Colonic inflammation up-regulates voltage-gated sodium channels in bladder sensory neurons via activation of peripheral transient potential vanilloid 1 receptors

Neurogastroenterology and Motility

Volumn 24, Issue 6, 2012, Pages

  Lei, Q ^a   Malykhina, A P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bladder DRG neurons; Colonic inflamm ation; Pelvic organ cross sensitization; Resiniferatoxin

Indexed keywords

RESINIFERATOXIN; SODIUM CHLORIDE; TETRODOTOXIN; VANILLOID RECEPTOR 1; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER; COLITIS; CONTROLLED STUDY; DESCENDING COLON; MALE; NONHUMAN; PELVIS PAIN SYNDROME; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SODIUM CURRENT; UPREGULATION;

ANIMALS; COLITIS; COLON; DITERPENES; MALE; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SODIUM CHANNELS; TRPV CATION CHANNELS; UP-REGULATION;

EID: 84861197462     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2012.01910.x     Document Type: Article

References (49)

1. Caterina MJ, Schumacher MA, Tominaga M et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997; 389: 816-24.
2. Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 2001; 24: 487-517.
3. Dib-Hajj SD, Black JA, Waxman SG. Voltage-gated sodium channels: therapeutic targets for pain. Pain Med 2009; 10: 1260-9.
4. Dib-Hajj SD, Cummins TR, Black JA et al. Sodium channels in normal and pathological pain. Annu Rev Neurosci 2010; 33: 325-47.
5. Waxman SG. Channel, neuronal and clinical function in sodium channelopathies: from genotype to phenotype. Nat Neurosci 2007; 10: 405-9.
6. Campbell JN, Meyer RA. Mechanisms of neuropathic pain. Neuron 2006; 52: 77-92.
7. Devor M. Sodium channels and mechanisms of neuropathic pain. J Pain 2006; 7(1 Suppl. 1): S3-12.
8. Caterina MJ, Leffler A, Malmberg AB et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000; 288: 306-13.
9. Holzer P, Maggi CA. Stimulation and propagation of the ascending enteric reflex contraction: role of tachykinins and acetylcholine. Regul Pept 1993; 46: 383-5.
10. Rigoni M, Trevisani M, Gazzieri D et al. Neurogenic responses mediated by vanilloid receptor-1 (TRPV1) are blocked by the high affinity antagonist, iodo-resiniferatoxin. Br J Pharmacol 2003; 138: 977-85.
11. Su X, Wachtel RE, Gebhart GF. Capsaicin sensitivity and voltage-gated sodium currents in colon sensory neurons from rat dorsal root ganglia. Am J Physiol 1999; 277(6 Pt 1): G1180-8.
12. Szallasi A, Nilsson S, Farkas-Szallasi T et al. Vanilloid (capsaicin) receptors in the rat: distribution in the brain, regional differences in the spinal cord, axonal transport to the periphery, and depletion by systemic vanilloid treatment. Brain Res 1995; 703: 175-83.
13. 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.
14. Asfaw TS, Hypolite J, Northington GM et al. Acute colonic inflammation triggers detrusor instability via activation of TRPV1 receptors in a rat model of pelvic organ cross-sensitization. Am J Physiol Regul Integr Comp Physiol 2011; 300: R1392-400.
15. Ustinova EE, Fraser MO, Pezzone MA. Colonic irritation in the rat sensitizes urinary bladder afferents to mechanical and chemical stimuli: an afferent origin of pelvic organ cross-sensitization. Am J Physiol Renal Physiol 2006; 290: F1478-87.
16. Brumovsky PR, Gebhart GF. Visceral organ cross-sensitization - an integrated perspective. Auton Neurosci 2010; 153: 106-15.
17. Malykhina AP. Neural mechanisms of pelvic organ cross-sensitization. Neuroscience 2007; 149: 660-72.
18. Ustinova EE, Fraser MO, Pezzone MA. Cross-talk and sensitization of bladder afferent nerves. Neurourol Urodyn 2010; 29: 77-81.
19. Pezzone MA, Liang R, Fraser MO. A model of neural cross-talk and irritation in the pelvis: implications for the overlap of chronic pelvic pain disorders. Gastroenterology 2005;128: 1953-64.
20. Qin C, Malykhina AP, Akbarali HI et al. Cross-organ sensitization of lumbosacral spinal neurons receiving urinary bladder input in rats with inflamed colon. Gastroenterology 2005;129: 1967-78.
21. Ustinova EE, Gutkin DW, Pezzone MA. Sensitization of pelvic nerve afferents and mast cell infiltration in the urinary bladder following chronic colonic irritation is mediated by neuropeptides. Am J Physiol Renal Physiol 2007; 292: F123-30.
22. Malykhina AP, Qin C, Greenwood-Van MB et al. Hyperexcitability of convergent colon and bladder dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol Motil 2006; 18: 936-48.
