Neuroprotection by lowering cholesterol: A decrease in membrane cholesterol content reduces transporter-mediated glutamate release from brain nerve terminals

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 10, 2012, Pages 1553-1561

  Krisanova, N ^a   Sivko, R ^a   Kasatkina, L ^a   Borisova, T ^a  

^a PALLADIN INSTITUTE OF BIOCHEMISTRY   (Ukraine)

Author keywords

Ambient glutamate; Cholesterol; Methyl cyclodextrin; Neuroprotection; Synaptosomes; Transporter mediated glutamate release

Indexed keywords

CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; CHOLESTEROL; FILIPIN; GLUTAMATE DEHYDROGENASE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; HYDROGENASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; METHYL BETA CYCLODEXTRIN;

ANIMAL CELL; ARTICLE; BRAIN HOMOGENATE; BRAIN HYPOXIA; BRAIN ISCHEMIA; BRAIN NERVE CELL; BRAIN SYNAPTOSOME; CELL MEMBRANE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; HYDROPHILICITY; ISOTOPE LABELING; MALE; MEMBRANE DEPOLARIZATION; NERVE ENDING; NEUROPROTECTION; NEUROTOXICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; RAT; SPECTROFLUOROMETRY; STROKE; SYNAPSE VESICLE; TRAUMATIC BRAIN INJURY;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BETA-CYCLODEXTRINS; BRAIN; BRAIN INJURIES; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CELL MEMBRANE; CHOLESTEROL; GLUTAMIC ACID; HYPOXIA-ISCHEMIA, BRAIN; MALE; MEMBRANE POTENTIALS; NERVE ENDINGS; NEUROPROTECTIVE AGENTS; PROTONS; RATS; RATS, WISTAR; SODIUM; STROKE; SYNAPTIC VESICLES; SYNAPTOSOMES;

RATTUS;

EID: 84864255374     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.06.005     Document Type: Article

References (57)

