Semaphorin 3E-Plexin-D1 Signaling Controls Pathway-specific Synapse Formation in the Striatum

Overview

Journal Nat Neurosci

Date 2011 Dec 20

PMID 22179111

Citations 68

Authors

Jun B Ding

Won-Jong Oh

Bernardo L Sabatini

Chenghua Gu

Affiliations

Soon will be listed here.

Abstract

The proper formation of synaptic connectivity in the mammalian brain is critical for complex behavior. In the striatum, balanced excitatory synaptic transmission from multiple sources onto two classes of principal neurons is required for coordinated and voluntary motor control. Here we show that the interaction between the secreted semaphorin 3E (Sema3E) and its receptor Plexin-D1 is a critical determinant of synaptic specificity in cortico-thalamo-striatal circuits in mice. We find that Sema3e (encoding Sema3E) is highly expressed in thalamostriatal projection neurons, whereas in the striatum Plxnd1 (encoding Plexin-D1) is selectively expressed in direct-pathway medium spiny neurons (MSNs). Despite physical intermingling of the MSNs, genetic ablation of Plxnd1 or Sema3e results in functional and anatomical rearrangement of thalamostriatal synapses specifically in direct-pathway MSNs without effects on corticostriatal synapses. Thus, our results demonstrate that Sema3E and Plexin-D1 specify the degree of glutamatergic connectivity between a specific source and target in the complex circuitry of the basal ganglia.

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References

Micheva K, Smith S . Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron. 2007; 55(1):25-36. PMC: 2080672. DOI: 10.1016/j.neuron.2007.06.014. View

Yamagata M, Sanes J . Synaptic localization and function of Sidekick recognition molecules require MAGI scaffolding proteins. J Neurosci. 2010; 30(10):3579-88. PMC: 2863080. DOI: 10.1523/JNEUROSCI.6319-09.2010. View

Johnson-Venkatesh E, Umemori H . Secreted factors as synaptic organizers. Eur J Neurosci. 2010; 32(2):181-90. PMC: 4127169. DOI: 10.1111/j.1460-9568.2010.07338.x. View

Chauvet S, Cohen S, Yoshida Y, Fekrane L, Livet J, Gayet O . Gating of Sema3E/PlexinD1 signaling by neuropilin-1 switches axonal repulsion to attraction during brain development. Neuron. 2007; 56(5):807-22. PMC: 2700040. DOI: 10.1016/j.neuron.2007.10.019. View

Surmeier D, Song W, Yan Z . Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci. 1996; 16(20):6579-91. PMC: 6578920. View

Raju D, Shah D, Wright T, Hall R, Smith Y . Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J Comp Neurol. 2006; 499(2):231-43. PMC: 2571956. DOI: 10.1002/cne.21099. View

Graybiel A, Aosaki T, Flaherty A, Kimura M . The basal ganglia and adaptive motor control. Science. 1994; 265(5180):1826-31. DOI: 10.1126/science.8091209. View

Gu C, Yoshida Y, Livet J, Reimert D, Mann F, Merte J . Semaphorin 3E and plexin-D1 control vascular pattern independently of neuropilins. Science. 2004; 307(5707):265-8. DOI: 10.1126/science.1105416. View

Wickens J, Reynolds J, Hyland B . Neural mechanisms of reward-related motor learning. Curr Opin Neurobiol. 2003; 13(6):685-90. DOI: 10.1016/j.conb.2003.10.013. View

10.

Tran T, Rubio M, Clem R, Johnson D, Case L, Tessier-Lavigne M . Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature. 2009; 462(7276):1065-9. PMC: 2842559. DOI: 10.1038/nature08628. View

11.

Shen K, Fetter R, Bargmann C . Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell. 2004; 116(6):869-81. DOI: 10.1016/s0092-8674(04)00251-x. View

12.

Rakic P, Bourgeois J, Eckenhoff M, Zecevic N, Goldman-Rakic P . Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science. 1986; 232(4747):232-5. DOI: 10.1126/science.3952506. View

13.

Fox M, Sanes J, Borza D, Eswarakumar V, Fassler R, Hudson B . Distinct target-derived signals organize formation, maturation, and maintenance of motor nerve terminals. Cell. 2007; 129(1):179-93. DOI: 10.1016/j.cell.2007.02.035. View

14.

Suto F, Tsuboi M, Kamiya H, Mizuno H, Kiyama Y, Komai S . Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron. 2007; 53(4):535-47. DOI: 10.1016/j.neuron.2007.01.028. View

15.

Albin R, Young A, Penney J . The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989; 12(10):366-75. DOI: 10.1016/0166-2236(89)90074-x. View

16.

Williams M, de Wit J, Ghosh A . Molecular mechanisms of synaptic specificity in developing neural circuits. Neuron. 2010; 68(1):9-18. PMC: 3327884. DOI: 10.1016/j.neuron.2010.09.007. View

17.

Kawaguchi Y, Wilson C, Emson P . Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. J Neurophysiol. 1989; 62(5):1052-68. DOI: 10.1152/jn.1989.62.5.1052. View

18.

Pecho-Vrieseling E, Sigrist M, Yoshida Y, Jessell T, Arber S . Specificity of sensory-motor connections encoded by Sema3e-Plxnd1 recognition. Nature. 2009; 459(7248):842-6. PMC: 2847258. DOI: 10.1038/nature08000. View

19.

Tsai H, Zhang F, Adamantidis A, Stuber G, Bonci A, De Lecea L . Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science. 2009; 324(5930):1080-4. PMC: 5262197. DOI: 10.1126/science.1168878. View

20.

Sanes J, Yamagata M . Many paths to synaptic specificity. Annu Rev Cell Dev Biol. 2009; 25:161-95. DOI: 10.1146/annurev.cellbio.24.110707.175402. View