Role of enteric neurotransmission in host defense and protection of the gastrointestinal tract

Autonomic Neuroscience: Basic and Clinical

Volumn 181, Issue 1, 2014, Pages 94-106

  Sharkey, Keith A ^a   Savidge, Tor C ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Microbiome; Microbiota; Myenteric plexus; Neurotransmitters; Primary afferent nerves; Submucosal plexus; Sympathetic nerve; Vagus nerve

Indexed keywords

MICROBIOME; MICROBIOTA; MYENTERIC PLEXUS; NEUROTRANSMITTERS; PRIMARY AFFERENT NERVES; SUBMUCOSAL PLEXUS; SYMPATHETIC NERVE; VAGUS NERVE;

ANIMALS; BACTERIAL PHYSIOLOGICAL PHENOMENA; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, MUCOSAL; SYNAPTIC TRANSMISSION;

EID: 84893922235     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2013.12.006     Document Type: Review

References (200)

1. Abbott N.J., Ronnback L., Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7:41-53.
2. Abdo H., Derkinderen P., Gomes P., Chevalier J., Aubert P., Masson D., Galmiche J.P., Vanden Berghe P., Neunlist M., Lardeux B. Enteric glial cells protect neurons from oxidative stress in part via reduced glutathione. FASEB J. 2010, 24:1082-1094.
3. Abdo H., Mahe M.M., Derkinderen P., Bach-Ngohou K., Neunlist M., Lardeux B. The omega-6 fatty acid derivative 15-deoxy-Delta(1)(2), (1)(4)-prostaglandin J2 is involved in neuroprotection by enteric glial cells against oxidative stress. J. Physiol. 2012, 590:2739-2750.
4. Anitha M., Vijay-Kumar M., Sitaraman S.V., Gewirtz A.T., Srinivasan S. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology 2012, 143(1006-1016):e1004.
5. Asano Y., Hiramoto T., Nishino R., Aiba Y., Kimura T., Yoshihara K., Koga Y., Sudo N. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 303:G1288-G1295.
6. Axelson J., Ekelund M., Hakanson R., Sundler F. Gastrin and the vagus interact in the trophic control of the rat oxyntic mucosa. Regul. Pept. 1988, 22:237-243.
7. Bach-Ngohou K., Mahe M.M., Aubert P., Abdo H., Boni S., Bourreille A., Denis M.G., Lardeux B., Neunlist M., Masson D. Enteric glia modulate epithelial cell proliferation and differentiation through 15-deoxy-12,14-prostaglandin J2. J. Physiol. 2010, 588:2533-2544.
8. Backhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., Gordon J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307:1915-1920.
9. Bailey M.T., Lubach G.R., Coe C.L. Prenatal stress alters bacterial colonization of the gut in infant monkeys. J. Pediatr. Gastroenterol. Nutr. 2004, 38:414-421.
10. Baker S.A., Hennig G.W., Salter A.K., Kurahashi M., Ward S.M., Sanders K.M. Distribution and Ca2+ signaling in fibroblast-like (PDGFRalpha+) cells in the murine gastric fundus. J. Physiol. 2013, 591:6193-6208.
11. Bangsgaard Bendtsen K.M., Krych L., Sorensen D.B., Pang W., Nielsen D.S., Josefsen K., Hansen L.H., Sorensen S.J., Hansen A.K. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One 2012, 7:e46231.
12. Barajon I., Serrao G., Arnaboldi F., Opizzi E., Ripamonti G., Balsari A., Rumio C. Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. 2009, 57:1013-1023.
13. Barreau F., Cartier C., Leveque M., Ferrier L., Moriez R., Laroute V., Rosztoczy A., Fioramonti J., Bueno L. Pathways involved in gut mucosal barrier dysfunction induced in adult rats by maternal deprivation: corticotrophin-releasing factor and nerve growth factor interplay. J. Physiol. 2007, 580:347-356.
14. Barrett K.E., Keely S.J. Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu. Rev. Physiol. 2000, 62:535-572.
15. Bassotti G., Villanacci V., Maurer C.A., Fisogni S., Di Fabio F., Cadei M., Morelli A., Panagiotis T., Cathomas G., Salerni B. The role of glial cells and apoptosis of enteric neurones in the neuropathology of intractable slow transit constipation. Gut 2006, 55:41-46.
16. Bischoff S.C. Physiological and pathophysiological functions of intestinal mast cells. Semin. Immunopathol. 2009, 31:185-205.
17. Bjerknes M., Cheng H. Modulation of specific intestinal epithelial progenitors by enteric neurons. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12497-12502.
18. Blackshaw L.A., Brookes S.J., Grundy D., Schemann M. Sensory transmission in the gastrointestinal tract. Neurogastroenterol. Motil. 2007, 19:1-19.
19. Boesmans W., Martens M.A., Weltens N., Hao M.M., Tack J., Cirillo C., Vanden Berghe P. Imaging neuron-glia interactions in the enteric nervous system. Front. Cell. Neurosci. 2013, 7:183.
20. Boudry G., Morise A., Seve B., Le Huerou-Luron I. Effect of milk formula protein content on intestinal barrier function in a porcine model of LBW neonates. Pediatr. Res. 2011, 69:4-9.
21. Brandtzaeg P. Gate-keeper function of the intestinal epithelium. Benefic. Microbes 2013, 4:67-82.
22. Brun P., Giron M.C., Qesari M., Porzionato A., Caputi V., Zoppellaro C., Banzato S., Grillo A.R., Spagnol L., De Caro R., Pizzuti D., Barbieri V., Rosato A., Sturniolo G.C., Martines D., Zaninotto G., Palu G., Castagliuolo I. Toll-like receptor 2 regulates intestinal inflammation by controlling integrity of the enteric nervous system. Gastroenterology 2013, 145:1323-1333.
