Neuroplasticity of A-type potassium channel complexes induced by chronic alcohol exposure enhances dendritic calcium transients in hippocampus

详细信息    查看全文

• 作者：Patrick J. Mulholland ; Kathryn B. Spencer ; Wei Hu ; Sven Kroener…
• 关键词：Back ; propagating action potentials ; CA1 pyramidal neurons ; Chronic alcohol ; Dendritic calcium transients ; KChIP3 ; Kv4.2 channels
• 刊名：Psychopharmacology
• 出版年：2015
• 出版时间：June 2015
• 年：2015
• 卷：232
• 期：11
• 页码：1995-2006
• 全文大小：1,312 KB
• 参考文献：Abrahao KP, Ariwodola OJ, Butler TR, Rau AR, Skelly MJ, Carter E, Alexander NP, McCool BA, Souza-Formigoni ML, Weiner JL (2013) Locomotor sensitization to ethanol impairs NMDA receptor-dependent synaptic plasticity in the nucleus accumbens and increases ethanol self-administration. J Neurosci 33:4834鈥?842View Article PubMed Central PubMed
  Aldridge GM, Podrebarac DM, Greenough WT, Weiler IJ (2008) The use of total protein stains as loading controls: an alternative to high-abundance single-protein controls in semi-quantitative immunoblotting. J Neurosci Methods 172:250鈥?54View Article PubMed Central PubMed
  Alexander JC, McDermott CM, Tunur T, Rands V, Stelly C, Karhson D, Bowlby MR, An WF, Sweatt JD, Schrader LA (2009) The role of calsenilin/DREAM/KChIP3 in contextual fear conditioning. Learn Mem 16:167鈥?77View Article PubMed Central PubMed
  Badanich KA, Doremus-Fitzwater TL, Mulholland PJ, Randall PK, Delpire E, Becker HC (2011) NR2B-deficient mice are more sensitive to the locomotor stimulant and depressant effects of ethanol. Genes Brain Behav 10:805鈥?16View Article PubMed Central PubMed
  Bernard C, Johnston D (2003) Distance-dependent modifiable threshold for action potential back-propagation in hippocampal dendrites. J Neurophysiol 90:1807鈥?816View Article PubMed
  Caporale N, Dan Y (2008) Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci 31:25鈥?6View Article PubMed
  Carpenter-Hyland EP, Chandler LJ (2006) Homeostatic plasticity during alcohol exposure promotes enlargement of dendritic spines. Eur J Neurosci 24:3496鈥?506View Article PubMed
  Carpenter-Hyland EP, Woodward JJ, Chandler LJ (2004) Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors. J Neurosci 24:7859鈥?868View Article PubMed
  Cartlidge D, Redmond AD (1990) Alcohol and conscious level. Biomed Pharmacother 44:205鈥?08View Article PubMed
  Castellino RC, Morales MJ, Strauss HC, Rasmusson RL (1995) Time- and voltage-dependent modulation of a Kv1.4 channel by a beta-subunit (Kv beta 3) cloned from ferret ventricle. Am J Physiol 269:H385鈥揌391PubMed
  Chen X, Yuan LL, Zhao C, Birnbaum SG, Frick A, Jung WE, Schwarz TL, Sweatt JD, Johnston D (2006) Deletion of Kv4.2 gene eliminates dendritic A-type K+ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurosci: Off J Soc Neurosci 26:12143鈥?2151View Article
  Clapp P, Gibson ES, Dell鈥檃cqua ML, Hoffman PL (2010) Phosphorylation regulates removal of synaptic N-methyl-d-aspartate receptors after withdrawal from chronic ethanol exposure. J Pharmacol Exp Ther 332:720鈥?29View Article PubMed Central PubMed
  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 Miera E, Rudy B (1999) Molecular diversity of K+ channels. Ann N Y Acad Sci 868:233鈥?85View Article PubMed
  Colbert CM (2001) Back-propagating action potentials in pyramidal neurons: a putative signaling mechanism for the induction of Hebbian synaptic plasticity. Restor Neurol Neurosci 19:199鈥?11PubMed
  Covarrubias M, Bhattacharji A, De Santiago-Castillo JA, Dougherty K, Kaulin YA, Na-Phuket TR, Wang G (2008) The neuronal Kv4 channel complex. Neurochem Res 33:1558鈥?567View Article PubMed
  Deng P, Pang ZP, Lei Z, Shikano S, Xiong Q, Harvey BK, London B, Wang Y, Li M, Xu ZC (2011) Up-regulation of A-type potassium currents protects neurons against cerebral ischemia. J Cereb Blood Flow Metab 31:1823鈥?835View Article PubMed Central PubMed
