Luminal administration ex vivo of a live Lactobacillus species moderates mouse jejunal motility within minutes

FASEB Journal

Volumn 24, Issue 10, 2010, Pages 4078-4088

  Wang, Bingxian ^a,b   Mao, Yu Kang ^a   Diorio, Caroline ^a   Pasyk, Michael ^a   Wu, Richard You ^a   Bienenstock, John ^a,b   Kunze, Wolfgang A ^a,b  

^a McMaster Brain Body Institute   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Enteric nervous system; Probiotics; Small intestine

Indexed keywords

PROBIOTIC AGENT;

ANIMAL EXPERIMENT; ARTICLE; IC 50; INTESTINE MOTILITY; JEJUNUM; LACTOBACILLUS REUTERI; LATENT PERIOD; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BAGG ALBINO MOUSE; GASTROINTESTINAL MOTILITY; LACTOBACILLUS; PHYSIOLOGY;

LACTOBACILLUS; LACTOBACILLUS REUTERI; LACTOBACILLUS SALIVARIUS;

ANIMALS; GASTROINTESTINAL MOTILITY; JEJUNUM; LACTOBACILLUS; MALE; MICE; MICE, INBRED BALB C; PROBIOTICS;

EID: 77957848189     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-153841     Document Type: Article

References (93)