23. Buhner S., Li Q., Berger T., Vignali S., Barbara G., De Giorgio R., Stanghellini V., Schemann M. Submucous rather than myenteric neurons are activated by mucosal biopsy supernatants from irritable bowel syndrome patients. Neurogastroenterol. Motil. 2012, 24:1134-e1572.
24. Buhner S., Li Q., Vignali S., Barbara G., De Giorgio R., Stanghellini V., Cremon C., Zeller F., Langer R., Daniel H., Michel K., Schemann M. Activation of human enteric neurons by supernatants of colonic biopsy specimens from patients with irritable bowel syndrome. Gastroenterology 2009, 137:1425-1434.
25. Buresi M.C., Vergnolle N., Sharkey K.A., Keenan C.M., Andrade-Gordon P., Cirino G., Cirillo D., Hollenberg M.D., MacNaughton W.K. Activation of proteinase-activated receptor-1 inhibits neurally evoked chloride secretion in the mouse colon in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288:G337-G345.
26. Cameron H.L., Perdue M.H. Muscarinic acetylcholine receptor activation increases transcellular transport of macromolecules across mouse and human intestinal epithelium in vitro. Neurogastroenterol. Motil. 2007, 19:47-56.
27. Castagliuolo I., Lamont J.T., Qiu B., Fleming S.M., Bhaskar K.R., Nikulasson S.T., Kornetsky C., Pothoulakis C. Acute stress causes mucin release from rat colon: role of corticotropin releasing factor and mast cells. Am. J. Physiol. Gastrointest. Liver Physiol. 1996, 271:G884-G892.
28. Cenac N., Andrews C.N., Holzhausen M., Chapman K., Cottrell G., Andrade-Gordon P., Steinhoff M., Barbara G., Beck P., Bunnett N.W., Sharkey K.A., Ferraz J.G., Shaffer E., Vergnolle N. Role for protease activity in visceral pain in irritable bowel syndrome. J. Clin. Invest. 2007, 117:636-647.
29. Cervi A.L., Lukewich M.K., Lomax A.E. Neural regulation of gastrointestinal inflammation: role of the sympathetic nervous system 2014, (in press, AUTNEU-D-13-121).
30. Chandrasekharan B., Bala V., Kolachala V.L., Vijay-Kumar M., Jones D., Gewirtz A.T., Sitaraman S.V., Srinivasan S. Targeted deletion of neuropeptide Y (NPY) modulates experimental colitis. PLoS One 2008, 3:e3304.
31. Chandrasekharan B., Jeppsson S., Pienkowski S., Belsham D.D., Sitaraman S.V., Merlin D., Kokkotou E., Nusrat A., Tansey M.G., Srinivasan S. Tumor necrosis factor-neuropeptide y cross talk regulates inflammation, epithelial barrier functions, and colonic motility. Inflamm. Bowel Dis. 2013, 19:2535-2546.
32. Chandrasekharan B., Nezami B.G., Srinivasan S. Emerging neuropeptide targets in inflammation: NPY and VIP. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304:G949-G957.
33. Chen C., Brown D.R., Xie Y., Green B.T., Lyte M. Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock 2003, 20:183-188.
34. Chiocchetti R., Mazzuoli G., Albanese V., Mazzoni M., Clavenzani P., Lalatta-Costerbosa G., Lucchi M.L., Di Guardo G., Marruchella G., Furness J.B. Anatomical evidence for ileal Peyer's patches innervation by enteric nervous system: a potential route for prion neuroinvasion?. Cell Tissue Res. 2008, 332:185-194.
35. Chu S., Schubert M.L. Gastric secretion. Curr. Opin. Gastroenterol. 2013, 29:636-641.
36. Cipriani S., Mencarelli A., Chini M.G., Distrutti E., Renga B., Bifulco G., Baldelli F., Donini A., Fiorucci S. The bile acid receptor GPBAR-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. PLoS One 2011, 6:e25637.
37. Clevers H.C., Bevins C.L. Paneth cells: maestros of the small intestinal crypts. Annu. Rev. Physiol. 2013, 75:289-311.
38. Cogan T.A., Thomas A.O., Rees L.E., Taylor A.H., Jepson M.A., Williams P.H., Ketley J., Humphrey T.J. Norepinephrine increases the pathogenic potential of Campylobacter jejuni. Gut 2007, 56:1060-1065.
39. Collins S.M., Surette M., Bercik P. The interplay between the intestinal microbiota and the brain. Nat. Rev. Microbiol. 2012, 10:735-742.
40. Conlin V.S., Wu X., Nguyen C., Dai C., Vallance B.A., Buchan A.M., Boyer L., Jacobson K. Vasoactive intestinal peptide ameliorates intestinal barrier disruption associated with Citrobacter rodentium-induced colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297:G735-G750.
41. Costantini T.W., Bansal V., Krzyzaniak M., Putnam J.G., Peterson C.Y., Loomis W.H., Wolf P., Baird A., Eliceiri B.P., Coimbra R. Vagal nerve stimulation protects against burn-induced intestinal injury through activation of enteric glia cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G1308-G1318.
42. Costantini T.W., Krzyzaniak M., Cheadle G.A., Putnam J.G., Hageny A.M., Lopez N., Eliceiri B.P., Bansal V., Coimbra R. Targeting alpha-7 nicotinic acetylcholine receptor in the enteric nervous system: a cholinergic agonist prevents gut barrier failure after severe burn injury. Am. J. Pathol. 2012, 181:478-486.
43. Costes L.M., Boeckxstaens G.E., de Jonge W.J., Cailotto C. Neural networks in intestinal immunoregulation. Organogenesis 2013, 9:216-223.
44. Crivellato E., Soldano F., Travan L. A light and electron microscopic quantitative analysis of nerve-immune cell contacts in the gut-associated lymphoid tissue of the mouse colon. J. Submicrosc. Cytol. Pathol. 2002, 34:55-66.
