In vivo 1H MRS study in microlitre voxels in the hippocampus of a mouse model of Down syndrome at 11.7 T

NMR in Biomedicine

Volumn 27, Issue 10, 2014, Pages 1143-1150

  Santin, Mathieu D ^a,b   Valabrègue, Romain ^a,b   Rivals, Isabelle ^c   Pénager, Romain ^a   Paquin, Raphaël ^a,b   Dauphinot, Luce ^a   Albac, Christelle ^a   Delatour, Benoit ^a   Potier, Marie Claude ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c PSL RESEARCH UNIVERSITY   (France)

Author keywords

Down syndrome; Hippocampus; Inhibition; Metabolite; MRS

Indexed keywords

AMINO ACIDS; BIOMOLECULES; ENZYME INHIBITION; MAMMALS;

DOWN SYNDROME; GAMMA-AMINOBUTYRIC ACIDS; HIGHLY-CORRELATED; HIPPOCAMPUS; LINEAR COMBINATION MODEL; METABOLITE CONCENTRATIONS; PHARMACOLOGICAL TREATMENT; WHETHER DIFFERENCES;

METABOLITES;

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; INOSITOL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN SYNDROME; EXCITATION AND STIMULATION; HIPPOCAMPUS; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; METABOLITE; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROMETER; PRINCIPAL COMPONENT ANALYSIS; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; ANIMAL; BRAIN CHEMISTRY; C57BL MOUSE; DISEASE MODEL; FEMALE; HEMISPHERIC DOMINANCE; METABOLISM; MOUSE MUTANT; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE; PATHOLOGY; PROCEDURES;

ANIMALS; BRAIN CHEMISTRY; DISEASE MODELS, ANIMAL; DOMINANCE, CEREBRAL; DOWN SYNDROME; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTON MAGNETIC RESONANCE SPECTROSCOPY;

EID: 84908071660     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3155     Document Type: Article

References (47)

