Seizure control by decanoic acid through direct AMPA receptor inhibition

Brain

Volumn 139, Issue 2, 2016, Pages 431-443

  Chang, Pishan ^a   Augustin, Katrin ^a   Boddum, Kim ^b   Williams, Sophie ^b   Sun, Min ^b   Terschak, John A ^c   Hardege, Jörg D ^c   Chen, Philip E ^a   Walker, Matthew C ^b   Williams, Robin S B ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF HULL   (United Kingdom)

Author keywords

AMPA receptors; decanoic acid; epilepsy; ketogenic diet; seizure control

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; ANTICONVULSIVE AGENT; DECANOIC ACID; KETONE; MEDIUM CHAIN TRIACYLGLYCEROL; PERAMPANEL; DECANOIC ACID DERIVATIVE; PROTEIN BINDING;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; EPILEPSY; EX VIVO STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HETEROLOGOUS EXPRESSION; HIPPOCAMPAL SLICE; KETOGENIC DIET; MALE; NEUROTRANSMISSION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; RAT; SEIZURE; XENOPUS; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; FEMALE; HIPPOCAMPUS; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; SEIZURES; SPRAGUE DAWLEY RAT; XENOPUS LAEVIS;

ANIMALS; DECANOIC ACIDS; FEMALE; HIPPOCAMPUS; MALE; ORGAN CULTURE TECHNIQUES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SEIZURES; XENOPUS LAEVIS;

EID: 84977079443     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv325     Document Type: Article

References (63)

