Channelopathies and dendritic dysfunction in fragile X syndrome

Brain Research Bulletin

Volumn 103, Issue , 2014, Pages 11-17

  Brager, Darrin H ^a   Johnston, Daniel ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Dendrites; Fmr1; FMRP; Integration; Voltage gated ion channels

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; ION CHANNEL; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

CELL FUNCTION; CHANNELOPATHY; DENDRITE; FRAGILE X SYNDROME; HUMAN; NERVE CELL PLASTICITY; NEUROMODULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SYNAPTIC TRANSMISSION; ANIMAL; FEMALE; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CHANNELOPATHIES; DENDRITES; FEMALE; FRAGILE X SYNDROME; HUMANS; MALE; NEURONAL PLASTICITY;

EID: 84898428838     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2014.01.002     Document Type: Review

References (107)

1. Aizenman C.D., Linden D.J. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat. Neurosci. 2000, 3:109-111.
2. Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 1994, 78:23-33. The Dutch-Belgian Fragile X Consortium.
3. Antar L.N., Afroz R., Dictenberg J.B., Carroll R.C., Bassell G.J. Metabotropic glutamate receptor activation regulates fragile X mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J. Neurosci. 2004, 24:2648-2655.
4. Bechara E.G., Didiot M.C., Melko M., Davidovic L., Bensaid M., Martin P., Castets M., Pognonec P., Khandjian E.W., Moine H., Bardoni B. A novel function for fragile X mental retardation protein in translational activation. PLoS Biol. 2009, 7:e16.
5. Beck H., Yaari Y. Plasticity of intrinsic neuronal properties in CNS disorders. Nat. Rev. Neurosci. 2008, 9:357-369.
6. Berger T., Senn W., Lüscher H.-R. Hyperpolarization-activated current Ih disconnects somatic and dendritic spike initiation zones in layer V pyramidal neurons. J. Neurophysiol. 2003, 90:2428-2437.
7. Bernard C., Johnston D. Distance-dependent modifiable threshold for action potential back-propagation in hippocampal dendrites. J. Neurophysiol. 2003, 90:1807-1816.
8. Bi G.Q., Poo M.M. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 1998, 18:10464-10472.
9. Bittner K.C., Andrasfalvy B.K., Magee J.C. Ion channel gradients in the apical tuft region of CA1 pyramidal neurons. PLoS ONE 2012, 7:e46652.
10. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
11. Brager D.H., Akhavan A.R., Johnston D. Impaired dendritic expression and plasticity of h-channels in the fmr1(-/y) mouse model of fragile X syndrome. Cell Rep. 2012, 1:225-233.
12. Brenner R., Jegla T.J., Wickenden A., Liu Y., Aldrich R.W. Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta subunits, hKCNMB3 and hKCNMB4. J. Biol. Chem. 2000, 275:6453-6461.
13. Brown M.R., Kronengold J., Gazula V.-R., Chen Y., Strumbos J.G., Sigworth F.J., Navaratnam D., Kaczmarek L.K. Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nat. Neurosci. 2010, 13:819-821.
14. Brown V., et al. Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 2001, 107:477-487.
15. Campanac E., Daoudal G., Ankri N., Debanne D. Downregulation of dendritic I(h) in CA1 pyramidal neurons after LTP. J. Neurosci. 2008, 28:8635-8643.
16. Chen L., Yun S.W., Seto J., Liu W., Toth M. The fragile X mental retardation protein binds and regulates a novel class of mRNAs containing U rich target sequences. Neuroscience 2003, 120:1005-1017.
17. + current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurosci. 2006, 26:12143-12151.
18. + influx. J. Neurophysiol. 1995, 73:2553-2557.
19. + channel densities in the soma and axon initial segment of subicular pyramidal neurons. J. Neurosci. 1996, 16:6676-6686.
20. Comery T.A., Harris J.B., Willems P.J., Oostra B.A., Irwin S.A., Weiler I.J., Greenough W.T. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. USA 1997, 94:5401-5404.
21. Darnell J.C., Jensen K.B., Jin P., Brown V., Warren S.T., Darnell R.B. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 2001, 107:489-499.
