The proton gradient of secretory granules and glutamate transport in blood platelets during cholesterol depletion of the plasma membrane by methyl-β-cyclodextrin

Neurochemistry International

Volumn 59, Issue 6, 2011, Pages 965-975

  Borisova, Tatiana ^a   Kasatkina, Ludmila ^a,b   Ostapchenko, Ludmila ^b  

^a PALLADIN INSTITUTE OF BIOCHEMISTRY   (Ukraine)

^b TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

Author keywords

Cholesterol; Glutamate release; Human blood platelets; Methyl cyclodextrin; Na+ dependent glutamate uptake; Plasma membrane potential; Rabbit blood platelets; The proton gradient of secretory granules

Indexed keywords

ACRIDINE ORANGE; ADENOSINE TRIPHOSPHATASE; BETA CYCLODEXTRIN; CHOLESTEROL; FILIPIN; FLUORESCENT DYE; GLUTAMATE DEHYDROGENASE; GLUTAMIC ACID; HYDROGEN; PROTON PUMP;

ACIDIFICATION; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONFOCAL LASER MICROSCOPY; ENZYME ASSAY; EXOCYTOSIS; FLOW CYTOMETRY; HUMAN; IMAGING; NONHUMAN; PH; PRIORITY JOURNAL; RABBIT; SECRETORY GRANULE; THROMBOCYTE; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION;

ANIMALS; BETA-CYCLODEXTRINS; BLOOD PLATELETS; CELL MEMBRANE; CHOLESTEROL; GLUTAMIC ACID; HUMANS; PROTON PUMP INHIBITORS; PROTON PUMPS; RABBITS; SECRETORY VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEINS;

ORYCTOLAGUS CUNICULUS;

EID: 80255138169     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.07.007     Document Type: Article

References (81)

