Chronological assessment of mast cell-mediated gut dysfunction and mucosal inflammation in a rat model of chronic psychosocial stress

Brain, Behavior, and Immunity

Volumn 24, Issue 7, 2010, Pages 1166-1175

  Vicario, María ^a,b   Guilarte, Mar ^b   Alonso, Carmen ^a,b   Yang, Pinchang ^c   Martínez, Cristina ^a,b   Ramos, Laura ^a,b   Lobo, Beatriz ^a,b   González, Ana ^a,b   Guilà, Meritxell ^a,b   Pigrau, Marc ^a,b   Saperas, Esteban ^a,b   Azpiroz, Fernando ^a,b   Santos, Javier ^a,b  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

Irritable bowel syndrome; Mast cells; Psychosocial stress

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL INFILTRATION; CELL PERMEABILIZATION; CROWDING; ENTERITIS; GASTROINTESTINAL DISEASE; HISTOPATHOLOGY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEUKOCYTE COUNT; MALE; MAST CELL; MENTAL STRESS; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CELL COUNT; COLON; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; CROWDING; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GASTROINTESTINAL TRACT; HOUSING, ANIMAL; ILEUM; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; IRRITABLE BOWEL SYNDROME; JEJUNUM; MALE; MAST CELLS; MITOCHONDRIA; PERMEABILITY; RATS; RATS, INBRED WKY; SOCIAL ENVIRONMENT; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 79959831052     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.06.002     Document Type: Article

References (69)

