TRP channels in visceral pain

Open Pain Journal

Volumn 6, Issue SPEC.ISSUE.1, 2013, Pages 23-30

  Blackshaw, L Ashley ^a,b   Brierley, Stuart M ^b   Harrington, Andrea M ^b   Hughes, Patrick A ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Inflammation; Mechanosensitivity; Pain

Indexed keywords

CAPSAICIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M8; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 4;

ARTICLE; DISEASE SEVERITY; ESOPHAGUS MUCOSA; HUMAN; MECHANOTRANSDUCTION; NOCICEPTION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SENSORY NERVE; SIGNAL TRANSDUCTION; STOMACH JUICE; VISCERAL PAIN;

EID: 84876087084     PISSN: None     EISSN: 18763863     Source Type: Journal    
DOI: 10.2174/1876386301306010023     Document Type: Article

References (101)

1. Brierley SM, Jones III RCW, Gebhart GF, et al. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 2004; 127: 166-78.
2. Page AJ, Martin CM, Blackshaw LA. Vagal mechanoreceptors and chemoreceptors in mouse stomach and esophagus. J Neurophysiol 2002; 87: 2095-103.
3. Brierley SM, Page AJ, Hughes PA, et al. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 2008; 134: 2059-69.
4. Hughes PA, Brierley SM, Martin CM, et al. Post-inflammatory colonic afferent sensitization: different subtypes, different pathways, and different time-courses. Gut 2009; 58(10): 1333-41.
5. Berthoud HR, Kressel M, Raybould HE, et al. Vagal sensors in the rat duodenal mucosa: distribution and structure as revealed by in vivo DiI-tracing. Anat Embryol (Berl) 1995; 191: 203-12.
6. Berthoud HR, Powley TL. Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor. J Comp Neurol 1992; 319: 261-76.
7. Lynn PA, Olsson C, Zagorodnyuk V, et al. Rectal intraganglionic laminar endings are transduction sites of extrinsic mechanoreceptors in the guinea pig rectum. Gastroenterology 2003; 125: 786-94.
8. Zagorodnyuk VP, Brookes SJ. Transduction sites of vagal mechanoreceptors in the guinea pig esophagus. J Neurosci 2000; 20: 6249-55.
9. Blumberg H, Haupt P, Janig W, Kohler W. Encoding of visceral noxious stimuli in the discharge patterns of visceral afferent fibres from the colon. Pflugers Arch Eur J Physiol 1983; 398: 33-40.
10. Morrison JFB. Splanchnic slowly adapting mechanoreceptors with punctate receptove fields in the mesentery and the gastrointestinal tract of the cat. J Physiol 1973; 233: 349-61.
11. Song X, Chen BN, Zagorodnyuk VP, et al. Identification of medium/high threshold extrinsic mechanosensitive afferent nerves to the gastrointestinal tract. Gastroenterology 2009; 137(1): 274-84.
12. Brierley SM, Jones III RCW, Xu L, Gebhart GF, Blackshaw LA. Activation of splanchnic and pelvic colonic afferents by bradykinin in mice. Neurogastroenterol Motil 2005; 17: 854-62.
13. Brierley SM, Jones III RCW, Xu L, et al. Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 2005; 567: 267-81.
14. Andrews PL, Sanger GJ. Abdominal vagal afferent neurones: an important target for the treatment of gastrointestinal dysfunction. Curr Opin Pharmacol 2002; 2: 650-6.
15. Blackshaw LA, Gebhart GF. The pharmacology of gastrointestinal nociceptive pathways. Curr Opin Pharmacol 2002; 2: 642-9.
16. Brunsden AM, Brookes SJ, Bardhan KD, Grundy D. Mechanisms underlying mechanosensitivity of mesenteric afferent fibers to vascular flow. Am J Physiol Gastrointest Liver Physiol 2007; 293: G422-8.
17. Yu S, Undem BJ, Kollarik M. Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. J Physiol 2005; 563: 831-42.
18. Booth CE, Kirkup AJ, Hicks GA, Humphrey PP, Grundy D. Somatostatin sst(2) receptor-mediated inhibition of mesenteric afferent nerves of the jejunum in the anesthetized rat. Gastroenterology 2001; 121: 358-69.
19. Sengupta JN, Saha JK, Goyal RK. Stimulus-response function studies of esophageal mechanosensitive nociceptors in sympathetic afferents of opossum. J Neurophysiol 1990; 64: 796-812.
20. Clapham DE. TRP channels as cellular sensors. Nature 2003; 426: 517-24.
