Bifidobacterium longum and Lactobacillus helveticus synergistically suppress stress-related visceral hypersensitivity through hypothalamic-pituitary-adrenal axis modulation

Journal of Neurogastroenterology and Motility

Volumn 24, Issue 1, 2018, Pages 138-146

  Ait Belgnaoui, Afifa ^a,b   Payard, Isabelle ^a   Rolland, Claire ^b   Harkat, Cherryl ^a   Braniste, Viorica ^c   Théodorou, Vassillia ^a   Tompkins, Thomas A ^b  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^b LALLEMAND SAS   (France)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Chronic stress; Glucocorticoid receptors; Probiotics; Visceral pain

Indexed keywords

GLUCOCORTICOID RECEPTOR; MESSENGER RNA; PROBIOTIC AGENT; STRESS HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIFIDOBACTERIUM LONGUM; CHRONIC STRESS; CONTROLLED STUDY; GENE EXPRESSION; HIPPOCAMPUS; HORMONE BLOOD LEVEL; HYPERSENSITIVITY; HYPOTHALAMUS; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INTESTINE DISTENSION; LACTOBACILLUS HELVETICUS; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; VISCERAL PAIN;

EID: 85039935670     PISSN: 20930879     EISSN: 20930887     Source Type: Journal    
DOI: 10.5056/jnm16167     Document Type: Article

References (53)

1. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clinical Epidemiol 2014;6:71-80
2. Chey WD, Kurlander J, Eswaran S. Irritable bowel syndrome: a clinical review. JAMA 2015;313:949-958
3. Whitehead WE, Crowell MD, Robinson JC, Heller BR, Schuster MM. Effects of stressful life events on bowel symptoms: subjects with irritable bowel syndrome compared with subjects without bowel dysfunction. Gut 1992;33:825-830
4. Moloney RD, O'Mahony SM, Dinan TG, Cryan JF. Stress-induced visceral pain: toward animal models of irritable-bowel syndrome and associated comorbidities. Frontiers Psychiatry 2015;6:15
5. Thijssen AY, Jonkers DM, Leue C, et al. Dysfunctional cognitions, anxiety and depression in irritable bowel syndrome. J Clin Gastroenterol 2010;44:e236-e241
6. Pacák K, Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001;22:502-548
7. Watts AG. Glucocorticoid regulation of peptide genes in neuroendocrine CRH neurons: a complexity beyond negative feedback. Front Neuroendocrinol 2005;26:109-130
8. Harris AP, Holmes MC, de Kloet ER, Chapman KE, Seckl JR. Mineralocorticoid and glucocorticoid receptor balance in control of HPA axis and behaviour. Psychoneuroendocrinology 2013;38:648-658
9. Mizoguchi K, Ishige A, Aburada M, Tabira T. Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 2003;119:887-897
10. Johnson AC, Tran L, Schulkin J, Greenwood-Van Meerveld B. Importance of stress receptor-mediated mechanisms in the amygdala on visceral pain perception in an intrinsically anxious rat. Neurogastroenterol Motil 2012;24:479-486, e219
11. Dinan TG, Cryan JF. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012;37:1369-1378
12. Jeffery IB, O'Toole PW, öhman L, et al. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut 2012;61:997-1006
13. Rajilic-Stojanovic M, Biagi E, Heilig HG, et al. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology 2011;141:1792-1801
14. Tap J, Derrien M, Törnblom H, et al. Identification of an intestinal microbiota signature associated with severity of irritable bowel syndrome. Gastroenterology 2017;152:111-123, e8
15. Crouzet L, Gaultier E, Del'Homme C, et al. The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil 2013;25:e272-e282
16. Vrieze A, Van Nood E, Holleman F, et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012;143:913-916, e7
17. Suskind DL, Brittnacher MJ, Wahbeh G, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn's disease. Inflamm Bowel Dis 2015;21:556-563
18. Pinn DM, Aroniadis OC, Brandt LJ. Is fecal microbiota transplantation the answer for irritable bowel syndrome? A single-center experience. Am J Gastroenterol 2014;109:1831-1832
19. Mazurak N, Broelz E, Storr M, Enck P. Probiotic therapy of the irritable bowel syndrome: why is the evidence still poor and what can be done about it? J Neurogastroenterol Motil 2015;21:471-485
20. Sisson G, Ayis S, Sherwood RA, Bjarnason I. Randomised clinical trial: a liquid multi-strain probiotic vs. placebo in the irritable bowel syndrome-a 12 week double-blind study. Aliment Pharmacol Ther 2014;40:51-62
21. Kamiya T, Wang L, Forsythe P, et al. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 2006;55:191-196
22. Ma X, Mao YK, Wang B, Huizinga JD, Bienenstock J, Kunze W. Lactobacillus reuteri ingestion prevents hyperexcitability of colonic DRG neurons induced by noxious stimuli. Am J Physiol Gastrointest Liver 2009;296:G868-G875
23. McKernan DP, Fitzgerald P, Dinan TG, Cryan JF. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil 2010;22:1029-1035, e268
24. Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH. Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 2007;56:1522-1528
25. Ait-Belgnaoui A, Colom A, Braniste V, et al. Probiotic gut effect prevents the chronic psychological stress-induced brain activity abnormality in mice. Neurogastroenterol Motil 2014;26:510-520
26. Zheng G, Wu SP, Hu Y, Smith DE, Wiley JW, Hong S. Corticosterone mediates stress-related increased intestinal permeability in a region-specific manner. Neurogastroenterol Motil 2013;25:e127-e139
27. Zheng G, Hong S, Hayes JM, Wiley JW. Chronic stress and peripheral pain: evidence for distinct, region-specific changes in visceral and somatosensory pain regulatory pathways. Exp Neurol 2015;273:301-311
28. Fourie NH, Wang D, Abey SK, et al. Structural and functional alterations in the colonic microbiome of the rat in a model of stress induced irritable bowel syndrome. Gut microbes 2017;8:33-45
29. Annaházi A, Dabek M, Gecse K, et al. Proteinase-activated receptor-4 evoked colorectal analgesia in mice: an endogenously activated feed-back loop in visceral inflammatory pain. Neurogastroenterol Motil 2012;24:76-85, e13
30. Moloney RD, Desbonnet L, Clarke G, Dinan TG, Cryan JF. The microbiome: stress, health and disease. Mamm Genome 2014;25:49-74
31. Grenham S, Clarke G, Cryan JF, Dinan TG. Brain-gut-microbe communication in health and disease. Front Physiol 2011;2:94
32. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012;10:735-742
33. Borre YE, Moloney RD, Clarke G, Dinan TG, Cryan JF. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Adv Exp Med Biol 2014;817:373-403
34. Luczynski P, McVey Neufeld KA, Oriach CS, Clarke G, Dinan TG, Cryan JF. Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior. Int J Neuropsychopharmacol 2016;19:pyw020
35. Braniste V, Al-Asmakh M, Kowal C, et al. The gut microbiota influences blood-brain barrier permeability in mice. Science Transl Med 2014;6:263ra158
36. O'Mahony SM, Felice VD, Nally K, et al. Disturbance of the gut microbiota in early-life selectively affects visceral pain in adulthood without impacting cognitive or anxiety-related behaviors in male rats. Neuroscience 2014;277:885-901
37. Saggioro A. Probiotics in the treatment of irritable bowel syndrome. J Clin Gastroenterol 2004;38(6 suppl):S104-S106
38. Kim HJ, Camilleri M, McKinzie S, et al. A randomized controlled trial of a probiotic, VSL#3, on gut transit and symptoms in diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther 2003;17:895-904
39. Kim HJ, Vazquez Roque MI, Camilleri M, et al. A randomized controlled trial of a probiotic combination VSL# 3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil 2005;17:687-696
40. Ohland CL, Kish L, Bell H, et al. Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology 2013;38:1738-1747
41. Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol 2007;9:356-367
42. Savignac HM, Tramullas M, Kiely B, Dinan TG, Cryan JF. Bifidobacteria modulate cognitive processes in an anxious mouse strain. Behav Brain Res 2015;287:59-72
43. Savignac HM, Kiely B, Dinan TG, Cryan JF. Bifidobacteria exert strain-specific effects on stress-related behavior and physiology in BALB/c mice. Neurogastroenterol Motil 2014;26:1615-1627
44. Videlock EJ, Shih W, Adeyemo M, et al. The effect of sex and irritable bowel syndrome on HPA axis response and peripheral glucocorticoid receptor expression. Psychoneuroendocrinology 2016;69:67-76
45. Zhang G, Zhao BX, Hua R, et al. Hippocampal microglial activation and glucocorticoid receptor down-regulation precipitate visceral hypersensitivity induced by colorectal distension in rats. Neuropharmacology 2016;102:295-303
46. Prusator DK, Greenwood-Van Meerveld B. Amygdala-mediated mechanisms regulate visceral hypersensitivity in adult females following early life stress: importance of the glucocorticoid receptor and corticotropin-releasing factor. Pain 2017;158:296-305
47. Wouters MM, Van Wanrooy S, Casteels C, et al. Altered brain activation to colorectal distention in visceral hypersensitive maternal-separated rats. Neurogastroenterol Motil 2012;24:678-685, e297
48. Moussaoui N, Braniste V, Ait-Belgnaoui A, et al. Changes in intestinal glucocorticoid sensitivity in early life shape the risk of epithelial barrier defect in maternal-deprived rats. PLoS One 2014;9:e88382
49. Barreau F, Cartier C, Ferrier L, Fioramonti J, Bueno L. Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology 2004;127:524-534
50. Sandrini S, Aldriwesh M, Alruways M, Freestone P. Microbial endocrinology: host-bacteria communication within the gut microbiome. J Endocrinol 2015;225:R21-R34
51. Hegde M, Wood TK, Jayaraman A. The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Applied microbiology and biotechnology 2009;84:763-776
52. Karavolos MH, Winzer K, Williams P, Khan CM. Pathogen espionage: multiple bacterial adrenergic sensors eavesdrop on host communication systems. Mol Microbiol 2013;87:455-465
53. Beury-Cirou A, Tannières M, Minard C, et al. At a supra-physiological concentration, human sexual hormones act as quorum-sensing inhibitors. PLoS One 2013;8:e83564