Interactions between bacteria and the gut mucosa: Do enteric neurotransmitters acting on the mucosal epithelium influence intestinal colonization or infection?

Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health

Volumn , Issue , 2010, Pages 89-109

  Green, Benedict T ^a   Brown, David R ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84877093690     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4419-5576-0_5     Document Type: Chapter

References (128)

1. Al-Jahmany, A. A., Schultheiss, G., and Diener, M. 2004. Effects of dopamine on ion transport across the rat distal colon. Pflugers Arch. 448:605-612.
2. Anlauf, M., Schäfer, M. K., Eiden, L., and Weihe, E. 2003. Chemical coding of the human gastrointestinal nervous system: cholinergic, VIPergic, and catecholaminergic phenotypes. J. Comp. Neurol. 459:90-111.
3. Arciszewski, M., Pierzynowski, S., and Ekblad, E. 2005. Lipopolysaccharide induces cell death in cultured porcine myenteric neurons. Dig. Dis. Sci. 50:1661-1668.
4. Arciszewski, M. B., Sand, E., Ekblad, E. 2008. Vasoactive intestinal peptide rescues cultured rat myenteric neurons from lipopolysaccharide induced cell death. Regul Pept. 146:218-223.
5. Aschenbach, J. R., Seidler, T., Ahrens, F., Schrödl, W., Buchholz, I., Garz, B., Krüger, M., and Gäbel, G. 2003. Luminal salmonella endotoxin affects epithelial and mast cell function in the proximal colon of pigs. Scand. J. Gastroenterol. 38:719-726.
6. Bäck, N., Ahonen, M., Soinila, S., Kivilaakso, E., and Kiviluoto, T. 1995. Catecholaminesynthesizing enzymes in the rat stomach. Histochem. Cell Biol. 104:63-67.
7. Baglole, C. J., Davison, J. S., and Meddings, J. B. 2005. Epithelial distribution of neural receptors in the guinea pig small intestine. Can. J. Physiol. Pharmacol. 83:389-395.
8. Bansal, T., Englert, D., Lee, J., Hegde, M., Wood, T. K., and Jayaraman, A. 2007. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect. Immun. 75:4597-4607.
9. Barajon, I., Serrao, G., Arnaboldi, F., Opizzi, E., Ripamonti, G., Balsari, A., and Rumio, C. 2009. Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. 57:1013-1023.
10. Bates, J. M., Akerlund, J., Mittge, E., and Guillemin, K. 2007. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2:371-382.
11. Bauer, E., Williams, B. A., Smidt, H., Verstegen, M. W., and Mosenthin, R. 2006. Influence of the gastrointestinal microbiota on development of the immune system in young animals. Curr. Issues Intest. Microbiol. 7:35-51.
12. Black, I. B., Bohn, M. C., Jonakait, G. M., and Kessler, J. A. 1981. Transmitter phenotypic expression in the embryo. Ciba Found. Symp. 83:177-193.
13. Bogunovic, M., Davé, S. H., Tilstra, J. S., Chang, D. T., Harpaz, N., Xiong, H., Mayer, L. F., and Plevy, S. E. 2007. Enteroendocrine cells express functional Toll-like receptors. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1770-G1783.
14. Braun, T., Voland, P., Kunz, L., Prinz, C., and Gratzl, M. 2007. Enterochromaffin cells of the human gut: sensors for spices and odorants. Gastroenterology 132:1890-1901.
15. Brogden, K. A., Guthmiller, J. M., Salzet, M., and Zasloff, M. 2005. The nervous system and innate immunity: the neuropeptide connection. Nat. Immunol. 6:558-564.
16. Brown, D. R., and O'Grady, S. M. 1997. Regulation of ion transport in the porcine intestinal tract by enteric neurotransmitters and hormones. Comp. Biochem. Physiol. 118A:309-317.
17. Brown, D. R., and O'Grady, S. M. 2008. The Ussing chamber and measurement of drug actions on mucosal ion transport. In: Current Protocols in Pharmacology, vol 41. Wiley, NY, pp. 7.12.1-7.12.17.
18. Brown, D. R., and Price, L. D. 2007. Characterization of Salmonella enterica serovar Typhimurium DT104 invasion in an epithelial cell line (IPEC J2) from porcine small intestine. Vet. Microbiol. 120:328-333.
