BMP signaling specifies the development of a large and fast CNS synapse

Nature Neuroscience

Volumn 16, Issue 7, 2013, Pages 856-864

  Xiao, Le ^a,c   Michalski, Nicolas ^a,d   Kronander, Elin ^a   Gjoni, Enida ^a   Genoud, Christel ^b   Knott, Graham ^a   Schneggenburger, Ralf ^a  

^a EPFL   (Switzerland)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; BONE MORPHOGENETIC PROTEIN RECEPTOR 1B; CALCIUM BINDING PROTEIN; COMPLEMENTARY DNA; SMAD1 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SYNAPTOTAGMIN II; VESICULAR GLUTAMATE TRANSPORTER 2; BMPR1A PROTEIN, MOUSE; BMPR1B PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; EARLY GROWTH RESPONSE FACTOR 2; EGR2 PROTEIN, MOUSE; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; BRAIN ELECTROPHYSIOLOGY; CENTRAL NERVOUS SYSTEM; COCHLEAR NUCLEUS; CONTROLLED STUDY; DROSOPHILA; ELECTRON MICROSCOPY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE DELETION; GENETIC ASSOCIATION; GENOTYPE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; AGE; ANIMAL; C57BL MOUSE; CEREBELLUM; CYTOLOGY; DEFICIENCY; ELECTROSTIMULATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; NEWBORN; PHYSIOLOGY; RHOMBENCEPHALON; SYNAPSE; TRANSGENIC MOUSE; ULTRASTRUCTURE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CALCIUM-BINDING PROTEINS; CENTRAL NERVOUS SYSTEM; CEREBELLUM; EARLY GROWTH RESPONSE PROTEIN 2; ELECTRIC STIMULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN VITRO TECHNIQUES; INHIBITORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84891685800     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3414     Document Type: Article

References (55)

