Combined genetic and pharmacological inhibition of TRPV1 and P2X3 attenuates colorectal hypersensitivity and afferent sensitization

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 305, Issue 9, 2013, Pages

  Kiyatkin, Michael E ^a   Feng, Bin ^a   Schwartz, Erica S ^a   Gebhart, G F ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Pelvic nerve; Purinergic receptor; Single fiber; Transient receptor potential; Visceral pain

Indexed keywords

A 889425; AGENTS AFFECTING PROTEIN METABOLISM; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X3 RECEPTOR ANTAGONIST; PURINERGIC RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; ZYMOSAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLORECTAL AFFERENT NEURON SENSITIZATION; COLORECTAL DISEASE; COLORECTAL DISTENSION; COLORECTAL HYPERSENSITIVITY; CONTROLLED STUDY; GENE; GENETICS; INTESTINE DISTENSION; MALE; MOUSE; NOCICEPTION; NONHUMAN; P2X3 GENE; PRIORITY JOURNAL; SENSITIZATION; TRPV1 GENE;

PELVIC NERVE; PURINERGIC RECEPTOR; SINGLE FIBER; TRANSIENT RECEPTOR POTENTIAL; VISCERAL PAIN;

ANIMALS; BEHAVIOR, ANIMAL; COLON; HYPERSENSITIVITY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PAIN; RECEPTORS, PURINERGIC P2X3; RECTUM; TRPV CATION CHANNELS;

EID: 84886995115     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00180.2013     Document Type: Article

References (56)