21. Dhaka A, Viswanath V, Patapoutian A. TRP ion channels and temperature sensation. Annu Rev Neurosci 2006; 29: 135-61.
22. Christensen AP, Corey DP. TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 2007; 8: 510-21.
23. Broad LM, Mogg AJ, Beattie RE, Ogden AM, Blanco MJ, Bleakman D. TRP channels as emerging targets for pain therapeutics. Expert Opin Ther Targets 2009; 13: 69-81.
24. Bessac BF, Jordt SE. Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control. Physiology (Bethesda) 2008; 23: 360-70.
25. Nishida M, Kurose H. Roles of TRP channels in the development of cardiac hypertrophy. Naunyn Schmiedebergs Arch Pharmacol 2008; 378: 395-406.
26. Hoenderop JG, Bindels RJ. Calciotropic and magnesiotropic TRP channels. Physiology (Bethesda) 2008; 23: 32-40.
27. Christianson JA, Traub RJ, Davis BM. Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. J Comp Neurol 2006; 494: 246-59.
28. Robinson DR, McNaughton PA, Evans ML, Hicks GA. Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 2004; 16: 113-24.
29. Schicho R, Florian W, Liebmann I, Holzer P, Lippe IT. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur J Neurosci 2004; 19: 1811-8.
30. Ward S, Bayguinov J, Won K, Grundy D, Berthoud HR. Distribution of the vanilloid receptor (VR1) in the gastrointestinal tract. J Comp Neurol 2003; 465: 121-35.
31. 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.
32. Liedtke W, Friedman JM. Abnormal osmotic regulation in TRPV4-/-mice. Proc Natl Acad Sci USA 2003; 100: 13698-703.
33. Smith PL, Maloney KN, Pothen RG, Clardy J, Clapham DE. Bisandrographolide from Andrographis paniculata Activates TRPV4 Channels. J Biol Chem 2006; 281: 29897-904.
34. Zhang L, Jones S, Brody K, Costa M, Brookes SJ. Thermosensitive transient receptor potential channels in vagal afferent neurons of the mouse. Am J Physiol Gastrointest Liver Physiol 2004; 286: G983-91.
35. Bautista DM, Jordt S-E, Nikai T, et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006; 124: 1269-82.
36. Macpherson L, Dubin A, Evans M, et al. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 2007; 445: 541-5.
37. McNamara CR, Mandel-Brehm J, Bautista DM, et al. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA 2007; 104: 13525-30.
38. Bandell M, Story GM, Hwang SW, et al. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 2004; 41: 849-57.
39. Bautista DM, Movahed P, Hinman A, et al. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 2005; 102: 12248-52.
40. Jordt S-E, Bautista DM, Chuang H-h, et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 2004; 427: 260-5.
41. Xu H, Delling M, Jun J, Clapham DE. Oregano, thyme and clovederived flavors and skin sensitizers activate specific TRP channels. Nat Neurosci 2006; 9: 628-35.
42. Brierley SM, Hughes PA, Page AJ, et al. Novel and specific roles for the ion channel TRPA1 in visceral sensory transduction. Gastroenterology 2008; 134: 32.
43. Chuang H-h, Neuhausser WM, Julius D. The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 2004; 43: 859-69.
44. Story GM, Peier AM, Reeve AJ, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 2003; 112: 819-29.
45. Laird J, Martinez-Caro L, Garcia-Nicas E, Cervero F. A new model of visceral pain and referred hyperalgesia in the mouse. Pain 2001; 92: 335-42.
46. Blackshaw LA, Page AJ, Partosoedarso ER. Acute effects of capsaicin on gastrointestinal vagal afferents. Neuroscience 2000; 96: 407-16.
47. Caterina MJ, Leffler A, Malmberg AB, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000; 288: 306-13.
48. Bielefeldt K, Davis BM. Differential effects of ASIC3 and TRPV1 deletion on gastroesophageal sensation in mice. Am J Physiol Gastrointest Liver Physiol 2008; 294: G130-8.
49. Rong W, Hillsley K, Davis JB, Hicks G, Winchester WJ, Grundy D. Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. J Physiol 2004; 560: 867-81.
50. Jones RCW, III, Xu L, Gebhart GF. 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 2005; 25: 10981-9.
