DOI: 10.1523/jneurosci.0936-11.2011. Deletion of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel Auxiliary Subunit TRIP8b Impairs Hippocampal<i>I</i><sub>h</sub>Localization and Function and Promotes Antidepressant Behavior in Mice

Deletion of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel Auxiliary Subunit TRIP8b Impairs HippocampalIhLocalization and Function and Promotes Antidepressant Behavior in Mice

10.1523/jneurosci.0936-11.2011

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

Output properties of neurons are greatly shaped by voltage-gated ion channels, whose biophysical properties and localization within axodendritic compartments serve to significantly transform the original input. The hyperpolarization-activated current,Ih, is mediated by hyperpolarization-activated cyclic nucleotide-gated (HCN) channels and plays a fundamental role in influencing neuronal excitability by regulating both membrane potential and input resistance. In neurons such as cortical and hippocampal pyramidal neurons, the subcellular localization of HCN channels plays a critical functional role, yet mechanisms controlling HCN channel trafficking are not fully understood. Because ion channel function and localization are often influenced by interacting proteins, we generated a knock-out mouse lacking the HCN channel auxiliary subunit, tetratricopeptide repeat-containing Rab8b-interacting protein (TRIP8b). Eliminating expression of TRIP8b dramatically reducedIhexpression in hippocampal pyramidal neurons. Loss ofIh-dependent membrane voltage properties was attributable to reduction of HCN channels on the neuronal surface, and there was a striking disruption of the normal expression pattern of HCN channels in pyramidal neuron dendrites. In heterologous cells and neurons, absence of TRIP8b increased HCN subunit targeting to and degradation by lysosomes. Mice lacking TRIP8b demonstrated motor learning deficits and enhanced resistance to multiple tasks of behavioral despair with high predictive validity for antidepressant efficacy. We observed similar resistance to behavioral despair in distinct mutant mice lacking HCN1 or HCN2. These data demonstrate that interaction with the auxiliary subunit TRIP8b is a major mechanism underlying proper expression of HCN channels andIhin vivo, and suggest that targetingIhmay provide a novel approach to treatment of depression.

Bibliography

Lewis, A. S., Vaidya, S. P., Blaiss, C. A., Liu, Z., Stoub, T. R., Brager, D. H., Chen, X., Bender, R. A., Estep, C. M., Popov, A. B., Kang, C. E., Van Veldhoven, P. P., Bayliss, D. A., Nicholson, D. A., Powell, C. M., Johnston, D., & Chetkovich, D. M. (2011). Deletion of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel Auxiliary Subunit TRIP8b Impairs HippocampalIhLocalization and Function and Promotes Antidepressant Behavior in Mice. The Journal of Neuroscience, 31(20), 7424â7440.

Authors 17

Alan S. Lewis (first)
Sachin P. Vaidya (additional)
Cory A. Blaiss (additional)
Zhiqiang Liu (additional)
Travis R. Stoub (additional)
Darrin H. Brager (additional)
Xiangdong Chen (additional)
Roland A. Bender (additional)
Chad M. Estep (additional)
Andrey B. Popov (additional)
Catherine E. Kang (additional)
Paul P. Van Veldhoven (additional)
Douglas A. Bayliss (additional)
Daniel A. Nicholson (additional)
Craig M. Powell (additional)
Daniel Johnston (additional)
Dane M. Chetkovich (additional)

