Colitis decreases mechanosensitive K2p channel expression and function in mouse colon sensory neurons

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 1, 2011, Pages

  La, Jun Ho ^a   Gebhart, G F ^a  

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

Author keywords

Dorsal root ganglia neurons; Mechanosensitive channels; TREK channels

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM CHANNEL TRAAK; POTASSIUM CHANNEL TREK 1; POTASSIUM CHANNEL TREK 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COLITIS; CONTROLLED STUDY; GENE EXPRESSION; LUMBOSACRAL PLEXUS; LUMBOSACRAL SPINE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL GANGLION; THORACOLUMBAR SPINE;

ANIMALS; CELLS, CULTURED; COLITIS; COLON; GANGLIA, SPINAL; GENE EXPRESSION; MALE; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; SENSORY RECEPTOR CELLS; SPLANCHNIC NERVES; TRINITROBENZENESULFONIC ACID;

EID: 79959836378     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00417.2010     Document Type: Article

References (55)

1. Al-Taher A, Bashein A, Nolan T, Hollingsworth M, Brady G. Global cDNA amplification combined with real-time RT-PCR: accurate quantification of multiple human potassium channel genes at the single cell level. Yeast 17: 201-210, 2000.
2. Alloui A, Zimmermann K, Mamet J, Duprat F, Noel J, Chemin J, Guy N, Blondeau N, Voilley N, Rubat-Coudert C, Borsotto M, Romey G, Heurteaux C, Reeh P, Eschalier A, Lazdunski M. TREK-1, a K+ channel involved in polymodal pain perception. EMBO J 25: 2368-2376, 2006.
3. Baker SA, Hatton WJ, Han J, Hennig GW, Britton FC, Koh SD. Role of TREK-1 potassium channel in bladder overactivity after partial bladder outlet obstruction in mouse. J Urol 183: 793-800, 2010.
4. Baker SA, Hennig GW, Han J, Britton FC, Smith TK, Koh SD. Methionine and its derivatives increase bladder excitability by inhibiting stretch-dependent K(+) channels. Br J Pharmacol 153: 1259-1271, 2008.
5. Bang H, Kim Y, Kim D. TREK-2, a new member of the mechanosensitive tandem-pore K+ channel family. J Biol Chem 275: 17412-17419, 2000.
6. Brierley SM, Carter R, Jones W III, 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. Brierley SM, Hughes PA, Page AJ, Kwan KY, Martin CM, O'Donnell TA, Cooper NJ, Harrington AM, Adam B, Liebregts T, Holtmann G, Corey DP, Rychkov GY, Blackshaw LA. The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137: 2084-2095, 2009.
8. Brierley SM, Jones RC 3rd, Gebhart GF, Blackshaw LA. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127: 166-178, 2004.
9. Brierley SM, Page AJ, Hughes PA, Adam B, Liebregts T, Cooper NJ, Holtmann G, Liedtke W, Blackshaw LA. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 134: 2059-2069, 2008.
10. 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 135: 937-46, 946, 2008.
11. Chen X, Gebhart GF. Differential purinergic signaling in bladder sensory neurons of naive and bladder-inflamed mice. Pain 148: 462-472, 2010.
12. Christianson JA, McIlwrath SL, Koerber HR, Davis BM. Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 140: 247-257, 2006.
13. Dang K, Bielefeldt K, Gebhart GF. Differential responses of bladder lumbosacral and thoracolumbar dorsal root ganglion neurons to purinergic agonists, protons, and capsaicin. J Neurosci 25: 3973-3984, 2005.
14. Dang K, Lamb K, Cohen M, Bielefeldt K, Gebhart GF. Cyclophosphamide-induced bladder inflammation sensitizes and enhances P2X receptor function in rat bladder sensory neurons. J Neurophysiol 99: 49-59, 2008.
