Inward-rectifying potassium (Kir) channels regulate pacemaker activity in spinal nociceptive circuits during early life

Journal of Neuroscience

Volumn 33, Issue 8, 2013, Pages 3352-3362

  Li, Jie ^a   Blankenship, Meredith L ^a   Baccei, Mark L ^a  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1;

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EVOKED RESPONSE; FLUORESCENCE MICROSCOPY; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL MEMBRANE STEADY POTENTIAL; NEWBORN; NOCICEPTION; NONHUMAN; PACEMAKER NERVE CELL; PATCH CLAMP; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPIKE WAVE; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION;

AGE FACTORS; ANIMALS; BIOLOGICAL CLOCKS; CELLS, CULTURED; FEMALE; MALE; MEMBRANE POTENTIALS; NERVE NET; NOCICEPTION; ORGAN CULTURE TECHNIQUES; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD;

EID: 84874220682     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4365-12.2013     Document Type: Article

References (73)

1. Abbott GW, Butler MH, Bendahhou S, Dalakas MC, Ptacek LJ, Goldstein SA (2001) MiRP2 forms potassium channels in skeletal muscle with Kv3.4 and is associated with periodic paralysis. Cell 104:217-231. CrossRef Medline
2. Aizenman CD, Muñoz-Elías G, Cline HT (2002) Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34:623-634. CrossRef Medline
3. Baccei ML, Fitzgerald M (2004) Development of GABAergic and glycinergic transmission in the neonatal rat dorsal horn. J Neurosci 24:4749-4757. CrossRef Medline
4. Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11:18-29. CrossRef Medline
5. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC (2004) Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429:523-530. CrossRef Medline
6. Brocard F, Tazerart S, Vinay L (2010) Do pacemakers drive the central pattern generator for locomotion in mammals? Neuroscientist 16:139-155. CrossRef Medline
7. Chen X, Johnston D (2005) Constitutively active G-protein-gated inwardly rectifying K channels in dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 25:3787-3792. CrossRef Medline
8. Cheunsuang O, Maxwell D, Morris R (2002) Spinal lamina I neurones that express neurokinin 1 receptors: II. Electrophysiological characteristics, responses to primary afferent stimulation and effects of a selective muopioid receptor agonist. Neuroscience 111:423-434. CrossRef Medline
9. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, Saganich M, Vega-Saenz de ME, Rudy B (1999) Molecular diversity of K channels. Ann N Y Acad Sci 868: 233-285. CrossRef Medline
10. Day M, Carr DB, Ulrich S, Ilijic E, Tkatch T, Surmeier DJ (2005) Dendritic excitability of mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2, and Kleak channels. J Neurosci 25:8776-8787. CrossRef Medline
11. Del Negro CA, Koshiya N, Butera RJ Jr, Smith JC (2002) Persistent sodium current, membrane properties and bursting behavior of pre-botzinger complex inspiratory neurons in vitro. J Neurophysiol 88:2242-2250. CrossRef Medline
12. Derjean D, Bertrand S, Le Masson G, Landry M, Morisset V, Nagy F (2003) Dynamic balance of metabotropic inputs causes dorsal horn neurons to switch functional states. Nat Neurosci 6:274-281. CrossRef Medline
13. Dhamoon AS, Pandit SV, Sarmast F, Parisian KR, Guha P, Li Y, Bagwe S, Taffet SM, Anumonwo JM (2004) Unique Kir2.x properties determine regional and species differences in the cardiac inward rectifier K current. Circ Res 94:1332-1339. CrossRef Medline
14. Fakler B, Brändle U, Glowatzki E, Weidemann S, Zenner HP, Ruppersberg JP (1995) Strong voltage-dependent inward rectification of inward rectifier K channels is caused by intracellular spermine. Cell 80:149-154. CrossRef Medline
