The role of transient receptor potential vanilloid 1 (Trpv1) receptors in dextran sulfate-induced colitis in mice

Journal of Molecular Neuroscience

Volumn 42, Issue 1, 2010, Pages 80-88

  Szitter, Istvan ^a   Pozsgai, Gabor ^a   Sandor, Katalin ^a   Elekes, Krisztian ^a   Kemeny, Agnes ^a   Perkecz, Aniko ^a   Szolcsanyi, Janos ^a   Helyes, Zsuzsanna ^a   Pinter, Erika ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Capsaicin sensitive sensory nerves; Disease activity index; Histopathological scoring; IL 1 ; Myeloperoxidase (MPO) activity; Neurogenic inflammation

Indexed keywords

CYTOKINE; DEXTRAN SULFATE; INTERLEUKIN 1BETA; MYELOPEROXIDASE; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; FECES ANALYSIS; FEMALE; HISTOPATHOLOGY; MOUSE; NONHUMAN;

ANIMALS; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-1BETA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEROXIDASE; TRPV CATION CHANNELS;

ANIMALIA; MUS;

EID: 77955174633     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-010-9366-5     Document Type: Article

References (68)

1. S Anavi-Goffer AA Coutts 2003 Cellular distribution of vanilloid VR1 receptor immunoreactivity in the guinea-pig myenteric plexus Eur J Pharmacol 458 61 71 10.1016/S0014-2999(02)02653-5 1:CAS:528:DC%2BD38Xpslalt7g%3D 12498908 (Pubitemid 36050702)
2. A Arranz C Abad Y Juarranz J Leceta C Martinez RP Gomariz 2008 Vasoactive intestinal peptide as a healing mediator in Crohn's disease Neuroimmunomodulation 15 46 53 1:CAS:528:DC%2BD1cXptVyhtL4%3D 18667799
3. KA Barada MI Kafrouni K CIea 2001 Experimental colitis decreases rat jejunal amino acid absorption: role of capsaicin sensitive primary afferents Life Sci 69 69 3121 3131 10.1016/S0024-3205(01)01418-7 1:CAS:528: DC%2BD3MXos12mtro%3D 11758837 (Pubitemid 33044705)
4. L Bartho R Benko R Patacchini, et al. 2004 Effects of capsaicin on visceral smooth muscle: a valuable tool for sensory neurotransmitter identification Eur J Pharmacol 500 500 143 157 10.1016/j.ejphar.2004.07.020 1:CAS:528:DC%2BD2cXotFClurk%3D 15464028 (Pubitemid 39304004)
5. R Boismenu Y Chen K Chou A El-Sheikh R Buelow 2002 Orally administered RDP58 reduces the severity of dextran sodium sulphate induced colitis Ann Rheum Dis 61 Suppl 2 ii19 ii24 1:CAS:528:DC%2BD38XovFagtLk%3D 12379615
6. P Brun C Mastrotto E Beggiao, et al. 2005 Neuropeptide neurotensin stimulates intestinal wound healing following chronic intestinal inflammation Am J Physiol Gastrointest Liver Physiol 288 G621 G629 10.1152/ajpgi.00140.2004 1:CAS:528:DC%2BD2MXjtlyjsLk%3D 15764810 (Pubitemid 40388173)
7. I Castagliuolo CC Wang L Valenick A Pasha S Nikulasson RE Carraway C Pothoulakis 1999 Neurotensin is a proinflammatory neuropeptide in colonic inflammation J Clin Investig 103 843 849 10.1172/JCI4217 1:CAS:528: DyaK1MXhvFarsr4%3D 10079105
8. MJ Caterina D Julius 2001 The vanilloid receptor: a molecular gateway to the pain pathway Annu Rev Neurosci 24 24 487 517 10.1146/annurev.neuro.24.1.487 1:CAS:528:DC%2BD3MXls1Shs7o%3D 11283319 (Pubitemid 32695237)
9. MJ Caterina MA Schumacher M Tominaga TA Rosen JD Levine D Julius 1997 The capsaicin receptor: a heat-activated ion channel in the pain pathway Nature 389 389 816 824 1:CAS:528:DyaK2sXmvFSksbs%3D 9349813
10. A Cavani CJ Hackett KJ Wilson JB Rothbard SI Katz 1995 Characterization of epitopes recognized by hapten-specific CD4+ T-cells J Immunol 154 154 1232 1238 1:CAS:528:DyaK2MXjt1Kkurc%3D 7529797
