Differential visceral pain sensitivity and colonic morphology in four common laboratory rat strains

Experimental Physiology

Volumn 99, Issue 2, 2014, Pages 359-367

  O'Malley, Dervla ^a,b   Julio Pieper, Marcela ^a   O'Mahony, Siobhain M ^a,b   Dinan, Timothy G ^a,b   Cryan, John F ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPERPLASIA; COLON; CONTROLLED STUDY; DIGESTIVE SYSTEM INFLAMMATION; DISEASE ASSOCIATION; DISEASE EXACERBATION; DISEASE PREDISPOSITION; ENTEROPATHY; EXPERIMENTAL RAT; GASTROINTESTINAL TRACT; GOBLET CELL; HYPOTHESIS; MALE; MUCOSA THICKNESS; MUSCLE THICKNESS; NOCICEPTION; NONHUMAN; PAIN THRESHOLD; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; STRESS; THICKNESS; VISCERAL PAIN;

ANIMALS; COLON; GOBLET CELLS; HYPERPLASIA; INFLAMMATION; IRRITABLE BOWEL SYNDROME; MALE; MUSCLES; PAIN THRESHOLD; RATS; RATS, INBRED F344; RATS, INBRED LEW; RATS, INBRED SHR; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; VISCERAL PAIN;

EID: 84895071472     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/expphysiol.2013.076109     Document Type: Article

References (42)

