The role of transient receptor potential vanilloid 1 in mechanical and chemical visceral hyperalgesia following experimental colitis.
The transient receptor potential vanilloid 1 receptor (TRPV1) is an important nociceptor involved in neurogenic inflammation. We aimed to examine the role of TRPV1 in experimental colitis and in the development of visceral hypersensitivity to mechanical and chemical stimulation. Male Sprague-Dawley rats received a single dose of trinitrobenzenesulfonic acid (TNBS) in the distal colon. In the preemptive group, rats received the TRPV1 receptor antagonist JYL1421 (10 mumol/kg, i.v.) or vehicle 15 min prior to TNBS followed by daily doses for 7 days. In the post-inflammation group, rats received JYL1421 daily for 7 days starting on day 7 following TNBS. The visceromotor response (VMR) to colorectal distension (CRD), intraluminal capsaicin, capsaicin vehicle (pH 6.7) or acidic saline (pH 5.0) was assessed in all groups and compared with controls and naïve rats. Colon inflammation was evaluated with H&E staining and myeloperoxidase (MPO) activity. TRPV1 immunoreactivity was assessed in the thoraco-lumbar (TL) and lumbo-sacral (LS) dorsal root ganglia (DRG) neurons. In the preemptive vehicle group, TNBS resulted in a significant increase in the VMR to CRD, intraluminal capsaicin and acidic saline compared the JYL1421-treated group (P<0.05). Absence of microscopic colitis and significantly reduced MPO activity was also evident compared with vehicle-treated rats (P<0.05). TRPV1 immunoreactivity in the TL (69.1+/-4.6%) and LS (66.4+/-4.2%) DRG in vehicle-treated rats was increased following TNBS but significantly lower in the preemptive JYL1421-treated group (28.6+/-3.9 and 32.3+/-2.3 respectively, P<0.05). JYL1421 in the post-inflammation group improved microscopic colitis and significantly decreased the VMR to CRD compared with vehicle (P<0.05, >/=30 mm Hg) but had no effect on the VMR to chemical stimulation. TRPV1 immunoreactivity in the TL and LS DRG was no different from vehicle or naïve controls. These results suggest an important role for TRPV1 channel in the development of inflammation and subsequent mechanical and chemical visceral hyperalgesia.
Miranda
A
A
Department of Pediatrics, Division of Pediatric Gastroenterology, Medical College of Wisconsin, Milwaukee, WI 53226, USA. amiranda@mcw.edu
Nordstrom
E
E
Mannem
A
A
Smith
C
C
Banerjee
B
B
Sengupta
J N
JN
D000818:Animals; D002211:Capsaicin / Q000494:pharmacology; D003092:Colitis / Q000139:chemically induced / Q000150:complications*; D004195:Disease Models, Animal; D004334:Drug Administration Schedule; D004347:Drug Interactions; D004576:Electromyography; D005727:Ganglia, Spinal / Q000166:cytology; D005769:Gastrointestinal Motility / Q000187:drug effects; D006930:Hyperalgesia / Q000145:classification / Q000209:etiology* / Q000378:metabolism*; D008297:Male; D009474:Neurons / Q000187:drug effects / Q000378:metabolism; D051381:Rats; D017207:Rats, Sprague-Dawley; D012020:Reflex, Abdominal / Q000187:drug effects / Q000502:physiology; D013449:Sulfonamides / Q000494:pharmacology; D050916:TRPV Cation Channels / Q000037:antagonists & inhibitors / Q000502:physiology*; D013890:Thiourea / Q000031:analogs & derivatives / Q000494:pharmacology; D013997:Time Factors; D014302:Trinitrobenzenesulfonic Acid / Q000009:adverse effects; D017833:Visceral Afferents / Q000187:drug effects / Q000503:physiopathology