11. CL Chan P Facer D JBea 2003 Sensory fibres expressing capsaicin receptor TRPV1 in patients with rectal hypersensitivity and faecal urgency Lancet 361 361 385 391 10.1016/S0140-6736(03)12392-6 1:CAS:528:DC%2BD3sXptFejug%3D%3D 12573376 (Pubitemid 36164972)
12. DE Clapham C Montell G Schultz D Julius 2003 Compendium of voltage-gated ion channels: transient receptor potential channels Pharmacol Rev 55 55 591 596 10.1124/pr.55.4.6 14657417 (Pubitemid 37500520)
13. HS Cooper SN Murthy RS Shah DJ Sedergran 1993 Clinicopathologic study of dextran sulfate sodium experimental murine colitis Lab Invest 69 69 238 249 1:CAS:528:DyaK2cXhs1Smtr0%3D 8350599
14. MJ Domek F Iwata B EIea 1995 Anti-neutrophil serum attenuates dextran sulfate sodium-induced colonic damage in the rat Scan J Gastroenterol 30 30 1089 1094 10.3109/00365529509101612 1:STN:280:DyaK287lvVemug%3D%3D
15. B Egger M Bajaj-Elliott TT MacDonald R Inglin VE Eysselein MW Büchler 2000 Characterisation of acute murine dextran sodium sulphate colitis: cytokine profile and dose dependency Digestion 62 62 240 248 10.1159/000007822 1:CAS:528:DC%2BD3cXoslWju70%3D 11070407
16. R Eliakim F Karmeli E Okon D Rachmilewitz 1995 Ketotifen ameliorates capsaicin-augmented acetic acid-induced colitis Dig Dis Sci 40 40 503 508 10.1007/BF02064357 1:CAS:528:DyaK2MXlt1elu7g%3D 7534678
17. K Fujino Y Takami SG de la Fuente KA Ludwig CR Mantyh 2004 Inhibition of the vanilloid receptor subtype-1 attenuates TNBS colitis J Gastrointest Surg 8 8 842 848 10.1016/j.gassur.2004.07.011 15531237 (Pubitemid 41115737)
18. C Goso S Evangelista M Tramontana S Manzini PM Blumberg A Szallasi 1993 Topical capsaicin administration protects against trinitrobenzene sulfonic acid-induced colitis in the rat Eur J Pharmacol 249 249 185 190 10.1016/0014-2999(93)90431-G 1:CAS:528:DyaK2cXksFKjuw%3D%3D 8287899 (Pubitemid 23328885)
19. KJ Gross C Pothoulakis 2007 Role of neuropeptides in inflammatory bowel disease Inflamm Bowel Dis 13 13 918 932 10.1002/ibd.20129 17343284 (Pubitemid 47203871)
20. D Grundy 2002 Neuroanatomy of visceral nociception: vagal and splanchnic afferent Gut 1 i2 i5 10.1136/gut.51.suppl-1.i2 Suppl 1
21. Helyes Z, Pinter E, Szolcsanyi J (2009) Regulatory role of sensory neuropeptides in inflammation. In: Kovacs M, Merchenthaler I (eds) Neuropeptides and peptide analogs, pp 111-141. Research Signpost
22. P Holzer 1991 Capsaicin: cellular targets, mechanisms of action and selectivity for thin sensory neurons Pharmacol Rev 43 43 143 201 1:CAS:528:DyaK3MXlvFOmtL8%3D 1852779
23. P Holzer 2002 Sensory neurone responses to mucosal noxae in the upper gut: relevance to mucosal integrity and gastrointestinal pain Neurogastroenterol Motil 14 14 459 475 10.1046/j.1365-2982.2002.00353.x 1:STN:280: DC%2BD38vpvVCqsA%3D%3D 12358674 (Pubitemid 35216329)
24. P Holzer 2004 Vanilloid receptor TRPV1: hot on the tongue and inflaming the colon Neurogastroenterol Motil 16 16 697 699 10.1111/j.1365-2982.2004.00598. x 15601418 (Pubitemid 40022775)
25. Holzer P, Bartho L (1996) Sensory neurons in the intestine. In: Gepetti P, Holzer P (eds) Neurogenic inflammation. CRC Press, Boca Raton
26. P Holzer CA Maggi 1998 Dissociation of dorsal root ganglion neurons into afferent and efferent-like neurons Neuroscience 86 86 389 398 1:CAS:528:DyaK1cXktlGgtLw%3D 9881854
