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Research Article

Oral Delivery of Pathogens from the Intestine to the Nervous System

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Pages 71-78 | Published online: 03 Oct 2008

References

  • Aguzzi, A., Montrasio, F. and Kaeser, P.S. (2001) “Prions: health scare and biological challenge”, Nat. Rev. Mol. Cell Biol. 2, 118–126. Aguzzi, A., Heppner, F.L., Heikenwalder, M., Prinz, M., Mertz, K., Seeger, H. and Glatzel, M. (2003) “Immune system and peripheral nerves in propagation of prions to CNS”, Br. Med. Bull. 66, 141–159.
  • Anisman, H., Baines, M.G., Berczi, I., Bernstein, C.N., Blennerhassett, M.G., Gorczynski, R.M., Greenberg, A.H., Kisil, F.T., Mathison, R.D., Nagy, E., Nance, D.M., Perdue, M.H., Pomerantz, D.K., Sabbadini, E.R., Stanisz, A. and Warrington, R.J. (1996a) “Neuroimmune mechanisms in health and disease: 1. Health”, CMAJ 155, 867–874.
  • Anisman, H., Baines, M.G., Berczi, I., Bernstein, C.N., Blennerhassett, M.G., Gorczynski, R.M., Greenberg, A.H., Kisil, F.T., Mathison, R.D., Nagy, E., Nance, D.M., Perdue, M.H., Pomerantz, D.K., Sabbadini, E.R., Stanisz, A. and Warrington, R.J. (1996b) “Neuroimmune mechanisms in health and disease: 2. Disease”, CMAJ 155, 1075–1082.
  • Atwood, W.J., Berger, J.R., Kaderman, R., Tornatore, C.S. and Major, E.O. (1993) “Human immunodeficiency virus type 1 infection of the brain”, Clin. Microbiol. Rev. 6, 339–366.
  • Aucouturier, P. and Carnaud, C.J. (2002) “The immune system and prion diseases: a relationship of complicity and blindness”, Leukoc. Biol. 72, 1075–1083.
  • Bailey, M., Plunkett, F.J., Rothkotter, H.J., Vega-Lopez, M.A., Haverson, K. and Stokes, C.R. (2001) “Regulation of mucosal immune responses in effector sites”, Proc. Nutr. Soc. 60, 427– 435.
  • Bartz, J.C., Kincaid, A.E. and Bessen, R.A. (2002) “Rapid prion neuroinvasion following tongue infection”, J. Virol. 77, 583–591.
  • Bartz, J.C., Kincaid, A.E. and Bessen, R.A. (2003) “Rapid prion neuro- invasion following tongue infection”, J. Virol. 77, 583–591.
  • Bearer, E.L. and Satpute-Krishnan, P. (2002) “The role of the cyto- skeleton in the life cycle of viruses and intracellular bacteria: tracks, motors, and polymerization machines”, Curr. Drug Targets. Infect. Disord. 2, 247–264.
  • Beekes, M. and McBride, P.A. (2000) “Early accumulation of pathological PrP in the enteric nervous system and gut-associated lymphoid tissue of hamsters orally infected with scrapie”, Neurosci. Lett. 278, 181–184.
  • Blomer, U., Ganser, A. and Scherr, M. (2002) “Invasive drug delivery”, Adv. Exp. Med. Biol. 513, 431–451.
  • Bloom, P.D. and Boedeker, E.C. (1996) “Mucosal immune responses to intestinal bacterial pathogens”, Semin. Gastrointest. Dis. 7, 151–166.
  • Blumberg, R.S., Lencer, W.I., Zhu, X., Kim, H.S., Claypool, S., Balk, S.P., Saubermann, L.J. and Colgan, S.P. (1999) “Antigen presentation by intestinal epithelial cells”, Immunol. Lett. 69, 7–11.
  • Brayden, D.J. and Baird, A.W. (2001) “Microparticle vaccine approaches to stimulate mucosal immunisation”, Microbes Infect. 3, 867– 876.
