The Kv4.2 Potassium Channel Subunit Is Required for Pain Plasticity

Neuron

Volumn 50, Issue 1, 2006, Pages 89-100

  Hu, Hui Juan ^a   Carrasquillo, Yarimar ^a   Karim, Farzana ^a   Jung, Wonil E ^b   Nerbonne, Jeanne M ^a   Schwarz, Thomas L ^b   Gereau IV, Robert W ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

MOLNEURO; PROTEINS; SIGNALING

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; POTASSIUM CHANNEL; POTASSIUM CHANNEL SUBUNIT KV4.2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; MUTATIONAL ANALYSIS; NERVE EXCITABILITY; NOCICEPTION; NONHUMAN; PAIN; PLASTICITY; PRIORITY JOURNAL; SPINAL CORD; SPINAL CORD DORSAL HORN; TACTILE STIMULATION; THERMAL STIMULATION; WILD TYPE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; CARRAGEENAN; CELLS, CULTURED; CONSTRICTION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENZYME INHIBITORS; FLAVONOIDS; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; MUTAGENESIS; NEURONAL PLASTICITY; PAIN; PAIN MEASUREMENT; PATCH-CLAMP TECHNIQUES; PHORBOL ESTERS; POSTERIOR HORN CELLS; PROTEIN SUBUNITS; REACTION TIME; ROTAROD PERFORMANCE TEST; SHAL POTASSIUM CHANNELS; SPINAL CORD; TRANSFECTION;

EID: 33646014745     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.03.010     Document Type: Article

References (46)