19. Brown, D. R., and Price, L. D. 2008. Catecholamines and sympathomimetic drugs decrease early Salmonella Typhimurium uptake into porcine Peyer's patches. FEMS Immunol. Med. Microbiol 52:29-35.
20. Burns, A. J., and Thapar, N. 2006. Advances in ontogeny of the enteric nervous system. Neurogastroenterol. Motil. 18:876-887.
21. Butta, N., Larrucea, S., Gonzalez-Manchon, C., Alonso, S., and Parrilla, R. 2004. alpha-Adrenergic-mediated activation of human reconstituted fibrinogen receptor (integrin alphaIIbbeta3) in Chinese hamster ovary cells. Thromb. Haemost. 92:1368-1376.
22. Chang, E. B., Field, M., and Miller, R. J. 1983. Enterocyte alpha 2-adrenergic receptors: yohimbine and p-aminoclonidine binding relative to ion transport. Am. J. Physiol. 244:G76-G82.
23. Chen, C., Brown, D. R., Xie, Y., Green, B. T., and Lyte, M. 2003. Catecholamines modulate Escherichia coli O157:H7 adherence to murine cecal mucosa. Shock 20:183-188.
24. Chen, C., Lyte, M., Stevens, M. P., Vulchanova, L., and Brown, D. R. 2006. Mucosally-directed adrenergic nerves and sympathomimetic drugs enhance non-intimate adherence of Escherichia coli O157:H7 to porcine cecum and colon. Eur. J. Pharmacol. 539:116-124.
25. 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.
26. Clark, M. A., and Jepson, M. A. 2003. Intestinal M cells and their role in bacterial infection. Int. J. Med. Microbiol. 293:17-39.
27. Costa, M., Brookes, S. J., and Hennig, G. W. 2000. Anatomy and physiology of the enteric nervous system. Gut 47:15-19.
28. Cotterell, D. J., Munday, K. A., and Poat, J. A. The binding of [3H]prazosin and [3H]clonidine to rat jejunal epithelial cell membranes. Biochem Pharmacol. 33:751-756.
29. Crane, J. K., Choudhari, S. S., Naeher, T. M., and Duffey, M. E. 2006. Mutual enhancement of virulence by enterotoxigenic and enteropathogenic Escherichia coli. Infect. Immun. 74:1505-1515.
30. Defaweux, V., Dorban, G., Demonceau, C., Piret, J., Jolois, O., Thellin, O., Thielen, C., Heinen, E., and Antoine, N. 2005. Interfaces between dendritic cells, other immune cells, and nerve fibres in mouse Peyer's patches: potential sites for neuroinvasion in prion diseases. Microsc. Res. Tech. 66:1-9.
31. Delahunty, M., Zennadi, R., and Telen, M. J. 2006. LW protein: a promiscuous integrin receptor activated by adrenergic signaling. Transfus. Clin. Biol. 13:44-49.
32. Ding, J., Magnotti, L. J, Huang, Q., Xu, D. Z., Condon, M. R., and Deitch, E. A. 2001. Hypoxia combined with Escherichia coli produces irreversible gut mucosal injury characterized by increased intestinal cytokine production and DNA degradation. Shock 16:189-195.
33. Donowitz, M., Cusolito, S., Battisti, L., Fogel, R., and Sharp, G. W. 1982. Dopamine stimulation of active Na and Cl absorption in rabbit ileum: interaction with alpha 2-adrenergic and specific dopamine receptors. J. Clin. Invest. 69:1008-1016.
34. Donowitz, M., Elta, G., Battisti, L., Fogel, R., and Label-Schwartz, E. 1983. Effect of dopamine and bromocriptine on rat ileal and colonic transport. Stimulation of absorption and reversal of cholera toxin-induced secretion. Gastroenterology 84:516-523.
35. Downing, J. E., and Miyan, J. A. 2000. Neural immunoregulation: emerging roles for nerves in immune homeostasis and disease. Immunol. Today 21:281-289.
36. Dupont, J. R., Jervis, H. R., and Sprinz, H. 1965. Auerbach's plexus of the rat cecum in relation to the germfree state. J. Comp. Neurol. 125:11-18.
37. Eisenhofer, G., Aneman, A., Friberg, P., Hooper, D., Fåndriks, L., Lonroth, H., Hunyady, B., and Mezey, E. 1997. Substantial production of dopamine in the human gastrointestinal tract. J. Clin. Endocrinol. Metab. 82:3864-3871.