1. Frank, D. N., and Pace, N. R. (2008) Gastrointestinal microbiology enters the metagenomics era. Curr. Opin. Gastroenterol. 24, 4-10
2. Kinross, J. M., von Roon, A. C., Holmes, E., Darzi, A., and Nicholson, J. K. (2008) The human gut microbiome: implications for future health care. Curr. Gastroenterol. Rep. 10, 396-403
3. O'Hara, A. M., and Shanahan, F. (2006) The gut flora as a forgotten organ. EMBO Rep. 7, 688-693
4. Walker, R., and Buckley, M. (2006) Probiotic Microbes: The Scientific Basis, American Academy of Microbiology, Washington, DC
5. Backhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., and Gordon, J. I. (2005) Host-bacterial mutualism in the human intestine. Science 307, 1915-1920
6. Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K., and Littman, D. R. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498
7. Umesaki, Y., Setoyama, H., Matsumoto, S., Imaoka, A., and Itoh, K. (1999) Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect. Immun. 67, 3504-3511
8. Talham, G. L., Jiang, H. Q., Bos, N. A., and Cebra, J. J. (1999) Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect. Immun. 67, 1992-2000
9. Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X. N., Kubo, C., and Koga, Y. (2004) Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J. Physiol. 558, 263-275 (Pubitemid 39077406)
10. Collins, S. M., and Bercik, P. (2009) The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 136, 2003-2014
11. Forsythe, P., Sudo, N., Dinan, T., Taylor, V. H., and Bienenstock, J. (2010) Mood and gut feelings. Brain Behav Immun 24, 9-16
12. Forsythe, P., and Bienenstock, J. (2008) Probiotics in Neurology and Psychiatry. Therapeutic Microbiology: Probiotics and Related Strategies (Versalovic, J., and Wilson, M., eds) pp. 285-298, ASM Press, Herndon, VA
13. Powley, T. L., Wang, X. Y., Fox, E. A., Phillips, R. J., Liu, L. W., and Huizinga, J. D. (2008) Ultrastructural evidence for communication between intramuscular vagal mechanoreceptors and interstitial cells of Cajal in the rat fundus. Neurogastroenterol. Motil. 20, 69-79
14. Mazzia, C., and Clerc, N. (1997) Ultrastructural relationships of spinal primary afferent fibres with neuronal and non-neuronal cells in the myenteric plexus of the cat oesophago-gastric junction. Neuroscience 80, 925-937 (Pubitemid 27334631)
15. Cervero, F., and Sharkey, K. A. (1988) An electrophysiological and anatomical study of intestinal afferent fibres in the rat. J. Physiol. 401, 381-397
16. Rong, W., Hillsley, K., Davis, J. B., Hicks, G., Winchester, W. J., and Grundy, D. (2004) Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. J. Physiol. 560, 867-881 (Pubitemid 39530124)
17. D'Souza, A. L., Rajkumar, C., Cooke, J., and Bulpitt, C. J. (2002) Probiotics in prevention of antibiotic associated diarrhoea: meta-analysis. Brit. Med. J. 324, 1361
18. Gionchetti, P., Rizzello, F., Lammers, K. M., Morselli, C., Sollazzi, L., Davies, S., Tambasco, R., Calabrese, C., and Campieri, M. (2006) Antibiotics and probiotics in treatment of inflammatory bowel disease. World J. Gastroenterol. 12, 3306-3313
19. Guarner, F., Khan, A., Garisch, J., Eliakim, R., Gangl, A., Thomson, A., Krabshuis, J., and Le Mair, T. (2008) World Gastroenterology Organisation Practice Guideline: Probiotics and prebiotics. http://www.worldgastroenterology. org/
20. Rousseaux, C., Thuru, X., Gelot, A., Barnich, N., Neut, C., Dubuquoy, L., Dubuquoy, C., Merour, E., Geboes, K., Chamaillard, M., Ouwehand, A., Leyer, G., Carcano, D., Colombel, J. F., Ardid, D., and Desreumaux, P. (2007) Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat. Med. 13, 35-37
21. Verdu, E. F., Bercik, P., Verma-Gandhu, M., Huang, X. X., Blennerhassett, P., Jackson, W., Mao, Y., Wang, L., Rochat, F., and Collins, S. M. (2006) Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 55, 182-190
22. Kamiya, T., Wang, L., Forsythe, P., Goettsche, G., Mao, Y., Wang, Y., Tougas, G., and Bienenstock, J. (2006) Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 55, 191-196 (Pubitemid 43117276)
23. Verdú, E. F., Bercík, P., Bergonzelli, G. E., Huang, X.-X., Blennerhasset, P., Rochat, F., Fiaux, M., Mansourian, R., Corthésy- Theulaz, I., and Collins, S. M. (2004) Lactobacillus paracasei normalizes muscle hypercontractility in a murine model of postinfective gut dysfunction. Gastroenterology 127, 826-837
24. O'Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., O'Sullivan, G. C., Kiely, B., Collins, J. K., Shanahan, F., and Quigley, E. M. (2005) Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128, 541-551
