Review article: Mechanisms of initiation and perpetuation of gut inflammation by stress

Alimentary Pharmacology and Therapeutics

Volumn 16, Issue 12, 2002, Pages 2017-2028

  Hart, A ^a   Kamm, M A ^a  

^a ST MARK S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; DEXAMETHASONE; GLUCOCORTICOID RECEPTOR; MUCIN; NEUROKININ 1 RECEPTOR ANTAGONIST; NEUROTENSIN; NOLPITANTIUM; STEROID; SUBSTANCE P; TRINITROBENZENESULFONIC ACID;

ADRENERGIC SYSTEM; AUTONOMIC NERVOUS SYSTEM; CHOLINERGIC SYSTEM; COLON MUCOSA; CORTICOSTEROID THERAPY; CORTICOTROPIN RELEASE; CROHN DISEASE; ENTERITIS; HISTOLOGY; HUMAN; INFLAMMATION; INFLAMMATORY DISEASE; INTESTINE MUCOSA PERMEABILITY; MAST CELL; NEUROENDOCRINOLOGY; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; STRESS; T LYMPHOCYTE; ULCERATIVE COLITIS;

ANIMALS; HUMANS; IMMUNITY, MUCOSAL; INFLAMMATORY BOWEL DISEASES; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; NEUROSECRETORY SYSTEMS; PERMEABILITY; STRESS, PSYCHOLOGICAL;

EID: 0036909243     PISSN: 02692813     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2036.2002.01359.x     Document Type: Review

References (125)

1. Mitchell CM, Drossman DA, Survey of the AGA membership relating to patients with functional gastrointestinal disorders. Gastroenterology 1987; 92(5 Part 1): 1282-4.
2. National Foundation for Ileitis and Colitis. Challenges in 17BD Research. Agenda for the '90s. Washington DC: National foundation for Ileitis and Colitis, 1990.
3. Robertson DA, Ray J, Diamond I, et al. Personality profile and affective state of patients with inflammatory bowel disease. Gut 1989; 30(5): 623-6.
4. Theis MK, Boyko EJ. Patient perceptions of causes of inflammatory bowel disease [letter]. Am J Gastroenterol 1994; 89(10): 1920.
5. Murray JB. New trends in psychosomatic research. Genet Psychol Monogr 1977: 96: 3-74.
6. Engel GL, Salzman LF. A double standard for psychosomatic papers? N Engl J Med 1973; 288(1): 44-6.
7. Engel GL. Psychological factors in ulcerative colitis in man and gibbon. Gastroenterology 1969; 57(3): 362-5.
8. Alexander T. An objective study of psychological factors in ulcerative colitis in children. Appl Ther 1965; 7(10): 837-9.
9. Salem SN, Shubair KS. Non-specific ulcerative colitis in Bedouin Arabs. Lancet 1967; 1(7488): 473-5.
10. Helzer JE, Stillings WA, Chammas S, et al. A controlled study of the association between ulcerative colitis and psychiatric diagnoses. Dig Dis Sci 1982; 27(6): 513-8.
11. Helzer JE, Chammas S, Norland CC, et al. A study of the association between Crohn's disease and psychiatric illness. Gastroenterology 1984; 86(2): 324-30.
12. Fava GA, Pavan L. Large bowel disorders. I. Illness configuration and life events. Psychother Psychosom 1976; 27(2): 93-9.
13. Feldman F, Cantor D, Soll S, et al. Psychiatric study of a consecutive series of 34 patients with ulcerative colitis. BMJ 1967; 3(556): 14-7.
14. Hislop IG. Onset setting in inflammatory bowel disease. Med J Aust 1974; 1(25): 981-4.
15. Mendeloff AI, Monk M, Siegel CI, Lilienfeld A. Illness experience and life stresses in patients with irritable colon and with ulcerative colitis. An epidemiologic study of ulcerative colitis and regional enteritis in Baltimore. 1960-64. N Eng. J Med 1970; 282(1): 14-7.
16. Riley SA, Mani V, Goodman MJ, et al. Why do patients with ulcerative colitis relapse? Gut 1990; 31(2): 179-83.
17. von Wietersheim J, Kohler T, Feiereis H. Relapse-precipitating life events and feelings in patients with inflammatory bowel disease. Psychother Psychosom 1992; 58(2): 103-12.
