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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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Research works printed but not linked: 67

  1. Bischoff, 2016, Mast cells in gastrointestinal disorders, Eur. J. Pharmacol, 778, 139, 10.1016/j.ejphar.2016.02.018 · DOI
  2. Boeckxstaens, 2017, Neuroimmune factors in functional gastrointestinal disorders: a focus on irritable bowel syndrome, Neurogastroenterol. Motil, 29, e13007, 10.1111/nmo.13007 · DOI
  3. Heffner, 2014, Stress and anxiety effects on positive skin test responses in young adults with allergic rhinitis, Ann. Allergy Asthma Immunol, 113, 13, 10.1016/j.anai.2014.03.008 · DOI
  4. Andrae, 2013, Evaluation of the irritable bowel syndrome quality of life (IBS-QOL) questionnaire in diarrhea-predominant irritable bowel syndrome patients, Health Qual Life Outcomes, 11, 208, 10.1186/1477-7525-11-208 · DOI
  5. Priftis, 2009, Dysregulation of the stress response in asthmatic children, Allergy, 64, 18, 10.1111/j.1398-9995.2008.01948.x · DOI
  6. Santos, 2000, Chronic stress impairs rat growth and jejunal epithelial barrier function: role of mast cells, Am. J. Physiol. Gastrointest. Liver Physiol, 278, G847, 10.1152/ajpgi.2000.278.6.G847 · DOI
  7. SÖderholm, 2002, Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine, Gastroenterology, 123, 1099, 10.1053/gast.2002.36019 · DOI · Paper page
  8. Wallon, 2008, Corticotropin-releasing hormone (CRH) regulates macromolecular permeability via mast cells in normal human colonic biopsies in vitro, Gut, 57, 50, 10.1136/gut.2006.117549 · DOI
  9. Santos, 1999, Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat, Am. J. Physiol, 277, G391
  10. Lennon, 2013, Early life stress triggers persistent colonic barrier dysfunction and exacerbates colitis in adult IL-10-/- mice, Inflamm. Bowel Dis, 19, 712, 10.1097/MIB.0b013e3182802a4e · DOI
  11. Moeser, 2007, Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs, Am. J. Physiol. Gastrointest. Liver Physiol, 293, G413, 10.1152/ajpgi.00304.2006 · DOI
  12. Bale, 2004, CRF and CRF receptors: role in stress responsivity and other behaviors, Annu. Rev. Pharmacol. Toxicol, 44, 525, 10.1146/annurev.pharmtox.44.101802.121410 · DOI · Paper page
  13. Coin, 2013, Genetically encoded chemical probes in cells reveal the binding path of urocortin-I to CRF class B GPCR, Cell, 155, 1258, 10.1016/j.cell.2013.11.008 · DOI
  14. la Fleur, 2005, Role of peripheral corticotropin-releasing factor and urocortin II in intestinal inflammation and motility in terminal ileum, Proc. Natl. Acad. Sci. USA, 102, 7647, 10.1073/pnas.0408531102 · DOI
  15. Liu, 2014, The role of corticotropin-releasing hormone receptor 1 in the development of colitis-associated cancer in mouse model, Endocr. Relat. Cancer, 21, 639, 10.1530/ERC-14-0239 · DOI
  16. Boyer, 2015, Early-life dietary spray-dried plasma influences immunological and intestinal injury responses to later-life Salmonella Typhimurium challenge, Br. J. Nutr, 113, 783, 10.1017/S000711451400422X · DOI
  17. Mahajan, 2014, Urocortin 3 expression at baseline and during inflammation in the colon: corticotropin releasing factor receptors cross-talk, Peptides, 54, 58, 10.1016/j.peptides.2014.01.007 · DOI
  18. Taché, 2009, A role for corticotropin-releasing factor in functional gastrointestinal disorders, Curr. Gastroenterol. Rep, 11, 270, 10.1007/s11894-009-0040-4 · DOI
  19. Asadi, 2012, Substance P (SP) induces expression of functional corticotropin-releasing hormone receptor-1 (CRHR-1) in human mast cells, J. Invest. Dermatol, 132, 324, 10.1038/jid.2011.334 · DOI
  20. Cao, 2006, Corticotropin-releasing hormone induces vascular endothelial growth factor release from human mast cells via the cAMP/protein kinase A/p38 mitogen-activated protein kinase pathway, Mol. Pharmacol, 69, 998, 10.1124/mol.105.019539 · DOI
  21. Papadopoulou, 2005, Regulation of corticotropin-releasing hormone receptor-2 expression in human cord blood-derived cultured mast cells, J. Mol. Endocrinol, 35, R1, 10.1677/jme.1.01833 · DOI · Paper page
  22. Cao, 2005, Human mast cells express corticotropin-releasing hormone (CRH) receptors and CRH leads to selective secretion of vascular endothelial growth factor, J. Immunol, 174, 7665, 10.4049/jimmunol.174.12.7665 · DOI · Paper page
