Effect of reflux-induced inflammation on transient receptor potential vanilloid one (TRPV1) expression in primary sensory neurons innervating the oesophagus of rats

Neurogastroenterology and Motility

Volumn 19, Issue 8, 2007, Pages 681-691

  Banerjee, B ^a   Medda, B K ^a   Lazarova, Z ^a   Bansal, N ^b   Shaker, R ^a   Sengupta, J N ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b MARQUETTE UNIVERSITY   (United States)

Author keywords

Dorsal root ganglia; Nodose ganglia; Oesophagitis; Reflux; Spinal cord; Substance P

Indexed keywords

ISOLECTIN B4; OMEPRAZOLE; PROTEIN; SUBSTANCE P; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESOPHAGITIS; ESOPHAGUS; GASTROESOPHAGEAL REFLUX; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; MALE; NODOSE GANGLION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYLORUS STENOSIS; RAT; SENSORY NERVE CELL; SPINAL CORD; SPINAL GANGLION; STOMACH FUNDUS;

ANIMALS; DISEASE MODELS, ANIMAL; ESOPHAGUS; GANGLIA, SPINAL; GASTROESOPHAGEAL REFLUX; IMMUNOHISTOCHEMISTRY; MALE; NEURONS, AFFERENT; NODOSE GANGLION; PLANT LECTINS; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANCE P; TRPV CATION CHANNELS;

EID: 34447540326     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2007.00947.x     Document Type: Article

References (56)

