Cell-type specific channelopathies in the prefrontal cortex of the fmr1-/y mouse model of fragile X syndrome

eNeuro

Volumn 2, Issue 6, 2015, Pages

  Kalmbach, Brian E ^a   Johnston, Daniel ^a   Brager, Darrin H ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Dendrite; Excitability; Fragile X syndrome; Ion channel; Prefrontal cortex

Indexed keywords

FMR1 PROTEIN, MOUSE; FRAGILE X MENTAL RETARDATION PROTEIN;

ANIMAL; CHANNELOPATHY; CYTOLOGY; DISEASE MODEL; FRAGILE X SYNDROME; GENETICS; HIPPOCAMPUS; KNOCKOUT MOUSE; MALE; METABOLISM; NERVE CELL; PREFRONTAL CORTEX;

ANIMALS; CHANNELOPATHIES; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; HIPPOCAMPUS; MALE; MICE, KNOCKOUT; NEURONS; PREFRONTAL CORTEX;

EID: 84989930071     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0114-15.2015     Document Type: Article

References (87)

1. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, Rhodes KJ (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403:553–556. CrossRef Medline
2. Antar LN, Afroz R, Dictenberg JB, Carroll RC, Bassell GJ (2004) Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J Neurosci 24:2648–2655. CrossRef Medline
3. Avesar D, Gulledge AT (2012) Selective serotonergic excitation of callosal projection neurons. Front Neural Circuits 6. CrossRef Medline
4. Bechara EG, Didiot MC, Melko M, Davidovic L, Bensaid M, Martin P, Castets M, Pognonec P, Khandjian EW, Moine H, Bardoni B (2009) A novel function for fragile X mental retardation protein in translational activation. PLoS Biol 7:e16 CrossRef Medline
5. Bekkers JM (2000) Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J Physiol 525:611–620. Medline
6. Bekkers JM, Delaney AJ (2001) Modulation of excitability by alpha-dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons. J Neurosci 21:6553–6560. Medline
7. Bernard C, Anderson A, Becker A, Poolos NP, Beck H, Johnston D (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305:532–535. CrossRef Medline
8. Bhakar AL, Dölen G, Bear MF (2012) The pathophysiology of fragile X (and what it teaches us about synapses). Annu Rev Neurosci 35:417–443. CrossRef Medline
9. Brager DH, Akhavan AR, Johnston D (2012) Impaired dendritic expression and plasticity of h-channels in the fmr1(-/y) mouse model of fragile X syndrome. Cell Rep 1:225–233. CrossRef Medline
10. h in hippocampal CA1 pyramidal neurons. J Neurosci 27:13926–13937. CrossRef Medline
11. Brager DH, Johnston D (2014) Channelopathies and dendritic dysfunction in fragile X syndrome. Brain Res Bull 103:11–17. CrossRef Medline
12. Brown MR, Kronengold J, Gazula V-R, Chen Y, Strumbos JG, Sig-worth FJ, Navaratnam D, Kaczmarek LK (2010) Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nat Neurosci 13:819–821. CrossRef Medline
13. Bureau I, Shepherd GMG, Svoboda K (2008) Circuit and plasticity defects in the developing somatosensory cortex of Fmr1 knockout mice. J Neurosci 28:5178–5188. CrossRef
14. Carr DB, Andrews GD, Glen WB, Lavin A (2007) 2-Noradrenergic receptors activation enhances excitability and synaptic integration in rat prefrontal cortex pyramidal neurons via inhibition of HCN currents. J Physiol 584:437–450. CrossRef Medline
15. Carrasquillo Y, Burkhalter A, Nerbonne JM (2012) A-type K+ channels encoded by Kv4.2, Kv4.3, and Kv1.4 differentially regulate intrinsic excitability of cortical pyramidal neurons. J Physiol 590: 3877–3890. CrossRef Medline
16. 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–H391. Medline
17. Castle NA, Fadous S, Logothetis DE, Wang GK (1994) Aminopyridine block of Kv1.1 potassium channels expressed in mammalian cells and Xenopus oocytes. Mol Pharmacol 45:1242–1252. Medline
18. Christophe E, Doerflinger N, Lavery DJ, Molnár Z, Charpak S, Audi-nat E (2005) Two populations of layer V pyramidal cells of the mouse neocortex: development and sensitivity to anesthetics. J Neurophysiol 94:3357–3367. CrossRef Medline