1. 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 57: 923-929, 2008.
2. Bortolotti M, Coccia G, Grossi G, Miglioli M. The treatment of functional dyspepsia with red pepper. Aliment Pharmacol Ther 16: 1075-1082, 2002.
3. Bouin M, Plourde V, Boivin M, Riberdy M, Lupien F, Laganiere M, Verrier P, Poitras P. Rectal distention testing in patients with irritable bowel syndrome: sensitivity, specificity, and predictive values of pain sensory thresholds. Gastroenterology 122: 1771-1777, 2002.
4. Bray D, Duke T. Conformational spread: the propagation of allosteric states in large multiprotein complexes. Annu Rev Biophys Biomol Struct 33: 53-73, 2004.
5. Brederson JD, Chu KL, Reilly RM, Brown BS, Kym PR, Jarvis MF, McGaraughty S. TRPV1 antagonist, A-889425, inhibits mechanotransmission in a subclass of rat primary afferent neurons following peripheral inflammation. Synapse 66: 187-195, 2012.
6. Brierley SM, Carter R, Jones W, 3rd, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA. Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567: 267-281, 2005.
7. Christianson JA, Gebhart GF. Assessment of colon sensitivity by luminal distension in mice. Nat Protoc 2: 2624-2631, 2007.
8. Christianson JA, Traub RJ, Davis BM. Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. J Comp Neurol 494: 246-259, 2006.
9. De Schepper HU, De Winter BY, Van Nassauw L, Timmermans JP, Herman AG, Pelckmans PA, De Man JG. TRPV1 receptors on unmyelinated C-fibres mediate colitis-induced sensitization of pelvic afferent nerve fibres in rats. J Physiol 586: 5247-5258, 2008.
10. Docherty RJ, Yeats JC, Bevan S, Boddeke HW. Inhibition of calcineurin inhibits the desensitization of capsaicin-evoked currents in cultured dorsal root ganglion neurones from adult rats. Pflügers Arch 431: 828-837, 1996.
11. Feng B, Brumovsky PR, Gebhart GF. Differential roles of stretchsensitive pelvic nerve afferents innervating mouse distal colon and rectum. Am J Physiol Gastrointest Liver Physiol 298: G402-G409, 2010.
12. Feng B, Gebhart GF. Characterization of silent afferents in the pelvic and splanchnic innervations of the mouse colorectum. Am J Physiol Gastrointest Liver Physiol 300: G170-G180, 2011.
13. Feng B, Kiyatkin ME, La JH, Ge P, Solinga R, Silos-Santiago I, Gebhart GF. Activation of guanylate cyclase-C attenuates stretch responses and sensitization of mouse colorectal afferents. J Neurosci 33: 9831-9839, 2013.
14. Feng B, La JH, Schwartz ES, Tanaka T, McMurray TP, Gebhart GF. Long-term sensitization of mechanosensitive and-insensitive afferents in mice with persistent colorectal hypersensitivity. Am J Physiol Gastrointest Liver Physiol 302: G676-G683, 2012.
15. Gever JR, Cockayne DA, Dillon MP, Burnstock G, Ford AP. Pharmacology of P2X channels. Pflügers Arch 452: 513-537, 2006.
16. 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 11: 946-958, 1999.
17. Hamilton SG, Wade A, McMahon SB. The effects of inflammation and inflammatory mediators on nociceptive behaviour induced by ATP analogues in the rat. Br J Pharmacol 126: 326-332, 1999.
18. Hamilton SG, Warburton J, Bhattacharjee A, Ward J, McMahon SB. ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia. Brain 123: 1238-1246, 2000.
19. 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 133: 184-194, 2007.
20. Jones RC 3rd, 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 25: 10981-10989, 2005.
21. King B, Chen CC, Akopian AN, Burnstock G, Wood JN. A role for calcineurin in the desensitization of the P2X3 receptor. Neuroreport 8: 1099-1102, 1997.
22. Kiyatkin M, Gebhart G. Role of TRPV1 and P2X3 in mechanosensation in colorectal primary afferents. In: Program No 47305 2012 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2012.
23. Kyloh M, Nicholas S, Zagorodnyuk VP, Brookes SJ, Spencer NJ. Identification of the visceral pain pathway activated by noxious colorectal distension in mice. Front Neurosci 5: 16, 2011.
24. Lembo T, Munakata J, Mertz H, Niazi N, Kodner A, Nikas V, Mayer EA. Evidence for the hypersensitivity of lumbar splanchnic afferents in irritable bowel syndrome. Gastroenterology 107: 1686-1696, 1994.
25. Lu SG, Zhang X, Gold MS. Intracellular calcium regulation among subpopulations of rat dorsal root ganglion neurons. J Physiol 577: 169-190, 2006.
26. Lynn PA, Olsson C, Zagorodnyuk V, Costa M, Brookes SJ. Rectal intraganglionic laminar endings are transduction sites of extrinsic mechanoreceptors in the guinea pig rectum. Gastroenterology 125: 786-794, 2003.
27. McGaraughty S, Chu KL, Brown BS, Zhu CZ, Zhong C, Joshi SK, Honore P, Faltynek CR, Jarvis MF. Contributions of central and peripheral TRPV1 receptors to mechanically evoked and spontaneous firing of spinal neurons in inflamed rats. J Neurophysiol 100: 3158-3166, 2008.
28. Mertz H, Naliboff B, Munakata J, Niazi N, Mayer EA. Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 109: 40-52, 1995.
29. 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 148: 1021-1032, 2007.