C466314:JYL 1421; D013449:Sulfonamides; D050916:TRPV Cation Channels; C493922:Trpv1 protein, rat; D014302:Trinitrobenzenesulfonic Acid; D013890:Thiourea; D002211:Capsaicin
Neuron. 2002 Sep 26;36(1):57-68
12367506
Brain Res. 2003 Feb 14;963(1-2):190-6
12560124
Lancet. 2003 Feb 1;361(9355):385-91
12573376
Cell Tissue Res. 2003 Mar;311(3):277-87
12658436
Gut. 2003 May;52(5):713-9
12692058
Pain. 2003 Oct;105(3):489-97
14527709
Dig Dis Sci. 2004 Jan;49(1):96-101
14992442
Br J Pharmacol. 2000 Jan;129(1):193-9
10694220
Nature. 2000 May 11;405(6783):183-7
10821274
Prog Brain Res. 2000;129:375-87
11098705
Br J Pharmacol. 2001 Mar;132(5):1084-94
11226139
Annu Rev Neurosci. 2001;24:487-517
11283319
Am J Physiol Gastrointest Liver Physiol. 2001 May;280(5):G787-94
11292585
Neuropharmacology. 2001 Apr;40(5):696-701
11311897
Lancet. 2001 Apr 28;357(9265):1338-9
11343743
J Neurochem. 2001 Jun;77(6):1660-3
11413249
J Physiol. 2001 Aug 1;534(Pt 3):813-25
11483711
J Biol Chem. 2001 Aug 17;276(33):31163-70
11333266
Peptides. 2001 Sep;22(9):1439-46
11514026
Neurosci Lett. 2002 Feb 8;319(1):53-7
11814652
Am J Gastroenterol. 2002 Feb;97(2):389-96
11866278
Neuron. 2002 Aug 15;35(4):721-31
12194871
Eur J Gastroenterol Hepatol. 2002 Oct;14(10):1067-72
12362096
Eur J Neurosci. 2004 Apr;19(7):1811-8
15078554
Neuroreport. 2004 Mar 22;15(4):655-8
15094470
Br J Pharmacol. 2004 Apr;141(8):1313-20
15051629
Eur J Gastroenterol Hepatol. 2004 Sep;16(9):897-902
15316415
Br J Pharmacol. 2004 Oct;143(3):411-21
15351778
J Neurocytol. 2004 May;33(3):321-9
15475687
Gut. 1972 Oct;13(10):841
5087084
Brain Res. 1988 May 31;450(1-2):153-69
3401708
Can J Physiol Pharmacol. 1988 Apr;66(4):422-5
3167675
Gastroenterology. 1990 Feb;98(2):269-77
2153086
Gastroenterology. 1992 Jan;102(1):18-27
1309357
Neurosci Lett. 1991 Sep 30;131(1):113-6
1791969
Clin Exp Pharmacol Physiol. 1992 Oct;19(10):717-22
1424301
Am J Physiol. 1994 Apr;266(4 Pt 1):G560-7
8178994
Gastroenterology. 1994 Dec;107(6):1686-96
7958680
Neurosci Lett. 1997 May 30;228(1):29-32
9197280
Br J Pharmacol. 1997 Aug;121(7):1461-7
9257928
Aliment Pharmacol Ther. 1998 Mar;12(3):219-28
9570256
Life Sci. 1998;63(4):293-304
9698038
J Neurosci. 1998 Aug 15;18(16):6081-92
9698303
Nature. 1999 Apr 1;398(6726):436-41
10201375
Pharmacol Rev. 1999 Jun;51(2):159-212
10353985
J Gastrointest Surg. 2004 Nov;8(7):842-7; discussion 847-8
15531237
Neurogastroenterol Motil. 2004 Dec;16(6):811-8
15601431
Neurogastroenterol Motil. 2005 Jun;17(3):410-4
15916628
Eur J Pharmacol. 2005 Jul 4;517(1-2):35-44
15978575
Inflammopharmacology. 2005;13(1-3):161-77
16259736
Cell Tissue Res. 2006 Jan;323(1):27-41
16142452
J Neurosci. 2005 Nov 23;25(47):10981-9
16306411
Mol Pain. 2006;2:3
16417630
Pain. 2006 Jul;123(1-2):179-86
16630696
Am J Physiol Gastrointest Liver Physiol. 2006 Aug;291(2):G219-28
16565418
Neurosci Lett. 2006 Oct 9;406(3):250-5
16942839
Inflamm Res. 2006 Oct;55(10):416-22
17109068
Gastroenterology. 2007 Feb;132(2):615-27
17258716
Neuroscience. 2007 Mar 16;145(2):699-707
17257769
Exp Neurol. 2007 Apr;204(2):667-79
17303123