  • Brown, K.L., Stewart, K., Ritchie, D.L., Mabbott, N.A., Williams, A., Fraser, H., Morrison, W.I. and Bruce, M.E. (1999) “Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells”, Nat. Med. 5, 1308–1312.
  • Brown, K.L., Ritchie, D.L., McBride, P.A. and Bruce, M.E. (2000) “Detection of PrP in extraneural tissues”, Microsc. Res. 50, 40–45.
  • Charlton, K.M. (1994) “The pathogenesis of rabies and other lyssaviral infections: recent studies”, Curr. Top. Microbiol. Immunol. 187, 95–119.
  • Chen, J.J., Gershon, A.A., Li, Z.S., Lungu, O. and Gershon, M.D. (2003) “Latent and lytic infection of isolated guinea pig enteric ganglia by varicella zoster virus”, J. Med. Virol. 70 (Suppl. 1), S71–S78.
  • Clark, M.A. and Jepson, M.A. (2003) “Intestinal M cells and their role in bacterial infection”, Int. J. Med. Microbiol. 293, 17–39.
  • Clark, M.A., Jepson, M.A. and Hirst, B.H. (2001) “Exploiting M cells for drug and vaccine delivery”, Adv. Drug Deliv. Rev. 50, 81–106.
  • Collins, S.M. (2001) “Peripheral mechanisms of symptom generation in irritable bowel syndrome”, Can. J. Gastroenterol. 15, 14B-16B, Review.
  • Cooke, H.J. (2000) “Neurotransmitters in neuronal reflexes regulating intestinal secretion”, Ann. N.Y. Acad. Sci. 915, 77–80.
  • Didierlaurent, A., Sirard, J.C., Kraehenbuhl, J.P. and Neutra, M.R. (2002) “How the gut senses its content”, Cell. Microbiol. 4, 61–72.
  • Dowdle, W.R., De Gourville, E., Kew, O.M., Pallansch, M.A. and Wood, D.J. (2003) “Polio eradication: the OPV paradox”, Rev. Med. Virol. 13, 277–291.
  • Downing, J.E. and Miyan, J.A. (2000) “Neural immunoregulation: emerging roles for nerves in immune homeostasis and disease”, Immunol. Today 21, 281–289.
  • Dramsi, S. and Cossart, P. (1998) “Intracellular pathogens and the actin cytoskeleton”, Annu. Rev. Cell. Dev. Biol. 14, 137–166.
  • Drevets, D.A. (1999) “Dissemination of Listeria monocytogenes by infected phagocytes”, Infect. Immun. 67, 3512–3517.
  • Dvorak, A.M., Osage, J.E., Monanhan, R.A. and Dickersin, G.R. (1980) “Crohn’s disease: transmission electron microscopic studies. III. Target tissues. Proliferation of and injury to smooth muscle and the autonomic nervous system”, Human Pathol. 11, 620–634.
  • Enquist, L.W. (2002) “Exploiting circuit-specific spread of pseudorabies virus in the central nervous system: insights to pathogenesis and circuit tracers”, J. Infect. Dis. 186, S209–S214.
  • Falk, P.G., Hooper, L.V., Midtvedt, T. and Gordon, J.I. (1998) “Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology”, Microbiol. Mol. Biol. Rev. 62, 1157–1170.
  • Feher, E., Altdorfer, K., Bagameri, G. and Feher, J. (2001) “Neuro- immune interactions in experimental colitis. An immuno- electron microscopic study”, Neuroimmunomodulation 9, 247–255.
  • Finke, D. and Kraehenbuhl, J.P. (2001) “Formation of Peyer’s patches”, Curr. Opin. Genet. Dev. 11, 561–567, Review.
  • Ford, M.J., Burton, L.J., Morris, R.J. and Hall, S.M. (2002) “Selective expression of prion protein in peripheral tissues of the adult mouse”, Neuroscience 113, 177–192.
  • Fournier, J.G. (2001) “Nonneuronal cellular prion protein”, Int. Rev. Cytol. 208, 121–160.
  • Genton, L. and Kudsk, K.A. (2003) “Interactions between the enteric nervous system and the immune system: role of neuropeptides and nutrition”, Am. J. Surg. 186, 253–258.