1. Armario A, Gavalda A & Marti J (1995). Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats. Psychoneuroendocrinology 20, 879-890.
2. Artis D, Wang ML, Keilbaugh SA, He W, Brenes M, Swain GP, Knight PA, Donaldson DD, Lazar MA, Miller HR, Schad GA, Scott P & Wu GD (2004). RELMβ/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proc Natl Acad Sci U S A 101, 13596-13600.
3. Berton O, Aguerre S, Sarrieau A, Mormede P & Chaouloff F (1998). Differential effects of social stress on central serotonergic activity and emotional reactivity in Lewis and spontaneously hypertensive rats. Neuroscience 82, 147-159.
4. Blackler R, Syer S, Bolla M, Ongini E & Wallace JL (2012). Gastrointestinal-sparing effects of novel NSAIDs in rats with compromised mucosal defence. PLoS One 7, e35196.
5. Blanchard EB, Lackner JM, Sanders K, Krasner S, Keefer L, Payne A, Gudleski GD, Katz L, Rowell D, Sykes M, Kuhn E, Gusmano R, Carosella AM, Firth R & Dulgar-Tulloch L (2007). A controlled evaluation of group cognitive therapy in the treatment of irritable bowel syndrome. Behav Res Ther 45, 633-648.
6. Calogero AE, Sternberg EM, Bagdy G, Smith C, Bernardini R, Aksentijevich S, Wilder RL, Gold PW & Chrousos GP (1992). Neurotransmitter-induced hypothalamic-pituitary-adrenal axis responsiveness is defective in inflammatory disease-susceptible Lewis rats: in vivo and in vitro studies suggesting globally defective hypothalamic secretion of corticotropin-releasing hormone. Neuroendocrinology 55, 600-608.
7. Chadwick VS, Chen W, Shu D, Paulus B, Bethwaite P, Tie A & Wilson I (2002). Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 122, 1778-1783.
8. Cohen H, Zohar J, Gidron Y, Matar MA, Belkind D, Loewenthal U, Kozlovsky N & Kaplan Z (2006). Blunted HPA axis response to stress influences susceptibility to posttraumatic stress response in rats. Biol Psychiatry 59, 1208-1218.
9. De La Garza R 2nd & Mahoney JJ 3rd (2004). 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 1021, 209-218.
10. Dignass AU, Tsunekawa S & Podolsky DK (1994). Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology 106, 1254-1262.
11. Dinan TG, Quigley EM, Ahmed SM, Scully P, O'Brien S, O'Mahony L, O'Mahony S, Shanahan F & Keeling PW (2006). Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology 130, 304-311.
12. Drueke TB, Hennessen U, Lucas PA, Nabarra B, Ben Nasr L, Thomasset M, Lacour B, Coudrier E & McCarron DA (1990). Epithelial abnormalities in intestine and kidney of the spontaneously hypertensive rat. Am J Hypertens 3, 195S-201S.
13. Gibney SM, Gosselin RD, Dinan TG & Cryan JF (2010). Colorectal distension-induced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience 165, 675-683.
14. Gué M, Del Rio-Lacheze C, Eutamene H, Théodorou V, Fioramonti J & Buéno L (1997). Stress-induced visceral hypersensitivity to rectal distension in rats: role of CRF and mast cells. Neurogastroenterol Motil 9, 271-279.
15. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L & Hansson GC (2008). The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105, 15064-15069.
16. Kawanishi C, Fukuda M, Tamura R, Nishijo H & Ono T (1997). Effects of repeated cold stress on feeding, avoidance behavior, and pain-related nerve fiber activity. Physiol Behav 62, 849-855.
17. Langen B & Dost R (2011). Comparison of SHR, WKY and Wistar rats in different behavioural animal models: effect of dopamine D1 and alpha2 agonists. Atten Defic Hyperact Disord 3, 1-12.
18. Lübcke R & Barbezat GO (1988). Intestinal ion transport in rats with spontaneous arterial hypertension. Clin Sci (Lond) 75, 127-133.
19. McCall RD, Haskill S, Zimmermann EM, Lund PK, Thompson RC & Sartor RB (1994). Tissue interleukin 1 and interleukin-1 receptor antagonist expression in enterocolitis in resistant and susceptible rats. Gastroenterology 106, 960-972.
20. Mayer EA, Bradesi S, Chang L, Spiegel BM, Bueller JA & Naliboff BD (2008). Functional GI disorders: from animal models to drug development. Gut 57, 384-404.
21. Mayer EA, Naliboff BD, Chang L & Coutinho SV (2001). V. Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 280, G519-G524.
22. Miller MM, Morrison JH & McEwen BS (2012). Basal anxiety-like behavior predicts differences in dendritic morphology in the medial prefrontal cortex in two strains of rats. Behav Brain Res 229, 280-288.
23. 2B receptors modulate visceral hypersensitivity in a stress-sensitive animal model of brain-gut axis dysfunction. Neurogastroenterol Motil 22, 573-578, e124.
24. O'Malley D, Cryan JF & Dinan TG (2013). Crosstalk between interleukin-6 and corticotropin-releasing factor modulate submucosal plexus activity and colonic secretion. Brain Behav Immun 30, 115-124.
25. O'Malley D, Dinan TG & Cryan JF (2012). Interleukin-6 modulates colonic transepithelial ion transport in the stress-sensitive Wistar Kyoto rat. Front Pharmacol 3, 190.
26. O'Malley D, Julio-Pieper M, Gibney SM, Dinan TG & Cryan JF (2010a). Distinct alterations in colonic morphology and physiology in two rat models of enhanced stress-induced anxiety- and depression-like behavior. Stress 13, 114-122.
27. O'Malley D, Julio-Pieper M, Gibney SM, Gosselin RD, Dinan TG & Cryan JF (2010b). Differential stress-induced alterations of colonic corticotropin-releasing factor receptors in the Wistar Kyoto rat. Neurogastroenterol Motil 22, 301-311.
28. O'Malley D, Liston M, Hyland NP, Dinan TG & Cryan JF (2011a). 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 300, G241-G252.
29. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF & Dinan TG (2009). Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65, 263-267.
30. O'Mahony SM, Tramullas M, Fitzgerald P & Cryan JF (2012). Rodent models of colorectal distension. Curr Protoc Neurosci Chapter 9, Unit 9.40.
31. O'Malley D, Quigley EM, Dinan TG & Cryan JF (2011b). Do interactions between stress and immune responses lead to symptom exacerbations in irritable bowel syndrome? Brain Behav Immun 25, 1333-1341.
32. Pare WP (1992). The performance of WKY rats on three tests of emotional behavior. Physiol Behav 51, 1051-1056.
33. Pemberton AD, Knight PA, Gamble J, Colledge WH, Lee JK, Pierce M & Miller HR (2004a). Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. J Immunol 173, 1894-1901.
34. Pemberton AD, Knight PA, Wright SH & Miller HR (2004b). Proteomic analysis of mouse jejunal epithelium and its response to infection with the intestinal nematode, Trichinella spiralis. Proteomics 4, 1101-1108.
35. Quigley EM (2006). Changing face of irritable bowel syndrome. World J Gastroenterol 12, 1-5.
36. Quigley EM, Abdel-Hamid H, Barbara G, Bhatia SJ, Boeckxstaens G, De Giorgio R, Delvaux M, Drossman DA, Foxx-Orenstein AE, Guarner F, Gwee KA, Harris LA, Hungin AP, Hunt RH, Kellow JE, Khalif IL, Kruis W, Lindberg G, Olano C, Moraes-Filho JP, Schiller LR, Schmulson M, Simrén M & Tzeuton C (2012). A global perspective on irritable bowel syndrome: a consensus statement of the World Gastroenterology Organisation Summit Task Force on irritable bowel syndrome. J Clin Gastroenterol 46, 356-366.
37. Ramos A, Berton O, Mormède P & Chaouloff F (1997). A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85, 57-69.
38. Ringel Y & Drossman DA (2001). Psychosocial aspects of Crohn's disease. Surg Clin North Am 81, 231-252, x.
39. Saito YA & Talley NJ (2008). Genetics of irritable bowel syndrome. Am J Gastroenterol 103, 2100-2104; quiz 2105.
40. Shepard JD & Myers DA (2008). Strain differences in anxiety-like behavior: association with corticotropin-releasing factor. Behav Brain Res 186, 239-245.
41. Shichijo K, Gottfried M, Sekine I & Pappas TN (2000). Dextran sulfate sodium-induced colitis in immunodeficient rats. Dig Dis Sci 45, 2320-2326.
42. Spiller R (2006). How inflammation changes neuromuscular function and its relevance to symptoms in diverticular disease. J Clin Gastroenterol 40 Suppl 3, S117-S120.