Synaptotagmin-7 is essential for Ca2+-triggered delayed asynchronous release but not for Ca2+-dependent vesicle priming in retinal ribbon synapses

Journal of Neuroscience

Volumn 35, Issue 31, 2015, Pages 11024-11033

  Luo, Fujun ^a   Bacaj, Taulant ^a   Südhof, Thomas C ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Active zone; Calcium channel; Ribbon synapse; Vesicle fusion

Indexed keywords

CALCIUM ION; EGTAZIC ACID; NEUROTRANSMITTER; SYNAPTOTAGMIN; SYNAPTOTAGMIN 9; SYNAPTOTAGMIN I; SYNAPTOTAGMIN II; UNCLASSIFIED DRUG; CALCIUM;

ADULT; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CONNECTOME; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; FEMALE; GENOTYPE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REPETITION PRIMING; RETINA AMACRINE CELL; RETINA ROD; RETINAL RIBBON SYNAPSE; SYNAPSE; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP; ANIMAL; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; RETINA; RETINA BIPOLAR GANGLION CELL; SYNAPSE VESICLE;

AMACRINE CELLS; ANIMALS; CALCIUM; MICE; MICE, KNOCKOUT; RETINA; RETINAL BIPOLAR CELLS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNAPTOTAGMINS;

EID: 84938808605     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0759-15.2015     Document Type: Article

References (45)