  • Ghani, A.C., Donnelly, C.A., Ferguson, N.M. and Anderson, R.M. (2003) “Updated projections of future vCJD deaths in the UK”, BMC Infect. Dis. 3, 4.
  • Ghosh, S. (2002) “Intestinal entry of prions”, Z. Gastroenterol. 40, 37–39.
  • Giaroni, C., De Ponti, F., Cosentino, M., Lecchini, S. and Frigo, G. (1999) “Plasticity in the enteric nervous system”, Gastroenterology 117, 1438–1458.
  • Glatzel, M., Heppner, F.L., Albers, K.M. and Aguzzi, A. (2001) “Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion”, Neuron 31, 25–34.
  • Gombojav, A., Ishiguro, N., Horiuchi, M., Serjmyadag, D. and Byambaa, B. (2003) “Amino acid polymorphisms of PrP gene in Mongolian sheep”, J. Vet. Med. Sci. 65, 75–81.
  • 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.
  • Hainfellner, J.A. and Budka, H. (1999) “Disease associated prion protein may deposit in the peripheral nervous system in human transmissible spongiform encephalopathies”, Acta Neuropathol. (Berl.) 98, 458–460.
  • Hansen, M.B. (2003) “The enteric nervous system II: gastrointestinal functions”, Pharmacol. Toxicol. 92, 249–257.
  • Heggebo, R., Gonzalez, L., Press, C.M., Gunnes, G., Espenes, A. and Jeffrey, M. (2003) “Disease-associated PrP in the enteric nervous system of scrapie-affected Suffolk sheep”, J. Gen. Virol. 84, 1327– 1338.
  • Heppner, F.L., Christ, A.D., Klein, M.A., Prinz, M., Fried, M., Kraehenbuhl, J.P. and Aguzzi, A. (2001) “Transepithelial prion transport by M cells”, Nat. Med. 7, 976–977.
  • Hershberg, R.M. and Mayer, L.F. (2000) “Antigen processing and presentation by intestinal epithelial cells—polarity and complexity”, Immunol. Today 21, 123–128.
  • Hirokawa, N. (1997) “The mechanisms of fast and slow transport in neurons: identification and characterization of the new kinesin superfamily motors”, Curr. Opin. Neurobiol. 7, 605–614.
  • Holt, P.G. (2000) “Parasites, atopy, and the hygiene hypothesis: resolution of a paradox?”, Lancet 356, 1699–1701.
  • Houston, F., Goldmann, W., Chong, A., Jeffrey, M., Gonzalez, L., Foster, J., Parnham, D. and Hunter, N. (2003) “Prion diseases: BSE in sheep bred for resistance to infection”, Nature 423, 498.
  • Holzer, P., Michl, T., Danzer, M., Jocic, M., Schicho, R. and Lippe, I.T. (2001) “Surveillance of the gastrointestinal mucosa by sensory neurons”, J. Physiol. Pharmacol. 52, 505–521.
  • Huang, F.P., Farquhar, C.F., Mabbott, N.A., Bruce, M.E. and MacPherson, G.G. (2002) “Migrating intestinal dendritic cells transport PrP(Sc) from the gut”, J. Gen. Virol. 83, 267–271.
  • Jones, S.L. and Blikslager, A.T. (2002) “Role of the enteric nervous system in the pathophysiology of secretory diarrhea”, J. Vet. Intern. Med. 16, 222–228.
  • Kimberlin, R.H. and Walker, C.A. (1989) “Pathogenesis of scrapie in mice after intragastric infection”, Virus Res. 12, 213–220.
  • Kimberlin, R.H., Hall, S.M. and Walker, C.A. (1983) “Pathogenesis of mouse scrapie. Evidence for direct neural spread of infection to the CNS after injection of sciatic nerve”, J. Neurol. Sci. 61, 315–325.
  • Kinnunen, E., Junttila, O., Haukka, J. and Hovi, T. (1998) “Nationwide oral poliovirus vaccination campaign and the incidence of Guillain- Barre Syndrome”, Am. J. Epidemiol. 147, 69–73.