1. T. Aiuchi, T. Daimatsu, K. Nakaya, and Y. Nakamura Fluorescence changes of rhodamine 6G associated with changes in membrane potential in synaptosomes Biochim. Biophys. Acta 685 1982 289 296 (Pubitemid 12116237)
2. S. Amisten, O.O. Braun, A. Bengtsson, and D. Erlinge Gene expression profiling for the identification of G-protein coupled receptors in human platelets Thromb. Res. 122 2008 47 57 (Pubitemid 351601841)
3. R. Bali, L. Savino, D.A. Ramirez, N.M. Tsvetkova, L. Bagatolli, and F. Tablin Macroscopic domain formation during cooling in the platelet plasma membrane: an issue of low cholesterol content Biochim. Biophys. Acta 1788 2009 1229 1237
4. S.S. Banerjee, and D.H. Chen Cyclodextrin conjugated magnetic colloidal nanoparticles as a nanocarrier for targeted anticancer drug delivery Nanotechnology 19 2008 1 7
5. K. Barnes, J.C. Ingram, M.D.M. Bennett, G.W. Stewart, and S.A. Baldwin Methyl-beta-cyclodextrin stimulates glucose uptake in Clone 9 cells: a possible role for lipid rafts Biochem. J. 378 2004 343 351 (Pubitemid 38367225)
6. B. Begni, L. Tremolizzo, C. D'Orlando, M.S. Bono, R. Garofolo, M. Longoni, and C. Ferrarese Substrate-induced modulation of glutamate uptake in human platelets Br. J. Pharmacol. 145 2005 792 799 (Pubitemid 41076286)
7. P. Bezzi, G. Carmignoto, L. Pasti, S. Vesce, D. Rossi, B. Lodi Rizzini, T. Pozzan, and A. Volterra Prostaglandins stimulate calcium-dependent glutamate release in astrocytes Nature 391 1998 281 285 (Pubitemid 28099014)
8. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
9. T. Borisova, N.V. Krisanova, R.V. Sivko, and A. Borysov Cholesterol depletion attenuates tonic release but increases the ambient level of glutamate in rat brain synaptosomes Neurochem. Int. 56 2010 466 478
10. T.A. Borisova, R.V. Sivko, A. Borysov, and N.V. Krisanova B. Diverse presynaptic mechanisms underlying methyl-beta-cyclodextrin - mediated changes in glutamate transport Cell. Mol. Neurobiol. 30 2010 1013 1023
11. S.L. Brownlow, A.G.S. Harper, M.T. Harper, and S.O. Sage A role for hTRPC1 and lipid raft domains in store-mediated calcium entry in human platelets Cell Calcium 35 2004 107 113 (Pubitemid 38139670)
12. M.E. Butchbach, G. Tian, H. Guo, and C.L. Lin Association of excitatory amino acid transporters, especially EAAT2, with cholesterol-rich lipid raft microdomains: importance for excitatory amino acid transporter localization and function J. Biol. Chem. 279 2004 34388 34396 (Pubitemid 39318064)
13. F.J. Byfield, H. Aranda-Espinoza, V.G. Romanenko, G.H. Rothblat, and I. Levitan Cholesterol depletion increases membrane stiffness of aortic endothelial cells Biophys. J. 87 2004 3336 3343 (Pubitemid 40468588)
14. A.C. Carvalho, R.W. Colman, and R.S. Lees Platelet function in hyperlipoproteinemia N. Engl. J. Med. 290 1974 434 438
15. 3H]-ketanserin binding Life Sci. 46 1990 1755 1764 (Pubitemid 20190745)
16. N. Chetty, and N.H. Naran Platelet hyperreactivity in hyperlipidaemia with specific reference to platelet lipids and fatty acid composition Clin. Chim. Acta 213 1992 1 13 (Pubitemid 23003709)
17. F. Franconi, M. Miceli, L. Alberti, G. Seghieri, M.G. Demontis, and A. Tagliamonte Further insights into the anti-aggregating activity of NMDA in human platelets Br. J. Pharmacol. 124 1998 35 40 (Pubitemid 28210040)
18. M.I. González, B.T. Susarla, and K.M. Fournier Constitutive endocytosis and recycling of the neuronal glutamate transporter, excitatory amino acid carrier 1 J. Neurochem. 103 2007 1917 1931 (Pubitemid 350130098)
19. M. Gottlieb, Y. Wang, and V.I. Teichberg Blood-mediated scavenging of cerebrospinal fluid glutamate J. Neurochem. 87 2003 119 126 (Pubitemid 37210646)
20. K. Gousset, N.M. Tsvetkova, J.H. Crowe, and F. Tablin Important role of raft aggregation in the signaling events of cold-induced platelet activation Biochem. Biophys. Acta 1660 2004 7 15 (Pubitemid 38128327)
