Differential dorso-ventral distributions of Kv4.2 and HCN proteins confer distinct integrative properties to hippocampal CA1 pyramidal cell distal dendrites

Journal of Biological Chemistry

Volumn 287, Issue 21, 2012, Pages 17656-17661

  Marcelin, Béatrice ^a,b   Lugo, Joaquin N ^c   Brewster, Amy L ^c   Liu, Zhiqiang ^d   Lewis, Alan S ^d   McClelland, Shawn ^e   Chetkovich, Dane M ^d   Baram, Tallie Z ^e   Anderson, Anne E ^c   Becker, Albert ^f   Esclapez, Monique ^a,b   Bernard, Christophe ^a,b  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOWN-REGULATION; HIPPOCAMPAL CELLS; INTEGRATIVE PROPERTIES; POST-TRANSCRIPTIONAL; PYRAMIDAL CELL; SYNAPTIC INPUT; UP-REGULATION;

BIOCHEMISTRY; BIOLOGY;

BRAIN;

CYCLIC NUCLEOTIDE GATED CHANNEL; HYPERPOLARIZATION ACTIVATED CYCLIC AMP GATED CHANNEL 1; HYPERPOLARIZATION ACTIVATED CYCLIC AMP GATED CHANNEL 2; SHAL POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACK PROPAGATION; CONTROLLED STUDY; DENDRITE; DOWN REGULATION; HIPPOCAMPAL CA1 REGION; HYPERPOLARIZATION; MALE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC INHIBITION; TEMPORAL SUMMATION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DENDRITES; DOWN-REGULATION; ION CHANNELS; NERVE TISSUE PROTEINS; ORGAN SPECIFICITY; POTASSIUM CHANNELS; PYRAMIDAL CELLS; RATS; SHAL POTASSIUM CHANNELS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84861203337     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C112.367110     Document Type: Article

References (38)

