Mast cell activation is involved in stress-induced epithelial barrier dysfunction in the esophagus

Journal of Digestive Diseases

Volumn 16, Issue 4, 2015, Pages 186-196

  Zhong, Chan Juan ^a   Wang, Kun ^a   Zhang, Lu ^a   Yang, Chang Qing ^a   Zhang, Kuo ^b   Zhou, Shu Pei ^b   Duan, Li Ping ^a  

^a PEKING UNIVERSITY THIRD HOSPITAL   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Dilated intercellular space; Mast cell; Stress; Tight junction; Tryptase

Indexed keywords

ALCIAN BLUE; ANAPHASE PROMOTING COMPLEX SUBUNIT 4; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; PROTEINASE ACTIVATED RECEPTOR 2; TIGHT JUNCTION PROTEIN; TRYPTASE;

ACCESSORY CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL COUNTING; CELL PROLIFERATION; CHRONIC STRESS; CONTROLLED STUDY; ESOPHAGUS; ESOPHAGUS DISEASE; ESOPHAGUS MUCOSA; ESOPHAGUS STRESS INDUCED BARRIER DYSFUNCTION; IMMOBILIZATION STRESS; INTERCELLULAR SPACE; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CYTOLOGY; EPITHELIUM; IMMUNOLOGY; INTRACELLULAR SPACE; MENTAL STRESS; METABOLISM; MUTANT RAT STRAIN; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELL PROLIFERATION; EPITHELIUM; ESOPHAGUS; INTRACELLULAR SPACE; MAST CELLS; RATS; RATS, MUTANT STRAINS; RECEPTOR, PAR-2; STRESS, PSYCHOLOGICAL; TIGHT JUNCTION PROTEINS; TRYPTASES;

EID: 84928554141     PISSN: 17512972     EISSN: 17512980     Source Type: Journal    
DOI: 10.1111/1751-2980.12226     Document Type: Article

References (38)

