Membrane cholesterol regulates different modes of synaptic vesicle release and retrieval at the frog neuromuscular junction

European Journal of Neuroscience

Volumn 38, Issue 7, 2013, Pages 2978-2987

  Rodrigues, Hermann A ^a   Lima, Ricardo F ^a,c   Fonseca, Matheus De C ^a   Amaral, Ernani A ^a,d   Martinelli, Patrícia M ^a   Naves, Lígia A ^a   Gomez, Marcus V ^a   Kushmerick, Christopher ^a   Prado, Marco A M ^b   Guatimosim, Cristina ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b ROBARTS RESEARCH INSTITUTE   (Canada)

^c FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^d UNIVERSIDADE FEDERAL DOS VALES DO JEQUITINHONHA E MUCURI   (Brazil)

Author keywords

Cholesterol; Fluorescence microscopy; FM1 43; Neuromuscular junction; Synaptic vesicle

Indexed keywords

BETA CYCLODEXTRIN DERIVATIVE; CHOLESTEROL; FM1 43; METHYL-BETA-CYCLODEXTRIN; MUSCLE RELAXANT AGENT; NICOTINIC RECEPTOR; POTASSIUM CHLORIDE; PYRIDINIUM DERIVATIVE; QUATERNARY AMMONIUM DERIVATIVE;

ANIMAL; BULLFROG; CELL MEMBRANE; DRUG EFFECTS; EXOCYTOSIS; FLUORESCENCE MICROSCOPY; METABOLISM; MICROELECTRODE; MINIATURE ENDPLATE POTENTIAL; NEUROMUSCULAR SYNAPSE; PHYSIOLOGY; SYNAPSE VESICLE; TISSUE CULTURE TECHNIQUE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; BETA-CYCLODEXTRINS; CELL MEMBRANE; CHOLESTEROL; EXOCYTOSIS; MICROELECTRODES; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MINIATURE POSTSYNAPTIC POTENTIALS; NEUROMUSCULAR AGENTS; NEUROMUSCULAR JUNCTION; POTASSIUM CHLORIDE; PYRIDINIUM COMPOUNDS; QUATERNARY AMMONIUM COMPOUNDS; RANA CATESBEIANA; RECEPTORS, NICOTINIC; SYNAPTIC VESICLES; TISSUE CULTURE TECHNIQUES;

EID: 84885402664     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12300     Document Type: Article

References (51)