38. Elenkov, I. J., Wilder, R. L., Chrousos, G. P., and Vizi, E. S. 2000. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol. Rev. 52:595-638.
39. Esmaili, A., Nazir, S. F., Borthakur, A., Yu, D., Turner, J. R., Saksena, S., Singla, A., Hecht, G. A., Alrefai, W. A., and Gill, R. K. 2009. Enteropathogenic Escherichia coli infection inhibits intestinal serotonin transporter function and expression. Gastroenterology 137:2074-2083.
40. Flierl, M. A., Rittirsch, D., Huber-Lang, M., Sarma, J. V., and Ward, P. A. 2008. Catecholamines - Crafty weapons in the inflammatory arsenal of immune/inflammatory cells or opening Pandora's box? Mol. Med. 14:195-204.
41. Freestone, P. P., Haigh, R. D., and Lyte, M. 2007a. Specificity of catecholamine-induced growth in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. FEMS Microbiol. Lett. 269:221-228.
42. Freestone, P. P., Haigh, R. D., and Lyte, M. 2007b. Blockade of catecholamine-induced growth by adrenergic and dopaminergic receptor antagonists in Escherichia coli O157:H7, Salmonella enterica and Yersinia enterocolitica. BMC Microbiol. 7:8.
43. Furness, J. B. 2006. The Enteric Nervous System, Blackwell, Malden, MA.
44. Fuxe, K., Ferré, S., Canals, M., Torvinen, M., Terasmaa, A., Marcellino, D., Goldberg, S. R., Staines, W., Jacobsen, K. X., Lluis, C., Woods, A. S., Agnati, L. F., and Franco, R. 2005. Adenosine A2A and dopamine D2 heteromeric receptor complexes and their function. J. Mol. Neurosci. 26:209-220.
45. Gonkowski, S., Kaminska, B., Bossowska, A., Korzon, M., Landowski, P., and Majewski, M. 2003. The influence of experimental Bacteroides fragilis infection on substance P and somatostatin-immunoreactive neural elements in the porcine ascending colon - a preliminary report. Folia Morphol. (Warsz) 62:455-457.
46. Green, B. T., and Brown, D. R. 2006. Differential effects of clathrin and actin inhibitors on internalization of Escherichia coli and Salmonella choleraesuis in porcine jejunal Peyer's patches. Vet. Microbiol. 113:117-122.
47. Green, B. T., Lyte, M., Kulkarni-Narla, A., and Brown, D. R. 2003. Neuromodulation of enteropathogen internalization in Peyer's patches from porcine jejunum. J. Neuroimmunol. 141:74-82.
48. Green, B. T., Lyte, M., Chen, C., Xie, Y., Casey, M. A., Kulkarni-Narla, A., Vulchanova, L., and Brown, D. R. 2004. Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. Am. J. Physiol. Gastrointest. Liver Physiol. 287:G1238-G1246.
49. Gu, L., Wang, H., Guo, Y.-L., and Zen, K. 2008. Heparin blocks the adhesion of E. coli O157:H7 to human colonic epithelial cells. Biochem. Biophys. Res. Comm. 369:1061-1064.
50. Hague, C., Lee, S. E., Chen, Z., Prinster, S. C., Hall, R. A., and Minneman, K. P. 2006. Heterodimers of alpha1B- and alpha1D-adrenergic receptors form a single functional entity. Mol. Pharmacol. 69:45-55.
51. Handley, S. A., Dube, P. H., and Miller, V. L. 2006. Histamine signaling through the H2 receptor in the Peyer's patch is important for controlling Yersinia enterocolitica infection. Proc. Natl. Acad. Sci. USA 103:9268-9273.
52. Harrison, C., and Traynor, J. R. 2003. The [35S]GTPgammaS binding assay: approaches and applications in pharmacology. Life Sci. 74:489-508.
53. Hecht, G., Marrero, J. A., Danilkovich, A., Matkowskyj, K. A., Savkovic, S. D., Koutsouris, A., and Benya, R. V. 1999. Pathogenic Escherichia coli increase Cl-secretion from intestinal epithelia by upregulating galanin-1 receptor expression. J. Clin. Invest. 104:253-262.