51. Birder LA, Nakamura Y, Kiss S, et al. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 2002; 5: 856-60.
52. Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Ann Rev Neurosci 2001; 24: 487-517.
53. Matthews PJ, Aziz Q, Facer P, Davis JB, Thompson DG, Anand P. Increased capsaicin receptor TRPV1 nerve fibres in the inflamed human oesophagus. Eur J Gastroenterol Hepatol 2004; 16: 897-902.
54. Bhat YM, Bielefeldt K. Capsaicin receptor (TRPV1) and nonerosive reflux disease. Eur J Gastroenterol Hepatol 2006; 18: 263-70.
55. 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.
56. Kollarik M, Ru F, Undem BJ. Acid-sensitive vagal sensory pathways and cough. Pulm Pharmacol Ther 2007; 20: 402-11.
57. Suzuki M, Mizuno A, Kodaira K, Imai M. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 2003; 278: 22664-8.
58. Sipe W, Brierley SM, Martin CM, et al. transient receptor potential vanilloid 4 mediates protease activated receptor 2-induced sensitization of colonic afferent nerves and visceral hyperalgesia. Am J Physiol Gastrointest Liver Physiol 2008; 294: G1288-98.
59. Cenac N, Altier C, Chapman K, Liedtke W, Zamponi G, Vergnolle N. Transient receptor potential vanilloid-4 has a major role in visceral hypersensitivity symptoms. Gastroenterology 2008; 135: 937-46.
60. Brierley SM, Castro J, Harrington AM, et al. TRPA1 contributes to specific mechanically activated currents and sensory neuron mechanical hypersensitivity. J Physiol 2011; 589: 3575-93.
61. Yang J, Li Y, Zuo X, Zhen Y, Yu Y, Gao L. Transient receptor potential ankyrin-1 participates in visceral hyperalgesia following experimental colitis. Neurosci Lett 2008; 440: 237-41.
62. Harrington AM, Hughes PA, Martin CM, et al. A novel role for TRPM8 in visceral afferent function. Pain 2011; 152: 1459-68.
63. Soboloff J, Spassova M, Hewavitharana T, et al. TRPC channels: integrators of multiple cellular signals. Handb Exp Pharmacol 2007: 179: 575-91.
64. Grant AD, Cottrell GS, Amadesi S, et al. Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia. J Physiol 2006; 578: 715-33.
65. Amadesi S, Nie J, Vergnolle N, et al. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 2004; 24: 4300-12.
66. Jeske NA, Patwardhan AM, Gamper N, Price TJ, Akopian AN, Hargreaves KM. Cannabinoid WIN 55,212-2 regulates TRPV1 phosphorylation in sensory neurons. J Biol Chem 2006; 281: 32879-90.
67. Levine JD, Alessandri-Haber N. TRP channels: targets for the relief of pain. Biochim Biophys Acta 2007; 1772: 989-1003.
68. Dai Y, Wang S, Tominaga M, et al. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 2007; 117: 1979-87.
69. Wang S, Dai Y, Fukuoka T, et al. Phospholipase C and protein kinase A mediate bradykinin sensitization of TRPA1: a molecular mechanism of inflammatory pain. Brain 2008; 131: 1241-51.
70. Yu S, Ouyang A. TRPA1 in bradykinin-induced mechanical hypersensitivity of vagal C fibers in guinea pig esophagus. Am J Physiol Gastrointest Liver Physiol 2009; 296: G255-65.
71. Delmas P, Wanaverbecq N, Abogadie FC, Mistry M, Brown DA. Signaling microdomains define the specificity of receptor-mediated InsP(3) pathways in neurons. Neuron 2002; 34: 209-20.
72. Prescott ED, Julius D. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 2003; 300: 1284-8.
73. Nozawa K, Kawabata-Shoda E, Doihara H, et al. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc Natl Acad Sci USA 2009; 106: 3408-13.
74. Purhonen AK, Louhivuori LM, Kiehne K, Kerman KE, Herzig KH. TRPA1 channel activation induces cholecystokinin release via extracellular calcium. FEBS Lett 2008; 582: 229-32.
75. Kollarik M, Undem BJ. Activation of bronchopulmonary vagal afferent nerves with bradykinin, acid and vanilloid receptor agonists in wild-type and TRPV1-/-mice. J Physiol 2004; 555: 115-23.
76. Akopian AN, Ruparel NB, Jeske NA, Hargreaves KM. Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J Physiol 2007; 583: 175-93.
77. Mayer EA, Gebhart GF. Basic and clinical aspects of visceral hyperalgesia. Gastroenterology 1994; 107: 271-93.
