Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia

Journal of Histochemistry and Cytochemistry

Volumn 57, Issue 11, 2009, Pages 1013-1023

  Barajon, Isabella ^a   Serrao, Graziano ^a   Arnaboldi, Francesca ^a   Opizzi, Emanuela ^a   Ripamonti, Gerlomina ^a   Balsari, Andrea ^a   Rumio, Cristiano ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

DRGs; ENS; Man; Mouse; TLR3; TLR4; TLR7; Toll like receptors

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; PARAFFIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; VIRUS RNA; TOLL LIKE RECEPTOR;

ANIMAL TISSUE; ARTICLE; BACTERIAL MEMBRANE; CENTRAL NERVOUS SYSTEM; FEMALE; GLIA CELL; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN TISSUE; ILEUM; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; INTESTINE; INTESTINE INNERVATION; LARGE INTESTINE; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; MOUSE; MYENTERIC PLEXUS; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE; SENSORY NERVE CELL; SPINAL GANGLION; ANIMAL; GENE EXPRESSION REGULATION; INNERVATION; METABOLISM;

BACTERIA (MICROORGANISMS); MURINAE; NEGIBACTERIA;

ANIMALS; ENTERIC NERVOUS SYSTEM; FEMALE; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; HUMANS; ILEUM; INTESTINE, LARGE; MICE; MYENTERIC PLEXUS; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTORS;

EID: 70449730854     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/jhc.2009.953539     Document Type: Article

References (58)

1. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783-801
2. Berthoud HR, Blackshaw LA, Brookes SJ, Grundy D (2004) Neuroanatomy of extrinsic afferents supplying the gastrointestinal tract. Neurogastroenterol Motil 16(suppl 1):28-33
3. Bomsel M, Alfsen A (2003) Entry of viruses through the epithelial barrier: pathogenic trickery. Nat Rev Mol Cell Biol 4:57-68
4. Bsibsi M, Ravid R, Gveric D, van Noort JM (2002) Broad expression of Toll-like receptors in the human central nervous system. J Neuropathol Exp Neurol 61:1013-1021
5. Cario E (2005) Bacterial interaction with cells of the intestinal mucosa: Toll-like receptors and Nod2. Gut 54:1182-1193
6. Carpentier PA, Begolka WS, Olson JK, Elhofy A, Karpus WJ, Miller SD (2005) Differential activation of astrocytes by innate and adaptive immune stimuli. Glia 49:360-374
7. Castagliuolo I, LaMont JT, Letourneau R, Kelly C, O'Keane JC, Jaffer A, Theoharides TC, et al. (1994) Neuronal involvement in the intestinal effects of clostridium difficile toxin A and vibrio cholerae enterotoxin in rat ileum. Gastroenterology 107:657-665
8. Chen JJ, Gershon AA, Li ZS, Lungu O, Gershon MD (2003) Latent and lytic infection of isolated guinea pig enteric ganglia by varicella zoster virus. J Med Virol 70(suppl 1):S71-78
9. Daffis S, Samuel MA, Suthar MS, Gale M Jr, Diamond MS (2008) Toll-like receptor 3 has a protective role against West Nile virus infection. J Virol 82:10349-10358
10. Furness JB (2000) Types of neurons in the enteric nervous system. J Auton Nerv Syst 81:87-96
11. Furrie E, Macfarlane S, Thomson G, Macfarlane GT, Microbiology & Gut Biology Group, Tayside Tissue & Tumour Bank (2005) Toll-like receptors 2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115:565-574
12. Goehler LE, Gaykema RP, Hansen MK, Anderson K, Maier SF, Watkins LR (2000) Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton Neurosci 85:49-59
13. Goehler LE, Gaykema RP, Opitz N, Reddaway R, Badr N, Lyte M (2005) Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 19:334-344
14. Goehler LE, Lyte M, Gaykema RP (2007) Infection-induced viscerosensory signals from the gut enhance anxiety: implications for psychoneuroimmunology. Brain Behav Immun 21:721-726
15. Harris G, KuoLee R, Chen W (2006) Role of Toll-like receptors in health and diseases of gastrointestinal tract. World J Gastroenterol 12:2149-2160
16. Hassan F, Islam S, Tumurkhuu G, Naiki Y, Koide N, Mori I, Yoshida T, et al. (2006) Intracellular expression of toll-like receptor 4 in neuroblastoma cells and their unresponsiveness to lipopolysaccharide. BMC Cancer 8:281-289
17. Holland-Cunz S, Goppl M, Rauch U, Bar C, Klotz M, Schafer KH (2006) Acquired intestinal aganglionosis after a lytic infection with varicella-zoster virus. J Pediatr Surg 41:e29-e31
18. Holzer P (2006) Efferent-like roles of afferent neurons in the gut: blood flow regulation and tissue protection. Auton Neurosci 125:70-75
19. Holzer P (2007) Role of visceral afferent neurons in mucosal inflammation and defense. Curr Opin Pharmacol 7:563-569
20. Holzer P, Maggi CA (1998) Dissociation of dorsal root ganglion neurons into afferent and efferent-like neurons. Neuroscience 86:389-398
21. Hooper LV, Gordon JI (2001) Commensal host-bacterial relationships in the gut. Science 292:1115-1118
22. Hosoi T, Okuma Y, Matsuda T, Nomura Y (2005) Novel pathway for LPS-induced afferent vagus nerve activation: possibile role of nodose ganglion. Auton Neurosci 120:104-107
23. Irie H, Harada Y, Yoshihashi H, Kimura T, Kojima M, Kataoka M, Saito M, et al. (1989) Spread of herpes simplex virus type-1 (Miyama 1GC strain) to the central nervous system after intraperitoneal inoculation: the role of the myenteric plexus of the gut. Arch Virol 105:247-257
24. Jackson AC, Rossiter JP, Lafon M (2006) Expression of Toll-like receptor 3 in the human cerebellar cortex in rabies, herpes simplex encephalitis, and other neurological diseases. J Neurovirol 12:229-234
25. Kamiya T, Wang L, Forsythe P, Goettsche G, Mao Y, Wang Y, Tougas G, et al. (2006) Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut 55:191-196
26. Kamm K, Hoppe S, Breves G, Schröder B, Schemann M (2004) Effects of the probiotic yeast Saccharomyces boulardii on the neurochemistry of myenteric neurones in pig jejunum. Neurogastroenterol Motil 16:53-60
27. Kawai T, Akira S (2007) Antiviral signaling through pattern recognition receptors. J Biochem 141:137-145
28. Kielian T (2006) Toll-like receptors in central nervous system glial inflammation and homeostasis. J Neurosci Res 83:711-730
29. Kordasti S, Sjöval H, Lundgren O, Svensson L (2004) Serotonin and vasoactive intestinal peptide antagonists attenuate rotavirus diarrhoea. Gut 53:952-957
30. Lafon M, Megret F, Lafage M, Prehaud C (2006) The innate immune facet of brain: human neurons express TLR-3 and sense viral dsRNA. J Mol Neurosci 29:185-194
