Selective saturation of slow endocytosis at a giant glutamatergic central synapse lacking dynamin 1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 45, 2008, Pages 17555-17560

  Lou, Xuelin ^a   Paradise, Summer ^a   Ferguson, Shawn M ^a   De Camilli, Pietro ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calyx of held; Clathrin; Exocytosis; Synaptic transmission; Vesicle recycling

Indexed keywords

CLATHRIN; DYNAMIN I;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAPACITANCE BLOOD VESSEL; CONTROLLED STUDY; ENDOCYTOSIS; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SYNAPSE;

ANIMALS; DYNAMIN I; ENDOCYTOSIS; LINEAR MODELS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 56249083913     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0809621105     Document Type: Article

References (35)

1. Royle SJ, Lagnado L (2003) Endocytosis at the synaptic terminal. J Physiol 553:345-355.
2. Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701-728.
3. Wu LG, Ryan TA, Lagnado L (2007) Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. J Neurosci 27:11793-11802.
4. Harata NC, Aravanis AM, Tsien RW (2006) Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J Neurochem 97:1546-1570.
5. Granseth B, Odermatt B, Royle SJ, Lagnado L (2006) Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51:773-786.
6. Balaji J, Ryan TA (2007) Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc Natl Acad Sci USA 104:20576-20581.
7. Heerssen H, Fetter RD, Davis GW (2008) Clathrin dependence of synaptic-vesicle formation at the Drosophila neuromuscular junction. Curr Biol 18:401-409.
8. Zenisek D, Steyer JA, Feldman ME, Almers W (2002) A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 35:1085-1097.
9. LoGiudice L, Matthews G (2007) Endocytosis at ribbon synapses. Traffic 8:1123-1128.
10. Koenig JH, Ikeda K (1989) Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 9:3844-3860.
11. Shupliakov O, et al. (1997) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259-263.
12. Jockusch WJ, Praefcke GJ, McMahon HT, Lagnado L (2005) Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46:869-878.
13. Yamashita T, Hige T, Takahashi T (2005) Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307:124-127.
14. Newton AJ, Kirchhausen T, Murthy VN (2006) Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci USA 103:17955-17960.
15. Xu J, et al. (2008) GTP-independent rapid and slow endocytosis at a central synapse. Nat Neurosci 11:45-53.
16. Ferguson SM, et al. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570-574.
17. Hayashi M, et al. (2008) Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc Natl Acad Sci USA 105:2175-2180.
18. Gillis KD (2000) Admittance-based measurement of membrane capacitance using the EPC-9 patch-clamp amplifier. Pflugers Arch 439:655-664.
19. Korogod N, Lou X, Schneggenburger R (2007) Posttetanic potentiation critically depends on an enhanced Ca(2+) sensitivity of vesicle fusion mediated by presynaptic PKC. Proc Natl Acad Sci USA 104:15923-15928.
20. Lou X, Korogod N, Brose N, Schneggenburger R (2008) Phorbol esters modulate spontaneous and Ca2+-evoked transmitter release via acting on both Munc13 and protein kinase C. J Neurosci 28:8257-8267.
21. Lou X, Scheuss V, Schneggenburger R (2005) Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature 435:497-501.
22. Wu W, Xu J, Wu XS, Wu LG (2005) Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 25:11676-11683.
23. Fernandez-Alfonso T, Ryan TA (2004) The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41:943-953.
24. Balaji J, Armbruster M, Ryan TA (2008) Calcium control of endocytic capacity at a CNS synapse. J Neurosci 28:6742-6749.
25. Hull C, von Gersdorff H (2004) Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal. Neuron 44:469-482.
26. Thomas P, Lee AK, Wong JG, Almers W (1994) A triggered mechanism retrieves membrane in seconds after Ca(2+)-stimulated exocytosis in single pituitary cells. J Cell Biol 124:667-675.
27. Renden R, von Gersdorff H (2007) Synaptic vesicle endocytosis at a CNS nerve terminal: Faster kinetics at physiological temperatures and increased endocytotic capacity during maturation. J Neurophysiol 98:3349-3359.
28. Clayton EL, Evans GJ, Cousin MA (2008) Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation. J Neurosci 28:6627-6632.
29. Wu W, Wu LG (2007) Rapid bulk endocytosis and its kinetics of fission pore closure at a central synapse. Proc Natl Acad Sci USA 104:10234-10239.
30. 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.
31. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344.
32. Rosenboom H, Lindau M (1994) Exo-endocytosis and closing of the fission pore during endocytosis in single pituitary nerve terminals internally perfused with high calcium concentrations. Proc Natl Acad Sci USA 91:5267-5271.
33. Cnops L, et al. (2007) Age- and experience-dependent expression of dynamin I and synaptotagmin I in cat visual system. J Comp Neurol 504:254-264.
34. Jaffe AB, Hall A (2005) Rho GTPases: Biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269.
35. Wolfel M, Lou X, Schneggenburger R (2007) A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27:3198-3210.