15. Fink M, Duprat F, Heurteaux C, Lesage F, Romey G, Barhanin J, Lazdunski M (1996) Dominant negative chimeras provide evidence for homo and heteromultimeric assembly of inward rectifier K channel proteins via their N-terminal end. FEBS Lett 378:64-68. CrossRef Medline
16. Fleidervish IA, Libman L, Katz E, Gutnick MJ (2008) Endogenous polyamines regulate cortical neuronal excitability by blocking voltage-gated Na channels. Proc Natl Acad Sci U S A 105:18994-18999. CrossRef Medline
17. Goldstein SA, Bockenhauer D, O'Kelly I, Zilberberg N (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2:175-184. CrossRef Medline
18. Gonzalez-Islas C, Wenner P (2006) Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 49:563-575. CrossRef Medline
19. Graham BA, Brichta AM, Callister RJ (2008) Recording temperature affects the excitability of mouse superficial dorsal horn neurons, in vitro. J Neurophysiol 99:2048-2059. CrossRef Medline
20. Grudt TJ, Perl ER (2002) Correlations between neuronal morphology and electrophysiological features in the rodent superficial dorsal horn. J Physiol 540:189-207. CrossRef Medline
21. Guo W, Wei F, Zou S, Robbins MT, Sugiyo S, Ikeda T, Tu JC, Worley PF, Dubner R, Ren K (2004) Group I metabotropic glutamate receptor NMDA receptor coupling and signaling cascade mediate spinal dorsal horn NMDA receptor 2B tyrosine phosphorylation associated with inflammatory hyperalgesia. J Neurosci 24:9161-9173. CrossRef Medline
22. Hanson MG, Milner LD, Landmesser LT (2008) Spontaneous rhythmic activity in early chick spinal cord influences distinct motor axon pathfinding decisions. Brain Res Rev 57:77-85. CrossRef Medline
23. Hibino H, Inanobe A, Furutani K, Murakami S, Findlay I, Kurachi Y (2010) Inwardly rectifying potassium channels: their structure, function, and physiological roles. Physiol Rev 90:291-366. CrossRef Medline
24. Ishihara K, Yan DH (2007) Low-affinity spermine block mediating outward currents through Kir2.1 and Kir2.2 inward rectifier potassium channels. J Physiol 583:891-908. CrossRef Medline
25. Jin W, Lu Z (1998) A novel high-affinity inhibitor for inward-rectifier K channels. Biochemistry 37:13291-13299. CrossRef Medline
26. Kar S, Quirion R (1995) Neuropeptide receptors in developing and adult rat spinal cord: an in vitro quantitative autoradiography study of calcitonin gene-related peptide, neurokinins, mu-opioid, galanin, somatostatin, neurotensin and vasoactive intestinal polypeptide receptors. J Comp Neurol 354:253-281. CrossRef Medline
27. Kawasaki Y, Kohno T, Zhuang ZY, Brenner GJ, Wang H, Van Der Meer C, Befort K, Woolf CJ, Ji RR (2004) Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiberinduced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci 24:8310-8321. CrossRef Medline
28. Lancaster MK, Dibb KM, Quinn CC, Leach R, Lee JK, Findlay JB, Boyett MR (2000) Residues and mechanisms for slow activation and Ba2 block of the cardiac muscarinic K channel, Kir3.1/Kir3.4. J Biol Chem 275: 35831-35839. CrossRef Medline
29. Laube G, Bernstein HG, Wolf G, Veh RW (2002) Differential distribution of spermidine/spermine-like immunoreactivity in neurons of the adult rat brain. J Comp Neurol 444:369-386. CrossRef Medline
30. Leao RM, Li S, Doiron B, Tzounopoulos T (2012) Diverse levels of an inwardly rectifying potassium conductance generate heterogeneous neuronal behavior in a population of dorsal cochlear nucleus pyramidal neurons. J Neurophysiol 107:3008-3019. CrossRef Medline
31. Li J, Baccei ML (2011) Pacemaker neurons within newborn spinal pain circuits. J Neurosci 31:9010-9022. CrossRef Medline
32. Light AR, Perl ER (1979) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:133-150. CrossRef Medline