78. De Schepper HU, De Winter BY, Van Nassauw L, et al. TRPV1 receptors on unmyelinated C-fibres mediate colitis-induced sensitization of pelvic afferent nerve fibres in rats. J Physiol 2008; 586: 5247-58.
79. Sengupta JN, Snider A, Su X, Gebhart GF. Effects of kappa opioids in the inflamed rat colon. Pain 1999; 79: 175-85.
80. Jones RC, 3rd, Otsuka E, Wagstrom E, Jensen CS, Price MP, Gebhart GF. Short-term sensitization of colon mechanoreceptors is associated with long-term hypersensitivity to colon distention in the mouse. Gastroenterology 2007; 133: 184-94.
81. Winston J, Shenoy M, Medley D, Naniwadekar A, Pasricha PJ. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterology 2007; 132: 615-27.
82. Miranda A, Nordstrom E, Mannem A, Smith C, Banerjee B, Sengupta JN. The role of transient receptor potential vanilloid 1 in mechanical and chemical visceral hyperalgesia following experimental colitis. Neuroscience 2007; 148: 1021-32.
83. Xu GY, Winston JH, Shenoy M, Yin H, Pendyala S, Pasricha PJ. Transient receptor potential vanilloid 1 mediates hyperalgesia and is up-regulated in rats with chronic pancreatitis. Gastroenterology 2007; 133: 1282-92.
84. Morenilla-Palao C, Planells-Cases R, Garcia-Sanz N, Ferrer-Montiel A. Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J Biol Chem 2004; 279: 25665-72.
85. Akbar A, Yiangou Y, Facer P, Walters JR, Anand P, Ghosh S. Increased capsaicin receptor TRPV1-expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut 2008; 57: 923-9.
86. Chan CL, Facer P, Davis JB, et al. Sensory fibres expressing capsaicin receptor TRPV1 in patients with rectal hypersensitivity and faecal urgency. Lancet 2003; 361: 385-91.
87. Adam B, Liebregts T, Best J, et al. A combination of peppermint oil and caraway oil attenuates the post-inflammatory visceral hyperalgesia in a rat model. Scand J Gastroenterol 2006; 41: 155-60.
88. Lembo T, Munakata J, Mertz H, et al. Evidence for the hypersensitivity of lumbar splanchnic afferents in irritable bowel syndrome. Gastroenterology 1994; 107: 1686-96.
89. Ritchie J. Pain from distention of the pelvic colon by inflating a balloon in the irritable bowel syndrome. Gut 1973; 6: 105-12.
90. Azpiroz F, Bouin M, Camilleri M, et al. Mechanisms of hypersensitivity in IBS and functional disorders. Neurogastroenterol Motil 2007; 19: 62-88.
91. Barbara G, Stanghellini V, De Giorgio R, et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology 2004; 126: 693-702.
92. Dunlop SP, Jenkins D, Spiller RC. Distinctive clinical, psychological, and histological features of postinfective irritable bowel syndrome. Am J Gastroenterol 2003; 98: 1578-83.
93. Spiller RC, Jenkins D, Thornley JP, et al. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in postdysenteric irritable bowel syndrome. Gut 2000; 47: 804-11.
94. Alvarez DF, King JA, Weber D, Addison E, Liedtke W, Townsley MI. Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: a novel mechanism of acute lung injury. Circ Res 2006; 99: 988-95.
95. Hammer J, Fuhrer M, Pipal L, Matiasek J. Hypersensitivity for capsaicin in patients with functional dyspepsia. Neurogastroenterol Motil 2008; 20: 125-33.
96. Rosch W, Liebregts T, Gundermann KJ, Vinson B, Holtmann G. Phytotherapy for functional dyspepsia: a review of the clinical evidence for the herbal preparation STW 5. Phytomedicine 2006; 13 (Suppl 5): 114-21.
97. Wong GY, Gavva NR. Therapeutic potential of vanilloid receptor TRPV1 agonists and antagonists as analgesics: Recent advances and setbacks. Brain Res Rev 2009; 60: 267-77.
98. Hicks GA. TRP channels as therapeutic targets: hot property, or time to cool down? Neurogastroenterol Motil 2006; 18: 590-4.
99. Holzer P. TRPV1: a new target for treatment of visceral pain in IBS? Gut 2008; 57: 882-4.
100. Storr M. TRPV1 in colitis: is it a good or a bad receptor?--a viewpoint. Neurogastroenterol Motil 2007; 19: 625-9.
101. Blackshaw LA, Brierley SM, Hughes PA. TRP channels: new targets for visceral pain. Gut 2010; 59: 126-35.