23. Pan XQ, Gonzalez JA, Chang S et al. Experimental colitis triggers the release of substance P and calcitonin gene-related peptide in the urinary bladder via TRPV1 signaling pathways. Exp Neurol 2010; 225: 262-73.
24. Liu L, Oortgiesen M, Li L et al. Capsaicin inhibits activation of voltage-gated sodium currents in capsaicin-sensitive trigeminal ganglion neurons. J Neurophysiol 2001; 85: 745-58.
25. Malykhina AP, Qin C, Foreman RD et al. Colonic inflammation increases Na+ currents in bladder sensory neurons. NeuroReport 2004; 15: 2601-5.
26. Christianson JA, Liang R, Ustinova EE et al. Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 2007; 128: 235-43.
27. Cregg R, Momin A, Rugiero F et al. Pain channelopathies. J Physiol 2010;588: 1897-904.
28. Beyak MJ, Ramji N, Krol KM et al. Two TTX-resistant Na+ currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol 2004; 287: G845-55.
29. Beyak MJ, Vanner S. Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neurones: the role of voltage-gated ion channels. Neurogastroenterol Motil 2005; 17: 175-86.
30. Bielefeldt K, Ozaki N, Gebhart GF. Mild gastritis alters voltage-sensitive sodium currents in gastric sensory neurons in rats. Gastroenterology 2002; 122: 752-61.
31. Bielefeldt K, Ozaki N, Gebhart GF. Experimental ulcers alter voltage-sensitive sodium currents in rat gastric sensory neurons. Gastroenterology 2002; 122: 394-405.
32. King DE, Macleod RJ, Vanner SJ. Trinitrobenzenesulphonic acid colitis alters Na 1.8 channel expression in mouse dorsal root ganglia neurons. Neurogastroenterol Motil 2009; 21: 880-e64.
33. Chen X, Gebhart GF. Differential purinergic signaling in bladder sensory neurons of naive and bladder-inflamed mice. Pain 2010; 148: 462-72.
34. Miranda-Morales M, Ochoa-Cortes F, Stern E et al. Axon reflexes evoked by transient receptor potential vanilloid 1 activation are mediated by tetrodotoxin-resistant voltage-gated Na+ channels in intestinal afferent nerves. J Pharmacol Exp Ther 2010; 334: 566-75.
35. Berkley KJ. A life of pelvic pain. Physiol Behav 2005; 86: 272-80.
36. Amir R, Devor M. Functional cross-excitation between afferent A- and C-neurons in dorsal root ganglia. Neuroscience 2000; 95: 189-95.
37. Amir R, Michaelis M, Devor M. Burst discharge in primary sensory neurons: triggered by subthreshold oscillations, maintained by depolarizing afterpotentials. J Neurosci 2002; 22: 1187-98.
38. Amir R, Kocsis JD, Devor M. Multiple interacting sites of ectopic spike electrogenesis in primary sensory neurons. J Neurosci 2005; 25: 2576-85.
39. Amir R, Devor M. Chemically mediated cross-excitation in rat dorsal root ganglia. J Neurosci 1996; 16: 4733-41.
40. Cang CL, Zhang H, Zhang YQ et al. PKCepsilon-dependent potentiation of TTX-resistant Nav1.8 current by neurokinin-1 receptor activation in rat dorsal root ganglion neurons. Mol Pain 2009; 5: 33.
41. Ma K, Zhou QH, Chen J et al. TTX-R Na+ current-reduction by celecoxib correlates with changes in PGE(2) and CGRP within rat DRG neurons during acute incisional pain. Brain Res 2008; 1209: 57-64.
42. Natura G, von Banchet GS, Schaible HG. Calcitonin gene-related peptide enhances TTX-resistant sodium currents in cultured dorsal root ganglion neurons from adult rats. Pain 2005; 116: 194-204.
43. Pinto V, Derkach VA, Safronov BV. Role of TTX-sensitive and TTX-resistant sodium channels in Adelta- and C-fiber conduction and synaptic transmission. J Neurophysiol 2008; 99: 617-28.
44. Bernardini N, Neuhuber W, Reeh PW et al. Morphological evidence for functional capsaicin receptor expression and calcitonin gene-related peptide exocytosis in isolated peripheral nerve axons of the mouse. Neuroscience 2004; 126: 585-90.
45. Bautista DM, Jordt SE, Nikai T et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006; 124: 1269-82.
46. Salas MM, Hargreaves KM, Akopian AN. TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1. Eur J Neurosci 2009; 29: 1568-78.
47. Staruschenko A, Jeske NA, Akopian AN. Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel. J Biol Chem 2010; 285: 15167-77.
48. Ohta T, Imagawa T, Ito S. Novel gating and sensitizing mechanism of capsaicin receptor (TRPV1): tonic inhibitory regulation of extracellular sodium through the external protonation sites on TRPV1. J Biol Chem 2008; 283: 9377-87.
49. Sculptoreanu A, Kullmann FA, Artim DE et al. Nitro-oleic acid inhibits firing and activates TRPV1- and TRPA1-mediated inward currents in dorsal root ganglion neurons from adult male rats. J Pharmacol Exp Ther 2010; 333: 883-95.