Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells

Journal of Neuroscience

Volumn 23, Issue 4, 2003, Pages 1329-1339

  Holt, Matthew ^a   Cooke, Anne ^a   Wu, Minnie M ^a   Lagnado, Leon ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Actin; Calcium; Endocytosis; Macropinocytosis; Phosphatidylinositol 3 kinase; Synapse

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CALCIUM; CYTOCHALASIN D; DEXTRAN; DYE; LATRUNCULIN B; PHOSPHATIDYLINOSITOL 3 KINASE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE; IMAGING; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; RETINA BIPOLAR GANGLION CELL; SYNAPSE;

EID: 0037442516     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-04-01329.2003     Document Type: Article

References (63)

1. Araki N, Johnson MT, Swanson JA (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 135:1249-1260.
2. Behrens UD, Wagner HJ (1996) Adaptation-dependent changes of bipolar cell terminals in fish retina: effects on overall morphology and spinule formation in Ma and Mb cells. Vision Res 36:3901-3911.
3. Berthiaume EP, Medina C, Swanson JA (1995) Molecular size-fractionation during endocytosis in macrophages. J Cell Biol 129:989-998.
4. Brown SP, Masland RH (2001) Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells. Nat Neurosci 4:44-51.
5. Burrone J, Lagnado L (2000) Synaptic depression and the kinetics ofexocytosis in retinal bipolar cells. J Neurosci 20:568-578.
6. Clague MJ, Thorpe C, Jones AT (1995) Phosphatidylinositol 3-kinase regulation of fluid phase endocytosis. FEBS Lett 367:272-274.
7. Cole JC, Villa BR, Wilkinson RS (2000) Disruption of actin impedes transmitter release in snake motor terminals. J Physiol (Lond) 525:579-586.
8. Cremona O, De Camilli P (2001) Phosphoinositides in membrane traffic at the synapse. J Cell Sci 114:1041-1052.
9. Crowder RJ, Freeman RS (1999) The survival of sympathetic neurons promoted by potassium depolarization, but not by cyclic AMP, requires phosphatidylinositol 3-kinase and Akt. J Neurochem 73:466-475.
10. Dowling JE (1987) The retina: an approachable part of the brain. Cambridge, MA: Harvard UP.
11. Dunaevsky A, Connor EA (2000) F-actin is concentrated in nonrelease domains at frog neuromuscular junctions. J Neurosci 20:6007-6012.
12. 2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291:1051-1055.
13. Fried RC, Blaustein MP (1978) Retrieval and recycling of synaptic vesicle membrane in pinched-off nerve terminals (synaptosomes). J Cell Biol 78:685-700.
14. Fujimoto LM, Roth R, Heuser JE, Schmid SL (2000) Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1:161-171.
15. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21:607-616.
16. Gad H, Ringstad N, Low P, Kjaerulff O, Gustafsson J, Wenk M, Di Paolo G, Nemoto Y, Crun J, Ellisman MH, De Camilli P, Shupliakov O, Brodin L (2000) Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27:301-312.
17. 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.
18. Greengard P,Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
19. 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.
20. Hirokawa N, Sobue K, Kanda K, Harada A, Yorifuji H (1989) The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J Cell Biol 108:111-126.
21. Ikegami K, Koike T (2000) Membrane depolarization-mediated survival of sympathetic neurons occurs through both phosphatidylinositol 3-kinase and CaM kinase II-dependent pathways. Brain Res 866:218-226.
22. Job C, Lagnado L (1998) Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells. J Cell Biol 143:1661-1672.
23. Koenig J, 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.
24. Koenig J, Ikeda K (1996) Synaptic vesicles have two distinct recycling pathways. J Cell Biol 135:797-808.
25. Lagnado L, Gomis A, Job C (1996) Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17:957-967.
26. Lamaze C, Schmid SL (1995) The emergence of clathrin-independent pinocytic pathways. Curr Opin Cell Biol 7:573-580.
27. Mandell JW, Townes-Anderson E, Czernik AJ, Cameron R, Greengard P, De CamilliP (1990) Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5:19-33.
28. Martin TF (1998) Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol 14:231-264.
29. Mennerick S, Matthews G (1996) Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17:1241-1249.