21. K. Gousset, W.F. Wolkers, N.M. Tsvetkova, A.E. Oliver, C.L. Field, N.J. Walker, J.H. Crowe, and F. Tablin Evidence for a physiological role for membrane rafts in human platelets J. Cell. Physiol. 190 2002 117 128
22. S. Grgurevich, R. Krishnan, M.M. White, and L.K. Jennings Role of in vitro cholesterol depletion in mediating human platelet aggregation J. Thromb. Haemost. 1 2003 576 586
23. +-alkali cation countertransport in secretary granule swelling during exocytosis FEBS Lett. 148 1982 1 4 (Pubitemid 13225231)
24. P.Y. Grosse, F. Bressolle, P. Rouanet, J.M. Joulia, and F. Pinguet Methyl-beta-cyclodextrin and doxorubicin pharmacokinetics and tissue concentrations following bolus injection of these drugs alone or together in the rabbit Int. J. Pharm. 180 1999 215 223 (Pubitemid 29238205)
25. G. Hoogland, I.W. Bos, F. Kupper, G. van Willigen, H.A. Spierenburg, O. van Nieuwenhuizen, and P.N. de Graan Thrombin-stimulated glutamate uptake in human platelets is predominantly mediated by the glial glutamate transporter EAAT2 Neurochem. Int. 47 2005 499 506 (Pubitemid 41266880)
26. S. Ilangumaran, and D.C. Hoessli Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane Biochem. J. 335 1998 433 440 (Pubitemid 28491081)
27. M. Jadot, F. Andrianaivo, F. Dubois, and R. Wattiaux Effects of methylcyclodextrin on lysosomes Eur. J. Biochem. 268 2001 1392 1399 (Pubitemid 32231892)
28. H. Jeulin, V. Venard, D. Carapito, C. Finance, and F. Kedzierewicz Effective ribavirin concentration in mice brain using cyclodextrin as a drug carrier: evaluation in a measles encephalitis mode Antivir. Res. 81 2009 261 266
29. +-dependent glutamate uptake in platelets during depolarization of their plasma membrane Neurochem. Int. 56 2010 711 719
30. U. Klein, G. Gimpl, and F. Fahrenholz Alteration of the myometrial plasma cholesterol content with β-cyclodextrin modulates the binding affinity of the oxytocin receptor Biochemistry 34 1995 13784 13793
31. H.S. Kruth, and M. Vaughan Quantification of low density lipoprotein binding and cholesterol accumulation by single human fibroblasts using fluorescence microscopy J. Lipid. Res. 21 1980 123 130 (Pubitemid 10120444)
32. J.S. Kuo, S.F. Chen, H.J. Huang, C.S. Yang, P.J. Tsai, and C.M. Hsueh The involvement of glutamate in recall of the conditioned NK cell response J. Neuroimmunol. 118 2001 245 255
33. T. Lang, D. Bruns, D. Wenzel, D. Riedel, P. Holroyd, C. Thiele, and R. Jahn SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis EMBO J. 20 2001 2202 2213 (Pubitemid 32410590)
34. Y. Lange, J. Ye, and T.L. Steck How cholesterol homeostasis is regulated by plasma membrane cholesterol in excess of phospholipids Proc. Natl. Acad. Sci. USA 101 2004 11664 11667 (Pubitemid 39095353)
35. Y. Lange, J. Ye, and T.L. Steck Activation of membrane cholesterol by displacement from phospholipids J. Biol. Chem. 280 2005 36126 36131 (Pubitemid 41633884)
36. E. Larson, B. Howlett, and A. Jagendorf Artificial reductant enhancement of the Lowry method for protein determination Anal. Biochem. 155 1986 243 248 (Pubitemid 16060156)
37. I. Levitan, A.E. Christian, T.N. Tulenko, and G.H. Rothblat Membrane cholesterol content modulates activation of volume-regulated anion current in bovine endothelial cells J. Gen. Physiol. 115 2000 405 416 (Pubitemid 30196589)
38. +-ATPases in human platelets Biochem. J. 390 2005 243 252 (Pubitemid 41192250)
39. D.E. MacIntyre, and T.J. Rink The role of platelet membrane potential in the initiation of platelet aggregation Thromb. Haemost. 47 1982 22 26 (Pubitemid 12180419)
40. M.P. Mahaut-Smith, T.J. Rink, S.C. Collins, and S.O. Sage Voltage-gated potassium channels and the control of membrane potential in human platelets J. Physiol. 428 1990 723 735 (Pubitemid 20313682)
41. R. Mangano, and R. Schwarcz The human platelets as a model for the glutamatergic neuron: platelet uptake of l-glutamate J. Neurochem. 36 1981 1067 1076 (Pubitemid 11100094)