  Dittmer A, Dittmer J (2006) Beta-actin is not a reliable loading control in Western blot analysis. Electrophoresis 27:2844鈥?845View Article PubMed
  Fontan-Lozano A, Suarez-Pereira I, Gonzalez-Forero D, Carrion AM (2011) The A-current modulates learning via NMDA receptors containing the NR2B subunit. PLoS One 6:e24915View Article PubMed Central PubMed
  Gould TJ (2010) Addiction and cognition. Addict Sci Clin Pract 5:4鈥?4PubMed Central PubMed
  Hendricson AW, Maldve RE, Salinas AG, Theile JW, Zhang TA, Diaz LM, Morrisett RA (2007) Aberrant synaptic activation of N-methyl-D-aspartate receptors underlies ethanol withdrawal hyperexcitability. J Pharmacol Exp Ther 321:60鈥?2View Article PubMed
  Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869鈥?75View Article PubMed
  Holmes A, Fitzgerald PJ, MacPherson KP, DeBrouse L, Colacicco G, Flynn SM, Masneuf S, Pleil KE, Li C, Marcinkiewcz CA, Kash TL, Gunduz-Cinar O, Camp M (2012) Chronic alcohol remodels prefrontal neurons and disrupts NMDAR-mediated fear extinction encoding. Nat Neurosci 15:1359鈥?361View Article PubMed Central PubMed
  Holopainen IE (2005) Organotypic hippocampal slice cultures: a model system to study basic cellular and molecular mechanisms of neuronal cell death, neuroprotection, and synaptic plasticity. Neurochem Res 30:1521鈥?528View Article PubMed
  Jeanes ZM, Buske TR, Morrisett RA (2011) In vivo chronic intermittent ethanol exposure reverses the polarity of synaptic plasticity in the nucleus accumbens shell. J Pharmacol Exp Ther 336:155鈥?64View Article PubMed Central PubMed
  Jerng HH, Pfaffinger PJ, Covarrubias M (2004) Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 27:343鈥?69View Article PubMed
  Jo A, Kim HK (2011) Up-regulation of dendritic Kv4.2 mRNA by activation of the NMDA receptor. Neurosci Lett 496:129鈥?34View Article PubMed
  Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M (2000) Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol 525(Pt 1):75鈥?1View Article PubMed Central PubMed
  Jung SC, Kim J, Hoffman DA (2008) Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons. Neuron 60:657鈥?71View Article PubMed Central PubMed
  Kash TL, Baucum AJ 2nd, Conrad KL, Colbran RJ, Winder DG (2009) Alcohol exposure alters NMDAR function in the bed nucleus of the stria terminalis. Neuropsychopharmacology 34:2420鈥?429View Article PubMed Central PubMed
  Kass RS, Tsien RW (1975) Multiple effects of calcium antagonists on plateau currents in cardiac Purkinje fibers. J Gen Physiol 66:169鈥?92View Article PubMed
  Kaufmann WA, Matsui K, Jeromin A, Nerbonne JM, Ferraguti F (2012) Kv4.2 potassium channels segregate to extrasynaptic domains and influence intrasynaptic NMDA receptor NR2B subunit expression. Brain Struct Funct
  Kerti K, Lorincz A, Nusser Z (2012) Unique somato-dendritic distribution pattern of Kv4.2 channels on hippocampal CA1 pyramidal cells. Eur J Neurosci 35:66鈥?5View Article PubMed Central PubMed
  Kim J, Wei DS, Hoffman DA (2005) Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 569:41鈥?7View Article PubMed Central PubMed
  Kroener S, Mulholland PJ, New NN, Gass JT, Becker HC, Chandler LJ (2012) Chronic alcohol exposure alters behavioral and synaptic plasticity of the rodent prefrontal cortex. PLoS One 7:e37541View Article PubMed Central PubMed
  Kunjilwar K, Qian Y, Pfaffinger PJ (2013) Functional stoichiometry underlying KChIP regulation of Kv4.2 functional expression. J Neurochem 126:462鈥?72View Article PubMed Central PubMed
  Lack AK, Diaz MR, Chappell A, DuBois DW, McCool BA (2007) Chronic ethanol and withdrawal differentially modulate pre- and postsynaptic function at glutamatergic synapses in rat basolateral amygdala. J Neurophysiol 98:3185鈥?196View Article PubMed Central PubMed
