β-Hydroxybutyrate supports synaptic vesicle cycling but reduces endocytosis and exocytosis in rat brain synaptosomes

Neurochemistry International

Volumn 93, Issue , 2016, Pages 73-81

  Hrynevich, Sviatlana V ^a   Waseem, Tatyana V ^a   Hébert, Audrey ^b   Pellerin, Luc ^b   Fedorovich, Sergei V ^a  

^a INSTITUTE OF PHOTOBIOLOGY   (Belarus)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Endocytosis; Ketogenic diet; Ketone bodies; Synaptic vesicles; Synaptosomes; Hydroxybutyrate

Indexed keywords

3 HYDROXYBUTYRIC ACID; ACRIDINE ORANGE; GLUCOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN CELL CULTURE; BRAIN SYNAPTOSOME; CELL CYCLE; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; ENDOCYTOSIS; ENERGY RESOURCE; EXOCYTOSIS; KETOGENESIS; KETOGENIC DIET; MALE; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; ANIMAL; BRAIN; DRUG EFFECTS; SYNAPTOSOME; WISTAR RAT;

3-HYDROXYBUTYRIC ACID; ANIMALS; BRAIN; ENDOCYTOSIS; EXOCYTOSIS; MALE; RATS; RATS, WISTAR; SYNAPTIC VESICLES; SYNAPTOSOMES;

EID: 84958741342     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.12.014     Document Type: Article

References (60)