1. Cavelier P., Attwell D. Tonic release of glutamate by a DIDS-sensitive mechanism in rat hippocampal slices. J. Physiol. 2005, 564:397-410.
2. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 2001, 65:1-105.
3. Rossi D.J., Oshima T., Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 2000, 403:316-321.
4. Yi J.H., Hazell A.S. Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem. Int. 2006, 48:394-403.
5. Phillis J.W., Ren J., O'Regan M.H. Transporter reversal as a mechanism of glutamate release from the ischemic rat cerebral cortex: studies with dl-threo-beta-benzyloxyaspartate. Brain Res. 2000, 868:105-112.
6. Grewer C., Gameiro A., Zhang Z., Tao Z., Braams S., Rauen T. Glutamate forward and reverse transport: from molecular mechanism to transporter-mediated release after ischemia. IUBMB Life 2008, 60:609-619.
7. Nishida A., Iwata H., Kudo Y., Kobayashi T., Matsuoka Y., Kanai Y., Endou H. Measurement of glutamate uptake and reversed transport by rat synaptosome transporters. Biol. Pharm. Bull. 2004, 27:813-816.
8. Butchbach M., Tian G., Guo H., Lin C.L. Association of excitatory amino acid transporters, especially EAAT2, with cholesterol-rich lipid raft microdomains. J. Biol. Chem. 2004, 279:34388-34396.
9. González M.I., Susarla B.T., Fournier K.M. Constitutive endocytosis and recycling of the neuronal glutamate transporter, excitatory amino acid carrier 1. J. Neurochem. 2007, 103:1917-1931.
10. Lang T., Bruns D., Wenzel D., Riedel D., Holroyd P., Thiele C., Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 2001, 20:2202-2213.
11. Tsai H.I., Tsai L.H., Chen M.Y., Chou Y.C. Cholesterol deficiency perturbs actin signaling and glutamate homeostasis in hippocampal astrocytes. Brain Res. 2006, 1104:27-38.
12. Borisova T., Krisanova N., Sivko R., Borysov A. Cholesterol depletion attenuates tonic release but increases the ambient level of glutamate in rat brain synaptosomes. Neurochem. Int. 2010, 56:466-478.
13. Jennings L.J., Xu Q.W., Firth T.A. Cholesterol inhibits spontaneous action potentials and calcium currents in guinea pig gallbladder smooth muscle. Am. J. Physiol. 1999, 277:1017-1026.
14. Borisova T., Sivko R., Borysov A., Krisanova N. Diverse presynaptic mechanisms underlying methyl-beta-cyclodextrin-mediated changes in glutamate transport. Cell. Mol. Neurobiol. 2010, 30:1013-1023.
15. Kirsch C., Eckert G.P., Mueller W.E. Statin effects on cholesterol micro-domains in brain plasma membranes. Biochem. Pharmacol. 2003, 65:843-856.
16. Sierra S., Ramos M.C., Molina P., Esteo C., Vázquez J.A., Burgos J.S. Statins as neuroprotectants: a comparative in vitro study of lipophilicity, blood-brain-barrier penetration, lowering of brain cholesterol, and decrease of neuron cell death. J. Alzheimers Dis. 2011, 23:307-318.
17. Funck V.R., de Oliveira C.V., Pereira L.M., Rambo L.M., Ribeiro L.R., Royes L.F.F., Ferreira J., Guerra G.P., Furian A.F., Oliveira M.S., Mallmann C.A., de Mello C.F., Oliveira M.S. Differential effects of atorvastatin treatment and withdrawal on pentylenetetrazol-induced seizures. Epilepsia 2011, 52:2094-2104.
18. Bösel J., Gandor F., Harms C., Synowitz M., Harms U., Djoufack P.C., Megow D., Dirnagl U., Hörtnagl H., Fink K.B., Endres M. Neuroprotective effects of atorvastatin against glutamate-induced excitotoxicity in primary cortical neurones. J. Neurochem. 2005, 92:1386-1398.
19. Wood W.G., Eckert G.P., Igbavboa U., Müller W.E. Statins and neuroprotection: a prescription to move the field forward. Ann. N. Y. Acad. Sci. 2010, 1199:69-76.
20. Wang Q., Yan J., Chen X., Li J., Yang Y., Weng J., Deng C., Yenari M.A. Statins: multiple neuroprotective mechanisms in neurodegenerative diseases. Exp. Neurol. 2011, 230:27-34.
21. Cotman C.W. Isolation of synaptosomal and synaptic plasma membrane fractions. Methods Enzymol. 1974, 31:445-452.
22. Larson E., Howlett B., Jagendorf A. Artificial reductant enhancement of the Lowry method for protein determination. Anal. Biochem. 1986, 155:243-248.
23. Klein U., Gimpl G., Fahrenholz F. Alteration of the myometrial plasma cholesterol content with β-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry 1995, 34:13784-13793.
24. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37:911-917.
25. Zlatkis A., Zak B., Boyle A.J. A new method for the direct determination of serum cholesterol. J. Lab. Clin. Med. 1953, 41:486-492.
26. Kruth H.S., Vaughan M. Quantification of low density lipoprotein binding and cholesterol accumulation by single human fibroblasts using fluorescence microscopy. J. Lipid. Res. 1980, 21:123-130.
27. Nicholls D.G., Sihra T.S. Synaptosomes possess an exocytotic pool of glutamate. Nature 1986, 321:772-773.
28. Bezzi P., Carmignoto G., Pasti L., Vesce S., Rossi D., Rizzini B.L., Pozzan T., Volterra A. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 1998, 391:281-285.
29. Borisova T., Kasatkina L., Ostapchenko L. The proton gradient of secretory granules and glutamate transport in blood platelets during cholesterol depletion of the plasma membrane by methyl-beta-cyclodextrin. Neurochem. Int. 2011, 59:965-975.
30. Jadot M., Andrianaivo F., Dubois F., Wattiaux R. Effects of methylcyclodextrin on lysosomes. Eur. J. Biochem. 2001, 268:1392-1399.
