Striatum and entorhinal cortex atrophy in AD mouse models: MRI comprehensive analysis

Neurobiology of Aging

Volumn 36, Issue 2, 2015, Pages 776-788

  Micotti, Edoardo ^a   Paladini, Alessandra ^a   Balducci, Claudia ^a   Tolomeo, Daniele ^a   Frasca, Angelisa ^a   Marizzoni, Moira ^b   Filibian, Marta ^a   Caroli, Anna ^a   Valbusa, Giovanni ^c   Dix, Sophie ^d   O'Neill, Mike ^d   Ozmen, Laurence ^e   Czech, Christian ^e   Richardson, Jill C ^f   Frisoni, Giovanni B ^b   Forloni, Gianluigi ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

^c Ephoran Multi Imaging Solutions Srl   (Italy)

^d ELI LILLY AND COMPANY   (United States)

^e F HOFFMANN LA ROCHE LTD   (Switzerland)

^f GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Alzheimer's disease; Animal models; IMI PharmaCog; MRI; MRS; Pharmacology; Translational research

Indexed keywords

BIOLOGICAL MARKER; GLUTAMIC ACID; INOSITOL; SYNAPTOPHYSIN; AMYLOID PRECURSOR PROTEIN; GLUTAMIC ACID DERIVATIVE; PRESENILIN; TAU PROTEIN;

ALZHEIMER DISEASE; AMINO ACID BRAIN LEVEL; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN SIZE; BRAIN VENTRICLE; CELL ACTIVATION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE ASSOCIATION; DISEASE COURSE; ENTORHINAL CORTEX; FEMALE; GENOTYPE; GLIA CELL; MALE; MOUSE; MOUSE MODEL; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN DEPLETION; WILD TYPE MOUSE; ANIMAL; ATROPHY; DISEASE MODEL; GENE EXPRESSION; GENETICS; HIPPOCAMPUS; HUMAN; METABOLISM; MUTATION; PATHOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ATROPHY; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; ENTORHINAL CORTEX; FEMALE; GENE EXPRESSION; GLUTAMATES; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MICE, TRANSGENIC; MUTATION; PRESENILINS; TAU PROTEINS;

EID: 84922772178     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.10.027     Document Type: Article

References (47)

