The modulation of voltage-gated potassium channels by anisotonicity in trigeminal ganglion neurons

Neuroscience

Volumn 154, Issue 2, 2008, Pages 482-495

  Chen, L ^a,b,c   Liu, C ^a   Liu, L ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

hypertonicity; hypotonicity; intracellular signaling pathway; TRPV4; voltage gated potassium channels

Indexed keywords

4ALPHA PHORBOL DIDECANOATE; CYCLIC AMP DEPENDENT PROTEIN KINASE; HYPERTONIC SOLUTION; VANILLOID RECEPTOR 4; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MALE; MUSCLE HYPOTONIA; NONHUMAN; OSMOLALITY; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; TRIGEMINUS GANGLION;

ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DATA INTERPRETATION, STATISTICAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HYPERTONIC SOLUTIONS; HYPOTONIC SOLUTIONS; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PATCH-CLAMP TECHNIQUES; PHORBOL ESTERS; POTASSIUM CHANNELS, VOLTAGE-GATED; RATS; RATS, SPRAGUE-DAWLEY; SECOND MESSENGER SYSTEMS; TRIGEMINAL GANGLION; TRPV CATION CHANNELS;

EID: 46549089200     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.03.046     Document Type: Article

References (72)

1. Akins P.T., and McCleskey E.W. Characterization of potassium currents in adult rat sensory neurons and modulation by opioids and cyclic AMP. Neuroscience 56 (1993) 759-769
2. Alessandri-Haber N., Dina O.A., Joseph E.K., Reichling D., and Levine J.D. A transient receptor potential vanilloid 4-dependent mechanism of hyperalgesia is engaged by concerted action of inflammatory mediators. J Neurosci 26 (2006) 3864-3874
3. Alessandri-Haber N., Dina O.A., Yeh J.J., Parada C.A., Reichling D.B., and Levine J.D. Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J Neurosci 24 (2004) 4444-4452
4. Alessandri-Haber N., Joseph E., Dina O.A., Liedtke W., and Levine J.D. TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 118 (2005) 70-79
5. Alessandri-Haber N., Yeh J.J., Boyd A.E., Parada C.A., Chen X., Reichling D.B., and Levine J.D. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39 (2003) 497-511
6. Amir R., Liu C.N., Kocsis J.D., and Devor M. Oscillatory mechanism in primary sensory neurones. Brain 125 (2002) 421-435
7. Andrew R.D., Fagan M., Ballyk B.A., and Rosen A.S. Seizure susceptibility and the osmotic state. Brain Res 498 (1989) 175-180
8. Azouz R., Alroy G., and Yaari Y. Modulation of endogenous firing patterns by osmolarity in rat hippocampal neurones. J Physiol 502 (1997) 175-187
9. Baraban S.C., and Schwartzkroin P.A. Effects of hyposmolar solutions on membrane currents of hippocampal interneurons and mossy cells in vitro. J Neurophysiol 79 (1998) 1108-1112
10. Birinyi-Strachan L.C., Gunning S.J., Lewis R.J., and Nicholson G.M. Block of voltage-gated potassium channels by Pacific ciguatoxin-1 contributes to increased neuronal excitability in rat sensory neurons. Toxicol Appl Pharmacol 204 (2005) 175-186
11. Cardenas C.G., Del Mar L.P., and Scroggs R.S. Variation in serotonergic inhibition of calcium currents in four types of rat sensory neurons differentiated by membranes properties. J Neurophysiol 74 (1995) 1870-1879
12. Catacuzzeno L., Fioretti B., and Franciolini F. Voltage-gated outward K currents in frog saccular hair cells. J Neurophysiol 90 (2003) 3688-3701
13. Davies A.M. The trigeminal system: an advantageous experimental model for studying neuronal development. Development 103 (1988) 175-183
14. Doerner D., Pitler T.A., and Alger B.E. Protein kinase C activators block specific calcium and potassium current components in isolated hippocampal neurons. J Neurosci 8 (1988) 4069-4078
15. Du J.Q., Sun C.W., and Tang J.S. Effect of angiotensin II type 1 receptor on delayed rectifier potassium current in catecholaminergic CATH.a cells. Acta Pharmacol Sin 25 (2004) 1145-1150
16. Everill B., and Kocsis J.D. Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J Neurophysiol 82 (1999) 700-708
17. ffrench-Mullen J.M., Plata-Salaman C.R., Buckley N.J., and Danks P. Muscarine modulation by a G-protein alpha-subunit of delayed rectifier K+ current in rat ventromedial hypothalamic neurones. J Physiol 474 (1994) 21-26
18. Galeotti N., Ghelardini C., and Bartolini A. The role of potassium channels in antihistamine analgesia. Neuropharmacology 38 (1999) 1893-1901