54. Hooper, L. V. 2004. Bacterial contributions to mammalian gut development. Trends Microbiol. 12:129-134.
55. Horger, S., Schultheiss, G., and Diener, M. 1998. Segment-specific effects of epinephrine on ion transport in the colon of the rat. Am. J. Physiol. 275:G1367-G1376.
56. Hori, Y., Nihei, Y., Kurokawa, Y., Kuramasu, A., Makabe-Kobayashi, Y., Terui, T., Doi, H., Satomi, S., Sakurai, E., Nagy, A., Watanabe, T., and Ohtsu, H. 2002. Accelerated clearance of Escherichia coli in experimental peritonitis of histamine-deficient mice. J. Immunol. 169:1978-1983.
57. Huidobro-Toro, J. P., and Donoso, M. V. 2004. Sympathetic co-transmission: the coordinated action of ATP and noradrenaline and their modulation by neuropeptide Y in human vascular neuroeffector junctions. Eur. J. Pharmacol. 500:27-35.
58. Irving, P. M., and Gibson, P. R. 2008. Infections and IBD. Nat. Clin. Pract. Gastroenterol. Hepatol. 5:18-27.
59. Kennedy, B., and Ziegler, M. G. 2000. Ontogeny of epinephrine metabolic pathways in the rat: role of glucocorticoids. Int. J. Dev. Neurosci. 18:53-59.
60. Kin, N. W., and Sanders, V. M. 2006. It takes nerve to tell T and B cells what to do. J. Leukoc. Biol. 79:1093-1104.
61. Kulkarni-Narla, A., Beitz, A. J., and Brown, D. R. 1999. Catecholaminergic, cholinergic and peptidergic innervation of gut-associated lymphoid tissue in porcine jejunum and ileum. Cell Tissue Res. 298:275-286.
62. Lange, S., and Delbro, D. S. 1995. Adrenoceptor-mediated modulation of Evans blue dye permeation of rat small intestine. Dig. Dis. Sci. 40:2623-2629.
63. Lawley, T. D., Bouley, D. M., Hoy, Y. E., Gerke, C., Relman, D. A., and Monack, D. M. 2008. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect. Immun. 76:403-416.
64. Levite, M., and Chowers, Y. 2001. Nerve-driven immunity: neuropeptides regulate cytokine secretion of T cells and intestinal epithelial cells in a direct, powerful and contextual manner. Ann. Oncol. 12 Suppl 2:S19-S25.
65. Levite, M., Chowers, Y., Ganor, Y., Besser, M., Hershkovits, R., and Cahalon L. 2001. Dopamine interacts directly with its D3 and D2 receptors on normal human T cells, and activates beta1 integrin function. Eur. J. Immunol. 31:3504-3512.
66. Ley, R. E., Peterson, D. A., and Gordon, J. I. 2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837-848.
67. Li, Z. S., Pham, T. D., Tamir, H., Chen, J. J., and Gershon, M. D. 2004. Enteric dopaminergic neurons: definition, developmental lineage, and effects of extrinsic denervation. J. Neurosci. 24:1330-1339.
68. Linden, D. R., and Farrugia, G. 2008. Autonomic control of gastrointestinal function. In: Clinical Autonomic Disorders, 3rd ed. Low, P. A., and Benarroch, E. E. (eds.), Lippincott Williams and Wilkins, Baltimore, pp. 88-105.
69. Llewellyn-Smith, I. J., Wilson, A. J., Furness, J. B., Costa, M., and Rush, R. A. 1981. Ultrastructural identification of noradrenergic axons and their distribution within the enteric plexuses of the guinea-pig small intestine. J. Neurocytol. 10:331-352.
70. Llewellyn-Smith, I. J., Furness, J. B., O'Brien, P. E., and Costa, M. 1984. Noradrenergic nerves in human small intestine. Distribution and ultrastructure. Gastroenterology 87:513-529.
71. Lomax, A. E., Linden, D. R., Mawe, G. M., and Sharkey, K. A. 2006. Effects of gastrointestinal inflammation on enteroendocrine cells and enteric neural reflex circuits. Auton. Neurosci. 126-127:250-257.
72. Lomax, A. E., Sharkey, K. A., and Furness, J. B. 2010. The participation of the sympathetic innervation of the gastrointestinal tract in disease states. Neurogastroenterol. Motil. 22:7-18.