25. Tanida, M., Yamano, T., Maeda, K., Okumura, N., Fukushima, Y., and Nagai, K. (2005) Effects of intraduodenal injection of Lactobacillus johnsonii La1 on renal sympathetic nerve activity and blood pressure in urethane-anesthetized rats. Neurosci. Lett. 389, 109-114
26. Yamano, T., Tanida, M., Niijima, A., Maeda, K., Okumura, N., Fukushima, Y., and Nagai, K. (2006) Effects of the probiotic strain Lactobacillus johnsonii strain La1 on autonomic nerves and blood glucose in rats. Life Sci. 79, 1963-1967 (Pubitemid 44485122)
27. Kunze, W. A., Foster, J. A., Mao, Y., Ma, X. J., and Bienenstock, J. (2007) Lactobacillus Sp (LB) probiotic congestion by rats blocks memory in DRG neurons of repeated colorectal distensions. Poster presentation EE11, Annual Meeting of the Society for Neuroscience, San Diego, CA, USA
28. Kamm, K., Hoppe, S., Breves, G., Schroder, B., and Schemann, M. (2004) Effects of the probiotic yeast Saccharomyces boulardii on the neurochemistry of myenteric neurones in pig jejunum. Neurogastroenterol. Motil. 16, 53-60
29. Iyer, L. M., Aravind, L., Coon, S. L., Klein, D. C., and Koonin, E. V. (2004) Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role? Trends Genet. 20, 292-299
30. Kunze, W. A., Mao, Y. K., Wang, B., Huizinga, J. D., Ma, X., Forsythe, P., and Bienenstock, J. (2009) Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J. Cell. Mol. Med. 13, 2261-2270
31. Wang, B., Mao, Y. K., Diorio, C., Wang, L., Huizinga, J. D., Bienenstock, J., and Kunze, W. (2009) Lactobacillus reuteri ingestion and IK(Ca) channel blockade have similar effects on rat colon motility and myenteric neurones. Neurogastroenterol. Motil. 22, 98-107, e33
32. Mao, Y., Wang, B., and Kunze, W. (2006) Characterization of myenteric sensory neurons in the mouse small intestine. J. Neurophysiol. 96, 998-1010 (Pubitemid 44371496)
33. Siragusa, S., De Angelis, M., Di Cagno, R., Rizzello, C. G., Coda, R., and Gobbetti, M. (2007) Synthesis of γ-aminobutyric acid (GABA) by lactic acid bacteria isolated from Italian cheese varieties. Appl. Environ. Microbiol. 73, 7283-7290
34. Hayakawa, K., Kimura, M., Kasaha, K., Matsumoto, K., Sansawa, H., and Yamori, Y. (2004) Effect of a γ-aminobutyric acid-enriched dairy product on the blood pressure of spontaneously hypertensive and normotensive Wistar-Kyoto rats. Br. J. Nutr. 92, 411-417
35. Furness, J. B. (2006) The Enteric Nervous System, Blackwell Publishing, Hoboken, NJ, USA
36. Krantis, A. (2000) GABA in the mammalian enteric nervous system. News. Physiol. Sci. 15, 284-290
37. Ma, X., Mao, Y. K., Wang, B., Huizinga, J. D., Bienenstock, J., and Kunze, W. A. (2009) Lactobacillus reuteri ingestion prevents hyperexcitability of colonic DRG neurons induced by noxious stimuli. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G868-G875
38. Nguyen, T. V., Matsuyama, H., Baell, J., Hunne, B., Fowler, C. J., Smith, J. E., Nurgali, K., and Furness, J. B. (2007) Effects of compounds that influence IK (KCNN4) channels on afterhyperpolarizing potentials, and determination of IK channel sequence, in guinea pig enteric neurons. J. Neurophysiol. 97, 2024-2031
39. Krantis, A., and Harding, R. K. (1987) GABA-related actions in isolated in vitro preparations of the rat small intestine. Eur. J. Pharmacol. 141, 291-298
40. Minocha, A., and Galligan, J. J. (1993) Excitatory and inhibitory responses mediated by GABAA and GABAB receptors in guinea pig distal colon. Eur. J. Pharmacol. 230, 187-193
41. McCarthy, E. L. (1934) Mariotte's bottle. Science 80, 100
42. Bulbring, E., and Lin, R. C. (1958) The effect of intraluminal application of 5-hydroxytryptamine and 5-hydroxytryptophan on peristalsis; the local production of 5-HT and its release in relation to intraluminal pressure and propulsive activity. J. Physiol. 140, 381-407
43. Hirst, G. D., Holman, M. E., and Spence, I. (1974) Two types of neurones in the myenteric plexus of duodenum in the guinea pig. J. Physiol. 236, 303-326
44. Nurgali, K., Nguyen, T. V., Matsuyama, H., Thacker, M., Robbins, H. L., and Furness, J. B. (2007) Phenotypic changes of morphologically identified guinea-pig myenteric neurons following intestinal inflammation. J. Physiol. 583, 593-609
45. Motulsky, H. J. (1999) Analyzing Data with GraphPad Prism, GraphPad, San Diego, CA, USA
46. Huizinga, J. D., Ambrous, K., and Der-Silaphet, T. (1998) Co-operation between neural and myogenic mechanisms in the control of distension-induced peristalsis in the mouse small intestine. J. Physiol. 506, 843-856 (Pubitemid 28062105)