1. Adzic M., Djordjevic A., Demonacos C., Krstic-Demonacos M., Radojcic M.B. The role of phosphorylated glucocorticoid receptor in mitochondrial functions and apoptotic signalling in brain tissue of stressed Wistar rats. Int. J. Biochem. Cell. Biol. 2009, 41:2181-2188.
2. Al-Chaer E.D., Kawasaki M., Pasricha P.J. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 2000, 119:1276-1285.
3. Alonso C., Santos J. A closer look at mucosal inflammation in irritable bowel syndrome: sex- and gender-related disparities-quantity, quality, or both?. Am. J. Gastroenterol. 2009, 104:401-403.
4. Armario A., Ortiz R., Balasch J. Effect of crowding on some physiological and behavioral variables in adult male rats. Physiol. Behav. 1984, 32:35-37.
5. Barbara G., Wang B., Stanghellini V., de Giorgio R., Cremon C., Di Nardo G., Trevisani M., Campi B., Geppetti P., Tonini M., Bunnett N.W., Grundy D., Corinaldesi R. Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 2007, 132:26-37.
6. Bennett E.J., Tennant C.C., Piesse C., Badcock C.A., Kellow J.E. Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 1998, 43:256-261.
7. Bhatnagar S., Dallman M.F. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 1998, 84:1025-1039.
8. Bhatnagar S., Vining C., Iyer V., Kinni V. Changes in hypothalamic-pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J. Neuroendocrinol. 2006, 18:13-24.
9. Böhmelt A.H., Nater U.M., Franke S., Hellhammer D.H., Ehlert U. Basal and stimulated hypothalamic-pituitary-adrenal axis activity in patients with functional gastrointestinal disorders and healthy controls. Psychosom. Med. 2005, 67:288-294.
10. Boudry G., Jury J., Yang P.C., Perdue M.H. Chronic psychological stress alters epithelial cell turn-over in rat ileum. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292:G1228-G1232.
11. Bowers S.L., Bilbo S.D., Dhabhar F.S., Nelson R.J. Stressor-specific alterations in corticosterone and immune responses in mice. Brain. Behav. Immun. 2008, 22:105-113.
12. Bugajski J., Gadek-Michalska A. Effect of cyclooxygenase inhibitors on the vasopressin induced ACTH and corticosterone response during crowding stress. J. Physiol. Pharmacol. 2003, 54:247-256.
13. Caso J.R., Leza J.C., Menchen L. The effects of physical and psychological stress on the gastrointestinal tract: lessons from animal models. Curr. Mol. Med. 2008, 8:299-312.
14. Chang L., Sundaresh S., Elliott J., Anton P.A., Baldi P., Licudine A., Mayer M., Vuong T., Hirano M., Naliboff B.D., Ameen V.Z., Mayer E.A. Dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis in irritable bowel syndrome. Neurogastroenterol. Motil. 2009, 21:149-159.
15. Chin A.C., Lee W.Y., Nusrat A., Vergnolle N., Parkos C.A. Neutrophil-mediated activation of epithelial protease-activated receptors-1 and -2 regulates barrier function and transepithelial migration. J. Immunol. 2008, 181:5702-5710.
16. Chin A.C., Parkos C.A. Pathobiology of neutrophil transepithelial migration: implications in mediating epithelial injury. Annu. Rev. Pathol. 2007, 2:111-143.
17. Chrousos G.P. Stress and disorders of the stress system. Nat. Rev. Endocrinol. 2009, 5:374-381.
18. Collins S.M., Bercik P. The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 2009, 136:2003-2014.
19. Collins S.M., McHugh K., Jacobson K., Khan I., Riddell R., Murase K., Weingarten H.P. Previous inflammation alters the response of the rat colon to stress. Gastroenterology 1996, 111:1509-1515.
20. Dinan T.G., Quigley E.M., Ahmed S.M., Scully P., O'Brien S., O'Mahony L., O'Mahony S., Shanahan F., Keeling P.W. Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker?. Gastroenterology 2006, 130:304-311.
21. Engler H., Dawils L., Hoves S., Kurth S., Stevenson J.R., Schauenstein K., Stefanski V. Effects of social stress on blood leukocyte distribution: the role of alpha- and beta-adrenergic mechanisms. J. Neuroimmunol. 2004, 156:153-162.
22. Faresjo A., Grodzinsky E., Johansson S., Wallander M.A., Timpka T., Akerlind I. Psychosocial factors at work and in every day life are associated with irritable bowel syndrome. Eur. J. Epidemiol. 2007, 22:473-480.
23. Fukudo S. Role of corticotropin-releasing hormona in irritable bowel syndrome and intestinal inflammation. J. Gastroenterol. 2007, 42:48-51.
24. Fukudo S., Nomura T., Hongo M. Impact of corticotropin-releasing hormone on gastrointestinal motility and adrenocorticotropic hormone in normal controls and patients with irritable bowel syndrome. Gut 1998, 42:845-849.
25. Gadek-Michalska A., Bugajski J. Repeated handling, restraint, or chronic crowding impair the hypothalamic-pituitary-adrenocortical response to acute restraint stress. J. Physiol. Pharmacol. 2003, 54:449-459.