22. Darnell J.C., Van Driesche S.J., Zhang C., Hung K.Y.S., Mele A., Fraser C.E., Stone E.F., Chen C., Fak J.J., Chi S.W., Licatalosi D.D., Richter J.D., Darnell R.B. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 2011, 146:247-261.
23. Deng P.-Y., Rotman Z., Blundon J.A., Cho Y., Cui J., Cavalli V., Zakharenko S.S., Klyachko V.A. FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron 2013, 77:696-711.
24. Deng P.-Y., Sojka D., Klyachko V.A. Abnormal presynaptic short-term plasticity and information processing in a mouse model of fragile X syndrome. J. Neurosci. 2011, 31:10971-10982.
25. Desai N.S., Rutherford L.C., Turrigiano G.G. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat. Neurosci. 1999, 2:515-520.
26. Dictenberg J.B., Swanger S.A., Antar L.N., Singer R.H., Bassell G.J. A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell 2008, 14:926-939.
27. DiFrancesco D. Pacemaker mechanisms in cardiac tissue. Ann. Rev. Physiol. 1993, 55:455-472.
28. + channels: a new family of large-conductance ion channels. Trends Neurosci. 1994, 17:155-160.
29. Fan Y., Fricker D., Brager D.H., Chen X., Lu H.-C., Chitwood R.A., Johnston D. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat. Neurosci. 2005, 8:1542-1551.
30. Fähling M., Mrowka R., Steege A., Kirschner K.M., Benko E., Förstera B., Persson P.B., Thiele B.J., Meier J.C., Scholz H. Translational regulation of the human achaete-scute homologue-1 by fragile X mental retardation protein. J. Biol. Chem. 2009, 284:4255-4266.
31. Feng Y., Absher D., Eberhart D.E., Brown V., Malter H.E., Warren S.T. FMRP associates with polyribosomes as an mRNP, and the I304 N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1997, 1:109-118.
32. Frick A., Johnston D. Plasticity of dendritic excitability. J. Neurobiol. 2005, 64:100-115.
33. Frick A., Magee J., Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci. 2004, 7:126-135.
34. Frick A., Magee J., Koester H.J., Migliore M., Johnston D. Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons. J. Neurosci. 2003, 23:3243-3250.
35. V3.1 potassium channel in high-frequency firing neurons. J. Neurobiol. 1998, 37:69-79.
36. Gasparini S., Magee J.C. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J. Neurosci. 2006, 26:2088-2100.
37. Gibson J.R., Bartley A.F., Hays S.A., Huber K.M. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol. 2008, 100:2615-2626.
38. Golding N.L., Kath W.L., Spruston N. Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J. Neurophysiol. 2001, 86:2998-3010.
39. Golding N.L., Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 1998, 21:1189-1200.
40. Golowasch J., Abbott L.F., Marder E. Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J. Neurosci. 1999, 19:RC33.
41. Gonçalves J.T., Anstey J.E., Golshani P., Portera-Cailliau C. Circuit level defects in the developing neocortex of fragile X mice. Nat. Neurosci. 2013.
42. V4.2. J. Neurosci. 2011, 31:5693-5698.
43. Grover L.M., Teyler T.J. Two components of long-term potentiation induced by different patterns of afferent activation. Nature 1990, 347:477-479.
44. Gulledge A.T., Kampa B.M., Stuart G.J. Synaptic integration in dendritic trees. J. Neurobiol. 2005, 64:75-90.
45. Harnett M.T., Xu N.-L., Magee J.C., Williams S.R. Potassium channels control the interaction between active dendritic integration compartments in layer 5 cortical pyramidal neurons. Neuron 2013, 79:516-529.
46. Hays S.A., Huber K.M., Gibson J.R. Altered neocortical rhythmic activity states in Fmr1 KO mice are due to enhanced mGluR5 signaling and involve changes in excitatory circuitry. J. Neurosci. 2011, 31:14223-14234.
47. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 1997, 387:869-875.
48. Hou L., Antion M.D., Hu D., Spencer C.M., Paylor R., Klann E. Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 2006, 51:441-454.
