PRMT7 deficiency causes dysregulation of the HCN channels in the CA1 pyramidal cells and impairment of social behaviors.
Action Potentials
Animals
Behavior, Animal
Biomarkers
CA1 Region, Hippocampal
/ metabolism
Cell Line
Gene Expression Regulation
Humans
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
/ genetics
Mice
Mice, Knockout
Patch-Clamp Techniques
Protein-Arginine N-Methyltransferases
/ deficiency
Pyramidal Cells
/ metabolism
Social Behavior
Journal
Experimental & molecular medicine
ISSN: 2092-6413
Titre abrégé: Exp Mol Med
Pays: United States
ID NLM: 9607880
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
22
10
2019
accepted:
05
03
2020
revised:
14
02
2020
pubmed:
10
4
2020
medline:
3
8
2021
entrez:
10
4
2020
Statut:
ppublish
Résumé
HCN channels regulate excitability and rhythmicity in the hippocampal CA1 pyramidal cells. Perturbation in the HCN channel current (I
Identifiants
pubmed: 32269286
doi: 10.1038/s12276-020-0417-x
pii: 10.1038/s12276-020-0417-x
pmc: PMC7210990
doi:
Substances chimiques
Biomarkers
0
Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
0
PRMT7 protein, mouse
EC 2.1.1.319
Protein-Arginine N-Methyltransferases
EC 2.1.1.319
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
604-614Subventions
Organisme : Korea Health Industry Development Institute (KHIDI)
ID : HI17C1438
Pays : International
Organisme : National Research Foundation of Korea (NRF)
ID : 2016R1A5A2945889
Pays : International
Organisme : National Research Foundation of Korea (NRF)
ID : 2017R1A2B2010237
Pays : International
Organisme : National Research Foundation of Korea (NRF)
ID : 2018R1D1A1B07041560
Pays : International
Références
Monteggia, L. M., Eisch, A. J., Tang, M. D., Kaczmarek, L. K. & Nestler, E. J. Cloning and localization of the hyperpolarization-activated cyclic nucleotide-gated channel family in rat brain. Brain Res. Mol. Brain Res. 81, 129–139 (2000).
pubmed: 11000485
Ludwig, A., Zong, X., Jeglitsch, M., Hofmann, F. & Biel, M. A family of hyperpolarization-activated mammalian cation channels. Nature 393, 587–591 (1998).
pubmed: 9634236
Santoro, B., Grant, S. G., Bartsch, D. & Kandel, E. R. Interactive cloning with the SH3 domain of N-src identifies a new brain specific ion channel protein, with homology to eag and cyclic nucleotide-gated channels. Proc. Natl Acad. Sci. USA 94, 14815–14820 (1997).
pubmed: 9405696
Ishii, T. M., Takano, M., Xie, L. H., Noma, A. & Ohmori, H. Molecular characterization of the hyperpolarization-activated cation channel in rabbit heart sinoatrial node. J. Biol. Chem. 274, 12835–12839 (1999).
pubmed: 10212270
Seifert, R. et al. Molecular characterization of a slowly gating human hyperpolarization-activated channel predominantly expressed in thalamus, heart, and testis. Proc. Natl Acad. Sci. USA 96, 9391–9396 (1999).
pubmed: 10430953
Robinson, R. B. & Siegelbaum, S. A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 65, 453–480 (2003).
pubmed: 12471170
Lupica, C. R., Bell, J. A., Hoffman, A. F. & Watson, P. L. Contribution of the hyperpolarization-activated current (I(h)) to membrane potential and GABA release in hippocampal interneurons. J. Neurophysiol. 86, 261–268 (2001).
pubmed: 11431507
Nolan, M. F. et al. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119, 719–732 (2004).
pubmed: 15550252
Meuth, S. G. et al. Membrane resting potential of thalamocortical relay neurons is shaped by the interaction among TASK3 and HCN2 channels. J. Neurophysiol. 96, 1517–1529 (2006).
pubmed: 16760342
Biel, M., Wahl-Schott, C., Michalakis, S. & Zong, X. Hyperpolarization-activated cation channels: from genes to function. Physiol. Rev. 89, 847–885 (2009).
pubmed: 19584315
Magee, J. C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18, 7613–7624 (1998).
pubmed: 9742133
pmcid: 6793032
Tsay, D., Dudman, J. T. & Siegelbaum, S. A. HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56, 1076–1089 (2007).
pubmed: 18093528
pmcid: 2435011
Magee, J. C. Dendritic integration of excitatory synaptic input. Nat. Rev. Neurosci. 1, 181–190 (2000).
pubmed: 11257906
Kim, C. S., Brager, D. H. & Johnston, D. Perisomatic changes in h-channels regulate depressive behaviors following chronic unpredictable stress. Mol. Psychiatry 23, 892–903 (2018).