18. Duffy LC, Zielezny MA, Marshall JR, et al. Lag time between stress events and risk of recurrent episodes of inflammatory bowel disease. Epidemiology 1991; 2(2): 141-5.
19. Duffy LC, Zielezny MA, Marshall JR, et al. Relevance of major stress events as an indicator of disease activity prevalence in inflammatory bowel disease. Behav Med 1991; 17(3): 101-10.
20. Porcelli P, Zaka S, Centonze S, et al. Psychological distress and levels of disease activity in inflammatory bowel disease. Ital J Gastroenterol 1994; 26(3): 111-5.
21. Greene BR, Blanchard EB, Wan CK. Long-term monitoring of psychosocial stress and symptomatology in inflammatory bowel disease. Behav Res Ther 1994; 32(2): 217-26.
22. Levenstein S, Prantera C, Varvo V, et al. Psychological stress and disease activity in ulcerative colitis: A multidimensional cross-sectional study [see comments]. Am J Gastroenterol 1994; 89(8): 1219-25.
23. Guyatt G, Mitchell A, Irvine EJ, et al. A new measure of health status for clinical trials in inflammatory bowel disease. Gastroenterology 1989; 96(3): 804-10.
24. Irvine EJ, Feagan B, Rochon J, et al. Quality of life: A valid and reliable measure of therapeutic efficacy in the treatment of inflammatory bowel disease. Canadian Crohn's Relapse Prevention Trial Study Group. Gastroenterology 1994; 106(2): 287-96.
25. Turnbull GK, Vallis TM. Quality of life in inflammatory bowel disease: The interaction of disease activity with psychosocial function. Am J Gastroenterol 1995; 90(9): 1450-4.
26. Levenstein S, Prantera C, Varvo V, et al. Stress and exacerbation in ulcerative colitis: A prospective study of patients enrolled in remission. Am J Gastroenterol 2000; 95(5): 1213-20.
27. North CS, Alpers DH, Helzer JE, et al. Do life events or depression exacerbate inflammatory bowel disease? A prospective study. Ann Intern Med 1991; 114(5): 381-6.
28. Talal AH, Drossman DA. Psychosocial factors in inflammatory bowel disease. Gastroenterol Clin North Am 1995; 24(3): 699-716.
29. Grace WJ, Pinsky RH, Wolff HG. The treatment of ulcerative colitis. II. Gastroenterology 1951; 26: 462-8.
30. Karush A, Daniels GE, O'Connor JF, et al. The response to psychotherapy in chronic ulcerative colitis. I. Pretreatment factors. Psychosom Med 1968; 30(3): 255-76.
31. Karush A, Daniels GE, O'Connor JF, et al. The response to psychotherapy in chronic ulcerative colitis. II. Factors arising from the therapeutic situation. Psychosom Med 1969; 31(3): 201-26.
32. Freyberger H, Kunsebeck HW, Lempa W, et al. Psychotherapeutic interventions in alexithymic patients. With special regard to ulcerative colitis and Crohn patients. Psychother Psychosom 1985; 44(2): 72-81.
33. Milne B, Joachim G, Niedhardt J. A stress management programme for inflammatory bowel disease patients. J Adv Nuts 1986; 11(5): 561-7.
34. Schwarz SP, Blanchard EB. Evaluation of a psychological treatment for inflammatory bowel disease. Behav Res Ther 1991; 29(2): 167-77.
35. Jantschek G, Zeitz M, Pritsch M, et al. Effect of psychotherapy on the course of Crohn's disease. Results of the German prospective multicenter psychotherapy treatment study on Crohn's disease. German Study Group on Psychosocial Intervention in Crohn's Disease. Scand J Gastroenterol 1998; 33(12): 1289-96.
36. Collins SM, McHugh K, Jacobson K, et al. Previous inflammation alters the response of the rat colon to stress. Gastroenterology 1996; 111(6): 1509-15.
37. Santos J, Antolin M, Malagelada JR. Social stress induces reversible inflammation and persistent barrier dysfunction in the rat intestine. Gastroenterology 2001; 120: 297 (abstract).
38. Soderholm JD, Yang PC, Vohra A, et al. Chronic psychological stress induces epithelial barrier disruption, bacterial penetration and mucosal inflammation in ileum and colon of naive rats. Gastroenterology 2001; 120: 372 (abstract).
