Neuregulin 1 regulates excitability of fast-spiking neurons through Kv1.1 and acts in epilepsy

Nature Neuroscience

Volumn 15, Issue 2, 2012, Pages 267-273

  Li, Ke Xin ^a   Lu, Ying Mei ^a   Xu, Zheng Hao ^a   Zhang, Jing ^a   Zhu, Jun Ming ^a   Zhang, Jian Ming ^a   Cao, Shu Xia ^a   Chen, Xiao Juan ^a   Chen, Zhong ^a   Luo, Jian Hong ^a,b   Duan, Shumin ^a,b   Li, Xiao Ming ^a,b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; PARVALBUMIN; PENTETRAZOLE; PILOCARPINE; POTASSIUM CHANNEL KV1.1; VOLTAGE GATED POTASSIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; EPILEPTIC STATE; GENE DELETION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNEURON; MOUSE; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; CAVEOLIN 1; CELL LINE, TRANSFORMED; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ELECTRIC STIMULATION; EPILEPSY; FEMALE; HIPPOCAMPUS; HUMANS; IMMUNOPRECIPITATION; KV1.1 POTASSIUM CHANNEL; MALE; MICE; MICE, TRANSGENIC; NEUREGULIN-1; NEURONS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PENTYLENETETRAZOLE; PEPTIDES; PILOCARPINE; POTASSIUM CHANNEL BLOCKERS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; TYRPHOSTINS;

EID: 84856293318     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3006     Document Type: Article

References (50)

