Proton and phosphorus magnetic resonance spectroscopy of a mouse model of Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 31, Issue SUPPL. 3, 2012, Pages

  Mlynárik, Vladimír ^a   Cacquevel, Matthias ^a   Sun Reimer, Lili ^a   Janssens, Sharon ^a   Cudalbu, Cristina ^a   Lei, Hongxia ^a   Schneider, Bernard L ^a   Aebischer, Patrick ^a   Gruetter, Rolf ^a  

^a EPFL   (Switzerland)

Author keywords

5xFAD; Alzheimer's disease; in vivo NMR spectroscopy; metabolic profile; transgenic mice

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE TRIPHOSPHATE; ALANINE; ASCORBIC ACID; ASPARTIC ACID; CHOLINE; CREATINE; CREATINE KINASE; GLUCOSE; GLUTAMIC ACID; GLUTATHIONE; LACTIC ACID; N ACETYLASPARTIC ACID; PHOSPHOETHANOLAMINE; TAURINE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; GENE MUTATION; IN VIVO STUDY; MAGNETIC FIELD; MOUSE; NEUROCHEMISTRY; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; TRANSGENIC MOUSE;

EID: 84866865925     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-112072     Document Type: Article

References (68)

1. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L, et al. (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706.
2. Rogaev EI, Sherrington R, Rogaeva EA, Levesque G, Ikeda M, Liang Y, Chi H, Lin C, Holman K, Tsuda T, et al. (1995) Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376, 775-778.
3. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, Chi H, Lin C, Li G, Holman K, Tsuda T, Mar L, Foncin JF, Bruni AC, Montesi MP, Sorbi S, Rainero I, Pinessi L, Nee L, Chumakov I, Pollen D, Brookes A, Sanseau P, Polinsky RJ,WascoW, Da Silva HA, Haines JL, Perkicak- Vance MA, Tanzi RE, Roses AD, Fraser PE, Rommens JM, St George-HyslopPH(1995) Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375, 754-760.
4. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, Hillebrand M, Joosse M, Kwon JM, Nowotny P, Che LK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JB, Schofield PR, Andreadis A, Snowden J, Craufurd D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P (1998) Association of missense and 5-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705.
5. Hall AM, Roberson ED (2011) Mouse models of Alzheimer's disease Brain Res Bull, doi:10.1016/j.brainresbull.2011. 1011.1017
6. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: Intracellular A- and synaptic dysfunction. Neuron 39, 409-421.
7. Grueninger F, Bohrmann B, Czech C, Ballard TM, Frey JR, Weidensteiner C, von Kienlin M, Ozmen L (2010) Phosphorylation of Tau at S422 is enhanced by A- in TauPS2APP triple transgenic mice. Neurobiol Dis 37, 294-306.
8. Eriksen JL, Janus CG (2007) Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav Genet 37, 79-100.
9. Morrissette DA, Parachikova A, Green KN, LaFerla FM (2009) Relevance of transgenic mouse models to human Alzheimer disease. J Biol Chem 284, 6033-6037.
10. Mandal PK (2007) Magnetic resonance spectroscopy (MRS) and its application in Alzheimer's disease. Concepts Magn Reson A 30A, 40-64.
11. Mandal PK, Akolkar H (2011) A new experimental approach and signal processing scheme for the detection and quantitation of 31P brain neurochemicals from in vivo MRS studies using dual tuned (1H/31P) head coil. Biochem Biophys Res Commun 412, 302-306.
12. Yesavage JA, O'Hara R, Kraemer H, Noda A, Taylor JL, Ferris S, Gely-Nargeot MC, Rosen A, Friedman L, Sheikh J, Derouesne C (2002) Modeling the prevalence and incidence of Alzheimer's disease and mild cognitive impairment. J Psychiatr Res 36, 281-286.
13. Doraiswamy PM, Charles HC, Krishnan KR (1998) Prediction of cognitive decline in early Alzheimer's disease. Lancet 352, 1678.