19. Galeotti N., Ghelardini C., and Bartolini A. Involvement of potassium channels in amitriptyline and clomipramine analgesia. Neuropharmacology 40 (2001) 75-84
20. Gao X., Wu L., and O'Neil R.G. Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase c-dependent and -independent pathways. J Biol Chem 278 (2003) 27129-27137
21. + currents in adult rat sensory neurons. J Neurophysiol 75 (1996) 2629-2646
22. 2+ currents in neurons of the honeybee olfactory pathway. J Exp Biol 206 (2003) 117-129
23. Guler A.D., Lee H., Iida T., Shimizu I., Tominaga M., and Caterina M.J. Heat-evoked activation of the ion channel TRPV4. J Neurosci 22 (2002) 6408-6414
24. Gutman G.A., Chandy K.G., Grissmer S., Lazdunski M., McKinnon D., Pardo L.A., Robertson G.A., Rudy B., Sanguinetti M.C., Stuhmer W., and Wang X. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev 57 (2005) 473-508
25. Hamamoto D.T., Forkey M.W., Davis W.L., Kajander K.C., and Simone D.A. The role of pH and osmolarity in evoking the acetic acid-induced wiping response in a model of nociception in frogs. Brain Res 862 (2000) 217-229
26. Hampson R.E., Evans G.J., Mu J., Zhuang S.Y., King V.C., Childers S.R., and Deadwyler S.A. Role of cyclic AMP dependent protein kinase in cannabinoid receptor modulation of potassium "A-current" in cultured rat hippocampal neurons. Life Sci 56 (1995) 2081-2088
27. Harper A.A., and Lawson S.N. Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359 (1985) 31-46
28. Harriott A.M., Dessem D., and Gold M.S. Inflammation increases the excitability of masseter muscle afferents. Neuroscience 141 (2006) 433-442
29. Ishikawa K., Tanaka M., Black J.A., and Waxman S.G. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22 (1999) 502-507
30. Jonas E.A., and Kaczmarek L.K. Regulation of potassium channels by protein kinases. Curr Opin Neurobiol 6 (1996) 318-323
31. Kilb W., Dierkes P.W., Sykova E., Vargova L., and Luhmann H.J. Hypoosmolar conditions reduce extracellular volume fraction and enhance epileptiform activity in the CA3 region of the immature rat hippocampus. J Neurosci Res 84 (2006) 119-129
32. Kim Y., Park M.K., Uhm D.Y., Shin J., and Chung S. Modulation of delayed rectifier potassium channels by alpha1-adrenergic activation via protein kinase C zeta and p62 in PC12 cells. Neurosci Lett 387 (2005) 43-48
33. Lazarov N.E. Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus. Prog Neurobiol 66 (2002) 19-59
34. -/- mice. Proc Natl Acad Sci U S A 100 (2003) 13698-13703
35. Liedtke W., and Kim C. Functionality of the TRPV subfamily of TRP ion channels: add mechano-TRP and osmo-TRP to the lexicon!. Cell Mol Life Sci 62 24 (2005) 2985-3001
36. Liu L., Chen L., Liedtke W., and Simon S.A. Changes in osmolality sensitize the response to capsaicin in trigeminal sensory neurons. J Neurophysiol 97 (2007) 2001-2015
37. Liu L., and Simon S.A. Modulation of IA currents by capsaicin in rat trigeminal ganglion neurons. J Neurophysiol 89 (2003) 1387-1401
38. Liu L., Yang T., and Simon S.A. The protein tyrosine kinase inhibitor, genistein, decreases excitability of nociceptive neurons. Pain 112 (2004) 131-141
39. + channels by subtypes of protein kinase C. FEBS Lett 267 (1990) 25-28
40. Mason H.S., Latten M.J., Godoy L.D., Horowitz B., and Kenyon J.L. Modulation of Kv1.5 currents by protein kinase A, tyrosine kinase, and protein tyrosine phosphatase requires an intact cytoskeleton. Mol Pharmacol 61 (2002) 285-293
41. Mathie A., Wooltorton J.R., and Watkins C.S. Voltage-activated potassium channels in mammalian neurons and their block by novel pharmacological agents. Gen Pharmacol 30 (1998) 13-24
42. Matran R., Martling C.R., and Lundberg J.M. Inhibition of cholinergic and non-adrenergic, non-cholinergic bronchoconstriction in the guinea pig mediated by neuropeptide Y and alpha 2-adrenoceptors and opiate receptors. Eur J Pharmacol 163 (1989) 15-23
43. Misonou H., and Trimmer J.S. Determinants of voltage-gated potassium channel surface expression and localization in mammalian neurons. Crit Rev Biochem Mol Biol 39 (2004) 125-145
44. Moreno H., Vega-Saenz D.M., Nadal M.S., Amarillo Y., and Rudy B. Modulation of Kv3 potassium channels expressed in CHO cells by a nitric oxide-activated phosphatase. J Physiol 530 (2001) 345-358
45. Mu J., Zhuang S.Y., Hampson R.E., and Deadwyler S.A. Protein kinase-dependent phosphorylation and cannabinoid receptor modulation of potassium A current (IA) in cultured rat hippocampal neurons. Pflugers Arch 439 (2000) 541-546