1. D. Attwell, and A. Gibb Neuroenergetic and the kinetic design of excitatory synapses Nat. Rev. Neurosci. 6 2005 841 849
2. D. Attwell, and S.B. Laughlin An energy budget for signaling in the grey matter of the brain J. Cereb. Blood Flow. Metab. 21 2001 1133 1145
3. K. Ballaban-Gil, C. Callahan, C. O'Dell, M. Pappo, S. Moshe, and S. Shinnar Complications of the ketogenic diet Epilepsia 39 1998 744 748
4. ATP channels and reduces ischaemic damage in rat hippocampus J. Neurochem. 90 2004 1243 1250
5. L.H. Bergersen Lactate transport and signaling in the brain: potential therapeutic targets and roles in body-brain interaction J. Cereb. Blood Flow. Metab. 35 2015 176 185
6. G.J. Brewer, J.R. Torricelli, E.K. Evege, and P.J. Price Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination J. Neurosci. Res. 35 1993 567 576
7. G.J. Brewer Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus J. Neurosci. Res. 42 1995 674 683
8. J. Burrone, Z. Li, and V. Murthy Studying vesicle cycling in presynaptic terminals using the genetically encoded probe synaptopHluorin Nat. Protoc. 1 2006 2970 2978
9. M.A. Castro, F.A. Beltran, S. Brauchi, and I.I. Concha A metabolic switch in brain: glucose and lactate metabolism modulation by ascorbic acid J. Neurochem. 110 2009 423 440
10. M.A. Cousin, and P.J. Robinson Two mechanisms of synaptic vesicle recycling in rat brain synaptosomes J. Neurochem. 75 2000 1645 1653
11. E.N. Dedkova, and L.A. Blatter Role of β-hydroxybutyrate, its polymer poly-β-hydroxybutyrate and inorganic polyphosphate in mammalian health and disease Front. Physiol. 5 2014 260
12. P. Dhar-Chowdhury, B. Malester, P. Rajacic, and W.A. Coetzee The regulation of ion channels and transporters by glycolytically derived ATP Cell. Mol. Life Sci. 64 2007 3069 3083
13. K.A.C. Elliott, M.E. Greig, and M.P. Benoy The metabolism of lactic and pyruvic acids in normal and tumour tissues. III Rat liver, brain and testis Biochem. J. 31 1937 1003 1020
14. S.V. Fedorovich, T.V. Waseem, T.V. Lavrukevich, and S.V. Konev Role of calcium in exocytosis induced by hypotonic swelling Ann. N. Y. Acad. Sci. 1048 2005 337 340
15. L.B. Gano, M. Patel, and J.M. Rho Ketogenic diets, mitochondria, and neurological diseases J. Lipid Res. 55 2014 2211 2228
16. J.R. Garbow, J.M. Doherty, R.C. Schugar, S. Travers, M.L. Weber, A.E. Wentz, N. Ezenwajiaku, D.G. Cotter, E.M. Brunt, and P.A. Crawford Hepatic steatosis, inflammation, and ER stress in mice maintained long term on a very low-carbohydrate ketogenic diet Am. J. Physiol. Gastrointest. Liver Physiol. 300 2011 G956 G967
17. ATP channel activity confers resistance to epileptic seizures Neuron 74 2012 719 730
18. F. Hajos An improved method for the preparation of synaptosomal fractions in high purity Brain Res. 93 1975 485 489
19. J.J. Harris, R. Jolivet, and D. Attwell Synaptic energy use and supply Neuron 75 2012 762 777
20. R.A. Hawkins, D.H. Williamson, and H.A. Krebs Ketone-body utilization by adult and suckling rat brain in vivo Biochem. J. 122 1971 13 18
21. C.D. Holmgren, M. Mukhtarov, A.E. Malkov, I.Y. Popova, P. Bregestovski, and Y. Zilberter Energy substrate availability as a determinant of neuronal resting potential, GABA signaling and spontaneous network activity in the neonatal cortex in vitro J. Neurochem. 112 2010 900 912
22. S.V. Hrynevich, T.G. Pekun, T.V. Waseem, and S.V. Fedorovich Influence of glucose deprivation on membrane potentials of plasma membranes, mitochondria and synaptic vesicles in rat brain synaptosomes Neurochem. Res. 40 2015 1188 1196
23. Y. Hua, A. Woehler, M. Kahms, V. Haucke, E. Neher, and J. Klingauf Blocking endocytosis enhances short-term synaptic depression under conditions of normal availability of vesicles Neuron 80 2013 343 349
24. A. Ikemoto, D.G. Bole, and T. Ueda Glycolisis and glutamate accumulation into synaptic vesicles. Role of glyceraldehyde phosphate dehydrogenase and 3-phosphoglycerate kinase J. Biol. Chem. 278 2003 5929 5940
25. Y. Izumi, K. Ishii, H. Katsuki, A.M. Benz, and C.F. Zorumski β-hydroxybutyrate fuels synaptic function during development. Histological and physiological evidence in rat hippocampal slices J. Clin. Invest 101 1998 1121 1132
26. N. Juge, J.A. Gray, H. Omote, T. Miyaji, T. Inoue, C. Hara, H. Uneyama, R.H. Edwards, R.A. Nicoll, and Y. Moriyama Metabolic control of vesicular glutamate transport and release Neuron 68 2010 99 112
27. A. Julio-Amilpas, T. Montiel, E. Soto-Tinoco, C. Geronimo-Olvera, and L. Massieu Protection of hypoglycemia-induced neuronal death by β-hydroxybutyrate involves the preservation of energy levels and decreased production of reactive oxygen species J. Cereb. Blood Flow. Metab. 35 2015 851 860
28. R.A. Kauppinen, and D.G. Nicholls Synaptosomal bioenergetics. The role of glycolisis, pyruvate oxidation and responses to hypoglycaemia Eur. J. Biochem. 158 1986 159 165
29. S.S. Kety, and C.F. Schmidt The effects of active and passive hyperventilation on cerebral blood flow, cerebral oxygen consumption, cardiac output, and blood pressure of normal young men J. Clin. Invest 25 1946 107 119
30. D.Y. Kim, J. Vallejo, and J.M. Rho Ketones prevent synaptic dysfunction induced by mitochondrial respiratory complex inhibitors J. Neurochem. 114 2010 130 141
