Altered expression and secretion of colonic Interleukin-6 in a stress-sensitive animal model of brain-gut axis dysfunction

Journal of Neuroimmunology

Volumn 235, Issue 1-2, 2011, Pages 48-55

  O'Malley, Dervla ^a   Dinan, Timothy G ^a,b   Cryan, John F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Interleukin 6; Irritable bowel syndrome; Submucosal neurons; Wistar Kyoto rat

Indexed keywords

CALCIUM; INTERLEUKIN 6; RECOMBINANT INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; COLON MUCOSA; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; ENTEROPATHY; INTESTINE INNERVATION; MALE; NERVE CELL EXCITABILITY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SPRAGUE DAWLEY RAT; STRAIN DIFFERENCE; TISSUE SECTION; WISTAR KYOTO RAT;

ANIMALS; BRAIN; COLON; DISEASE MODELS, ANIMAL; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-6; IRRITABLE BOWEL SYNDROME; MALE; RATS; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL;

EID: 79958016326     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2011.04.003     Document Type: Article

References (48)

1. Armario A., Gavalda A., Marti J. Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology 1995, 20:879-890.
2. Bohmelt 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.
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
4. Buhner S., Li Q., Vignali S., Barbara G., de Giorgio R., Stanghellini V., Cremon C., Zeller F., Langer R., Daniel H., Michel K., Schemann M. Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology 2009, 137:1425-1434.
5. Cenac N., Andrews C.N., Holzhausen M., Chapman K., Cottrell G., Andrade-Gordon P., Steinhoff M., Barbara G., Beck P., Bunnett N.W., Sharkey K.A., Ferraz J.G., Shaffer E., Vergnolle N. Role for protease activity in visceral pain in irritable bowel syndrome. J. Clin. Invest. 2007, 117:636-647.
6. Chadwick V.S., Chen W., Shu D., Paulus B., Bethwaite P., Tie A., Wilson I. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 2002, 122:1778-1783.
7. Clarke G., Quigley E.M., Cryan J.F., Dinan T.G. Irritable bowel syndrome: towards biomarker identification. Trends Mol. Med. 2009.
8. De La Garza R., Mahoney J.J. A distinct neurochemical profile in WKY rats at baseline and in response to acute stress: implications for animal models of anxiety and depression. Brain Res. 2004, 1021:209-218.
9. 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.
10. Dinan T.G., Clarke G., Quigley E.M., Scott L.V., Shanahan F., Cryan J., Cooney J., Keeling P.W. Enhanced cholinergic-mediated increase in the pro-inflammatory cytokine IL-6 in irritable bowel syndrome: role of muscarinic receptors. Am. J. Gastroenterol. 2008, 103:2570-2576.
11. Drossman D.A., Creed F.H., Olden K.W., Svedlund J., Toner B.B., Whitehead W.E. Psychosocial aspects of the functional gastrointestinal disorders. Gut 1999, 45(Suppl 2):II25-II30.
12. Fitzgerald P., Cassidy Eugene M., Clarke G., Scully P., Barry S., Quigley Eamonn M.M., Shanahan F., Cryan J., Dinan Timothy G. Tryptophan catabolism in females with irritable bowel syndrome: relationship to interferon-gamma, severity of symptoms and psychiatric co-morbidity. Neurogastroenterol. Motil. 2008, 20:1291-1297.
13. Folks D.G. The interface of psychiatry and irritable bowel syndrome. Curr. Psychiatry Rep. 2004, 6:210-215.
14. Furness J.B. Types of neurons in the enteric nervous system. J. Auton. Nerv. Syst. 2000, 81:87-96.
15. Gibney S.M., Gosselin R.D., Dinan T.G., Cryan J.F. Colorectal distension-induced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience 2010, 165:675-683.
16. Gosselin R.D., Gibney S., O'Malley D., Dinan T.G., Cryan J.F. Region specific decrease in glial fibrillary acidic protein immunoreactivity in the brain of a rat model of depression. Neuroscience 2009, 159:915-925.
17. Greenwood-Van Meerveld B., Johnson A.C., Cochrane S., Schulkin J., Myers D.A. Corticotropin-releasing factor 1 receptor-mediated mechanisms inhibit colonic hypersensitivity in rats. Neurogastroenterol. Motil. 2005, 17:415-422.
18. Gunter W.D., Shepard J.D., Foreman R.D., Myers D.A., Greenwood-Van Meerveld B. Evidence for visceral hypersensitivity in high-anxiety rats. Physiol. Behav. 2000, 69:379-382.
19. Hyland NP G.S., Gosselin R.D., Lee K., Dinan T.G., Cryan J.F. Assessment of colonic secretory function and faecal output in viscerally hypersensitive Wistar Kyoto rats. Gastroenterology 2008, A277.
20. Hyland N.P., Julio-Pieper M., O'Mahony S.M., Bulmer D.C., Lee K., Quigley E.M., Dinan T.G., Cryan J.F. A distinct subset of submucosal mast cells undergoes hyperplasia following neonatal maternal separation: a role in visceral hypersensitivity?. Gut 2009, 58:1029-1030. author reply 1030-1.
21. Kelles A., Janssens J., Tack J. IL-1beta and IL-6 excite neurones and suppress cholinergic neurotransmission in the myenteric plexus of the guinea pig. Neurogastroenterol. Motil. 2000, 12:531-538.