31. Laukoetter MG, Nava P, Nusrat A (2008) Role of the intestinal barrier in inflammatory bowel disease. World J Gastroenterol 14:401-407
32. Lewis P, Lentz TL (1998) Rabies virus entry into cultured rat hippocampal neurons. J Neurocytol 27:559-573
33. Lewis SD, Butchi NB, Khaleduzzaman M, Morgan TW, Du M, Pourciau S, Baker DG, et al. (2008) Toll-like receptor 7 is not necessary for retroviral neuropathogenesis but does contribute to virus-induced neuroinflammation. J Neurovirol 17:1-11
34. Lomax AE, Linden DR, Mawe GM, Sharkey KA (2006) Effects of gastrointestinal inflammation on enteroendocrine cells and enteric neural reflex circuits. Auton Neurosci 126-127:250-257
35. Ma B, von Wasielewski R, Lindenmaier W, Dittmar KE (2007) Immmunohistochemical study of the blood and lymphatic vasculature and the innervation of mouse gut and gut-associated lymphoid tissue. Anat Histol Embryol 36:62-74
36. Macpherson AJ, Uhr T (2004a) Compartmentalization of the mucosal immune responses to commensal intestinal bacteria. Ann N Y Acad Sci 1029:36-43
37. Macpherson AJ, Uhr T (2004b) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303:1662-1665
38. McBride PA, Schulz-Schaeffer WJ, Donaldson M, Bruce M, Diringer H, Kretzschmar HA, 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
39. Ménager P, Roux P, Mégret F, Bourgeois JP, Le Sourd AM, Danckaert A, Lafage M, et al. (2009) Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Pathog 5:1-15
40. Morris AP, Estes MK (2001) Microbes and microbial toxins: paradigms for microbial-mucosal interactions. VIII. Pathological consequences of rotavirus infection and its enterotoxin. Am J Physiol Gastrointest Liver Physiol 281:G303-310
41. Morrison LA, Sidman RL, Fields BN (1991) Direct spread of reovirus from the intestinal lumen to the central nervous system through vagal autonomic nerve fibers. Proc Natl Acad Sci USA 88:3852-3856
42. Mueller S, Wimmer E, Cello J (2005) Poliovirus and poliomyelitis: a tale of guts, brains, and an accidental event. Virus Res 111:175-193
43. Neunlist M, Van Landeghem L, Bourreille A, Savidge T (2008) Neuroglial crosstalk in inflammatory bowel disease. J Intern Med 263:577-583
44. Niedergang F, Kweon MN (2005) New trends in antigen uptake in the gut mucosa. Trends Microbiol 13:485-490
45. Oberste MS, Maher K, Flemister MR, Marchetti G, Kilpatrick DR, Pallansch MA (2000) Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol 38:1170-1174
46. Ortega-Cava CF, Ishihara Shunji Rumi MA, Kawashima K, Ishimura N, Kazumori H, Udagawa J, Kadowaki Y, et al. (2003) Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J Immunol 170:3977-3985
47. Orvedahl A, Levine B (2008) Autophagy and viral neurovirulence. Cell Microbiol 10:1747-1756
48. Patterson CE, Daley JK, Rall GF (2002) Neuronal survival strategies in the face of RNA viral infection. J Infect Dis 186(suppl 2):215-219
49. Pothoulakis C, Castigliuolo I, LaMont JT (1998) Nerves and intestinal mast cells modulate responses to enterotoxins. News Physiol Sci 13:58-63
50. Rumio C, Besusso D, Arnaboldi F, Palazzo M, Selleri S, Gariboldi S, Akira S, et al. (2006) Activation of smooth muscle and myenteric plexus cells of jejunum via Toll-like receptor 4. J Cell Physiol 178:47-54
51. Selgrad M, De Giorgio R, Fini L, Cogliandro RF, Williams S, Stanghellini V, Barbara G, et al. (2009) JC virus infects the enteric glia of patients with chronic idiopathic intestinal pseudo-obstruction. Gut 58:25-32
52. Smith PD, Meng G, Salazar-Gonzalez JF, Shaw GM (2003) Macrophage HIV-1 infection and the gastrointestinal tract reservoir. J Leukoc Biol 74:642-649
53. Sobol CV, Belostotsskaya GB, Kenworthy MW (2005) Calcium signalling in rat brain neurons and differentiation of PC-12 cells induced by application of a probiotic product. Neurophysiol 3:284-293
54. Svensson L, Bergquist J, Wennerås C (2004) Neuromodulation of experimental Shigella infection reduces damage to the gut mucosa. Microbes Infect 6:256-264
55. Uronen-Hansson H, Allen J, Osman M, Squires G, Klein N, Callard RE (2004) Toll-like receptor 2 (TLR2) and TLR4 are present inside human dendritic cells, associated with microtubules and the Golgi apparatus but are not detectable on the cell surface: integrity of microtubules is required for interleukin-12 production in response to internalized bacteria. Immunology 111:173-178
56. Vasina V, Barbara G, Talamonti L, Stanghellini V, Corinaldesi R, Tonini M, De Ponti F, et al. (2006) Enteric neuroplasticity evoked by inflammation. Auton Neurosci 126-127:264-272
57. Vulchanova L, Casey MA, Crabb GW, Kennedy WR, Brown DR (2007) Anatomical evidence for enteric neuroimmune interactions in Peyer's patches. J Neuroimmunol 185:64-74
58. Wood JD (2004) Enteric neuroimmunophysiology and pathophysiology. Gastroenterology 127:635-657