1. Alabi, A.A. & Tsien, R.W. (2012) Synaptic vesicle pools and dynamics. Cold Spring Harb. Perspect. Biol., 4, a013680.
2. Becherer, U., Guatimosim, C. & Betz, W. (2001) Effects of staurosporine on exocytosis and endocytosis at frog motor nerve terminals. J. Neurosci., 21, 782-787.
3. Betz, W.J. & Bewick, G.S. (1992) Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science, 255, 200-203.
4. Betz, W.J., Mao, F. & Bewick, G.S. (1992) Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals. J. Neurosci., 12, 363-375.
5. Brown, D.A. & Rose, K.J. (1992) Sorting of GPI-anchored proteins to glycolipid enriched membrane subdomains during transport to the apical cell surface. Cell, 68, 533-544.
6. Ceccarelli, B., Hurlbut, W.P. & Mauro, A. (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol., 57, 499-524.
7. Cho, W.J., Jeremic, A., Jin, H., Ren, G. & Jena, B.P. (2007) Neuronal fusion pore assembly requires membrane cholesterol. Cell Biol. Int., 31, 1301-1308.
8. Chung, C., Barylko, B., Leitz, J., Liu, X. & Kavalali, E.T. (2010) Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J. Neurosci., 30, 1363-1376.
9. Colliver, T.L., Pyott, S.J., Achalabun, M. & Ewing, A.G. (2000) VMAT-mediated changes in quantal size and vesicular volume. J. Neurosci., 20, 5267-5282.
10. Croft, B.G., Fortin, G.D., Corera, A.T., Edwards, R.H., Beaudet, A., Trudeau, L.E. & Fon, E.A. (2005) Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice. Mol. Biol. Cell, 16, 306-315.
11. Dason, J.S., Smith, A.J., Marin, L. & Charlton, M.P. (2010) Vesicular sterols are essential for vesicle cycling. J. Neurosci., 30, 15856-15865.
12. Foster, L.J., De Hoog, C.L. & Mann, M. (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. USA, 100, 5813-5818.
13. Fredj, N.B. & Burrone, J. (2009) A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat. Neurosci., 12, 751-758.
14. Guatimosim, C., Romano-Silva, M.A., Cruz, J.S., Beirão, P.S., Kalapothakis, E., Moraes-Santos, T., Cordeiro, M.N., Diniz, C.R., Gomez, M.V. & Prado, M.A. (1997) A toxin from the spider Phoneutria nigriventer that blocks calcium channels coupled to exocytosis. Brit. J. Pharmacol., 122, 591-597.
15. Guatimosim, C., Romano-Silva, M.A., Gomez, M.V. & Prado, M.A. (1998a) Use of fluorescent probes to follow membrane traffic in nerve terminals. Braz. J. Med. Biol. Res., 31, 1491-1500.
16. Guatimosim, C., Romano-Silva, M.A., Gomez, M.V. & Prado, M.A. (1998b) Recycling of synaptic vesicles at the frog neuromuscular junction in the presence of strontium. J. Neurochem., 70, 2477-2483.
17. Harder, T., Scheiffele, P., Verkade, P. & Simons, K. (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol., 141, 929-942.
18. Heuser, J.E. & Reese, T.S. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol., 57, 315-344.
19. Hua, Z., Leal-Ortiz, S., Foss, S.M., Waites, C.L., Garner, C.C., Voglmaier, S.M. & Edwards, R.H. (2011) v-SNARE composition distinguishes synaptic vesicle pools. Neuron, 17, 474-487.
20. Katz, B. & Thesleff, S. (1957) On the factors which determine the amplitude of the miniature end-plate potential. J. Physiol., 137, 267-278.
21. Kilsdonk, E.P., Yancey, P.G., Stoudt, G.W., Bangerter, F.W., Johnson, W.J., Phillips, M.C. & Rothblat, G.H. (1995) Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem., 270, 17250-17256.
22. Lingwood, D., Kaiser, H.J., Levental, I. & Simons, K. (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. T., 37, 955-960.
23. Mailman, T., Hariharan, M. & Karten, B. (2011) Inhibition of neuronal cholesterol biosynthesis with lovastatin leads to impaired synaptic vesicle release even in the presence of lipoproteins or geranylgeraniol. J. Neurochem., 119, 1002-1015.
24. Murthy, V.N. & De Camilli, P. (2003) Cell biology of the presynaptic terminal. Annu. Rev. Neurosci., 26, 701-728.
25. Ohtani, Y., Irie, T., Uekama, K., Fukunaga, K. & Pitha, J. (1989) Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes. Eur. J. Biochem., 186, 17-22.