1. Adams J.P., Anderson A.E., Varga A.W., Dineley K.T., Cook R.G., Pfaffinger P.J., and Sweatt J.D. The A-type potassium channel kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J. Neurochem. 75 (2000) 2277-2287
2. Adwanikar H., Karim F., and Gereau R.W. Inflammation persistently enhances nocifensive behaviors mediated by spinal group I mGluRs through sustained ERK activation. Pain 111 (2004) 125-135
3. Barry D.M., Xu H., Schuessler R.B., and Nerbonne J.M. Functional knockout of the transient outward current, long-QT syndrome, and cardiac remodeling in mice expressing a dominant-negative Kv4 alpha subunit. Circ. Res. 83 (1998) 560-567
4. Basbaum A.I. Memories of Pain. Sci. Med. (Phila.) (November/December) (1996) 22-31
5. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
6. Ciruela A., Dixon A.K., Bramwell S., Gonzalez M.I., Pinnock R.D., and Lee K. Identification of MEK1 as a novel target for the treatment of neuropathic pain. Br. J. Pharmacol. 138 (2003) 751-756
7. Coetzee W.A., Amarillo Y., Chiu J., Chow A., Lau D., McCormack T., Moreno H., Nadal M.S., Ozaita A., Pountney D., et al. Molecular diversity of K+ channels. Ann. N Y Acad. Sci. 868 (1999) 233-285
8. Edwards F.A., Konnerth A., Sakmann B., and Takahashi T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch. 414 (1989) 600-612
9. Fu K.Y., Light A.R., and Maixner W. Relationship between nociceptor activity, peripheral edema, spinal microglial activation and long-term hyperalgesia induced by formalin. Neuroscience 101 (2000) 1127-1135
10. Fu K.Y., Light A.R., and Maixner W. Long-lasting inflammation and long-term hyperalgesia after subcutaneous formalin injection into the rat hindpaw. J. Pain 2 (2001) 2-11
11. Galan A., Lopez-Garcia J.A., Cervero F., and Laird J.M. Activation of spinal extracellular signaling-regulated kinase-1 and -2 by intraplantar carrageenan in rodents. Neurosci. Lett. 322 (2002) 37-40
12. Gereau R.W., and Heinemann S.F. Role of protein kinase C phosphorylation in rapid desensitization of metabotropic glutamate receptor 5. Neuron 20 (1998) 143-151
13. Guo W., Jung W.E., Marionneau C., Aimond F., Xu H., Yamada K.A., Schwarz T.L., Demolombe S., and Nerbonne J.M. Targeted deletion of Kv4.2 eliminates Ito,f and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ. Res. 97 (2005) 1342-1350
14. Hu H.J., and Gereau R.W. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J. Neurophysiol. 90 (2003) 1680-1688
15. Hu H.J., Glauner K.S., and Gereau R.W. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. I. Modulation of A-type K+ currents. J. Neurophysiol. 90 (2003) 1671-1679
16. Hugel S., and Schlichter R. Presynaptic P2X receptors facilitate inhibitory GABAergic transmission between cultured rat spinal cord dorsal horn neurons. J. Neurosci. 20 (2000) 2121-2130
17. Jerng H.H., Pfaffinger P.J., and Covarrubias M. Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol. Cell Neurosci. 27 (2004) 343-369
18. Ji R., and Rupp F. Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: relationship to c-fos induction. J. Neurosci. 17 (1997) 1776-1785
19. Ji R.R., and Woolf C.J. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol. Dis. 8 (2001) 1-10
20. Ji R.-R., Baba H., Brenner G.J., and Woolf C.J. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat. Neurosci. 2 (1999) 1114-1119
21. Ji R.R., Befort K., Brenner G.J., and Woolf C.J. ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J. Neurosci. 22 (2002) 478-485
22. Ji R.R., Kohno T., Moore K.A., and Woolf C.J. Central sensitization and LTP: do pain and memory share similar mechanisms?. Trends Neurosci. 26 (2003) 696-705
23. Karim F., Wang C.-C., and Gereau R.W. Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J. Neurosci. 21 (2001) 3771-3779
24. Karim F., Hu H.J., Adwanikar H., Kaplan D.R., and Gereau R.W. Impaired inflammatory pain and thermal hyperalgesia in mice expressing neuron-specific dominant negative mitogen activated protein kinase kinase (MEK). Mol Pain 2 (2006) 2
25. Kawasaki Y., Kohno T., Zhuang Z.Y., Brenner G.J., Wang H., Van Der Meer C., Befort K., Woolf C.J., and Ji R.R. Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J. Neurosci. 24 (2004) 8310-8321
26. Kim J., Wei D.S., and Hoffman D.A. Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J. Physiol. 569 (2005) 41-57
27. Kominato Y., Tachibana T., Dai Y., Tsujino H., Maruo S., and Noguchi K. Changes in phosphorylation of ERK and Fos expression in dorsal horn neurons following noxious stimulation in a rat model of neuritis of the nerve root. Brain Res. 967 (2003) 89-97
28. Lever I.J., Pezet S., McMahon S.B., and Malcangio M. The signaling components of sensory fiber transmission involved in the activation of ERK MAP kinase in the mouse dorsal horn. Mol. Cell Neurosci. 24 (2003) 259-270
29. Malin S.A., and Nerbonne J.M. Molecular heterogeneity of the voltage-gated fast transient outward K+ current, I(Af), in mammalian neurons. J. Neurosci. 21 (2001) 8004-8014
30. Mogil J.S., Wilson S.G., Bon K., Lee S.E., Chung K., Raber P., Pieper J.O., Hain H.S., Belknap J.K., Hubert L., et al. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 80 (1999) 67-82
31. Nassar M.A., Stirling L.C., Forlani G., Baker M.D., Matthews E.A., Dickenson A.H., and Wood J.N. Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc. Natl. Acad. Sci. USA 101 (2004) 12706-12711
32. Pezet S., Malcangio M., Lever I.J., Perkinton M.S., Thompson S.W., Williams R.J., and McMahon S.B. Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn. Mol. Cell Neurosci. 21 (2002) 684-695
33. Pongs O. Voltage-gated potassium channels: from hyperexcitability to excitement. FEBS Lett. 452 (1999) 31-35
34. Puig S., and Sorkin L.S. Formalin-evoked activity in identified primary afferent fibers: systemic lidocaine suppresses phase-2 activity. Pain 64 (1996) 345-355
35. Ramakers G.M., and Storm J.F. A postsynaptic transient K(+) current modulated by arachidonic acid regulates synaptic integration and threshold for LTP induction in hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA 99 (2002) 10144-10149
36. Ruscheweyh R., and Sandkuhler J. Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro. J. Physiol. 541 (2002) 231-244
37. Sandkuhler J., and Liu X. Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur. J. Neurosci. 10 (1998) 2476-2480
38. Schrader L.A., Birnbaum S.G., Nadin B.M., Ren Y., Bui D., Anderson A.E., and Sweatt J.D. ERK/MAPK regulates the Kv4.2 potassium channel by direct phosphorylation of the pore-forming subunit. Am. J. Physiol. Cell Physiol. 290 (2005) C852-C861
39. Song W.J. Genes responsible for native depolarization-activated K+ currents in neurons. Neurosci. Res. 42 (2002) 7-14
40. Song X.-s., Cao J.-l., Xu Y.-b., He J.-h., Zhang L.-c., and Zeng Y.-m. Activation of ERK/CREB pathway in spinal cord contributes to chronic constrictive injury-induced neuropathic pain in rats. Acta Pharmacol. Sin. 26 (2005) 789-798
41. Watanabe S., Hoffman D.A., Migliore M., and Johnston D. Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 99 (2002) 8366-8371
42. Willis W.D. Long-term potentiation in spinothalamic neurons. Brain Res. Brain Res. Rev. 40 (2002) 202-214
43. Woolf C.J., and Costigan M. Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc. Natl. Acad. Sci. USA 96 (1999) 7723-7730
44. Yang D., and Gereau R.W. Peripheral group II metabotropic glutamate receptors mediate endogenous anti-allodynia in inflammation. Pain 106 (2003) 411-417
45. Yuan L.L., Adams J.P., Swank M., Sweatt J.D., and Johnston D. Protein kinase modulation of dendritic K+ channels in hippocampus involves a mitogen-activated protein kinase pathway. J. Neurosci. 22 (2002) 4860-4868
46. Zeitz K.P., Giese K.P., Silva A.J., and Basbaum A.I. The contribution of autophosphorylated alpha-calcium-calmodulin kinase II to injury-induced persistent pain. Neuroscience 128 (2004) 889-898