14. Jessen F, Gur O, Block W, Ende G, Frolich L, Hammen T, Wiltfang J, Kucinski T, Jahn H, Heun R, MaierW, Kolsch H, Kornhuber J, Traber F (2009) A multicenter 1H-MRS study of the medial temporal lobe in AD and MCI. Neurology 72, 1735-1740.
15. Miller BL, Moats RA, Shonk T, Ernst T,Woolley S, Ross BD (1993) Alzheimer disease: Depiction of increased cerebral myo-inositol with proton MR spectroscopy. Radiology 187, 433-437.
16. Moats RA, Ernst T, Shonk TK, Ross BD (1994) Abnormal cerebral metabolite concentrations in patients with probable Alzheimer disease. Magn Reson Med 32, 110-115.
17. Schuff N, Amend DL, Meyerhoff DJ, Tanabe JL, Norman D, Fein G, Weiner MW (1998) Alzheimer disease: Quantitative H-1 MR spectroscopic imaging of frontoparietal brain. Radiology 207, 91-102.
18. Klunk WE, Panchalingam K, Moossy J, McClure RJ, Pettegrew JW (1992) N-acetyl-L-aspartate and other amino acid metabolites in Alzheimer's disease brain: A preliminary proton nuclear magnetic resonance study. Neurology 42, 1578-1585.
19. Schuff N, Amend D, Ezekiel F, Steinman SK, Tanabe J, Norman D, JagustW, Kramer JH, Mastrianni JA, Fein G,Weiner MW (1997) Changes of hippocampal N-acetyl aspartate and volume in Alzheimer's disease. A proton MR spectroscopic imaging and MRI study. Neurology 49, 1513-1521.
20. Huang W, Alexander GE, Chang L, Shetty HU, Krasuski JS, Rapoport SI, Schapiro MB (2001) Brain metabolite concentration and dementia severity in Alzheimer's disease: A 1H MRS study. Neurology 57, 626-632.
21. Kantarci K, Petersen RC, Boeve BF, Knopman DS, Tang-Wai DF, O'Brien PC, Weigand SD, Edland SD, Smith GE, Ivnik RJ, Ferman TJ, Tangalos EG, Jack CR Jr (2004) 1HMR spectroscopy in common dementias. Neurology 63, 1393-1398.
22. Pfefferbaum A, Adalsteinsson E, Spielman D, Sullivan EV, Lim KO (1999) In vivo spectroscopic quantification of the N-acetyl moiety, creatine, and choline from large volumes of brain gray and white matter: Effects of normal aging. Magn Reson Med 41, 276-284.
23. Chantal S, Labelle M, Bouchard RW, Braun CM, Boulanger Y (2002) Correlation of regional proton magnetic resonance spectroscopic metabolic changes with cognitive deficits in mild Alzheimer disease. Arch Neurol 59, 955-962.
24. Watanabe T, Shiino A, Akiguchi I (2010) Absolute quantification in proton magnetic resonance spectroscopy is useful to differentiate amnesic mild cognitive impairment from Alzheimer's disease and healthy aging. Dement Geriatr Cogn Disord 30, 71-77.
25. Ackl N, Ising M, SchreiberYA, Atiya M, Sonntag A, Auer DP (2005) Hippocampal metabolic abnormalities in mild cognitive impairment and Alzheimer's disease. Neurosci Lett 384, 23-28.
26. Wang ZQ, Zhao C, Yu L, Zhou WD, Li KC (2009) Regional metabolic changes in the hippocampus and posterior cingulate area detected with 3-Tesla magnetic resonance spectroscopy in patients with mild cognitive impairment and Alzheimer disease. Acta Radiol 50, 312-319.
27. Rupsingh R, Borrie M, Smith M, Wells JL, Bartha R (2011) Reduced hippocampal glutamate in Alzheimer disease. Neurobiol Aging 32, 802-810.
28. Adalsteinsson E, Sullivan EV, Kleinhans N, Spielman DM, Pfefferbaum A (2000) Longitudinal decline of the neuronal marker N-acetyl aspartate in Alzheimer's disease. Lancet 355, 1696-1697.
29. Ernst T, Chang L, Melchor R, Mehringer CM (1997) Frontotemporal dementia and early Alzheimer disease: Differentiation with frontal lobe H-1 MR spectroscopy. Radiology 203, 829-836.
30. Antuono PG, Jones JL,Wang Y, Li SJ (2001) Decreased glutamate + glutamine in Alzheimer's disease detected in vivo with 1H-MRS at 0.5 T. Neurology 56, 737-742.
31. Kara F, Braakman N, van Buchem MA, de Groot HJM, Alia A (2011) Prospects of magnetic resonance spectroscopy in mouse models of Alzheimer's disease. Curr Med Imaging Rev 7, 80-87.
32. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, A- elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