31. O. Lowry, H. Rosenbrough, H. Farr, and R. Randall Protein measurements with Folin reagent J. Biol. Chem. 193 1951 265 279
32. ATP channel receptor sensitivity J. Neurochem. 132 2015 520 531
33. M.C. McKenna, J.T. Tildon, J.H. Stevenson, I.B. Hopkins, X. Huang, and R. Couto Lactate transport by cortical synaptosomes from adult rat brain: characterization of kinetics and inhibitor specificity Dev. Neurosci. 20 1998 300 309
34. M.A. McNally, and A.L. Hartman Ketone bodies in epilepsy J. Neurochem. 121 2012 28 35
35. G. Miesenbock, D.A. De Angelis, and J.E. Rothman Vizualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins Nature 394 1998 192 195
36. F.D. Morgenthaler, R. Kraftsik, S. Catsikas, P.J. Magistretti, and J.-Y. Chatton Glucose and lactate are equally effective in energizing activity-dependent synaptic vesicle turnover in purified cortical neurons Neuroscience 141 2006 157 165
37. M. Mukhtarov, A. Ivanov, Y. Zilberter, and P. Bregestovski Inhibition of spontaneous network activity in neonatal hippocampal slices by energy substrates is not correlated with intracellular acidification J. Neurochem. 116 2011 316 321
38. M. Osada-Oka, Y. Hashiba, S. Akiba, S. Imaoka, and T. Sato Glucose is necessary for stabilization of hypoxia-inducible factor-1á under hypoxia: contribution of the pentose phosphate pathway to this stabilization FEBS Lett. 584 2010 3073 3079
39. A. Paoli, A. Bianco, E. Damiani, and G. Bosco Ketogenic diet in neuromuscular and neurodegenerative diseases Biomed. Res. Int. 2014 2014 474296
40. D. Pathak, L. Shields, B.A. Mendelsohn, D. Haddad, W. Lin, A.A. Gerencser, H. Kim, M.D. Brand, R.H. Edwards, and K. Nakamura The role of mitochondrially derived ATP in synaptic vesicle recycling J. Biol. Chem. 290 2015 22325 22336
41. L. Pellerin, and P.J. Magistretti Sweet sixteen for ANLS J. Cereb. Blood Flow. Metab. 32 2012 1152 1166
42. M.G. Peterman The ketogenic diet in the treatment of epilepsy: a preliminary report Am. J. Dis. Child. 28 1924 28 33
43. K. Pierre, and L. Pellerin Monocarboxylate transporters in the central nervous system: distribution, regulation and function J. Neurochem. 94 2005 1 14
44. V. Rangaraju, N. Calloway, and T.A. Ryan Activity-driven local ATP synthesis is required for synaptic function Cell 156 2014 825 835
45. C. Robinet, and L. Pellerin Brain-derived neurotrophic factor enhances the expression of the monocarboxylate transporter 2 through translation activation in mouse cultured cortical neurons J. Cereb. Blood Flow. Metab. 30 2010 286 298
46. P. Rodriguez-Rodriguez, A. Almeida, and J.P. Bolanos Brain energy metabolism in glutamate-receptor activation and excitotoxicity: role for APC/C-Cdh1 in the balance glycolysis/penthose phosphate pathway Neurochem. Int. 62 2013 750 756
47. F.S. Rolleston, and E.A. Newsholme Effects of fatty acids, ketone bodies, lactate and pyruvate on glucose utilization by guinea-pig cerebral cortex slices Biochem. J. 104 1967 519 523
48. A. Sampath, E.H. Kossoff, S.L. Furth, P.L. Pyzik, and E.P. Vining Kidney stones ant ketogenic diet: risk factors and prevention J. Child. Neurol. 22 2007 375 378
49. C.E. Stafstrom, and J.M. Rho The ketogenic diet as a treatment paradigm for diverse neurological disorders Front Pharmacol 3 2012 59
50. T.C. Südhof The synaptic vesicle cycle Annu. Rev. Neurosci. 27 2004 509 547
51. T.C. Südhof Neurotransmitter release: the last millisecond in the life of a synaptic vesicle Neuron 80 2013 675 690
52. A.S. Tarasenko, M.V. Linetska, L.G. Storchak, and N.H. Himmelreich Effectiveness of extracellular lactate/pyruvate for sustaining synaptic vesicle proton gradient generation and vesicular accumulation of GABA J. Neurochem. 99 2006 787 796
53. M. Toei, R. Saum, and M. Forgac Regulation and isoform function of the V-ATPases Biochemistry 49 2010 4715 4723
54. Y.C. Tsai, Y.C. Chou, A.B. Wu, C.M. Hu, C.Y. Chen, F.A. Chen, and J.A. Lee Stereoselective effects of 3-hydroxybutyrate on glucose utilization of rat cardiomyocytes Life Sci. 78 2006 1385 1391
55. T.V. Waseem, A.A. Rakovich, T.V. Lavrukevich, S.V. Konev, and S.V. Fedorovich Calcium regulates the mode of exocytosis induced by hypotonic shock in isolated neuronal presynaptic endings Neurochem. Int. 46 2005 235 242
56. T.V. Waseem, V.A. Kolos, L.P. Lapatsina, and S.V. Fedorovich Hypertonic shrinking but not hypotonic swelling increases sodium concentration in rat brain synaptosomes Brain Res Bull. 73 2007 135 142
57. T.V. Waseem, and S.V. Fedorovich Presynaptic glycine receptors influence plasma membrane potential and glutamate release Neurochem. Res. 35 2010 1188 1195
58. B.G. Wilhelm, S. Mandad, S. Truckenbrodt, K. Kröhnert, C. Schäfer, B. Rammner, S.J. Koo, G.A. Claβen, M. Krauss, V. Haucke, H. Urlaub, and S.O. Rizzoli Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins Science 344 2014 1023 1028
59. H. White, and B. Venkatesh Clinical review: ketones and brain injury Crit. Care 15 2011 219
60. F. Zoccarato, L. Cavallini, and A. Alexandre The pH-sensitive dye acridine orange as a tool to monitor exocytosis/endocytosis in synaptosomes J. Neurochem. 72 1999 625 633