45. Crivellato E., Soldano F., Travan L., Fusaroli P., Mallardi F. Apposition of enteric nerve fibers to plasma cells and immunoblasts in the mouse small bowel. Neurosci. Lett. 1998, 241:123-126.
46. de Jonge W.J. Mast cells in intestinal inflammation, barrier function, and postoperative motility. J. Pediatr. Gastroenterol. Nutr. 2011, 53(Suppl. 2):S56-S57.
47. de Jonge W.J. The gut's little brain in control of intestinal immunity. ISRN Gastroenterol. 2013, 2013:630159.
48. Deloose E., Janssen P., Depoortere I., Tack J. The migrating motor complex: control mechanisms and its role in health and disease. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:271-285.
49. Devkota S., Chang E.B. Nutrition, microbiomes, and intestinal inflammation. Curr. Opin. Gastroenterol. 2013, 29:603-607.
50. Dhawan S., Cailotto C., Harthoorn L.F., de Jonge W.J. Cholinergic signalling in gut immunity. Life Sci. 2012, 91:1038-1042.
51. Dinan T.G., Cryan J.F. Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology. Psychoneuroendocrinology 2012, 37:1369-1378.
52. Engel M.A., Becker C., Reeh P.W., Neurath M.F. Role of sensory neurons in colitis: increasing evidence for a neuroimmune link in the gut. Inflamm. Bowel Dis. 2011, 17:1030-1033.
53. Esposito G., Capoccia E., Turco F., Palumbo I., Lu J., Steardo A., Cuomo R., Sarnelli G., Steardo L. Palmitoylethanolamide improves colon inflammation through an enteric glia/toll like receptor 4-dependent PPAR-alpha activation. Gut 2014, (in press). 10.1136/gutjnl-2013-305005.
54. Fasano A. Zonulin, regulation of tight junctions, and autoimmune diseases. Ann. N. Y. Acad. Sci. 2012, 1258:25-33.
55. Fasano A., Shea-Donohue T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat. Clin. Pract. Gastroenterol. Hepatol. 2005, 2:416-422.
56. Felten S.Y., Felten D.L., Bellinger D.L., Olschowka J.A. Noradrenergic and peptidergic innervation of lymphoid organs. Chem. Immunol. 1992, 52:25-48.
57. Fihn B.M., Sjoqvist A., Jodal M. Involvement of enteric nerves in permeability changes due to deoxycholic acid in rat jejunum in vivo. Acta Physiol. Scand. 2003, 178:241-250.
58. Flamant M., Aubert P., Rolli-Derkinderen M., Bourreille A., Neunlist M.R., Mahe M.M., Meurette G., Marteyn B., Savidge T., Galmiche J.P., Sansonetti P.J., Neunlist M. Enteric glia protect against Shigella flexneri invasion in intestinal epithelial cells: a role for S-nitrosoglutathione. Gut 2011, 60:473-484.
59. Forsythe P., Kunze W.A., Bienenstock J. On communication between gut microbes and the brain. Curr. Opin. Gastroenterol. 2012, 28:557-562.
60. Freestone P.P., Sandrini S.M., Haigh R.D., Lyte M. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol. 2008, 16:55-64.
61. Furness J.B. The Enteric Nervous System 2006, Blackwell Pub., Malden, Mass., (xiii, 274 pp.).
62. Furness J.B. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:286-294.
63. Furness J.B., Kunze W.A., Bertrand P.P., Clerc N., Bornstein J.C. Intrinsic primary afferent neurons of the intestine. Prog. Neurobiol. 1998, 54:1-18.
64. Furness J.B., Rivera L.R., Cho H.J., Bravo D.M., Callaghan B. The gut as a sensory organ. Nat. Rev. Gastroenterol. Hepatol. 2013, 10:729-740.
65. Gareau M.G., Jury J., Perdue M.H. Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G198-G203.
66. Gautron L., Rutkowski J.M., Burton M.D., Wei W., Wan Y., Elmquist J.K. Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen. J. Comp. Neurol. 2013, 521:3741-3767.
67. Gershon M.D. 5-Hydroxytryptamine (serotonin) in the gastrointestinal tract. Curr. Opin. Endocrinol. Diabetes Obes. 2013, 20:14-21.
68. Geurts L., Neyrinck A.M., Delzenne N.M., Knauf C., Cani P.D. Gut microbiota controls adipose tissue expansion, gut barrier and glucose metabolism: novel insights into molecular targets and interventions using prebiotics. Benefic. Microbes 2013, 25:1-15.
69. Gomes P., Chevalier J., Boesmans W., Roosen L., van den Abbeel V., Neunlist M., Tack J., Vanden Berghe P. ATP-dependent paracrine communication between enteric neurons and glia in a primary cell culture derived from embryonic mice. Neurogastroenterol. Motil. 2009, 21:870-e62.
70. Gougeon P.Y., Lourenssen S., Han T.Y., Nair D.G., Ropeleski M.J., Blennerhassett M.G. The pro-inflammatory cytokines IL-1beta and TNFalpha are neurotrophic for enteric neurons. J. Neurosci. 2013, 33:3339-3351.
71. Green B.T., Bunnett N.W., Kulkarni-Narla A., Steinhoff M., Brown D.R. Intestinal type 2 proteinase-activated receptors: expression in opioid-sensitive secretomotor neural circuits that mediate epithelial ion transport. J. Pharmacol. Exp. Ther. 2000, 295:410-416.
72. Green B.T., Lyte M., Kulkarni-Narla A., Brown D.R. Neuromodulation of enteropathogen internalization in Peyer's patches from porcine jejunum. J. Neuroimmunol. 2003, 141:74-82.
73. Greenwood B., Mantle M. Mucin and protein release in the rabbit jejunum: effects of bethanechol and vagal nerve stimulation. Gastroenterology 1992, 103:496-505.