  Lilliehook C, Bozdagi O, Yao J, Gomez-Ramirez M, Zaidi NF, Wasco W, Gandy S, Santucci AC, Haroutunian V, Huntley GW, Buxbaum JD (2003) Altered Abeta formation and long-term potentiation in a calsenilin knock-out. J Neurosci 23:9097鈥?106PubMed
  Lindblad B, Olsson R (1976) Unusually high levels of blood alcohol? JAMA 236:1600鈥?602View Article PubMed
  Lockridge A, Yuan LL (2011) Spatial learning deficits in mice lacking A-type K(+) channel subunits. Hippocampus 21:1152鈥?156View Article PubMed
  Lovinger DM, Roberto M (2013) Synaptic effects induced by alcohol. Curr Top Behav Neurosci 13:31鈥?6View Article PubMed
  Lugo JN, Brewster AL, Spencer CM, Anderson AE (2012) Kv4.2 knockout mice have hippocampal-dependent learning and memory deficits. Learn Mem 19:182鈥?89View Article PubMed Central PubMed
  Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci: Off J Soc Neurosci 18:7613鈥?624
  Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417鈥?28View Article PubMed
  McGuier NS, Padula AE, Lopez MF, Woodward JJ, Mulholland PJ (2014) Withdrawal from chronic intermittent alcohol exposure increases dendritic spine density in the lateral orbitofrontal cortex of mice. Alcohol
  Menegola M, Trimmer JS (2006) Unanticipated region- and cell-specific downregulation of individual KChIP auxiliary subunit isotypes in Kv4.2 knock-out mouse brain. J Neurosci 26:12137鈥?2142View Article PubMed
  Mitra NK, Mukherjee A (2001) Effect of ethanol on dendrites of hippocampal neurons. J Anat Soc India 50:28鈥?0
  Mulholland PJ, Chandler LJ (2007) The thorny side of addiction: adaptive plasticity and dendritic spines. Sci World J 7:9鈥?1View Article
  Mulholland PJ, Becker HC, Woodward JJ, Chandler LJ (2011) Small conductance calcium-activated potassium type 2 channels regulate alcohol-associated plasticity of glutamatergic synapses. Biol Psychiatry 69:625鈥?32View Article PubMed Central PubMed
  Nelson TE, Ur CL, Gruol DL (2005) Chronic intermittent ethanol exposure enhances NMDA-receptor-mediated synaptic responses and NMDA receptor expression in hippocampal CA1 region. Brain Res 1048:69鈥?9View Article PubMed
  Nerbonne JM, Gerber BR, Norris A, Burkhalter A (2008) Electrical remodelling maintains firing properties in cortical pyramidal neurons lacking KCND2-encoded A-type K+ currents. J Physiol 586:1565鈥?579View Article PubMed Central PubMed
  Obara I, Bell RL, Goulding SP, Reyes CM, Larson LA, Ary AW, Truitt WA, Szumlinski KK (2009) Differential effects of chronic ethanol consumption and withdrawal on homer/glutamate receptor expression in subregions of the accumbens and amygdala of P rats. Alcohol Clin Exp Res 33:1924鈥?934View Article PubMed Central PubMed
  Qiang M, Denny AD, Ticku MK (2007) Chronic intermittent ethanol treatment selectively alters N-methyl-D-aspartate receptor subunit surface expression in cultured cortical neurons. Mol Pharmacol 72:95鈥?02View Article PubMed
  Sabeti J (2011) Ethanol exposure in early adolescence inhibits intrinsic neuronal plasticity via sigma-1 receptor activation in hippocampal CA1 neurons. Alcohol Clin Exp Res 35:885鈥?04View Article PubMed Central PubMed
  Sabeti J, Gruol DL (2008) Emergence of NMDAR-independent long-term potentiation at hippocampal CA1 synapses following early adolescent exposure to chronic intermittent ethanol: role for sigma-receptors. Hippocampus 18:148鈥?68View Article PubMed
  Spiga S, Lintas A, Diana M (2008) Addiction and cognitive functions. Ann N Y Acad Sci 1139:299鈥?06View Article PubMed
  Teplin LA, Abram KM, Michaels SK (1989) Blood alcohol level among emergency room patients: a multivariate analysis. J Stud Alcohol 50:441鈥?47View Article PubMed
