Cholesterol depletion from the plasma membrane impairs proton and glutamate storage in synaptic vesicles of nerve terminals

Journal of Molecular Neuroscience

Volumn 41, Issue 3, 2010, Pages 358-367

  Tarasenko, Alla S ^a   Sivko, Roman V ^a   Krisanova, Natalia V ^a   Himmelreich, Nina H ^a   Borisova, Tatiana A ^a  

^a PALLADIN INSTITUTE OF BIOCHEMISTRY   (Ukraine)

Author keywords

Cholesterol; Exocytosis; Glutamate transporters; Methyl cyclodextrin; Synaptic vesicle proton gradient; Synaptosomes

Indexed keywords

CHOLESTEROL; GLUTAMIC ACID; METHYL BETA CYCLODEXTRIN; PROTON;

ACIDIFICATION; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CALCIUM TRANSPORT; CELL MEMBRANE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME RELEASE; EXOCYTOSIS; FLUORESCENCE ANALYSIS; NERVE ENDING; NEUROTRANSMITTER UPTAKE; NONHUMAN; PROTEIN TRANSPORT; PROTON TRANSPORT; RAT; RECYCLING; SYNAPSE VESICLE;

ANIMALS; BETA-CYCLODEXTRINS; CALCIUM SIGNALING; CELL MEMBRANE; CHOLESTEROL; CYTOSOL; EXOCYTOSIS; GLUTAMIC ACID; HYDROGEN-ION CONCENTRATION; MALE; PRESYNAPTIC TERMINALS; PROTONS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

RATTUS;

EID: 77954543290     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-010-9351-z     Document Type: Article

References (66)

