Type III neuregulin 1 is required for multiple forms of excitatory synaptic plasticity of mouse cortico-amygdala circuits

Journal of Neuroscience

Volumn 33, Issue 23, 2013, Pages 9655-9666

  Jiang, Li ^a,b   Emmetsberger, Jaime ^a,b   Talmage, David A ^a,b   Role, Lorna W ^a,b,c  

^a STONY BROOK UNIVERSITY   (United States)

^b Center for Nervous Systems Disorders Research   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CHOLINERGIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEU DIFFERENTIATION FACTOR; NICOTINE;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; CALIBRATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IMMUNOFLUORESCENCE; MOUSE; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; WILCOXON SIGNED RANKS TEST;

AMYGDALA; ANIMALS; CEREBRAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE NET; NEUREGULIN-1; NEURONAL PLASTICITY; ORGAN CULTURE TECHNIQUES; SYNAPTIC TRANSMISSION;

EID: 84878503226     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2888-12.2013     Document Type: Article

References (51)

1. Abe Y, Namba H, Kato T, Iwakura Y, Nawa H (2011) Neuregulin-1 signals from the periphery regulate AMPA receptor sensitivity and expression in GABAergic interneurons in developing neocortex. J Neurosci 31: 5699-5709. CrossRef Medline
2. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:207-221. CrossRef Medline
3. Bae JS, Pasaje CF, Park BL, Cheong HS, Kim JH, Kim JY, Shin JG, Park CS, Kim BJ, Lee CS, Lee M, Choi WH, Shin TM, Hwang J, Shin HD, Woo SI (2012) Genetic association analysis of ERBB4 polymorphisms with the risk of schizophrenia and SPEM abnormality in a Korean population. Brain Res 1466:146-151. CrossRef Medline
4. Bao J, Wolpowitz D, Role LW, Talmage DA (2003) Back-signaling by the Nrg-1 intracellular domain. J Cell Biol 161:1133-1141. CrossRef Medline
5. Bao J, Lin H, Ouyang Y, Lei D, Osman A, Kim TW, Mei L, Dai P, Ohlemiller KK, Ambron RT (2004) Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nat Neurosci 7:1250-1258. CrossRef Medline
6. +/- knock-outs compared with wild-type mice. J Neurosci 27:4519-4529. CrossRef Medline
7. Brinkmann BG, Agarwal A, Sereda MW, Garratt AN, Müller T, Wende H, Stassart RM, Nawaz S, Humml C, Velanac V, Radyushkin K, Goebbels S, Fischer TM, Franklin RJ, Lai C, Ehrenreich H, Birchmeier C, Schwab MH, Nave KA (2008) Neuregulin-1/ErbB signaling serves distinct functions in myelination of the peripheral and central nervous system. Neuron 59:581-595. CrossRef Medline
8. Buonanno A, Kwon OB, Yan L, Gonzalez C, Longart M, Hoffman D, Vullhorst D (2008) Neuregulins and neuronal plasticity: possible relevance in schizophrenia. Novartis Found Symp 289:165-177. CrossRef
9. Canetta SE, Luca E, Pertot E, Role LW, Talmage DA (2011) Type III Nrg1 back-signaling enhances functional TRPV1 along sensory axons contributing to basal and inflammatory thermal pain sensation. PloS One 6:e25108. CrossRef Medline
10. Carlsen J, Záborszky L, Heimer L (1985) Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J Comp Neurol 234:155-167. CrossRef Medline
11. Chang Q, Fischbach GD (2006) An acute effect of neuregulin 1 beta to suppress α7-containing nicotinic acetylcholine receptors in hippocampal interneurons. J Neurosci 26:11295-11303. CrossRef Medline
12. Chen B, Wang SS, Hattox AM, Rayburn H, Nelson SB, McConnell SK (2008a) The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc Natl Acad Sci U S A 105:11382-11387. CrossRef Medline
13. Chen YJ, Johnson MA, Lieberman MD, Goodchild RE, Schobel S, Lewandowski N, Rosoklija G, Liu RC, Gingrich JA, Small S, Moore H, Dwork AJ, Talmage DA, Role LW (2008b) Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. J Neurosci 28:6872-6883. CrossRef Medline
14. Chen Y, Hancock ML, Role LW, Talmage DA (2010a) Intramembranous valine linked to schizophrenia is required for neuregulin 1 regulation of the morphological development of cortical neurons. J Neurosci 30:9199-9208. CrossRef Medline
15. Chen YJ, Zhang M, Yin DM, Wen L, Ting A, Wang P, Lu YS, Zhu XH, Li SJ, Wu CY, Wang XM, Lai C, Xiong WC, Mei L, Gao TM (2010b) ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc Natl Acad Sci U S A 107:21818-21823. CrossRef Medline
16. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757-771. CrossRef Medline
17. Fazzari P, Paternain AV, Valiente M, Pla R, Luján R, Lloyd K, Lerma J, Marín O, Rico B (2010) Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464:1376-1380. CrossRef Medline
18. Fenster C, Vullhorst D, Buonanno A (2012) Acute neuregulin-1 signaling influences AMPA receptor-mediated responses in cultured cerebellar granule neurons. Brain Res Bull 87:21-29. CrossRef Medline
19. Freedman R, Leonard S, Gault JM, Hopkins J, Cloninger CR, Kaufmann CA, Tsuang MT, Farone SV, Malaspina D, Svrakic DM, Sanders A, Gejman P (2001) Linkage disequilibrium for schizophrenia at the chromosome 15q13-14 locus of the α7-nicotinic acetylcholine receptor subunit gene (CHRNA7). Am J Med Genet 105:20-22. CrossRef Medline
20. Hancock ML, Canetta SE, Role LW, Talmage DA (2008) Presynaptic type III neuregulin1-ErbB signaling targets α7 nicotinic acetylcholine receptors to axons. J Cell Biol 181:511-521. CrossRef Medline
21. Hancock ML, Nowakowski DW, Role LW, Talmage DA, Flanagan JG (2011) Type III neuregulin 1 regulates pathfinding of sensory axons in the developing spinal cord and periphery. Development 138:4887-4898. CrossRef Medline