33. Liu GX, Derst C, Schlichthörl G, Heinen S, Seebohm G, Bruggemann A, Kummer W, Veh RW, Daut J, Preisig-Muller R (2001) Comparison of cloned Kir2 channels with native inward rectifier K channels from guinea-pig cardiomyocytes. J Physiol 532:115-126. CrossRef Medline
34. Liu XJ, Gingrich JR, Vargas-Caballero M, Dong YN, Sengar A, Beggs S, Wang SH, Ding HK, Frankland PW, Salter MW (2008) Treatment of inflammatory and neuropathic pain by uncoupling Src from the NMDA receptor complex. Nat Med 14:1325-1332. CrossRef Medline
35. Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366-369. CrossRef Medline
36. Lorenzo LE, Ramien M, St Louis M, De Koninck Y, Ribeiro-da-Silva A (2008) Postnatal changes in the Rexed lamination and markers of nociceptive afferents in the superficial dorsal horn of the rat. J Comp Neurol 508:592-604. CrossRef Medline
37. Lu Z, MacKinnon R (1994) Electrostatic tuning of Mg2 affinity in an inward-rectifier K channel. Nature 371:243-246. CrossRef Medline
38. Luscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA (1997) G proteincoupled inwardly rectifying K channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19:687-695. CrossRef Medline
39. Marker CL, Luján R, Loh HH, Wickman K (2005) Spinal G-protein-gated potassium channels contribute in a dose-dependent manner to the analgesic effect of mu-and deltabut not kappa-opioids. J Neurosci 25:3551-3559. CrossRef Medline
40. Marker CL, Luján R, Colon J, Wickman K (2006) Distinct populations of spinal cord lamina II interneurons expressing G-protein-gated potassium channels. J Neurosci 26:12251-12259. CrossRef Medline
41. Matsuda H, Saigusa A, Irisawa H (1987) Ohmic conductance through the inwardly rectifying K channel and blocking by internal Mg2. Nature 325:156-159. CrossRef Medline
42. Miake J, Marban E, Nuss HB (2002) Biological pacemaker created by gene transfer. Nature 419:132-133. CrossRef Medline
43. Owen JM, Quinn CC, Leach R, Findlay JB, Boyett MR (1999) Effect of extracellular cations on the inward rectifying K channels Kir2.1 and Kir3.1/Kir3.4. Exp Physiol 84:471-488. CrossRef Medline
44. Panama BK, Lopatin AN (2006) Differential polyamine sensitivity in inwardly rectifying Kir2 potassium channels. J Physiol 571:287-302. CrossRef Medline
45. Pearson HA, Dolphin AC (1993) Inhibition of omega-conotoxin-sensitive Ca2 channel currents by internal Mg2 in cultured rat cerebellar granule neurones. Pflugers Arch 425:518-527. CrossRef Medline
46. Peña F, Ramirez JM (2004) Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network. J Neurosci 24: 7549-7556. CrossRef Medline
47. Preisig-Muller R, Schlichthörl G, Goerge T, Heinen S, Bruggemann A, Rajan S, Derst C, Veh RW, Daut J (2002) Heteromerization of Kir2.x potassium channels contributes to the phenotype of Andersen's syndrome. Proc Natl Acad Sci U S A 99:7774-7779. CrossRef Medline
48. Pruss H, Derst C, Lommel R, Veh RW (2005) Differential distribution of individual subunits of strongly inwardly rectifying potassium channels (Kir2 family) in rat brain. Brain Res Mol Brain Res 139:63-79. CrossRef Medline
49. Pujic Z, Matsumoto I, Wilce PA (1995) Expression of the genes coding for ornithine decarboxylase and its regulatory protein antizyme in the developing rat brain. Dev Neurosci 17:286-291. CrossRef Medline
50. Ramirez JM, Tryba AK, Peña F (2004) Pacemaker neurons and neuronal networks: an integrative view. Curr Opin Neurobiol 14:665-674. CrossRef Medline
51. Reali C, Fossat P, Landry M, Russo RE, Nagy F (2011) Intrinsic membrane properties of spinal dorsal horn neurones modulate nociceptive information processing in vivo. J Physiol 589:2733-2743. CrossRef Medline
52. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480. CrossRef Medline
53. Romani A (2007) Regulation of magnesium homeostasis and transport in mammalian cells. Arch Biochem Biophys 458:90-102. CrossRef Medline