27. T Iwanaga O Hoshi H Han T Fujita 1994 Morphological analysis of acute ulcerative colitis experimentally induced by dextran sulfate sodium in the guinea pig: some possible mechanisms of cecal ulceration J Gastroenterol 29 29 430 438 10.1007/BF02361239 1:STN:280:DyaK2M%2FjvFGmsg%3D%3D 7951852 (Pubitemid 24262710)
28. N Jancso A Jancso-Gabor J Szolcsanyi 1967 Direct evidence for neurogenic inflammation and its prevention by denervation and treatment with capsaicin Br J Pharmacol Chemother 31 31 138 150 1:STN:280:DyaF1c%2FhsF2nuw%3D%3D 6055248
29. N Jancso A Jancso-Gabor J Szolcsanyi 1968 The role of the sensory nerve endings in neurogenic inflammation induced in human skin and in the eye and paw of the rat Br J Pharmacol Chemother 33 33 32 41 1:CAS:528:DyaF1cXktV2gtro%3D 4298238
30. F Kazunori SG de la Fuente PN Theodore CR Mantyh 2003 Dextran sulfate sodium-induced enterocolitis is attenuated in vanilloid receptor-1 knockout mice [abstract] Gastroenterology 124 124 300
31. N Kihara SG de la Fuente F Fujino T Takahashi TN Pappas CR Mantyh 2003 Vanilloid receptor-1 containing primary sensory neurones mediate dextran sulphate sodium induced colitis in rats Gut 52 52 713 719 10.1136/gut.52.5.713 1:CAS:528:DC%2BD3sXjvVeiu7k%3D 12692058 (Pubitemid 36528875)
32. ES Kimball NH Wallace CR Schneider MR D'Andrea PJ Homby 2004 Vanilloid receptor 1 antagonist attenuate disease severity in dextran sulphate sodium-induced colitis in mice Neurogastroenterol Motil 16 16 811 818 10.1111/j.1365-2982.2004.00549.x 1:STN:280:DC%2BD2cnis1ersg%3D%3D 15601431 (Pubitemid 40022788)
33. CF Krieglstein WH Cerwinka FS Laroux 2001 Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide J Exp Med 194 194 1207 1218 10.1084/jem.194.9.1207 1:CAS:528:DC%2BD3MXot12msLc%3D 11696587 (Pubitemid 33055040)
34. FW Leung 1992 Role of capsaicin-sensitive afferent nerves in mucosal injury and injury-induced hyperaemia in rat colon Am J Physiol 262 262 G332 G337 1:STN:280:DyaK387ntV2htg%3D%3D 1539665
35. K-Y Ling D Bhalla D Hollander 1988 Mechanisms of carrageenan injury of IEC18 small intestinal epithelial cell monolayers Gastroenterology 95 95 1487 1495 1:CAS:528:DyaL1MXls1aj 2460392
36. F Massa A Sibaev G Marsicano H Blaudzun M Storr B Lutz 2006 Vanilloid receptor (TRPV1)-deficient mice show increased susceptibility to dinitrobenzene sulfonic acid induced colitis J Mol Med 84 84 142 146 10.1007/s00109-005-0016-2 1:CAS:528:DC%2BD28XhtVaisr8%3D 16389550 (Pubitemid 43201254)
37. DM McCafferty JL Wallace KA Sharkey 1997 Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat Am J Physiol 272 272 G272 G280 1:CAS:528:DyaK2sXhvVGgsbk%3D 9124351
38. GP Morris PL Beck MS Herridge WT Depew MR Szewczuk JL Wallace 1989 Hapten induced model of chronic inflammation and ulceration in the rat colon Gastroenterology 96 96 795 803 1:STN:280:DyaL1M7itFeqtQ%3D%3D 2914642
39. FH Mourad KA Barada NA Bou Rached CI Khoury NE Saade CF Nassar 2006 Inhibitoty effect of experimental colitis on fluid absorption in rat jejunum: role of the enteric nervous system, VIP and nitric oxide Am J Physiol Gastrointest Liver Physiol 290 290 G262 G268 10.1152/ajpgi.00271.2005 1:CAS:528:DC%2BD28XhsFKhtL4%3D 16123200
40. MF Neurath I Fuss BL Kelsall E Stuber W Strober 1995 Antibodies to interleukin 12 abrogate established experimental colitis in mice J Exp Med 182 182 1281 1290 10.1084/jem.182.5.1281 1:CAS:528:DyaK2MXovFWru7s%3D 7595199