47. Gallego, D., Clave, P., Donovan, J., Rahmati, R., Grundy, D., Jimenez, M., and Beyak, M. J. (2008) The gaseous mediator, hydrogen sulphide, inhibits in vitro motor patterns in the human, rat and mouse colon and jejunum. Neurogastroenterol. Motil. 20, 1306-1316
48. Abdu, F., Hicks, G. A., Hennig, G., Allen, J. P., and Grundy, D. (2002) Somatostatin sst(2) receptors inhibit peristalsis in the rat and mouse jejunum. Am. J. Physiol. Gastrointest. Liver Physiol. 282, G624-G633
49. Neal, K. B., Parry, L. J., and Bornstein, J. C. (2009) Strainspecific genetics, anatomy and function of enteric neural serotonergic pathways in inbred mice. J. Physiol. 587, 567-586
50. Chiocchetti, R., Mazzuoli, G., Albanese, V., Mazzoni, M., Clavenzani, P., Lalatta-Costerbosa, G., Lucchi, M. L., Di Guardo, G., Marruchella, G., and Furness, J. B. (2008) Anatomical evidence for ileal Peyer's patches innervation by enteric nervous system: a potential route for prion neuroinvasion? Cell Tissue Res. 332, 185-194
51. Keast, J. R., Furness, J. B., and Costa, M. (1984) Origins of peptide and norepinephrine nerves in the mucosa of the guinea pig small intestine. Gastroenterology 86, 637-644
52. Furness, J. B., Robbins, H. L., Xiao, J., Stebbing, M. J., and Nurgali, K. (2004) Projections and chemistry of Dogiel type II neurons in the mouse colon. Cell Tissue Res. 317, 1-12 (Pubitemid 38962049)
53. Colquhoun, D. (1998) Binding, gating, affinity and efficacy: the interpretation of structure- activity relationships for agonists and of the effects of mutating receptors. Br. J. Pharmacol. 125, 924-947
54. Sarna, S. K. (2007) Enteric descending and afferent neural signaling stimulated by giant migrating contractions: essential contributing factors to visceral pain. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G572-G581
55. Cherubini, E., and North, R. A. (1984) Actions of γ-aminobutyric acid on neurones of guinea-pig myenteric plexus. Br. J. Pharmacol. 82, 93-100
56. Zhou, X., and Galligan, J. J. (2000) GABA(A) receptors on calbindin-immunoreactive myenteric neurons of guinea pig intestine. J. Auton. Nerv. Syst. 78, 122-135
57. Hanani, M., Francke, M., Hartig, W., Grosche, J., Reichenbach, A., and Pannicke, T. (2000) Patch-clamp study of neurons and glial cells in isolated myenteric ganglia. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G644-G651
58. Jessen, K. R. (1981) GABA and the enteric nervous system. A neurotransmitter function? Mol Cell Biochem. 38(Spec. No.), 69-76
59. Park, K. B., and Oh, S. H. (2007) Cloning, sequencing and expression of a novel glutamate decarboxylase gene from a newly isolated lactic acid bacterium, Lactobacillus brevis OPK-3. Bioresour. Technol. 98, 312-319
60. Xiao, J., Nguyen, T. V., Ngui, K., Strijbos, P. J., Selmer, I. S., Neylon, C. B., and Furness, J. B. (2004) Molecular and functional analysis of hyperpolarisation-activated nucleotide-gated (HCN) channels in the enteric nervous system. Neuroscience 129, 603-614
61. 2+-activated, intermediate- conductance potassium channels on motility of the rat small intestine, in vivo. Neurogastroenterol. Motil. 19, 383-389
62. Wood, J. D. (1972) Excitation of intestinal muscle by atropine, tetrodotoxin, and xylocaine. Am. J. Physiol. 222, 118-125
63. Waterman, S. A., Costa, M., and Tonini, M. (1994) Accommodation mediated by enteric inhibitory reflexes in the isolated guinea-pig small intestine. J. Physiol. 474, 539-546 (Pubitemid 24060785)
64. + channels in urinary bladder smooth muscle cells. J. Pharmacol. Sci. 100, 237-241
65. Pedarzani, P., McCutcheon, J. E., Rogge, G., Jensen, B. S., Christophersen, P., Hougaard, C., Strobaek, D., and Stocker, M. (2005) Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current I(AHP) and modulates the firing properties of hippocampal pyramidal neurons. J. Biol. Chem. 280, 41404-41411
66. Biel, M., Wahl-Schott, C., Michalakis, S., and Zong, X. (2009) Hyperpolarization-activated cation channels: from genes to function. Physiol. Rev. 89, 847-885
67. Yanagida, H., Inoue, R., Tanaka, M., and Ito, Y. (2000) Temperature- sensitive gating of cation current in guinea pig ileal muscle activated by hyperpolarization. Am. J. Physiol. Cell Physiol. 278, C40-C48
68. Burley, J. R., and Dolphin, A. C. (2000) Overlapping selectivity of neurotoxin and dihydropyridine calcium channel blockers in cerebellar granule neurones. Neuropharmacology 39, 1740-1755