1. Buzsaki, G. (2006) Rhythms of the Brain, Oxford University Press Inc., New York
2. Segal, M., Richter-Levin, G., and Maggio, N. (2010) Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20, 1332-1338
3. Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176 (Pubitemid 46095716)
4. Thompson, C. L., Pathak, S. D., Jeromin, A., Ng, L. L., MacPherson, C. R., Mortrud, M. T., Cusick, A., Riley, Z. L., Sunkin, S. M., Bernard, A., Puchalski, R. B., Gage, F. H., Jones, A. R., Bajic, V. B., Hawrylycz, M. J., and Lein, E. S. (2008) Genomic anatomy of the hippocampus. Neuron 60, 1010-1021
5. van Strien, N. M., Cappaert, N. L., and Witter, M. P. (2009) The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 10, 272-282
6. Leonardo, E. D., Richardson-Jones, J. W., Sibille, E., Kottman, A., and Hen, R. (2006) Molecular heterogeneity along the dorsal-ventral axis of the murine hippocampal CA1 field: a microarray analysis of gene expression. Neuroscience 137, 177-186 (Pubitemid 43031485)
7. Brun, V. H., Solstad, T., Kjelstrup, K. B., Fyhn, M., Witter, M. P., Moser, E. I., and Moser, M. B. (2008) Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18, 1200-1212
8. Giocomo, L. M., and Hasselmo, M. E. (2009) Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. J. Neurosci. 29, 7625-7630
9. Giocomo, L. M., and Hasselmo, M. E. (2008) Time constants of h current in layer ii stellate cells differ along the dorsal to ventral axis of medial entorhinal cortex. J. Neurosci. 28, 9414-9425
10. Giocomo, L. M., Zilli, E. A., Fransén, E., and Hasselmo, M. E. (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315, 1719-1722 (Pubitemid 46515627)
11. Boehlen, A., Heinemann, U., and Erchova, I. (2010) The range of intrinsic frequencies represented by medial entorhinal cortex stellate cells extends with age. J. Neurosci. 30, 4585-4589
12. Garden, D. L., Dodson, P. D., O'Donnell, C., White, M. D., and Nolan, M. F. (2008) Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 60, 875-889
13. Marcelin, B., Liu, Z., Chen, Y., Lewis, A. S., Becker, A., McClelland, S., Chetkovich, D. M., Migliore, M., Baram, T. Z., Esclapez, M., and Bernard, C. (2012) Dorsoventral differences in intrinsic properties in developing CA1 pyramidal cells. J. Neurosci. 32, 3736-3747
14. Kjelstrup, K. B., Solstad, T., Brun, V. H., Hafting, T., Leutgeb, S., Witter, M. P., Moser, E. I., and Moser, M. B. (2008) Finite scale of spatial representation in the hippocampus. Science 321, 140-143 (Pubitemid 351956252)
15. O'Keefe, J., and Nadel, L. (1978) The Hippocampus as a Cognitive Map, Oxford University, Oxford
16. Johnston, D., and Narayanan, R. (2008) Active dendrites: colorful wings of the mysterious butterflies. Trends Neurosci. 31, 309-316
17. +channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875
18. Magee, J. C. (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18, 7613-7624
19. Narayanan, R., and 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 (Pubitemid 350251113)
20. Marcelin, B., Chauvière, L., Becker, A., Migliore, M., Esclapez, M., and Bernard, C. (2009) h channel-dependent deficit of theta oscillation resonance and phase shift in temporal lobe epilepsy. Neurobiol. Dis. 33, 436-447
21. Magee, J. C., and Johnston, D. (2005) Plasticity of dendritic function. Curr. Opin. Neurobiol. 15, 334-342 (Pubitemid 40806446)
22. Pike, F. G., Goddard, R. S., Suckling, J. M., Ganter, P., Kasthuri, N., and Paulsen, O. (2000) Distinct frequency preferences of different types of rat hippocampal neurons in response to oscillatory input currents. J. Physiol. 529, 205-213
23. Hutcheon, B., and Yarom, Y. (2000) Resonance, oscillation, and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216-222 (Pubitemid 30236181)
24. Hu, H., Vervaeke, K., and Storm, J. F. (2002) Two forms of electrical resonance at theta frequencies, generated by M-current, h-current, and persistent Na+ current in rat hippocampal pyramidal cells. J. Physiol. 545, 783-805 (Pubitemid 36024420)
25. Noam, Y., Bernard, C., and Baram, T. Z. (2011) Toward an integrated view of HCN channel role in epilepsy. Curr. Opin. Neurobiol. 21, 873-879
26. McClelland, S., Flynn, C., Dubé, C., Richichi, C., Zha, Q., Ghestem, A., Esclapez, M., Bernard, C., and Baram, T. Z. (2011) Neuron-restrictive silencer factor-mediated hyperpolarization-activated cyclic nucleotide gated channelopathy in experimental temporal lobe epilepsy. Ann. Neurol. 70, 454-464
27. Esclapez, M., Hirsch, J. C., Ben-Ari, Y., and Bernard, C. (1999) Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J. Comp. Neurol. 408, 449-460 (Pubitemid 29211174)
28. Bernard, C., and Johnston, D. (2003) Distance-dependent modifiable threshold for action potential backpropagation in hippocampal dendrites. J. Neurophysiol. 90, 1807-1816 (Pubitemid 37129387)
29. Narayanan, R., and Johnston, D. (2008) The h channel mediates location dependence and plasticity of intrinsic phase response in rat hippocampal neurons. J. Neurosci. 28, 5846-5860
30. Lugo, J. N., Barnwell, L. F., Ren, Y., Lee, W. L., Johnston, L. D., Kim, R., Hrachovy, R. A., Sweatt, J. D., and Anderson, A. E. (2008) Altered phosphorylation and localization of the A-type channel, Kv4.2, in status epilepticus. J. Neurochem. 106, 1929-1940
31. Lu, H. C., She, W. C., Plas, D. T., Neumann, P. E., Janz, R., and Crair, M. C. (2003) Adenylyl cyclase I regulates AMPA receptor trafficking during mouse cortical "barrel" map development. Nat. Neurosci. 6, 939-947 (Pubitemid 37064755)
32. Lewis, A. S., Schwartz, E., Chan, C. S., Noam, Y., Shin, M., Wadman, W. J., Surmeier, D. J., Baram, T. Z., Macdonald, R. L., and Chetkovich, D. M. (2009) Alternatively spliced isoforms of TRIP8b differentially control h channel trafficking and function. J. Neurosci. 29, 6250-6265
33. + channels in hippocampus involves a mitogen-activated protein kinase pathway. J. Neurosci. 22, 4860-4868
34. Bernard, C., Anderson, A., Becker, A., Poolos, N. P., Beck, H., and Johnston, D. (2004) Acquired dendritic channelopathy in temporal lobe epilepsy. Science 305, 532-535 (Pubitemid 38971346)
35. Santoro, B., Wainger, B. J., and Siegelbaum, S. A. (2004) Regulation of HCN channel surface expression by a novel C-terminal protein-protein interaction. J. Neurosci. 24, 10750-10762 (Pubitemid 39557650)
36. Zolles, G., Wenzel, D., Bildl, W., Schulte, U., Hofmann, A., Müller, C. S., Thumfart, J. O., Vlachos, A., Deller, T., Pfeifer, A., Fleischmann, B. K., Roeper, J., Fakler, B., and Klöcker, N. (2009) Association with the auxiliary subunit PEX5R/Trip8b controls responsiveness of HCN channels to cAMP and adrenergic stimulation. Neuron 62, 814-825
37. Maggio, N., and Segal, M. (2007) Unique regulation of long term potentiation in the rat ventral hippocampus. Hippocampus 17, 10-25 (Pubitemid 46218670)
38. Schulz, D. J., Goaillard, J. M., and Marder, E. E. (2007) Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proc. Natl. Acad. Sci. U.S.A. 104, 13187-13191 (Pubitemid 351737614)