Communication between gastrointestinal bacteria and the nervous system

Current Opinion in Pharmacology

Volumn 12, Issue 6, 2012, Pages 667-672

  Bravo, Javier A ^a   Julio Pieper, Marcela ^a   Forsythe, Paul ^b,c   Kunze, Wolfgang ^c   Dinan, Timothy G ^e,f   Bienenstock, John ^b,d   Cryan, John F ^e,f  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE VALPARAÍSO   (Chile)

^b MCMASTER UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY COLLEGE CORK   (Ireland)

^f UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACITRACIN; NATAMYCIN; NEOMYCIN; PROBIOTIC AGENT;

ANXIETY; ARTICLE; BIFIDOBACTERIUM LONGUM; BIFIDOBACTERIUM LONGUM INFANTIS; CENTRAL NERVOUS SYSTEM; DEPRESSION; DIGESTIVE SYSTEM FUNCTION DISORDER; DRUG MECHANISM; GASTROINTESTINAL TRACT FUNCTION; HEPATIC ENCEPHALOPATHY; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOMODULATION; INTESTINE FLORA; IRRITABLE COLON; LACTOBACILLUS RHAMNOSUS; MENTAL DISEASE; MENTAL STRESS; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL;

EID: 84870548338     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2012.09.010     Document Type: Review

References (52)