pubmed: 28416809
Hajisoltani, R. et al. Hyperexcitability of hippocampal CA1 pyramidal neurons in male offspring of a rat model of autism spectrum disorder (ASD) induced by prenatal exposure to valproic acid: a possible involvement of Ih channel current. Brain Res. 1708, 188–199 (2019).
pubmed: 30537517
Yi, F. et al. Autism-associated SHANK3 haploinsufficiency causes Ih channelopathy in human neurons. Science 352, aaf2669 (2016).
pubmed: 26966193
pmcid: 4901875
Nicholson, T. B., Chen, T. & Richard, S. The physiological and pathophysiological role of PRMT1-mediated protein arginine methylation. Pharmacol. Res. 60, 466–474 (2009).
pubmed: 19643181
Bedford, M. T. & Clarke, S. G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1–13 (2009).
pubmed: 19150423
pmcid: 3372459
Biggar, K. K. & Li, S. S. Non-histone protein methylation as a regulator of cellular signalling and function. Nat. Rev. Mol. Cell Biol. 16, 5–17 (2015).
pubmed: 25491103
Wei, H., Mundade, R., Lange, K. C. & Lu, T. Protein arginine methylation of non-histone proteins and its role in diseases. Cell Cycle 13, 32–41 (2014).
pubmed: 24296620
Boisvert, F. M., Dery, U., Masson, J. Y. & Richard, S. Arginine methylation of MRE11 by PRMT1 is required for DNA damage checkpoint control. Genes Dev. 19, 671–676 (2005).
pubmed: 15741314
pmcid: 1065720
Bedford, M. T. & Richard, S. Arginine methylation an emerging regulator of protein function. Mol. Cell 18, 263–272 (2005).
pubmed: 15866169
Dhar, S. S. et al. Trans-tail regulation of MLL4-catalyzed H3K4 methylation by H4R3 symmetric dimethylation is mediated by a tandem PHD of MLL4. Genes Dev. 26, 2749–2762 (2012).
pubmed: 23249737
pmcid: 3533079
Lee, S. Y. et al. Methylation determines the extracellular calcium sensitivity of the leak channel NALCN in hippocampal dentate granule cells. Exp. Mol. Med. 51, 119 (2019).
pmcid: 6802672
Jeong, H. J. et al. Prmt7 deficiency causes reduced skeletal muscle oxidative metabolism and age-related obesity. Diabetes 65, 1868–1882 (2016).
pubmed: 27207521
Penagarikano, O. et al. Exogenous and evoked oxytocin restores social behavior in the Cntnap2 mouse model of autism. Sci. Transl. Med. 7, 271ra278 (2015).
Seibenhener, M. L. & Wooten, M. W. Isolation and culture of hippocampal neurons from prenatal mice. J. Vis. Exp. e3634 (2012).
Vuong, T. A. et al. A Sonic hedgehog coreceptor, BOC regulates neuronal differentiation and neurite outgrowth via interaction with ABL and JNK activation. Cell. Signal. 30, 30–40 (2017).
pubmed: 27871935
Vuong, T. A. et al. SGTb regulates a surface localization of a guidance receptor BOC to promote neurite outgrowth. Cell. Signal. 55, 100–108 (2019).
pubmed: 30639199
Tran, P. et al. TGF-beta-activated kinase 1 (TAK1) and apoptosis signal-regulating kinase 1 (ASK1) interact with the promyogenic receptor Cdo to promote myogenic differentiation via activation of p38MAPK pathway. J. Biol. Chem. 287, 11602–11615 (2012).
pubmed: 22337877
pmcid: 3320910
Vuong, T. A. et al. PRMT7 methylates and suppresses GLI2 binding to SUFU thereby promoting its activation. Cell Death Differ. https://doi.org/10.1038/s41418-019-0334-5 (2019).
Vuong, T. A. et al. SGTb regulates a surface localization of a guidance receptor BOC to promote neurite outgrowth. Cell. Signal. 55, 100–108 (2019).
pubmed: 30639199
Okuyama, T., Kitamura, T., Roy, D. S., Itohara, S. & Tonegawa, S. Ventral CA1 neurons store social memory. Science 353, 1536–1541 (2016).
pubmed: 27708103
pmcid: 5493325
Yang, M., Silverman, J. L. & Crawley, J. N. Automated three-chambered social approach task for mice. Curr. Protoc. Neurosci. Chapter 8, Unit 8.26 (2011).