1. Mehta AJ, de Caestecker JS, Camm AJ, Northfield TC. Sensitization to painful distention and abnormal sensory perception in the esophagus. Gastroenterology 1995 108 : 311 9.
2. Peghini PL, Johnston BT, Leite LP, Castell DO. Mucosal acid exposure sensitizes a subset of normal subjects to intra-oesophageal balloon distension. Eur J Gastroenterol Hepatol 1996 8 : 979 83.
3. Sarkar S, Hobson AR, Furlong PL, Woolf CJ, Thompson DG, Aziz Q. Central neural mechanisms mediating human visceral hypersensitivity. Am J Physiol Gastrointest Liver Physiol 2001 281 : G1196 202.
4. Baranauskas G, Nistri A. Sensitization of pain pathways in the spinal cord: cellular mechanisms. Prog Neurobiol 1998 54 : 349 65.
5. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 2002 36 : 57 68.
6. Ji RR, Kohno T, Moore KA, Woolf CJ. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 2003 26 : 696 705.
7. Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science 2000 288 : 1765 9.
8. Ibuki T, Hama AT, Wang XT, Pappas GD, Sagen J. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 1997 76 : 845 58.
9. Patterson LM, Zheng H, Ward SM, Berthoud HR. Vanilloid receptor (VR1) expression in vagal afferent neurons innervating the gastrointestinal tract. Cell Tissue Res 2003 311 : 277 87.
10. Ward SM, Bayguinov J, Won KJ, Grundy D, Berthoud HR. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J Comp Neurol 2003 465 : 121 35.
11. Page AJ, Brierley SM, Martin CM et al. Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 2005 54 : 1408 15.
12. Fujino K, de la Fuente SG, Takami Y, Takahashi T, Mantyh CR. Attenuation of acid induced oesophagitis in VR-1 deficient mice. Gut 2006 55 : 34 40.
13. Matthews PJ, Aziz Q, Facer P, Davis JB, Thompson DG, Anand P. Increased capsaicin receptor TRPV1 nerve fibres in the inflamed human esophagus. Eur J Gastroenterol Hepatol 2004 16 : 897 902.
14. De PL, Chu CJ, Moriello AS, Kellner JC, Walker JM, Di MV. Actions of two naturally occurring saturated N-acyldopamines on transient receptor potential vanilloid 1 (TRPV1) channels. Br J Pharmacol 2004 143 : 251 6.
15. De PL, Di MV. Lipids as regulators of the activity of transient receptor potential type V1 (TRPV1) channels. Life Sci 2005 77 : 1651 66.
16. Ross RA. Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 2003 140 : 790 801.
17. Schicho R, Schemann M, Holzer P, Lippe IT. Mucosal acid challenge activates nitrergic neurons in myenteric plexus of rat stomach. Am J Physiol Gastrointest Liver Physiol 2001 281 : G1316 21.
18. Omura N, Kashiwagi H, Chen G, Suzuki Y, Yano F, Aoki T. Establishment of surgically induced chronic acid reflux esophagitis in rats 10. Scand J Gastroenterol 1999 34 : 948 53.
19. Schneider T, Issekutz AC. Quantitation of eosinophil and neutrophil infiltration into rat lung by specific assays for eosinophil peroxidase and myeloperoxidase. Application in a Brown Norway rat model of allergic pulmonary inflammation 4. J Immunol Methods 1996 198 : 1 14.
20. Drewes AM, Schipper KP, Dimcevski G et al. Multimodal assessment of pain in the esophagus: a new experimental model. Am J Physiol Gastrointest Liver Physiol 2002 283 : G95 103.
21. Pedersen J, Reddy H, Funch-Jensen P, rendt-Nielsen L, Gregersen H, Drewes AM. Differences between male and female responses to painful thermal and mechanical stimulation of the human esophagus. Dig Dis Sci 2004 49 : 1065 74.
22. Pedersen J, Reddy H, Funch-Jensen P, rendt-Nielsen L, Gregersen H, Drewes AM. Cold and heat pain assessment of the human oesophagus after experimental sensitisation with acid. Pain 2004 110 : 393 9.
23. Sarkar S, Aziz Q, Woolf CJ, Hobson AR, Thompson DG. Contribution of central sensitisation to the development of non-cardiac chest pain. Lancet 2000 356 : 1154 9.
24. Hu WH, Martin CJ, Talley NJ. Intraesophageal acid perfusion sensitizes the esophagus to mechanical distension: a Barostat study. Am J Gastroenterol 2000 95 : 2189 94.
25. Barish CF, Castell DO, Richter JE. Graded esophageal balloon distention. A new provocative test for noncardiac chest pain. Dig Dis Sci 1986 31 : 1292 8.
26. Richter JE. A critical review of current medical therapy for gastroesophageal reflux disease. J Clin Gastroenterol 1986 8 (Suppl. 1) : 72 80.
27. Garrison DW, Chandler MJ, Foreman RD. Viscerosomatic convergence onto feline spinal neurons from esophagus, heart and somatic fields: effects of inflammation. Pain 1992 49 : 373 82.
28. Medda BK, Sengupta JN, Lang IM, Shaker R. Response properties of the brainstem neurons of the cat following intra-esophageal acid-pepsin infusion. Neuroscience 2005 135 : 1285 94.
29. Hwang SJ, Oh JM, Valtschanoff JG. Expression of the vanilloid receptor TRPV1 in rat dorsal root ganglion neurons supports different roles of the receptor in visceral and cutaneous afferents. Brain Res 2005 1047 : 261 6.
