Role of visceral afferent neurons in mucosal inflammation and defense

Current Opinion in Pharmacology

Volumn 7, Issue 6, 2007, Pages 563-569

  Holzer, Peter ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

3 (2,4 DIMETHOXYBENZYLIDENE)ANABASEINE; ANTIINFLAMMATORY AGENT; BACLOFEN; BICARBONATE; BRADYKININ; BUNGAROTOXIN RECEPTOR AGONIST; CAPSAZEPINE; GHRELIN; LAFUTIDINE; MELATONIN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANTIINFLAMMATORY ACTIVITY; CELL FUNCTION; DIGESTIVE SYSTEM INFLAMMATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG SYNTHESIS; GASTROESOPHAGEAL REFLUX; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL MUCOSA; GASTROINTESTINAL SECRETION; HOMEOSTASIS; HORMONE ACTION; HUMAN; ILEITIS; INTESTINE INNERVATION; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; RISK ASSESSMENT; RISK FACTOR; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STOMACH ACID; STOMACH CONTENT; STOMACH EMPTYING; STOMACH INNERVATION; STOMACH PROTECTION; VAGUS NERVE STIMULATION;

ANIMALS; GASTRIC MUCOSA; GASTROENTERITIS; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; NERVE FIBERS; NEURONS, AFFERENT; VAGUS NERVE;

EID: 36549020979     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coph.2007.09.004     Document Type: Review

References (56)

