Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells

Nature Neuroscience

Volumn 10, Issue 10, 2007, Pages 1268-1276

  Midorikawa, Mitsuharu ^a,d   Tsukamoto, Yoshihiko ^b   Berglund, Ken ^a,c   Ishii, Masaaki ^b   Tachibana, Masao ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b HYOGO COLLEGE OF MEDICINE   (Japan)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM ION; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CURRENT; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVATION; GOLDFISH; NONHUMAN; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; SENSORY NERVE CELL; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

ANALYSIS OF VARIANCE; ANIMALS; BICUCULLINE; CALCIUM; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ENZYME INHIBITORS; GABA ANTAGONISTS; GOLDFISH; IMAGING, THREE-DIMENSIONAL; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C-ALPHA; RETINA; RETINAL BIPOLAR CELLS; SYNAPSES; SYNAPTIC VESICLES; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS;

EID: 34748865486     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1963     Document Type: Article

References (39)

1. von Gersdorff, H., Vardi, E., Matthews, G. & Sterling, P. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 16, 1221-1227 (1996).
2. Lenzi, D., Crum, J., Ellisman, M.H. & Roberts, W.M. Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 36, 649-659 (2002).
3. tom Dieck, S. et al. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 168, 825-836 (2005).
4. Lenzi, D. & von Gersdorff, H. Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines. Bioessays 23, 831-840 (2001).
5. Zhai, R.G. & Bellen, H.J. The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19, 262-270 (2004).
6. Dowling, J.E. The Retina: an Approachable Part of the Brain (Harvard Univ. Press, Cambridge, Massachusetts, 1987).
7. Zenisek, D., Davila, V., Wan, L. & Almers, W. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J. Neurosci. 23, 2538-2548 (2003).
8. Zenisek, D., Horst, N.K., Merrifield, C., Sterling, P. & Matthews, G. Visualizing synaptic ribbons in the living cell. J. Neurosci. 24, 9752-9759 (2004).
9. Zenisek, D., Steyer, J.A. & Almers, W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406, 849-854 (2000).
10. Zenisek, D., Steyer, J.A., Feldman, M.E. & Almers, W. A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 35, 1085-1097 (2002).
11. Llobet, A., Cooke, A. & Lagnado, L. Exocytosis at the ribbon synapse of retinal bipolar cells studied in patches of presynaptic membrane. J. Neurosci. 23, 2706-2714 (2003).
12. Mennerick, S. & Matthews, G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17, 1241-1249 (1996).
13. Sakaba, T., Tachibana, M., Matsui, K. & Minami, N. Two components of transmitter release in retinal bipolar cells: exocytosis and mobilization of synaptic vesicles. Neurosci. Res. 27, 357-370 (1997).
14. von Gersdorff, H., Sakaba, T., Berglund, K. & Tachibana, M. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21, 1177-1188 (1998).
15. Suzuki, S. & Kaneko, A. Identification of bipolar cell subtypes by protein kinase C-like immunoreactivity in the goldfish retina. Vis. Neurosci. 5, 223-230 (1990).
16. Osborne, N.N., Wood, J. & Groome, N. The occurrence of three calcium-independent protein kinase C subspecies (delta, epsilon and zeta) in retina of different species. Brain Res. 637, 156-162 (1994).
17. Minami, N., Berglund, K., Sakaba, T., Kohmoto, H. & Tachibana, M. Potentiation of transmitter release by protein kinase C in goldfish retinal bipolar cells. J. Physiol. (Lond.) 512, 219-225 (1998).
18. Berglund, K., Midorikawa, M. & Tachibana, M. Increase in the pool size of releasable synaptic vesicles by the activation of protein kinase C in goldfish retinal bipolar cells. J. Neurosci. 22, 4776-4785 (2002).
19. von Gersdorff, H. Synaptic ribbons: versatile signal transducers. Neuron 29, 7-10 (2001).
20. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399 (1998).
21. Tachibana, M., Okada, T., Arimura, T., Kobayashi, K. & Piccolino, M. Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. J. Neurosci. 13, 2898-2909 (1993).
22. Steyer, J.A. & Almers, W. Tracking single secretory granules in live chromaffin cells by evanescent-field fluorescence microscopy. Biophys. J. 76, 2262-2271 (1999).
23. Becherer, U., Moser, T., Stuhmer, W. & Oheim, M. Calcium regulates exocytosis at the level of single vesicles. Nat. Neurosci. 6, 846-853 (2003).
24. Diggle, P.J. Statistical Analysis of Spatial Point Patterns (Arnold, London, 2003).
25. Allen, M.B. Structure, physiology, and biochemistry of the chryophyceae. Annu. Rev. Microbiol. 23, 29-46 (1969).
26. Hull, C., Studholme, K., Yazulla, S. & von Gersdorff, H. Diurnal changes in exocytosis and the number of synaptic ribbons at active zones of an ON-type bipolar cell terminal. J. Neurophysiol. 96, 2025-2033 (2006).
27. Raviola, E. & Raviola, G. Structure of the synaptic membranes in the inner plexiform layer of the retina: a freeze-fracture study in monkeys and rabbits. J. Comp. Neurol. 209, 233-248 (1982).
28. Roberts, W.M., Jacobs, R.A. & Hudspeth, A.J. The hair cell as a presynaptic terminal. Ann. NY Acad. Sci. 635, 221-233 (1991).
29. von Gersdorff, H. & Matthews, G. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J. Neurosci. 17, 1919-1927 (1997).
30. Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513-515 (1994).
31. Heidelberger, R. Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. J. Gen. Physiol. 111, 225-241 (1998).
32. C receptors in rat retinal bipolar cells by protein kinase C. J. Physiol. (Lond.) 481, 325-330 (1994).
33. A currents in rabbit retinal rod bipolar cells. J. Neurophysiol. 76, 3070-3086 (1996).
34. Job, C. & Lagnado, L. Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells. J. Cell Biol. 143, 1661-1672 (1998).
35. Khimich, D. et al. Hair cell synaptic ribbons are essential for synchronous auditory signaling. Nature 434, 889-894 (2005).
36. Dick, O. et al. The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37, 775-786 (2003).
37. Ball, S.L. et al. Role of the β2 subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Invest. Ophthalmol. Vis. Sci. 43, 1595-1603 (2002).
38. Tachibana, M. & Okada, T. Release of endogenous excitatory amino acids from ON-type bipolar cells isolated from the goldfish retina. J. Neurosci. 11, 2199-2208 (1991).
39. Suzuki, S., Tachibana, M. & Kaneko, A. Effects of glycine and GABA on isolated bipolar cells of the mouse retina. J. Physiol. (Lond.) 421, 645-662 (1990).