30. Castagliuolo I, Keates AC, Qiu B et al. Increased substance P responses in dorsal root ganglia and intestinal macrophages during Clostridium difficile toxin A enteritis in rats. Proc Natl Acad Sci USA 1997 94 : 4788 93.
31. Vizzard MA. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 2001 21 : 125 38.
32. De GR, Barbara G, Blennerhassett P et al. Intestinal inflammation and activation of sensory nerve pathways: a functional and morphological study in the nematode infected rat 1. Gut 2001 49 : 822 7.
33. Pidsudko Z, Wasowicz K, Sienkiewicz W, Kaleczyc J, Czaja K, Lakomy M. The influence of inflammation on the expression of neuropeptides in the ileum-projecting primary sensory neurones in the pig 1. Folia Morphol (Warsz) 2003 62 : 235 7.
34. Traub RJ, Hutchcroft K, Gebhart GF. The peptide content of colonic afferents decreases following colonic inflammation. Peptides 1999 20 : 267 73.
35. Guo A, Vulchanova L, Wang J, Li X, Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 1999 11 : 946 58.
36. Tohda C, Sasaki M, Konemura T, Sasamura T, Itoh M, Kuraishi Y. Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J Neurochem 2001 76 : 1628 35.
37. Christianson JA, McIlwrath SL, Koerber HR, Davis BM. Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 2006 140 : 247 57.
38. Zwick M, Davis BM, Woodbury CJ et al. Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse 2. J Neurosci 2002 22 : 4057 65.
39. Schicho R, Liebmann I, Lippe IT. Extracellular signal-regulated kinase-1 and -2 are activated by gastric luminal injury in dorsal root ganglion neurons via N-methyl-D-aspartate receptors. Neuroscience 2005 134 : 505 14.
40. Hwang SJ, Burette A, Valtschanoff JG. VR1-positive primary afferents contact NK1-positive spinoparabrachial neurons. J Comp Neurol 2003 460 : 255 65.
41. Hwang SJ, Burette A, Rustioni A, Valtschanoff JG. Vanilloid receptor VR1-positive primary afferents are glutamatergic and contact spinal neurons that co-express neurokinin receptor NK1 and glutamate receptors. J Neurocytol 2004 33 : 321 9.
42. Horie S, Michael GJ, Priestley JV. Co-localization of TRPV1-expressing nerve fibers with calcitonin-gene-related peptide and substance P in fundus of rat stomach 9. Inflammopharmacology 2005 13 : 127 37.
43. Amaya F, Shimosato G, Nagano M et al. NGF and GDNF differentially regulate TRPV1 expression that contributes to development of inflammatory thermal hyperalgesia. Eur J Neurosci 2004 20 : 2303 10.
44. Breese NM, George AC, Pauers LE, Stucky CL. Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 2005 115 : 37 49.
45. Kollarik M, Dinh QT, Fischer A, Undem BJ. Capsaicin-sensitive and -insensitive vagal bronchopulmonary C-fibres in the mouse. J Physiol 2003 551 : 869 79.
46. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997 389 : 816 24.
47. Szallasi A, Nilsson S, Hokfelt T, Lundberg JM. Visualizing vanilloid (capsaicin) receptors in pig spinal cord by [3H]resiniferatoxin autoradiography. Brain Res 1994 655 : 237 40.
48. Szallasi A, Blumberg PM. Vanilloid receptors: new insights enhance potential as a therapeutic target. Pain 1996 68 : 195 208.
49. Szallasi A. Vanilloid-sensitive neurons: a fundamental subdivision of the peripheral nervous system. J Peripher Nerv Syst 1996 1 : 6 18.
50. Szallasi A, Joo F, Blumberg PM. Duration of desensitization and ultrastructural changes in dorsal root ganglia in rats treated with resiniferatoxin, an ultrapotent capsaicin analog. Brain Res 1989 503 : 68 72.
51. Danzer M, Samberger C, Schicho R, Lippe IT, Holzer P. Immunocytochemical characterization of rat brainstem neurons with vagal afferent input from the stomach challenged by acid or ammonia. Eur J Neurosci 2004 19 : 85 92.
52. Danzer M, Jocic M, Samberger C et al. Stomach-brain communication by vagal afferents in response to luminal acid backdiffusion, gastrin, and gastric acid secretion. Am J Physiol Gastrointest Liver Physiol 2004 286 : G403 11.
53. Holzer P, Michl T, Danzer M, Jocic M, Schicho R, Lippe IT. Surveillance of the gastrointestinal mucosa by sensory neurons. J Physiol Pharmacol 2001 52 : 505 21.
54. Michl T, Jocic M, Heinemann A, Schuligoi R, Holzer P. Vagal afferent signaling of a gastric mucosal acid insult to medullary, pontine, thalamic, hypothalamic and limbic, but not cortical, nuclei of the rat brain. Pain 2001 92 : 19 27.
55. Raybould HE. The future of GI and liver research: editorial perspectives. IV. Visceral afferents: an update. Am J Physiol Gastrointest Liver Physiol 2003 284 : G880 2.
56. Huang TY, Hanani M. Morphological and electrophysiological changes in mouse dorsal root ganglia after partial colonic obstruction. Am J Physiol Gastrointest Liver Physiol 2005 289 : G670 8.