74. Gross E.R., Gershon M.D., Margolis K.G., Gertsberg Z.V., Li Z., Cowles R.A. Neuronal serotonin regulates growth of the intestinal mucosa in mice. Gastroenterology 2012, 143(408-417):e402.
75. Gross K.J., Pothoulakis C. Role of neuropeptides in inflammatory bowel disease. Inflamm. Bowel Dis. 2007, 13:918-932.
76. Gulbransen B.D., Bains J.S., Sharkey K.A. Enteric glia are targets of the sympathetic innervation of the myenteric plexus in the guinea pig distal colon. J. Neurosci. 2010, 30:6801-6809.
77. Gulbransen B.D., Bashashati M., Hirota S.A., Gui X., Roberts J.A., MacDonald J.A., Muruve D.A., McKay D.M., Beck P.L., Mawe G.M., Thompson R.J., Sharkey K.A. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nat. Med. 2012, 18:600-604.
78. Gulbransen B.D., Sharkey K.A. Purinergic neuron-to-glia signaling in the enteric nervous system. Gastroenterology 2009, 136:1349-1358.
79. Gulbransen B.D., Sharkey K.A. Novel functional roles for enteric glia in the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol. 2012, 9:625-632.
80. Hadzijahic N., Renehan W.E., Ma C.K., Zhang X., Fogel R. Myenteric plexus destruction alters morphology of rat intestine. Gastroenterology 1993, 105:1017-1028.
81. Hemarajata P., Versalovic J. Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Ther. Adv. Gastroenterol. 2013, 6:39-51.
82. Hoffman J.M., Tyler K., MacEachern S.J., Balemba O.B., Johnson A.C., Brooks E.M., Zhao H., Swain G.M., Moses P.L., Galligan J.J., Sharkey K.A., Greenwood-Van Meerveld B., Mawe G.M. Activation of colonic mucosal 5-HT(4) receptors accelerates propulsive motility and inhibits visceral hypersensitivity. Gastroenterology 2012, 142(844-854):e844.
83. Hoffmann P., Mazurkiewicz J., Holtmann G., Gerken G., Eysselein V.E., Goebell H. Capsaicin-sensitive nerve fibres induce epithelial cell proliferation, inflammatory cell immigration and transforming growth factor-alpha expression in the rat colonic mucosa in vivo. Scand. J. Gastroenterol. 2002, 37:414-422.
84. Holle G.E. Changes in the structure and regeneration mode of the rat small intestinal mucosa following benzalkonium chloride treatment. Gastroenterology 1991, 101:1264-1273.
85. Holle G.E., Dietl J., Demir I. Influence of the intramural innervation on the morphogenesis of the enteroendocrine cells and the genetic construct involved. Int. J. Mol. Med. 2003, 11:275-285.
86. Holzer P. Gastroduodenal mucosal defense. Curr. Opin. Gastroenterol. 2000, 16:469-478.
87. Holzer P. Local microcirculatory reflexes and afferent signalling in response to gastric acid challenge. Gut 2000, 47(Suppl. 4):iv46-iv48. (discussion iv52).
88. Holzer P. Role of visceral afferent neurons in mucosal inflammation and defense. Curr. Opin. Pharmacol. 2007, 7:563-569.
89. Hughes D.T., Clarke M.B., Yamamoto K., Rasko D.A., Sperandio V. The QseC adrenergic signaling cascade in Enterohemorrhagic E. coli (EHEC). PLoS Pathog. 2009, 5:e1000553.
90. Hughes P.A., Harrington A.M., Castro J., Liebregts T., Adam B., Grasby D.J., Isaacs N.J., Maldeniya L., Martin C.M., Persson J., Andrews J.M., Holtmann G., Blackshaw L.A., Brierley S.M. Sensory neuro-immune interactions differ between Irritable Bowel Syndrome subtypes. Gut 2013, 62:1456-1465.
91. Ikehara O., Hayashi H., Waguri T., Kaji I., Karaki S., Kuwahara A., Suzuki Y. Subepithelial trypsin induces enteric nerve-mediated anion secretion by activating proteinase-activated receptor 1 in the mouse cecum. J. Physiol. Sci. 2012, 62:211-219.
92. Ikehara O., Hayashi H., Watanabe Y., Yamamoto H., Mochizuki T., Hoshino M., Suzuki Y. Proteinase-activated receptors-1 and 2 induce electrogenic Cl- secretion in the mouse cecum by distinct mechanisms. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G115-G125.
93. Izzo A.A., Sharkey K.A. Cannabinoids and the gut: new developments and emerging concepts. Pharmacol. Ther. 2010, 126:21-38.
94. Janig W., Morrison J.F. Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. Prog. Brain Res. 1986, 67:87-114.
95. Jonsson M., Norrgard O., Forsgren S. Presence of a marked nonneuronal cholinergic system in human colon: study of normal colon and colon in ulcerative colitis. Inflamm. Bowel Dis. 2007, 13:1347-1356.
96. Kamiya T., Wang L., Forsythe P., Goettsche G., Mao Y., Wang Y., Tougas G., Bienenstock J. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 2006, 55:191-196.
97. Karavolos M.H., Winzer K., Williams P., Khan C.M. Pathogen espionage: multiple bacterial adrenergic sensors eavesdrop on host communication systems. Mol. Microbiol. 2013, 87:455-465.
98. Keely S., Kelly C.J., Weissmueller T., Burgess A., Wagner B.D., Robertson C.E., Harris J.K., Colgan S.P. Activated fluid transport regulates bacterial-epithelial interactions and significantly shifts the murine colonic microbiome. Gut Microbes 2012, 3:250-260.
99. Keita A.V., Carlsson A.H., Cigehn M., Ericson A.C., McKay D.M., Soderholm J.D. Vasoactive intestinal polypeptide regulates barrier function via mast cells in human intestinal follicle-associated epithelium and during stress in rats. Neurogastroenterol. Motil. 2013, 25:e406-e417.