19. 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 868:233–285. Medline
20. Colbert CM, Magee JC, Hoffman DA, Johnston D (1997) Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J Neurosci 17:6512–6521. Medline
21. Contractor A, Klyachko VA, Portera-Cailliau C (2015) Altered neuronal and circuit excitability in fragile X syndrome. Neuron 87:699– 715. CrossRef Medline
22. Cook EP, Guest JA, Liang Y, Masse NY, Colbert CM (2007) Dendrite-to-soma input/output function of continuous time-varying signals in hippocampal CA1 pyramidal neurons. J Neurophysiol 98:2943– 2955. CrossRef Medline
23. Darnell JC, Van Driesche SJ, Zhang C, Hung KYS, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, Licatalosi DD, Richter JD, Darnell RB (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146:247–261. Cross-Ref Medline
24. Dembrow N, Johnston D (2014) Subcircuit-specific neuromodulation in the prefrontal cortex. Front Neural Circuits 8:54. CrossRef Med-line
25. Dembrow NC, Chitwood RA, Johnston D (2010) Projection-specific neuromodulation of medial prefrontal cortex neurons. J Neurosci 30:16922–16937. CrossRef Medline
26. Dembrow NC, Zemelman BV, Johnston D (2015) Temporal dynamics of L5 dendrites in medial prefrontal cortex regulate integration versus coincidence detection of afferent inputs. J Neurosci 35: 4501–4514. CrossRef Medline
27. Deng P-Y, Rotman Z, Blundon JA, Cho Y, Cui J, Cavalli V, Zakharenko SS, Klyachko VA (2013) FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron 77:696–711. CrossRef
28. Dictenberg JB, Swanger SA, Antar LN, Singer RH, Bassell GJ (2008) A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Developmental Cell 14:926–939. CrossRef Medline
29. Dougherty KA, Nicholson DA, Diaz L, Buss EW, Neuman KM, Chetkovich DM, Johnston D (2013) Differential expression of HCN subunits alters voltage-dependent gating of h-channels in CA1 pyramidal neurons from dorsal and ventral hippocampus. J Neurophysiol 109:1940–1953. CrossRef Medline
30. Fähling M, Mrowka R, Steege A, Kirschner KM, Benko E, Förstera B, Persson PB, Thiele BJ, Meier JC, Scholz H (2009) Translational regulation of the human Achaete-scute homologue-1 by fragile X mental retardation protein. Journal of Biological Chemistry 284: 4255–4266. CrossRef Medline
31. Fan Y, Fricker D, Brager DH, Chen X, Lu H-C, Chitwood RA, Johnston D (2005) Activity-dependent decrease of excitability in rat hippocampal neurons through increases in Ih. Nat Neurosci 8:1542–1551. CrossRef
32. Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126–135. CrossRef Medline
33. Gasparini S, Losonczy A, Chen X, Johnston D, Magee JC (2007) Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons. J Physiol 580: 787–800. CrossRef Medline
34. Gee S, Ellwood I, Patel T, Luongo F, Deisseroth K, Sohal VS (2012) Synaptic activity unmasks dopamine D2 receptor modulation of a specific class of layer V pyramidal neurons in prefrontal cortex. J Neurosci 32:4959–4971. CrossRef Medline
35. Gibson JR, Bartley AF, Hays SA, Huber KM (2008) Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J Neurophysiol 100:2615–2626. CrossRef Medline
36. Gonçalves JT, Anstey JE, Golshani P, Portera-Cailliau C (2013) Circuit level defects in the developing neocortex of fragile X mice. Nat Neurosci 16:903–909. CrossRef Medline
37. Gross C, Yao X, Pong DL, Jeromin A, Bassell GJ (2011) Fragile X mental retardation protein regulates protein expression and mRNA translation of the potassium channel Kv4.2. J Neurosci 31:5693– 5698. CrossRef Medline
38. Hagerman RJ, Ono MY, Hagerman PJ (2005) Recent advances in fragile X: a model for autism and neurodegeneration. Curr Opin Psychiatry 18:490–496. CrossRef Medline
39. Harris-Warrick RM, Coniglio LM, Levini RM, Gueron S, Gucken-heimer J (1995) Dopamine modulation of two subthreshold currents produces phase shifts in activity of an identified motoneuron. J Neurophysiol 74:1404–1420. Medline
