Treatment effects in a transgenic mouse model of alzheimer's disease: A magnetic resonance spectroscopy study after passive immunization

Neuroscience

Volumn 259, Issue , 2014, Pages 94-100

  Marjanska M ^a   Weigand, S D ^b   Preboske, G ^c   Wengenack, T M ^d   Chamberlain, R ^a   Curran, G L ^d   Poduslo, J F ^d   Garwood, M ^a   Kobayashi, D ^e   Lin, J C ^e   Jack, C R ^c  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c Mayo Clinic   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

^e PFIZER INC   (United States)

Author keywords

MRS; Myo inositol; N acetylaspartate; Treatment detection

Indexed keywords

AMYLOID PRECURSOR PROTEIN; INOSITOL; N ACETYLASPARTIC ACID; PONEZUMAB; PRESENILIN 1;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; IN VIVO STUDY; MOUSE; NON INVASIVE MEASUREMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OUTCOME ASSESSMENT; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; SENILE PLAQUE; TRANSGENIC MOUSE; TREATMENT OUTCOME;

AD; ADIABATIC FULL-PASSAGE; ADIABATIC HALF-PASSAGE; AFP; AHP; ALZHEIMER'S DISEASE; CRAMÉR-RAO LOWER BOUNDS; CRLBS; FID; FREE INDUCTION DECAY; MAGNETIC RESONANCE SPECTROSCOPY; MINS; MRS; MYO-INOSITOL; N-ACETYLASPARTATE; NAA; TCR; TOTAL CREATINE, SUM OF CREATINE AND PHOSPHOCREATINE; TREATMENT DETECTION; WILD-TYPE; WT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ASPARTIC ACID; BRAIN; CHOLINE; DISEASE MODELS, ANIMAL; HUMANS; IMMUNIZATION, PASSIVE; INOSITOL; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; PEPTIDE FRAGMENTS; PRESENILIN-1; STATISTICS, NONPARAMETRIC;

EID: 84891354025     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.11.052     Document Type: Article

References (49)