100. Keita A.V., Soderholm J.D. The intestinal barrier and its regulation by neuroimmune factors. Neurogastroenterol. Motil. 2010, 22:718-733.
101. Klapproth H., Reinheimer T., Metzen J., Munch M., Bittinger F., Kirkpatrick C.J., Hohle K.D., Schemann M., Racke K., Wessler I. Non-neuronal acetylcholine, a signalling molecule synthezised by surface cells of rat and man. Naunyn Schmiedebergs Arch. Pharmacol. 1997, 355:515-523.
102. Knights D., Lassen K.G., Xavier R.J. Advances in inflammatory bowel disease pathogenesis: linking host genetics and the microbiome. Gut 2013, 62:1505-1510.
103. Krzyzaniak M., Peterson C., Loomis W., Hageny A.M., Wolf P., Reys L., Putnam J., Eliceiri B., Baird A., Bansal V., Coimbra R. Postinjury vagal nerve stimulation protects against intestinal epithelial barrier breakdown. J. Trauma 2011, 70:1168-1175. (discussion 1175-1166).
104. Kugler E.M., Mazzuoli G., Demir I.E., Ceyhan G.O., Zeller F., Schemann M. Activity of protease-activated receptors in primary cultured human myenteric neurons. Front. Neurosci. 2012, 6:133.
105. Kunze W.A., Mao Y.K., Wang B., Huizinga J.D., Ma X., Forsythe P., Bienenstock J. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J. Cell. Mol. Med. 2009, 13:2261-2270.
106. Kurahashi M., Zheng H., Dwyer L., Ward S.M., Don Koh S., Sanders K.M. A functional role for the 'fibroblast-like cells' in gastrointestinal smooth muscles. J. Physiol. 2011, 589:697-710.
107. Laukoetter M.G., Bruewer M., Nusrat A. Regulation of the intestinal epithelial barrier by the apical junctional complex. Curr. Opin. Gastroenterol. 2006, 22:85-89.
108. Lawson V.A., Furness J.B., Klemm H.M., Pontell L., Chan E., Hill A.F., Chiocchetti R. The brain to gut pathway: a possible route of prion transmission. Gut 2010, 59:1643-1651.
109. Lin H.C., Pimentel M. Bacterial concepts in irritable bowel syndrome. Rev. Gastroenterol. Disord. 2005, 5(Suppl. 3):S3-S9.
110. Lomax A.E., Sharkey K.A., Furness J.B. The participation of the sympathetic innervation of the gastrointestinal tract in disease states. Neurogastroenterol. Motil. 2010, 22:7-18.
111. Lozupone C.A., Stombaugh J.I., Gordon J.I., Jansson J.K., Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012, 489:220-230.
112. Lundgren O., Jodal M., Jansson M., Ryberg A.T., Svensson L. Intestinal epithelial stem/progenitor cells are controlled by mucosal afferent nerves. PLoS One 2011, 6:e16295.
113. Lyte M., Vulchanova L., Brown D.R. Stress at the intestinal surface: catecholamines and mucosa-bacteria interactions. Cell Tissue Res. 2011, 343:23-32.
114. Ma X., Mao Y.K., Wang B., Huizinga J.D., Bienenstock J., Kunze W. Lactobacillus reuteri ingestion prevents hyperexcitability of colonic DRG neurons induced by noxious stimuli. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296:G868-G875.
115. MacEachern S.J., Patel B.A., McKay D.M., Sharkey K.A. Nitric oxide regulation of colonic epithelial ion transport: a novel role for enteric glia in the myenteric plexus. J. Physiol. 2011, 589:3333-3348.
116. Macia L., Thorburn A.N., Binge L.C., Marino E., Rogers K.E., Maslowski K.M., Vieira A.T., Kranich J., Mackay C.R. Microbial influences on epithelial integrity and immune function as a basis for inflammatory diseases. Immunol. Rev. 2012, 245:164-176.
117. Mao Y.K., Kasper D.L., Wang B., Forsythe P., Bienenstock J., Kunze W.A. Bacteroides fragilis polysaccharide A is necessary and sufficient for acute activation of intestinal sensory neurons. Nat. Commun. 2013, 4:1465.
118. Margolis K.G., Gershon M.D. Neuropeptides and inflammatory bowel disease. Curr. Opin. Gastroenterol. 2009, 25:503-511.
119. Martelli D., McKinley M.J., McAllen R.M. The cholinergic anti-inflammatory pathway: a critical review 2014, (this volume, AUTNEU-D-13-00093).
120. Matteoli G., Gomez-Pinilla P.J., Nemethova A., Di Giovangiulio M., Cailotto C., van Bree S.H., Michel K., Tracey K.J., Schemann M., Boesmans W., Vanden Berghe P., Boeckxstaens G.E. A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut 2014, (in press). 10.1136/gutjnl-2013-304676.
121. McCole D.F., Barrett K.E. Varied role of the gut epithelium in mucosal homeostasis. Curr. Opin. Gastroenterol. 2007, 23:647-654.
122. McGuckin M.A., Linden S.K., Sutton P., Florin T.H. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 2011, 9:265-278.
123. McVey Neufeld K.A., Mao Y.K., Bienenstock J., Foster J.A., Kunze W.A. The microbiome is essential for normal gut intrinsic primary afferent neuron excitability in the mouse. Neurogastroenterol. Motil. 2013, 25:183-e188.
124. Meurette G., Blanchard C., Duchalais-Dassonneville E., Coquenlorge S., Aubert P., Wong M., Lehur P.A., Neunlist M. Sacral nerve stimulation enhances epithelial barrier of the rectum: results from a porcine model. Neurogastroenterol. Motil. 2012, 24(267-273):e110.
125. Miampamba M., Maillot C., Million M., Tache Y. Peripheral CRF activates myenteric neurons in the proximal colon through CRF(1) receptor in conscious rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 282:G857-G865.