  • Kitamoto, T., Mohri, S., Ironside, J.W., Miyoshi, I., Tanaka, T., Kitamoto, N., Itohara, S., Kasai, N., Katsuki, M., Higuchi, J., Muramoto, T. and
  • Shin, R.W. (2002) “Follicular dendritic cell of the knock-in mouse provides a new bioassay for human prions”, Biochem. Biophys. Res. Commun. 294, 280–286.
  • Kraehenbuhl, J.P. and Neutra, M.R. (2000) “Epithelial M cells: differentiation and function”, Annu. Rev. Cell Dev. Biol. 16, 301–332, Review.
  • Kraehenbuhl, J.P., Hopkins, S.A., Kerneis, S. and Pringault, E. (1997) “Antigen sampling by epithelial tissues: implication for vaccine design”, Behring. Inst. Mitt. 98, 24–32.
  • Kraehenbuhl, J.P., Pringault, E. and Neutra, M.R. (2004) “Intestinal epithelia and barrier functions”, Aliment. Pharmacol. Ther. 11, 8–9, Review.
  • Krammer, H.J. and Kuhnel, W. (1993) “Topography of the enteric nervous system in Peyer’s patches of the porcine small intestine”, Cell. Tissue Res. 272, 267–272.
  • Kunze, W.A. and Furness, J.B. (1999) “The enteric nervous system and regulation of intestinal motility”, Annu. Rev. Physiol. 61, 117– 142.
  • Kunzi, V., Glatzel, M., Nakano, M.Y., Greber, U.F., Van Leuven, F. and Aguzzi, A. (2002) “Unhampered prion neuroinvasion despite impaired fast axonal transport in transgenic mice overexpressing four-repeat tau”, J. Neurosci. 22, 7471–7477.
  • Mabbott, N.A. and Bruce, M.E. (2002) “Follicular dendritic cells as targets for intervention in transmissible spongiform encephalo- pathies”, Semin. Immunol. 14, 285–293.
  • Mabbott, N.A., Young, J., McConnell, I. and Bruce, M.E. (2003) “Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility”, J. Virol. 77, 6845–6854.
  • Matthews, D. and Cooke, B.C. (2003) “The potential for transmissible spongiform encephalopathies in non-ruminant livestock and fish”, Rev. Sci. Tech. 22, 283–296.
  • Mayer, L. (1998) “Current concepts in mucosal immunity. I. Antigen presentation in the intestine: new rules and regulations”, Am. J. Physiol. 274, G7–G9.
  • McBride, P.A., Schulz-Schaeffer, W.J., Donaldson, M., Bruce, M., Diringer, H., Kretzschmar, H.A. and Beekes, M. (2001) “Early spread of scrapie from the gastrointestinal tract to the central nervous system involves autonomic fibers of the splanchnic and vagus nerves”, J. Virol. 75, 9320–9327.
  • Mettenleiter, T.C. (2003) “Pathogenesis of neurotropic herpesviruses: role of viral glycoproteins in neuroinvasion and transneuronal spread”, Virus Res. 92, 197–206.
  • Morel, E., Fouquet, S., Chateau, D., Yvernault, L., Frobert, Y., Pincon-Raymond, M., Chambaz, J., Pillot, T. and Rousset, M. (2003) “The cellular prion protein PrPc is expressed in human enterocytes in cell-cell junctional domains”, J. Biol. Chem., Epub ahead of print.
  • Mowat, A.M. and Viney, J.L. (1997) “The anatomical basis of intestinal immunity”, Immunol. Rev. 156, 145–166.
  • Neutra, M.R., Mantis, N.J. and Kraehenbuhl, J.P. (2001) “Collaboration of epithelial cells with organized mucosal lymphoid tissues”, Nat. Immunol. 2, 1004–1009.
  • Press, C. McL., Heggebø, R. and Espenes, A. (2004) “Involvement of gut-associated lymphoid tissue of ruminants in the spread of transmissible spongiform encephalopathies”, Adv. Drug Del. Rev. 56, 885–899.