26. +-ATPase of adrenal secretory granules Rapid partial purification and reconstitution into proteoliposomes. Biochem. J., 271, 127-131.
27. Ramirez, D.M. & Kavalali, E.T. (2011) Differential regulation of spontaneous and evoked neurotransmitter release at central synapses. Curr. Opin. Neurobiol., 21, 275-282.
28. Ramirez, D.M. & Kavalali, E.T. (2012) The role of non-canonical SNAREs in synaptic vesicle recycling. Cell Logist., 2, 20-27.
29. Ribchester, R.R., Mao, F. & Betz, W.J. (1994) Optical measurements of activity-dependent membrane recycling in motor nerve terminals of mammalian skeletal muscle. Proc. Biol. Sci., 255, 61-66.
30. Richards, D.A., Guatimosim, C. & Betz, W.J. (2001) Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron, 27, 551-559.
31. Rizzoli, S.O. & Betz, W.J. (2005) Synaptic vesicle pools. Nat. Rev. Neurosci., 6, 57-69.
32. Rodal, S.K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B. & Sandvig, K. (1999) Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell, 10, 961-974.
33. Royle, S.J. & Lagnado, L. (2003) Endocytosis at the synaptic terminal. J. Physiol., 553, 345-355.
34. Sara, Y., Virmani, T., Deák, F., Liu, X. & Kavalali, E.T. (2005) An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron, 45, 563-573.
35. Simons, K. & Ikonen, E. (1997) Functional rafts in cell membranes. Nature, 387, 569-572.
36. Simons, K. & van Meer, G. (1988) Lipid sorting in epithelial cells. Biochemistry, 27, 6197-6202.
37. Smith, A.J., Sugita, S. & Charlton, M.P. (2010) Cholesterol-dependent kinase activity regulates transmitter release from cerebellar synapses. J. Neurosci., 30, 6116-6121.
38. Stetzkowski-Marden, F., Gaus, K., Recouvreur, M., Cartaud, A. & Cartaud, J. (2006) Agrin elicits membrane lipid condensation at sites of acetylcholine receptor clusters in C2C12 myotubes. J. Lipid Res., 47, 2121-2133.
39. Sudhof, T.C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci., 27, 509-547.
40. Sulzer, D. & Pothos, E.N. (2000) Regulation of quantal size by presynaptic mechanisms. Rev. Neuroscience., 11, 159-212.
41. Tarasenko, A.S., Sivko, R.V., Krisanova, N.V., Himmelreich, N.H. & Borisova, T.A. (2010) Cholesterol depletion from the plasma membrane impairs proton and glutamate storage in synaptic vesicles of nerve terminals. J. Mol. Neurosci., 41, 358-367.
42. Teixeira, G., Vieira, L.B., Gomez, M.V. & Guatimosim, C. (2012) Cholesterol as a key player in the balance of evoked and spontaneous glutamate release in rat brain cortical synaptosomes. Neurochem. Int., 61, 1151-1159.
43. Thiele, C., Hannah, M.J., Fahrenholz, F. & Huttner, W.B. (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat. Cell Biol., 2, 42-49.
44. Van der Kloot, W., Molgo, J., Cameron, R. & Colasante, C. (2002) Vesicle size and transmitter release at the frog neuromuscular junction when quantal acetylcholine content is increased or decreased. J. Physiol., 541, 385-393.
45. Wasser, C.R. & Kavalali, E.T. (2009) Leaky synapses: regulation of spontaneous neurotransmission in central synapses. Neuroscience, 158, 177-188.
46. Wasser, C.R., Ertunc, M., Liu, X. & Kavalali, E.T. (2007) Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. J. Physiol., 579, 413-429.
47. Wu, Y., Yeh, F.L., Mao, F. & Chapman, E.R. (2009) Biophysical characterization of styryl dye-membrane interactions. Biophys. J., 97, 101-109.
48. Yoshinaka, K., Kumanogoh, H., Nakamura, S. & Maekawa, S. (2004) Identification of V-ATPase as a major component in the raft fraction prepared from the synaptic plasma membrane and the synaptic vesicle of rat brain. Neurosci. Lett., 363, 168-172.
49. Zamir, O. & Charlton, M.P. (2006) Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions. J. Physiol., 571, 83-99.
50. Zefirov, A.L., Abdrakhmanov, M.M. & Grigor'ev, P.N. (2004) Kiss-and-run quantal secretion in frog nerve-muscle synapse. B. Exp. Biol. Med., 137, 107-110.
51. Zhang, B., Koh, Y.H., Beckstead, R.B., Budnik, V., Ganetzky, B. & Bellen, H.J. (1998) Synaptic vesicle size and number are regulated by a chlatrin adaptor protein required for endocytosis. Neuron, 21, 1466-1475.