEAK and Fn14 deficiencies prevent PSA-related symptoms, resulting in resistance to decreased body temperature, less severe reactions, and maintained physical activity. Numbers of MCs after PSA are similar between genotypes in different tissue regions, such as ear skin and the trachea, tongue, peritoneum, lungs, and bone marrow. Moreover, in vitro studies revealed no differences in degranulation or mediator release between WT and Fn14-/- BMMCs after IgE-FcεRI stimulation. In vivo and in vitro histamine and platelet-activating factor administration increases Fn14 receptor expression in lungs and ECs. Moreover, Fn14 deficiency in ECs maintained in vitro impermeability when stimulated by mediators or activated BMMCs but not by TWEAK-/- BMMCs, indicating that Fn14 is crucial for endothelial barrier function. TWEAK/Fn14 deletion or TWEAK-blocking antibody prevented histamine/platelet-activating factor-induced vascular subcutaneous permeability. Circulating soluble TWEAK levels were increased in patients with anaphylaxis, and plasma from those patients increased Fn14 expression in ECs.CONCLUSION: The TWEAK/Fn14 axis participates in anaphylactic reactions. Inhibition of TWEAK/Fn14 interaction could be efficacious in anaphylaxis therapy.",
keywords = "Anaphylaxis/immunology, Animals, Capillary Permeability/physiology, Cytokine TWEAK/immunology, Endothelial Cells/metabolism, Histamine/immunology, Mice, Mice, Knockout, Platelet Activating Factor/immunology, TWEAK Receptor/immunology, endothelial cells, TNF-like weak inducer of apoptosis/fibroblast growth factor–inducible molecule 14 axis, mast cells, Anaphylaxis, vascular permeability",
author = "Nerea Mendez-Barbero and Alma Yuste-Montalvo and Emilio Nu{\~n}ez-Borque and Jensen, {Bettina M} and Carmen Guti{\'e}rrez-Mu{\~n}oz and Jaime Tome-Amat and Mar{\'i}a Garrido-Arandia and Araceli D{\'i}az-Perales and Contanza Ballesteros-Martinez and Laguna, {Jose Julio} and Beitia, {J M} and Poulsen, {Lars K} and Javier Cuesta-Herranz and Blanco-Colio, {Luis Miguel} and Vanesa Esteban",
note = "Copyright {\textcopyright} 2019 The Authors. Published by Elsevier Inc. All rights reserved.",
year = "2020",
month = feb,
doi = "10.1016/j.jaci.2019.09.019",
language = "English",
volume = "145",
pages = "583--596.e6",
journal = "The Journal of allergy and clinical immunology",
issn = "0091-6749",
publisher = "Mosby, Inc",
number = "2",

}

RIS

TY - JOUR

T1 - The TNF-like weak inducer of the apoptosis/fibroblast growth factor-inducible molecule 14 axis mediates histamine and platelet-activating factor-induced subcutaneous vascular leakage and anaphylactic shock