49. Huber K.M., Gallagher S.M., Warren S.T., Bear M.F. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA 2002, 99:7746-7750.
50. Jaffe D.B., Johnston D., Lasser-Ross N., Lisman J.E., Miyakawa H., Ross W.N. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature 1992, 357:244-246.
51. Johnston D., Christie B.R., Frick A., Gray R., Hoffman D.A., Schexnayder L.K., Watanabe S., Yuan L.-L. Active dendrites, potassium channels and synaptic plasticity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:667-674.
52. Kanai Y., Dohmae N., Hirokawa N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 2004, 43:513-525.
53. Kapur A., Yeckel M.F., Gray R., Johnston D. L-type calcium channels are required for one form of hippocampal mossy fiber LTP. J. Neurophysiol. 1998, 79:2181-2190.
54. V4.2 channels on hippocampal CA1 pyramidal cells. Eur. J. Neurosci. 2012, 35:66-75.
55. V4.2 in hippocampal neurons. Neuron 2007, 54:933-947.
56. Kole M.H.P., Hallermann S., Stuart G.J. Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J. Neurosci. 2006, 26:1677-1687.
57. Larkum M.E., Kaiser K.M., Sakmann B. Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl. Acad. Sci. USA 1999, 96:14600-14604.
58. Larkum M.E., Waters J., Sakmann B., Helmchen F. Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. J. Neurosci. 2007, 27:8999-9008.
59. Larkum M.E., Zhu J.J. Signaling of layer 1 and whisker-evoked Ca2+ and Na+ action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J. Neurosci. 2002, 22:6991-7005.
60. Lauterborn J.C., Rex C.S., Kramár E., Chen L.Y., Pandyarajan V., Lynch G., Gall C.M. Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J. Neurosci. 2007, 27:10685-10694.
61. Lee H.Y., Ge W.-P., Huang W., He Y., Wang G.X., Rowson-Baldwin A., Smith S.J., Jan Y.N., Jan L.Y. Bidirectional regulation of dendritic voltage-gated potassium channels by the fragile X mental retardation protein. Neuron 2011, 72:630-642.
62. Li Z., Zhang Y., Ku L., Wilkinson K.D., Warren S.T., Feng Y. The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 2001, 29:2276-2283.
63. Losonczy A., Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 2006, 50:291-307.
64. Losonczy A., Makara J.K., Magee J.C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 2008, 452:436-441.
65. Lörincz A., Notomi T., Tamás G., Shigemoto R., Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat. Neurosci. 2002, 5:1185-1193.
66. Magee J.C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 1998, 18:7613-7624.
67. Magee J.C. Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat. Neurosci. 1999, 2:508-514.
68. Magee J.C., Johnston D. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J. Physiol. (Lond.) 1995, 487(Pt 1):67-90.
69. Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997, 275:209-213.
70. Magee J.C., Johnston D. Plasticity of dendritic function. Curr. Opin. Neurobiol. 2005, 15:334-342.
71. Makara J.K., Losonczy A., Wen Q., Magee J.C. Experience-dependent compartmentalized dendritic plasticity in rat hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2009, 12:1485-1487.
72. Martina M., Vida I., Jonas P. Distal initiation and active propagation of action potentials in interneuron dendrites. Science 2000, 287:295-300.
73. Meredith R.M., Holmgren C.D., Weidum M., Burnashev N., Mansvelder H.D. Increased threshold for spike-timing-dependent plasticity is caused by unreliable calcium signaling in mice lacking fragile X gene FMR1. Neuron 2007, 54:627-638.
74. + channel Slo1 in axons and nerve terminals of mammalian brain and cultured neurons. J. Comp. Neurol. 2006, 496:289-302.
75. Narayanan R., Johnston D. Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron 2007, 56:1061-1075.
76. Nimchinsky E.A., Oberlander A.M., Svoboda K. Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci. 2001, 21:5139-5146.
77. Pape H.C. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu. Rev. Physiol. 1996, 58:299-327.