1. Arai AC. GYKI 52466 has positive modulatory effects on AMPA receptors. Brain Res 2001; 892: 396-400
2. Arai Y, Mizuguchi M, Takashima S. Developmental changes of glutamate receptors in the rat cerebral cortex and hippocampus. Anat Embryol (Berl) 1997; 195: 65-70
3. Beneyto M, Meador-Woodruff JH. Expression of transcripts encoding AMPA receptor subunits and associated postsynaptic proteins in the macaque brain. J Comp Neurol 2004; 468: 530-54
4. Bough KJ, Rho JM. Anticonvulsant mechanisms of the ketogenic diet. Epilepsia 2007; 48: 43-58
5. Ceolin L, Bortolotto ZA, Bannister N, Collingridge GL, Lodge D, Volianskis A. A novel anti-epileptic agent, perampanel, selectively inhibits AMPA receptor-mediated synaptic transmission in the hippocampus. Neurochem Int 2012; 61: 517-22
6. Chang P, Orabi B, Deranieh RM, Dham M, Hoeller O, Shimshoni JA, et al. The antiepileptic drug valproic acid and other medium-chain fatty acids acutely reduce phosphoinositide levels independently of inositol in Dictyostelium. Dis Model Mech 2012; 5: 115-24
7. Chang P, Terbach N, Plant N, Chen PE, Walker MC, Williams RS. Seizure control by ketogenic diet-associated medium chain fatty acids. Neuropharmacology 2013; 69: 105-14
8. Chang P, Walker MC, Williams RS. Seizure-induced reduction in PIP3 levels contributes to seizure-activity and is rescued by valproic acid. Neurobiol Dis 2014a; 62: 296-306
9. Chang P, Zuckermann A, Williams S, Close AJ, Cano-Jaimez M, McEvoy JP, et al. Seizure control by derivatives of medium chain fatty acids associated with the ketogenic diet show novel branchingpoint structure for enhanced potency. J Pharmacol Exp Ther 2014b; 352: 43-52
10. Chapman AG. Glutamate and epilepsy. J Nutr 2000; 130: 1043S-5S
11. Clements JD, Lester RA, Tong G, Jahr CE, Westbrook GL. The time course of glutamate in the synaptic cleft. Science 1992; 258: 1498-501
12. Courchesne-Loyer A, Fortier M, Tremblay-Mercier J, Chouinard-Watkins R, Roy M, Nugent S, et al. Stimulation of mild, sustained ketonemia by medium-chain triacylglycerols in healthy humans: estimated potential contribution to brain energy metabolism. Nutrition 2013; 29: 635-40
13. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 1989; 495: 387-95
14. Dean HG, Bonser JC, Gent JP. HPLC analysis of brain and plasma for octanoic and decanoic acids. Clin Chem 1989; 35: 1945-8
15. Friedman LK, Pellegrini-Giampietro DE, Sperber EF, Bennett MV, Moshe SL, Zukin RS. Kainate-induced status epilepticus alters glutamate and GABAA receptor gene expression in adult rat hippocampus: an in situ hybridization study. J Neurosci 1994; 14: 2697-707
16. Haidukewych D, Forsythe WI, Sills M. Monitoring octanoic and decanoic acids in plasma from children with intractable epilepsy treated with medium-chain triglyceride diet. Clin Chem 1982; 28: 642-5
17. Hughes SD, Kanabus M, Anderson G, Hargreaves IP, Rutherford T, O'Donnell M, et al. The ketogenic diet component decanoic acid increases mitochondrial citrate synthase and complex I activity in neuronal cells. J Neurochem 2014; 129: 426-33
18. Huttenlocher PR. Ketonemia and seizures: metabolic and anticonvulsant effects of two ketogenic diets in childhood epilepsy. Pediatr Res 1976; 10: 536-40
19. Huttenlocher PR, Wilbourn AJ, Signore JM. Medium-chain triglycerides as a therapy for intractable childhood epilepsy. Neurology 1971; 21: 1097-103
20. Juge N, Gray JA, Omote H, Miyaji T, Inoue T, Hara C, et al. Metabolic control of vesicular glutamate transport and release. Neuron 2010; 68: 99-112
21. Kim DY, Simeone KA, Simeone TA, Pandya JD, Wilke JC, Ahn Y, et al. Ketone bodies mediate anti-seizure effects through mitochondrial permeability transition. Ann Neurol 2015; 78: 77-87
22. Kinsman SL, Vining EP, Quaskey SA, Mellits D, Freeman JM. Efficacy of the ketogenic diet for intractable seizure disorders: review of 58 cases. Epilepsia 1992; 33: 1132-6
23. Kossoff EH, Rho JM. Ketogenic diets: evidence for short-and longterm efficacy. Neurotherapeutics 2009; 6: 406-14
24. Laux L, Blackford R. The ketogenic diet in Dravet syndrome. J Child Neurol 2013; 28: 1041-4
25. Levy RG, Cooper PN, Giri P. Ketogenic diet and other dietary treatments for epilepsy. Cochrane Database Syst Rev 2012; 3: CD001903
26. Likhodii SS, Musa K, Mendonca A, Dell C, Burnham WM, Cunnane SC. Dietary fat, ketosis, and seizure resistance in rats on the ketogenic diet. Epilepsia 2000; 41: 1400-10
27. Liu YM. Medium-chain triglyceride (MCT) ketogenic therapy. Epilepsia 2008; 49 Suppl 8: 33-6
28. Masino SA, Li T, Theofilas P, Sandau US, Ruskin DN, Fredholm BB, et al. A ketogenic diet suppresses seizures in mice through adenosine A(1) receptors. J Clin Invest 2011; 121: 2679-83
29. Meldrum BS, Rogawski MA. Molecular targets for antiepileptic drug development. Neurotherapeutics 2007; 4: 18-61
30. Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, et al. AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. J Comput Chem 2009; 30: 2785-91
31. Nakamura J, Miwa T, Sasaki H, Shibasaki J, Kaneto H. Effect of straight chain fatty acids on seizures induced by picrotoxin and pentylenetetrazole in mice. J Pharmacobiodyn 1990; 13: 76-81