39. Soderholm JD, Yang PC, Vohra A, et al. Chronic psychological stress induces mucosal inflammation in the ileum and colon of naive rats: Role of mast cells. Gastroenterology 2001; 120: 3747 (abstract).
40. Stout C, Snyder RL. Ulcerative colitis-like lesion in Siamang gibbons. Gastroenterology 1969; 57(3): 256-61.
41. Wood JD, Peck OC, Tefend KS, et al. Evidence that colitis is initiated by environmental stress and sustained by fecal factors in the cotton-top tamarin (Saguinus oedipus). Dig Dis Sci 2000; 45(2): 385-93.
42. Saunders KE, Shen Z, Dewhirst FE, et al. Novel intestinal Helicobacter species isolated from cotton-top tamarins (Saguinus oedipus) with chronic colitis. J Clin Microbiol 1999; 37(1): 146-51.
43. Soderholm JD, Yates D, MacQueen G, et al. Early maternal deprivation predisposes adult rats to colonic mucosal barrier dysfunction in response to mild stress. Gastroenterology 2001; 120: 113 (abstract).
44. Qiu BS, Vallance BA, Blennerhassett PA, et al. The role of CD4+ lymphocytes in the susceptibility of mice to stressinduced reactivation of experimental colitis. Nat Med 1999; 5(10): 1178-82.
45. Million M, Tache Y, Anton P. Susceptibility of Lewis and Fischer rats to stress-induced worsening of TNB-colitis: Protective role of brain CRF. Am J Physiol 1999; 276(4 Part 1): G1027-36.
46. Mathé G. The need of a physiologic and pathophysiolgic definition of stress. Biomed Pharmacother 2000; 54: 119-21.
47. The Diagnostic and Statistical Manual of Mental Disorders, 4th Edn (DSM-IV). Washington DC: American Psychiatric Association. 1994.
48. Mertz H, Morgan V, Tanner G, et al. Regional cerebral activation in irritable bowel syndrome and control subjects with painful and nonpainful rectal distention. Gastroenterology 2000; 118(5): 842-8.
49. Bennett EJ, Tennant CC, Piesse C, et al. Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 1998; 43(2): 256-61.
50. Gwee KA, Leong YL, Graham C, et al. The role of psychological and biological factors in postinfective gut dysfunction. Gut 1999; 44(3): 400-6.
51. Janssen HA, Muris JW, Knotterus JA. The clinical course and prognostic determinants of the irritable bowel syndrome: A literature review. Scand J Gastroenterol 1998; 33(6): 561-7.
52. Tache Y, Martinez V, Million M, et al. Corticotropin-releasing factor and the brain-gut motor response to stress. Can J Gastroenterol 1999; 13(Suppl. A): 18-25A.
53. Bueno L, Gue M, Fabre C, et al. Involvement of central dopamine and D1 receptors in stress-induced colonic motor alterations in rats. Brain Res Bull 1992; 29(2): 135-40.
54. Kimzey SL, Johnson PC, Ritzman SE, et al. Hematology and immunology studies: The second manned Skylab mission. Aviat Space Environ Meal 1976; 47(4): 383-90.
55. Schleifer SJ, Keller SE, Camerino M. et al. Suppression of lymphocyte stimulation following bereavement. J Am Meal Assoc 1983; 250(3): 374-7.
56. Kiecolt-Glaser JK, Garner W, Speicher C, et al. Psychosocial modifiers of immunocompetence in medical students. Psychosom Meal 1984; 46(1): 7-14.
57. Kiecolt-Glaser JK, Marucha PT, Malarkey WB, et al. Slowing of wound healing by psychological stress [see comments]. Lancet 1995; 346(8984): 1194-6.
58. Cohen S, Tyrrell DA, Smith AP. Psychological stress and susceptibility to the common cold [see comments]. N Engl J Meal 1991; 325(9): 606-12.
59. Black S, Humphrey JH, Niven JSF. Inhibition of mantoux reaction by direct suggestion under hypnosis. BMJ 1965; 6: 1649-52.
60. Glaser R, Kiecolt-Glaser JK, Bonneau RH, et al. Stress-induced modulation of the immune response to recombinant hepatitis B vaccine. Psychosom Med 1992; 54(1): 22-9.