33. Dedeoglu A, Choi JK, Cormier K, Kowall NW, Jenkins BG (2004) Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that express mutant human APP shows altered neurochemical profile. Brain Res 1012, 60-65.
34. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C,Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4, 97-100.
35. Oberg J, Spenger C, Wang FH, Andersson A, Westman E, Skoglund P, Sunnemark D, Norinder U, Klason T, Wahlund LO, LindbergM(2008) Age related changes in brain metabolites observed by 1HMRS in APP/PS1 mice. Neurobiol Aging 29, 1423-1433.
36. Marjanska M, Curran GL, Wengenack TM, Henry PG, Bliss RL, Poduslo JF, Jack CR Jr, Ugurbil K, Garwood M (2005) Monitoring disease progression in transgenic mouse models of Alzheimer's disease with proton magnetic resonance spectroscopy. Proc Natl Acad Sci U S A 102, 11906-11910.
37. Jack CR Jr, Marjanska M,Wengenack TM, ReyesDA, Curran GL, Lin J, Preboske GM, Poduslo JF, Garwood M (2007) Magnetic resonance imaging of Alzheimer's pathology in the brains of living transgenic mice: A new tool in Alzheimer's disease research. Neuroscientist 13, 38-48.
38. Choi JK, Jenkins BG, Carreras I, Kaymakcalan S, Cormier K, KowallNW, DedeogluA(2010) Anti-inflammatory treatment in AD mice protects against neuronal pathology. Exp Neurol 223, 377-384.
39. McGowan E, Sanders S, Iwatsubo T, Takeuchi A, Saido T, Zehr C, Yu X, Uljon S, Wang R, Mann D, Dickson D, Duff K (1999) Amyloid phenotype characterization of transgenic mice overexpressing both mutant amyloid precursor protein and mutant presenilin 1 transgenes. Neurobiol Dis 6, 231-244.
40. Chen SQ,Wang PJ, Ten GJ, ZhanW, Li MH, Zang FC (2009) Role of myo-inositol by magnetic resonance spectroscopy in early diagnosis of Alzheimer's disease in APP/PS1 transgenic mice. Dement Geriatr Cogn Disord 28, 558-566.
41. Jankowsky JL, Slunt HH, Ratovitski T, JenkinsNA, Copeland NG, Borchelt DR (2001) Co-expression of multiple transgenes in mouse CNS: A comparison of strategies. Biomol Eng 17, 157-165.
42. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue-amyloid peptide in vivo: Evidence for augmentation of a 42-specific- secretase. Hum Mol Genet 13, 159-170.
43. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, FroschMP(2006) Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24, 516-524.
44. Burgess BL, McIsaac SA, Naus KE, Chan JY, Tansley GH, Yang J, Miao F, Ross CJ, van Eck M, Hayden MR, van Nostrand W, St George-Hyslop P, Westaway D, Wellington CL (2006) Elevated plasma triglyceride levels precede amyloid deposition in Alzheimer's disease mouse models with abundant A- in plasma. Neurobiol Dis 24, 114-127.
45. Richards JG, Higgins GA, Ouagazzal AM, Ozmen L, Kew JN, Bohrmann B, Malherbe P, Brockhaus M, Loetscher H, Czech C, Huber G, Bluethmann H, Jacobsen H, Kemp JA (2003) PS2APP transgenic mice, coexpressing hPS2mut and hAPPswe, show age-related cognitive deficits associated with discrete brain amyloid deposition and inflammation. J Neurosci 23, 8989-9003.
46. von Kienlin M, Kunnecke B, Metzger F, Steiner G, Richards JG, Ozmen L, Jacobsen H, Loetscher H (2005) Altered metabolic profile in the frontal cortex of PS2APP transgenic mice, monitored throughout their life span. Neurobiol Dis 18, 32-39.
47. Kim J, Lee S-P, Michaelis ML, Choi I-Y (2009) Detecting progression of Alzheimer's disease pathology in the triple transgenic mouse brain using 1H MRS. In: Proc ISMRM 17th Scientific Meeting&Exhibition. International Society for Magnetic Resonance in Medicine, Honolulu, USA, p. 3302.
48. Choi JK, Dedeoglu A, JenkinsBG(2007) Application ofMRS to mouse models of neurodegenerative illness. NMR Biomed 20, 216-237.