73. Lundgren, O. 2002. Enteric nerves and diarrhoea. Pharmacol. Toxicol. 90:109-120.
74. Lundgren, O. 2004. Interface between the intestinal environment and the nervous system. Gut 53 Suppl 2: ii16-ii18.
75. Macpherson, A. J., and Slack, E. 2007. The functional interactions of commensal bacteria with intestinal secretory IgA. Curr. Opin. Gastroenterol. 23:673-678.
76. Malo, M. S., Biswas, S., Abedrapo, M. A., Yeh, L., Chen, A., and Hodin, R. A. 2006. The proinflammatory cytokines, IL-1beta and TNF-alpha, inhibit intestinal alkaline phosphatase gene expression. DNA Cell Biol. 25:684-695.
77. Matkowskyj, K. A., Danilkovich, A., Marrero, J., Savkovic, S. D., Hecht, G., and Benya, R. V. 2000. Galanin-1 receptor up-regulation mediates the excess colonic fluid production caused by infection with enteric pathogens. Nat. Med. 6:1048-1051.
78. Meredith, E. J., Chamba, A., Holder, M. J., Barnes, N. M., and Gordon, J. 2005. Close encounters of the monoamine kind: immune cells betray their nervous disposition. Immunology 115:289-295.
79. 1-adrenoceptor and CXCR chemokine receptor dimerization. J. Mol. Neurosci. 26:161-168.
80. Motomura, Y., Ghia, J. E., Wang, H., Akiho, H., El-Sharkawy, R. T., Collins, M., Wan, Y., McLaughlin, J. T., and Khan, W. I. 2008. Enterochromaffin cell and 5-hydroxytryptamine responses to the same infectious agent differ in Th1 and Th2 dominant environments. Gut 57:475-481.
81. Mourad, F. H., and Nassar, C. F. 2000. Effect of vasoactive intestinal polypeptide (VIP) antagonism on rat jejunal fluid and electrolyte secretion induced by cholera and Escherichia coli enterotoxins. Gut 47:382-386.
82. Mowat, A. M. 2003. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3:331-341.
83. Neunlist, M., Barouk, J., Michel, K., Just, I., Oreshkova, T., Schemann, M., and Galmiche, J. P. 2003. Toxin B of Clostridium difficile activates human VIP submucosal neurons, in part via an IL-1beta-dependent pathway. Am. J. Physiol. Gastrointest. Liver Physiol. 285:G1049-G1055.
84. Oh, C., Suzuki, S., Nakashima, I., Yamashita, K., and Nakano, K. 1988. Histamine synthesis by non-mast cells through mitogen-dependent induction of histidine decarboxylase. Immunology 65:143-148.
85. O'Hara, J. R., Skinn, A. C., MacNaughton, W. K., Sherman, P. M., and Sharkey, K. A. 2006. Consequences of Citrobacter rodentium infection on enteroendocrine cells and the enteric nervous system in the mouse colon. Cell. Microbiol. 8:646-660.
86. Olsen, P. S., Poulsen, S. S., and Kirkegaard, P. 1985. Adrenergic effects on secretion of epidermal growth factor from Brunner's glands. Gut 26:920-927.
87. Palazzo, M., Balsari, A., Rossini, A., Selleri, S., Calcaterra, C., Gariboldi, S., Zanobbio, L., Arnaboldi, F., Shirai, Y. F., Serrao, G., and Rumio, C. 2007. Activation of enteroendocrine cells via TLRs induces hormone, chemokine, and defensin secretion. J. Immunol. 178:4296-4303.
88. Pascual, D. W. 2004. The role of tachykinins on bacterial infections. Front. Biosci. 9:3209-3217.
89. Patel, P., Nankova, B. B., LaGamma, E. F. 2005. Butyrate, a gut-derived environmental signal, regulates tyrosine hydroxylase gene expression via a novel promoter element. Brain Res. Dev. Brain Res. 160:53-62.
90. Pettersson, G. 1979. The neural control of the serotonin content in mammalian enterochromaffin cells. Acta Physiol. Scand. Suppl. 470:1-30.
91. Pidsudko, Z., Kaleczyc, J., Wasowicz, K., Sienkiewicz, W., Majewski, M., Zajac, W., and Lakomy, M. 2008. Distribution and chemical coding of intramural neurons in the porcine ileum during proliferative enteropathy. J. Comp. Pathol. 138:23-31.
