Donut-like topology of synaptic vesicles with a central cluster of mitochondria wrapped into membrane protrusions: A novel structure-function module of the adult calyx of held

Journal of Neuroscience

Volumn 26, Issue 1, 2006, Pages 109-116

  Wimmer, Verena C ^a   Horstmann, Heinz ^a   Groh, Alexander ^a   Kuner, Thomas ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

3D reconstruction; Mitochondrial function; Presynaptic mechanisms; Synaptic transmission; Synaptic vesicle topology; Viral gene transfer

Indexed keywords

GREEN FLUORESCENT PROTEIN; ION CHANNEL; SYNAPTOPHYSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; CALYX OF HELD; ELECTRON MICROSCOPY; FLUORESCENCE; GENE TRANSFER; HEARING; MITOCHONDRION; NONHUMAN; POSTNATAL DEVELOPMENT; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; THREE DIMENSIONAL IMAGING; VIRUS GENE;

AGE FACTORS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; CELL MEMBRANE; COCHLEAR NERVE; COCHLEAR NUCLEUS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PSEUDOPODIA; RATS; RATS, SPRAGUE-DAWLEY; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPTIC VESICLES;

EID: 30644467361     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3268-05.2006     Document Type: Article

References (37)

1. Billups B, Forsythe ID (2002) Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 22:5840-5847.
2. Blatchley BJ, Cooper WA, Coleman JR (1987) Development of auditory brainstem response to tone pip stimuli in the rat. Brain Res 429:75-84.
3. Borst JG, Helmchen F, Sakmann B (1995) Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol (Lond) 489:825-840.
4. Brodin L, Bakeeva L, Shupliakov O (1999) Presynaptic mitochondria and the temporal pattern of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:365-372.
5. de Felipe P, Martin V, Cortes ML, Ryan M, Izquierdo M (1999) Use of the 2A sequence from foot-and-mouth disease virus in the generation of retroviral vectors for gene therapy. Gene Ther 6:198-208.
6. de Lange RP, de Roos AD, Borst JG (2003) Two modes of vesicle recycling in the rat calyx of Held. J Neurosci 23:10164-10173.
7. Fiala JC, Harris KM (1999) Dendritic structure. In: Dendrites (Stuart G, Sprouston N, Haüsser M, eds), 1-34. Oxford: Oxford UP.
8. Hayashi Y, Majewska AK (2005) Dendritic spine geometry: functional implication and regulation. Neuron 46:529-532.
9. Helmchen F, Borst JG, Sakmann B (1997) Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72:1458-1471.
10. Hollenbeck PJ (2005) Mitochondria and neurotransmission: evacuating the synapse. Neuron 47:331-333.
11. Kandler K, Friauf E (1993) Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328:161-184.
12. 2+ clearance at the calyx of Held. J Neurosci 25:6057-6065.
13. King MJ, Atwood HL, Govind CK (1996) Structural features of crayfish phasic and tonic neuromuscular terminals. J Comp Neurol 372:618-626.
14. Kirkeby S, Moe D, Bog-Hansen TC, van Noorden CJ (1993) Biotin carboxylases in mitochondria and the cytosol from skeletal and cardiac muscle as detected by avidin binding. Histochemistry 100:415-421.
15. Kuromi H, Kidokoro Y (1998) Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20:917-925.
16. Leao RM, Kushmerick C, Pinaud R, Renden R, Li GL, Taschenberger H, Spirou G, Levinson SR, von Gersdorff H (2005) Presynaptic Na channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J Neurosci 25:3724-3738.
17. Lisenbee CS, Karnik SK, Trelease RN (2003) Overexpression and mislocalization of a tail-anchored GFP redefines the identity of peroxisomal ER. Traffic 4:491-501.
18. Matsushita K, Morrell CN, Cambien B, Yang SX, Yamakuchi M, Bao C, Hara MR, Quick RA, Cao W, O'Rourke B, Lowenstein JM, Pevsner J, Wagner DD, Lowenstein CJ (2003) Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor. Cell 115:139-150.
19. Matsushita K, Morrell CN, Mason RJ, Yamakuchi M, Khanday FA, Irani K, Lowenstein CJ (2005) Hydrogen peroxide regulation of endothelial exocytosis by inhibition of N-ethylmaleimide sensitive factor. J Cell Biol 170:73-79.
20. McAlpine D (2005) Creating a sense of auditory space. J Physiol (Lond) 566:21-28.
21. Morest DK (1968) The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Z Anat Entwicklungsgesch 127:201-220.
22. Muller M, Mironov SL, Ivannikov MV, Schmidt J, Richter DW (2005) Mitochondrial organization and motility probed by two-photon microscopy in cultured mouse brainstem neurons. Exp Cell Res 303:114-127.
23. Polyakov VY, Soukhomlinova MY, Fais D (2003) Fusion, fragmentation, and fission of mitochondria. Biochemistry (Mosc) 68:838-849.
24. Renden R, Taschenberger H, Puente N, Rusakov DA, Duvoisin R, Wang LY, Lehre KP, von Gersdorff H (2005) Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of Held synapses. J Neurosci 25:8482-8497.
25. Reuss S (2000) Introduction to the superior olivary complex. Microsc Res Tech 51:303-306.
26. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57-69.
27. Rouiller EM, Cronin-Schreiber R, Fekete DM, Ryugo DK (1986) The central projections of intracellularly labeled auditory nerve fibers in cats: an analysis of terminal morphology. J Comp Neurol 249:261-278.
28. Rowland KC, Irby NK, Spirou GA (2000) Specialized synapse-associated structures within the calyx of Held. J Neurosci 20:9135-9144.
29. Sätzler K, Sohl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lubke JH (2002) 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.
30. Skulachev VP (2001) Mitochondrial filaments and clusters as intracellular power-transmitting cables. Trends Biochem Sci 26:23-29.
31. Sudhof TC (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-653.
32. Svoboda K, Tank DW, Denk W (1996) Direct measurement of coupling between dendritic spines and shafts. Science 272:716-719.
33. Szebenyi G, Smith GM, Li P, Brady ST (2002) Overexpression of neurofilament H disrupts normal cell structure and function. J Neurosci Res 68:185-198.
34. Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173.
35. Taschenberger H, Leao RM, Rowland KC, Spirou GA, von Gersdorff H (2002) Optimizing synaptic architecture and efficiency for highfrequency transmission. Neuron 36:1127-1143.
36. von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53-64.
37. Wimmer VC, Nevian T, Kuner T (2004) Targeted in vivo expression of proteins in the calyx of Held. Pflügers Arch 449:319-333.