  • Prinz, M., Heikenwalder, M., Junt, T., Schwarz, P., Glatzel, M., Heppner, F.L., Fu, Y.X., Lipp, M. and Aguzzi, A. (2003b) “Positioning of follicular dendritic cells within the spleen controls prion neuro- invasion”, Nature 425, 957–962.
  • Race, R., Oldstone, M. and Chesebro, B. (2000) “Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: role of prion protein expression in peripheral nerves and spleen”, J. Virol. 74, 828–833.
  • Raeber, A.J., Montrasio, F., Hegyi, I., Frigg, R., Klein, M.A., Aguzzi, A. and Weissmann, C. (2001) “Studies on prion replication in spleen”, Dev. Immunol. 8, 291–304.
  • Santos, J. and Perdue, M.H. (2000) “Stress and neuroimmune regulation of gut mucosal function”, Gut 47, 49–51.
  • Shanahan, F. (1999) “Intestinal lymphoepithelial communication”, Adv. Exp. Med. Biol. 473, 1–9.
  • Shao, L., Serrano, D. and Mayer, L. (2001) “The role of epithelial cells in immune regulation in the gut”, Semin. Immunol. 13, 163–176.
  • Sharkey, K.A. and Kroese, A.B. (2001) “Consequences of intestinal inflammation on the enteric nervous system: neuronal activation induced by inflammatory mediators”, Anat. Rec. 262, 79–90.
  • Shmakov, A.N., McLennan, N.F., McBride, P., Farquhar, C.F., Bode, J., Rennison, K.A. and Ghosh, S. (2000) “Cellular prion protein is expressed in the human enteric nervous system”, Nat. Med. 6, 840–841.
  • Shtylik, A.V., Otellin, V.A. and Nozdrachev, A.D. (1998) “Innervation of grouped lymphoid nodules (Peyer’s patches) by the enteric nervous system and the topography of their interior neural elements in the rat”, Morfologiia 114, 34–39.
  • Sitohy, B. and El-Salhy, M. (2002) “Changes in the colonic enteric nervous system in rats with chemically induced colon dysplasia and carcinoma”, Acta Oncol. 41, 543–549.
  • Smith, G.A., Gross, S.P. and Enquist, L.W. (2001) “Herpes viruses use bidirectional fast-axonal transport to spread in sensory neurons”, Proc. Natl Acad. Sci. USA 98, 3466–3470.
  • Stead, R.H. (1992) “Innervation of mucosal immune cells in the gastrointestinal tract”, Reg. Immunol. 4, 91–99.
  • Thackray, A.M., Klein, M.A. and Bujdoso, R. (2003) “Subclinical prion disease induced by oral inoculation”, J. Virol. 77, 7991–7998.
  • Thomzig, A., Kratzel, C., Lenz, G., Kruger, D. and Beekes, M. (2003) “Widespread PrPSc accumulation in muscles of hamsters orally infected with scrapie”, EMBO Rep. 4, 530–533.
  • Vajdy, M. (2003) “Induction of optimal immune responses against human immunodeficiency virus at mucosal portals of entry”, Curr. Drug Targets Immune Endocr. Metabol. Disord. 3, 222–233.
  • Williams, R.M., Bienenstock, J. and Stead, R.H. (1995) “Mast cells: the neuroimmune connection”, Chem. Immunol. 61, 208–235.
  • Yamanaka, T., Helgeland, L., Farstad, I.N., Fukushima, H., Midtvedt, T. and Brandtzaeg, P. (2003) “Microbial colonization drives lymphocyte accumulation and differentiation in the follicle-associated epithelium of Peyer’s patches”, J. Immunol. 170, 816–822.
  • Zhao, H., Otaki, J.M. and Firestein, S. (1996) “Adenovirus- mediated gene transfer in olfactory neurons in vivo”, J. Neurobiol. 30, 521–530.
  • Zho, F. and Neutra, M.R. (2002) “Antigen delivery to mucosa-associated lymphoid tissues using liposomes as a carrier”, Biosci. Rep. 22, 355–369, Review.

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