31. Trikash I., Gumenyuk V., Lishko V. The fusion of synaptic vesicle membranes studied by lipid mixing: the R18 fluorescence assay validity. Chem. Phys. Lipids 2010, 163:778-786.
32. Dalby N.O., Mody I. Activation of NMDA receptors in rat dentate gyrus granule cells by spontaneous and evoked transmitter release. J. Neurophysiol. 2003, 90:786-797.
33. Sah P., Hestrin S., Nicoll R.A. Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science 1989, 246:815-818.
34. Jabaudon D., Scanziani M., Gähwiler B.H., Gerber U. Acute decrease in net glutamate uptake during energy deprivation. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5610-5615.
35. +-ATPase in rat brain synaptic vesicles. J. Biol. Chem. 1989, 264:8281-8288.
36. + homeostasis induced by the protonophore carbonyl cyanide-p-trifluoromethoxyphenyl-hydrazon in isolated nerve terminals. Mol. Pharm. 1998, 53:734-774.
37. Zoccarato F., Cavallini L., Alexandre A. The pH-sensitive dye acridine orange as a tool to monitor exocytosis/endocytosis in synaptosomes. J. Neurochem. 1999, 72:625-633.
38. Borisova T., Krisanova N. Presynaptic transporter-mediated release of glutamate evoked by the protonophore FCCP increases under altered gravity conditions. Adv. Space Res. 2008, 42:1971-1979.
39. Xu Y., Yan J., Zhou P., Li J., Gao H., Xia Y., Wang Q. Neurotransmitter receptors and cognitive dysfunction in Alzheimer's disease and Parkinson's disease. Prog. Neurobiol. 2012, 97:1-13.
40. Abulrob A., Tauskela J.S., Mealing G., Brunette E., Faid K., Stanimirovic D. Protection by cholesterol-extracting cyclodextrins: a role for N-methyl-d-aspartate receptor redistribution. J. Neurochem. 2005, 92:1477-1486.
41. Robinson M.B. Acute regulation of sodium-dependent glutamate transporters: a focus on constitutive and regulated trafficking. Handb. Exp. Pharmacol. 2006, 175:251-275.
42. Nagaraja T.N., Knight R.A., Croxen R.L., Konda K.P., Fenstermacher J.D. Acute neurovascular unit protection by simvastatin in transient cerebral ischemia. Neurol. Res. 2006, 28:826-830.
43. Sironi L., Cimino M., Guerrini U., Calvio A.M., Lodetti B., Asdente M., Balduini W., Paoletti R., Tremoli E. Treatment with statins after induction of focal ischemia in rats reduces the extent of brain damage. Arterioscler. Thromb. Vasc. Biol. 2003, 23:322-327.
44. Berger C., Xia F., Maurer M.H., Schwab S. Neuroprotection by pravastatin in acute ischemic stroke in rats. Brain Res. Rev. 2008, 58:48-56.
45. Chen J., Zhang C., Jiang H., Li Y., Zhang L., Robin A., Katakowski M., Lu M., Chopp M. Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J. Cereb. Blood Flow Metab. 2005, 25:281-290.
46. Zhang L., Zhang Z.G., Ding G.L., Jiang Q., Liu X., Meng H., Hozeska A., Zhang C., Li L., Morris D., Zhang R.L., Lu M., Chopp M. Multitargeted effects of statin-enhanced thrombolytic therapy for stroke with recombinant human tissue-type plasminogen activator in the rat. Circulation 2005, 112:3486-3494.
47. Sugiura S., Yagita Y., Sasaki T., Todo K., Terasaki Y., Ohyama N., Hori M., Kitagawa K. Postischemic administration of HMG CoA reductase inhibitor inhibits infarct expansion after transient middle cerebral artery occlusion. Brain Res. 2007, 1181:125-129.
48. Endres M., Laufs U., Huang Z., Nakamura T., Huang P., Moskowitz M.A., Liao J.K. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8880-8885.
49. Hess D.C., Demchuk A.M., Brass L.M., Yatsu F.M. HMG-CoA reductase inhibitors (statins): a promising approach to stroke prevention. Neurology 2000, 54:790-796.
50. Zacco A., Togo J., Spence K., Ellis A., Lloyd D., Furlong S., Piser T. 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitors protect cortical neurons from excitotoxicity. J. Neurosci. 2003, 23:11104-11111.
51. Wang Q., Zengin A., Deng C., Li Y., Newell K.A., Yang G.Y., Lu Y., Wilder-Smith E.P., Zhao H., Huang X.F. High dose of simvastatin induces hyperlocomotive and anxiolytic-like activities: the association with the up-regulation of NMDA receptor binding in the rat brain. Exp. Neurol. 2009, 216:132-138.
52. Ponce J., de la Ossa N.P., Hurtado O., Millan M., Arenillas J.F., Dávalos A., Gasull T. Simvastatin reduces the association of NMDA receptors to lipid rafts: a cholesterol-mediated effect in neuroprotection. Stroke 2008, 39:1269-1275.
53. Yan J., Xu Y., Zhu C., Zhang L., Wu A., Yang Y., Xiong Z., Deng C., Huang X.F., Yenari M.A., Yang Y.G., Ying W., Wang Q. Simvastatin prevents dopaminergic neurodegeneration in experimental parkinsonian models: the association with anti-inflammatory responses. PLoS One 2011, 6:e20945.
54. Ramirez C., Tercero I., Pineda A., Burgos J.S. Simvastatin is the statin that most efficiently protects against kainate-induced excitotoxicity and memory impairment. J. Alzheimers Dis. 2011, 24:161-174.
55. Camargo F., Erickson R.P., Garver W.S., Hossain G.S., Carbone P.N., Heidenreich R.A., Blanchard J. Cyclodextrins in the treatment of a mouse model of Niemann-Pick C disease. Life Sci. 2001, 70:131-142.
56. Monnaert V., Tilloy S., Bricout H., Fenart L., Cecchelli R., Monflier E. Behavior of alpha-, beta-, and gamma-cyclodextrins and their derivatives on an in vitro model of blood-brain barrier. J. Pharmacol. Exp. Ther. 2004, 310:745-751.
57. +-dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) of the blood-brain barrier. A mechanism for glutamate removal. J. Biol. Chem. 1999, 274:31891-31895.