1. Bard F., Cannon C., Barbour R., Burke R.L., Games D., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Liebergurg I., Motter R., Nguyen M., Soriano F., Vasquez N., Weiss K., Welch B., Seubert P., Schenk D., Yednock T. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nature Med 2000, 6:916-919.
2. Bonate P.L. Analysis of pretest-posttest designs 2000, Chapman & Hall/CRC, Boca Raton.
3. Brand A., Richter-Landsberg C., Leibfritz D. Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 1993, 15:289-298.
4. Chen S.Q., Cai Q., Shen Y.Y., Wang P.J., Teng G.J., Zhang W., Zang F.C. Age-related changes in brain metabolites and cognitive function in APP/PS1 transgenic mice. Behav Brain Res 2012, 235:1-6.
5. Chen S.Q., Wang P.J., Ten G.J., Zhan W., Li M.H., Zang F.C. Role of myo-inositol by magnetic resonance spectroscopy in early diagnosis of Alzheimer's disease in APP/PS1 transgenic mice. Dement Geriatr Cogn Disord 2009, 28:558-566.
6. Choi J.K., Dedeoglu A., Jenkins B.G. Application of MRS to mouse models of neurodegenerative illness. NMR Biomed 2007, 20:216-237.
7. Choi J.K., Jenkins B.G., Carreras I., Kaymakcalan S., Cormier K., Kowall N.W., Dedeoglu A. Anti-inflammatory treatment in AD mice protects against neuronal pathology. Exp Neurol 2010, 223:377-384.
8. Dedeoglu A., Choi J.K., Cormier K., Kowall N.W., Jenkins B.G. Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that express mutant human APP shows altered neurochemical profile. Brain Res 2004, 1012:60-65.
9. DeMattos R.B., Bales K.R., Cummins D.J., Dodart J.C., Paul S.M., Holtzman D.M. Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2001, 98:8850-8855.
10. Forster D., Davies K., Williams S. Magnetic resonance spectroscopy in vivo of neurochemicals in a transgenic model of Alzheimer's disease: A longitudinal study of metabolites, relaxation time, and behavioral analysis in TASTPM and wild-type mice. Magn Reson Med 2013, 69:944-955.
11. Fox J. Applied regression analysis and generalized linear models 2008, Sage, Los Angeles.
12. Freeman G.B., Lin J.C., Pons J., Raha N.M. 39-week toxicity and toxicokinetic study of ponezumab (PF-04360365) in cynomolgus monkeys with 12-week recovery period. J Alzheimers Dis 2012, 28:531-541.
13. Garwood M., DelaBarre L. The return of the frequency sweep: designing adiabatic pulses for contemporary NMR. J Magn Reson 2001, 153:155-177.
14. Garwood M., Ke Y. Symmetric pulses to induce arbitrary flip angles with compensation for RF inhomogeneity and resonance offsets. J Magn Reson 1991, 94:511-525.
15. Govindaraju V., Young K., Maudsley A.A. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 2000, 13:129-153.
16. Gruetter R. Automatic, localized in vivo adjustment of all first- and second-order shim coils. Magn Reson Med 1993, 29:804-811.
17. Gruetter R., Tkac I. Field mapping without reference scan using asymmetric echo-planar techniques. Magn Reson Med 2000, 43:319-323.
18. Hartman R.E., Izumi Y., Bales K.R., Paul S.M., Wozniak D.F., Holtzman D.M. Treatment with an amyloid-beta antibody ameliorates plaque load, learning deficits, and hippocampal long-term potentiation in a mouse model of Alzheimer's disease. J Neurosci 2005, 25:6213-6220.
19. Hebert L.E., Scherr P.A., Bienias J.L., Bennett D.A., Evans D.A. Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 2003, 60:1119-1122.
20. Hennig J., Nauerth A., Friedburg H. RARE imaging: a fast imaging method for clinical MR. Magn Reson Med 1986, 3:823-833.
21. Henry P.G., Marjanska M., Walls J.D., 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.
22. Holcomb L., Gordon M.N., 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 C.M., Eckman C., Younkin S., Hsiao K., Duff K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 1998, 4:97-100.
23. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
24. Jack C.R., Garwood M., Wengenack T.M., Borowski B., Curran G.L., Lin J., Adriany G., Grohn O.H., Grimm R., Poduslo J.F. In vivo visualization of Alzheimer's amyloid plaques by magnetic resonance imaging in transgenic mice without a contrast agent. Magn Reson Med 2004, 52:1263-1271.
25. Jack C.R., Marjanska M., Wengenack T.M., Reyes D.A., Curran G.L., Lin J., Preboske G.M., Poduslo J.F., Garwood M. Magnetic resonance imaging of Alzheimer's pathology in the brains of living transgenic mice: a new tool in Alzheimer's disease research. Neuroscientist 2007, 13:38-48.
26. Jansen D., Zerbi V., Janssen C.I.F., Dederen P., Mutsaers M.P.C., Hafkemeijer A., Janssen A.L., Nobelen C.L.M., Veltien A., Asten J.J., Heerschap A., Kiliaan A.J. A longitudinal study of cognition, proton MR spectroscopy and synaptic and neuronal pathology in aging wild-type and A beta PPswe-PS1dE9 mice. PLoS One 2013, 8:e63643.