41. T Ohkusa I Okayasu I Ozaki M Yamada R Nakaya 1990 Changes in bacterial phagocytosis of macrophage in experimental ulcerative colitis [abstract] Gastroenterology 98 98 A467
42. M Okayama R Tsubouchi S Kato K Takeuchi 2004 Protective effect of lafutidine, a novel histamine H2-receptor antagonist, on dextran sulfate sodium-induced colonic inflammation through capsaicin-sensitive afferent neurons in rats Dig Dis Sci 49 49 1696 1704 10.1023/B:DDAS.0000043389.96490.76 1:CAS:528:DC%2BD2cXnvFGrsLo%3D 15573930 (Pubitemid 39335559)
43. I Okayasu S Hatakeyama M Yamada T Ohkusa Y Inagaki R Nakaya 1990 A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice Gastroenterology 98 98 694 702 1:STN:280:DyaK3c7ivVSnuw%3D%3D 1688816
44. LM Patterson H Zheng SM Ward HR Berthoud 2003 Vanilloid receptor (VR1) expression in vagal afferent neurons innervating the gastrointestinal tract Cell Tissue Res 311 311 277 287 1:CAS:528:DC%2BD3sXitlOqs7k%3D 12658436
45. D Philippe D Chakass T Xea 2006 Mu opioid receptor expression is increased in inflammatory bowel diseases: implications for homeostatic intestinal inflammation Gut 55 55 815 823 10.1136/gut.2005.080887 1:CAS:528:DC%2BD28XlvVOht7g%3D 16299031 (Pubitemid 43764552)
46. D Philippe L Dubuquoy H Groux V Brun MTV Chuoï-mariot C Gaveriaux-ruff C J-f BL Kieffer P Desreumaux 2003 Anti-inflammatory properties of the μ opioid receptor support its use in the treatment of colon inflammation J Clin Investig 111 1329 1338 1:CAS:528:DC%2BD3sXjsFCrsro%3D 12727924
47. S Poonyachoti A Kulkarni-Narla DR Brown 2002 Chemical coding of neurons expressing delta- and kappa-opioid receptor and type I vanilloid receptor immunoreactivities in the porcine ileum Cell Tissue Res 307 307 23 33 10.1007/s00441-001-0480-0 1:CAS:528:DC%2BD3MXovFSgsLY%3D 11810311 (Pubitemid 34017114)
48. D Rachmilewitz K Katakura K Fea 2004 Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis Gastroenterology 126 126 520 528 10.1053/j.gastro.2003.11.019 1:CAS:528:DC%2BD2cXhvV2rtrw%3D 14762789 (Pubitemid 38182309)
49. HC Rath M Schultz F Rea 2001 Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice Infect Immun 69 69 2277 2285 10.1128/IAI.69.4.2277-2285.2001 1:CAS:528:DC%2BD3MXisVSlsrw%3D 11254584 (Pubitemid 32241818)
50. M Reinshagen B Egger F Procaccino, et al. 1997 Neuropeptides in inflammatory bowel disease Inflamm Bowel Dis 3 3 303 313 10.1002/ibd.3780030409
51. M Reinshagen G Flaming E Sea 1998 Calcitonin gene-related peptide mediates the protective effect of sensory nerves in a model of colonic injury J Pharmacol Exp Ther 286 286 657 661 1:CAS:528:DyaK1cXlsVWiur0%3D 9694917
52. M Reinshagen A Patel M Sottili 1994 Protective function of extrinsic sensory neurons in acute rabbit experimental colitis Gastroenterology 106 106 1208 1214 1:STN:280:DyaK2c3ivFCmuw%3D%3D 7513664
53. M Reinshagen A Patel M Sottili S French C Stemini VE Eysselein 1996 Action of sensory neurons in an experimental colitis model of injury and repair Am J Physiol 270 270 G79 G86 1:CAS:528:DyaK28XhtVynsbk%3D 8772504
54. RB Sartor SK Anderle N Rifai GD AT WJ Cromartie JH Schwab 1989 Protracted anemia associated with chronic, relapsing systemic inflammation induced by arthropathic peptidoglycan-polysaccharide polymers in rats Infect Immun 57 57 1177 1185 1:CAS:528:DyaL1MXhvFShu7c%3D 2784417