1. Sanes, J.R. & Yamagata, M. Many paths to synaptic specificity. Annu. Rev. Cell Dev. Biol. 25, 161-195 (2009).
2. Walmsley, B., Alvarez, F.J. & Fyffe, R.E.W. Diversity of structure and function at mammalian central synapses. Trends Neurosci. 21, 81-88 (1998).
3. Sherman, S.M. & Guillery, R.W. On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators" . Proc. Natl. Acad. Sci. USA 95, 7121-7126 (1998).
4. Borst, J.G. & Soria van Hoeve, J. The calyx of held synapse: from model synapse to auditory relay. Annu. Rev. Physiol. 74, 199-224 (2012).
5. Sätzler, K. et al. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J. Neurosci. 22, 10567-10579 (2002).
6. Bergsman, J.B., De Camilli, P. & McCormick, D.A. Multiple large inputs to principal cells in the mouse medial nucleus of the trapezoid body. J. Neurophysiol. 92, 545-552 (2004).
7. Rodríguez-Contreras, A., de Lange, R.P.J., Lucassen, P.J. & Borst, J.G.G. Branching of calyceal afferents during postnatal development in the rat auditory brainstem. J. Comp. Neurol. 496, 214-228 (2006).
8. Cant, N.B. & Benson, C.G. Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res. Bull. 60, 457-474 (2003).
9. Case, D.T., Zhao, X. & Gillespie, D.C. Functional refinement in the projection from ventral cochlear nucleus to lateral superior olive precedes hearing onset in rat. PLoS ONE 6, e20756 (2011).
10. Grothe, B., Pecka, M. & McAlpine, D. Mechanisms of sound localization in mammals. Physiol. Rev. 90, 983-1012 (2010).
11. Hoffpauir, B.K., Grimes, J.L., Mathers, P.H. & Spirou, G.A. Synaptogenesis of the calyx of Held: rapid onset of function and one-to-one morphological innervation. J. Neurosci. 26, 5511-5523 (2006).
12. Rodríguez-Contreras, A., van Hoeve, J.S., Habets, R.L., Locher, H. & Borst, J.G. Dynamic development of the calyx of Held synapse. Proc. Natl. Acad. Sci. USA 105, 5603-5608 (2008).
13. Hoffpauir, B.K., Kolson, D.R., Mathers, P.H. & Spirou, G.A. Maturation of synaptic partners: functional phenotype and synaptic organization tuned in synchrony. J. Physiol. (Lond.) 588, 4365-4385 (2010).
14. Erazo-Fischer, E., Striessnig, J. & Taschenberger, H. The role of physiological afferent nerve activity during in vivo maturation of the calyx of Held synapse. J. Neurosci. 27, 1725-1737 (2007).
15. Taschenberger, H. & von Gersdorff, H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J. Neurosci. 20, 9162-9173 (2000).
16. Chuhma, N., Koyano, K. & Ohmori, H. Synchronisation of neurotransmitter release during postnatal development in a calyceal presynaptic terminal of rat. J. Physiol. (Lond.) 530, 93-104 (2001).
17. Futai, K., Okada, M., Matsuyama, K. & Takahashi, T. High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J. Neurosci. 21, 3342-3349 (2001).
18. Koike-Tani, M., Saitoh, N. & Takahashi, T. Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J. Neurosci. 25, 199-207 (2005).
19. Yang, Y.M. et al. GluA4 is indispensable for driving fast neurotransmission across a high-fidelity central synapse. J. Physiol. (Lond.) 589, 4209-4227 (2011).
20. Toyoshima, M. et al. Deficiency of neural recognition molecule NB-2 affects the development of glutamatergic auditory pathways from the ventral cochlear nucleus to the superior olivary complex in mouse. Dev. Biol. 336, 192-200 (2009).
21. Aberle, H. et al. Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33, 545-558 (2002).
22. Marqués, G. et al. The Drosophila BMP type II receptor Wishful Thinking regulates neuromuscular synapse morphology and function. Neuron 33, 529-543 (2002).
23. McCabe, B.D. et al. The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39, 241-254 (2003).
24. Miyazono, K., Kamiya, Y. & Morikawa, M. Bone morphogenetic protein receptors and signal transduction. J. Biochem. 147, 35-51 (2010).
25. Rawson, J.M., Lee, M., Kennedy, E.L. & Selleck, S.B. Drosophila neuromuscular synapse assembly and function require the TGF-? type I receptor saxophone and the transcription factor Mad. J. Neurobiol. 55, 134-150 (2003).
26. McCabe, B.D. et al. Highwire regulates presynaptic BMP signaling essential for synaptic growth. Neuron 41, 891-905 (2004).
27. Ball, R.W. et al. Retrograde BMP signaling controls synaptic growth at the NMJ by regulating trio expression in motor neurons. Neuron 66, 536-549 (2010).
28. Kalinovsky, A. et al. Development of axon-target specificity of ponto-cerebellar afferents. PLoS Biol. 9, e1001013 (2011).
29. Liem, K.F. Jr., Tremml, G., Roelink, H. & Jessell, T.M. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979 (1995).
30. Zhang, D., Mehler, M.F., Song, Q. & Kessler, J.A. Development of bone morphogenetic protein receptors in the nervous system and possible roles in regulating trkC expression. J. Neurosci. 18, 3314-3326 (1998).
31. Bond, A.M., Bhalala, O.G. & Kessler, J.A. The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Dev. Neurobiol. 72, 1068-1084 (2012).
32. Graham, A., Francis-West, P., Brickell, P. & Lumsden, A. The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 372, 684-686 (1994).
33. Augsburger, A., Schuchardt, A., Hoskins, S., Dodd, J. & Butler, S. BMPs as mediators of roof plate repulsion of commissural neurons. Neuron 24, 127-141 (1999).
34. Miyagi, M. et al. Bone morphogenetic protein receptor expressions in the adult rat brain. Neuroscience 176, 93-109 (2011); erratum 183, 278 (2011).
35. Carulli, D. et al. Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J. Comp. Neurol. 494, 559-577 (2006).
36. Peterson, R.S. et al. CD44 modulates Smad1 activation in the BMP-7 signaling pathway. J. Cell Biol. 166, 1081-1091 (2004).
37. Mishina, Y., Hanks, M.C., Miura, S., Tallquist, M.D. & Behringer, R.R. Generation of Bmpr/Alk3 conditional knockout mice. Genesis 32, 69-72 (2002).
38. Voiculescu, O., Charnay, P. & Schneider-Maunoury, S. Expression pattern of a Krox-20/Cre knock-in allele in the developing hindbrain, bones, and peripheral nervous system. Genesis 26, 123-126 (2000).
39. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69, 304-316 (2011).
40. Yi, S.E., Daluiski, A., Pederson, R., Rosen, V. & Lyons, K.M. The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127, 621-630 (2000).
41. Schneggenburger, R., Meyer, A.C. & Neher, E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23, 399-409 (1999).
42. Denk, W. & Horstmann, H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329 (2004).
43. Kim, G. & Kandler, K. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat. Neurosci. 6, 282-290 (2003).
44. Koehl, A. et al. Gene expression profiling of the rat superior olivary complex using serial analysis of gene expression. Eur. J. Neurosci. 20, 3244-3258 (2004).
45. Friedland, D.R., Popper, P., Eernisse, R. & Cioffi, J.A. Differentially expressed genes in the rat cochlear nucleus. Neuroscience 142, 753-768 (2006).
46. Ji, S.J. & Jaffrey, S.R. Intra-axonal translation of SMAD1/5/8 mediates retrograde regulation of trigeminal ganglia subtype specification. Neuron 74, 95-107 (2012).
47. Foletta, V.C. et al. Direct signaling by the BMP type II receptor via the cytoskeletal regulator LIMK1. J. Cell Biol. 162, 1089-1098 (2003); erratum 163, 421 (2003).
48. Lee-Hoeflich, S.T. et al. Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO J. 23, 4792-4801 (2004).
49. Eaton, B.A. & Davis, G.W. LIM Kinase1 controls synaptic stability downstream of the type II BMP receptor. Neuron 47, 695-708 (2005).
50. Ruediger, S. et al. Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473, 514-518 (2011).
51. Farago, A.F., Awatramani, R.B. & Dymecki, S.M. Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50, 205-218 (2006).
52. Renier, N. et al. Genetic dissection of the function of hindbrain axonal commissures. PLoS Biol. 8, e1000325 (2010).
53. Meyer, A.C., Neher, E. & Schneggenburger, R. Estimation of quantal size and number of functional active zones at the calyx of Held synapse by nonstationary EPSC variance analysis. J. Neurosci. 21, 7889-7900 (2001).
54. Xiao, L. et al. Developmental expression of Synaptotagmin isoforms in single calyx of Held-generating neurons. Mol. Cell Neurosci. 44, 374-385 (2010).
55. Knott, G.W., Quairiaux, C., Genoud, C. & Welker, E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34, 265-273 (2002).