γ-Hydroxybutyrate (Xyrem) ameliorates clinical symptoms and neuropathology in a mouse model of Alzheimer's disease

Neurobiology of Aging

Volumn 36, Issue 2, 2015, Pages 832-844

  Klein, Christian ^a   Mathis, Chantal ^a   Leva, Géraldine ^a   Patte Mensah, Christine ^a   Cassel, Jean Christophe ^a   Maitre, Michel ^a   Mensah Nyagan, Ayikoe G ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Alzheimer's disease; A peptides; Neprilysin; Xyrem; Hydroxybutyrate

Indexed keywords

AMYLOID BETA PROTEIN; HISTONE DEACETYLASE; MEMBRANE METALLOENDOPEPTIDASE; OXYBATE SODIUM; PHOSPHORAMIDON; HISTONE DEACETYLASE INHIBITOR;

ACUTE DRUG ADMINISTRATION; ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CHRONIC DRUG ADMINISTRATION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; MOUSE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; BRAIN; CELL CULTURE; COGNITION; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULARLY TARGETED THERAPY; ORAL DRUG ADMINISTRATION; PSYCHOLOGY;

ADMINISTRATION, ORAL; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; CELLS, CULTURED; COGNITION; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; MICE; MOLECULAR TARGETED THERAPY; NEPRILYSIN; SODIUM OXYBATE;

EID: 84922771242     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.10.003     Document Type: Article

References (66)