1. Allen JA, Halverson-Tamboli RA, Rasenick MM (2007) Lipid rafts microdomains and neurotransmitter signaling. Nat Rev Neurosci 8:128-140
2. Amador E, Dorfman LE, Wacker WE (1963) Serum lactic dehydrogenase activity: an analytical assessment of current assays. Clin Chem 12:391-399
3. Barnies K, Ingram J, Bennet M, Stewart G, Baldwin S (2004) Methylbeta- cyclodextrin stimulates glucose uptake in clone 9 cells: a possible role for lipid rafts. Biochem J 378:343-351
4. Berman SB, Hastings TG (1997) Inhibition of glutamate transport in synaptosomes by dopamine oxidation and reactive oxygen species. J Neurochem 69:1185-1195
5. Borisova T, Krisanova N, Sivko R, Borysov A (2010) Cholesterol depletion attenuates tonic release but increases the ambient level of glutamate in rat brain synaptosomes. Neurochem Int 56:466-478
6. Burger K, Gimpl G, Fahrenholz F (2000) Regulation of receptor function by cholesterol. Cell Mol Life Sci 57:1577-1592
7. Butchbach M, Tian G, Guo H, Lin CG (2004) Association of excitatory amino acid transporters, especially EAAT2, with cholesterol-rich lipid raft microdomains. J Biol Chem 279:34388-34396
8. Cevc G, Richardsen H (1999) Lipid vesicles and membrane fusion. Adv Drug Deliv Rev 38:207-232
9. Chattopadhyay A, Paila YD (2007) Lipid-protein interactions, regulation and dysfunction of brain cholesterol. Biochem Biophys Res Commun 354:627-633
10. Cho WJ, Jeremic A, Jin H, Ren G, Jena BP (2007) Neuronal fusion pore assembly requires membrane cholesterol. Cell Biol Int 31:1301-1308
11. Christian AE, Haynes MP, Phillips MC, Rothblat GH (1997) Use of cyclodextrins for manipulating cellular cholesterol content. J Lipid Res 38:2264-2272
12. Churchward MA, Rogasevskaia T, Hofgen J, Bau J, Coorseen JR (2005) Cholesterol facilitates the native mechanism of Ca2+-triggered membrane fusion. J Cell Sci 118:4833-4848
13. Cotman CW (1974) Isolation of synaptosomal and synaptic plasma membrane fractions. Meth Enzymol 31:445-452
14. De Lorenzo RJ, Freedman SD (1978) Calcium dependent neurotransmitter release and protein phosphorylation in synaptic vesicles. Biochem Biophys Res Commun 80:183-192
15. Deutsch JW, Kelly RB (1981) Lipids of synaptic vesicles: relevance to the mechanism of membrane fusion. Biochemistry 20:378-385
16. Dietschy JM, Turley SD (2001) Cholesterol metabolism in the brain. Curr Opin Lipidol 12:105-112
17. Dröse S, Altendorf K (1997) Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J Exp Biol 200:1-8
18. Eroglu C, Brugger B, Wieland F, Sinning I (2003) Glutamate-binding affinity of Drosophila metabotropic glutamate receptor is modulated by association with lipid rafts. Proc Natl Acad Sci U S A 100:10219-10224
19. Floor E, Leventhal PS, Schaeffer SF (1990) Partial purification and characterization of the vacuolar H(+)-ATPase of mammalian synaptic vesicles. J Neurochem 55:1663-1670
20. Fong TM, McNamee MG (1986) Correlation between acetylcholine receptor function and structural properties of membranes. Biochemistry 25:830-840
21. Gil C, Soler-Jover A, Blasi J (2005) Aguilera synaptic proteins and SNARE complexes are localized in lipid rafts from brain synaptosomes. Biochem Biophys Res Commun 329:117-124
22. Gonzáles MI, Susarla BT, Fournier KM, Sheldon AL, Robinson MB (2007) Constitutive endocytosis and recycling of the neuronal glutamate transporter, excitatory amino acid carrier 1. J Neurochem 103:1917-1931
23. Hering H, Lin CC, Sheng M (2003) Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J Neurosci 23:3262-3271
24. Hill W, An B, Johnson J (2002) Endogenously expressed epithelial sodium channel is present in lipid rafts in A6 cells. J Biol Chem 277:33541-33544 366 J Mol Neurosci (2010) 41:358-367
25. Huss M, Wieczorek H (2009) Inhibitors of V-ATPases: old and new players. J Exp Biol 212:341-346
26. Jadot M, Andrianaivo F, Dubois F, Wattiaux R (2001) Effects of methylcyclodextrin on lysosomes. Eur J Biochem 268:1392-1399
27. Jennings LJ, Xu QW, Firth TA, Nelson MT, Mawe GM (1999) Cholesterol inhibits spontaneous action potentials and calcium currents in guinea pig gallbladder smooth muscle. Am J Physiol 277:1017-1026
28. Kato N, Nakanishi M, Hirashima N (2003) Cholesterol depletion inhibits store-operated calcium currents and exocytotic membrane fusion in RBL-2H3 cells. Biochemistry 42:11808-11814
29. Klein U, Gimpl G, Fahrenholz F (1995) Alteration of the myometrial plasma membrane cholesterol content with β-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry 34:13784-13793
30. Krysanova NV, Sivko RV, Krupko OA, Borisova TA (2007) Methylbeta- cyclodextrin influences glutamate transport in the rat brain nerve terminals by depletion of membrane cholesterol. Ukr Biokhim Zh 79:29-37
31. Lang T, Bruns D, Wenzel D et al (2001) SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 20:2202-2213
32. Lange Y, Ye J, Rigney M, Steck TL (1999) Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res 40:2264-2269
33. Lange Y, Ye J, Steck TL (2004) How cholesterol homeostasis is regulated by plasma membrane cholesterol in excess of phospholipids. Proc Natl Acad Sci U S A 101:11664-11667