26. Gamallo A., Villanua A., Trancho G., Fraile A. Stress adaptation and adrenal activity in isolated and crowded rats. Physiol. Behav. 1986, 36:217-221.
27. Gareau M.G., Silva M.A., Perdue M.H. Pathophysiological mechanisms of stress-induced intestinal damage. Curr. Mol. Med. 2008, 8:274-281.
28. Gay J., Kokkotou E., O'Brien M., Pothoulakis C., Karalis K.P. Corticotropin-releasing hormone deficiency is associated with reduced local inflammation in a mouse model of experimental colitis. Endocrinology 2008, 149:3403-3409.
29. Guilarte M., Santos J., de Torres I., Alonso C., Vicario M., Ramos L., Martínez C., Casellas F., Saperas E., Malagelada J.R. Diarrhoea-predominant IBS patients show mast cell activation and hyperplasia in the jejunum. Gut 2007, 56:203-209.
30. Karalis K., Sano H., Redwine J., Listwak S., Wilder R.L., Chrousos G.P. Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo. Science 1991, 254:421-423.
31. Kaushik S., Kaur J. Effect of chronic cold stress on intestinal epithelial cell proliferation and inflammation in rats. Stress 2005, 8:191-197.
32. Keita, A.V., Söderholm, J.D., Ericson, A.C., 2010. Stress-induced barrier disruption of rat follicle-associated epithelium involves corticotropin-releasing hormone, acetylcholine, substance P, and mast cells. Neurogastroenterol. Motil. [Epub ahead of print].
33. Kiank C., Taché Y., Larauche M. Stress-related modulation of inflammation in experimental models of bowel disease and post-infectious irritable bowel syndrome: role of corticotropin-releasing factor receptors. Brain. Behav. Immun. 2010, 24:41-48.
34. Kokkotou E., Torres D., Moss A.C., O'Brien M., Grigoriadis D.E., Karalis K., Pothoulakis C. Corticotropin-releasing hormone receptor 2-deficient mice have reduced intestinal inflammatory responses. J. Immunol. 2006, 177:3355-3361.
35. La Fleur S.E., Wick E.C., Idumalla P.S., Grady E.F., Bhargava A. Role of peripheral corticotropin-releasing factor and urocortin II in intestinal inflammation and motility in terminal ileum. Proc. Natl. Acad. Sci. 2005, 102:7647-7652.
36. Levine S. Maternal and environmental influences on the adrenocortical response to stress in weaning rats. Science 1967, 156:258-260.
37. Lipkin M., Bell B., Sherlock P. Cell proliferation kinetics in the gastrointestinal tract of man. I. Cell renewal in colon and rectum. J. Clin. Invest. 1963, 42:767-776.
38. Ma S., Morilak D.A. Chronic intermittent cold stress sensitises the hypothalamic-pituitary-adrenal response to a novel acute stress by enhancing noradrenergic influence in the rat paraventricular nucleus. J. Neuroendocrinol. 2005, 17:761-769.
39. Maehly A.C., Chance B. The assay of catalases and peroxidases. Methods of Biochemical analysis 1954, 357. Wiley Interscience, New York. D. Glick (Ed.).
40. Maunder R.G., Levenstein S. The role of stress in the development and clinical course of inflammatory bowel disease: epidemiological evidence. Curr. Mol. Med. 2008, 8:247-252.
41. McLean P.G., Picard C., Garcia-Villar R., Ducos de Lahitte R., Moré J., Fioramonti J., Bueno L. Effects of nematode infection on sensitivity to intestinal distension: role of tachykinin NK2 receptors. Eur. J. Pharmacol. 1997, 337:279-282.
42. Mönnikes H., Tebbe J.J., Hildebrandt M., Arck P., Osmanoglou E., Rose M., Klapp B., Wiedenmann B., Heymann-Mönnikes I. Role of stress in functional gastrointestinal disorders. Evidence for stress-induced alterations in gastrointestinal motility and sensitivity. Digest. Dis. 2001, 19:201-211.
43. Murray C.D.R., Flynn J., Ratcliffe L., Jacyna M.R., Kamm M.A., Emmanuel A.V. Effect of acute physical and psychological stress on gut autonomic innervation in irritable bowel syndrome. Gastroenterology 2004, 127:1695-1703.
44. Nicholl B.I., Halder S.L., Macfarlane G.J., Thompson D.G., O'Brien S., Musleh M., McBeth J. Psychosocial risk markers for new onset irritable bowel syndrome - results of a large prospective population-based study. Pain 2008, 137:147-155.
45. O'Mahony S.M., Marchesi J.R., Scully P., Codling C., Ceolho A.M., Quigley E.M., Cryan J.F., Dinan T.G. Early life stress alters behaviour, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiat. 2009, 65:263-267.
46. O'Malley D., Julio-Pieper M., Gibney S.M., Gosselin R.D., Dinan T.G., Cryan J.F. Differential stress-induced alterations of colonic corticotropin-releasing factor receptors in the Wistar Kyoto rat. Neurogastroenterol. Motil. 2010, 22:301-311.
47. Palsson O.S., Drossman D.A. Psychiatric and psychological dysfunction in irritable bowel syndrome and the role of psychological treatments. Gastroenterol. Clin. N. Am. 2005, 34:281-303.