42. Y. Maruyama A patch-clamp study of mammalian platelets and their voltage-gated potassium current J. Physiol. 391 1987 467 485 (Pubitemid 17161452)
43. V. Monnaert, S. Tilloy, H. Bricout, L. Fenart, R. Cecchelli, and E. Monflier Behavior of alpha-, beta-, and gamma-cyclodextrins and their derivatives on an in vitro model of blood-brain barrier J. Pharmacol. Exp. Ther. 310 2004 745 751 (Pubitemid 38988921)
44. C.N. Morrell, H. Sun, M. Ikeda, J.C. Beique, A.M. Swaim, E. Mason, T.V. Martin, L.E. Thompson, O. Gozen, D. Ampagoomian, R. Sprengel, J. Rothstein, N. Faraday, R. Huganir, and C.J. Lowenstein Glutamate mediates platelet activation through the AMPA receptor J. Exp. Med. 205 2008 575 584 (Pubitemid 351439305)
45. D.G. Nicholls, and T.S. Sihra Synaptosomes possess an exocytotic pool of glutamate Nature 321 1986 772 773 (Pubitemid 16077902)
46. +-dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) of the blood-brain barrier. A mechanism for glutamate removal J. Biol. Chem. 274 1999 31891 31895
47. H. Osamah, R. Mira, S. Sorina, K. Shlomo, and A. Michael Reduced platelet aggregation after fluvastatin therapy is associated with altered platelet lipid composition and drug binding to the platelets Br. J. Clin. Pharmacol. 44 1 1997 77 83
48. +-ATPase of adrenal secretory granules. Rapid partial purification and reconstitution into proteoliposomes Biochem. J. 271 1990 127 131 (Pubitemid 20331207)
49. E. Pipili Platelet membrane potential: simultaneous measurement of diSC3(5) fluorescence and optical density Thromb. Haemost. 54 1985 645 649 (Pubitemid 16195310)
50. E.G. Popov, Z.A. Gabbazov, I.Yu. Gavrilov, E.Ya. Pozin, and A.G. Mejlumian Accumulation and release of acridine derivatives by intact platelets Thomb. Res. 47 1987 639 645 (Pubitemid 18034543)
51. S. Rainesalo, T. Keränen, J. Peltola, and P. Saransaari Glutamate uptake in blood platelets from epileptic patients Neurochem. Int. 43 2003 389 392 (Pubitemid 36561292)
52. S.K. Rodal, G. Skretting, O. Garred, F. Vilhardt, B. van Deurs, and K. Sandvig Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles Mol. Biol. Cell 10 1999 961 974 (Pubitemid 29193724)
53. F.A. Ruiz, C.R. Lea, E. Oldfield, and R. Docampo Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes J. Biol. Chem. 279 2004 44250 44257 (Pubitemid 39430828)
54. M. Shaikh, J. Mohanty, P.K. Singh, W.M. Nau, and H. Pal Complexation of acridine orange by cucurbit[7]uril and beta-cyclodextrin: photophysical effects and pKa shifts Photochem. Photobiol. Sci. 7 4 2008 408 414 (Pubitemid 351490301)
55. K.M. Shastri, A.C. Carvalho, and R.S. Lees Platelet function and platelet lipid composition in the dyslipoproteinemias J. Lipid. Res. 21 1980 467 472 (Pubitemid 11235483)
56. S.J. Shattil, R. Anaya-Galindo, J. Bennett, R.W. Colman, and R.A. Cooper Platelet hypersensitivity induced by cholesterol incorporation J. Clin. Invest. 55 1975 636 643
57. S.J. Shattil, J.S. Bennett, R.W. Colman, and R.A. Cooper Abnormalities of cholesterol-phospholipid composition in platelets and low-density lipoproteins of human hyperbetalipoproteinemia J. Lab. Clin. Med. 89 1977 341 353 (Pubitemid 8100790)
58. M. Shiraishi, E. Tani, and A. Miyamoto Modulation of rabbit platelet aggregation and calcium mobilization by platelet cholesterol content J. Vet. Med. Sci. 72 2010 285 292
59. H.J. Shu, C.M. Zeng, C. Wang, D.F. Covey, C.F. Zorumski, and S. Mennerick Cyclodextrins sequester neuroactive steroids and differentiate mechanisms that rate limit steroid actions Br. J. Pharmacol. 150 2007 164 175 (Pubitemid 46160606)
60. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572 (Pubitemid 27248754)
61. T.L. Steck, J. Ye, and Y. Lange Probing red cell membrane cholesterol movement with cyclodextrin Biophys. J. 83 2002 2118 2125
62. M.J. Stuart, J.M. Gerrard, and J.G. White Effect of cholesterol on production of thromboxane B2 by platelets in vitro N. Engl. J. Med. 302 1980 6 10 (Pubitemid 10212230)