30. Merrifield CJ, Moss SE, Ballestrem C, Imhof BA, Giese G, Wunderlich I, Almers W (1999) Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol 1:72-74.
31. Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4:691-698.
32. Miller TM, Tansey MG, Johnson Jr EM, Creedon DJ (1997) Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization-and insulinlike growth factor 1-mediated survival of cerebellar granule cells. J Biol Chem 272:9847-9853.
33. Morales M, Colicos MA, Goda Y (2000) Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 27:539-550.
34. Morton WM, Ayscough KR, McLaughlin PJ (2000) Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol 2:376-378.
35. Neves G, Lagnado L (1999) The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J Physiol (Lond) 515:181-202.
36. Neves G, Gomis A, Lagnado L (2001) Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc Natl Acad Sci USA 98:15282-15287.
37. Nichols BJ, Lippincott-Schwartz J (2001) Endocytosis without clathrin coats. Trends Cell Biol 11:406-412.
38. Orth JD, Krueger EW, Cao H, McNiven MA (2002) From the cover: the large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci USA 99:167-172.
39. Osborne SL, Meunier FA, Schiavo G (2001) Phosphoinositides as key regulators of synaptic function. Neuron 32:9-12.
40. Pike LJ (1992) Phosphatidylinositol 4-kinases and the role of polyphosphoinositides in cellular regulation. Endocr Rev 13:692-706.
41. Qualmann B, Kelly RB (2000) Syndapin isoforms participate in receptormediated endocytosis and actin organization. J Cell Biol 148:1047-1062.
42. Qualmann B, Kessels MM, Kelly RB (2000) Molecular links between endocytosis and the actin cytoskeleton. J Cell Biol 150:F111-F116.
43. Richards DA, Guatimosim C, Betz WJ (2000) Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27:551-559.
44. Roos J, Kelly RB (1999) The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr Biol 9:1411-1414.
45. Rouze NC, Schwartz EA (1998) Continuous and transient vesicle cycling at a ribbon synapse. J Neurosci 18:8614-8624.
46. Sankaranarayanau S, Atluri PP, Ryan TA (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci, in press.
47. Shupliakov O, Bloom O, Gustafsson JS, Kjaerulff O, Low P, Tomilin N, Pieribone VA, Greengard P, Brodin L (2002) Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci USA 99:14476-14481,
48. Slepnev VI, De Camilli P (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 1:161-172.
49. Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M (1997) Adaptation of retinal processing to image contrast and spatial scale. Nature 386:69-73.
50. Swanson JA, Watts C (1995) Macropinocytosis. Trends Cell Biol 5:424-428.
51. Takei K, Mundigl O, Daniell L, De Camilli P (1996) The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 133:1237-1250.
52. Teng H, Wilkinson RS (2000) Clathrin-mediated endocytosis near active zones in snake motor boutons. J Neurosci 20:7986-7993.
53. 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.
54. Toker A, Cantley LC (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature 387:673-676.
55. Vlahos CJ, Matter WF, Hui KY, Brown RF (1994) A specific inhibitor ofphosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran4-one (LY294002). J Biol Chem 269:5241-5248.
56. von Gersdorff H, Matthews G (1994) Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367:735-739.
57. von Gersdorff H, Vardi E, Matthews G, Sterling P (1996) Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 16:1221-1227.
58. von Kriegstein K, Schmitz F, Link E, Sudhof TC (1999) Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur J Neurosci 11:1335-1348.
59. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM, Hasson T, Carragher BO, Milligan RA, Sweeney HL (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401:505-508.
60. West MA, Prescott AR, Eskelinen EL, Ridley AJ, Watts C (2000) Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 10:839-848.
61. Yazulla S, Studholme KM (1992) Light-dependent plasticity of the synaptic terminals of Mb bipolar cells in goldfish retina. J Comp Neurol 320:521-530.
62. ZenisekD, Steyer JA, Almers W (2000) Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406:849-854.
63. 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.