  Truchet B, Manrique C, Sreng L, Chaillan FA, Roman FS, Mourre C (2012) Kv4 potassium channels modulate hippocampal EPSP-spike potentiation and spatial memory in rats. Learn Mem 19:282鈥?93View Article PubMed
  Urso T, Gavaler JS, Van Thiel DH (1981) Blood ethanol levels in sober alcohol users seen in an emergency room. Life Sci 28:1053鈥?056View Article PubMed
  Watanabe S, Hoffman DA, Migliore M, Johnston D (2002) Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 99:8366鈥?371View Article PubMed Central PubMed
  Wu YW, Grebenyuk S, McHugh TJ, Rusakov DA, Semyanov A (2012) Backpropagating action potentials enable detection of extrasynaptic glutamate by NMDA receptors. Cell Rep 1:495鈥?05View Article PubMed Central PubMed
  Yuan LL, Adams JP, Swank M, Sweatt JD, Johnston D (2002) Protein kinase modulation of dendritic K+ channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22:4860鈥?868PubMed
  Zhang Y, Su P, Liang P, Liu T, Liu X, Liu XY, Zhang B, Han T, Zhu YB, Yin DM, Li J, Zhou Z, Wang KW, Wang Y (2010) The DREAM protein negatively regulates the NMDA receptor through interaction with the NR1 subunit. J Neurosci: Off J Soc Neurosci 30:7575鈥?586View Article
  Zhou FC, Anthony B, Dunn KW, Lindquist WB, Xu ZC, Deng P (2007) Chronic alcohol drinking alters neuronal dendritic spines in the brain reward center nucleus accumbens. Brain Res 1134:148鈥?61View Article PubMed Central PubMed
  
• 作者单位：Patrick J. Mulholland (1)
  Kathryn B. Spencer (1)
  Wei Hu (2)
  Sven Kroener (2)
  L. Judson Chandler (1)
  
  1. Department of Neuroscience, Medical University of South Carolina, Charleston Alcohol Research Center, 67 President Street, IOP 462 North, Charleston, SC, 29425, USA
  2. School of Behavioral and Brain Sciences, The University of Texas at Dallas, Dallas, TX, 75080, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Pharmacology and Toxicology
  Psychiatry
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-2072

文摘

Rationale Chronic alcohol-induced cognitive impairments and maladaptive plasticity of glutamatergic synapses are well-documented. However, it is unknown if prolonged alcohol exposure affects dendritic signaling that may underlie hippocampal dysfunction in alcoholics. Back-propagation of action potentials (bAPs) into apical dendrites of hippocampal neurons provides distance-dependent signals that modulate dendritic and synaptic plasticity. The amplitude of bAPs decreases with distance from the soma that is thought to reflect an increase in the density of Kv4.2 channels toward distal dendrites. Objective The aim of this study was to quantify changes in hippocampal Kv4.2 channel function and expression using electrophysiology, Ca2+ imaging, and western blot analyses in a well-characterized in vitro model of chronic alcohol exposure. Results Chronic alcohol exposure significantly decreased expression of Kv4.2 channels and KChIP3 in hippocampus. This reduction was associated with an attenuation of macroscopic A-type K+ currents in CA1 neurons. Chronic alcohol exposure increased bAP-evoked Ca2+ transients in the distal apical dendrites of CA1 pyramidal neurons. The enhanced bAP-evoked Ca2+ transients induced by chronic alcohol exposure were not related to synaptic targeting of N-methyl-d-aspartate (NMDA) receptors or morphological adaptations in apical dendritic arborization. Conclusions These data suggest that chronic alcohol-induced decreases in Kv4.2 channel function possibly mediated by a downregulation of KChIP3 drive the elevated bAP-associated Ca2+ transients in distal apical dendrites. Alcohol-induced enhancement of bAPs may affect metaplasticity and signal integration in apical dendrites of hippocampal neurons leading to alterations in hippocampal function.