92. Rumio, C., Besusso, D., Arnaboldi, F., Palazzo, M., Selleri, S., Gariboldi, S., Akira, S., Uematsu, S., Bignami, P., Ceriani, V., Ménard, S., and Balsari, A. 2006. Activation of smooth muscle and myenteric plexus cells of jejunum via Toll-like receptor 4. J. Cell Physiol. 208:47-54.
93. Schäfermeyer, A., Gratzl, M., Rad, R., Dossumbekova, A., Sachs, G., and Prinz, C. 2004. Isolation and receptor profiling of ileal enterochromaffin cells. Acta Physiol. Scand. 182:53-62.
94. Schmidt, P. T., Eriksen, L., Loftager, M., Rasmussen, T. N., and Holst, J. J. 1999. Fast acting nervous regulation of immunoglobulin A secretion from isolated perfused porcine ileum. Gut 45:679-685.
95. Schmidt, L. D., Xie, Y., Lyte, M., Vulchanova, L., and Brown, D. R. 2007. Autonomic neurotransmitters modulate immunoglobulin A secretion in porcine colonic mucosa. J. Neuroimmunol. 185:20-28.
96. Schreiber, K. L., and Brown, D. R. 2005. Adrenocorticotrophic hormone modulates Escherichia coli O157:H7 adherence to porcine colonic mucosa. Stress 8:185-190.
97. Schreiber, K. L., Price, L. D., and Brown, D. R. 2007. Evidence for neuromodulation of enteropathogen invasion in the intestinal mucosa. J. Neuroimmune Pharmacol. 2:329-337.
98. Scott, L. D., and Cahall, D. L. 1982. Influence of the interdigestive myoelectric complex on enteric flora in the rat. Gastroenterology 82:737-745.
99. Senard, J. M., Langin, D., Estan, L., and Paris, H. 1990. Identification of alpha 2-adrenoceptors and non-adrenergic idazoxan binding sites in rabbit colon epithelial cells. Eur. J. Pharmacol. 191:59-68.
100. Sharma, R., and Schumacher, U. 1996. The diet and gut microflora influence the distribution of enteroendocrine cells in the rat intestine. Experientia 52:664-670.
101. Shibolet, O., and Podolsky, D. K. 2007. TLRs in the Gut. IV. Negative regulation of Toll-like receptors and intestinal homeostasis: addition by subtraction. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1469-G1473.
102. Simon, C., and Ternaux, J. P. 1990. Regulation of serotonin release from enterochromaffin cells of rat cecum mucosa. J. Pharmacol. Exp. Ther. 253:825-832.
103. Sinclair, J. F., Dean-Nystrom, E. A., and O'Brien, A. D. 2006. The established intimin receptor Tir and the putative eucaryotic intimin receptors nucleolin and beta1 integrin localize at or near the site of enterohemorrhagic Escherichia coli O157:H7 adherence to enterocytes in vivo. Infect. Immun. 74:1255-1265.
104. Snipes, R. L. 1997. Intestinal absorptive surface in mammals of different sizes. Adv. Anat. Embryol. Cell Biol. 138: III-VIII, 1-90.
105. Spiller, R. C. 2002. Role of nerves in enteric infection. Gut 51:759-762.
106. Sternini, C., Anselmi, L., and Rozengurt, E. 2008. Enteroendocrine cells: a site of 'taste' in gastrointestinal chemosensing. Curr. Opin. Endocrinol. Diabetes Obes. 15:73-78.
107. Strange, P. G. 2008. Signaling mechanisms of GPCR ligands. Curr. Opin. Drug Discov. Devel. 11:196-202.
108. Straub, R. H., Wiest, R., Strauch, U. G., Härle, P., and Schölmerich, J. 2006. The role of the sympathetic nervous system in intestinal inflammation. Gut 55:1640-1649.
109. Straub, R. H., Grum, F., Strauch, U. G., Capellino, S., Bataille, F., Bleich, A., Falk, W., Schölmerich, J., and Obermeier, F. 2008. Anti-inflammatory role of sympathetic nerves in chronic intestinal inflammation. Gut 57:911-921.
110. Suzuki, K., Ha, S. A., Tsuji, M., and Fagarasan, S. 2007. Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut. Semin. Immunol. 19:127-135.
111. Timmermans, J. P., Adriaensen, D., Cornelissen, W., and Scheuermann, D. W. 1997. Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes. Comp. Biochem. Physiol. A Physiol. 118:331-340.