46. Ocana M., Cendan C.M., Cobos E.J., Entrena J.M., and Baeyens J.M. Potassium channels and pain: present realities and future opportunities. Eur J Pharmacol 500 (2004) 203-219
47. Oliver D., Lien C.C., Soom M., Baukrowitz T., Jonas P., and Fakler B. Functional conversion between A-type and delayed rectifier K+ channels by membrane lipids. Science 304 (2004) 265-270
48. + current: role of protein kinase C-alpha. Am J Physiol Cell Physiol 281 (2001) C17-C23
49. Rasband M.N., Park E.W., Vanderah T.W., Lai J., Porreca F., and Trimmer J.S. Distinct potassium channels on pain-sensing neurons. Proc Natl Acad Sci U S A 98 (2001) 13373-13378
50. Rasband M.N., and Trimmer J.S. Voltage-gated potassium channels in sensory neurons. Nociceptive Membrane 57 (2006) 323-351
51. + channels and their functions in small dorsal root ganglion neurones of rat. J Physiol 493 (1996) 393-408
52. Saly V., and Andrew R.D. CA3 neuron excitation and epileptiform discharge are sensitive to osmolality. J Neurophysiol 69 (1993) 2200-2208
53. Schwartzkroin P.A., Baraban S.C., and Hochman D.W. Osmolarity, ionic flux, and changes in brain excitability. Epilepsy Res 32 (1998) 275-285
54. + currents in neurons of the dorsal root ganglion of the adult rat. J Pharmacol Exp Ther 310 (2004) 159-168
55. Sessle B.J. Neural mechanisms and pathways in craniofacial pain. Can J Neurol Sci 26 (1999) S7-S11
56. Slugg R.M., Meyer R.A., and Campbell J.N. Response of cutaneous A- and C-fiber nociceptors in the monkey to controlled-force stimuli. J Neurophysiol 83 (2000) 2179-2191
57. Stewart T., Beyak M.J., and Vanner S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol 552 (2003) 797-807
58. + current in hippocampal neurons. Nature 336 (1988) 379-381
59. Sun C., Du J., Raizada M.K., and Sumners C. Modulation of delayed rectifier potassium current by angiotensin II in CATH.a cells. Biochem Biophys Res Commun 310 (2003) 710-714
60. Sun H., Oudit G.Y., Ramirez R.J., Costantini D., and Backx P.H. The phosphoinositide 3-kinase inhibitor LY294002 enhances cardiac myocyte contractility via a direct inhibition of Ik, slow currents. Cardiovasc Res 62 (2004) 509-520
61. Suzuki M., Mizuno A., Kodaira K., and Imai M. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem 278 (2003) 22664-22668
62. Takeda M., Tanimoto T., Ikeda M., Nasu M., Kadoi J., Yoshida S., and Matsumoto S. Enhanced excitability of rat trigeminal root ganglion neurons via decrease in A-type potassium currents following temporomandibular joint inflammation. Neuroscience 138 (2006) 621-630
63. Todaka H., Taniguchi J., Satoh J., Mizuno A., and Suzuki M. Warm temperature-sensitive transient receptor potential vanilloid 4 (TRPV4) plays an essential role in thermal hyperalgesia. J Biol Chem 279 (2004) 35133-35138
64. Traynelis S.F., and Dingledine R. Role of extracellular space in hyperosmotic suppression of potassium-induced electrographic seizures. J Neurophysiol 61 (1989) 927-938
65. Viana F., de la Pena E., Pecson B., Schmidt R.F., and Belmonte C. Swelling-activated calcium signalling in cultured mouse primary sensory neurons. Eur J Neurosci 13 (2001) 722-734
66. Voets T., Prenen J., Vriens J., Watanabe H., Janssens A., Wissenbach U., Bodding M., Droogmans G., and Nilius B. Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277 (2002) 33704-33710
67. Vriens J., Watanabe H., Janssens A., Droogmans G., Voets T., and Nilius B. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A 101 (2004) 396-401
68. Wu R.L., Butler D.M., and Barish M.E. Potassium current development and its linkage to membrane expansion during growth of cultured embryonic mouse hippocampal neurons: sensitivity to inhibitors of phosphatidylinositol 3-kinase and other protein kinases. J Neurosci 18 (1998) 6261-6278
69. + current of pancreas-specific afferent neurons in a rat model of chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 291 (2006) G424-G431
70. Yellen G. The voltage-gated potassium channels and their relatives. Nature 419 (2002) 35-42
71. Yoshimura N., and de Groat W.C. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 19 (1999) 4644-4653
72. Yost C.S. Potassium channels: basic aspects, functional roles, and medical significance. Anesthesiology 90 (1999) 1186-1203