1. Balducci C., Forloni G. APP transgenic mice: their use and limitations. Neuromolecular Med. 2011, 13:117-137.
2. Balducci C., Tonini R., Zianni E., Nazzaro C., Fiordaliso F., Salio M., Vismara L., Gardoni F., Di Luca M., Carli M., Forloni G. Cognitive deficits associated with alteration of synaptic metaplasticity precede plaque deposition in AbetaPP23 transgenic mice. J.Alzheimers Dis. 2010, 21:1367-1381.
3. Benilova I., Karran E., De Strooper B. The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 2012, 15:349-357.
4. Bohanna I., Georgiou-Karistianis N., Egan G.F. Connectivity-based segmentation of the striatum in Huntington's disease: vulnerability of motor pathways. Neurobiol. Dis. 2011, 42:475-481.
5. Braak H., Braak E. Alzheimer's disease: striatal amyloid deposits and neurofibrillary changes. J.Neuropathol. Exp. Neurol. 1990, 49:215-224.
6. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
7. Burggren A.C., Renner B., Jones M., Donix M., Suthana N.A., Martin-Harris L., Ercoli L.M., Miller K.J., Siddarth P., Small G.W., Bookheimer S.Y. Thickness in entorhinal and subicular cortex predicts episodic memory decline in mild cognitive impairment. Int. J. Alzheimers Dis. 2011, 2011:956053.
8. Caroli A., Frisoni G.B. Quantitative evaluation of Alzheimer's disease. Expert Rev. Med. Devices 2009, 6:569-588.
9. El Tayara Nel T., Volk A., Dhenain M., Delatour B. Transverse relaxation time reflects brain amyloidosis in young APP/PS1 transgenic mice. Magn. Reson. Med. 2007, 58:179-184.
10. Esteras N., Alquezar C., Bartolome F., Antequera D., Barrios L., Carro E., Cerdan S., Martin-Requero A. Systematic evaluation of magnetic resonance imaging and spectroscopy techniques for imaging a transgenic model of Alzheimer's disease (AbetaPP/PS1). J.Alzheimers Dis. 2012, 30:337-353.
11. Falangola M.F., Dyakin V.V., Lee S.P., Bogart A., Babb J.S., Duff K., Nixon R., Helpern J.A. Quantitative MRI reveals aging-associated T2 changes in mouse models of Alzheimer's disease. NMR Biomed. 2007, 20:343-351.
12. Fellgiebel A., Wille P., Muller M.J., Winterer G., Scheurich A., Vucurevic G., Schmidt L.G., Stoeter P. Ultrastructural hippocampal and white matter alterations in mild cognitive impairment: a diffusion tensor imaging study. Dement Geriatr. Cogn. Disord. 2004, 18:101-108.
13. Filibian M., Frasca A., Maggioni D., Micotti E., Vezzani A., Ravizza T. Invivo imaging of glia activation using 1H-magnetic resonance spectroscopy to detect putative biomarkers of tissue epileptogenicity. Epilepsia 2013, 53:1907-1916.
14. Forloni G., Sclip A., Borsello T., Balducci C. The neurodegeneration in Alzheimer disease and the prion protein. Prion 2013, 7:60-65.
15. Forster D., Davies K., Williams S. Magnetic resonance spectroscopy invivo 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.
16. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 1997, Press, A, London.
17. Griffey R., Flamig D. VAPOR for solvent-suppressed, short-echo, volume-localized proton spectrocopy. J.Magn. Reson. 1990, 88:161-166.
18. Gruetter R. Automatic, localized invivo adjustment of all first- and second-order shim coils. Magn. Reson. Med. 1993, 29:804-811.
19. Higuchi M., Iwata N., Matsuba Y., Sato K., Sasamoto K., Saido T.C. 19F and 1H MRI detection of amyloid beta plaques invivo. Nat. Neurosci. 2005, 8:527-533.
20. Howlett D.R., Richardson J.C., Austin A., Parsons A.A., Bate S.T., Davies D.C., Gonzalez M.I. Cognitive correlates of Abeta deposition in male and female mice bearing amyloid precursor protein and presenilin-1 mutant transgenes. Brain Res. 2004, 1017:130-136.
21. Jonckers E., Van Audekerke J., De Visscher G., Van der Linden A., Verhoye M. Functional connectivity fMRI of the rodent brain: comparison of functional connectivity networks in rat and mouse. PLoS One 2011, 6:e18876.
22. Kantarci K., Petersen R.C., Boeve B.F., Knopman D.S., Weigand S.D., O'Brien P.C., Shiung M.M., Smith G.E., Ivnik R.J., Tangalos E.G., Jack C.R. DWI predicts future progression to Alzheimer disease in amnestic mild cognitive impairment. Neurology 2005, 64:902-904.
23. Kantarci K., Weigand S.D., Petersen R.C., Boeve B.F., Knopman D.S., Gunter J., Reyes D., Shiung M., O'Brien P.C., Smith G.E., Ivnik R.J., Tangalos E.G., Jack C.R. Longitudinal 1H MRS changes in mild cognitive impairment and Alzheimer's disease. Neurobiol. Aging 2007, 28:1330-1339.
24. Klunk W.E., Price J.C., Mathis C.A., Tsopelas N.D., Lopresti B.J., Ziolko S.K., Bi W., Hoge J.A., Cohen A.D., Ikonomovic M.D., Saxton J.A., Snitz B.E., Pollen D.A., Moonis M., Lippa C.F., Swearer J.M., Johnson K.A., Rentz D.M., Fischman A.J., Aizenstein H.J., DeKosky S.T. Amyloid deposition begins in the striatum of presenilin-1 mutation carriers from two unrelated pedigrees. J.Neurosci. 2007, 27:6174-6184.
25. Knight W.D., Okello A.A., Ryan N.S., Turkheimer F.E., Rodriguez Martinez de Llano S., Edison P., Douglas J., Fox N.C., Brooks D.J., Rossor M.N. Carbon-11-Pittsburgh compound B positron emission tomography imaging of amyloid deposition in presenilin 1 mutation carriers. Brain 2011, 134(Pt 1):293-300.