1. E.A. Mayer Gut feelings: the emerging biology of gut-brain communication Nat Rev Neurosci 12 2011 453 466
2. S.M. Collins, E. Denou, E.F. Verdu, and P. Bercik The putative role of the intestinal microbiota in the irritable bowel syndrome Dig Liver Dis 41 2009 850 853
3. J. Cryan, and S. O'Mahony The microbiome-gut-brain axis: from bowel to behaviour Neurogastroenterol Motil 23 2010 187 192
4. S.H. Rhee, C. Pothoulakis, and E.A. Mayer Principles and clinical implications of the brain-gut-enteric microbiota axis Nat Rev Gastroenterol Hepatol 6 2009 306 314
5. J.A. Bravo, P. Forsythe, M.V. Chew, E. Escaravage, H.M. Savignac, T.G. Dinan, J. Bienenstock, and J.F. Cryan Ingestion of lactobacillus strain regulates emotional behavior and central gaba receptor expression in a mouse via the vagus nerve Proc Natl Acad Sci USA 108 2011 16050 16055
6. E.M. Quigley Probiotics in functional gastrointestinal disorders: what are the facts? Curr Opin Pharmacol 8 2008 704 708
7. G. Clarke, J.F. Cryan, T.G. Dinan, and E.M. Quigley Review article: probiotics for the treatment of irritable bowel syndrome - focus on lactic acid bacteria Aliment Pharmacol Ther 35 2012 403 413
8. G.D. Abrams, H. Bauer, and H. Sprinz Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice Lab Invest 12 1963 355 364
9. H.A. Gordon, and E. Bruckner-Kardoss Effect of normal microbial flora on intestinal surface area Am J Physiol 201 1961 175 178
10. S. Grenham, G. Clarke, J.F. Cryan, and T.G. Dinan Brain-gut-microbe communication in health and disease Front Physiol 2 2011 94
11. Y. Umesaki, Y. Okada, S. Matsumoto, A. Imaoka, and H. Setoyama Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce mhc class ii molecules and fucosyl asialo gm1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse Microbiol Immunol 39 1995 555 562
12. J.K. Marshall, M. Thabane, A.X. Garg, W. Clark, J. Meddings, and S.M. Collins Intestinal permeability in patients with irritable bowel syndrome after a waterborne outbreak of acute gastroenteritis in Walkerton, Ontario Aliment Pharmacol Ther 20 2004 1317 1322
13. S.M. O'Mahony, N.P. Hyland, T.G. Dinan, and J.F. Cryan Maternal separation as a model of brain-gut axis dysfunction Psychopharmacology (Berl) 214 2011 71 88
14. N.M. Bass Review article: the current pharmacological therapies for hepatic encephalopathy Aliment Pharmacol Ther 25 Suppl. 1 2007 23 31
15. B.L. Williams, M. Hornig, T. Buie, M.L. Bauman, M. Cho Paik, I. Wick, A. Bennett, O. Jabado, D.L. Hirschberg, and W.I. Lipkin Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances PLoS ONE 6 2011 e24585
16. J.B. Adams, L.J. Johansen, L.D. Powell, D. Quig, and R.A. Rubin Gastrointestinal flora and gastrointestinal status in children with autism - comparisons to typical children and correlation with autism severity BMC Gastroenterol 11 2011 22
17. S.M. Finegold, D. Molitoris, Y. Song, C. Liu, M.L. Vaisanen, E. Bolte, M. McTeague, R. Sandler, H. Wexler, and E.M. Marlowe Gastrointestinal microflora studies in late-onset autism Clin Infect Dis 35 2002 S6 S16
18. J.A. Bravo, T.G. Dinan, and J.F. Cryan Alterations in the central crf system of two different rat models of comorbid depression and functional gastrointestinal disorders Int J Neuropsychopharmacol 14 2010 666 683
19. D. O'Malley, T.G. Dinan, and J.F. Cryan Neonatal maternal separation in the rat impacts on the stress responsivity of central corticotropin-releasing factor receptors in adulthood Psychopharmacology (Berl) 214 2011 221 229
20. S.M. O'Mahony, J.R. Marchesi, P. Scully, C. Codling, A.M. Ceolho, E.M. Quigley, J.F. Cryan, and T.G. Dinan Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses Biol Psychiatry 65 2009 263 267
21. L.E. Goehler, S.M. Park, N. Opitz, M. Lyte, and R.P. Gaykema Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior Brain Behav Immun 22 2008 354 366
22. M. Lyte, W. Li, N. Opitz, R.P. Gaykema, and L.E. Goehler Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia citrobacter rodentium Physiol Behav 89 2006 350 357
23. M.G. Gareau, E. Wine, D.M. Rodrigues, J.H. Cho, M.T. Whary, D.J. Philpott, G. Macqueen, and P.M. Sherman Bacterial infection causes stress-induced memory dysfunction in mice Gut 60 2011 307 317
24. N. Sudo, Y. Chida, Y. Aiba, J. Sonoda, N. Oyama, X.N. Yu, C. Kubo, and Y. Koga Postnatal microbial colonization programs the hypothalamic-pituitary- adrenal system for stress response in mice J Physiol 558 2004 263 275
25. K.M. Neufeld, N. Kang, J. Bienenstock, and J.A. Foster Reduced anxiety-like behavior and central neurochemical change in germ-free mice Neurogastroenterol Motil 23 2011 255 264
26. R.D. Heijtz, S. Wang, F. Anuar, Y. Qian, B. Bjorkholm, A. Samuelsson, M.L. Hibberd, H. Forssberg, and Pettersson S Normal gut microbiota modulates brain development and behavior Proc Natl Acad Sci USA 108 2011 3047 3052
27. P. Bercik, S.M. Collins, and E.F. Verdu Microbes and the gut-brain axis Neurogastroenterol Motil 2012
28. P. Bercik, E. Denou, J. Collins, W. Jackson, J. Lu, J. Jury, Y. Deng, P. Blennerhassett, J. Macri, and K.D. McCoy The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice Gastroenterology 141 2011 599 609 609 e591-593