126. Moore B.A., Kim D., Vanner S. Neural pathways regulating Brunner's gland secretion in guinea pig duodenum in vitro. Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 279:G910-G917.
127. Moore B.A., Sharkey K.A., Mantle M. Neural mediation of cholera toxin-induced mucin secretion in the rat small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 1993, 265:G1050-G1056.
128. Moore B.A., Sharkey K.A., Mantle M. Role of 5-HT in cholera toxin-induced mucin secretion in the rat small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 1996, 270:G1001-G1009.
129. Moro F., Levenez F., Durual S., Plaisancie P., Thim L., Giraud A.S., Cuber J.C. Secretion of the trefoil factor TFF3 from the isolated vascularly perfused rat colon. Regul. Pept. 2001, 101:35-41.
130. Mueller K., Michel K., Krueger D., Demir I.E., Ceyhan G.O., Zeller F., Kreis M.E., Schemann M. Activity of protease-activated receptors in the human submucous plexus. Gastroenterology 2011, 141(2088-2097):e2081.
131. Murakami M., Ohta T., Ito S. Lipopolysaccharides enhance the action of bradykinin in enteric neurons via secretion of interleukin-1beta from enteric glial cells. J. Neurosci. Res. 2009, 87:2095-2104.
132. Natividad J.M., Verdu E.F. Modulation of intestinal barrier by intestinal microbiota: pathological and therapeutic implications. Pharmacol. Res. 2013, 69:42-51.
133. Neunlist M., Aubert P., Bonnaud S., Van Landeghem L., Coron E., Wedel T., Naveilhan P., Ruhl A., Lardeux B., Savidge T., Paris F., Galmiche J.P. Enteric glia inhibit intestinal epithelial cell proliferation partly through a TGF-beta1-dependent pathway. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292:G231-G241.
134. Neunlist M., Toumi F., Oreschkova T., Denis M., Leborgne J., Laboisse C.L., Galmiche J.P., Jarry A. Human ENS regulates the intestinal epithelial barrier permeability and a tight junction-associated protein ZO-1 via VIPergic pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:G1028-G1036.
135. Neunlist M., Van Landeghem L., Mahe M.M., Derkinderen P., des Varannes S.B., Rolli-Derkinderen M. The digestive neuronal-glial-epithelial unit: a new actor in gut health and disease. Nat. Rev. Gastroenterol. Hepatol. 2013, 10:90-100.
136. Nguyen C., Coelho A.M., Grady E., Compton S.J., Wallace J.L., Hollenberg M.D., Cenac N., Garcia-Villar R., Bueno L., Steinhoff M., Bunnett N.W., Vergnolle N. Colitis induced by proteinase-activated receptor-2 agonists is mediated by a neurogenic mechanism. Can. J. Physiol. Pharmacol. 2003, 81:920-927.
137. Nijhuis L.E., Olivier B.J., de Jonge W.J. Neurogenic regulation of dendritic cells in the intestine. Biochem. Pharmacol. 2010, 80:2002-2008.
138. O'Malley D., Quigley E.M., Dinan T.G., Cryan J.F. Do interactions between stress and immune responses lead to symptom exacerbations in irritable bowel syndrome. Brain Behav. Immun. 2011, 25:1333-1341.
139. Ochoa-Cortes F., Ramos-Lomas T., Miranda-Morales M., Spreadbury I., Ibeakanma C., Barajas-Lopez C., Vanner S. Bacterial cell products signal to mouse colonic nociceptive dorsal root ganglia neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G723-G732.
140. Ogata H., Podolsky D.K. Trefoil peptide expression and secretion is regulated by neuropeptides and acetylcholine. Am. J. Physiol. Gastrointest. Liver Physiol. 1997, 273:G348-G354.
141. Ohman L., Simren M. Intestinal microbiota and its role in irritable bowel syndrome (IBS). Curr. Gastroenterol. Rep. 2013, 15:323.
142. Ouellette A.J. Paneth cell alpha-defensins in enteric innate immunity. Cell. Mol. Life Sci. 2011, 68:2215-2229.
143. Overman E.L., Rivier J.E., Moeser A.J. CRF induces intestinal epithelial barrier injury via the release of mast cell proteases and TNF-alpha. PLoS One 2012, 7:e39935.
144. Pacheco A.R., Sperandio V. Inter-kingdom signaling: chemical language between bacteria and host. Curr. Opin. Microbiol. 2009, 12:192-198.
145. Peniche A.G., Savidge T.C., Dann S.M. Recent insights into Clostridium difficile pathogenesis. Curr. Opin. Infect. Dis. 2013, 26:447-453.
146. Perez-Burgos A., Wang B., Mao Y.K., Mistry B., McVey Neufeld K.A., Bienenstock J., Kunze W. Psychoactive bacteria Lactobacillus rhamnosus (JB-1) elicits rapid frequency facilitation in vagal afferents. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304:G211-G220.
147. Powell D.W., Mifflin R.C., Valentich J.D., Crowe S.E., Saada J.I., West A.B. Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am. J. Physiol. Cell Physiol. 1999, 277:C183-C201.
148. Powley T.L., Phillips R.J. Vagal intramuscular array afferents form complexes with interstitial cells of Cajal in gastrointestinal smooth muscle: analogues of muscle spindle organs?. Neuroscience 2011, 186:188-200.
149. Rhee S.H., Pothoulakis C., Mayer E.A. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat. Rev. Gastroenterol. Hepatol. 2009, 6:306-314.
150. Ridaura V.K., Faith J.J., Rey F.E., Cheng J., Duncan A.E., Kau A.L., Griffin N.W., Lombard V., Henrissat B., Bain J.R., Muehlbauer M.J., Ilkayeva O., Semenkovich C.F., Funai K., Hayashi D.K., Lyle B.J., Martini M.C., Ursell L.K., Clemente J.C., Van Treuren W., Walters W.A., Knight R., Newgard C.B., Heath A.C., Gordon J.I. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 2013, 341:1241214.