112. Timmermans, J. P., Hens, J., and Adriaensen, D. 2001. Outer submucous plexus: an intrinsic nerve network involved in both secretory and motility processes in the intestine of large mammals and humans. Anat. Rec. 262:71-78.
113. Tutton, P. J., and Barkla, D. H. 1977. The influence of adrenoceptor activity on cell proliferation in colonic crypt epithelium and in colonic adenocarcinomata. Virchows Arch. B Cell. Pathol. 24:139-146.
114. Tutton, P. J., and Helme, R. D. 1974. The influence of adrenoreceptor activity on crypt cell proliferation in the rat jejunum. Cell Tissue Kinet. 7:125-136.
115. Uribe, A., Alam, M., Johansson, O., Midtvedt, T., and Theodorsson, E. 1994. Microflora modulates endocrine cells in the gastrointestinal mucosa of the rat. Gastroenterology 107:1259-1269.
116. Valet, P., Senard, J. M., Devedjian, J. C., Planat, V., Salomon, R., Voisin, T., Drean, G., Couvineau, A., Daviaud, D., Denis, C., Laburthe, M., and Paris, H. 1993. Characterization and distribution of alpha 2-adrenergic receptors in the human intestinal mucosa. J. Clin. Invest. 91:2049-2057.
117. Vasina, V., Barbara, G., Talamonti, L., Stanghellini, V., Corinaldesi, R., Tonini, M., De Ponti, F., and De Giorgio, R. 2006. Enteric neuroplasticity evoked by inflammation. Auton. Neurosci. 126-127:264-272.
118. Vieira-Coelho, M. A., and Soares-da-Silva, P. 1993. Dopamine formation, from its immediate precursor 3, 4-dihydroxyphenylalanine, along the rat digestive tract. Fundam. Clin. Pharmacol. 7:235-243.
119. Vieira-Coelho, M. A., and Soares-da-Silva, P. 1998. Alpha2-adrenoceptors mediate the effect of dopamine on adult rat jejunal electrolyte transport. Eur. J. Pharmacol. 356:59-65.
120. Vieira-Coelho, M. A., and Soares-da-Silva, P. 2001. Comparative study on sodium transport and Na+, K+-ATPase activity in Caco-2 and rat jejunal epithelial cells: effects of dopamine. Life Sci. 69:1969-1981.
121. Vlisidou, I., Lyte, M., van Diemen, P. M., Hawes, P., Monaghan, P., Wallis, T. S., and Stevens, M. P. 2004. The neuroendocrine stress hormone norepinephrine augments Escherichia coli O157:H7-induced enteritis and adherence in a bovine ligated ileal loop model of infection. Infect. Immun. 72:5446-5451.
122. Vulchanova, L., Casey, M. A., Crabb, G. W., Kennedy, W. R., and Brown, D. R. 2007. Anatomical evidence for enteric neuroimmune interactions in Peyer's patches. J. Neuroimmunol. 185:64-74.
123. Walters, N., Trunkle, T., Sura, M., and Pascual, D. W. 2005. Enhanced immunoglobulin A response and protection against Salmonella enterica serovar Typhimurium in the absence of the substance P receptor. Infect. Immun. 73:317-324.
124. Wang, B., Mao, Y. K., Diorio, C., Wang, L., Huizinga, J. D., Bienenstock, J., Kunze, W. 2010. Lactobacillus reuteri ingestion and IK (Ca) channel blockade have similar effects on rat colon motility and myenteric neurones. Neurogastroenterol. Motil. 22:98-107.
125. Wang, Y. F., Mao, Y. K., Xiao, Q., Daniel, E. E., Borkowski, K. R., McDonald, T. J. 1997. The distribution of NPY-containing nerves and the catecholamine contents of canine enteric nerve plexuses. Peptides 18:221-234.
126. Wang, H., Steeds, J., Motomura, Y., Deng, Y., Verma-Gandhu, M., El-Sharkawy, R. T., McLaughlin, J. T., Grencis, R. K., and Khan, W. I. 2007. CD4+ T cell-mediated immunological control of enterochromaffin cell hyperplasia and 5-hydroxytryptamine production in enteric infection. Gut 56:949-957.
127. Wood, J. D. 2007. Effects of bacteria on the enteric nervous system: implications for the irritable bowel syndrome. J. Clin. Gastroenterol. 41(5 Suppl 1):S7-S19.
128. 2. Am. J. Physiol. 241:G416-G421.