63. A.S. Tarasenko, R.V. Sivko, N.V. Krisanova, N.H. Himmelreich, and T.A. Borisova Cholesterol depletion from the plasma membrane impairs proton and glutamate storage in synaptic vesicles of nerve terminals J. Mol. Neurosci. 41 2010 358 367
64. E. Taverna, E. Saba, J. Rowe, M. Francolini, F. Clementi, and P. Rosa Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes J. Biol. Chem. 279 2004 5127 5134 (Pubitemid 38220529)
65. C. Thiele, M.J. Hannah, F. Fahrenholz, and W.B. Huttner Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles Nat. Cell. Biol. 2 2000 42 49
66. Y. Toyama, E. Pais, H.J. Meiselman, and T. Alexy Effects of cyclodextrins on RBC aggregation and blood viscosity Clin. Hemorheol. Microcirc. 36 2007 173 180 (Pubitemid 46328577)
67. L. Tremolizzo, J.C. DiFrancesco, V. Rodriguez-Menendez, E. Sirtori, M. Longoni, A. Cassetti, M. Bossi, S. El Mestikawy, G. Cavaletti, and C. Ferrarese Human platelets express the synaptic markers VGLUT1 and 2 and release glutamate following aggregation Neurosci. Lett. 404 2006 262 265 (Pubitemid 44108439)
68. H.I. Tsai, L.H. Tsai, M.Y. Chen, and Y.C. Chou Cholesterol deficiency perturbs actin signaling and glutamate homeostasis in hippocampal astrocytes Brain Res. 1104 2006 27 38
69. 2+ and protein kinase C in the serotonin (5-HT) transport in human platelets Cell Calcium 31 2002 235 244 (Pubitemid 34778059)
70. M. Van Lier, S. Verhoef, S. Cauwenberghs, J.W. Heemskerk, J.W. Akkerman, and H.F. Heijnen Role of membrane cholesterol in platelet calcium signalling in response to VWF and collagen under stasis and flow Thromb. Haemost. 99 2008 1068 1078 (Pubitemid 351810489)
71. A.A. Waheed, Y. Shimada, H.F.G. Heijnen, M. Nakamura, M. Inomata, M. Hayashi, S. Iwashita, J.W. Slot, and Y. Ohno-Iwashita Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts) PNAS. 98 2001 4926 4931 (Pubitemid 32397059)
72. Y. Wang, M. Gottlieb, and V.I. Teichberg An evaluation of erythrocytes as plasma glutamate scavengers for enhanced brain-to-blood glutamate efflux Neurochem. Res. 29 2004 755 760 (Pubitemid 38429194)
73. C.R. Wasser, M. Ertunc, X. Liu, and E.T. Kavalali Cholesterol-dependent balance between evoked and spontaneous vesicle recycling J. Physiol. 579 2007 413 429 (Pubitemid 46351759)
74. J.G. White The dense bodies of human platelets: Inherent electron opacity of the serotonin storage particles Blood 33 1969 598 606
75. F. Xia, X. Gao, E. Kwan, P.P. Lam, L. Chan, K. Sy, L. Sheu, M.B. Wheeler, H.Y. Gaisano, and R.G. Tsushima Disruption of pancreatic beta-cells lipid rafts modifies Kv2.1 channel gating and insulin exocytosis J. Biol. Chem. 279 2004 24685 24691 (Pubitemid 38725336)
76. F. Xia, Y.M. Leung, G. Gaisano, X. Gao, Y. Chen, J.E. Manning Fox, A. Bhattacharjee, M.B. Wheeler, H.Y. Gaisano, and R.G. Tsushima Targeting of Kv4, Cav1.2 and SNARE proteins to cholesterol-rich lipid rafts in pancreatic alpha-cells: effects on glucagon stimulus-secretion coupling Endocrinology 148 2007 2157 2167
77. P.G. Yancey, W.V. Rodrigueza, E.P. Kilsdonk, G.W. Stoudt, W.J. Johnson, M.C. Phillips, and G.H. Rothblat Cellular cholesterol efflux mediated by cyclodextrins J. Biol. Chem. 271 1996 16026 16034
78. J. Zahavi, J.D. Betteridge, N.A. Jones, D.J. Galton, and V.V. Kakkar Enhanced in vivo platelet release reaction and malondialdehyde formation in patients with hyperlipidemia Am. J. Med. 70 1981 59 64 (Pubitemid 11183517)
79. O. Zamir, and M.P. Charlton Cholesterol and synaptic transmitter release at crayfish neuromuscular junctions J. Physiol. 571 2006 83 99
80. R. Zidovetzki, and I. Levitan Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies Biochim. Biophys. Acta 1768 2007 1311 1324 (Pubitemid 46782714)
81. A. Zlatkis, B. Zak, and A.J. Boyle A new method for the direct determination of serum cholesterol J. Lab. Clin. Med. 41 1953 486 492