Kv2 dysfunction after peripheral axotomy enhances sensory neuron responsiveness to sustained input

Experimental Neurology

Volumn 251, Issue , 2014, Pages 115-126

  Tsantoulas, Christoforos ^a   Zhu, Lan ^a   Yip, Ping ^b   Grist, John ^a   Michael, Gregory J ^b   McMahon, Stephen B ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Dorsal root ganglia; Neuropathic pain; Potassium channel

Indexed keywords

MESSENGER RNA; NEUROFILAMENT 200 PROTEIN; NEUROFILAMENT PROTEIN; POTASSIUM CHANNEL KV2.1; POTASSIUM CHANNEL KV2.2; SHAB POTASSIUM CHANNEL; STROMATOXIN 1; TOXIN; UNCLASSIFIED DRUG;

ADULT; AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SIZE; CHRONIC PAIN; CONTROLLED STUDY; DOWN REGULATION; EX VIVO STUDY; GENE EXPRESSION; HYPERSENSITIVITY; IMMUNOREACTIVITY; INTRACELLULAR RECORDING; LOSS OF FUNCTION MUTATION; MALE; MECHANICAL STRESS; MYELINATED NERVE; NERVE CELL EXCITABILITY; NERVE FIBER TRANSECTION; NERVE LESION; NERVE POTENTIAL; NEUROPATHIC PAIN; NEUROPATHOLOGY; NONHUMAN; POTASSIUM CHANNELOPATHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; RAT; REFRACTORY PERIOD; SENSORY NERVE CELL; SPINAL GANGLION; TEMPERATURE STRESS; TRANSCRIPTION REGULATION;

EID: 84889562504     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.11.011     Document Type: Article

References (91)