48. Piche T., Barbara G., Aubert P., Bruley des Varannes S., Dainese R., Nano J.L., Cremon C., Stanghellini V., De Giorgio R., Galmiche J.P., Neunlist M. Impaired intestinal integrity in the colon of irritable bowel syndrome patients: involvement of soluble mediators. Gut 2009, 58:196-201.
49. Ponferrada A., Caso J.R., Alou L., Colón A., Sevillano D., Moro M.A., Lizasoain I., Menchén P., Gómez-Lus M.L., Lorenzo P., Cos E., Leza J.C., Menchén L. The role of PPARgamma on restoration of colonic homeostasis after experimental stress-induced inflammation and dysfunction. Gastroenterology 2007, 132:1791-1803.
50. Psarra A.M.G., Solakidi S., Sekeris C.E. The mitochondrion as a primary site of action of regulatory agents involved in neuroimmunomodulation. Ann. N.Y. Acad. Sci. 2006, 1088:12-22.
51. Reber S.O., Birkeneder L., Veenema A.H., Obermeier F., Falk W., Straub R.H., Neumann I.D. Adrenal insufficiency and colonic inflammation after a novel chronic psycho-social stress paradigm in mice. implications and mechanisms. Endocrinology 2007, 148:670-682.
52. Reber S.O., Obermeier F., Straub H.R., Falk W., Neumann I.D. Chronic intermittent psychosocial stress (social defeat/overcrowding) in mice increases the severity of an acute DSS-induced colitis and impairs regeneration. Endocrinology 2006, 147:4968-4976.
53. Santos J., Alonso C., Vicario M., Ramos L., Lobo B., Malagelada J.R. Neuropharmacology of stress-induced mucosal inflammation: implications for inflammatory bowel disease and irritable bowel syndrome. Curr. Mol. Med. 2008, 8:258-273.
54. Santos J., Benjamin M., Yang P.C., Prior T., Perdue M.H. Chronic stress impairs rat growth and jejunal epithelial barrier function: role of mast cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 278:G847-G854.
55. Santos J., Bienenstock J., Perdue M.H. Innervation of lymphoid tissue and functional consequences of neurotransmitter and neuropeptide release. Food Allergy and Intolerance 2002, 51-67. W.B. Saunders, London. second ed. J. Brostoff, S.J. Challacombe (Eds.).
56. Santos J., Yang P.C., Söderholm J.D., Benjamin M., Perdue M.H. Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat. Gut 2001, 48:630-636.
57. Santos J., Yates D., Guilarte M., Vicario M., Alonso C., Perdue M.H. Stress neuropeptides evoke epithelial responses via mast cell activation in the rat colon. Psychoneuroendocrinology 2008, 33:1248-1256.
58. Saunders P.R., Miceli P., Vallance B.A., Wang L., Pinto S., Tougas G., Kamath M., Jacobson K. Noradrenergic and cholinergic neural pathways mediate stress-induced reactivation of colitis in the rat. Auton. Neurosci. 2006, 124:56-68.
59. Savkovic S.D., Koutsouris A., Hecht G. Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration of neutrophils. Infect. Immun. 1996, 64:4480-4487.
60. Smith F., Clark J.E., Overman B.L., Tozel C.C., Huang J.H., Rivier J.E., Blikslager A.T., Moeser A.J. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298:G352-G363.
61. Söderholm J.D., Yang P.C., Ceponis P., Vohra A., Riddell R., Sherman P.M., Perdue M.H. Chronic stress induces mast cell-dependent bacterial adherence and initiates mucosal inflammation in the rat intestine. Gastroenterology 2002, 123:1099-1108.
62. Söderholm J.D., Yates D.A., Gareau M.G., Yang P.C., MacQueen G., Perdue M.H. Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283:G1257-G1263.
63. Somasundaram S., Rafi S., Hayllar J., Sigthorsson G., Jacob M., Price A.B., Macpherson A., Mahmod T., Scott D., Wrigglesworth J.M., Bjarnason I. Mitochondrial damage: a possible mechanism of the "topical" phase of NSAID induced injury to the rat intestine. Gut 1997, 41:344-353.
64. Stefanski V., Peschel A., Reber S. Social stress affects migration of blood T cells into lymphoid organs. J. Neuroimmunol. 2003, 138:17-24.
65. Taché Y., Bonaz B. Corticotropin-releasing factor receptors and stress-related alterations of gut motor function. J. Clin. Invest. 2007, 117:33-40.
66. Tamashiro K.L., Nguyen M.M., Sakai R.R. Social stress: from rodents to primates. Front. Neuroendocrinol. 2005, 26:27-40.
67. Teitelbaum A.A., Gareau M.G., Jury J., Yang P.C., Perdue M.H. Chronic peripheral administration of corticotropin-releasing factor causes colonic barrier dysfunction similar to psychological stress. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295:G452-G459.
68. Vicario M., Crespi M., Franch A., Amat C., Pelegrí C., Moretó M. Induction of colitis in young rats by dextran sulfate sodium. Digest. Dis. Sci. 2005, 50:143-150.
69. Wallon C., Yang P.C., Keita A.V., Ericson A.C., McKay D.M., Sherman P.M., Perdue M.H., Söderholm J.D. Corticotropin-releasing hormone (CRH) regulates macromolecular permeability via mast cells in normal human colonic biopsies in vitro. Gut 2008, 57:50-58.