1. Atluri PP, Regehr WG (1998) Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci 18:8214–8227. Medline
2. Babai N, Bartoletti TM, Thoreson WB (2010) Calcium regulates vesicle replenishment at the cone ribbon synapse. J Neurosci 30:15866–15877. CrossRef Medline
3. Bacaj T, Wu D, Yang X, Morishita W, Zhou P, Xu W, Malenka RC, Südhof TC (2013) Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release. Neuron 80:947–959. CrossRef Medline
4. Best AR, Regehr WG (2009) Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA. Neuron 62:555–565. CrossRef Medline
5. Bloomfield SA, Dacheux RF (2001) Rod vision: pathways and processing in the mammalian retina. Prog Retin Eye Res 20:351–384. CrossRef Medline
6. Burrone J, Neves G, Gomis A, Cooke A, Lagnado L (2002) Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron 33:101–112. CrossRef Medline
7. Cho S, Li GL, von Gersdorff H (2011) Recovery from short-term depression and facilitation is ultrafast and Ca2+ dependent at auditory hair cell synapses. J Neurosci 31:5682–5692. CrossRef Medline
8. Daw MI, Tricoire L, Erdelyi F, Szabo G, McBain CJ (2009) Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J Neurosci 29:11112–11122. CrossRef Medline
9. Deák F, Liu X, Khvotchev M, Li G, Kavalali ET, Sugita S, Südhof TC (2009) Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J Neurosci 29:8639-8648. CrossRef Medline
10. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147–6162. Medline
11. Fox MA, Sanes JR (2007) Synaptotagmin I and II are present in distinct subsets of central synapses. J Comp Neurol 503:280–296. CrossRef Medline
12. Gomis A, Burrone J, Lagnado L (1999) Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J Neurosci 19:6309–6317. Medline
13. Gustavsson N, Wei SH, Hoang DN, Lao Y, Zhang Q, Radda GK, Rorsman P, Südhof TC, Han W (2009) Synaptotagmin-7 is a principal Ca2+sensor for Ca2+ -induced glucagon exocytosis in pancreas. J Physiol 587:1169–1178. CrossRef Medline
14. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8:1319–1328. CrossRef Medline
15. Hosoi N, Sakaba T, Neher E (2007) Quantitative analysis of calciumdependent vesicle recruitment and its functional role at the calyx of Held synapse. J Neurosci 27:14286–14298. CrossRef Medline
16. Jarsky T, Tian M, Singer JH (2010) Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. J Neurosci 30:11885–11895. CrossRef Medline
17. Kaeser PS, Deng L, Wang Y, Dulubova I, Liu X, Rizo J, Südhof TC (2011) RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144:282–295. CrossRef Medline
18. Lipstein N, Sakaba T, Cooper BH, Lin KH, Strenzke N, Ashery U, Rhee JS, Taschenberger H, Neher E, Brose N (2013) Dynamic control of synaptic vesicle replenishment and short-term plasticity by Ca(2+)-calmodulin- Munc13-1 signaling. Neuron 10:82–96. CrossRef Medline
19. Liu H, Bai H, Hui E, Yang L, Evans CS, Wang Z, Kwon SE, Chapman ER (2014) Synaptotagmin 7 functions as a Ca2+-sensor for synaptic vesicle replenishment. Elife 3:e01524. CrossRef Medline
20. Maximov A, Südhof TC (2005) Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron 48:547–554. CrossRef Medline
21. Mehta B, Ke JB, Zhang L, Baden AD, Markowitz AL, Nayak S, Briggman KL, Zenisek D, Singer JH (2014) Global Ca2+ signaling drives ribbonindependent synaptic transmission at rod bipolar cell synapses. J Neurosci 34:6233–6244. CrossRef Medline
22. Mennerick S, Matthews G (1996) Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17:1241–1249. CrossRef Medline
23. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59:861–872. CrossRef Medline
24. Oesch NW, Diamond JS (2011) Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat Neurosci 14:1555–1561. CrossRef Medline
25. Protti DA, Llano I (1998) Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. J Neurosci 18:3715–3724. Medline
26. Ramirez DM, Khvotchev M, Trauterman B, Kavalali ET (2012) Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission. Neuron 73:121–134. CrossRef Medline
27. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197–1207. CrossRef Medline
28. Sakaba T, Neher E (2001) Calmodulin mediates rapid recruitment of fastreleasing synaptic vesicles at a calyx-type synapse. Neuron 32:1119–1131. CrossRef Medline
29. Schnee ME, Santos-Sacchi J, Castellano-Muñoz M, Kong JH, Ricci AJ (2011) Calcium-dependent synaptic vesicle trafficking underlies indefatigable release at the hair cell afferent fiber synapse. Neuron 70:326–338. CrossRef Medline
30. Schonn JS, Maximov A, Lao Y, Südhof TC, Sørensen JB (2008) Synaptotagmin-1 and -7 are functionally overlapping Ca2+ sensors for exocytosis in adrenal chromaffin cells. Proc Natl Acad Sci U S A 105: 3998–4003. CrossRef Medline
31. Shin OH, Lu J, Rhee JS, Tomchick DR, Pang ZP, Wojcik SM, Camacho-Perez M, Brose N, Machius M, Rizo J, Rosenmund C, Südhof TC (2010) Munc13 C2B domain is an activity-dependent Ca2+regulator of synaptic exocytosis. Nat Struct Mol Biol 17:280–288. CrossRef Medline
32. Singer JH, Diamond JS (2003) Sustained Ca2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J Neurosci 23:10923–10933. Medline
33. Singer JH, Diamond JS (2006) Vesicle depletion and synaptic depression at a mammalian ribbon synapse. J Neurophysiol 95:3191–3198. CrossRef Medline
34. Snellman J, Mehta B, Babai N, Bartoletti TM, Akmentin W, Francis A, Matthews G, Thoreson W, Zenisek D (2011) Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat Neurosci 14:1135–1141. CrossRef Medline
35. Sterling P, Matthews G (2005) Structure and function of ribbon synapses. Trends Neurosci 28:20–29. CrossRef Medline
36. Südhof TC (2013) Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80:675–690. CrossRef Medline
37. Sugita S, Han W, Butz S, Liu X, Fernández-Chacón R, Lao Y, Südhof TC (2001) Synaptotagmin VII as a plasma membrane Ca(2+) sensor in exocytosis. Neuron 30:459–473. CrossRef Medline
38. Sugita S, Shin OH, Han W, Lao Y, Südhof TC (2002) Synaptotagmins form a hierarchy of exocytotic Ca(2+) sensors with distinct Ca(2+) affinities. EMBO J 21:270–280. CrossRef Medline
39. Sun J, Pang ZP, Qin D, Fahim AT, Adachi R, Südhof TC (2007) A dual- Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450:676–682. CrossRef Medline
40. Takamori S, Holt M, Stenius K, Lemke EA, Grønborg M, Riedel D, Urlaub H, Schenck S, Brügger B, Ringler P, Müller SA, Rammner B, Gräter F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmüller H, Heuser J, Wieland F, Jahn R (2006) Molecular anatomy of a trafficking organelle. Cell 127:831–846. CrossRef Medline
41. Veruki ML, Mørkve SH, Hartveit E (2003) Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. J Physiol 549:759–774. CrossRef Medline
42. Wan QF, Zhou ZY, Thakur P, Vila A, Sherry DM, Janz R, Heidelberger R (2010) SV2 acts via presynaptic calcium to regulate neurotransmitter release. Neuron 66:884–895. CrossRef Medline
43. Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394:384–388. CrossRef Medline
44. Wen H, Linhoff MW, McGinley MJ, Li GL, Corson GM, Mandel G, Brehm P (2010) Distinct roles for two synaptotagmin isoforms in synchronous and asynchronous transmitter release at zebrafish neuromuscular junction. Proc Natl Acad Sci U S A 107:13906–13911. CrossRef Medline
45. Xu J, Mashimo T, Südhof TC (2007) Synaptotagmin-1, -2, and -9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54:567–581. CrossRef Medline