Skip to main content
SpringerLink
Log in
Book cover

Microbial Endocrinology pp 89–109Cite as

Interactions Between Bacteria and the Gut Mucosa: Do Enteric Neurotransmitters Acting on the Mucosal Epithelium Influence Intestinal Colonization or Infection?

  • Chapter
  • First Online:

Abstract

The intestinal epithelium is a critical barrier between the internal and external milieux of the mammalian host. Epithelial interactions between these two host environments have been shown to be modulated by several different, cross-communicating cell types residing in the gut mucosa. These include enteric neurons, whose activity is influenced by bacterial pathogens, and their secreted products. Neurotransmitters appear to influence epithelial associations with bacteria in the intestinal lumen. For example, internalization of Salmonella enterica and Escherichia coli O157:H7 into the Peyer’s patch mucosa of the small intestine is altered after the inhibition of neural activity with saxitoxin, a neuronal sodium channel blocker. Catecholamine neurotransmitters, such as dopamine and norepinephrine, also alter bacterial internalization in Peyer’s patches. In the large intestine, norepinephrine increases the mucosal adherence of E. coli. These neurotransmitter actions are mediated by well-defined catecholamine receptors situated on the basolateral membranes of epithelial cells rather than through direct interactions with luminal bacteria. Investigations of the involvement of neuroepithelial communication in the regulation of interactions between the intestinal mucosa and luminal bacteria will provide novel insights into the mechanisms underlying bacterial colonization and pathogenesis at mucosal surfaces.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   179.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   229.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Arciszewski, M., Pierzynowski, S., and Ekblad, E. 2005. Lipopolysaccharide induces cell death in cultured porcine myenteric neurons. Dig. Dis. Sci. 50:1661-1668.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bäck, N., Ahonen, M., Soinila, S., Kivilaakso, E., and Kiviluoto, T. 1995. Catecholamine-synthesizing enzymes in the rat stomach. Histochem. Cell Biol. 104:63-67.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Burns, A.J., and Thapar, N. 2006. Advances in ontogeny of the enteric nervous system. Neurogastroenterol. Motil. 18:876-887.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Clark, M.A., and Jepson, M.A. 2003. Intestinal M cells and their role in bacterial infection. Int. J. Med. Microbiol. 293:17-39.

    Article  PubMed  CAS  Google Scholar 

  • Costa, M., Brookes, S.J., and Hennig, G.W. 2000. Anatomy and physiology of the enteric nervous system. Gut 47:15-19.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Downing, J.E., and Miyan, J.A. 2000. Neural immunoregulation: emerging roles for nerves in immune homeostasis and disease. Immunol. Today 21:281-289.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Furness, J.B. 2006. The Enteric Nervous System, Blackwell, Malden, MA.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Harrison, C., and Traynor, J.R. 2003. The [35S]GTPgammaS binding assay: approaches and applications in pharmacology. Life Sci. 74:489-508.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hooper, L.V. 2004. Bacterial contributions to mammalian gut development. Trends Microbiol. 12:129-134.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Irving, P.M., and Gibson, P.R. 2008. Infections and IBD. Nat. Clin. Pract. Gastroenterol. Hepatol. 5:18-27.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Lundgren, O. 2002. Enteric nerves and diarrhoea. Pharmacol. Toxicol. 90:109-120.

    Article  PubMed  CAS  Google Scholar 

  • Lundgren, O. 2004. Interface between the intestinal environment and the nervous system. Gut 53 Suppl 2:ii16-ii18.

    Google Scholar 

  • Macpherson, A.J., and Slack, E. 2007. The functional interactions of commensal bacteria with intestinal secretory IgA. Curr. Opin. Gastroenterol. 23:673-678.

    Article  PubMed  CAS  Google Scholar 

  • Malo, M.S., Biswas, S., Abedrapo, M.A., Yeh, L., Chen, A., and Hodin, R.A. 2006. The pro-inflammatory cytokines, IL-1beta and TNF-alpha, inhibit intestinal alkaline phosphatase gene expression. DNA Cell Biol. 25:684-695.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Milligan, G., Wilson, S., and López-Gimenez, J.F. 2005. The specificity and molecular basis of alpha 1-adrenoceptor and CXCR chemokine receptor dimerization. J. Mol. Neurosci. 26:161-168.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Mowat, A.M. 2003. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3:331-341.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Pascual, D.W. 2004. The role of tachykinins on bacterial infections. Front. Biosci. 9:3209-3217.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Pettersson, G. 1979. The neural control of the serotonin content in mammalian enterochromaffin cells. Acta Physiol. Scand. Suppl. 470:1-30.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Schreiber, K.L., and Brown, D.R. 2005. Adrenocorticotrophic hormone modulates Escherichia coli O157:H7 adherence to porcine colonic mucosa. Stress 8:185-190.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Scott, L.D., and Cahall, D.L. 1982. Influence of the interdigestive myoelectric complex on enteric flora in the rat. Gastroenterology 82:737-745.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Snipes, R.L. 1997. Intestinal absorptive surface in mammals of different sizes. Adv. Anat. Embryol. Cell Biol. 138:III-VIII, 1-90.

    PubMed  CAS  Google Scholar 

  • Spiller, R.C. 2002. Role of nerves in enteric infection. Gut 51:759-762.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Strange, P.G. 2008. Signaling mechanisms of GPCR ligands. Curr. Opin. Drug Discov. Devel. 11:196-202.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Wu, Z.C., and Gaginella, T.S. 1981. Release of [3H]norepinephrine from nerves in rat colonic mucosa: effects of norepinephrine and prostaglandin E2. Am. J. Physiol. 241:G416-G421.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. United States Department of Agriculture, Research Pharmacologist, Agricultural Research Service, 1150 E, 1400 N, Logan, UT, 84341, USA

    Benedict T. Green

  2. Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN, 55108, USA

    David R. Brown

Authors
  1. Benedict T. Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David R. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David R. Brown .

Editor information

Editors and Affiliations

  1. Health Sciences Center, School of Pharmacy, Texas Tech University, 4th Street 3601, Lubbock, 79430, USA

    Mark Lyte

  2. School of Medicine, Dept. Infection, Immunity & Inflammation, University of Leicester, Leicester, United Kingdom

    Primrose P.E. Freestone

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag New York

About this chapter

Cite this chapter

Green, B.T., Brown, D.R. (2010). Interactions Between Bacteria and the Gut Mucosa: Do Enteric Neurotransmitters Acting on the Mucosal Epithelium Influence Intestinal Colonization or Infection?. In: Lyte, M., Freestone, P. (eds) Microbial Endocrinology. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-5576-0_5

Download citation

Publish with us

Policies and ethics

Search

Navigation