151. Rubino S.J., Selvanantham T., Girardin S.E., Philpott D.J. Nod-like receptors in the control of intestinal inflammation. Curr. Opin. Immunol. 2012, 24:398-404.
152. Ruhl A., Franzke S., Collins S.M., Stremmel W. Interleukin-6 expression and regulation in rat enteric glial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 280:G1163-G1171.
153. Ruhl A., Franzke S., Stremmel W. IL-1beta and IL-10 have dual effects on enteric glial cell proliferation. Neurogastroenterol. Motil. 2001, 13:89-94.
154. Rumio C., Besusso D., Arnaboldi F., Palazzo M., Selleri S., Gariboldi S., Akira S., Uematsu S., Bignami P., Ceriani V., Menard S., Balsari A. Activation of smooth muscle and myenteric plexus cells of jejunum via Toll-like receptor 4. J. Cell. Physiol. 2006, 208:47-54.
155. Salzman N.H. Paneth cell defensins and the regulation of the microbiome: detente at mucosal surfaces. Gut Microbes 2010, 1:401-406.
156. Sanders K.M., Hwang S.J., Ward S.M. Neuroeffector apparatus in gastrointestinal smooth muscle organs. J. Physiol. 2010, 588:4621-4639.
157. Santos J., Saperas E., Nogueiras C., Mourelle M., Antolin M., Cadahia A., Malagelada J.R. Release of mast cell mediators into the jejunum by cold pain stress in humans. Gastroenterology 1998, 114:640-648.
158. Santos J., Saunders P.R., Hanssen N.P., Yang P.C., Yates D., Groot J.A., Perdue M.H. Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat. Am. J. Physiol. Gastrointest. Liver Physiol. 1999, 277:G391-G399.
159. Saunders P.R., Hanssen N.P., Perdue M.H. Cholinergic nerves mediate stress-induced intestinal transport abnormalities in Wistar-Kyoto rats. Am. J. Physiol. Gastrointest. Liver Physiol. 1997, 273:G486-G490.
160. Savidge T.C. S-nitrosothiol signals in the enteric nervous system: lessons learnt from big brother. Front. Neurosci. 2011, 5:31.
161. Savidge T.C., Newman P., Pothoulakis C., Ruhl A., Neunlist M., Bourreille A., Hurst R., Sofroniew M.V. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 2007, 132:1344-1358.
162. Schaper J., Wagner A., Enigk F., Brell B., Mousa S.A., Habazettl H., Schafer M. Regional sympathetic blockade attenuates activation of intestinal macrophages and reduces gut barrier failure. Anesthesiology 2013, 118:134-142.
163. Schicho R., Schemann M., Pabst M.A., Holzer P., Lippe I.T. Capsaicin-sensitive extrinsic afferents are involved in acid-induced activation of distinct myenteric neurons in the rat stomach. Neurogastroenterol. Motil. 2003, 15:33-44.
164. Schmidt L.D., Xie Y., Lyte M., Vulchanova L., Brown D.R. Autonomic neurotransmitters modulate immunoglobulin A secretion in porcine colonic mucosa. J. Neuroimmunol. 2007, 185:20-28.
165. Schmidt P.T., Eriksen L., Loftager M., Rasmussen T.N., Holst J.J. Fast acting nervous regulation of immunoglobulin A secretion from isolated perfused porcine ileum. Gut 1999, 45:679-685.
166. Schubert M.L., Shamburek R.D. Control of acid secretion. Gastroenterol. Clin. North Am. 1990, 19:1-25.
167. Sharkey K.A., Lomax A.E., Bertrand P.P., Furness J.B. Electrophysiology, shape, and chemistry of neurons that project from guinea pig colon to inferior mesenteric ganglia. Gastroenterology 1998, 115:909-918.
168. Shen L., Weber C.R., Raleigh D.R., Yu D., Turner J.R. Tight junction pore and leak pathways: a dynamic duo. Annu. Rev. Physiol. 2011, 73:283-309.
169. Simren M., Barbara G., Flint H.J., Spiegel B.M., Spiller R.C., Vanner S., Verdu E.F., Whorwell P.J., Zoetendal E.G., Rome Foundation C. Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut 2013, 62:159-176.
170. Smith M.I., Yatsunenko T., Manary M.J., Trehan I., Mkakosya R., Cheng J., Kau A.L., Rich S.S., Concannon P., Mychaleckyj J.C., Liu J., Houpt E., Li J.V., Holmes E., Nicholson J., Knights D., Ursell L.K., Knight R., Gordon J.I. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013, 339:548-554.
171. Somasundaram K., Ganguly A.K. The effect of subdiaphragmatic vagotomy on the gastric mucus barrier in rats. Clin. Exp. Pharmacol. Physiol. 1987, 14:735-741.
172. Sommer F., Backhed F. The gut microbiota-masters of host development and physiology. Nat. Rev. Microbiol. 2013, 11:227-238.
173. Steck N., Mueller K., Schemann M., Haller D. Bacterial proteases in IBD and IBS. Gut 2012, 61:1610-1618.
174. Steinkamp M., Gundel H., Schulte N., Spaniol U., Pflueger C., Zizer E., von Boyen G.B. GDNF protects enteric glia from apoptosis: evidence for an autocrine loop. BMC Gastroenterol. 2012, 12:6.
175. Stephens R.L. Disparate effects of intracisternal RX 77368 and ODT8-SS on gastric acid and serotonin release: role of adrenal catecholamines. Regul. Pept. 1991, 36:21-28.
176. Stephens R.L., Tache Y. Intracisternal injection of a TRH analogue stimulates gastric luminal serotonin release in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 1989, 256:G377-G383.