15. Dulac C. Cloning of genes from single neurons. Curr Top Dev Biol 36: 245-258, 1998.
16. Ennes HS, Young SH, Raybould HE, Mayer EA. Intercellular communication between dorsal root ganglion cells and colonic smooth muscle cells in vitro. Neuroreport 8: 733-737, 1997.
17. Eutamene H, Bradesi S, Larauche M, Theodorou V, Beaufrand C, Ohning G, Fioramonti J, Cohen M, Bryant AP, Kurtz C, Currie MG, Mayer EA, Bueno L. Guanylate cyclase C-mediated antinociceptive effects of linaclotide in rodent models of visceral pain. Neurogastroenterol Motil 22: 312-e84, 2009.
18. 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.
19. Friedrich AE, Gebhart GE. Effects of spinal cholecystokinin receptor antagonists on morphine antinociception in a model of visceral pain in the rat. J Pharmacol Exp Ther 292: 538-544, 2000.
20. Han J, Gnatenco C, Sladek CD, Kim D. Background and tandem-pore potassium channels in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol 546: 625-639, 2003.
21. Holt AG, Asako M, Duncan RK, Lomax CA, Juiz JM, Altschuler RA. Deafness associated changes in expression of two-pore domain potassium channels in the rat cochlear nucleus. Hear Res 216-217: 146-153, 2006.
22. Hughes PA, Brierley SM, Young RL, Blackshaw LA. Localization and comparative analysis of acid-sensing ion channel (ASIC1, 2, and 3) mRNA expression in mouse colonic sensory neurons within thoracolumbar dorsal root ganglia. J Comp Neurol 500: 863-875, 2007.
23. 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.
24. Kang D, Choe C, Kim D. Thermosensitivity of the two-pore domain K+ channels TREK-2 and TRAAK. J Physiol 564: 103-116, 2005.
25. Kang D, Han J, Kim D. Mechanism of inhibition of TREK-2 (K2P10.1) by the Gq-coupled M3 muscarinic receptor. Am J Physiol Cell Physiol 291: C649-C656, 2006.
26. Kang D, Kim D. TREK2 (K2P10.1) and TRESK (K2P18.1) are major background K+ channels in dorsal root ganglion neurons. Am J Physiol Cell Physiol 291: C138-C146, 2006.
27. Kim D. Physiology and pharmacology of two-pore domain potassium channels. Curr Pharm Des 11: 2717-2736, 2005.
28. Kim Y, Gnatenco C, Bang H, Kim D. Localization of TREK-2 K+ channel domains that regulate channel kinetics and sensitivity to pressure, fatty acids and pHi. Pflügers Arch 442: 952-960, 2001.
29. La JH, Gebhart GF. Expression of mechanosensitive two pore-domain K+ channels in dorsal root ganglia neurons innervating mouse bladder and colon. Program No. 655.5 2009. In: Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009.
30. Lamb K, Zhong F, Gebhart GF, Bielefeldt K. Experimental colitis in mice and sensitization of converging visceral and somatic afferent pathways. Am J Physiol Gastrointest Liver Physiol 290: G451-G457, 2006.
31. Maingret F, Fosset M, Lesage F, Lazdunski M, Honore E. TRAAK is a mammalian neuronal mechano-gated K+ channel. J Biol Chem 274: 1381-1387, 1999.
32. Maingret F, Lauritzen I, Patel AJ, Heurteaux C, Reyes R, Lesage F, Lazdunski M, Honore E. TREK-1 is a heat-activated background K(+) channel. EMBO J 19: 2483-2491, 2000.
33. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honore E. Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel. J Biol Chem 274: 26691-26696, 1999.
34. Maingret F, Patel AJ, Lesage F, Lazdunski M, Honore E. Lysophospholipids open the two-pore domain mechano-gated K(+) channels TREK-1 and TRAAK. J Biol Chem 275: 10128-10133, 2000.