AU - Mendez-Barbero, Nerea

AU - Yuste-Montalvo, Alma

AU - Nuñez-Borque, Emilio

AU - Jensen, Bettina M

AU - Gutiérrez-Muñoz, Carmen

AU - Tome-Amat, Jaime

AU - Garrido-Arandia, María

AU - Díaz-Perales, Araceli

AU - Ballesteros-Martinez, Contanza

AU - Laguna, Jose Julio

AU - Beitia, J M

AU - Poulsen, Lars K

AU - Cuesta-Herranz, Javier

AU - Blanco-Colio, Luis Miguel

AU - Esteban, Vanesa

N1 - Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

PY - 2020/2

Y1 - 2020/2

N2 - BACKGROUND: Anaphylaxis includes mast cell (MC) activation, but less is known about downstream mechanisms (ie, vascular permeability controlled by endothelial cells [ECs]). The TNF-like weak inducer of apoptosis (TWEAK) and its sole receptor, fibroblast growth factor-inducible molecule 14 (Fn14), belong to the TNF superfamily and are involved in proinflammatory responses.OBJECTIVE: We sought to investigate the role of TWEAK/Fn14 axis in anaphylaxis.METHODS: In vivo vascular permeability and mouse models of passive systemic anaphylaxis (PSA) and active systemic anaphylaxis were applied to wild-type (WT), TWEAK- and Fn14-deficient mice (TWEAK-/- and Fn14-/-, respectively). Primary bone marrow-derived mast cells (BMMCs) and ECs from WT and Fn14-/- or TWEAK-/- mice were studied. The TWEAK/Fn14 axis was also investigated in human samples.RESULTS: Mice with PSA and active systemic anaphylaxis had increased Fn14 and TWEAK expression in lung tissues and increased serum soluble TWEAK concentrations. TWEAK and Fn14 deficiencies prevent PSA-related symptoms, resulting in resistance to decreased body temperature, less severe reactions, and maintained physical activity. Numbers of MCs after PSA are similar between genotypes in different tissue regions, such as ear skin and the trachea, tongue, peritoneum, lungs, and bone marrow. Moreover, in vitro studies revealed no differences in degranulation or mediator release between WT and Fn14-/- BMMCs after IgE-FcεRI stimulation. In vivo and in vitro histamine and platelet-activating factor administration increases Fn14 receptor expression in lungs and ECs. Moreover, Fn14 deficiency in ECs maintained in vitro impermeability when stimulated by mediators or activated BMMCs but not by TWEAK-/- BMMCs, indicating that Fn14 is crucial for endothelial barrier function. TWEAK/Fn14 deletion or TWEAK-blocking antibody prevented histamine/platelet-activating factor-induced vascular subcutaneous permeability. Circulating soluble TWEAK levels were increased in patients with anaphylaxis, and plasma from those patients increased Fn14 expression in ECs.CONCLUSION: The TWEAK/Fn14 axis participates in anaphylactic reactions. Inhibition of TWEAK/Fn14 interaction could be efficacious in anaphylaxis therapy.

AB - BACKGROUND: Anaphylaxis includes mast cell (MC) activation, but less is known about downstream mechanisms (ie, vascular permeability controlled by endothelial cells [ECs]). The TNF-like weak inducer of apoptosis (TWEAK) and its sole receptor, fibroblast growth factor-inducible molecule 14 (Fn14), belong to the TNF superfamily and are involved in proinflammatory responses.OBJECTIVE: We sought to investigate the role of TWEAK/Fn14 axis in anaphylaxis.METHODS: In vivo vascular permeability and mouse models of passive systemic anaphylaxis (PSA) and active systemic anaphylaxis were applied to wild-type (WT), TWEAK- and Fn14-deficient mice (TWEAK-/- and Fn14-/-, respectively). Primary bone marrow-derived mast cells (BMMCs) and ECs from WT and Fn14-/- or TWEAK-/- mice were studied. The TWEAK/Fn14 axis was also investigated in human samples.RESULTS: Mice with PSA and active systemic anaphylaxis had increased Fn14 and TWEAK expression in lung tissues and increased serum soluble TWEAK concentrations. TWEAK and Fn14 deficiencies prevent PSA-related symptoms, resulting in resistance to decreased body temperature, less severe reactions, and maintained physical activity. Numbers of MCs after PSA are similar between genotypes in different tissue regions, such as ear skin and the trachea, tongue, peritoneum, lungs, and bone marrow. Moreover, in vitro studies revealed no differences in degranulation or mediator release between WT and Fn14-/- BMMCs after IgE-FcεRI stimulation. In vivo and in vitro histamine and platelet-activating factor administration increases Fn14 receptor expression in lungs and ECs. Moreover, Fn14 deficiency in ECs maintained in vitro impermeability when stimulated by mediators or activated BMMCs but not by TWEAK-/- BMMCs, indicating that Fn14 is crucial for endothelial barrier function. TWEAK/Fn14 deletion or TWEAK-blocking antibody prevented histamine/platelet-activating factor-induced vascular subcutaneous permeability. Circulating soluble TWEAK levels were increased in patients with anaphylaxis, and plasma from those patients increased Fn14 expression in ECs.CONCLUSION: The TWEAK/Fn14 axis participates in anaphylactic reactions. Inhibition of TWEAK/Fn14 interaction could be efficacious in anaphylaxis therapy.

KW - Anaphylaxis/immunology

KW - Animals

KW - Capillary Permeability/physiology

KW - Cytokine TWEAK/immunology

KW - Endothelial Cells/metabolism

KW - Histamine/immunology

KW - Mice

KW - Mice, Knockout

KW - Platelet Activating Factor/immunology

KW - TWEAK Receptor/immunology

KW - endothelial cells

KW - TNF-like weak inducer of apoptosis/fibroblast growth factor–inducible molecule 14 axis

KW - mast cells

KW - Anaphylaxis

KW - vascular permeability

UR - http://www.scopus.com/inward/record.url?scp=85074166773&partnerID=8YFLogxK

U2 - 10.1016/j.jaci.2019.09.019

DO - 10.1016/j.jaci.2019.09.019

M3 - Journal article

C2 - 31679818

VL - 145

SP - 583-596.e6

JO - The Journal of allergy and clinical immunology

JF - The Journal of allergy and clinical immunology

SN - 0091-6749

IS - 2

ER -

ID: 61785305