  23. Smith, 1998, Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development, Neuron, 20, 1093, 10.1016/S0896-6273(00)80491-2 · DOI · Paper page
  24. Sun, 2007, Impact of CD40 ligand, B cells, and mast cells in peanut-induced anaphylactic responses, J. Immunol, 179, 6696, 10.4049/jimmunol.179.10.6696 · DOI
  25. Smith, 2010, Early weaning stress impairs development of mucosal barrier function in the porcine intestine, Am. J. Physiol. Gastrointest. Liver Physiol, 298, G352, 10.1152/ajpgi.00081.2009 · DOI
  26. Medland, 2016, Early life adversity in piglets induces long-term upregulation of the enteric cholinergic nervous system and heightened, sex-specific secretomotor neuron responses, Neurogastroenterol. Motil, 28, 1317, 10.1111/nmo.12828 · DOI
  27. Gourcerol, 2011, Activation of corticotropin-releasing factor receptor 2 mediates the colonic motor coping response to acute stress in rodents, Gastroenterology, 140, 1586, 10.1053/j.gastro.2011.01.039 · DOI
  28. Tao, 2009, Activation of corticotropin-releasing factor 2 receptor inhibits Purkinje neuron P-type calcium currents via Goα-dependent PKC epsilon pathway, Cell. Signal, 21, 1436, 10.1016/j.cellsig.2009.05.002 · DOI
  29. Yuan, 2012, Expression of corticotropin releasing factor receptor type 1 (CRF1) in the human gastrointestinal tract and upregulation in the colonic mucosa in patients with ulcerative colitis, Peptides, 38, 62, 10.1016/j.peptides.2012.07.028 · DOI
  30. Cyphert, 2011, Unique populations of lung mast cells are required for antigen-mediated bronchoconstriction, Clin. Exp. Allergy, 41, 260, 10.1111/j.1365-2222.2010.03583.x · DOI
  31. Yu, 2006, Mast cells can promote the development of multiple features of chronic asthma in mice, J. Clin. Invest, 116, 1633, 10.1172/JCI25702 · DOI
  32. Rivier, 2007, Stressin1-A, a potent corticotropin releasing factor receptor 1 (CRF1)-selective peptide agonist, J. Med. Chem, 50, 1668, 10.1021/jm0613875 · DOI
  33. Dautzenberg, 2001, Molecular biology of the CRH receptors– in the mood, Peptides, 22, 753, 10.1016/S0196-9781(01)00388-6 · DOI
  34. Hauger, 2006, Corticotropin releasing factor (CRF) receptor signaling in the central nervous system: new molecular targets, CNS Neurol. Disord. Drug Targets, 5, 453, 10.2174/187152706777950684 · DOI
  35. Balseiro-Gomez, 2015, Identification of a new exo-endocytic mechanism triggered by corticotropin-releasing hormone in mast cells, J. Immunol, 195, 2046, 10.4049/jimmunol.1500253 · DOI
  36. Wallon, 2009, Corticotropin-releasing hormone and mast cells in the regulation of mucosal barrier function in the human colon, Ann. N. Y. Acad. Sci, 1165, 206, 10.1111/j.1749-6632.2009.04030.x · DOI
  37. McNeil, 2015, Identification of a mast-cell-specific receptor crucial for pseudo-allergic drug reactions, Nature, 519, 237, 10.1038/nature14022 · DOI · Paper page
  38. Slominski, 2006, CRH functions as a growth factor/cytokine in the skin, J. Cell. Physiol, 206, 780, 10.1002/jcp.20530 · DOI
  39. Lakshmanan, 2008, Localization and gestation-dependent pattern of corticotrophin-releasing factor receptor subtypes in ovine fetal distal colon, Neurogastroenterol. Motil, 20, 1328, 10.1111/j.1365-2982.2008.01209.x · DOI
  40. O'Malley, 2010, Alterations in colonic corticotropin-releasing factor receptors in the maternally separated rat model of irritable bowel syndrome: differential effects of acute psychological and physical stressors, Peptides, 31, 662, 10.1016/j.peptides.2010.01.004 · DOI
  41. Groschwitz, 2009, Mast cells regulate homeostatic intestinal epithelial migration and barrier function by a chymase/Mcpt4-dependent mechanism, Proc. Natl. Acad. Sci. USA, 106, 22381, 10.1073/pnas.0906372106 · DOI
  42. Camilleri, 2012, Irritable bowel syndrome: methods, mechanisms, and pathophysiology. The confluence of increased permeability, inflammation, and pain in irritable bowel syndrome, Am. J. Physiol. Gastrointest. Liver Physiol, 303, G775, 10.1152/ajpgi.00155.2012 · DOI
  43. Issenman, 1993, Intestinal permeability compared in pediatric and adult patients with inflammatory bowel disease, Clin. Invest. Med, 16, 187
  44. Holowka, 2016, Roles for Ca2+ mobilization and its regulation in mast cell functions: recent progress, Biochem. Soc. Trans, 44, 505, 10.1042/BST20150273 · DOI