1. Orlando LA, Orlando RC. Dilated intercellular spaces as a marker of GERD. Curr Gastroenterol Rep 2009; 11: 190-194.
2. Farré R, De Vos R, Geboes K etal. Critical role of stress in increased oesophageal mucosa permeability and dilated intercellular spaces. Gut 2007; 56: 1191-1197.
3. Santos J, Yang PC, Söderholm JD, Benjamin M, Perdue MH. Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat. Gut 2001; 48: 630-636.
4. Vicario M, Guilarte M, Alonso C etal. Chronological assessment of mast cell-mediated gut dysfunction and mucosal inflammation in a rat model of chronic psychosocial stress. Brain Behav Immun 2010; 24: 1166-1175.
5. Söderholm JD, Yang PC, Ceponis P etal. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in rat intestine. Gastroenterology 2002; 123: 1099-1108.
6. Santos J, Yates D, Guilarte M, Vicario M, Alonso C, Perdue MH. Stress neuropeptides evoke epithelial responses via mast cell activation in the rat colon. Psychoneuroendocrinology 2008; 33: 1248-1256.
7. Yu S, Kollarik M, Ouyang A, Myers AC, Undem BJ. Mast cell-mediated long-lasting increases in excitability of vagal C fibers in guinea pig esophagus. Am J Physiol Gastrointest Liver Physiol 2007; 293: G850-856.
8. Jacob C, Yang PC, Darmoul D etal. Mast cell tryptase controls paracellular permeability of the intestine. Role of protease-activated receptor 2 and β-arrestins. J Biol Chem 2005; 280: 31936-31948.
9. Caughey GH. Mast cell tryptases and chymases in inflammation and host defense. Immunol Rev 2007; 217: 141-154.
10. He S, Gaça MD, Walls AF. A role for tryptase in the activation of human mast cells: modulation of histamine release by tryptase and inhibitors of tryptase. J Pharmacol Exp Ther 1998; 286: 289-297.
11. Itoh Y, Sendo T, Oishi R. Physiology and pathophysiology of proteinase-activated receptors (PARs): role of tryptase/PAR-2 in vascular endothelial barrier function. J Pharmacol Sci 2005; 97: 14-19.
12. Liu H, Miller DV, Lourenssen S, Wells RW, Blennerhassett MG, Paterson WG. Proteinase-activated receptor-2 activation evokes oesophageal longitudinal smooth muscle contraction via a capsaicin-sensitive and neurokinin-2 receptor-dependent pathway. Neurogastroenterol Motil 2010; 22: 210-267.
13. Cenac N, Garcia-Villar R, Ferrier L etal. Proteinase-activated receptor-2-induced colonic inflammation in mice: possible involvement of afferent neurons, nitric oxide, and paracellular permeability. J Immunol 2003; 170: 4296-4300.
14. Cenac N, Coelho AM, Nguyen C etal. Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am J Pathol 2002; 161: 1903-1915.
15. 2 activation alters colonic paracellular permeability in mice via IFN-γ-dependent and -independent pathways. J Physiol 2004; 558: 913-925.
16. Kandulski A, Wex T, Mönkemüller K etal. Proteinase-activated receptor-2 in the pathogenesis of gastroesophageal reflux disease. Am J Gastroenterol 2010; 105: 1934-1943.
17. Teitelbaum AA, Gareau MG, Jury J, Yang PC, Perdue MH. Chronic peripheral administration of corticotropin-releasing factor causes colonic barrier dysfunction similar to psychological stress. Am J Physiol Gastrointest Liver Physiol 2008; 295: G452-459.
18. Larauche M. Novel insights in the role of peripheral corticotropin-releasing factor and mast cells in stress-induced visceral hypersensitivity. Neurogastroenterol Motil 2012; 24: 201-205.
19. Keita AV, Söderholm JD, Ericson AC. Stress-induced barrier disruption of rat follicle-associated epithelium involves corticotropin-releasing hormone, acetylcholine, substance P, and mast cells. Neurogastroenterol Motil 2010; 22: 770-e222.
20. Wallon C, Yang PC, Keita AV etal. Corticotropin-releasing hormone (CRH) regulates macromolecular permeability via mast cells in normal human colonic biopsies in vitro. Gut 2008; 57: 50-58.
21. Stengel A, Taché Y. Corticotropin-releasing factor signaling and visceral response to stress. Exp Biol Med (Maywood) 2010; 235: 1168-1178.
22. Smith F, Clark JE, Overman BL etal. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am J Physiol Gastrointest Liver Physiol 2009; 298: G352-363.
23. Barreau F, Cartier C, Leveque M etal. Pathways involved in gut mucosal barrier dysfunction induced in adult rats by maternal deprivation: corticotrophin-releasing factor and nerve growth factor interplay. J Physiol 2007; 580: 347-356.
24. Wu SV, Yuan PQ, Wang L, Peng YL, Chen CY, Taché Y. Identification and characterization of multiple corticotropin-releasing factor type 2 receptor isoforms in the rat esophagus. Endocrinology 2007; 148: 1675-1687.
25. Gué M, Del Rio-Lacheze RC, Eutamene H, Théodorou V, Fioramonti J, Buéno L. Stress-induced visceral hypersensitivity to rectal distension in rats: role of CRF and mast cells. Neurogastroenterol Motil 1997; 9: 271-279.
26. Farré R, van Malenstein H, De Vos R etal. Short exposure of oesophageal mucosa to bile acids, both in acidic and weakly acidic conditions, can impair mucosal integrity and provoke dilated intercellular spaces. Gut 2008; 57: 1366-1374.
27. Farré R, Blondeau K, Clement D etal. Evaluation of oesophageal mucosa integrity by the intraluminal impedance technique. Gut 2011; 60: 885-892.
28. Tobey NA, Hosseini SS, Argote CM, Dobrucali AM, Awayda MS, Orlando RC. Dilated intercellular spaces and shunt permeability in nonerosive acid-damaged esophageal epithelium. Am J Gastroenterol 2004; 99: 13-22.
29. Souza RF, Huo X, Mittal V etal. Gastroesophageal reflux might cause esophagitis through a cytokine-mediated mechanism rather than caustic acid injury. Gastroenterology 2009; 137: 1776-1784.
30. Van Itallie CM, Fanning AS, Holmes J, Anderson JM. Occludin is required for cytokine-induced regulation of tight junction barriers. J Cell Sci 2010; 123: 2844-2852.
31. Liu LB, Xue YX, Liu YH, Wang YB. Bradykinin increases blood-tumor barrier permeability by down-regulating the expression levels of ZO-1, occludin, and claudin-5 and rearranging actin cytoskeleton. J Neurosci Res 2008; 86: 1153-1168.
32. Van Itallie C, Rahner C, Anderson JM. Regulated expression of claudin-4 decreases paracellular conductance through a selective decrease in sodium permeability. J Clin Invest 2001; 107: 1319-1327.
33. Wada M, Tamura A, Takahashi N, Tsukita S. Loss of claudins 2 and 15 from mice causes defects in paracellular Na+ flow and nutrient transport in gut and leads to death from malnutrition. Gastroenterology 2013; 144: 369-380.
34. Chen X, Oshima T, Shan J, Fukui H, Watari J, Miwa H. Bile salts disrupt human esophageal squamous epithelial barrier function by modulating tight junction proteins. Am J Physiol Gastrointest Liver Physiol 2012; 303: G199-208.
35. Oguro M, Koike M, Ueno T etal. Dissociation and dispersion of claudin-3 from the tight junction could be one of the most sensitive indicators of reflux esophagitis in a rat model of the disease. J Gastroenterol 2011; 46: 629-638.
36. Compton SJ, Cairns JA, Holgate ST, Walls AF. The role of mast cell tryptase in regulating endothelial cell proliferation, cytokine release, and adhesion molecule expression: tryptase induces expression of mRNA for IL-1 beta and IL-8 and stimulates the selective release of IL-8 from human umbilical vein endothelial cells. J Immunol 1998; 161: 1939-1946.
37. Yoshida N, Katada K, Handa O etal. Interleukin-8 production via protease-activated receptor 2 in human esophageal epithelial cells. Int J Mol Med 2007; 19: 335-340.
38. Yoshida N, Uchiyama K, Kuroda M etal. Interleukin-8 expression in the esophageal mucosa of patients with gastroesophageal reflux disease. Scand J Gastroenterol 2004; 39: 816-822.