22. Kindt S., Vanden Berghe P., Boesmans W., Roosen L., Tack J. Prolonged IL-1beta exposure alters neurotransmitter and electrically induced Ca responses in the myenteric plexus. Neurogastroenterol. Motil. 2009.
23. Lahmame A., Grigoriadis D.E., de Souza E.B., Armario A. Brain corticotropin-releasing factor immunoreactivity and receptors in five inbred rat strains: relationship to forced swimming behaviour. Brain Res. 1997, 750:285-292.
24. Li T., He S. Induction of IL-6 release from human T cells by PAR-1 and PAR-2 agonists. Immunol. Cell Biol. 2006, 84:461-466.
25. Lin H.W., Levison S.W. Context-dependent IL-6 potentiation of interferon- gamma-induced IL-12 secretion and CD40 expression in murine microglia. J. Neurochem. 2009, 111:808-818.
26. Lydiard R.B., Fossey M.D., Marsh W., Ballenger J.C. Prevalence of psychiatric disorders in patients with irritable bowel syndrome. Psychosomatics 1993, 34:229-234.
27. Macsharry J., O'Mahony L., Fanning A., Bairead E., Sherlock G., Tiesman J., Fulmer A., Kiely B., Dinan T.G., Shanahan F., Quigley E.M. Mucosal cytokine imbalance in irritable bowel syndrome. Scand. J. Gastroenterol. 2008, 43:1467-1476.
28. Mawe G.M., Strong D.S., Sharkey K.A. Plasticity of enteric nerve functions in the inflamed and postinflamed gut. Neurogastroenterol. Motil. 2009, 21:481-491.
29. McKernan D.P., Nolan A., Brint E.K., O'Mahony S.M., Hyland N.P., Cryan J.F., Dinan T.G. Toll-like receptor mRNA expression is selectively increased in the colonic mucosa of two animal models relevant to irritable bowel syndrome. PLoS One 2009, 4:e8226.
30. Natale L., Piepoli A.L., de Salvia M.A., de Salvatore G., Mitolo C.I., Marzullo A., Portincasa P., Moschetta A., Palasciano G., Mitolo-Chieppa D. Interleukins 1 beta and 6 induce functional alteration of rat colonic motility: an in vitro study. Eur. J. Clin. Invest. 2003, 33:704-712.
31. O'Malley D., Dinan T.G., Cryan J.F. IL-6 activates neurons of the sub-mucosal plexus via a MAPK-dependent mechanism: relevance to irritable bowel syndrome. Neurogastroenterol. Motil. 2009.
32. 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 behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry 2009, 65:263-267.
33. O'Mahony S.M., Bulmer D.C., Coelho A.M., Fitzgerald P., Bongiovanni C., Lee K., Winchester W., Dinan T.G., Cryan J.F. 5-HT(2B) receptors modulate visceral hypersensitivity in a stress-sensitive animal model of brain-gut axis dysfunction. Neurogastroenterol. Motil. 2010, 22(573-8):e124.
34. O'Malley D., Dinan T.G., Cryan J.F. 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 2010, 31:662-670.
35. O'Malley D., Julio-Pieper M., Gibney S.M., Dinan T.G., Cryan J.F. Distinct alterations in colonic morphology and physiology in two rat models of enhanced stress-induced anxiety- and depression-like behavior. Stress 2010, 13:114-122.
36. 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.
37. O'Malley D., Liston M., Hyland N.P., Dinan T.G., Cryan J.F. Colonic soluble mediators from the maternal separation model of irritable bowel syndrome activate submucosal neurons via an Interleukin-6-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300:G241-G252.
38. Pare W.P. The performance of WKY rats on three tests of emotional behavior. Physiol. Behav. 1992, 51:1051-1056.
39. Pare W.P. Passive-avoidance behavior in Wistar-Kyoto (WKY), Wistar, and Fischer-344 rats. Physiol. Behav. 1993, 54:845-852.
40. Quigley E.M. Changing face of irritable bowel syndrome. World J. Gastroenterol. 2006, 12:1-5.
41. Rittenhouse P.A., Lopez-Rubalcava C., Stanwood G.D., Lucki I. Amplified behavioral and endocrine responses to forced swim stress in the Wistar-Kyoto rat. Psychoneuroendocrinology 2002, 27:303-318.
42. Ruhl A., Franzke S., Collins S.M., Stremmel W. Interleukin-6 expression and regulation in rat enteric glial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280:G1163-G1171.
43. Saunders P.R., Maillot C., Million M., Tache Y. Peripheral corticotropin-releasing factor induces diarrhea in rats: role of CRF1 receptor in fecal watery excretion. Eur. J. Pharmacol. 2002, 435:231-235.
44. Song C., Earley B., Leonard B.E. Behavioral, neurochemical, and immunological responses to CRF administration. Is CRF a mediator of stress?. Ann. N.Y. Acad. Sci. 1995, 771:55-72.
45. Spiller R.C. Irritable bowel syndrome. Br. Med. Bull. 2004, 72:15-29.
46. Tilg H., Dinarello C.A., Mier J.W. IL-6 and APPs: anti-inflammatory and immunosuppressive mediators. Immunol. Today 1997, 18:428-432.
47. van Wagoner N.J., Benveniste E.N. Interleukin-6 expression and regulation in astrocytes. J. Neuroimmunol. 1999, 100:124-139.
48. Xia Y., Hu H.Z., Liu S., Ren J., Zafirov D.H., Wood J.D. IL-1beta and IL-6 excite neurons and suppress nicotinic and noradrenergic neurotransmission in guinea pig enteric nervous system. J. Clin. Invest. 1999, 103:1309-1316.