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Frontline science: Corticotropin‐releasing factor receptor subtype 1 is a critical modulator of mast cell degranulation and stress‐induced pathophysiology

Ayyadurai, Saravanan, Gibson, Amelia J, D'Costa, Susan, Overman, Elizabeth L, Sommerville, Laura J, Poopal, Ashwini C, Mackey, Emily, Li, Yihang, Moeser, Adam J·2017·Journal of Leukocyte Biology
DOI 10.1189/jlb.2hi0317-088rr
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Abstract

Life stress is a major risk factor in the onset and exacerbation of mast cell–associated diseases, including allergy/anaphylaxis, asthma, and irritable bowel syndrome. Although it is known that mast cells are highly activated upon stressful events, the mechanisms by which stress modulates mast cell function and disease pathophysiology remains poorly understood. Here, we investigated the role of corticotropin-releasing factor receptor subtype 1 (CRF1) in mast cell degranulation and associated disease pathophysiology. In a mast cell–dependent model of IgE-mediated passive systemic anaphylaxis (PSA), prophylactic administration of the CRF1-antagonist antalarmin attenuated mast cell degranulation and hypothermia. Mast cell–deficient KitW-sh/W-sh mice engrafted with CRF1−/− bone marrow–derived mast cells (BMMCs) exhibited attenuated PSA-induced serum histamine, hypothermia, and clinical scores compared with wild-type BMMC-engrafted KitW-sh/W-sh mice. KitW-sh/W-sh mice engrafted with CRF1−/− BMMCs also exhibited suppressed in vivo mast cell degranulation and intestinal permeability in response to acute restraint stress. Genetic and pharmacologic experiments with murine BMMCs, rat RBL-2H3, and human LAD2 mast cells demonstrated that although CRF1 activation did not directly induce MC degranulation, CRF1 signaling potentiated the degranulation responses triggered by diverse mast cell stimuli and was associated with enhanced release of Ca2+ from intracellular stores. Taken together, our results revealed a prominent role for CRF1 signaling in mast cells as a positive modulator of stimuli-induced degranulation and in vivo pathophysiologic responses to immunologic and psychologic stress.

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Metadata

Authors
Ayyadurai, S., Gibson, A. J., D'Costa, S., Overman, E. L., Sommerville, L. J., Poopal, A. C., Mackey, E., Li, Y., & Moeser, A. J.
Affiliations
  • Gastrointestinal Stress Biology Laboratory, Department of Large Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University , East Lansing, Michigan, USA
  • KeraFast , Boston, Massachusetts, USA
  • Department of Medicine, University of North Carolina , Chapel Hill, North Carolina, USA
  • Department of Biology, Methodist University , Fayetteville, North Carolina, USA
  • Department of Pathology, Duke University, School of Medicine , Durham, North Carolina, USA
Venue
Journal of Leukocyte Biology
Publisher
Oxford University Press (OUP)
Published
2017-07-06
Volume
102
Issue
6
Pages
1299-1312
ISSN
  • 0741-5400
  • 1938-3673
DOI
10.1189/jlb.2hi0317-088rr
Cited by
52
References
6
Language
en
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Funders
U.S. National Institutes of Health (R01 HD072968, DK097462, R03 DK097462)

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