61. Glaser R, Kiecolt-Glaser JK, Malarkey WB, et al. The influence of psychological stress on the immune response to vaccines. Ann N Y Acad Sci 1998; 840: 649-55.
62. Jabaaij L, van Hattum J, Vingerhoets JJ, et al. Modulation of immune response to rDNA hepatitis B vaccination by psychological stress. J Psychosom Res 1996; 41(2): 129-37.
63. Jabaaij L, Grosheide PM, Heijtink RA, et al. Influence of perceived psychological stress and distress on antibody response to low dose rDNA hepatitis B vaccine. J Psychosom Res 1993; 37(4): 361-9.
64. Ilnyckyj A, Shanahan F, Anton PA, et al. Quantification of the placebo response in ulcerative colitis. Gastroenterology 1997; 112(6): 1854-8.
65. Meyers S, Janowitz HD. The "natural history" of ulcerative colitis: An analysis of the placebo response. J Clin Gastroenterol 1989; 11(1): 33-7.
66. Bernstein CN. Placebos in medicine. Semin Gastrointest Dis 1999; 10(1): 3-7.
67. Djuric VJ, Bienenstock J, Perdue MH. Psychological and neural regulation of intestinal hypersensitivity. In: Berczi I, Szeleny J, eds. Advances in Psychoneuroimmunology. New York: Plenum Press. 1994; 291-301.
68. Shanahan F. A gut reaction: Lymphoepithelial communication in the intestine. Science 1997; 275(5308): 1897-8.
69. Kemler MA, Barendse GA, Van Kleef M. Relapsing ulcerative colitis associated with spinal cord stimulation. Gastroenterology 1999; 117(1): 215-7.
70. Barbara G, De Giorgio R, Stanghellini V, et al. Relapsing ulcerative colitis after spinal cord stimulation: A case of intestinal neurogenic inflammation? Gastroenterology 1999; 117(5): 1256-7.
71. Peck OC, Wood JD. Brain-gut interactions in ulcerative colitis. Gastroenterology 2000; 118(4): 807-8.
72. Saunders PR, Kosecka U, McKay DM. et al. Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine. Am J Physiol 1994; 267(5 Part 1): G794-9.
73. Saunders PR, Hanssen NP, Perdue MH. Cholinergic nerves mediate stress-induced intestinal transport abnormalities in Wistar-Kyoto rats. Am J Physiol 1997; 273(2 Part 1): G486-90.
74. Kiliaan AJ, Saunders PR, Bijlsma PB, et al. Stress stimulates transepithelial macromolecular uptake in rat jejunum. Am J Physiol 1998; 275(5 Part 1): G1037-44.
75. Santos J, Saunders PR, Hanssen NP, et al. Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat. Am J Physiol 1999; 277(2 Part 1): G391-9.
76. Santos J, Benjamin M, Yang PC, et al. Chronic stress impairs rat growth and jejunal epithelial barrier function: Role of mast cells. Am J Physiol Gastrointest Liver Physiol 2000; 278(6): G847-54.
77. Meddings JB, Swain MG. Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the rat. Gastroenterology 2000; 119(4): 1019-28.
78. Hilsden RJ, Meddings JB, Sutherland LR. Intestinal permeability changes in response to acetylsalicylic acid in relatives of patients with Crohn's disease. Gastroenterology 1996; 110(5): 1395-403.
79. Hollander D, Vadheim CM, Brettholz E, et al. Increased intestinal permeability in patients with Crohn's disease and their relatives. A possible etiologic factor. Ann Intern Med 1986; 105(6): 883-5.
80. May GR, Sutherland LR, Meddings JB. Is small intestinal permeability really increased in relatives of patients with Crohn's disease? Gastroenterology 1993; 104(6): 1627-32.
81. Peeters M, Geypens B, Claus D, et al. Clustering of increased small intestinal permeability in families with Crohn's disease. Gastroenterology 1997; 113(3): 802-7.
82. Yacyshyn BR, Meddings JB. CD45RO expression on circulating CD19+ B cells in Crohn's disease correlates with intestinal permeability. Gastroenterology 1995; 108(1): 132-7.
83. Wyatt J, Vogelsang H, Hubl W, et al. Intestinal permeability and the prediction of relapse in Crohn's disease. Lancet 1993; 341(8858): 1437-9.
84. Barclay GR, Turnberg LA. Effect of psychological stress on salt and water transport in the human jejunum. Gastroenterology 1987; 93(1): 91-7.