40. Harvey AL (2001) Twenty years of dendrotoxins. Toxicon 39:15–26. Medline
41. Hattox AM, Nelson SB (2007) Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol 98:3330–3340. CrossRef Medline
42. Hays SA, Huber KM, Gibson JR (2011) Altered neocortical rhythmic activity states in Fmr1 KO mice are due to enhanced mGluR5 signaling and involve changes in excitatory circuitry. J Neurosci 31:14223–14234. CrossRef Medline
43. Higgs MH, Spain WJ (2011) Kv1 channels control spike threshold dynamics and spike timing in cortical pyramidal neurones. J Physiol 589:5125–5142. CrossRef Medline
44. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544. Medline
45. Hoffman DA, Johnston D (1999) Neuromodulation of dendritic action potentials. J Neurophysiol 81:408–411. Medline
46. Hutcheon B, yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216–222. Medline
47. Jerng HH, Pfaffinger PJ, Covarrubias M (2004) Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 27:343–369. CrossRef Medline
48. Johnston D, Narayanan R (2008) Active dendrites: colorful wings of the mysterious butterflies. Trends Neurosci 31:309–316. CrossRef Medline
49. Kalmbach BE, Chitwood RA, Dembrow NC, Johnston D (2013) Dendritic generation of mGluR-mediated slow afterdepolarization in layer 5 neurons of prefrontal cortex. J Neurosci 33:13518–13532. CrossRef Medline
50. Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin Transports RNA. Neuron 43:513–525. CrossRef Medline
51. Kim J, Nadal MS, Clemens AM, Baron M, Jung S-C, Misumi Y, Rudy B, Hoffman DA (2008) Kv4 accessory protein DPPX (DPP6) is a critical regulator of membrane excitability in hippocampal CA1 pyramidal neurons. J Neurophysiol 100:1835–1847. CrossRef Medline
52. 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 Physi-oly 569:41–57. CrossRef Medline
53. Kole MHP, Hallermann S, Stuart GJ (2006) Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26:1677–1687. CrossRef Medline
54. Kole MHP, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633–647. CrossRef Medline
55. Korngreen A, Sakmann B (2000) Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J Physiol 525 Pt 3:621–639 Medline
56. Krueger DD, Osterweil EK, Chen SP, Tye LD, Bear MF (2011) Cognitive dysfunction and prefrontal synaptic abnormalities in a mouse model of fragile X syndrome. Proc Nat Acad Sci 108:2587– 2592. CrossRef Medline
57. Lee AT, Gee SM, Vogt D, Patel T, Rubenstein JL, Sohal VS (2014) Pyramidal neurons in prefrontal cortex receive subtype-specific forms of excitation and inhibition. Neuron 81:61–68. CrossRef Medline
58. Lee HY, Ge W-P, Huang W, He Y, Wang GX, Rowson-Baldwin A, Smith SJ, Jan YN, Jan LY (2011) Bidirectional regulation of dendritic voltage-gated potassium channels by the fragile X mental retardation protein. Neuron 72:630–642. CrossRef Medline
59. Li Z, Zhang Y, Ku L, Wilkinson KD, Warren ST, Feng Y (2001) The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res 29:2276–2283. Medline
60. London M, Häusser M (2005) Dendritic Computation. Annu Rev Neurosci 28:503–532. CrossRef Medline
61. Losonczy A, Makara JK, Magee JC (2008) Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452: 436–441. CrossRef Medline
62. Lörincz A, Notomi T, Tamás G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185–1193. CrossRef Medline
63. Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1:181–190. CrossRef Medline
64. Menon V, Leroux J, White CD, Reiss AL (2004) Frontostriatal deficits in fragile X syndrome: relation to FMR1 gene expression. Proc Nat Acad Sci 101:3615–3620. CrossRef Medline
65. Meredith RM, Holmgren CD, Weidum M, Burnashev N, Mansvelder HD (2007) Increased threshold for spike-timing-dependent plasticity is caused by unreliable calcium signaling in mice lacking fragile X gene Fmr1. Neuron 54:627–638. CrossRef Medline
66. Molnár Z, Cheung AFP (2006) Towards the classification of subpopulations of layer V pyramidal projection neurons. Neurosci Res 55:105–115. CrossRef Medline