References 54 Referenced 107

10.1042/0264-6021:3570635
10.1074/jbc.272.41.26023
10.1038/ng0997-49
10.1196/annals.1420.024
10.1016/j.yjmcc.2009.06.019
10.1038/nrn1846
10.1152/physrev.00029.2008
10.1111/j.1601-183X.2008.00455.x
10.1523/JNEUROSCI.3520-07.2007
10.1016/j.nbd.2008.12.004
10.1210/me.2006-0258
10.1073/pnas.0910297106
10.1016/j.bbamcr.2008.02.013 / Biochim Biophys Acta / Comparison of the PTS1- and Rab8b-binding properties of Pex5p and Pex5Rp/TRIP8b by Fransen (2008)
10.1093/cvr/cvn062
10.1371/journal.pone.0007266
10.1113/jphysiol.2002.029249
10.1523/JNEUROSCI.1531-09.2009
10.1523/JNEUROSCI.4968-07.2008
10.1152/jn.1996.76.2.683 / J Neurophysiol / Subthreshold membrane resonance in neocortical neurons by Hutcheon (1996)
{'key': '2023041303503419000_31.20.7424.20', 'first-page': '716.7', 'article-title': 'TRIP8b knockout mice exhibit reduced thalamocortical I h and pure absence epilepsy', 'volume': '35', 'author': 'Jaramillo', 'year': '2009', 'journal-title': 'Soc Neurosci Abstr'} / Soc Neurosci Abstr / TRIP8b knockout mice exhibit reduced thalamocortical I h and pure absence epilepsy by Jaramillo (2009)
10.1523/JNEUROSCI.3605-07.2007
10.1002/(SICI)1098-1063(2000)10:1<47::AID-HIPO5>3.0.CO;2-6
10.1016/j.neuron.2006.03.023
10.1038/nrn1938
10.1523/JNEUROSCI.0856-09.2009
10.4161/chan.4.3.11630 / Channels (Austin) / The fast and slow ups and downs of HCN channel regulation by Lewis (2010)
10.1038/nn962
10.1523/JNEUROSCI.18-19-07613.1998 / J Neurosci / Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons by Magee (1998)
10.1038/9158
10.1111/j.1601-1848.2004.00076.x
10.1016/j.bbr.2006.07.030
10.1016/j.neuron.2007.10.033
10.1016/S0092-8674(03)00884-5
10.1016/j.cell.2004.11.020
10.1002/cne.11039
10.1038/nn891
10.1016/S0896-6273(04)00146-1
10.1152/jn.00082.2009
10.1523/JNEUROSCI.3300-04.2004
10.1016/j.neuron.2009.05.009
10.1111/j.1528-1167.2010.02554.x
10.1016/j.neuron.2004.10.011
10.1074/jbc.M703736200
10.1016/j.brainres.2006.01.102
10.1016/j.nbd.2008.06.013
10.1126/science.1146221
10.1016/j.neuron.2007.11.015
10.1523/JNEUROSCI.3568-04.2005
10.1016/0003-2697(87)90649-X
10.1111/j.1432-1033.1994.tb18926.x / Eur J Biochem / Large-scale purification and further characterization of rat pristanoyl-CoA oxidase by Van Veldhoven (1994)
10.1016/j.pneurobio.2011.01.003
10.1152/jn.2000.83.5.3177 / J Neurophysiol / Site independence of EPSP time course is mediated by dendritic I h in neocortical pyramidal neurons by Williams (2000)
10.1677/JOE-09-0068
10.1016/j.neuron.2009.05.008

Dates

Type	When
Created	14 years, 3 months ago (May 18, 2011, 12:53 p.m.)
Deposited	2 years, 4 months ago (April 13, 2023, 4:31 p.m.)
Indexed	2 months, 3 weeks ago (June 14, 2025, 3:26 p.m.)
Issued	14 years, 3 months ago (May 18, 2011)
Published	14 years, 3 months ago (May 18, 2011)
Published Online	14 years, 3 months ago (May 18, 2011)
Published Print	14 years, 3 months ago (May 18, 2011)

Funders 0

None

BibTeX

@article{Lewis_2011, title={Deletion of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel Auxiliary Subunit TRIP8b Impairs HippocampalIhLocalization and Function and Promotes Antidepressant Behavior in Mice}, volume={31}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.0936-11.2011}, DOI={10.1523/jneurosci.0936-11.2011}, number={20}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Lewis, Alan S. and Vaidya, Sachin P. and Blaiss, Cory A. and Liu, Zhiqiang and Stoub, Travis R. and Brager, Darrin H. and Chen, Xiangdong and Bender, Roland A. and Estep, Chad M. and Popov, Andrey B. and Kang, Catherine E. and Van Veldhoven, Paul P. and Bayliss, Douglas A. and Nicholson, Daniel A. and Powell, Craig M. and Johnston, Daniel and Chetkovich, Dane M.}, year={2011}, month=may, pages={7424–7440} }

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