54. Romani AM, Scarpa A (2000) Regulation of cellular magnesium. Front Biosci 5:D720-D734. CrossRef Medline
55. Safronov BV, Pinto V, Derkach VA (2007) High-resolution single-cell imaging for functional studies in the whole brain and spinal cord and thick tissue blocks using light-emitting diode illumination. J Neurosci Methods 164:292-298. CrossRef Medline
56. Schoenmakers TJ, Visser GJ, Flik G, Theuvenet AP (1992) CHELATOR: an improved method for computing metal ion concentrations in physiological solutions. Biotechniques 12:870-874, 876-879. Medline
57. Schram G, Melnyk P, Pourrier M, Wang Z, Nattel S (2002) Kir2.4 and Kir2.1 K() channel subunits co-assemble: a potential new contributor to inward rectifier current heterogeneity. J Physiol 544:337-349. CrossRef Medline
58. Schroeder BC, Waldegger S, Fehr S, Bleich M, Warth R, Greger R, Jentsch TJ (2000) A constitutively open potassium channel formed by KCNQ1 and KCNE3. Nature 403:196-199. CrossRef Medline
59. Shin J, Shen F, Huguenard JR (2005) Polyamines modulate AMPA receptor-dependent synaptic responses in immature layer v pyramidal neurons. J Neurophysiol 93:2634-2643. CrossRef Medline
60. Shindo Y, Fujii T, Komatsu H, Citterio D, Hotta K, Suzuki K, Oka K (2011) Newly developed Mg2-selective fluorescent probe enables visualization of Mg2 dynamics in mitochondria. PLoS One 6:e23684. CrossRef Medline
61. Sugiura Y, Lee CL, Perl ER (1986) Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 234: 358-361. CrossRef Medline
62. Szucs P, Pinto V, Safronov BV (2009) Advanced technique of infrared LED imaging of unstained cells and intracellular structures in isolated spinal cord, brainstem, ganglia and cerebellum. J Neurosci Methods 177:369-380. CrossRef Medline
63. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53:749-790. CrossRef Medline
64. Takigawa T, Alzheimer C (2002) Phasic and tonic attenuation of EPSPs by inward rectifier K channels in rat hippocampal pyramidal cells. J Physiol 539:67-75. CrossRef Medline
65. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F (2007) Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98:613-628. CrossRef Medline
66. Tazerart S, Vinay L, Brocard F (2008) The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm. J Neurosci 28:8577-8589. CrossRef Medline
67. Töpert C, Döring F, Wischmeyer E, Karschin C, Brockhaus J, Ballanyi K, Derst C, Karschin A (1998) Kir2.4: a novel K inward rectifier channel associated with motoneurons of cranial nerve nuclei. J Neurosci 18:4096-4105. Medline
68. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450:50-55. CrossRef Medline
69. Watanabe S, Kusama-Eguchi K, Kobayashi H, Igarashi K (1991) Estimation of polyamine binding to macromolecules and ATP in bovine lymphocytes and rat liver. J Biol Chem 266:20803-20809. Medline
70. Yoshimura M, Jessell TM (1989) Membrane properties of rat substantia gelatinosa neurons in vitro. J Neurophysiol 62:109-118. Medline
71. Young CC, Stegen M, Bernard R, Muller M, Bischofberger J, Veh RW, Haas CA, Wolfart J (2009) Upregulation of inward rectifier K (Kir2) channels in dentate gyrus granule cells in temporal lobe epilepsy. J Physiol 587:4213-4233. CrossRef Medline
72. Zitron E, Kiesecker C, Luck S, Kathöfer S, Thomas D, Kreye VA, Kiehn J, Katus HA, Schoels W, Karle CA (2004) Human cardiac inwardly rectifying current IKir2.2 is upregulated by activation of protein kinase A. Cardiovasc Res 63:520-527. CrossRef Medline
73. Zitron E, Günth M, Scherer D, Kiesecker C, Kulzer M, Bloehs R, Scholz EP, Thomas D, Weidenhammer C, Kathöfer S, Bauer A, Katus HA, Karle CA (2008) Kir2.x inward rectifier potassium channels are differentially regulated by adrenergic alpha1A receptors. J Mol Cell Cardiol 44:84-94. CrossRef Medline