1. Absalom N., Eghorn L.F., Villumsen I.S., Karim N., Bay T., Olsen J.V., Knudsen G.M., Brauner-Osborne H., Frolund B., Clausen R.P., Chebib M., Wellendorph P. alpha4betadelta GABA(A) receptors are high-affinity targets for gamma-hydroxybutyric acid (GHB). Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13404-13409.
2. Akhtar M.J., Ahamed M., Fareed M., Alrokayan S.A., Kumar S. Protective effect of sulphoraphane against oxidative stress mediated toxicity induced by CuO nanoparticles in mouse embryonic fibroblasts BALB 3T3. J.Toxicol. Sci. 2012, 37:139-148.
3. Andriamampandry C., Taleb O., Kemmel V., Humbert J.P., Aunis D., Maitre M. Cloning and functional characterization of a gamma-hydroxybutyrate receptor identified in the human brain. FASEB J. 2007, 21:885-895.
4. Andriamampandry C., Taleb O., Viry S., Muller C., Humbert J.P., Gobaille S., Aunis D., Maitre M. Cloning and characterization of a rat brain receptor that binds the endogenous neuromodulator gamma-hydroxybutyrate (GHB). FASEB J. 2003, 17:1691-1693.
5. Belyaev N.D., Nalivaeva N.N., Makova N.Z., Turner A.J. Neprilysin gene expression requires binding of the amyloid precursor protein intracellular domain to its promoter: implications for Alzheimer disease. EMBO Rep. 2009, 10:94-100.
6. Benosman S., Gross I., Clarke N., Jochemsen A.G., Okamoto K., Loeffler J.P., Gaiddon C. Multiple neurotoxic stresses converge on MDMX proteolysis to cause neuronal apoptosis. Cell Death Differ. 2007, 14:2047-2057.
7. Campbell I.T. Gammahydroxybutyrate. Anaesthesia 1983, 38:1105-1106.
8. Carter L.P., Griffiths R.R., Mintzer M.Z. Cognitive, psychomotor, and subjective effects of sodium oxybate and triazolam in healthy volunteers. Psychopharmacology 2009, 206:141-154.
9. Castelli M.P. Multi-faceted aspects of gamma-hydroxybutyric acid: a neurotransmitter, therapeutic agent and drug of abuse. Mini Rev. Med. Chem. 2008, 8:1188-1202.
10. Chishti M.A., Yang D.S., Janus C., Phinney A.L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P.E., Carlson G.A., George-Hyslop P.S., Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J.Biol. Chem. 2001, 276:21562-21570.
11. El-Amouri S.S., Zhu H., Yu J., Gage F.H., Verma I.M., Kindy M.S. Neprilysin protects neurons against Abeta peptide toxicity. Brain Res. 2007, 1152:191-200.
12. El-Amouri S.S., Zhu H., Yu J., Marr R., Verma I.M., Kindy M.S. Neprilysin: an enzyme candidate to slow the progression of Alzheimer's disease. Am. J. Pathol. 2008, 172:1342-1354.
13. Felmlee M.A., Roiko S.A., Morse B.L., Morris M.E. Concentration-effect relationships for the drug of abuse gamma-hydroxybutyric acid. J.Pharmacol. Exp. Ther. 2010, 333:764-771.
14. Gonthier B., Koncina E., Satkauskas S., Perraut M., Roussel G., Aunis D., Kapfhammer J.P., Bagnard D. APKC-dependent recruitment of MMP-2 controls semaphorin-3A growth-promoting effect in cortical dendrites. PLoS One 2009, 4:e5099.
15. Goodwin A.K., Froestl W., Weerts E.M. Involvement of gamma-hydroxybutyrate (GHB) and GABA-B receptors in the acute behavioral effects of GHB in baboons. Psychopharmacology 2005, 180:342-351.
16. Grimm A., Lim Y.A., Mensah-Nyagan A.G., Gotz J., Eckert A. Alzheimer's disease, oestrogen and mitochondria: an ambiguous relationship. Mol. Neurobiol. 2012, 46:151-160.
17. Hanson L.R., Fine J.M., Svitak A.L., Faltesek K.A. Intranasal administration of CNS therapeutics to awake mice. J.Vis. Exp. 2013, 74. http://dx.doi.org/10.3791/4440.
18. Hanson L.R., Hafez D., Svitak A.L., Burns R.B., Li X., Frey W.H., Marr R.A. Intranasal phosphoramidon increases beta-amyloid levels in wild-type and NEP/NEP2-deficient mice. J.Mol. Neurosci. 2011, 43:424-427.
19. Hauw J.J., Hausser-Hauw C., De Girolami U., Hasboun D., Seilhean D. Neuropathology of sleep disorders: a review. J.Neuropathol. Exp. Neurol. 2011, 70:243-252.
20. Houghton W.C., Scammell T.E., Thorpy M. Pharmacotherapy for cataplexy. Sleep Med. Rev. 2004, 8:355-366.
21. Iwata N., Takaki Y., Fukami S., Tsubuki S., Saido T.C. Region-specific reduction of Abeta-degrading endopeptidase, neprilysin, in mouse hippocampus upon aging. J.Neurosci. Res. 2002, 70:493-500.
22. Jiang Q., Lee C.Y., Mandrekar S., Wilkinson B., Cramer P., Zelcer N., Mann K., Lamb B., Willson T.M., Collins J.L., Richardson J.C., Smith J.D., Comery T.A., Riddell D., Holtzman D.M., Tontonoz P., Landreth G.E. ApoE promotes the proteolytic degradation of Abeta. Neuron 2008, 58:681-693.
