ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 50, 2010, Pages 21818-21823

  Chen, Yong Jun ^a,b   Zhang, Meng ^a   Yin, Dong Min ^b   Wen, Lei ^b   Ting, Annie ^b   Wang, Pu ^a   Lu, Yi Sheng ^b   Zhu, Xin Hong ^a,b   Li, Shu Ji ^a   Wu, Cui Ying ^a   Wang, Xue Ming ^a   Lai, Cary ^c   Xiong, Wen Cheng ^b   Mei, Lin ^a,b   Gao, Tian Ming ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BRAIN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; PARVALBUMIN;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CONDITIONING; CONTRAST; FEAR; GABAERGIC TRANSMISSION; GENETIC SUSCEPTIBILITY; HIPPOCAMPUS; HYPOTHESIS; INTERNEURON; LONG TERM POTENTIATION; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PATHOGENESIS; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RECEPTOR BLOCKING; REGULATORY MECHANISM; SCHIZOPHRENIA; SIGNAL TRANSDUCTION;

ANIMALS; CONDITIONING (PSYCHOLOGY); FEAR; GABA-A RECEPTOR ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; INTERNEURONS; LONG-TERM POTENTIATION; MICE; MICE, KNOCKOUT; NEUREGULIN-1; PARVALBUMINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, GABA-A; SYNAPSES;

MUS;

EID: 78650756926     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1010669107     Document Type: Article

References (47)

1. Mei L, Xiong WC (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9:437-452.
2. Stefansson H, et al. (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71:877-892.
3. Law AJ, et al. (2006) Neuregulin 1 (NRG1) transcripts are differentially expressed in schizophrenia and regulated by 5′ SNPS associated with the disease. Proc Natl Acad Sci USA 103:6747-6752.
4. Yang JZ, et al. (2003) Association study of neuregulin 1 gene with schizophrenia. Mol Psychiatry 8:706-709.
5. Huang YZ, et al. (2000) Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26:443-455.
6. Ma L, et al. (2003) Ligand-dependent recruitment of the ErbB4 signaling complex into neuronal lipid rafts. J Neurosci 23:3164-3175.
7. Bjarnadottir M, et al. (2007) Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: Differential synaptic function in NRG1+/- knockouts compared with wild-type mice. J Neurosci 27:4519-4529.
8. Pitcher GM, Beggs S, Woo RS, Mei L, Salter MW (2008) ErbB4 is a suppressor of longterm potentiation in the adult hippocampus. NeuroReport 19:139-143.
9. Iyengar SS, Mott DD (2008) Neuregulin blocks synaptic strengthening after epileptiform activity in the rat hippocampus. Brain Res 1208:67-73.
10. Gu ZL, Jiang Q, Fu AKY, Ip NY, Yan Z (2005) Regulation of NMDA receptors by neuregulin signaling in prefrontal cortex. J Neurosci 25:4974-4984.
11. Kwon OB, Longart M, Vullhorst D, Hoffman DA, Buonanno A (2005) Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J Neurosci 25: 9378-9383.
12. Li B, Woo RS, Mei L, Malinow R (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54:583-597.
13. Vullhorst D, et al. (2009) Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 29:12255-12264.
14. Woo RS, et al. (2007) Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54:599-610.
15. Wen L, et al. (2010) Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci USA 107:1211-1216.
16. Kraushaar U, Jonas P (2000) Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20:5594-5607.
17. Wigström H, Gustafsson B (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301:603-604. (Pubitemid 13161529)
18. Meredith RM, Floyer-Lea AM, Paulsen O (2003) Maturation of long-term potentiation induction rules in rodent hippocampus: Role of GABAergic inhibition. J Neurosci 23: 11142-11146.
19. Akaike N, Hattori K, Oomura Y, Carpenter DO (1985) Bicuculline and picrotoxin block gamma-aminobutyric acid-gated Cl-conductance by different mechanisms. Experientia 41:70-71.
20. Yau HJ, Wang HF, Lai CR, Liu FC (2003) 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.
21. Neddens J, Buonanno A (2010) Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice. Hippocampus 20:724-744.
22. Fazzari P, et al. (2010) Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464:1376-1380.
23. Finlay BL, Darlington RB (1995) Linked regularities in the development and evolution of mammalian brains. Science 268:1578-1584.
24. del Río JA, de Lecea L, Ferrer I, Soriano E (1994) The development of parvalbuminimmunoreactivity in the neocortex of the mouse. Brain Res Dev Brain Res 81:247-259.
25. Hof PR, et al. (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. J Chem Neuroanat 16:77-116.
26. Chen YJJ, et al. (2008) Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. J Neurosci 28:6872-6883.
27. Barros CS, et al. (2009) Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proc Natl Acad Sci USA 106:4507-4512.
28. Tsien JZ, et al. (1996) Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87:1317-1326.
29. Shimizu E, Tang YP, Rampon C, Tsien JZ (2000) NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science 290:1170-1174.
30. Zakharenko SS, et al. (2003) Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39: 975-990.
31. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence. Mol Psychiatry, 10:40-68 image 5.
32. Frankland PW, Sakaguchi M, Arruda-Carvalho M (2008) Starting at the endophenotype: A role for alpha-CaMKII in schizophrenia? Mol Brain 1:5.
33. Law AJ, Kleinman JE, Weinberger DR, Weickert CS (2007) Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum Mol Genet 16:129-141.
34. Silberberg G, Darvasi A, Pinkas-Kramarski R, Navon R (2006) The involvement of ErbB4 with schizophrenia: Association and expression studies. Am J Med Genet B Neuropsychiatr Genet 141B:142-148.
35. Hahn CG, et al. (2006) Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nat Med 12:824-828.
36. Law AJ, et al. (2006) Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5′ SNPs associated with the disease. Proc Natl Acad Sci USA 103:6747-6752.
37. Chong VZ, et al. (2008) Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients. Schizophr Res 100:270-280.
38. Lewis DA, Sweet RA (2009) Schizophrenia from a neural circuitry perspective: Advancing toward rational pharmacological therapies. J Clin Invest 119:706-716.
39. Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274-285.
40. Kim JJ, Fanselow MS, DeCola JP, Landeira-Fernandez J (1992) Selective impairment of long-term but not short-term conditional fear by the N-methyl-D-aspartate antagonist APV. Behav Neurosci 106:591-596.
41. Lewis DA, Gonzalez-Burgos G (2006) Pathophysiologically based treatment interventions in schizophrenia. Nat Med 12:1016-1022.
42. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-324.
43. Beneyto M, Kristiansen LV, Oni-Orisan A, McCullumsmith RE, Meador-Woodruff JH (2007) Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 32:1888-1902.
44. García-Rivello H, et al. (2005) Dilated cardiomyopathy in Erb-b4-deficient ventricular muscle. Am J Physiol Heart Circ Physiol 289:H1153-H1160.
45. Arber S, Ladle DR, Lin JH, Frank E, Jessell TM (2000) ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101:485-498.
46. Hippenmeyer S, et al. (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3:e159.
47. Ting A, et al. (2010) Neuregulin1 promotes excitatory synapse development specifically in GABAergic interneurons. J Neurosci, in press.