1. Perucca, E., Alexandre, V. Jr. & Tomson, T. Old versus new antiepileptic drugs: the SANAD study. Lancet 370, 313; author reply 315-316 (2007). (Pubitemid 47094983)
2. Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486 (1997). (Pubitemid 27353633)
3. Lau, D. et al. Impaired fast-spiking, suppressed cortical inhibition, and increased susceptibility to seizures in mice lacking Kv3.2 K+ channel proteins. J. Neurosci. 20, 9071-9085 (2000). (Pubitemid 32042909)
4. Ogiwara, I. et al. Na(v)1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J. Neurosci. 27, 5903-5914 (2007). (Pubitemid 46849766)
5. Buonanno, A. The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits. Brain Res. Bull. 83, 122-131 (2010).
6. Mei, L. & Xiong, W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 9, 437-452 (2008). (Pubitemid 351704944)
7. Corfas, G., Roy, K. & Buxbaum, J.D. Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nat. Neurosci. 7, 575-580 (2004). (Pubitemid 38691892)
8. Lai, C. & Lemke, G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 6, 691-704 (1991).
9. Fazzari, P. et al. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464, 1376-1380 (2010).
10. Huang, Y.Z. et al. Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26, 443-455 (2000).
11. Yau, H.J., Wang, H.F., Lai, C. & Liu, F.C. Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences. Cereb. Cortex 13, 252-264 (2003). (Pubitemid 36236672)
12. Vullhorst, D. et al. Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J. Neurosci. 29, 12255-12264 (2009).
13. Woo, R.S. et al. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54, 599-610 (2007).
14. Wen, L. et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. USA 107, 1211-1216 (2010).
15. Chen, Y.J. et al. ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc. Natl. Acad. Sci. USA 107, 21818-21823 (2010).
16. Kwon, O.B., Longart, M., Vullhorst, D., Hoffman, D.A. & Buonanno, A. Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 25, 9378-9383 (2005). (Pubitemid 41464750)
17. Pitcher, G.M. et al. Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors. Nat. Med. 17, 470-478 (2011).
18. Goldberg, E.M. et al. K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58, 387-400 (2008). (Pubitemid 351615188)
19. Chattopadhyaya, B. et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 24, 9598-9611 (2004). (Pubitemid 39441514)
20. Di Cristo, G. et al. Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat. Neurosci. 7, 1184-1186 (2004). (Pubitemid 39426235)
21. Law, A.J., Shannon Weickert, C., Hyde, T.M., Kleinman, J.E. & Harrison, P.J. Neuregulin-1 (NRG-1) mRNA and protein in the adult human brain. Neuroscience 127, 125-136 (2004). (Pubitemid 38829158)
22. Ting, A.K. et al. Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. J. Neurosci. 31, 15-25 (2011).
23. Bjarnadottir, M. et al. Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1r/f knock-outs compared with wild-type mice. J. Neurosci. 27, 4519-4529 (2007). (Pubitemid 46663586)
24. Gu, Z., Jiang, Q., Fu, A.K., Ip, N.Y. & Yan, Z. Regulation of NMDA receptors by neuregulin signaling in prefrontal cortex. J. Neurosci. 25, 4974-4984 (2005). (Pubitemid 40712840)
25. Li, B., Woo, R.S., Mei, L. & Malinow, R. The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54, 583-597 (2007). (Pubitemid 46756136)
26. Fukazawa, R. et al. Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J. Mol. Cell. Cardiol. 35, 1473-1479 (2003). (Pubitemid 37491190)
27. García-Rivello, H. et al. Dilated cardiomyopathy in Erb-b4-deficient ventricular muscle. Am. J. Physiol. Heart Circ. Physiol. 289, H1153-H1160 (2005). (Pubitemid 41208959)
28. Arber, S., Ladle, D.R., Lin, J.H., Frank, E. & Jessell, T.M. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101, 485-498 (2000).
29. Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
30. Fisahn, A., Neddens, J., Yan, L. & Buonanno, A. Neuregulin-1 modulates hippocampal gamma oscillations: implications for schizophrenia. Cereb. Cortex 19, 612-618 (2009).
31. Neddens, J. & Buonanno, A. Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice. Hippocampus 20, 724-744 (2010).
32. Coetzee, W.A. et al. Molecular diversity of K+ channels. Ann. NY Acad. Sci. 868, 233-285 (1999).
33. Guan, D. et al. Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones. J. Physiol. (Lond.) 571, 371-389 (2006).
34. Robertson, B., Owen, D., Stow, J., Butler, C. & Newland, C. Novel effects of dendrotoxin homologues on subtypes of mammalian Kv1 potassium channels expressed in Xenopus oocytes. FEBS Lett. 383, 26-30 (1996). (Pubitemid 26093717)
35. Ziyatdinova, S. et al. Spontaneous epileptiform discharges in a mouse model of Alzheimer′s disease are suppressed by antiepileptic drugs that block sodium channels. Epilepsy Res. 94, 75-85 (2011).
36. Dreyfus, J. A Remarkable Medicine Has Been Overlooked: Including an Autobiography and the Clinical Section of the Broad Range of Use of Phenytoin (Continuum International Publishing Group, 1998).
37. Perucca, E. Pharmacological and therapeutic properties of valproate: a summary after 35 years of clinical experience. CNS Drugs 16, 695-714 (2002). (Pubitemid 35176854)
38. Gibson, J.R., Beierlein, M. & Connors, B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79 (1999).
39. Wang, H., Kunkel, D.D., Schwartzkroin, P.A. & Tempel, B.L. Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J. Neurosci. 14, 4588-4599 (1994). (Pubitemid 24237885)
40. Tanouye, M.A., Ferrus, A. & Fujita, S.C. Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc. Natl. Acad. Sci. USA 78, 6548-6552 (1981). (Pubitemid 12208180)
41. Holmes, T.C., Fadool, D.A., Ren, R. & Levitan, I.B. Association of Src tyrosine kinase with a human potassium channel mediated by SH3 domain. Science 274, 2089-2091 (1996). (Pubitemid 27020703)
42. Cook, K.K. & Fadool, D.A. Two adaptor proteins differentially modulate the phosphorylation and biophysics of Kv1.3 ion channel by SRC kinase. J. Biol. Chem. 277, 13268-13280 (2002). (Pubitemid 34952698)
43. Tucker, K. & Fadool, D.A. Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. J. Physiol. (Lond.) 542, 413-429 (2002). (Pubitemid 35190304)
44. Cascella, N.G., Schretlen, D.J. & Sawa, A. Schizophrenia and epilepsy: is there a shared susceptibility? Neurosci. Res. 63, 227-235 (2009).
45. Zuberi, S.M. et al. A novel mutation in the human voltage-gated potassium channel gene (Kv1.1) associates with episodic ataxia type 1 and sometimes with partial epilepsy. Brain 122, 817-825 (1999). (Pubitemid 29219257)
46. Liguori, R., Avoni, P., Baruzzi, A., Di Stasi, V. & Montagna, P. Familial continuous motor unit activity and epilepsy. Muscle Nerve 24, 630-633 (2001). (Pubitemid 32373024)
47. Schulte, U. et al. The epilepsy-linked Lgi1 protein assembles into presynaptic Kv1 channels and inhibits inactivation by Kvbeta1. Neuron 49, 697-706 (2006). (Pubitemid 43290129)
48. Strauss, K.A. et al. Recessive symptomatic focal epilepsy and mutant contactin-associated protein-like 2. N. Engl. J. Med. 354, 1370-1377 (2006).
49. Smart, S.L. et al. Deletion of the K(V)1.1 potassium channel causes epilepsy in mice. Neuron 20, 809-819 (1998). (Pubitemid 28199058)
50. Ostrom, R.S. et al. Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J. Biol. Chem. 276, 42063-42069 (2001).