78. Paradee W., Melikian H.E., Rasmussen D.L., Kenneson A., Conn P.J., Warren S.T. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 1999, 94:185-192.
79. Pfeiffer B.E., Zang T., Wilkerson J.R., Taniguchi M., Maksimova M.A., Smith L.N., Cowan C.W., Huber K.M. Fragile X mental retardation protein is required for synapse elimination by the activity-dependent transcription factor MEF2. Neuron 2010, 66:191-197.
80. Polsky A., Mel B.W., Schiller J. Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 2004, 7:621-627.
81. Ramakers G.M.J., 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 2002, 99:10144-10149.
82. Routh B.N., Johnston D., Brager D.H. Loss of functional A-type potassium channels in the dendrites of CA1 pyramidal neurons from a mouse model of fragile X syndrome. J. Neurosci. 2013, 33:19442-19450.
83. + channels designed for high-frequency repetitive firing. Trends Neurosci. 2001, 24:517-526.
84. Sailer C.A., Kaufmann W.A., Kogler M., Chen L., Sausbier U., Ottersen O.P., Ruth P., Shipston M.J., Knaus H.-G. Immunolocalization of BK channels in hippocampal pyramidal neurons. Eur. J. Neurosci. 2006, 24:442-454.
85. Schiller J., Major G., Koester H.J., Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 2000, 404:285-289.
86. Siegel M., Marder E., Abbott L.F. Activity-dependent current distributions in model neurons. Proc. Natl. Acad. Sci. USA 1994, 91:11308-11312.
87. Spruston N., Schiller Y., Stuart G., Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 1995, 297-300.
88. Steward O., Levy W.B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 1982, 2:284-291.
89. Steward O., Schuman E.M. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 2001, 24:299-325.
90. V3.1b. J. Neurosci. 2010, 30:10263-10271.
91. V3.1b potassium channels in the adult rat. Neuroscience 2010, 167:567-572.
92. Stuart G., Häusser M. Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 1994, 13:703-712.
93. Stuart G., Spruston N., Sakmann B., Häusser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 1997, 20:125-131.
94. Stuart G.J., Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 1994, 367:69-72.
95. Turrigiano G., Abbott L.F., Marder E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science 1994, 264:974-977.
96. Turrigiano G.G., Nelson S.B. Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 2000, 10:358-364.
97. V3.1 potassium channel to high-frequency firing in mouse auditory neurones. J. Physiol. (Lond.) 1998, 509(Pt 1):183-194.
98. Wang S.S., Denk W., Häusser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 2000, 3:1266-1273.
99. Wang Z., Xu N.-L., Wu C.-P., Duan S., Poo M.-M. Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 2003, 37:463-472.
100. + channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 2002, 99:8366-8371.
101. Weiler I.J., Irwin S.A., Klintsova A.Y., Spencer C.M., Brazelton A.D., Miyashiro K., Comery T.A., Patel B., Eberwine J., Greenough W.T. Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc. Natl. Acad. Sci. USA 1997, 94:5395-5400.
102. Xu J., Kang N., Jiang L., Nedergaard M., Kang J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J. Neurosci. 2005, 25:1750-1760.
103. Xu N.-L., Harnett M.T., Williams S.R., Huber D., O'Connor D.H., Svoboda K., Magee J.C. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 2012, 492:247-251.
104. Yang B., Desai R., Kaczmarek L.K. Slack and slick K(Na) channels regulate the accuracy of timing of auditory neurons. J. Neurosci. 2007, 27:2617-2627.
105. Zalfa F., Giorgi M., Primerano B., Moro A., di Penta A., Reis S., Oostra B., Bagni C. The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 2003, 112:317-327.
106. Zhang W., Linden D.J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 2003, 4:885-900.
107. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Ann. Rev. Physiol. 2002, 64:355-405.