177. Stoffels B., Hupa K.J., Snoek S.A., van Bree S., Stein K., Schwandt T., Vilz T.O., Lysson M., Veer C.V., Hornung V., Kalff J.C., de Jonge W.J., Wehner S. Post-operative ileus involves interleukin-1 receptor signaling in enteric glia. Gastroenterology 2014, 146:176-187.
178. Straub R.H., Wiest R., Strauch U.G., Harle P., Scholmerich J. The role of the sympathetic nervous system in intestinal inflammation. Gut 2006, 55:1640-1649.
179. Sun Y., Fihn B.M., Sjovall H., Jodal M. Enteric neurones modulate the colonic permeability response to luminal bile acids in rat colon in vivo. Gut 2004, 53:362-367.
180. Sun Y., Zhang M., Chen C.C., Gillilland M., Sun X., El-Zaatari M., Huffnagle G.B., Young V.B., Zhang J., Hong S.C., Chang Y.M., Gumucio D.L., Owyang C., Kao J.Y. Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice. Gastroenterology 2013, 144:1478-1487.
181. Szurszewski J.H., Ermilov L.G., Miller S.M. Prevertebral ganglia and intestinofugal afferent neurones. Gut 2002, 51(Suppl. 1):i6-i10.
182. Tixier E., Lalanne F., Just I., Galmiche J.P., Neunlist M. Human mucosa/submucosa interactions during intestinal inflammation: involvement of the enteric nervous system in interleukin-8 secretion. Cell. Microbiol. 2005, 7:1798-1810.
183. Toumi F., Neunlist M., Cassagnau E., Parois S., Laboisse C.L., Galmiche J.P., Jarry A. Human submucosal neurones regulate intestinal epithelial cell proliferation: evidence from a novel co-culture model. Neurogastroenterol. Motil. 2003, 15:239-242.
184. Turnbaugh P.J., Backhed F., Fulton L., Gordon J.I. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 2008, 3:213-223.
185. Turnbaugh P.J., Ley R.E., Mahowald M.A., Magrini V., Mardis E.R., Gordon J.I. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444:1027-1031.
186. Turner H.L., Turner J.R. Good fences make good neighbors: gastrointestinal mucosal structure. Gut Microbes 2010, 1:22-29.
187. Turner J.R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 2009, 9:799-809.
188. Valdez-Morales E.E., Overington J., Guerrero-Alba R., Ochoa-Cortes F., Ibeakanma C.O., Spreadbury I., Bunnett N.W., Beyak M., Vanner S.J. 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, 108:1634-1643.
189. Van Landeghem L., Chevalier J., Mahe M.M., Wedel T., Urvil P., Derkinderen P., Savidge T., Neunlist M. Enteric glia promote intestinal mucosal healing via activation of focal adhesion kinase and release of proEGF. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300:G976-G987.
190. Vergnolle N. Protease-activated receptors as drug targets in inflammation and pain. Pharmacol. Ther. 2009, 123:292-309.
191. von Boyen G.B., Steinkamp M., Geerling I., Reinshagen M., Schafer K.H., Adler G., Kirsch J. Proinflammatory cytokines induce neurotrophic factor expression in enteric glia: a key to the regulation of epithelial apoptosis in Crohn's disease. Inflamm. Bowel Dis. 2006, 12:346-354.
192. Ward N.L., Pieretti A., Dowd S.E., Cox S.B., Goldstein A.M. Intestinal aganglionosis is associated with early and sustained disruption of the colonic microbiome. Neurogastroenterol. Motil. 2012, 24:874-e400.
193. Xia Y., Hu H.Z., Liu S., Ren J., Zafirov D.H., Wood J.D. IL-1beta and IL-6 excite neurons and suppress nicotinic and noradrenergic neurotransmission in guinea pig enteric nervous system. J. Clin. Invest. 1999, 103:1309-1316.
194. Yu Y., Liu Z.Q., Liu X.Y., Yang L., Geng X.R., Yang G., Liu Z.G., Zheng P.Y., Yang P.C. Stress-derived corticotropin releasing factor breaches epithelial endotoxin tolerance. PLoS One 2013, 8:e65760.
195. Yuan P.Q., Million M., Wu S.V., Rivier J., Tache Y. Peripheral corticotropin releasing factor (CRF) and a novel CRF1 receptor agonist, stressin1-A activate CRF1 receptor expressing cholinergic and nitrergic myenteric neurons selectively in the colon of conscious rats. Neurogastroenterol. Motil. 2007, 19:923-936.
196. Yusta B., Holland D., Waschek J.A., Drucker D.J. Intestinotrophic glucagon-like peptide-2 (GLP-2) activates intestinal gene expression and growth factor-dependent pathways independent of the vasoactive intestinal peptide gene in mice. Endocrinology 2012, 153:2623-2632.
197. Zaki M., Coudron P.E., McCuen R.W., Harrington L., Chu S., Schubert M.L. H. pylori acutely inhibits gastric secretion by activating CGRP sensory neurons coupled to stimulation of somatostatin and inhibition of histamine secretion. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304:G715-G722.
198. Zhang Y., Li J. Carbachol ameliorates lipopolysaccharide-induced intestinal epithelial tight junction damage by down-regulating NF-kappabeta and myosin light-chain kinase pathways. Biochem. Biophys. Res. Commun. 2012, 428:321-326.
199. Zhou H., Liang H., Li Z.F., Xiang H., Liu W., Li J.G. Vagus nerve stimulation attenuates intestinal epithelial tight junctions disruption in endotoxemic mice through alpha7 nicotinic acetylcholine receptors. Shock 2013, 40:144-151.
200. Zucoloto S., de Deus D.A., Martins A.A., Muglia V.F., Kajiwara J.K., Garcia S.B. The relationship between myenteric neuronal denervation, smooth muscle thickening and epithelial cell proliferation in the rat colon. Res. Exp. Med. (Berl) 1997, 197:117-124.