29. W. Li, S.E. Dowd, B. Scurlock, V. Acosta-Martinez, and M. Lyte Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria Physiol Behav 96 2009 557 567
30. P.J. Whorwell, L. Altringer, J. Morel, Y. Bond, D. Charbonneau, L. O'Mahony, B. Kiely, F. Shanahan, and E.M. Quigley Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome Am J Gastroenterol 101 2006 1581 1590
31. L. O'Mahony, J. McCarthy, P. Kelly, G. Hurley, F. Luo, K. Chen, G.C. O'Sullivan, B. Kiely, J.K. Collins, and F. Shanahan Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles Gastroenterology 128 2005 541 551
32. M.C. Collado, E. Isolauri, and S. Salminen Specific probiotic strains and their combinations counteract adhesion of enterobacter sakazakii to intestinal mucus FEMS Microbiol Lett 285 2008 58 64
33. F.P. Martin, N. Sprenger, I. Montoliu, S. Rezzi, S. Kochhar, and J.K. Nicholson Dietary modulation of gut functional ecology studied by fecal metabonomics J Proteome Res 9 2010 5284 5295
34. S.C. Corr, Y. Li, C.U. Riedel, P.W. O'Toole, C. Hill, and C.G. Gahan Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius ucc118 Proc Natl Acad Sci USA 104 2007 7617 7621
35. S.V. Generoso, M. Viana, R. Santos, F.S. Martins, J.A. Machado, R.M. Arantes, J.R. Nicoli, M.I. Correia, and V.N. Cardoso Saccharomyces cerevisiae strain ufmg 905 protects against bacterial translocation, preserves gut barrier integrity and stimulates the immune system in a murine intestinal obstruction model Arch Microbiol 192 2010 477 484
36. Z. Liu, Y. Ma, and H. Qin Potential prevention and treatment of intestinal barrier dysfunction using active components of lactobacillus Ann Surg 254 2011 832 833 [author reply 833]
37. W.A. Kunze, Y.K. Mao, B. Wang, J.D. Huizinga, X. Ma, P. Forsythe, and J. Bienenstock Lactobacillus reuteri enhances excitability of colonic ah neurons by inhibiting calcium-dependent potassium channel opening J Cell Mol Med 13 2009 2261 2270
38. C. Rousseaux, X. Thuru, A. Gelot, N. Barnich, C. Neut, L. Dubuquoy, C. Dubuquoy, E. Merour, K. Geboes, and M. Chamaillard Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors Nat Med 13 2007 35 37
39. M.E. Sanders Impact of probiotics on colonizing microbiota of the gut J Clin Gastroenterol 45 Suppl. 2011 S115 S119
40. D. Guyonnet, O. Chassany, P. Ducrotte, C. Picard, M. Mouret, C.H. Mercier, and C. Matuchansky Effect of a fermented milk containing bifidobacterium animalis dn-173 010 on the health-related quality of life and symptoms in irritable bowel syndrome in adults in primary care: a multicentre, randomized, double-blind, controlled trial Aliment Pharmacol Ther 26 2007 475 486
41. E.F. Verdu, P. Bercik, M. Verma-Gandhu, X.X. Huang, P. Blennerhassett, W. Jackson, Y. Mao, L. Wang, F. Rochat, and S.M. Collins Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice Gut 55 2006 182 190
42. D.P. McKernan, P. Fitzgerald, T.G. Dinan, and J.F. Cryan The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat Neurogastroenterol Motil 22 2010 1029 1035 e1268
43. T. Kamiya, L. Wang, P. Forsythe, G. Goettsche, Y. Mao, Y. Wang, G. Tougas, and J. Bienenstock Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats Gut 55 2006 191 196
44. P. Bercik, E.F. Verdu, J.A. Foster, J. Macri, M. Potter, X. Huang, P. Malinowski, W. Jackson, P. Blennerhassett, and K.A. Neufeld Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice Gastroenterology 139 2010 2102 2112 e2101
45. P. Bercik, A.J. Park, D. Sinclair, A. Khoshdel, J. Lu, X. Huang, Y. Deng, P.A. Blennerhassett, M. Fahnestock, and D. Moine The anxiolytic effect of Bifidobacterium longum ncc3001 involves vagal pathways for gut-brain communication Neurogastroenterol Motil 23 2011 1132 1139
46. L. Desbonnet, L. Garrett, G. Clarke, B. Kiely, J.F. Cryan, and T.G. Dinan Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression Neuroscience 2010
47. D. Ma, P. Forsythe, and J. Bienenstock Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression Infect Immun 72 2004 5308 5314
48. K. Karimi, M.D. Inman, J. Bienenstock, and P. Forsythe Lactobacillus reuteri-induced regulatory t cells protect against an allergic airway response in mice Am J Respir Crit Care Med 179 2009 186 193
49. S.C. Duncker, T. Kamiya, L. Wang, P. Yang, and J. Bienenstock Probiotic Lactobacillus reuteri alleviates the response to gastric distension in rats J Nutr 141 2011 1813 1818
50. X. Ma, Y.K. Mao, B. Wang, J.D. Huizinga, J. Bienenstock, and W. Kunze Lactobacillus reuteri ingestion prevents hyperexcitability of colonic drg neurons induced by noxious stimuli Am J Physiol Gastrointest Liver Physiol 296 2009 G868 G875
51. B. Wang, Y.K. Mao, C. Diorio, M. Pasyk, R.Y. Wu, J. Bienenstock, and W.A. Kunze Luminal administration ex vivo of a live lactobacillus species moderates mouse jejunal motility within minutes FASEB J 24 2010 4078 4088
52. M. Messaoudi, R. Lalonde, N. Violle, H. Javelot, D. Desor, A. Nejdi, J.F. Bisson, C. Rougeot, M. Pichelin, and M. Cazaubiel Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus r0052 and Bifidobacterium longum r0175) in rats and human subjects Br J Nutr 105 2011 755 764