1. Abdulla F.A., Smith P.A. Axotomy- and autotomy-induced changes in Ca2+ and K+channel currents of rat dorsal root ganglion neurons. J. Neurophysiol. 2001, 85:644-658.
2. Blackburn-Munro G., Jensen B.S. The anticonvulsant retigabine attenuates nociceptive behaviours in rat models of persistent and neuropathic pain. Eur. J. Pharmacol. 2003, 460:109-116.
3. Blaine J.T., Ribera A.B. Kv2 channels form delayed-rectifier potassium channels in situ. J. Neurosci. 2001, 21:1473-1480.
4. Bocksteins E., Raes A.L., Van de Vijver G., Bruyns T., Van Bogaert P.P., Snyders D.J. Kv2.1 and silent Kv subunits underlie the delayed rectifier K+current in cultured small mouse DRG neurons. Am. J. Physiol. Cell Physiol. 2009, 296:C1271-C1278.
5. Bocksteins E., Labro A.J., Snyders D.J., Mohapatra D.P. The electrically silent Kv6.4 subunit confers hyperpolarized gating charge movement in Kv2.1/Kv6.4 heterotetrameric channels. PLoS One 2012, 7:e37143.
6. Calvo M., Bennett D.L. The mechanisms of microgliosis and pain following peripheral nerve injury. Exp. Neurol. 2012, 234:271-282.
7. Cao X.H., Byun H.S., Chen S.R., Cai Y.Q., Pan H.L. Reduction in voltage-gated K+channel activity in primary sensory neurons in painful diabetic neuropathy: role of brain-derived neurotrophic factor. J. Neurochem. 2010, 114:1460-1475.
8. Catacuzzeno L., Fioretti B., Pietrobon D., Franciolini F. The differential expression of low-threshold K+currents generates distinct firing patterns in different subtypes of adult mouse trigeminal ganglion neurones. J. Physiol. 2008, 586:5101-5118.
9. Cerda O., Trimmer J.S. Activity-dependent phosphorylation of neuronal Kv2.1 potassium channels by CDK5. J. Biol. Chem. 2011, 286:28738-28748.
10. Chew D.J., Carlstedt T., Shortland P.J. A comparative histological analysis of two models of nerve root avulsion injury in the adult rat. Neuropathol. Appl. Neurobiol. 2011, 37:613-632.
11. Chien L.Y., Cheng J.K., Chu D., Cheng C.F., Tsaur M.L. Reduced expression of A-type potassium channels in primary sensory neurons induces mechanical hypersensitivity. J. Neurosci. 2007, 27:9855-9865.
12. Deutsch E., Weigel A.V., Akin E.J., Fox P., Hansen G., Haberkorn C.J., Loftus R., Krapf D., Tamkun M.M. Kv2.1 cell surface clusters are insertion platforms for ion channel delivery to the plasma membrane. Mol. Biol. Cell 2012, 23:2917-2929.
13. Devor M. Sodium channels and mechanisms of neuropathic pain. J. Pain 2006, 7:S3-S12.
14. Dost R., Rostock A., Rundfeldt C. The anti-hyperalgesic activity of retigabine is mediated by KCNQ potassium channel activation. Naunyn Schmiedebergs Arch. Pharmacol. 2004, 369:382-390.
15. Du J., Haak L.L., Phillips-Tansey E., Russell J.T., McBain C.J. Frequency-dependent regulation of rat hippocampal somato-dendritic excitability by the K+channel subunit Kv2.1. J. Physiol. 2000, 522(Pt 1):19-31.
16. Everill B., Kocsis J.D. Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J. Neurophysiol. 1999, 82:700-708.
17. Everill B., Kocsis J.D. Nerve growth factor maintains potassium conductance after nerve injury in adult cutaneous afferent dorsal root ganglion neurons. Neuroscience 2000, 100:417-422.
18. Everill B., Rizzo M.A., Kocsis J.D. Morphologically identified cutaneous afferent DRG neurons express three different potassium currents in varying proportions. J. Neurophysiol. 1998, 79:1814-1824.
19. Feinshreiber L., Singer-Lahat D., Friedrich R., Matti U., Sheinin A., Yizhar O., Nachman R., Chikvashvili D., Rettig J., Ashery U., Lotan I. Non-conducting function of the Kv2.1 channel enables it to recruit vesicles for release in neuroendocrine and nerve cells. J. Cell Sci. 2010, 123:1940-1947.
20. Fink M., Duprat F., Lesage F., Heurteaux C., Romey G., Barhanin J., Lazdunski M. A new K+channel beta subunit to specifically enhance Kv2.2 (CDRK) expression. J. Biol. Chem. 1996, 271:26341-26348.
21. Frech G.C., VanDongen A.M., Schuster G., Brown A.M., Joho R.H. A novel potassium channel with delayed rectifier properties isolated from rat brain by expression cloning. Nature 1989, 340:642-645.
22. Gold M.S., Shuster M.J., Levine J.D. Characterization of six voltage-gated K+currents in adult rat sensory neurons. J. Neurophysiol. 1996, 75:2629-2646.