69. Kunze, W. A., Clerc, N., Bertrand, P. P., and Furness, J. B. (1999) Contractile activity in intestinal muscle evokes action potential discharge in guinea-pig myenteric neurons. J. Physiol. 517, 547-561
70. Bian, X., Zhou, X., and Galligan, J. J. (2004) R-type calcium channels in myenteric neurons of guinea pig small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G134-G142
71. North, R. A., and Tokimasa, T. (1987) Persistent calcium-sensitive potassium current and the resting properties of guineapig myenteric neurones. J. Physiol. 386, 333-353
72. Kunze, W. A., Bornstein, J. C., Furness, J. B., Hendriks, R., and Stephenson, D. S. (1994) Charybdotoxin and iberiotoxin but not apamin abolish the slow afterhyperpolarization in myenteric plexus neurons. Pflügers Arch. 428, 300-336 (Pubitemid 24287381)
73. Bush, T. G., Spencer, N. J., Watters, N., Sanders, K. M., and Smith, T. K. (2000) Spontaneous migrating motor complexes occur in both the terminal ileum and colon of the C57BL/6 mouse in vitro. Auton. Neurosci. 84, 162-168
74. Salinas, E. (2006) How behavioral constraints may determine optimal sensory representations. PLoS Biol. 4, e387
75. Kuhn, A., Aertsen, A., and Rotter, S. (2004) Neuronal integration of synaptic input in the fluctuation-driven regime. J. Neurosci. 24, 2345-2356 (Pubitemid 38327947)
76. Kunze, W. A., Furness, J. B., and Bornstein, J. C. (1993) Simultaneous intracellular recordings from enteric neurons reveal that myenteric AH neurons transmit via slow excitatory postsynaptic potentials. Neuroscience 55, 685-694
77. Studinger, P., Goldstein, R., and Taylor, J. A. (2007) Mechanical and neural contributions to hysteresis in the cardiac vagal limb of the arterial baroreflex. J. Physiol. 583, 1041-1048
78. Das, J., Ho, M., Zikherman, J., Govern, C., Yang, M., Weiss, A., Chakraborty, A. K., and Roose, J. P. (2009) Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 136, 337-351
79. + channel by acting at the extracellular side of the ionic pore. Anesthesiology 99, 1340-1345
80. + channel, hIK1, by volatile anesthetics. Eur. J. Pharmacol. 395, 95-101
81. Rugiero, F., Gola, M., Kunze, W. A., Reynaud, J. C., Furness, J. B., and Clerc, N. (2002) Analysis of whole-cell currents by patch clamp of guinea-pig myenteric neurones in intact ganglia. J. Physiol. 538, 447-463 (Pubitemid 35175373)
82. Zholos, A. V., Baidan, L. V., and Wood, J. D. (2002) Sodium conductance in cultured myenteric AH-type neurons from guinea-pig small intestine. Auton. Neurosci. 96, 93-102
83. Schemann, M., and Mazzuoli, G. (2009) Multifunctional mechanosensitive neurons in the enteric nervous system. Auton Neurosci 153, 21-25
84. Mazzuoli, G., and Schemann, M. (2009) Multifunctional rapidly adapting mechanosensitive enteric neurons (RAMEN) in the myenteric plexus of the guinea pig ileum. J. Physiol. 587, 4681-4694
85. Davies, P. J., Thomas, E. A., and Bornstein, J. C. (2006) Different types of potassium channels underlie the long afterhyperpolarization in guinea-pig sympathetic and enteric neurons. Auton. Neurosci. 124, 26-30
86. Nurgali, K., Stebbing, M. J., and Furness, J. B. (2004) Correlation of electrophysiological and morphological characteristics of enteric neurons in the mouse colon. J. Comp. Neurol. 468, 112-124
87. Furukawa, K., Taylor, G. S., and Bywater, R. A. (1986) An intracellular study of myenteric neurons in the mouse colon. J. Neurophysiol. 55, 1395-1406
88. Ren, J., Bian, X., DeVries, M., Schnegelsberg, B., Cockayne, D. A., Ford, A. P., and Galligan, J. J. (2003) P2X2 subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine. J. Physiol. 552, 809-821 (Pubitemid 37428422)
89. Shanahan, F. (2005) Physiological basis for novel drug therapies used to treat the inflammatory bowel diseases. I. Pathophysiological basis and prospects for probiotic therapy in inflammatory bowel disease. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G417-G421
90. Bienenstock, J., Croitoru, K., Ernst, P. B., and Stanisz, A. M. (1989) Nerves and neuropeptides in the regulation of mucosal immunity. Adv. Exp. Med. Biol. 257, 19-26
91. O'Dorisio, M. S. (1988) Neuropeptide modulation of the immune response in gut associated lymphoid tissue. Int. J. Neurosci. 38, 189-198
92. Stanisz, A. M., and Stanisz, J. A. (2000) Nerve growth factor and neuroimmune interactions in inflammatory diseases. Ann. N. Y. Acad. Sci. 917, 268-272
93. Mignini, F., Streccioni, V., and Amenta, F. (2003) Autonomic innervation of immune organs and neuroimmune modulation. Auton. Autacoid. Pharmacol. 23, 1-25