1. Holzer P. Efferent-like roles of afferent neurons in the gut: blood flow regulation and tissue protection. Auton Neurosci 125 (2006) 70-75
2. Holzer P. Treating visceral pain via molecular targets on afferent neurons: current and future. In: Pasricha P.J., Willis W.D., and Gebhart G.F. (Eds). Chronic Abdominal and Visceral Pain: Theory and Practice (2007), Informa Healthcare 245-269
3. Holzer P. Taste receptors in the gastrointestinal tract. V. Acid sensing in the gastrointestinal tract. Am J Physiol 292 (2007) G699-G705. Short review focussing on neural and non-neural mechanisms of acid sensing throughout the gastrointestinal tract, with emphasis on the roles played by acid-sensitive ion channels such as TRPV1 and ASIC3.
4. B receptor agonist baclofen reduces mechanosensitivity of afferent neurons supplying the gastrointestinal tract.
5. Omari T.I., Benninga M.A., Sansom L., Butler R.N., Dent J., and Davidson G.P. Effect of baclofen on esophagogastric motility and gastroesophageal reflux in children with gastroesophageal reflux disease: a randomized controlled trial. J Pediatr 149 (2006) 468-474
6. Grossi L., Cappello G., and Marzio L. Effect of an acute intraluminal administration of capsaicin on oesophageal motor pattern in GORD patients with ineffective oesophageal motility. Neurogastroenterol Motil 18 (2006) 632-636
7. Holzer P. Neural emergency system in the stomach. Gastroenterology 114 (1998) 823-839
8. Szolcsanyi J., and Bartho L. Capsaicin-sensitive afferents and their role in gastroprotection: an update. J Physiol (Paris) 95 (2001) 181-188
9. Akiba Y., Nakamura M., Nagata H., Kaunitz J.D., and Ishii H. Acid-sensing pathways in rat gastrointestinal mucosa. J Gastroenterol 37 Suppl 14 (2002) 133-138
10. Evangelista S. Role of sensory neurons in restitution and healing of gastric ulcers. Curr Pharm Des 12 (2006) 2977-2984
11. Holzer P., and Maggi C.A. Dissociation of dorsal root ganglion neurons into afferent and efferent-like neurons. Neuroscience 86 (1998) 389-398
12. Aihara E., Hayashi M., Sasaki Y., Kobata A., and Takeuchi K. Mechanisms underlying capsaicin-stimulated secretion in the stomach: comparison with mucosal acidification. J Pharmacol Exp Ther 315 (2005) 423-432. This study reports that although both acid and capsaicin activate a common pathway that leads to bicarbonate secretion in the murine stomach, they do so via different sensors and prostaglandin mechanisms.
13. - secretion in normal and slightly permeable stomachs. Am J Physiol 291 (2006) G464-G471
14. Ichikawa T., Kusakabe T., Gono Y., Shikama N., Hiruma H., Kawakami T., and Ishihara K. Nitric oxide synthase activity in rat gastric mucosa contributes to mucin synthesis elicited by calcitonin gene-related peptide. Biomed Res 27 (2006) 117-124
15. Mizuguchi S., Ohno T., Hattori Y., Kamata K., Arai K., Saeki T., Saigenji K., Hayashi I., Kuribayashi Y., and Majima M. Calcitonin gene-related peptide released by capsaicin suppresses myoelectrical activity of gastric smooth muscle. J Gastroenterol Hepatol 20 (2005) 611-618
16. Okajima K., and Harada N. Regulation of inflammatory responses by sensory neurons: molecular mechanism(s) and possible therapeutic applications. Curr Med Chem 13 (2006) 2241-2251
17. Shimozawa N., Okajima K., Harada N., Arai M., Ishida Y., Shimada S., Kurihara H., and Nakagata N. Contribution of sensory neurons to sex difference in the development of stress-induced gastric mucosal injury in mice. Gastroenterology 131 (2006) 1826-1834. This study reports that estrogen increases CGRP levels in dorsal root ganglia and reduces the vulnerability of the gastric mucosa to stress-induced injury.
18. Tan R., Bulbul M., Ongut G., Tosun O., and Izgut-Uysal V.N. Prostaglandins, capsaicin-sensitive sensory nerves and neutrophil infiltration, but not nitric oxide, contribute to cold restraint stress-induced gastric adaptation in rats. Clin Exp Pharmacol Physiol 33 (2006) 946-951
19. Shimozawa N., Okajima K., and Harada N. Estrogen and isoflavone attenuate stress-induced gastric mucosal injury by inhibiting decreases in gastric tissue levels of CGRP in ovariectomized rats. Am J Physiol 292 (2007) G615-G619
20. Fukushima K., Aoi Y., Kato S., and Takeuchi K. Gastro-protective action of lafutidine mediated by capsaicin-sensitive afferent neurons without interaction with TRPV1 and involvement of endogenous prostaglandins. World J Gastroenterol 12 (2006) 3031-3037
21. 2-receptor antagonist, through enhancement of sensory neuron activation contributes to the reduction of stress-induced gastric mucosal injury in rats. Dig Dis Sci 52 (2007) 469-477
22. Domotor A., Kereskay L., Szekeres G., Hunyady B., Szolcsanyi J., and Mozsik G. Participation of capsaicin-sensitive afferent nerves in the gastric mucosa of patients with Helicobacter pylori-positive or -negative chronic gastritis. Dig Dis Sci 52 (2007) 411-417
23. Mönnikes H., van der Voort I.R., Wollenberg B., Heymann-Mönnikes I., Tebbe J.J., Alt W., Arnold R., Klapp B.F., Wiedenmann B., and McGregor G.P. Gastric perception thresholds are low and sensory neuropeptide levels high in Helicobacter pylori-positive functional dyspepsia. Digestion 71 (2005) 111-123
24. 2 in the mucus gel layer, carbonic anhydrase in the epithelial cells, the basolateral sodium-proton exchanger-1, and TRPV1 on sensory neurons releasing CGRP.
25. Montrose M.H., Akiba Y., Takeuchi K., and Kaunitz J.D. Gastroduodenal mucosal defense. In: Johnson L.R. (Ed). Physiology of the Gastrointestinal Tract. edn 4 (2006), Academic Press 1259-1291
26. Holzer P. TRPV1 and the gut: from a tasty receptor for a painful vanilloid to a key player in hyperalgesia. Eur J Pharmacol 500 (2004) 231-241
27. Schicho R., Florian W., Liebmann I., Holzer P., and Lippe I.T. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur J Neurosci 19 (2004) 1811-1818
28. Brierley S.M., Carter R., Jones III W., Xu L., Robinson D.R., Hicks G.A., Gebhart G.F., and Blackshaw L.A. Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol (Lond) 567 (2005) 267-281
29. Faussone-Pellegrini M.S., Taddei A., Bizzoco E., Lazzeri M., Vannucchi M.G., and Bechi P. Distribution of the vanilloid (capsaicin) receptor type 1 in the human stomach. Histochem Cell Biol 124 (2005) 61-68