23. Guan D., Tkatch T., Surmeier D.J., Armstrong W.E., Foehring R.C. Kv2 subunits underlie slowly inactivating potassium current in rat neocortical pyramidal neurons. J. Physiol. 2007, 581:941-960.
24. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
25. Hille B., Armstrong C.M., MacKinnon R. Ion channels: from idea to reality. Nat. Med. 1999, 5:1105-1109.
26. Hugnot J.P., Salinas M., Lesage F., Guillemare E., de Weille J., Heurteaux C., Mattei M.G., Lazdunski M. Kv8.1, a new neuronal potassium channel subunit with specific inhibitory properties towards Shab and Shaw channels. EMBO J. 1996, 15:3322-3331.
27. Hwang P.M., Glatt C.E., Bredt D.S., Yellen G., Snyder S.H. A novel K+channel with unique localizations in mammalian brain: molecular cloning and characterization. Neuron 1992, 8:473-481.
28. Hwang P.M., Fotuhi M., Bredt D.S., Cunningham A.M., Snyder S.H. Contrasting immunohistochemical localizations in rat brain of two novel K+channels of the Shab subfamily. J. Neurosci. 1993, 13:1569-1576.
29. Ikematsu N., Dallas M.L., Ross F.A., Lewis R.W., Rafferty J.N., David J.A., Suman R., Peers C., Hardie D.G., Evans A.M. Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:18132-18137.
30. Johnston J., Griffin S.J., Baker C., Skrzypiec A., Chernova T., Forsythe I.D. Initial segment Kv2.2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in medial nucleus of the trapezoid body neurons. J. Physiol. 2008, 586:3493-3509.
31. Johnston J., Forsythe I.D., Kopp-Scheinpflug C. Going native: voltage-gated potassium channels controlling neuronal excitability. J. Physiol. 2010, 588:3187-3200.
32. Kajander K.C., Bennett G.J. Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in A beta and A delta primary afferent neurons. J. Neurophysiol. 1992, 68:734-744.
33. Kajander K.C., Wakisaka S., Bennett G.J. Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat. Neurosci. Lett. 1992, 138:225-228.
34. Kerschensteiner D., Stocker M. Heteromeric assembly of Kv2.1 with Kv9.3: effect on the state dependence of inactivation. Biophys. J. 1999, 77:248-257.
35. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363.
36. Kim D.S., Choi J.O., Rim H.D., Cho H.J. Downregulation of voltage-gated potassium channel alpha gene expression in dorsal root ganglia following chronic constriction injury of the rat sciatic nerve. Brain Res. Mol. Brain Res. 2002, 105:146-152.
37. Kramer J.W., Post M.A., Brown A.M., Kirsch G.E. Modulation of potassium channel gating by coexpression of Kv2.1 with regulatory Kv5.1 or Kv6.1 alpha-subunits. Am. J. Physiol. 1998, 274:C1501-C1510.
38. Leung Y.M., Kang Y., Gao X., Xia F., Xie H., Sheu L., Tsuk S., Lotan I., Tsushima R.G., Gaisano H.Y. Syntaxin 1A binds to the cytoplasmic C terminus of Kv2.1 to regulate channel gating and trafficking. J. Biol. Chem. 2003, 278:17532-17538.
39. Liu X., Chung K., Chung J.M. Ectopic discharges and adrenergic sensitivity of sensory neurons after spinal nerve injury. Brain Res. 1999, 849:244-247.
40. Liu C.N., Wall P.D., Ben-Dor E., Michaelis M., Amir R., Devor M. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 2000, 85:503-521.
41. Loeser J.D. Dorsal rhizotomy for the relief of chronic pain. J. Neurosurg. 1972, 36:745-750.
42. Malin S.A., Nerbonne J.M. Delayed rectifier K+currents, IK, are encoded by Kv2 alpha-subunits and regulate tonic firing in mammalian sympathetic neurons. J. Neurosci. 2002, 22:10094-10105.
43. McCarthy P.W., Lawson S.N. Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience 1990, 34:623-632.
44. Michael G.J., Averill S., Nitkunan A., Rattray M., Bennett D.L., Yan Q., Priestley J.V. Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J. Neurosci. 1997, 17:8476-8490.
45. Michael G.J., Averill S., Shortland P.J., Yan Q., Priestley J.V. Axotomy results in major changes in BDNF expression by dorsal root ganglion cells: BDNF expression in large trkB and trkC cells, in pericellular baskets, and in projections to deep dorsal horn and dorsal column nuclei. Eur. J. Neurosci. 1999, 11:3539-3551.
46. Michaelis M., Liu X., Janig W. Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion. J. Neurosci. 2000, 20:2742-2748.
47. Mishra S., Bhatnagar S., Goyal G.N., Rana S.P., Upadhya S.P. A comparative efficacy of amitriptyline, gabapentin, and pregabalin in neuropathic cancer pain: a prospective randomized double-blind placebo-controlled study. Am. J. Hosp. Palliat. Care 2012, 29:177-182.