  45. Abraham, 2010, Mast cell-orchestrated immunity to pathogens, Nat. Rev. Immunol, 10, 440, 10.1038/nri2782 · DOI · Paper page
  46. Balseiro-Gomez, 2016, Transient fusion ensures granule replenishment to enable repeated release after IgE-mediated mast cell degranulation, J. Cell Sci, 129, 3989, 10.1242/jcs.194340 · DOI
  47. Suzuki, 2010, Loss of TRPC1-mediated Ca2+ influx contributes to impaired degranulation in Fyn-deficient mouse bone marrow-derived mast cells, J. Leukoc. Biol, 88, 863, 10.1189/jlb.0510253 · DOI
  48. Dedkova, 2000, Mechanism of action of calcium ionophores on intact cells: ionophore-resistant cells, Membr. Cell Biol, 13, 357
  49. Kim, 2014, Emodin attenuates A23187-induced mast cell degranulation and tumor necrosis factor-α secretion through protein kinase C and IκB kinase 2 signaling, Eur. J. Pharmacol, 723, 501, 10.1016/j.ejphar.2013.09.066 · DOI
  50. Dautzenberg, 2016, Corticotropin-releasing factor receptors: CRF1 receptor—IUPHAR/BPS guide to pharmacology
  51. Dautzenberg, 2016, Corticotropin-releasing factor receptors: CRF2 receptor. IUPHAR/BPS guide to pharmacology. Available at: www.guidetopharmacology.org/GRAC/ObjectDisplayForward?objectId=213, Accessed September, 19, 2016
  52. Punn, 2012, Mapping structural determinants within third intracellular loop that direct signaling specificity of type 1 corticotropin-releasing hormone receptor, J. Biol. Chem, 287, 8974, 10.1074/jbc.M111.272161 · DOI
  53. Brailoiu, 2012, Urocortin 3 elevates cytosolic calcium in nucleus ambiguus neurons, J. Neurochem, 122, 1129, 10.1111/j.1471-4159.2012.07869.x · DOI
  54. Makarewich, 2015, Comparative effects of urocortins and stresscopin on cardiac myocyte contractility, J. Mol. Cell. Cardiol, 86, 179, 10.1016/j.yjmcc.2015.07.023 · DOI
  55. Walther, 2015, PDZK1/ NHERF3 differentially regulates corticotropin-releasing factor receptor 1 and serotonin 2A receptor signaling and endocytosis, Cell. Signal, 27, 519, 10.1016/j.cellsig.2014.12.019 · DOI
  56. Gilfillan, 2009, Amplification mechanisms for the enhancement of antigen-mediated mast cell activation, Immunol. Res, 43, 15, 10.1007/s12026-008-8046-9 · DOI
  57. Kuehn, 2007, G protein-coupled receptors and the modification of FcɛRI-mediated mast cell activation, Immunol. Lett, 113, 59, 10.1016/j.imlet.2007.08.007 · DOI
  58. Feng, 2006, Human mast cells express multiple EP receptors for prostaglandin E2 that differentially modulate activation responses, Blood, 107, 3243, 10.1182/blood-2005-07-2772 · DOI
  59. Kay, 2006, Prostaglandin E2 activates EP2 receptors to inhibit human lung mast cell degranulation, Br. J. Pharmacol, 147, 707, 10.1038/sj.bjp.0706664 · DOI
  60. Kuehn, 2008, Synergistic activation of phospholipases CΓ and Cß: a novel mechanism for PI3K-independent enhancement of FcɛRI-induced mast cell mediator release, Cell. Signal, 20, 625, 10.1016/j.cellsig.2007.11.016 · DOI
  61. Serra-Pages, 2012, E-prostanoid 2 receptors dampen mast cell degranulation via cAMP/PKA-mediated suppression of IgE-dependent signaling, J. Leukoc. Biol, 92, 1155, 10.1189/jlb.0212109 · DOI
  62. Wang, 2006, Prostaglandin E potentiates the immunologically stimulated histamine release from human peripheral blood-derived mast cells through EP1/EP3 receptors, Allergy, 61, 503, 10.1111/j.1398-9995.2006.01043.x · DOI
  63. Nguyen, 2002, Receptors and signaling mechanisms required for prostaglandin E2-mediated regulation of mast cell degranulation and IL-6 production, J. Immunol, 169, 4586, 10.4049/jimmunol.169.8.4586 · DOI
  64. Choi, 2015, Mast cell mediator responses and their suppression by pathogenic and commensal microorganisms, Mol. Immunol, 63, 74, 10.1016/j.molimm.2014.02.006 · DOI
  65. Choi, 2016, Loss of bladder epithelium induced by cytolytic mast cell granules, Immunity, 45, 1258, 10.1016/j.immuni.2016.11.003 · DOI
  66. McGowen, 2009, The mast cell activator compound 48/80 is safe and effective when used as an adjuvant for intradermal immunization with Bacillus anthracis protective antigen, Vaccine, 27, 3544, 10.1016/j.vaccine.2009.03.069 · DOI
  67. McLachlan, 2008, Mast cell activators: a new class of highly effective vaccine adjuvants, Nat. Med, 14, 536, 10.1038/nm1757 · DOI

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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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