67. Molyneaux BJ, Arlotta P, Menezes JRL, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427–437. CrossRef Medline
68. Morishima M, Morita K, Kubota Y, Kawaguchi Y (2011) Highly differentiated projection-specific cortical subnetworks. J Neurosci 31: 10380–10391. CrossRef Medline
69. Narayanan R, Johnston D (2007) Long-Term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron 56:1061–1075. CrossRef Medline
70. Otsuka T, Kawaguchi Y (2011) Cell diversity and connection specificity between callosal projection neurons in the frontal cortex. J Neurosci 31:3862–3870 CrossRef Medline
71. Patel AB, Hays SA, Bureau I, Huber KM, Gibson JR (2013) A target cell-specific role for presynaptic Fmr1 in regulating glutamate release onto neocortical fast-spiking inhibitory neurons. J Neurosci 33:2593–2604. CrossRef Medline
72. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453–480. CrossRef Medline
73. Routh BN, Johnston D, Brager DH (2013) Loss of functional A-type potassium channels in the dendrites of CA1 pyramidal neurons from a mouse model of fragile X syndrome. J Neurosci 33:19442– 19450. CrossRef Medline
74. Russell SN, Publicover NG, Hart PJ, Carl A, Hume JR, Sanders KM, Horowitz B (1994) Block by 4-aminopyridine of a Kv1.2 delayed rectifier K+ current expressed in Xenopus oocytes. J Physiol 481:571–584. CrossRef
75. Santoro MR, Bray SM, Warren ST (2012) Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu Rev Pathol 7:219–245. CrossRef Medline
76. Sheets PL, Suter BA, Kiritani T, Chan CS, Surmeier DJ, Shepherd GMG (2011) Corticospinal-specific HCN expression in mouse motor cortex: Ih-dependent synaptic integration as a candidate microcircuit mechanism involved in motor control. J Neurophysiol 106:2216–2231. CrossRef
77. Shepherd GMG (2013) Corticostriatal connectivity and its role in disease. Nat Rev Neurosci 14:278–291. CrossRef
78. Shin M, Brager D, Jaramillo TC, Johnston D, Chetkovich DM (2008) Mislocalization of h channel subunits underlies h channelopathy in temporal lobe epilepsy. Neurobiol Dis 32:26–36. CrossRef Medline
79. Stephens GJ, Garratt JC, Robertson B, Owen DG (1994) On the mechanism of 4-aminopyridine action on the cloned mouse brain potassium channel mKv1.1. J Physiol 477:187–196. CrossRef
80. Strumbos JG, Brown MR, Kronengold J, Polley DB, Kaczmarek LK (2010) Fragile X mental retardation protein is required for rapid experience-dependent regulation of the potassium channel Kv3.1b. J Neurosci 30:10263–10271. CrossRef Medline
81. Testa-Silva G, Loebel A, Giugliano M, de Kock CPJ, Mansvelder HD, Meredith RM (2012) Hyperconnectivity and slow synapses during early development of medial prefrontal cortex in a mouse model for mental retardation and autism. Cerebral Cortex 22:1333–1342. CrossRef
82. Tyzio R, Nardou R, Ferrari DC, Tsintsadze T, Shahrokhi A, Eftekhari S, Khalilov I, Tsintsadze V, Brouchoud C, Chazal G, Lemonnier E, Lozovaya N, Burnashev N, Ben-Ari Y (2014) Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343:675–679. CrossRef Medline
83. Ulrich D (2002) Dendritic resonance in rat neocortical pyramidal cells. J Neurophysiol 87:2753–2759. Medline
84. Vaidya SP, Johnston D (2013) Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons. Nat Neurosci 16:1812–1820. CrossRef Medline
85. Wang JM, Koldewyn K, Hashimoto R-I, Schneider A, Le L, Tassone F, Cheung K, Hagerman P, Hessl D, Rivera SM (2012) Male carriers of the FMR1 premutation show altered hippocampal-prefrontal function during memory encoding. Front Hum Neurosci 6. Cross-Ref
86. Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, Reis S, Ben Oostra, Bagni C (2003) The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112:317–327. Medline
87. Zhang Y, Bonnan A, Bony G, Ferezou I, Pietropaolo S, Ginger M, Sans N, Rossier J, Oostra B, LeMasson G, Frick A (2014) Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1. Nat Neurosci 1–12.