Concurrent psychological stress and infectious colitis is key to sustaining enhanced peripheral sensory signaling

Neurogastroenterology and Motility

Volumn 27, Issue 3, 2015, Pages 347-355

  Spreadbury, I ^a   Ochoa Cortes, F ^a   Ibeakanma, C ^a   Martin, N ^a   Hurlbut, D ^a   Vanner, S J ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Citrobacter rodentium; Dorsal root ganglia; IBS; Nociceptor; Psychological stress; Water avoidance stress

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL ISOLATION; CHRONIC STRESS; CITROBACTER RODENTIUM; COLITIS; CONTROLLED STUDY; CONVALESCENCE; CYTOKINE PRODUCTION; EXPERIMENTAL BEHAVIORAL TEST; HISTOPATHOLOGY; INFECTIOUS COLITIS; IRRITABLE COLON; MALE; MENTAL STRESS; MOUSE; NERVE CELL CULTURE; NERVE CELL EXCITABILITY; NOCICEPTION; NONHUMAN; PATCH CLAMP TECHNIQUE; PATHOGENESIS; POSTINFECTIOUS IRRITABLE BOWEL SYNDROME; PRIORITY JOURNAL; SPINAL GANGLION; VISCERAL PAIN; WATER AVOIDANCE STRESS TEST; ANIMAL; C57BL MOUSE; CELL CULTURE; COMPLICATION; ENTEROBACTERIACEAE INFECTION; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; CITROBACTER RODENTIUM; COLITIS; CYTOKINES; ENTEROBACTERIACEAE INFECTIONS; GANGLIA, SPINAL; MALE; MICE; MICE, INBRED C57BL; NEURONS; STRESS, PSYCHOLOGICAL;

EID: 84923221264     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12497     Document Type: Article

References (35)

1. Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther 2007; 26: 535-44.
2. Marshall JK, Thabane M, Garg AX, Clark WF, Moayyedi P, Collins SM. Eight year prognosis of postinfectious irritable bowel syndrome following waterborne bacterial dysentery. Gut 2010; 59: 605-11.
3. Spence MJ, Moss-Morris R. The cognitive behavioural model of irritable bowel syndrome: a prospective investigation of patients with gastroenteritis. Gut 2007; 56: 1066-71.
4. Luperchio SA, Newman JV, Dangler CA, Schrenzel MD, Brenner DJ, Steigerwalt AG, Schauer DB. Citrobacter rodentium, the causative agent of transmissible murine colonic hyperplasia, exhibits clonality: synonymy of C. rodentium and mouse-pathogenic Escherichia coli. J Clin Microbiol 2000; 38: 4343-50.
5. Ibeakanma C, Miranda-Morales M, Richards M, Bautista-Cruz F, Martin N, Hurlbut D, Vanner S. Citrobacter rodentium colitis evokes post-infectious hyperexcitability of mouse nociceptive colonic dorsal root ganglion neurons. J Physiol 2009; 587: 3505-21.
6. Ibeakanma C, Ochoa-Cortes F, Miranda-Morales M, McDonald T, Spreadbury I, Cenac N, Cattaruzza F, Hurlbut D et al. Brain-gut interactions increase peripheral nociceptive signaling in mice with postinfectious irritable bowel syndrome. Gastroenterology 2011; 141: 2098-108.
7. Hong S, Zheng G, Wu X, Snider NT, Owyang C, Wiley JW. Corticosterone mediates reciprocal changes in CB 1 and TRPV1 receptors in primary sensory neurons in the chronically stressed rat. Gastroenterology 2011; 140: 627-37.
8. Kiliaan AJ, Saunders PR, Bijlsma PB, Berin MC, Taminiau JA, Groot JA, Perdue MH. Stress stimulates transepithelial macromolecular uptake in rat jejunum. Am J Physiol 1998; 275: G1037-44.
9. Santos J, Saunders PR, Hanssen NP, Yang PC, Yates D, Groot JA, Perdue MH. Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat. Am J Physiol 1999; 277: G391-9.
10. Santos J, Yang PC, Soderholm JD, Benjamin M, Perdue MH. Role of mast cells in chronic stress induced colonic epithelial barrier dysfunction in the rat. Gut 2001; 48: 630-6.
11. Saunders PR, Kosecka U, McKay DM, Perdue MH. Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine. Am J Physiol 1994; 267: G794-9.
12. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 2010; 78: 1509-19.
13. Hart A, Kamm MA. Review article: mechanisms of initiation and perpetuation of gut inflammation by stress. Aliment Pharmacol Ther 2002; 16: 2017-28.
14. Beyak MJ, Ramji N, Krol KM, Kawaja MD, Vanner SJ. Two TTX-resistant Na+ currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol 2004; 287: G845-55.
15. Valdez-Morales E, Guerrero-Alba R, Ochoa-Cortes F, Benson J, Spreadbury I, Hurlbut D, Miranda-Morales M, Lomax AE et al. Release of endogenous opioids during a chronic IBD model suppresses the excitability of colonic DRG neurons. Neurogastroenterol Motil 2013; 25: 39-46.
16. Dunlop SP, Jenkins D, Neal KR, Spiller RC. Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology 2003; 125: 1651-9.
17. Gwee KA, Graham JC, McKendrick MW, Collins SM, Marshall JS, Walters SJ, Read NW. Psychometric scores and persistence of irritable bowel after infectious diarrhoea. Lancet 1996; 347: 150-3.
18. Gwee KA, Leong YL, Graham C, McKendrick MW, Collins SM, Walters SJ, Underwood JE, Read NW. The role of psychological and biological factors in postinfective gut dysfunction. Gut 1999; 44: 400-6.
19. Bhatia V, Tandon RK. Stress and the gastrointestinal tract. J Gastroenterol Hepatol 2005; 20: 332-9.
20. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. Citrobacter rodentium of mice and man. Cell Microbiol 2005; 7: 1697-706.
21. Petty NK, Bulgin R, Crepin VF, Cerdeno-Tarraga AM, Schroeder GN, Quail MA, Lennard N, Corton C et al. The Citrobacter rodentium genome sequence reveals convergent evolution with human pathogenic Escherichia coli. J Bacteriol 2010; 192: 525-38.
22. Valdez-Morales EE, Overington J, Guerrero-Alba R, Ochoa-Cortes F, Ibeakanma CO, Spreadbury I, Bunnett NW, Beyak M et al. Sensitization of peripheral sensory nerves by mediators from colonic biopsies of diarrhea-predominant irritable bowel syndrome patients: a role for PAR2. Am J Gastroenterol 2013; 108: 1634-43.
23. Ochoa-Cortes F, Guerrero-Alba R, Valdez-Morales EE, Spreadbury I, Barajas-Lopez C, Castro M, Bertrand J, Cenac N et al. Chronic stress mediators act synergistically on colonic nociceptive mouse dorsal root ganglia neurons to increase excitability. Neurogastroenterol Motil 2014; 26: 334-45.
24. Gareau MG, Wine E, Rodrigues DM, Cho JH, Whary MT, Philpott DJ, Macqueen G, Sherman PM. Bacterial infection causes stress-induced memory dysfunction in mice. Gut 2011; 60: 307-17.
25. Higgins LM, Frankel G, Douce G, Dougan G, MacDonald TT. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect Immun 1999; 67: 3031-9.
26. Elenkov IJ, Chrousos GP. Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann N Y Acad Sci 2002; 966: 290-303.
27. Glaser R, Kiecolt-Glaser JK, Marucha PT, MacCallum RC, Laskowski BF, Malarkey WB. Stress-related changes in proinflammatory cytokine production in wounds. Arch Gen Psychiatry 1999; 56: 450-6.
28. Chen J, Winston JH, Sarna SK. Neurological and cellular regulation of visceral hypersensitivity induced by chronic stress and colonic inflammation in rats. Neuroscience 2013; 248C: 469-78.
29. + T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect Immun 2003; 71: 5077-86.
30. Simmons CP, Goncalves NS, Ghaem-Maghami M, Bajaj-Elliott M, Clare S, Neves B, Frankel G, Dougan G et al. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-gamma. J Immunol 2002; 168: 1804-12.
31. Skinn AC, Vergnolle N, Zamuner SR, Wallace JL, Cellars L, MacNaughton WK, Sherman PM. Citrobacter rodentium infection causes iNOS-independent intestinal epithelial dysfunction in mice. Can J Physiol Pharmacol 2006; 84: 1301-12.
32. Lyte M, Li W, Opitz N, Gaykema RP, Goehler LE. Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav 2006; 89: 350-7.
33. Diaz HR, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, Hibberd ML, Forssberg H et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108: 3047-52.
34. Dinan TG, Cryan JF. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012; 37: 1369-78.
35. Matsumoto M, Kibe R, Ooga T, Aiba Y, Sawaki E, Koga Y, Benno Y. Cerebral low-molecular metabolites influenced by intestinal microbiota: a pilot study. Front Syst Neurosci 2013; 7: 9.