27. Kantarci K., Lowe V., Przybelski S.A., Senjem M.L., Weigand S.D., Ivnik R.J., Roberts R., Geda Y.E., Boeve B.F., Knopman D.S., Petersen R.C., Jack C.R. Magnetic resonance spectroscopy, beta-amyloid load, and cognition in a population-based sample of cognitively normal older adults. Neurology 2011, 77:951-958.
28. Karlnoski R.A., Rosenthal A., Alamed J., Ronan V., Gordon M.N., Gottschall P.E., Grimm J., Pons J., Morgan D. Deglycosylated anti-Aβ antibody dose-response effects on pathology and memory in APP transgenic mice. J Neuroimmune Pharmacol 2008, 3:187-197.
29. La Porte S.L., Bollini S.S., Lanz T.A., Abdiche Y.N., Rusnak A.S., Ho W.H., Kobayashi D., Harrabi O., Pappas D., Mina E.W., Milici A.J., Kawabe T.T., Bales K., Lin J.C., Pons J. Structural basis of C-terminal beta-amyloid peptide binding by the antibody ponezumab for the treatment of Alzheimer's disease. J Mol Biol 2012, 421:525-536.
30. Little R.J.A., Rubin D.B. Statistical analysis with missing data 2002, Wiley, Hoboken, N.J.
31. Marjanska M., Curran G.L., Wengenach T.M., Henry P.-G., Bliss R.L., Poduslo J.F., Jack C.R.J., Ugurbil K., Garwood M. Monitoring disease progression in transgenic mouse models of Alzheimer's disease with proton magnetic resonance spectroscopy. Proc Natl Acad of Sci U S A 2005, 102:11906-11910.
32. Mlynarik V., Cacquevel M., Sun-Reimer L., Janssens S., Cudalbu C., Lei H.X., Schneider B.L., Aebischer P., Gruetter R. Proton and phosphorus magnetic resonance spectroscopy of a mouse model of Alzheimer's disease. J Alzheimers Dis 2012, 31:S87-S99.
33. Murray ME, Przybelski SA, Lesnick T, Liesinger AM, Spychalla A, Gunter JL, Parisi JE, Boeve BF, Knopman DS, Petersen RC, Jack CR, Jr., Dickson DW, Kantarci K (2013) Aberrant tau and amyloid pathology underlies proton MR spectroscopic alterations in Alzheimer's disease. In: Alzheimer's Association International Conference Boston.
34. O'Brien P.C. The appropriateness of analysis of variance and multiple-comparison procedures. Biometrics 1983, 39:787-794.
35. Oberg J., Spenger C., Wang F.H., Andersson A., Westman E., Skoglund P., Sunnemark D., Norinder U., Klason T., Wahlund L.O., Lindberg M. Age related changes in brain metabolites observed by H-1 MRS in APP/PS1 mice. Neurobiol Aging 2008, 29:1423-1433.
36. 1H NMR spectra of the rat brain. J Magn Reson 1999, 141:104-120.
37. Provencher S.W. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 1993, 30:672-679.
38. 1H spectra with LCModel. NMR Biomed 2001, 14:260-264.
39. Selkoe D.J. Deciphering Alzheimer's disease: molecular genetics and cell biology yield major clues. J NIH Res 1995, 7:57-64.
40. Selkoe DJ, Molecular pathology of Alzheimer's disease: the role of amyloid. In: The dementias: blue book of neurology series, vol. 19. Growden, editor, Newton, MA: Butterworth-Heinemann; 1998. p. 257-283.
41. Senn S. Change from baseline and analysis of covariance revisited. Stat Med 2006, 25:4334-4344.
42. Silver M.S., Joseph R.I., Hoult D.I. Highly selective π/2 and π pulse generation. J Magn Reson 1984, 59:347-351.
43. 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med 1999, 41:649-656.
44. van Duijn S., Nabuurs R.J.A., van Duinen S.G., Natte R., van Buchem M.A., Alia A. Longitudinal monitoring of sex-related in vivo metabolic changes in the brain of Alzheimer's disease transgenic mouse using magnetic resonance spectroscopy. J Alzheimers Dis 2013, 34:1051-1059.
45. von Kienlin M., Kunnecke B., Metzger F., Steiner G., Richards J.G., Ozmen L., Jacobsen H., Loetscher H. Altered metabolic profile in the frontal cortex of PS2APP transgenic mice, monitored throughout their life span. Neurobiol Dis 2005, 18:32-39.
46. 1H-magnetic resonance spectroscopy can detect metabolic changes in APP/PS1 mice after donepezil treatment. BMC Neurosci 2009, 10:33.
47. Wilcock D., Rojiani A., Rosenthal A., Levkowitz G., Subbarao S., Alamed J., Wilson D., Wilson N., Freeman M.J., Gordon M.N., Morgan D. Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 2004, 24:6144-6151.
48. Wilcock D., Rojiani A., Rosenthal A., Subbarao S., Freeman M.J., Gordon M.N., Morgan D. Passive immunotherapy against Abeta in ages APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage. J Neuroinflamm 2004, 1:24.
49. Wilcock D.M., Alamed J., Gottschall P.E., Grimm J., Rosenthal A., Pons J., Ronan V., Symmonds K., Gordon M.N., Morgan D. Deglycosylated anti-amyloid-β antibodies eliminate cognitive deficits and reduce parenchymal amyloid with minimal vascular consequences in aged amyloid precursor protein transgenic mice. J Neurosci 2006, 26:5340-5346.