Synaptotagmin IV determines the linear Ca 2+ dependence of vesicle fusion at auditory ribbon synapses

Nature Neuroscience

Volumn 13, Issue 1, 2010, Pages 45-52

  Johnson, Stuart L ^a   Franz, Christoph ^b   Kuhn, Stephanie ^a,c   Furness, David N ^c   Rüttiger, Lukas ^b   Münkner, Stefan ^c,d   Rivolta, Marcelo N ^a   Seward, Elizabeth P ^a   Herschman, Harvey R ^e   Engel, Jutta ^c,d   Knipper, Marlies ^b   Marcotti, Walter ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c KEELE UNIVERSITY   (United Kingdom)

^d SAARLAND UNIVERSITY   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; NEUROTRANSMITTER; SYNAPTOTAGMIN; SYNAPTOTAGMIN I; SYNAPTOTAGMIN II; SYNAPTOTAGMIN IV; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; AUDITORY CORTEX; COCHLEA; CONTROLLED STUDY; EXOCYTOSIS; GERBIL; HAIR CELL; MEMBRANE FUSION; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RODENT; SENSOR; SPIKE; SYNAPSE; SYNAPSE VESICLE; VISUAL SYSTEM; AGE; ANIMAL; BIOPHYSICS; CATTLE; CELL CULTURE; CELL MEMBRANE POTENTIAL; CHROMAFFIN CELL; CYTOLOGY; ELECTROSTIMULATION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; METABOLISM; METHODOLOGY; MOUSE MUTANT; NEWBORN; PATCH CLAMP; PHYSIOLOGY; RAT; STATISTICAL MODEL; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WISTAR RAT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CALCIUM; CATTLE; CELLS, CULTURED; CHROMAFFIN CELLS; COCHLEA; ELECTRIC STIMULATION; EXOCYTOSIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERBILLINAE; GREEN FLUORESCENT PROTEINS; HAIR CELLS, AUDITORY; LINEAR MODELS; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC VESICLES; SYNAPTOTAGMIN I; SYNAPTOTAGMIN II; SYNAPTOTAGMINS; TIME FACTORS; TRANSFECTION;

EID: 73949120302     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2456     Document Type: Article

References (50)