22. Harrison PJ, Law AJ (2006) Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry 60:132-140. CrossRef Medline
23. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10:40-68. CrossRef Medline
24. Jiang L, Role LW (2008) Facilitation of cortico-amygdala synapses by nicotine: activity-dependent modulation of glutamatergic transmission. J Neurophysiol 99:1988-1999. CrossRef Medline
25. 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. CrossRef Medline
26. Leonard S, Freedman R (2006) Genetics of chromosome 15q13-q14 in schizophrenia. Biol Psychiatry 60:115-122. CrossRef Medline
27. Li B, Woo RS, Mei L, Malinow R (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54: 583-597. CrossRef Medline
28. López-Bendito G, Cautinat A, Sánchez JA, Bielle F, Flames N, Garratt AN, Talmage DA, Role LW, Charnay P, Marín O, Garel S (2006) Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125:127-142. CrossRef Medline
29. Lu CL, Wang YC, Chen JY, Lai IC, Liou YJ (2010) Support for the involvement of the ERBB4 gene in schizophrenia: a genetic association analysis. Neurosci Lett 481:120-125. CrossRef Medline
30. Mathew SV, Law AJ, Lipska BK, Dávila-Garcia MI, Zamora ED, Mitkus SN, Vakkalanka R, Straub RE, Weinberger DR, Kleinman JE, Hyde TM (2007) Alpha7 nicotinic acetylcholine receptor mRNA expression and binding in postmortem human brain are associated with genetic variation in neuregulin 1. Hum Mol Genet 16:2921-2932. CrossRef Medline
31. McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C, Rubenstein JL, Chen B (2011) Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci 31:549-564. CrossRef Medline
32. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700-703. CrossRef Medline
33. Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD (2005) Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47:817-831. CrossRef Medline
34. Muller JF, Mascagni F, McDonald AJ (2011) Cholinergic innervation of pyramidal cells and parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Comp Neurol 519:790-805. CrossRef Medline
35. Neddens J, Vullhorst D, Paredes D, Buonanno A (2009) Neuregulin links dopaminergic and glutamatergic neurotransmission to control hippocampal synaptic plasticity. Commun Integr Biol 2:261-264. CrossRef Medline
36. Paxinos G, Franklin K (2004) The mouse brain in stereotaxic coordinates, Ed 2. Amsterdam: Elsevier.
37. Pitcher GM, Beggs S, Woo RS, Mei L, Salter MW (2008) ErbB4 is a suppressor of long-term potentiation in the adult hippocampus. Neuroreport 19:139-143. CrossRef Medline
38. Pitcher GM, Kalia LV, Ng D, Goodfellow NM, Yee KT, Lambe EK, Salter MW (2011) Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors. Nat Med 17:470-478. CrossRef Medline
39. Quintes S, Goebbels S, Saher G, Schwab MH, Nave KA (2010) Neuron-glia signaling and the protection of axon function by Schwann cells. J Peripher Nerv Syst 15:10-16. CrossRef Medline
40. Sandrock AW Jr, Dryer SE, Rosen KM, Gozani SN, Kramer R, Theill LE, Fischbach GD (1997) Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science 276:599-603. CrossRef Medline
41. Schäfer MK, Eiden LE, Weihe E (1998) Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter: I. Central nervous system. Neuroscience 84:331-359. CrossRef Medline
42. Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, Janssen MJ, Buonanno A (2012) The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J Neurosci 32:2988-2997. CrossRef Medline
43. Stefanis NC, Hatzimanolis A, Smyrnis N, Avramopoulos D, Evdokimidis I, van Os J, Stefanis CN, Straub RE, Weinberger DR (2013) Schizophrenia candidate gene ERBB4: covert routes of vulnerability to psychosis detected at the population level. Schizophr Bull 39:349-357. CrossRef Medline
44. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J, Gunnarsdottir S, Ivarsson O, Chou TT, Hjaltason O, Birgisdottir B, Jonsson H, Gudnadottir VG, Gudmundsdottir E, Bjornsson A, Ingvarsson B, Ingason A, Sigfusson S, Hardardottir H, et al. (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71:877-892. CrossRef Medline
45. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681-694. CrossRef Medline
46. Ting AK, Chen Y, Wen L, Yin DM, Shen C, Tao Y, Liu X, Xiong WC, Mei L (2011) Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. J Neurosci 31:15-25. CrossRef Medline
47. Tsvetkov E, Shin RM, Bolshakov VY (2004) Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron 41:139-151. CrossRef Medline
48. Wenk GL (1997) The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol LearnMem 67:85-95. CrossRef Medline
49. Wolpowitz D, Mason TB, Dietrich P, Mendelsohn M, Talmage DA, Role LW (2000) Cysteine-rich domain isoforms of the neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron 25:79-91. CrossRef Medline
50. Yang X, Kuo Y, Devay P, Yu C, Role L (1998) A cysteine-rich isoform of neuregulin controls the level of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20:255-270. CrossRef Medline
51. Zhong C, Du C, Hancock M, Mertz M, Talmage DA, Role LW (2008) Presynaptic type III neuregulin 1 is required for sustained enhancement of hippocampal transmission by nicotine and for axonal targeting of α7 nicotinic acetylcholine receptors. J Neurosci 28:9111-9116. CrossRef Medline