49. Santacruz K, Lewis J, Spires T, Paulson J,Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, Forster C, YueM, Orne J, Janus C, Mariash A, Kuskowski M, Hyman B, Hutton M, Ashe KH (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476-481.
50. KimJ, Choi I-Y, DuffK, Lee P (2011) Neurochemical changes in olfactory system and hippocampus regions of Tau transgenic mice using 1H MRS. In: Proc ISMRM 19th Scientific Meeting & Exhibition. International Society for Magnetic Resonance in Medicine, Montreal, p. 2251.
51. Yang D, Xie Z, Stephenson D, Morton D, Hicks CD, Brown TM, Sriram R, O'Neill S, Raunig D, Bocan T (2011)Volumetric MRI and MRS provide sensitive measures of Alzheimer's disease neuropathology in inducible Tau transgenic mice (rTg4510). Neuroimage 54, 2652-2658.
52. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: Potential factors in amyloid plaque formation. J Neurosci 26, 10129- 10140.
53. Gruetter R, Tkáč I (2000) Field mapping without reference scan using asymmetric echo-planar techniques. Magn Reson Med 43, 319-323.
54. Mlynárik V, Gambarota G, Frenkel H, Gruetter R (2006) Localized short-echo-time proton MR spectroscopy with full signal-intensity acquisition. Magn Reson Med 56, 965-970.
55. Tkáč I, Starčuk Z, Choi IY, GruetterR(1999) In vivo 1HNMR spectroscopy of rat brain at 1ms echo time. Magn Reson Med 41, 649-656.
56. Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo protonNMRspectra. Magn Reson Med 30, 672-679.
57. Mlynárik V, Cudalbu C, Xin L, Gruetter R (2008) 1H NMR spectroscopy of rat brain in vivo at 14.1Tesla: Improvements in quantification of the neurochemical profile. J Magn Reson 194, 163-168.
58. Ordidge RJ, Connelly A, Lohman JAB (1986) Image-selected in vivo spectroscopy (ISIS) - a new technique for spatially selective NMR-spectroscopy. J Magn Reson 66, 283-294.
59. Luo Y, de Graaf RA, DelaBarre L, Tannus A, Garwood M (2001) BISTRO: An outer-volume suppression method that tolerates RF field inhomogeneity. Magn Reson Med 45, 1095- 1102.
60. Vanhamme L, van den Boogaart A, Van Huffel S (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129, 35-43.
61. Petroff OAC, Prichard JW, Behar KL, Alger JR, Denhollander JA, Shulman RG (1985) Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35, 781-788.
62. Jawhar S, Trawicka A, Jenneckens C, Bayer TA, Wirths O (2010) Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal A- aggregation in the 5xFAD mouse model of Alzheimer's disease. Neurobiol Aging 33, 196.e29-196.e40.
63. Shonk T, Ross BD (1995) Role of increased cerebral myoinositol in the dementia of Down syndrome. Magn Reson Med 33, 858-861.
64. Schmitt K, Grimm A, Kazmierczak A, Strosznajder JB, Gotz J, Eckert A (2011) Insights into mitochondrial dysfunction: Aging, amyloid-and tau - a deleterious trio Antioxid Redox Signal, doi:10.1089/ars.2011.4400
65. Mlynárik V, Kašparová S, Liptaj T, Dobrota D, Horecký J, Belan V (1998) Creatine kinase reaction rates in rat brain during chronic ischemia.Magn Reson Mater Phys 7, 162-165.
66. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG (2001) Age-dependent changes in brain, CSF, and plasma amyloid- protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21, 372-381.
67. Sasaki A, Shoji M, Harigaya Y, Kawarabayashi T, Ikeda M, Naito M, Matsubara E, Abe K, Nakazato Y (2002) Amyloid cored plaques in Tg2576 transgenic mice are characterized by giant plaques, slightly activated microglia, and the lack of paired helical filament-typed, dystrophic neurites. Virchows Arch 441, 358-367.
68. Gordon MN, Holcomb LA, Jantzen PT, DiCarlo G, Wilcock D, Boyett KW, Connor K, Melachrino J, O'Callaghan JP, Morgan D (2002) Time course of the development of Alzheimer-like pathology in the doubly transgenic PS1+APP mouse. Exp Neurol 173, 183-195.