48. Misonou H., Mohapatra D.P., Park E.W., Leung V., Zhen D., Misonou K., Anderson A.E., Trimmer J.S. Regulation of ion channel localization and phosphorylation by neuronal activity. Nat. Neurosci. 2004, 7:711-718.
49. Misonou H., Mohapatra D.P., Trimmer J.S. Kv2.1: a voltage-gated k+channel critical to dynamic control of neuronal excitability. Neurotoxicology 2005, 26:743-752.
50. Molander C., Hongpaisan J., Persson J.K. Distribution of c-fos expressing dorsal horn neurons after electrical stimulation of low threshold sensory fibers in the chronically injured sciatic nerve. Brain Res. 1994, 644:74-82.
51. Murakoshi H., Trimmer J.S. Identification of the Kv2.1K+channel as a major component of the delayed rectifier K+current in rat hippocampal neurons. J. Neurosci. 1999, 19:1728-1735.
52. Noguchi K., Kawai Y., Fukuoka T., Senba E., Miki K. Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J. Neurosci. 1995, 15:7633-7643.
53. O'Connell K.M., Loftus R., Tamkun M.M. Localization-dependent activity of the Kv2.1 delayed-rectifier K+channel. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:12351-12356.
54. Pal S., Hartnett K.A., Nerbonne J.M., Levitan E.S., Aizenman E. Mediation of neuronal apoptosis by Kv2.1-encoded potassium channels. J. Neurosci. 2003, 23:4798-4802.
55. Park S.Y., Choi J.Y., Kim R.U., Lee Y.S., Cho H.J., Kim D.S. Downregulation of voltage-gated potassium channel alpha gene expression by axotomy and neurotrophins in rat dorsal root ganglia. Mol. Cells 2003, 16:256-259.
56. Park K.S., Mohapatra D.P., Misonou H., Trimmer J.S. Graded regulation of the Kv2.1 potassium channel by variable phosphorylation. Science 2006, 313:976-979.
57. Peltola M.A., Kuja-Panula J., Lauri S.E., Taira T., Rauvala H. AMIGO is an auxiliary subunit of the Kv2.1 potassium channel. EMBO Rep. 2011, 12:1293-1299.
58. Pongs O., Schwarz J.R. Ancillary subunits associated with voltage-dependent K+channels. Physiol. Rev. 2010, 90:755-796.
59. Raja S.N., Meyer R.A., Campbell J.N. Peripheral mechanisms of somatic pain. Anesthesiology 1988, 68:571-590.
60. Rasband M.N., Park E.W., Vanderah T.W., Lai J., Porreca F., Trimmer J.S. Distinct potassium channels on pain-sensing neurons. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13373-13378.
61. Redman P.T., He K., Hartnett K.A., Jefferson B.S., Hu L., Rosenberg P.A., Levitan E.S., Aizenman E. Apoptotic surge of potassium currents is mediated by p38 phosphorylation of Kv2.1. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3568-3573.
62. Rose K., Ooi L., Dalle C., Robertson B., Wood I.C., Gamper N. Transcriptional repression of the M channel subunit Kv7.2 in chronic nerve injury. Pain 2011, 152:742-754.
63. Roza C., Lopez-Garcia J.A. Retigabine, the specific KCNQ channel opener, blocks ectopic discharges in axotomized sensory fibres. Pain 2008, 138:537-545.
64. Salinas M., de Weille J., Guillemare E., Lazdunski M., Hugnot J.P. Modes of regulation of shab K+channel activity by the Kv8.1 subunit. J. Biol. Chem. 1997, 272:8774-8780.
65. Salinas M., Duprat F., Heurteaux C., Hugnot J.P., Lazdunski M. New modulatory alpha subunits for mammalian Shab K+channels. J. Biol. Chem. 1997, 272:24371-24379.
66. Sano Y., Mochizuki S., Miyake A., Kitada C., Inamura K., Yokoi H., Nozawa K., Matsushime H., Furuichi K. Molecular cloning and characterization of Kv6.3, a novel modulatory subunit for voltage-gated K(+) channel Kv2.1. FEBS Lett. 2002, 512:230-234.
67. Sarmiere P.D., Weigle C.M., Tamkun M.M. The Kv2.1K+channel targets to the axon initial segment of hippocampal and cortical neurons in culture and in situ. BMC Neurosci. 2008, 9:112.
68. Scholz A., Gruss M., Vogel W. Properties and functions of calcium-activated K+channels in small neurones of rat dorsal root ganglion studied in a thin slice preparation. J. Physiol. 1998, 513(Pt 1):55-69.
69. Sharma N., D'Arcangelo G., Kleinlaus A., Halegoua S., Trimmer J.S. Nerve growth factor regulates the abundance and distribution of K+channels in PC12 cells. J. Cell Biol. 1993, 123:1835-1843.
70. Sheen K., Chung J.M. Signs of neuropathic pain depend on signals from injured nerve fibers in a rat model. Brain Res. 1993, 610:62-68.