30. Horie S., Michael G.J., and Priestley J.V. Co-localization of TRPV1-expressing nerve fibers with calcitonin-gene-related peptide and substance P in fundus of rat stomach. Inflammopharmacology 13 (2005) 127-137
31. Christianson J.A., McIlwrath S.L., Koerber H.R., and Davis B.M. Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 140 (2006) 247-257
32. Christianson J.A., Traub R.J., and Davis B.M. Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. J Comp Neurol 494 (2006) 246-259
33. Tashima K., Nakashima M., Kagawa S., Kato S., and Takeuchi K. Gastric hyperemic response induced by acid back-diffusion in rat stomachs following barrier disruption - relation to vanilloid type-1 receptors. Med Sci Monit 8 (2002) BR157-BR163
34. Kato S., Aihara E., Nakamura A., Xin H., Matsui H., Kohama K., and Takeuchi K. Expression of vanilloid receptors in rat gastric epithelial cells: role in cellular protection. Biochem Pharmacol 66 (2003) 1115-1121
35. Horie S., Yamamoto H., Michael G.J., Uchida M., Belai A., Watanabe K., Priestley J.V., and Murayama T. Protective role of vanilloid receptor type 1 in HCl-induced gastric mucosal lesions in rats. Scand J Gastroenterol 39 (2004) 303-312
36. - response. Dig Dis Sci 48 (2003) 1850-1856
37. Holzer P. Acid-sensitive ion channels in gastrointestinal function. Curr Opin Pharmacol 3 (2003) 618-625
38. Page A.J., Brierley S.M., Martin C.M., Price M.P., Symonds E., Butler R., Wemmie J.A., and Blackshaw L.A. Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 54 (2005) 1408-1415
39. Wultsch T, Painsipp E, Shahbazian A, Mitrovic M, Edelsbrunner M, Lazdunski M, Waldmann R, Holzer P: Deletion of the acid-sensing ion channel ASIC3 prevents gastritis-induced acid hyperresponsiveness of the stomach-brainstem axis. Pain 2007, in press.
40. Jones R.C., Xu L., and Gebhart G.F. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J Neurosci 25 (2005) 10981-10989
41. Burdyga G., Varro A., Dimaline R., Thompson D.G., and Dockray G.J. Ghrelin receptors in rat and human nodose ganglia: putative role in regulating CB-1 and MCH receptor abundance. Am J Physiol 290 (2006) G1289-G1297
42. Konturek P.C., Brzozowski T., Walter B., Burnat G., Hess T., Hahn E.G., and Konturek S.J. Ghrelin-induced gastroprotection against ischemia-reperfusion injury involves an activation of sensory afferent nerves and hyperemia mediated by nitric oxide. Eur J Pharmacol 536 (2006) 171-181. This study reports that the gastric orexigenic hormone ghrelin protects the gastric mucosa from ischemia-reperfusion-induced injury and promotes healing of gastric lesions through stimulation of sensory neurons.
43. Brzozowski T., Konturek P.C., Zwirska-Korczala K., Konturek S.J., Brzozowska I., Drozdowicz D., Sliwowski Z., Pawlik M., Pawlik W.W., and Hahn E.G. Importance of the pineal gland, endogenous prostaglandins and sensory nerves in the gastroprotective actions of central and peripheral melatonin against stress-induced damage. J Pineal Res 39 (2005) 375-385
44. Larauche M., Anton P.M., Peiro G., Eutamene H., Bueno L., and Fioramonti J. Role of capsaicin-sensitive afferent nerves in different models of gastric inflammation in rats. Auton Neurosci 110 (2004) 89-97
45. Kimball E.S., Wallace N.H., Schneider C.R., D'Andrea M.R., and Hornby P.J. Vanilloid receptor 1 antagonists attenuate disease severity in dextran sulphate sodium-induced colitis in mice. Neurogastroenterol Motil 16 (2004) 811-818
46. McVey D.C., Schmid P.C., Schmid H.H., and Vigna S.R. Endocannabinoids induce ileitis in rats via the capsaicin receptor (VR1). J Pharmacol Exp Ther 304 (2003) 713-722
47. + sensory neurons control beta cell stress and islet inflammation in autoimmune diabetes. Cell 127 (2006) 1123-1135
48. Massa F., Sibaev A., Marsicano G., Blaudzun H., Storr M., and Lutz B. Vanilloid receptor (TRPV1)-deficient mice show increased susceptibility to dinitrobenzene sulfonic acid induced colitis. J Mol Med 84 (2006) 142-146
49. Schicho R., Krueger D., Zeller F., Von Weyhern C.W., Frieling T., Kimura H., Ishii I., De Giorgio R., Campi B., and Schemann M. Hydrogen sulfide is a novel prosecretory neuromodulator in the Guinea-pig and human colon. Gastroenterology 131 (2006) 1542-1552
50. Goehler L.E., Gaykema R.P.A., Hansen M.K., Anderson K., Maier S.F., and Watkins L.R. Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton Neurosci Basic Clin 85 (2000) 49-59
51. Konsman J.P., Parnet P., and Dantzer R. Cytokine-induced sickness behaviour: mechanisms and implications. Trends Neurosci 25 (2002) 154-159
52. Pavlov V.A., and Tracey K.J. The cholinergic anti-inflammatory pathway. Brain Behav Immun 19 (2005) 493-499. Concise review of the vagal cholinergic anti-inflammatory pathway that leads to suppression of cytokine release from immune cells and inhibition of inflammation.
53. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., Li J.H., Wang H., Yang H., Ulloa L., et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421 (2003) 384-388
54. Pavlov V.A., Ochani M., Yang L.H., Gallowitsch-Puerta M., Ochani K., Lin X., Levi J., Parrish W.R., Rosas-Ballina M., Czura C.J., et al. Selective alpha7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Crit Care Med 35 (2007) 1139-1144
55. Ghia J.E., Blennerhassett P., Kumar-Ondiveeran H., Verdu E.F., and Collins S.M. The vagus nerve: a tonic inhibitory influence associated with inflammatory bowel disease in a murine model. Gastroenterology 131 (2006) 1122-1130. This study reports that the vagus nerve plays an anti-inflammatory role in dextrane sulfate sodium-evoked colitis. The anti-inflammatory effect involves nicotinic acetylcholine receptors and a macrophage-dependent mechanism.
56. de Jonge W.J., van der Zanden E.P., The F.O., Bijlsma M.F., van Westerloo D.J., Bennink R.J., Berthoud H.R., Uematsu S., Akira S., van den Wijngaard R.M., and Boeckxstaens G.E. Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2-STAT3 signaling pathway. Nat Immunol 6 (2005) 844-851. This study reports that experimentally induced postoperative inflammation and gastric ileus are attenuated by stimulation of the vagus nerve. This anti-inflammatory effect depends on activation of the Jak2-STAT3 signaling pathway in macrophages.