35. Malin SA, Christianson JA, Bielefeldt K, Davis BM. TPRV1 expression defines functionally distinct pelvic colon afferents. J Neurosci 29: 743-752, 2009.
36. Medhurst AD, Rennie G, Chapman CG, Meadows H, Duckworth MD, Kelsell RE, Gloger II, Pangalos MN. Distribution analysis of human twopore domain potassium channels in tissues of the central nervous system and periphery. Brain Res Mol Brain Res 86: 101-114, 2001.
37. 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.
38. Ness TJ, Gebhart GJ. Characterization of neuronal responses to noxious visceral and somatic stimuli in the medial lumbosacral spinal cord of the rat. J Neurophysiol 57: 1867-1892, 1987.
39. Ness TJ, Gebhart GJ. Characterization of neurons responsive to noxious colorectal distension in the T13-L2 spinal cord of the rat. J Neurophysiol 60: 1419-1438, 1988.
40. Noel J, Zimmermann K, Busserolles J, Deval E, Alloui A, Diochot S, Guy N, Borsotto M, Reeh P, Eschalier A, Lazdunski M. The mechanoactivated K+ channels TRAAK and TREK-1 control both warm and cold perception. EMBO J 28: 1308-1318, 2009.
41. Page AJ, Brierley SM, Martin CM, Price MP, Symonds E, Butler R, Wemmie JA, Blackshaw LA. Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 54: 1408-1415, 2005.
42. Patel AJ, Honore E, Maingret F, Lesage F, Fink M, Duprat F, Lazdunski M. A mammalian two pore domain mechano-gated S-like K+channel. EMBO J 17: 4283-4290, 1998.
43. Peixoto A, Monteiro M, Rocha B, Veiga-Fernandes H. Quantification of multiple gene expression in individual cells. Genome Res 14: 1938-1947, 2004.
44. Raybould HE, Gschossman JM, Ennes H, Lembo T, Mayer EA. Involvement of stretch-sensitive calcium flux in mechanical transduction in visceral afferents. J Auton Nerv Syst 75: 1-6, 1999.
45. 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.
46. Smirnov SV, Aaronson PI. Modulatory effects of arachidonic acid on the delayed rectifier K+ current in rat pulmonary arterial myocytes. Structural aspects and involvement of protein kinase C. Circ Res 79: 20-31, 1996.
47. Soliven B, Wang N. Arachidonic acid inhibits potassium conductances in cultured rat oligodendrocytes. Am J Physiol Cell Physiol 269: C341-C348, 1995.
48. Somjen GG. Low external NaCl concentration and low osmolarity enhance voltage-gated Ca currents but depress K currents in freshly isolated rat hippocampal neurons. Brain Res 851: 189-197, 1999.
49. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA. CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21: 7491-7505, 2001.
50. 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.
51. Toulouse M, Coelho AM, Fioramonti J, Lecci A, Maggi C, Bueno L. Role of tachykinin NK2 receptors in normal and altered rectal sensitivity in rats. Br J Pharmacol 129: 193-199, 2000.
52. Xian TL, Dyachenko V, Zuzarte M, Putzke C, Preisig-Muller R, Isenberg G, Daut J. The stretch-activated potassium channel TREK-1 in rat cardiac ventricular muscle. Cardiovasc Res 69: 86-97, 2006.
53. Xu L, Gebhart GF. Characterization of mouse lumbar splanchnic and pelvic nerve urinary bladder mechanosensory afferents. J Neurophysiol 99: 244-253, 2008.
54. Yamamoto Y, Hatakeyama T, Taniguchi K. Immunohistochemical colocalization of TREK-1, TREK-2 and TRAAK with TRP channels in the trigeminal ganglion cells. Neurosci Lett 454: 129-133, 2009.
55. Zhao H, Sprunger LK, Simasko SM. Expression of transient receptor potential channels and two-pore potassium channels in subtypes of vagal afferent neurons in rat. Am J Physiol Gastrointest Liver Physiol 298: G212-G221, 2010.