71. Song M.Y., Hong C., Bae S.H., So I., Park K.S. Dynamic modulation of the kv2.1 channel by SRC-dependent tyrosine phosphorylation. J. Proteome Res. 2012, 11:1018-1026.
72. Steinert J.R., Robinson S.W., Tong H., Haustein M.D., Kopp-Scheinpflug C., Forsythe I.D. Nitric oxide is an activity-dependent regulator of target neuron intrinsic excitability. Neuron 2011, 71:291-305.
73. Stocker M., Hellwig M., Kerschensteiner D. Subunit assembly and domain analysis of electrically silent K+ channel alpha-subunits of the rat Kv9 subfamily. J. Neurochem. 1999, 72:1725-1734.
74. Stoney S.D. Limitations on impulse conduction at the branch point of afferent axons in frog dorsal root ganglion. Exp. Brain Res. 1990, 80:512-524.
75. Study R.E., Kral M.G. Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain 1996, 65:235-242.
76. Sukhotinsky I., Ben-Dor E., Raber P., Devor M. Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. Eur. J. Pain 2004, 8:135-143.
77. Sun W., Miao B., Wang X.C., Duan J.H., Wang W.T., Kuang F., Xie R.G., Xing J.L., Xu H., Song X.J., Luo C., Hu S.J. Reduced conduction failure of the main axon of polymodal nociceptive C-fibres contributes to painful diabetic neuropathy in rats. Brain 2012, 135:359-375.
78. Swanson R., Marshall J., Smith J.S., Williams J.B., Boyle M.B., Folander K., Luneau C.J., Antanavage J., Oliva C., Buhrow S.A., et al. Cloning and expression of cDNA and genomic clones encoding three delayed rectifier potassium channels in rat brain. Neuron 1990, 4:929-939.
79. Tan Z.Y., Donnelly D.F., LaMotte R.H. Effects of a chronic compression of the dorsal root ganglion on voltage-gated Na+ and K+ currents in cutaneous afferent neurons. J. Neurophysiol. 2006, 95:1115-1123.
80. Thibault K., Calvino B., Dubacq S., Roualle-de-Rouville M., Sordoillet V., Rivals I., Pezet S. Cortical effect of oxaliplatin associated with sustained neuropathic pain: exacerbation of cortical activity and down-regulation of potassium channel expression in somatosensory cortex. Pain 2012, 153:1636-1647.
81. Tsantoulas C., Zhu L., Shaifta Y., Grist J., Ward J.P., Raouf R., Michael G.J., McMahon S.B. Sensory neuron downregulation of the Kv9.1 potassium channel subunit mediates neuropathic pain following nerve injury. J. Neurosci. 2012, 32:17502-17513.
82. Vacher H., Trimmer J.S. Diverse roles for auxiliary subunits in phosphorylation-dependent regulation of mammalian brain voltage-gated potassium channels. Pflugers Arch. 2011, 462:631-643.
83. Vega-Saenz de Miera E.C. Modification of Kv2.1 K+ currents by the silent Kv10 subunits. Brain Res. Mol. Brain Res. 2004, 123:91-103.
84. Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 2012, 13:227-232.
85. Wu Q., Henry J.L. Peripheral drive in Aalpha/beta-fiber neurons is altered in a rat model of osteoarthritis: changes in following frequency and recovery from inactivation. J. Pain Res. 2013, 6:207-221.
86. Wu G., Ringkamp M., Hartke T.V., Murinson B.B., Campbell J.N., Griffin J.W., Meyer R.A. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J. Neurosci. 2001, 21:RC140.
87. Yang E.K., Takimoto K., Hayashi Y., de Groat W.C., Yoshimura N. Altered expression of potassium channel subunit mRNA and alpha-dendrotoxin sensitivity of potassium currents in rat dorsal root ganglion neurons after axotomy. Neuroscience 2004, 123:867-874.
88. Yoon Y.W., Na H.S., Chung J.M. Contributions of injured and intact afferents to neuropathic pain in an experimental rat model. Pain 1996, 64:27-36.
89. Zhang J.M., Donnelly D.F., Song X.J., Lamotte R.H. Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J. Neurophysiol. 1997, 78:2790-2794.
90. Zhao X., Tang Z., Zhang H., Atianjoh F.E., Zhao J.Y., Liang L., Wang W., Guan X., Kao S.C., Tiwari V., Gao Y.J., Hoffman P.N., Cui H., Li M., Dong X., Tao Y.X. A long noncoding RNA contributes to neuropathic pain by silencing Kcna2 in primary afferent neurons. Nat. Neurosci. 2013, 1024-1031.
91. Zhu Y., Mehta K., Li C., Xu G.Y., Liu L., Colak T., Shenoy M., Pasricha P.J. Systemic administration of anti-NGF increases A-type potassium currents and decreases pancreatic nociceptor excitability in a rat model of chronic pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302:G176-G181.