85. Santos J, Saperas E, Nogueiras C, et al. Release of mast cell mediators into the jejunum by cold pain stress in humans. Gastroenterology 1998; 114(4): 640-8.
86. Castagliuolo I, LaMont JT, Qiu B, et al. Acute stress causes mucin release from rat colon: Role of corticotropin releasing factor and mast cells. Am J Physiol 1996; 271(5 Part 1): G884-92.
87. Castagliuolo I, Leeman SE, Bartolak-Suki E, et al. A neurotensin antagonist. SR 48692, inhibits colonic responses to immobilization stress in rats. Proc Natl Acad Sci USA 1996; 93(22): 12611-5.
88. Bailey MT, Coe CL. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999; 35(2): 146-55.
89. Spitz J, Hecht G, Taveras M. et al. The effect of dexamethasone administration on rat intestinal permeability: The role of bacterial adherence. Gastroenterology 1994; 106(1): 35-41.
90. Spitz JC, Ghandi S, Taveras M, et al. Characteristics of the intestinal epithelial barrier during dietary manipulation and glucocorticoid stress. Crit Care Med 1996; 24(4): 635-41.
91. Canil C, Rosenshine I, Ruschkowski S, et al. Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infect Immun 1993; 61(7): 2755-62.
92. Wira CR, Sandoe CP, Steele MG. Glucocorticoid regulation of the humoral immune system. I. In vivo effects of dexamethasone on IgA and IgG in serum and at mucosal surfaces. J Immunol 1990; 144(1): 142-6.
93. Karalis K, Sano H, Redwine J, et al. Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo. Science 1991; 254(5030): 421-3.
94. Stephanou A, Jessop DS, Knight RA, et al. Corticotrophin-releasing factor-like immunoreactivity and mRNA in human leukocytes. Brain Behav Immun 1990; 4(1): 67-73.
95. Kawahito Y, Sano H, Kawata M, et al. Local secretion of corticotropin-releasing hormone by enterochromaffin cells in human colon. Gastroenterology 1994; 106(4): 859-65.
96. Lovenberg TW, Chalmers DT, Liu C, et al. CRF2 alpha and CRF2 beta receptor mRNAs are differentially distributed between the rat central nervous system and peripheral tissues. Endocrinology 1995; 136(9): 4139-42.
97. Lovenberg TW, Liaw CW, Grigoriadis DE. et al. Cloning and characterization of a functionally distinct corticotropin-releasing factor receptor subtype from rat brain. Proc Natl Acad Sci USA 1995; 92(3): 836-40.
98. Merchenthaler I, Hynes MA, Vigh S, et al. Immunocytochemical localization of corticotropin releasing factor (CRF) in the rat spinal cord. Brain Res 1983; 275(2): 373-7.
99. van Tol EA, Petrusz P, Lund PK, et al. Local production of corticotropin releasing hormone is increased in experimental intestinal inflammation in rats. Gut 1996; 39(3): 385-92.
100. Wolter HJ. Corticotropin-releasing factor is contained within perikarya and nerve fibres of rat duodenum. Biochem Biophys Res Commun 1984; 122(1): 381-7.
101. Kawahito Y, Sano H, Mukai S, et al. Corticotropin releasing hormone in colonic mucosa in patients with ulcerative colitis. Gut 1995; 37(4): 544-51.
102. Webster EL, Tracey DE, Jutila MA, et al. Corticotropin-releasing factor receptors in mouse spleen: Identification of receptor-bearing cells as resident macrophages. Endocrinology 1990; 127(1): 440-52.
103. Singh VK. Stimulatory effect of corticotropin-releasing neurohormone on human lymphocyte proliferation and interleukin-2 receptor expression. J Neuroimmunol 1989; 23(3): 257-62.
104. Million M, Sanchez-Watts G, Miampamba M, et al. Urocortin and corticotrophin-releasing factor (CRF) receptor type 1 are expressed in the rat colon. Gastroenterology 2001; 120: 917 (abstract).
105. Ceccatelli S, Cintra A, Hokfelt T, et al. Coexistence of glucocorticoid receptor-like immunoreactivity with neuropeptides in the hypothalamic paraventricular nucleus. Exp Brain Res 1989; 78(1): 33-42.