1. Fuchs, P.A. Time and intensity coding at the hair cell's ribbon synapse. J. Physiol. (Lond.) 566, 7-12 (2005).
2. Moser, T., Neef, A. & Khimich, D. Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J. Physiol. (Lond.) 576, 55-62 (2006).
3. Juusola, M., French, A.S., Uusitalo, R.O. & Weckström, M. Information processing by graded-potential transmission through tonically active synapses. Trends Neurosci. 19, 292-297 (1996).
4. Sterling, P. & Matthews, G. Structure and function of ribbon synapses. Trends Neurosci. 28, 20-29 (2005).
5. Glowatzki, E. & Fuchs, P.A. Transmitter release at the hair cell ribbon synapse. Nat. Neurosci. 5, 147-154 (2002).
6. Singer, J.H., Lassová, L., Vardi, N. & Diamond, J.S. Coordinated multivesicular release at a mammalian ribbon synapse. Nat. Neurosci. 7, 826-833 (2004).
7. 2+ dependence of exocytosis during development of mouse inner hair cells. J. Physiol. (Lond.) 563, 177-191 (2005).
8. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595-605 (2004).
9. Johnson, S.L., Forge, A., Knipper, M., Münkner, S. & Marcotti, W. Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. J. Neurosci. 28, 7670-7678 (2008).
10. K,n contributes to maturation of the mouse outer hair cells. J. Physiol. (Lond.) 520, 653-660 (1999). (Pubitemid 29533025)
11. Beurg, M. et al. Calcium-and otoferlin-dependent exocytosis by immature outer hair cells. J. Neurosci. 28, 1798-1803 (2008).
12. Johnson, S.L., Franz, C., Knipper, M. & Marcotti, W. Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses. J. Physiol. (Lond.) 587, 1715-1726 (2009).
13. Lenzi, D. & von Gersdorff, H. Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines. Bioessays 23, 831-840 (2001).
14. Glowatzki, E., Grant, L. & Fuchs, P.A. Hair cell afferent synapses. Curr. Opin. Neurobiol. 18, 389-395 (2008).
15. Safeddine, S. & Wenthold, R.J. SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle-and synaptic membrane-associated proteins. Eur. J. Neurosci. 11, 803-812 (1999).
16. Südhof, T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547 (2004).
17. Roux, I. et al. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127, 277-289 (2006).
18. + channels in rodent inner hair cells. J. Neurosci. 27, 3174-3186 (2007).
19. Heidrych, P. et al. Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Hum. Mol. Genet. 18, 2779-2790 (2009).
20. Südhof, T.C. Synaptotagmins: why so many? J. Biol. Chem. 277, 7629-7632 (2002).
21. Dean, C. et al. Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat. Neurosci. 12, 767-776 (2009).
22. Littleton, J.T., Serano, T.L., Rubin, G.M., Ganetzky, B. & Chapman, E.R. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature 400, 757-760 (1999).
23. Zhang, Q., Fukuda, M., Van Bockstaele, E., Pascual, O. & Haydon, P.G. Synaptotagmin IV regulates glial glutamate release. Proc. Natl. Acad. Sci. USA 101, 9441-9446 (2004).
24. Ferguson, G.D., Anagnostaras, S.G., Silva, A.J. & Herschman, H.R. Defcits in memory and motor performance in synaptotagmin IV mutant mice. Proc. Natl. Acad. Sci. USA 97, 5598-5603 (2000).
25. V1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J. Neurosci. 25, 11577-11585 (2005).
26. Sobkowicz, H.M., Rose, J.E., Scott, G.E. & Slapnick, S.M. Ribbon synapses in the developing intact and cultured organ of Corti in the mouse. J. Neurosci. 2, 942-957 (1982).
27. Dallos, P. The active cochlea. J. Neurosci. 12, 4575-4585 (1992).
28. 2+ channels in mature outer hair cells supports outer hair cell afferent signaling. J. Neurosci. 27, 6442-6451 (2007).
29. 2+ dependence of exocytosis. J. Physiol. (Lond.) 583, 631-646 (2007).
30. Dulon, D., Safeddine, S., Jones, S.M. & Petit, C. Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J. Neurosci. 29, 10474-10487 (2009).
31. 2+ binding to synaptotagmin-1 C2 domains mediate neurotransmitter release. Proc. Natl. Acad. Sci. USA 106, 16469-16474 (2009).
32. Vician, L. et al. Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc. Natl. Acad. Sci. USA 92, 2164-2168 (1995).
33. Ting, J.T., Kelley, B.G. & Sullivan, J.M. Synaptotagmin IV does not alter excitatory fast synaptic transmission or fusion pore kinetics in mammalian CNS neurons. J. Neurosci. 26, 372-380 (2006).
34. Murphy, G.J., Glickfeld, L.L., Balsen, Z. & Isaacson, J.S. Sensory neuron signaling to the brain: properties of transmitter release from olfactory nerve terminals. J. Neurosci. 24, 3023-3030 (2004).
35. Zhang, Z., Bhalla, A., Dean, C., Chapman, E.R. & Jackson, M.B. Synaptotagmin IV: a multifunctional regulator of peptidergic nerve terminals. Nat. Neurosci. 12, 163-171 (2009).
36. Wang, C.-T. et al. Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424, 943-947 (2003).
37. 2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418, 340-344 (2002).
38. 2+ sensor for transmitter release at a central synapse. Cell 79, 717-727 (1994).
39. 2+ triggering of neurotransmitter release in central and neuromuscular synapses. J. Neurosci. 26, 13493-13504 (2006).
40. Littleton, J.T., Stern, M., Perin, M. & Bellen, H.J. Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc. Natl. Acad. Sci. USA 91, 10888-10892 (1994).
41. Chapman, E.R., Desai, R.C., Davis, A.F. & Tornehl, C.K. Delineation of the oligomerization, AP-2 binding and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273, 32966-32972 (1998).
42. Thomas, D.M., Ferguson, G.D., Herschman, H.R. & Elferink, L.A. Functional and biochemical analysis of the C2 domains of synaptotagmin IV. Mol. Biol. Cell 10, 2285-2295 (1999).
43. Stevens, C.F. & Sullivan, J.M. The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39, 299-308 (2003).
44. Nagy, G. et al. Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26, 632-643 (2006).
45. 2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567-581 (2007).
46. Moody, W.J. & Bosma, M.M. Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol. Rev. 85, 883-941 (2005).
47. 2+ transients. Nature 375, 784-787 (1995).
48. Marcotti, W., Johnson, S.L., Holley, M.C. & Kros, C.J. Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. J. Physiol. (Lond.) 548, 383-400 (2003).
49. Lenzi, D., Runyeon, J.W., Crum, J., Ellisman, M.K. & Roberts, W.M. Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J. Neurosci. 19, 119-132 (1999).
50. Furness, D.N. & Hackney, C.M. Cross-links between stereocilia in the guinea pig cochlea. Hear. Res. 18, 177-188 (1985).