30. Nealen ML, Gold MS, Thut PD, Caterina MJ. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90: 515-520, 2003.
31. Phillis BD, Martin CM, Kang D, Larsson H, Lindstrom EA, Martinez V, Blackshaw LA. Role of TRPV1 in high-threshold rat colonic splanchnic afferents is revealed by inflammation. Neurosci Lett 459: 57-61, 2009.
32. Plourde V, Lembo T, Shui Z, Parker J, Mertz H, Tache Y, Sytnik B, Mayer E. Effects of the somatostatin analogue octreotide on rectal afferent nerves in humans. Am J Physiol Gastrointest Liver Physiol 265: G742-G751, 1993.
33. Price TJ, Jeske NA, Flores CM, Hargreaves KM. Pharmacological interactions between calcium/calmodulin-dependent kinase II alpha and TRPV1 receptors in rat trigeminal sensory neurons. Neurosci Lett 389: 94-98, 2005.
34. Ritchie J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14: 125-132, 1973.
35. Robinson DR, McNaughton PA, Evans ML, Hicks GA. Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 16: 113-124, 2004.
36. 2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 123: 53-62, 2004.
37. Schwartz ES, Christianson JA, Chen X, La JH, Davis BM, Albers KM, Gebhart GF. Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation. Gastroenterology 140: 1283-1291; e1281-1282, 2011.
38. Shimizu I, Iida T, Guan Y, Zhao C, Raja SN, Jarvis MF, Cockayne DA, Caterina MJ. Enhanced thermal avoidance in mice lacking the ATP receptor P2X3. Pain 116: 96-108, 2005.
39. Shinoda M, Feng B, Gebhart GF. Peripheral and central P2X receptor contributions to colon mechanosensitivity and hypersensitivity in the mouse. Gastroenterology 137: 2096-2104, 2009.
40. Shinoda M, La JH, Bielefeldt K, Gebhart GF. Altered purinergic signaling in colorectal dorsal root ganglion neurons contributes to colorectal hypersensitivity. J Neurophysiol 104: 3113-3123, 2010.
41. Stanchev D, Blosa M, Milius D, Gerevich Z, Rubini P, Schmalzing G, Eschrich K, Schaefer M, Wirkner K, Illes P. Cross-inhibition between native and recombinant TRPV1 and P2X(3) receptors. Pain 143: 26-36, 2009.
42. Staruschenko A, Jeske NA, Akopian AN. Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel. J Biol Chem 285: 15167-15177, 2010.
43. Tanaka T, Shinoda M, Feng B, Albers KM, Gebhart GF. Modulation of visceral hypersensitivity by glial cell line-derived neurotrophic factor family receptor α-3 in colorectal afferents. Am J Physiol Gastrointest Liver Physiol 300: G418-G424, 2011.
44. Toulme E, Blais D, Leger C, Landry M, Garret M, Seguela P, Boue-Grabot E. An intracellular motif of P2X(3) receptors is required for functional cross-talk with GABA(A) receptors in nociceptive DRG neurons. J Neurochem 102: 1357-1368, 2007.
45. Traub RJ. Evidence for thoracolumbar spinal cord processing of inflammatory, but not acute colonic pain. Neuroreport 11: 2113-2116, 2000.
46. Trimble KC, Farouk R, Pryde A, Douglas S, Heading RC. Heightened visceral sensation in functional gastrointestinal disease is not site-specific. Evidence for a generalized disorder of gut sensitivity. Dig Dis Sci 40: 1607-1613, 1995.
47. Tsuda M, Hasegawa S, Inoue K. P2X receptors-mediated cytosolic phospholipase A2 activation in primary afferent sensory neurons contributes to neuropathic pain. J Neurochem 103: 1408-1416, 2007.
48. Ueno S, Tsuda M, Iwanaga T, Inoue K. Cell type-specific ATP-activated responses in rat dorsal root ganglion neurons. Br J Pharmacol 126: 429-436, 1999.
49. Verne GN, Robinson ME, Vase L, Price DD. Reversal of visceral and cutaneous hyperalgesia by local rectal anesthesia in irritable bowel syndrome (IBS) patients. Pain 105: 223-230, 2003.
50. Verne GN, Sen A, Price DD. Intrarectal lidocaine is an effective treatment for abdominal pain associated with diarrhea-predominant irritable bowel syndrome. J Pain 6: 493-496, 2005.
51. Wang G, Tang B, Traub RJ. Pelvic nerve input mediates descending modulation of homovisceral processing in the thoracolumbar spinal cord of the rat. Gastroenterology 133: 1544-1553, 2007.
52. Wiskur BJ, Tyler K, Campbell-Dittmeyer K, Chaplan SR, Wickenden AD, Greenwood-Van Meerveld B. A novel TRPV1 receptor antagonist JNJ-17203212 attenuates colonic hypersensitivity in rats. Methods Find Exp Clin Pharmacol 32: 557-564, 2010.
53. Wyndaele M, De Wachter S, De Man J, Minagawa T, Wyndaele JJ, Pelckmans PA, De Winter BY. Mechanisms of pelvic organ crosstalk: 1. Peripheral modulation of bladder inhibition by colorectal distention in rats. J Urol 190: 765-771, 2013.
54. Wynn G, Rong W, Xiang Z, Burnstock G. Purinergic mechanisms contribute to mechanosensory transduction in the rat colorectum. Gastroenterology 125: 1398-1409, 2003.
55. Xu GY, Huang LY. Ca2+/calmodulin-dependent protein kinase II potentiates ATP responses by promoting trafficking of P2X receptors. Proc Natl Acad Sci USA 101: 11868-11873, 2004.
56. Xu GY, Shenoy M, Winston JH, Mittal S, Pasricha PJ. P2X receptormediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut 57: 1230-1237, 2008.