106. Gudelsky GA, Berry SA, Meltzer HY. Neurotensin activates tuberoinfundibular dopamine neurons and increases serum corticosterone concentrations in the rat. Neuroendocrinology 1989; 49(6): 604-9.
107. Rowe W, Viau V, Meaney MJ, et al. Central administration of neurotensin stimulates hypothalamic-pituitary-adrenal activity. The paraventricular CRF neuron as a critical site of action. Ann N Y Acad Sci 1992; 668: 365-7.
108. Riegler M, Castagliuolo I, Wang C. et al. Neurotensin stimulates Cl(-) secretion in human colonic mucosa in vitro: Role of adenosine. Gastroenterology 2000; 119(2): 348-57.
109. Gui X, Carraway RE. Mast cell histamine mediates neurotensin-enhanced 3H-taurocholate absorption in jejenum. Gastroenterology 2001; 120: 1613 (abstract).
110. Kyosola K, Penttila O, Salaspuro M. Rectal mucosal adrenergic innervation and enterochromaffin cells in ulcerative colitis and irritable colon. Scand J Gastroenterol 1977; 12(3): 363-7.
111. McCafferty DM, Sharkey KA, Wallace JL. Beneficial effects of local or systemic lidocaine in experimental colitis. Am J Physiol 1994; 266(4 Part 1): G560-7.
112. Gaton J, Fernandez dlG, Velasco A. The role of the neurotransmitters acetylcholine and noradrenaline in the pathogenesis of stress ulcers. Comp Biochem Physiol C 1993; 106(1): 125-9.
113. Phillips TE. Both crypt and villus intestinal goblet cells secrete mucin in response to cholinergic stimulation. Am J Physiol 1992; 262(2 Part 1): G327-31.
114. Groot J, Bijlsma P, Van Kalkeren A, et al. Stress-induced decrease of the intestinal barrier function. The role of muscarinic receptor activation. Ann N Y Acad Sci 2000; 915: 237-46.
115. Holzer P, Holzer-Petsche U. Tachykinins in the gut. Part II. Roles in neural excitation, secretion and inflammation. Pharmacol Ther 1997; 73(3): 219-63.
116. Sturiale S, Barbara G, Qiu B. et al. Neutral endopeptidase (EC 3.4.24.11) terminates colitis by degrading substance P. Proc Natl Acad Sci USA 1999; 96(20): 11653-8.
117. Geboes K, Rutgeerts P, Ectors N, et al. Major histocompatibility class II expression on the small intestinal nervous system in Crohn's disease. Gastroenterology 1992; 103(2): 439-47.
118. Ruhl A, Franzke S, Collins SM, et al. Interleukin-6 expression and regulation in rat enteric glial cells. Am J Physiol Gastrointest Liver Physiol 2001; 280(6): G1163-71.
119. Stead RH, Tomioka M, Quinonez G, et al. Intestinal mucosal mast cells in normal and nematode-infected rat intestines are in intimate contact with peptidergic nerves. Proc Natl Acad Sci USA 1987; 84(9): 2975-9.
120. Theoharides TC, Spanos C, Pang X, et al. Stress-induced intracranial mast cell degranulation: A corticotropin-releasing hormone-mediated effect. Endocrinology 1995; 136(12): 5745-50.
121. Theoharides TC, Singh LK, Boucher W. et al. Corticotropin-releasing hormone induces skin mast cell degranulation and increased vascular permeability, a possible explanation for its proinflammatory effects. Endocrinology 1998; 139(1): 403-13.
122. Crowe SE, Luthra GK, Perdue MH. Mast cell mediated ion transport in intestine from patients with and without inflammatory bowel disease. Gut 1997; 41(6): 785-92.
123. Berin MC, Kiliaan AJ, Yang PC. The influence of mast cells on pathways of transepithelial antigen transport in rat intestine. J Immunol 1998; 161(5): 2561-6.
124. Perdue MH, Masson S, Wershil BK. et al. Role of mast cells in ion transport abnormalities associated with intestinal anaphylaxis. Correction of the diminished secretory response in genetically mast cell-deficient W/Wv mice by bone marrow transplantation. J Clin Invest 1991; 87(2): 687-93.
125. Castagliuolo I, Wershil BK, Karalis K. et al. Colonic mucin release in response to immobilization stress is mast cell dependent. Am J Physiol 1998; 274(6 Part 1): G1094-100.