1. Bittles AH, Bower C, Hussain R, Glasson EJ. The four ages of Down syndrome. Eur. J. Public Health 2007; 17: 221-225.
2. Sherman SL, Allen EG, Bean LH. Freeman SB Epidemiology of Down syndrome. Ment. Retard. Dev. Disabil. Res. Rev. 2007; 13: 221-227.
3. Lejeune J, Turpin R, Gautier M. Mongolism; a chromosomal disease (trisomy). Bull. Acad. Natl. Med. 1959; 143: 256-265.
4. Lott IT, Dierssen M. Cognitive deficits and associated neurological complications in individuals with Down's syndrome. Lancet Neurol. 2010; 9: 623-633.
5. Braudeau J, Delatour B, Duchon A, Pereira PL, Dauphinot L, de Chaumont F, Olivo-Marin JC, Dodd RH, Herault Y, Potier MC. Specific targeting of the GABA-A receptor alpha5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice. J. Psychopharmacol. 2011; 25: 1030-1042.
6. Contestabile A, Greco B, Ghezzi D, Tucci V, Benfenati F, Gasparini L. Lithium rescues synaptic plasticity and memory in Down syndrome mice. J. Clin. Invest. 2012; 123: 348-361.
7. Costa AC, Scott-McKean JJ, Stasko MR. Acute injections of the NMDA receptor antagonist memantine rescue performance deficits of the Ts65Dn mouse model of Down syndrome on a fear conditioning test. Neuropsychopharmacology 2008; 33: 1624-1632.
8. De la Torre R, De Sola S, Pons M, Duchon A, de Lagran MM, Farre M, Fito M, Benejam B, Langohr K, Rodriguez J, Pujadas M, Bizot JC, Cuenca A, Janel N, Catuara S, Covas MI, Blehaut H, Herault Y, Delabar JM, Dierssen M. Epigallocatechin-3-gallate, a DYRK1A inhibitor, rescues cognitive deficits in Down syndrome mouse models and in humans. Mol. Nutr. Food Res. 2013; 58: 278-288.
9. Fernandez F, Morishita W, Zuniga E, Nguyen J, Blank M, Malenka RC. Garner CC Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat. Neurosci. 2007; 10: 411-413.
10. Kleschevnikov AM, Belichenko PV, Gall J, George L, Nosheny R, Maloney MT, Salehi A, Mobley WC. Increased efficiency of the GABAA and GABAB receptor-mediated neurotransmission in the Ts65Dn mouse model of Down syndrome. Neurobiol. Dis. 2012; 45: 683-691.
11. Martinez-Cue C, Delatour B, Potier MC. Treating enhanced GABAergic inhibition in Down syndrome: use of GABA alpha5-selective inverse agonists. Neurosci. Biobehav. Rev. 2014; S0149-7634.
12. Martinez-Cue C, Martinez P, Rueda N, Vidal R, Garcia S, Vidal V, Corrales A, Montero JA, Pazos A, Florez J, Gasser R, Thomas AW, Honer M, Knoflach F, Trejo JL, Wettstein JG, Hernandez MC. Reducing GABAA alpha5 receptor-mediated inhibition rescues functional and neuromorphological deficits in a mouse model of Down syndrome. J. Neurosci. 2013; 33: 3953-3966.
13. Potier MC, Braudeau J, Dauphinot L, Delatour B. Reducing GABAergic inhibition restores cognitive functions in a mouse model of Down syndrome. CNS Neurol. Disorders Drug Targets 2013; 13: 8-15.
14. Salehi A, Faizi M, Colas D, Valletta J, Laguna J, Takimoto-Kimura R, Kleschevnikov A, Wagner SL, Aisen P, Shamloo M, Mobley WC. Restoration of norepinephrine-modulated contextual memory in a mouse model of Down syndrome. Sci. Transl. Med. 2009; 1: 7-17.
15. Stagni F, Magistretti J, Guidi S, Ciani E, Mangano C, Calza L, Bartesaghi R. Pharmacotherapy with fluoxetine restores functional connectivity from the dentate gyrus to field CA3 in the Ts65Dn mouse model of down syndrome. PLoS One 2013; 8: e61689.
16. Sturgeon X, Gardiner KJ. Transcript catalogs of human chromosome 21 and orthologous chimpanzee and mouse regions. Mamm. Genome 2011; 22: 261-271.
17. Reeves RH, Irving NG, Moran TH, Wohn A, Kitt C, Sisodia SS, Schmidt C, Bronson RT, DavissonMT. Amousemodel for Down syndrome exhibits learning and behaviour deficits. Nat. Genet. 1995; 11: 177-184.
18. Rueda N, Florez J, Martinez-Cue C. Mouse models of Down syndrome as a tool to unravel the causes of mental disabilities. Neural Plast. 2012; 2012: 584071.
19. Escorihuela RM, Fernandez-Teruel A, Vallina IF, Baamonde C, Lumbreras MA, Dierssen M, Tobena A, Florez J. A behavioral assessment of Ts65Dn mice: a putative Down syndrome model. Neurosci. Lett. 1995; 199: 143-146.
20. Holtzman DM, Santucci D, Kilbridge J, Chua-Couzens J, Fontana DJ, Daniels SE, Johnson RM, Chen K, Sun Y, Carlson E, Alleva E, Epstein CJ, Mobley WC. Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 13 333-13 338.
21. Braudeau J, Dauphinot L, Duchon A, Loistron A, Dodd RH, Herault Y, Delatour B, Potier MC. Chronic treatment with a promnesiant GABA-A alpha5-selective inverse agonist increases immediate early genes expression during memory processing in mice and rectifies their expression levels in a Down syndrome mouse model. Adv. Pharmacol. Sci. 2011; 2011: 153218.