23. Johnson-Wood K., Lee M., Motter R., Hu K., Gordon G., Barbour R., Khan K., Gordon M., Tan H., Games D., Lieberburg I., Schenk D., Seubert P., McConlogue L. Amyloid precursor protein processing and Abeta42 deposition in a transgenic mouse model of Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1550-1555.
24. Kawarabayashi T., Younkin L.H., Saido T.C., Shoji M., Ashe K.H., Younkin S.G. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J.Neurosci. 2001, 21:372-381.
25. Kemmel V., Klein C., Dembele D., Jost B., Taleb O., Aunis D., Mensah-Nyagan A.G., Maitre M. Asingle acute pharmacological dose of gamma-hydroxybutyrate (GHB) modifies multiple gene expression patterns in rat hippocampus and frontal cortex. Physiol. Genomics 2010, 41:146-160.
26. Kerridge C., Belyaev N.D., Nalivaeva N.N., Turner A.J. The Abeta-clearance protein transthyretin, like neprilysin, is epigenetically regulated by the amyloid precursor protein intracellular domain. J.Neurochem. 2014, 130:419-431.
27. Klein C., Kemmel V., Taleb O., Aunis D., Maitre M. Pharmacological doses of gamma-hydroxybutyrate (GHB) potentiate histone acetylation in the rat brain by histone deacetylase inhibition. Neuropharmacology 2009, 57:137-147.
28. Kothare S.V., Adams R., Valencia I., Faerber E.C., Grant M.L. Improved sleep and neurocognitive functions in a child with thalamic lesions on sodium oxybate. Neurology 2007, 68:1157-1158.
29. Leissring M.A., Farris W., Chang A.Y., Walsh D.M., Wu X., Sun X., Frosch M.P., Selkoe D.J. Enhanced proteolysis of beta-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron 2003, 40:1087-1093.
30. Li C., Hersh L.B. Neprilysin: assay methods, purification, and characterization. Methods Enzymol. 1995, 248:253-263.
31. Maitre M. The gamma-hydroxybutyrate signalling system in brain: organization and functional implications. Prog. Neurobiol. 1997, 51:337-361.
32. Mamelak M., Black J., Montplaisir J., Ristanovic R. Apilot study on the effects of sodium oxybate on sleep architecture and daytime alertness in narcolepsy. Sleep 2004, 27:1327-1334.
33. Maremmani I., Lamanna F., Tagliamonte A. Long-term therapy using GHB (sodium gamma hydroxybutyrate) for treatment-resistant chronic alcoholics. J.Psychoactive Drugs 2001, 33:135-142.
34. Marr R.A., Rockenstein E., Mukherjee A., Kindy M.S., Hersh L.B., Gage F.H., Verma I.M., Masliah E. Neprilysin gene transfer reduces human amyloid pathology in transgenic mice. J.Neurosci. 2003, 23:1992-1996.
35. Masliah E., Rockenstein E., Veinbergs I., Sagara Y., Mallory M., Hashimoto M., Mucke L. Beta-amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12245-12250.
36. Mawuenyega K.G., Sigurdson W., Ovod V., Munsell L., Kasten T., Morris J.C., Yarasheski K.E., Bateman R.J. Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 2010, 330:1774.
37. Mayer G. The use of sodium oxybate to treat narcolepsy. Expert Rev. Neurotherapeutics 2012, 12:519-529.
38. Miners J.S., Barua N., Kehoe P.G., Gill S., Love S. Abeta-degrading enzymes: potential for treatment of Alzheimer disease. J.Neuropathol. Exp. Neurol. 2011, 70:944-959.
39. Miners J.S., Van Helmond Z., Chalmers K., Wilcock G., Love S., Kehoe P.G. Decreased expression and activity of neprilysin in Alzheimer disease are associated with cerebral amyloid angiopathy. J.Neuropathol. Exp. Neurol. 2006, 65:1012-1021.
40. Miners S., Ashby E., Baig S., Harrison R., Tayler H., Speedy E., Prince J.A., Love S., Kehoe P.G. Angiotensin-converting enzyme levels and activity in Alzheimer's disease: differences in brain and CSF ACE and association with ACE1 genotypes. Am. J. Transl. Res. 2009, 1:163-177.
41. Mozes E., Hunya A., Posa A., Penke B., Datki Z. Anovel method for the rapid determination of beta-amyloid toxicity on acute hippocampal slices using MTT and LDH assays. Brain Res. Bull. 2012, 87:521-525.
42. Nalivaeva N.N., Beckett C., Belyaev N.D., Turner A.J. Are amyloid-degrading enzymes viable therapeutic targets in Alzheimer's disease?. J.Neurochem. 2012, 120(Suppl 1):167-185.
43. Nalivaeva N.N., Belyaev N.D., Lewis D.I., Pickles A.R., Makova N.Z., Bagrova D.I., Dubrovskaya N.M., Plesneva S.A., Zhuravin I.A., Turner A.J. Effect of sodium valproate administration on brain neprilysin expression and memory in rats. J.Mol. Neurosci. 2012, 46:569-577.
44. Nalivaeva N.N., Belyaev N.D., Turner A.J. Sodium valproate: an old drug with new roles. Trends Pharmacol. Sci. 2009, 30:509-514.
45. Nalivaeva N.N., Belyaev N.D., Zhuravin I.A., Turner A.J. The Alzheimer's amyloid-degrading peptidase, neprilysin: can we control it?. Int. J. Alzheimer's Dis. 2012, 2012:383796.