55. H Setoyama A Imaoka H Ishikawa Y Umesaki 2003 Prevention of gut inflammation by Bifidobacterium in dextran sulfate-treated gnotobiotic mice associated with Bacteroides strains isolated from ulcerative colitis patients Microbes Infect 5 5 115 122 10.1016/S1286-4579(02)00080-1 12650769 (Pubitemid 36316053)
56. M Storr 2007 TRPV1 in colitis: is it a good or a bad receptor?-a viewpoint Neurogastroenterol Motil 19 19 625 629 10.1111/j.1365-2982.2007.00946. x 1:CAS:528:DC%2BD2sXhtFyjsr7O 17539893 (Pubitemid 47084126)
57. W Strober I Fuss P Mannon 2007 The fundamental basis of inflammatory bowel disease J Clin Invest 117 117 514 521 10.1172/JCI30587 1:CAS:528:DC%2BD2sXis12hsbk%3D 17332878 (Pubitemid 46348505)
58. Szolcsanyi J (1982) Capsaicin type pungent agents producing pyrexia. In: Milton AS (ed) Handbook of experimental pharmacology. Springer, Berlin
59. Szolcsanyi J (1984) Capsaicin-sensitive chemoceptive neural system with dual sensory-efferent function. In: Chahl LA, Szolcsanyi J, Lembeck F (eds) Antidromic vasodilatation and neurogenic inflammation. Akadémiai Kiadó, Budapest, pp 27-56
60. J Szolcsanyi 1996 Capsaicin-sensitive sensory nerve terminals with local systemic efferent functions: facts and scopes of an unorthodox neuroregulatory mechanism Prog Brain Res 113 113 343 359 10.1016/S0079-6123(08)61097-3 1:CAS:528:DyaK2sXhslOjsr4%3D 9009744
61. E Talero S Sánchez-Fidalgo J Ramón Calvo V Motilva 2006 Galanin in the trinitrobenzene sulfonic acid rat model of experimental colitis Int Immunopharmacol 6 1404 1412 10.1016/j.intimp.2006.04.016 1:CAS:528:DC%2BD28XntVSqtrg%3D 16846834 (Pubitemid 44038681)
62. E Talero S Sanchez-Fidalgo JR Calvo V Motilva 2007 Chronic administration of galanin attenuates the TNBS-induced colitis in rats Regul Pept 141 141 96 104 10.1016/j.regpep.2006.12.029 1:CAS:528:DC%2BD2sXjs1KqsLw%3D 17331599 (Pubitemid 46482689)
63. T Tamaru H Kobayashi S Kishimoto G Kajiyama F Shimamoto WR Brown 1993 Histochemical study of colonic cancer in experimental colitis of rats Dig Dis Sci 38 38 529 537 10.1007/BF01316510 1:STN:280:DyaK3s7osFCksg%3D%3D 7680303
64. EF Verdu P Bercik C Bea 2000 Oral administration of antigens from intestinal flora anaerobic bacteria reduces the severity of experimental acute colitis in BALB/c mice Clin Exp Immunol 120 120 46 50 10.1046/j.1365-2249.2000. 01170.x 1:CAS:528:DC%2BD3cXisl2mt74%3D 10759762
65. MF Verma-Gondhu E Verdu P Bercik AP Blennerhassett N Al-Mutawaly J-E Ghia MS Collins 2007 Visceral pain perception is determined by the duration of colitis and associated neuropeptide expression in the mouse Gut 56 358 364 10.1136/gut.2006.100016 (Pubitemid 46579764)
66. A Vetuschi G Latella R Sferra R Caprilli E Gaudio 2002 Increased proliferation and apoptosis of colonic epithelial cells in dextran sulfate sodium-induced colitis in rats Dig Dis Sci 47 47 1447 1457 10.1023/A: 1015931128583 12141799 (Pubitemid 34753919)
67. SM Ward J Bayguinov KJ Won D Grundy HR Berthoud 2003 Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract J Comp Neurol 465 465 121 135 10.1002/cne.10801 12926020 (Pubitemid 37075684)
68. M Yamada T Ohkusa I Okayasu 1992 Occurence of dysplasia and adenocarcinoma after experimental chronic ulcerative colitis in hamsters induced by dextran sulphate sodium Gut 33 33 1521 1527 10.1136/gut.33.11.1521 1:CAS:528:DyaK3sXhs1Khu7k%3D 1333439