32. Neal EG, Chaffe H, Schwartz RH, Lawson MS, Edwards N, Fitzsimmons G, et al. A randomized trial of classical and mediumchain triglyceride ketogenic diets in the treatment of childhood epilepsy. Epilepsia 2009; 50: 1109-17
33. Neal EG, Cross JH. Efficacy of dietary treatments for epilepsy. J Hum Nutr Diet 2010; 23: 113-19
34. Oldendorf WH. Carrier-mediated blood-brain barrier transport of short-chain monocarboxylic organic acids. Am J Physiol 1973; 224: 1450-3
35. Page KA, Williamson A, Yu N, McNay EC, Dzuira J, McCrimmon RJ, et al. Medium-chain fatty acids improve cognitive function in intensively treated type 1 diabetic patients and support in vitro synaptic transmission during acute hypoglycemia. Diabetes 2009; 58: 1237-44
36. Pan Y, Larson B, Araujo JA, Lau W, de Rivera C, Santana R, et al. Dietary supplementation with medium-chain TAG has long-lasting cognition-enhancing effects in aged dogs. Br J Nutr 2010; 103: 1746-54
37. Pulsifer MB, Gordon JM, Brandt J, Vining EP, Freeman JM. Effects of ketogenic diet on development and behavior: preliminary report of a prospective study. Dev Med Child Neurol 2001; 43: 301-6
38. Rektor I. Perampanel, a novel, non-competitive, selective AMPA receptor antagonist as adjunctive therapy for treatment-resistant partialonset seizures. Expert Opin Pharmacother 2013; 14: 225-35
39. Rho JM, Sankar R. The ketogenic diet in a pill: is this possible? Epilepsia 2008; 49 (Suppl 8): 127-33
40. Rho JM, Stafstrom CE. The ketogenic diet: What has science taught us? Epilepsy Res 2011; 100: 203-346
41. Rogawski MA. Revisiting AMPA receptors as an antiepileptic drug target. Epilepsy Curr 2011; 11: 56-63
42. Rogawski MA, Donevan SD. AMPA receptors in epilepsy and as targets for antiepileptic drugs. Adv Neurol 1999; 79: 947-63
43. Rogawski MA, Hanada T. Preclinical pharmacology of perampanel, a selective non-competitive AMPA receptor antagonist. Acta Neurol Scand Suppl 2013; 19-24
44. Rugg-Gunn F. Adverse effects and safety profile of perampanel: a review of pooled data. Epilepsia 2014; 55 (Suppl 1): 13-15
45. Russo E, Gitto R, Citraro R, Chimirri A, De SG. New AMPA antagonists in epilepsy. Expert Opin Investig Drugs 2012; 21: 1371-89
46. Sada N, Lee S, Katsu T, Otsuki T, Inoue T. Epilepsy treatment. Targeting LDH enzymes with a stiripentol analog to treat epilepsy. Science 2015; 347: 1362-7
47. Sanderson DJ, Good MA, Seeburg PH, Sprengel R, Rawlins JN, Bannerman DM. The role of the GluR-A (GluR1) AMPA receptor subunit in learning and memory. Prog Brain Res 2008; 169: 159-78
48. Santos SD, Carvalho AL, Caldeira MV, Duarte CB. Regulation of AMPA receptors and synaptic plasticity. Neuroscience 2009; 158: 105-25
49. Sills MA, Forsythe WI, Haidukewych D. Role of octanoic and decanoic acids in the control of seizures. Arch Dis Child 1986a; 61: 1173-7
50. Sills MA, Forsythe WI, Haidukewych D, MacDonald A, Robinson M. The medium chain triglyceride diet and intractable epilepsy. Arch Dis Child 1986b; 61: 1168-72
51. Steinhoff BJ, Hamer H, Trinka E, Schulze-Bonhage A, Bien C, Mayer T, et al. A multicenter survey of clinical experiences with perampanel in real life in Germany and Austria. Epilepsy Res 2014; 108: 986-8
52. Szenasi G, Vegh M, Szabo G, Kertesz S, Kapus G, Albert M, et al. 2,3-benzodiazepine-type AMPA receptor antagonists and their neuroprotective effects. Neurochem Int 2008; 52: 166-83
53. Talos DM, Follett PL, Folkerth RD, Folkerth RD, Follett PL, Volpe JJ, et al. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. II. Human cerebral white matter and cortex. J Comp Neurol 2006; 497: 61-77
54. Thavendiranathan P, Mendonca A, Dell C, Likhodii SS, Musa K, Iracleous C, et al. The MCT ketogenic diet: effects on animal seizure models. Exp Neurol 2000; 161: 696-703
55. Thio LL, Wong M, Yamada KA. Ketone bodies do not directly alter excitatory or inhibitory hippocampal synaptic transmission. Neurology 2000; 54: 325-31
56. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 2010; 62: 405-96
57. Vanstraten AF, Ng YT. Update on the management of Lennox-Gastaut syndrome. Pediatr Neurol 2012; 47: 153-61
58. Veggiotti P, De Giorgis, V. Dietary treatments and new therapeutic perspective in GLUT1 deficiency syndrome. Curr Treat Options Neurol 2014; 16: 291
59. Wang G, Gilbert J, Man HY. AMPA receptor trafficking in homeostatic synaptic plasticity: functional molecules and signaling cascades. Neural Plast 2012; 2012: 825364
60. Washburn MS, Dingledine R. Block of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J Pharmacol Exp Ther 1996; 278: 669-78
61. Wlaz P, Socala K, Nieoczym D, Luszczki JJ, Zarnowska I, Zarnowski T, et al. Anticonvulsant profile of caprylic acid, a main constituent of the medium-chain triglyceride (MCT) ketogenic diet, in mice. Neuropharmacology 2012; 62: 1882-9
62. Wlaz P, Socala K, Nieoczym D, Zarnowski T, Zarnowska I, Czuczwar SJ, et al. Acute anticonvulsant effects of capric acid in seizure tests in mice. Prog Neuropsychopharmacol Biol Psychiatry 2015; 57: 110-16
63. Xu X, Muller-Taubenberger A, Adley KE, Pawolleck N, Lee VW, Wiedemann C, et al. Attenuation of phospholipid signaling provides a novel mechanism for the action of valproic acid. Eukaryot Cell 2007; 6: 899-906.