26. Marjanska M., Curran G.L., Wengenack T.M., Henry P.G., Bliss R.L., Poduslo J.F., Jack C.R., Ugurbil K., Garwood M. Monitoring disease progression in transgenic mouse models of Alzheimer's disease with proton magnetic resonance spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11906-11910.
27. McKinstry R.C., Mathur A., Miller J.H., Ozcan A., Snyder A.Z., Schefft G.L., Almli C.R., Shiran S.I., Conturo T.E., Neil J.J. Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb. Cortex 2002, 12:1237-1243.
28. Mlynarik V., Cacquevel M., Sun-Reimer L., Janssens S., Cudalbu C., Lei H., 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(Suppl 3):S87-S99.
29. Nairismägi J., Pitkänen A., Kettunen M.I., Kauppinen R.A., Kubova H. Status epilepticus in 12-day-old rats leads to temporal lobe neurodegeneration and volume reduction: a histologic and MRI study. Epilepsia 2006, 47:479-488.
30. Näslund J., Haroutunian V., Mohs R., Davis K.L., Davies P., Greengard P., Buxbaum J.D. Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 2000, 29:1571-1577.
31. Perego C., Fumagalli S., De Simoni M.G. Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J.Neuroinflammation 2011, 8:174.
32. Rattray I., Pitiot A., Lowe J., Auer D.P., Lima S.J., Schubert M.I., Prior M.J., Marsden C.A., Diaz F.P., Kendall D.A., Pardon M.C. Novel cage stress alters remote contextual fear extinction and regional T2 magnetic resonance relaxation times in TASTPM mice overexpressing amyloid. J.Alzheimers Dis. 2010, 20:1049-1068.
33. Ravizza T., Gagliardi B., Noe F., Boer K., Aronica E., Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol. Dis. 2008, 29:142-160.
34. Redwine J.M., Kosofsky B., Jacobs R.E., Games D., Reilly J.F., Morrison J.H., Young W.G., Bloom F.E. Dentate gyrus volume is reduced before onset of plaque formation in PDAPP mice: a magnetic resonance microscopy and stereologic analysis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:1381-1386.
35. Rhein V., Song X., Wiesner A., Ittner L.M., Baysang G., Meier F., Ozmen L., Bluethmann H., Drose S., Brandt U., Savaskan E., Czech C., Gotz J., Eckert A. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20057-20062.
36. Rutten B.P., Van der Kolk N.M., Schafer S., van Zandvoort M.A., Bayer T.A., Steinbusch H.W., Schmitz C. Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL/PS1M146L transgenic mice. Am. J. Pathol. 2005, 167:161-173.
37. Ryan N.S., Keihaninejad S., Shakespeare T.J., Lehmann M., Crutch S.J., Malone I.B., Thornton J.S., Mancini L., Hyare H., Yousry T., Ridgway G.R., Zhang H., Modat M., Alexander D.C., Rossor M.N., Ourselin S., Fox N.C. Magnetic resonance imaging evidence for presymptomatic change in thalamus and caudate in familial Alzheimer's disease. Brain 2013, 136(Pt 5):1399-1414.
38. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
39. Shah D., Jonckers E., Praet J., Vanhoutte G., Delgado Y.P.R., Bigot C., D'Souza D.V., Verhoye M., Van der Linden A. Resting state FMRI reveals diminished functional connectivity in a mouse model of amyloidosis. PLoS One 2013, 8:e84241.
40. Song S.K., Kim J.H., Lin S.J., Brendza R.P., Holtzman D.M. Diffusion tensor imaging detects age-dependent white matter changes in a transgenic mouse model with amyloid deposition. Neurobiol. Dis. 2004, 15:640-647.
41. Pievani M., Bocchetta M., Boccardi M., Cavedo E., Bonetti M., Thompson P.M., Frisoni G.B. Striatal morphology in early-onset and late-onset Alzheimer's disease: a preliminary study. Neurobiol. Aging 2013, 34:1728-1739.
42. Vanhoutte G., Pereson S., Delgado Y.P.R., Guns P.J., Asselbergh B., Veraart J., Sijbers J., Verhoye M., Van Broeckhoven C., Van der Linden A. Diffusion kurtosis imaging to detect amyloidosis in an APP/PS1 mouse model for Alzheimer's disease. Magn. Reson. Med. 2013, 69:1115-1121.
43. Velayudhan L., Proitsi P., Westman E., Muehlboeck J.S., Mecocci P., Vellas B., Tsolaki M., Kloszewska I., Soininen H., Spenger C., Hodges A., Powell J., Lovestone S., Simmons A. Entorhinal cortex thickness predicts cognitive decline in Alzheimer's disease. J.Alzheimers Dis. 2013, 33:755-766.
44. Villemagne V.L., Ataka S., Mizuno T., Brooks W.S., Wada Y., Kondo M., Jones G., Watanabe Y., Mulligan R., Nakagawa M., Miki T., Shimada H., O'Keefe G.J., Masters C.L., Mori H., Rowe C.C. High striatal amyloid beta-peptide deposition across different autosomal Alzheimer disease mutation types. Arch. Neurol. 2009, 66:1537-1544.
45. Wilson M., Reynolds G., Kauppinen R.A., Arvanitis T.N., Peet A.C. Aconstrained least-squares approach to the automated quantitation of invivo (1)H magnetic resonance spectroscopy data. Magn. Reson. Med. 2011, 65:1-12.
46. Yanagisawa D., Taguchi H., Ibrahim N.F., Morikawa S., Shiino A., Inubushi T., Hirao K., Shirai N., Sogabe T., Tooyama I. Preferred features of a fluorine-19 MRI probe for amyloid detection in the brain. J.Alzheimers Dis. 2014, 39:617-631.
47. Yang D., Xie Z., Stephenson D., Morton D., Hicks C.D., Brown T.M., Sriram R., O'Neill S., Raunig D., Bocan T. Volumetric MRI and MRS provide sensitive measures of Alzheimer's disease neuropathology in inducible tau transgenic mice (rTg4510). Neuroimage 2010, 54:2652-2658.