46. Nava F., Premi S., Manzato E., Campagnola W., Lucchini A., Gessa G.L. Gamma-hydroxybutyrate reduces both withdrawal syndrome and hypercortisolism in severe abstinent alcoholics: an open study vs. diazepam. Am. J. Drug Alcohol Abuse 2007, 33:379-392.
47. Ognibene E., Middei S., Daniele S., Adriani W., Ghirardi O., Caprioli A., Laviola G. Aspects of spatial memory and behavioral disinhibition in Tg2576 transgenic mice as a model of Alzheimer's disease. Behav. Brain Res. 2005, 156:225-232.
48. Pacheco-Quinto J., Eckman E.A. Endothelin-converting enzymes degrade intracellular beta-amyloid produced within the endosomal/lysosomal pathway and autophagosomes. J.Biol. Chem. 2013, 288:5606-5615.
49. Perez A., Morelli L., Cresto J.C., Castano E.M. Degradation of soluble amyloid beta-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brains. Neurochem. Res. 2000, 25:247-255.
50. Poirier R., Wolfer D.P., Welzl H., Tracy J., Galsworthy M.J., Nitsch R.M., Mohajeri M.H. Neuronal neprilysin overexpression is associated with attenuation of Abeta-related spatial memory deficit. Neurobiol. Dis. 2006, 24:475-483.
51. Saito T., Iwata N., Tsubuki S., Takaki Y., Takano J., Huang S.M., Suemoto T., Higuchi M., Saido T.C. Somatostatin regulates brain amyloid beta peptide Abeta42 through modulation of proteolytic degradation. Nat. Med. 2005, 11:434-439.
52. Scharf M.B., Brown D., Woods M., Brown L., Hirschowitz J. The effects and effectiveness of gamma-hydroxybutyrate in patients with narcolepsy. J.Clin. Psychiatry 1985, 46:222-225.
53. Scharf M.B., Fletcher K.A. GHB-new hope for narcoleptics?. Biol. Psychiatry 1989, 26:329-330.
54. Scrima L., Hartman P.G., Johnson F.H., Thomas E.E., Hiller F.C. The effects of gamma-hydroxybutyrate on the sleep of narcolepsy patients: a double-blind study. Sleep 1990, 13:479-490.
55. Shirotani K., Tsubuki S., Iwata N., Takaki Y., Harigaya W., Maruyama K., Kiryu-Seo S., Kiyama H., Iwata H., Tomita T., Iwatsubo T., Saido T.C. Neprilysin degrades both amyloid beta peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J.Biol. Chem. 2001, 276:21895-21901.
56. Sircar R., Basak A., Sircar D., Wu L.C. Effects of gamma-hydroxybutyric acid on spatial learning and memory in adolescent and adult female rats. Pharmacol. Biochem. Behav. 2010, 96:187-193.
57. Suzuki T., Nagano Y., Kouketsu A., Matsuura A., Maruyama S., Kurotaki M., Nakagawa H., Miyata N. Novel inhibitors of human histone deacetylases: design, synthesis, enzyme inhibition, and cancer cell growth inhibition of SAHA-based non-hydroxamates. J.Med. Chem. 2005, 48:1019-1032.
58. Tampellini D., Capetillo-Zarate E., Dumont M., Huang Z., Yu F., Lin M.T., Gouras G.K. Effects of synaptic modulation on beta-amyloid, synaptophysin, and memory performance in Alzheimer's disease transgenic mice. J.Neurosci. 2010, 30:14299-14304.
59. Turner A.J., Nalivaeva N.N. New insights into the roles of metalloproteinases in neurodegeneration and neuroprotection. Int. Rev. Neurobiol. 2007, 82:113-135.
60. van Nieuwenhuijzen P.S., McGregor I.S., Hunt G.E. The distribution of gamma-hydroxybutyrate-induced Fos expression in rat brain: comparison with baclofen. Neuroscience 2009, 158:441-455.
61. Wang R., Wang S., Malter J.S., Wang D.S. Effects of HNE-modification induced by Abeta on neprilysin expression and activity in SH-SY5Y cells. J.Neurochem. 2009, 108:1072-1082.
62. Wang Z., Yang D., Zhang X., Li T., Li J., Tang Y., Le W. Hypoxia-induced down-regulation of neprilysin by histone modification in mouse primary cortical and hippocampal neurons. PLoS One 2011, 6:e19229.
63. Wang Z., Zhang X.J., Li T., Li J., Tang Y., Le W. Valproic acid reduces neuritic plaque formation and improves learning deficits in APP(Swe)/PS1(A246E) transgenic mice via preventing the prenatal hypoxia-induced down-regulation of neprilysin. CNS Neurosci. Ther. 2014, 20:209-217.
64. Wendt G., Kemmel V., Patte-Mensah C., Uring-Lambert B., Eckert A., Schmitt M.J., Mensah-Nyagan A.G. Gamma-hydroxybutyrate, acting through an anti-apoptotic mechanism, protects native and amyloid-precursor-protein-transfected neuroblastoma cells against oxidative stress-induced death. Neuroscience 2014, 263:203-215.
65. Williams S.R., Turner J.P., Crunelli V. Gamma-hydroxybutyrate promotes oscillatory activity of rat and cat thalamocortical neurons by a tonic GABAB, receptor-mediated hyperpolarization. Neuroscience 1995, 66:133-141.
66. Yassine N., Lazaris A., Dorner-Ciossek C., Despres O., Meyer L., Maitre M., Mensah-Nyagan A.G., Cassel J.C., Mathis C. Detecting spatial memory deficits beyond blindness in tg2576 Alzheimer mice. Neurobiol. Aging 2013, 34:716-730.