22. Huang W, Galdzicki Z, van Gelderen P, Balbo A, Chikhale EG, Schapiro MB, Rapoport SI. Brain myo-inositol level is elevated in Ts65Dn mouse and reduced after lithium treatment. Neuro. Rep. 2000; 11: 445-448.
23. Duchon A, Raveau M, Chevalier C, Nalesso V, Sharp AJ, Herault Y. Identification of the translocation breakpoints in the Ts65Dn and Ts1Cje mouse lines: relevance for modeling Down syndrome. Mamm. Genome 2011; 22: 674-684.
24. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993; 29: 804-811.
25. Garwood M, DelaBarre L. The return of the frequency sweep: designing adiabatic pulses for contemporary NMR. J. Magn. Reson. 2001; 153; 155-177.
26. 1H NMR spectroscopy of rat brain at 1ms echo time. Magn. Reson. Med. 1999; 41: 649-656.
27. Henry PG, Marjanska M, Walls JD, Valette J, Gruetter R, Ugurbil K. Proton-observed carbon-edited NMR spectroscopy in strongly coupled second-order spin systems. Magn. Reson. Med. 2006; 55: 250-257.
28. Govindaraju V, Young K, Maudsley AA. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 2000; 13: 129-153.
29. Kaiser LG, Marjanska M, Matson GB, Iltis I, Bush SD, Soher BJ, Mueller S, Young K. (1)HMRS detection of glycine residue of reduced glutathione in vivo. J. Magn. Reson. 2010; 202: 259-266.
30. Whittle N, Sartori SB, Dierssen M, Lubec G. Singewald N. Fetal Downsyndrome brains exhibit aberrant levels of neurotransmitters critical for normalbrain development. Pediatrics 2007; 120: e1465-e1471.
31. Seidl R, Cairns N, Singewald N, Kaehler ST, Lubec G. Differences between GABA levels in Alzheimer's disease and Down syndrome with Alzheimer-like neuropathology. Naunyn Schmiedebergs Arch. Pharmacol. 2001; 363: 139-145.
32. Reynolds GP, Warner CE. Amino acid neurotransmitter deficits in adult Down's syndrome brain tissue. Neurosci. Lett. 1988; 94: 224-227.
33. 1H MRS) in children with Down syndrome. Pharmacol. Rep. 2010; 62: 1070-1077.
34. Smigielska-Kuzia J, Sobaniec W. Brain metabolic profile obtained by proton magnetic resonance spectroscopy HMRS in children with Down syndrome. Adv. Med. Sci. 2007; (52 Suppl.)1: 183-187.
35. 1H MRS at 14.1 T. NMR Biomed. 2010; 23: 578-583.
36. 1H NMR spectroscopy of the mouse brain at 9.4 T. Magn. Reson. Med. 2004; 52: 478-484.
37. Lamar M, Foy CM, Beacher F, Daly E, Poppe M, Archer N, Prasher V, Murphy KC, Morris RG, Simmons A, Lovestone S, Murphy DG. Down syndrome with and without dementia: an in vivo proton magnetic resonance spectroscopy study with implications for Alzheimer's disease. Neuroimage 2011; 57: 63-68.
38. Shonk T, Ross BD. Role of increased cerebral myo-inositol in the dementia of Down syndrome. Magn. Reson. Med. 1995; 33: 858-861.
39. 1H MRS study. Am. J. Psychiatry 1999; 156: 1879-1886.
40. Shetty HU, Schapiro MB, Holloway HW, Rapoport SI. Polyol profiles in Down syndrome. myo-inositol, specifically, is elevated in the cerebrospinal fluid. J. Clin. Invest. 1995; 95: 542-546.
41. Murphy EJ, Schapiro MB, Rapoport SI, Shetty HU. Phospholipid composition and levels are altered in Down syndrome brain. Brain Res. 2000; 867: 9-18.
42. Voronov SV, Frere SG, Giovedi S, Pollina EA, Borel C, Zhang H, Schmidt C, Akeson EC, Wenk MR, Cimasoni L, Arancio O, Davisson MT, Antonarakis SE, Gardiner K, De Camilli P, Di Paolo G. Synaptojanin 1-linked phosphoinositide dyshomeostasis and cognitive deficits in mouse models of Down's syndrome. Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 9415-9420.
43. Beacher F, Simmons A, Daly E, Prasher V, Adams C, Margallo-Lana ML, Morris R, Lovestone S, Murphy K, Murphy DG. Hippocampal myo-inositol and cognitive ability in adults with Down syndrome: an in vivo proton magnetic resonance spectroscopy study. Arch. Gen. Psychiatry 2005; 62: 1360-1365.
44. Peirce JL, Chesler EJ, Williams RW, Lu L. Genetic architecture of the mouse hippocampus: identification of gene loci with selective regional effects. Genes Brain Behav. 2003; 2: 238-252.
45. Suzuki M, Hagino H, Nohara S, Zhou SY, Kawasaki Y, Takahashi T, Matsui M, Seto H, Ono T, Kurachi M. Male-specific volume expansion of the human hippocampus during adolescence. Cereb. Cortex 2005; 15: 187-193.
46. Hibaoui Y, Grad I, Letourneau A, Sailani MR, Dahoun S, Santoni FA, Gimelli S, Guipponi M, Pelte MF, Bena F, Antonarakis SE, Feki A. Modelling and rescuing neurodevelopmental defect of Down syndrome using induced pluripotent stem cells from monozygotic twins discordant for trisomy 21. EMBO Mol. Med. 2014; 6: 259-277.
47. Gaetz W, Bloy L, Wang DJ, Port RG, Blaskey L, Levy SE, Roberts TP. GABA estimation in the brains of children on the autism spectrum: measurement precision and regional cortical variation. Neuroimage 2014; 86: 1-9.