Ryan, B. C., Young, N. B., Moy, S. S. & Crawley, J. N. Olfactory cues are sufficient to elicit social approach behaviors but not social transmission of food preference in C57BL/6J mice. Behav. Brain Res. 193, 235–242 (2008).
pubmed: 18586054
pmcid: 2630588
Santoro, B. et al. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci. 20, 5264–5275 (2000).
pubmed: 10884310
pmcid: 6772310
Moosmang, S., Biel, M., Hofmann, F. & Ludwig, A. Differential distribution of four hyperpolarization-activated cation channels in mouse brain. Biol. Chem. 380, 975–980 (1999).
pubmed: 10494850
Kim, C. S. & Johnston, D. A1 adenosine receptor-mediated GIRK channels contribute to the resting conductance of CA1 neurons in the dorsal hippocampus. J. Neurophysiol. 113, 2511–2523 (2015).
pubmed: 25652929
pmcid: 4416607
Yi, F. et al. Autism-associated SHANK3 haploinsufficiency causes Ih channelopathy in human neurons. Science 352, aaf2669 (2016).
pubmed: 26966193
pmcid: 4901875
Biel, M., Ludwig, A., Zong, X. & Hofmann, F. Hyperpolarization-activated cation channels: a multi-gene family. Rev. Physiol. Biochem. Pharmacol. 136, 165–181 (1999).
pubmed: 9932486
Jimenez, J. C. et al. Anxiety Cells in a Hippocampal-Hypothalamic Circuit. Neuron 97, 670–683.e676 (2018).
pubmed: 29397273
pmcid: 5877404
Whalley, K. Emotion: ‘anxiety cells’ drive avoidance. Nat. Rev. Neurosci. 19, 182 (2018).
pubmed: 29515189
Kim, C. S., Chang, P. Y. & Johnston, D. Enhancement of dorsal hippocampal activity by knockdown of HCN1 channels leads to anxiolytic- and antidepressant-like behaviors. Neuron 75, 503–516 (2012).
pubmed: 22884333
pmcid: 3418514
Koga, K. et al. Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain. Neuron 85, 377–389 (2015).
pubmed: 25556835
Arnold, E. C., McMurray, C., Gray, R. & Johnston, D. Epilepsy-induced reduction in HCN channel expression contributes to an increased excitability in dorsal, but not ventral, hippocampal CA1 neurons. eNeuro 6, https://doi.org/10.1523/eneuro.0036-19.2019 (2019).
Noam, Y., Bernard, C. & Baram, T. Z. Towards an integrated view of HCN channel role in epilepsy. Curr. Opin. Neurobiol. 21, 873–879 (2011).
pubmed: 21782415
pmcid: 3235400
Shin, M. & Chetkovich, D. M. Activity-dependent regulation of h channel distribution in hippocampal CA1 pyramidal neurons. J. Biol. Chem. 282, 33168–33180 (2007).
pubmed: 17848552
pmcid: 2685032
Herrmann, F., Pably, P., Eckerich, C., Bedford, M. T. & Fackelmayer, F. O. Human protein arginine methyltransferases in vivo-distinct properties of eight canonical members of the PRMT family. J. Cell Sci. 122, 667–677 (2009).
pubmed: 19208762
Bender, R. A. et al. Localization of HCN1 channels to presynaptic compartments: novel plasticity that may contribute to hippocampal maturation. J. Neurosci. 27, 4697–4706 (2007).
pubmed: 17460082
pmcid: 3086816
Huang, Z. et al. Presynaptic HCN1 channels regulate Cav3.2 activity and neurotransmission at select cortical synapses. Nat. Neurosci. 14, 478–486 (2011).
pubmed: 21358644
pmcid: 3068302
Brewster, A. L. et al. Quantitative analysis and subcellular distribution of mRNA and protein expression of the hyperpolarization-activated cyclic nucleotide-gated channels throughout development in rat hippocampus. Cereb. Cortex 17, 702–712 (2007).
pubmed: 16648453
Lorincz, A., Notomi, T., Tamas, G., Shigemoto, R. & Nusser, Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat. Neurosci. 5, 1185–1193 (2002).
pubmed: 12389030
Notomi, T. & Shigemoto, R. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J. Comp. Neurol. 471, 241–276 (2004).
pubmed: 14991560
Benarroch, E. E. HCN channels: function and clinical implications. Neurology 80, 304–310 (2013).
pubmed: 23319474
Postea, O. & Biel, M. Exploring HCN channels as novel drug targets. Nat. Rev. Drug Discov. 10, 903–914 (2011).
pubmed: 22094868
Lewis, A. S. & Chetkovich, D. M. HCN channels in behavior and neurological disease: too hyper or not active enough? Mol. Cell Neurosci. 46, 357–367 (2011).
pubmed: 21130878
Phillips, A. M., Kim, T., Vargas, E., Petrou, S. & Reid, C. A. Spike-and-wave discharge mediated reduction in hippocampal HCN1 channel function associates with learning deficits in a genetic mouse model of epilepsy. Neurobiol. Dis. 64, 30–35 (2014).
pubmed: 24368169
Vaidya, S. P. & Johnston, D. Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons. Nat. Neurosci. 16, 1812–1820 (2013).
pubmed: 24185428
pmcid: 3958963
Wang, M. et al. Neuronal basis of age-related working memory decline. Nature 476, 210–213 (2011).
pubmed: 21796118
pmcid: 3193794
Nava, C. et al. Prospective diagnostic analysis of copy number variants using SNP microarrays in individuals with autism spectrum disorders. Eur. J. Hum. Genet. 22, 71–78 (2014).
pubmed: 23632794