Heterogeneity in synaptic vesicle release at neuromuscular synapses of mice expressing synaptopHluorin

Journal of Neuroscience

Volumn 28, Issue 1, 2008, Pages 325-335

  Wyatt, Ryan M ^a   Balice Gordon, Rita J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Exocytosis; Neuromuscular; pHluorin; Synapse; Synaptic vesicle; Vesicle recycling

Indexed keywords

MEMBRANE PROTEIN; PROTEIN SYNAPTOPHLUORIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; CONTROLLED STUDY; FLUORESCENCE; MOUSE; NERVE ENDING; NERVE STIMULATION; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS; PRESYNAPTIC TERMINALS; RECEPTORS, NICOTINIC; RECOMBINANT FUSION PROTEINS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 38149034432     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3544-07.2008     Document Type: Article

References (43)

1. Balice-Gordon RJ, Lichtman JW (1993) In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions. J Neurosci 13:834-855.
2. Bennett MR, Lavidis NA (1989) The probability of quantal secretion at release sites in different calcium concentrations in toad (Bufo marinus) muscle. J Physiol (Lond) 418:219-233.
3. Betz WJ, Bewick GS (1992) Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255:200-203.
4. Caroni P (1997) Overexpression of growth-associated proteins in the neurons of adult transgenic mice. J Neurosci Methods 71:3-9.
5. Delgado R, Maureira C, Oliva C, Kidokoro Y, Labarca P (2000) Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 28:941-953.
6. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
7. Fernandez-Alfonso T, Kwan R, Ryan TA (2006) Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51:179-186.
8. Fukunaga H, Engel AG, Osame M, Lambert EH (1982) Paucity and disorganization of presynaptic membrane active zones in the Lambert-Eaton myasthenic syndrome. Muscle Nerve 5:686-697.
9. Fukunaga H, Engel AG, Lang B, Newsom-Davis J, Vincent A (1983) Passive transfer of Lambert-Eaton myasthenic syndrome with IgG from man to mouse depletes the presynaptic membrane active zones. Proc Natl Acad Sci USA 80:7636-7640.
10. Gaffield MA, Betz WJ (2006) Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat Protoc 1:2916-2921.
11. Gage PW, Murphy EC (1981) Facilitation of acetylcholine secretion at a mouse neuromuscular junction. Brain Res 204:327-337.
12. Glavinovic MI (1979) Change of statistical parameters of transmitter release during various kinetic tests in unparalyzed voltage-clamped rat diaphragm. J Physiol (Lond) 290:481-497.
13. Gonzalez M, Ruggiero FP, Chang Q, Shi YJ, Rich MM, Kraner S, Balice-Gordon RJ (1999) Disruption of TrkB-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions. Neuron 24:567-583.
14. Guerrero G, Reiff DF, Agarwal G, Ball RW, Borst A, Goodman CS, Isacoff EY (2005) Heterogeneity in synaptic transmission along a Drosophila larval motor axon. Nat Neurosci 8:1188-1196.
15. Hess DM, Scott MO, Potluri S, Pitts EV, Cisterni C, Balice-Gordon RJ (2007) Localization of TrkC to Schwann cells and effects of neurotrophin-3 signaling at neuromuscular synapses. J Comp Neurol 501:465-482.
16. 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.
17. Juranek J, Mukherjee K, Rickmann M, Martens H, Calka J, Sudhof TC, Jahn R (2006) Differential expression of active zone proteins in neuromuscular junctions suggests functional diversification. Eur J Neurosci 24:3043-3052.
18. Kamenskaya MA, Elmqvist D, Thesleff S (1975) Guanidine and neuromuscular transmission. II. Effect on transmitter release in response to repetitive nerve stimulation. Arch Neurol 32:510-518.
19. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF, Murthy VN (2005) Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci USA 102:6131-6136.
20. Liu Z, Lee H, Xiong Y, Sun C, Zhang X (2007) Far-field optical hyperlens magnifying sub-diffraction-limited objects. Science 315:1686.
21. McLachlan EM, Martin AR (1981) Non-linear summation of end-plate potentials in the frog and mouse. J Physiol (Lond) 311:307-324.
22. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195.
23. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599-612.
24. Nishimune H, Sanes JR, Carlson SS (2004) A synaptic laminin-calcium channel interaction organizes active zones in motor nerve terminals. Nature 432:580-587.
25. Polo-Parada L, Bose CM, Landmesser LT (2001) Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions. Neuron 32:815-828.
26. Poskanzer KE, Marek KW, Sweeney ST, Davis GW (2003) Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426:559-563.
27. Rees D (1978) A non-phosphate-buffered physiological saline for in vitro electrophysiological studies on the mammalina neuromuscular junctions. J Physiol (Lond) 278:8P-9P.
28. Reid B, Slater CR, Bewick GS (1999) Synaptic vesicle dynamics in rat fast and slow motor nerve terminals. J Neurosci 19:2511-2521.
29. Reid B, Martinov VN, Nja A, Lomo T, Bewick GS (2003) Activity-dependent plasticity of transmitter release from nerve terminals in rat fast and slow muscles. J Neurosci 23:9340-9348.
30. Reiff DF, Ihring A, Guerrero G, Isacoff EY, Joesch M, Nakai J, Borst A (2005) In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25:4766-4778.
31. Ribchester RR, Mao F, Betz WJ (1994) Optical measurements of activity-dependent membrane recycling in motor nerve terminals of mammalian skeletal muscle. Proc Biol Sci 255:61-66.
32. Rizzoli SO, Betz WJ (2004) The structural organization of the readily releasable pool of synaptic vesicles. Science 303:2037-2039.
33. Rowley KL, Mantilla CB, Ermilov LG, Sieck GC (2007) Synaptic vesicle distribution and release at rat diaphragm neuromuscular junctions. J Neurophysiol 98:478-487.
34. Sankaranarayanan S, Ryan TA (2000) Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol 2:197-204.
35. Sankaranarayanan S, Ryan TA (2001) Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 4:129-136.
36. Schikorski T, Stevens CF (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391-395.
37. Smolyaninov II, Hung YJ, Davis CC (2007) Magnifying superlens in the visible frequency range. Science 315:1699-1701.
38. Tabares L, Ruiz R, Linares-Clemente P, Gaffield MA, Alvarez de Toledo G, Fernandez-Chacon R, Betz WJ (2007) Monitoring synaptic function at the neuromuscular junction of a mouse expressing synaptopHluorin. J Neurosci 27:5422-5430.
39. Teng H, Cole JC, Roberts RL, Wilkinson RS (1999) Endocytic active zones: hot spots for endocytosis in vertebrate neuromuscular terminals. J Neurosci 19:4855-4866.
40. Vidal M, Morris R, Grosveld F, Spanopoulou E (1990) Tissue-specific control elements of the Thy-1 gene. EMBO J 9:833-840.
41. Willig KI, Rizzoli SO, Westphal V, Jahn R, Hell SW (2006) STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440:935-939.
42. Wood SJ, Slater CR (1997) The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast- and slow-twitch muscles. J Physiol (Lond) 500:165-176.
43. Wood SJ, Slater CR (2001) Safety factor at the neuromuscular junction. Prog Neurobiol 64:393-429.