34. Lange Y, Ye J, Steck TL (2005) Activation of membrane cholesterol by displacement from phospholipids. J Biol Chem 280:36126-36131
35. Larson E, Howlett B, Jagendorf A (1986) Artificial reductant enhancement of the Lowry method for protein determination. Anal Biochem 155:243-248
36. Launikonis BS, Stephenson DG (2001) Effects of membrane cholesterol manipulation on excitation-contraction coupling in skeletal muscle of the toad. J Physiol 534:71-85
37. Linetska MV, Storchak LG, Tarasenko AS, Himmelreich NH (2004) Involvement of membrane GABA transporter in alpha-latrotoxinstimulated [3H]GABA release. Neurochem Int 44:303-312
38. Martens J, O'Connell K, Tamkun M (2004) Targeting of ion channels to membrane microdomains: localization of Kv channels to lipid rafts. Trends Pharmacol Sci 25:16-21 (Pubitemid 38076952)
39. Mauch DH, Nägler K, Schumacher S et al (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354-1357
40. Mitter D, Reisinger C, Hinz B et al (2003) The synaptophysin/ synaptobrevin interaction critically depends on the cholesterol content. J Neurochem 84:35-42
41. Pfrieger FW (2003) Cholesterol homeostasis and function in neurons of the central nervous system. Cell Mol Life Sci 60:1158-1171
42. Rodal SK, 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
43. Rohrbough J, Broadie K (2005) Lipid regulation of the synaptic vesicle cycle. Nat Rev Neurosci 6:139-150
44. Romanenko VG, Rothblat GH, Levitan I (2002) Modulation of endothelial inward-rectifier K+ current by optical isomers of cholesterol. Biophys J 83:3211-3222
45. Roseth S, Fykse EM, Fonnum F (1995) Uptake of L-glutamate into rat brain synaptic vesicles: effect of inhibitors that bind specifically to the glutamate transporter. J Neurochem 65:96-103
46. Salaun C, James DJ, Chamberlain LH (2004) Lipid rafts and the regulation of exocytosis. Traffic 5:1-10
47. Salaun C, Gould GW, Chamberlain LH (2005) Lipid raft association of SNARE proteins regulates exocytosis in PC12 cells. J Biol Chem 280:19449-19453
48. Sivko R, Krisanova N, Borisova T (2009) Reduced cholesterol content and the effects of inhibitors on Na+-dependent glutamate transport in rat brain nerve terminals. Neurobiol. Lipids 8(2):6-11. http://neurobiologyoflipids.org/ content/8/2/
49. Sooksawate T, Simmonds MA (2001) Effects of membrane cholesterol on the sensitivity of the GABA(A) receptor to GABA in acutely dissociated rat hippocampal neurones. Neuropharmacology 40:178-184
50. Steck TL, Ye J, Lange Y (2002) Probing red cell membrane cholesterol movement with cyclopdextrin. Biophys J 83:2118-2125
51. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, McGraw TE (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci U S A 96:6775-6780
52. Tarasenko AS, Linetska MV, Storchak LG, Himmelreich NH (2006) Effectiveness of extracellular lactate/pyruvate for sustaining synaptic vesicle proton gradient generation and vesicular accumulation of GABA. J Neurochem 99:787-796
53. Taverna E, Saba E, Rowe J, Francolini M, Clementi F, Rosa P (2004) Role of lipid microdomains in p/q-type calcium channel (cav2.1) clustering and function in presynaptic membranes. J Biol Chem 279:5127-5134
54. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2:42-49
55. Trikash IO, Volynets GP, Remenyak OV, Gorchev VF (2008) Docking and fusion of synaptic vesicles in cell-free model system of exocytosis. Neurochem Int 53:401-407
56. Waseem TV, Kolos VA, Lapatsina LP, Fedorovich SV (2006) Influence of cholesterol depletion in plasma membrane of rat brain synaptosomes on calcium-dependent and calciumindependent exocytosis. Neurosci Lett 405:106-110
57. Wasser CR, Ertunc M, Liu X, Kavalali ET (2007) Cholesteroldependent balance between evoked and spontaneous vesicle recycling. J Physiol 579.2:413-429
58. Xia F, Gao X, Kwan E et al (2004) Disruption of pancreatic β-cells lipid rafts modifies Kv2.1 channel gating and insulin exocyrtosis. J Biol Chem 279:24685-24691
59. Xia F, Leung YM, Gaisano G et al (2007) Targeting of Kv4, Cav1.2 and SNARE proteins to cholesterol-rich lipid rafts in pancreatic a-cells: effects on glucagons stimulus-secretion coupling. Endocrinology 148:2157-2167
60. Yancey PG, Rodrigueza WV, Kilsdonk EP et al (1996) Cellular cholesterol efflux mediated by cyclodextrins. J Biol Chem 271:16026-16034
61. 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
62. Zamir O, Charlton MP (2006) Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions. J Physiol 571:83-99
63. Zhang J, Feng Y, Forgac M (1994) Proton conduction and bafilomycin binding by the V0 domain of the coated vesicle V-ATPase. J Biol Chem 269:23518-23523
64. Zhou Q, Petersen CC, Nicoll RA (2000) Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurons. J Physiol 525:195-206
65. Zidovetzki R, Levitan I (2007) Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim Biophys Acta 1768:1311-1324
66. Zoccarato F, Cavallini L, Alexandre A (1999) The pH-sensitive dye acridine orange as a tool to monitor exocytosis/endocytosis in synaptosomes. J Neurochem 72:625-633