Magnetization transfer contrast imaging reveals amyloid pathology in Alzheimer's disease transgenic mice

NeuroImage

Volumn 87, Issue , 2014, Pages 111-119

  Bigot, Christian ^a   Vanhoutte, Greetje ^a   Verhoye, Marleen ^a   Van der Linden, Annemie ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN REGION; CEREBRAL PEDUNCLE; DIAGNOSTIC ACCURACY; FEMALE; GLIOSIS; GRAY MATTER; HIPPOCAMPUS; IMAGE ANALYSIS; IMAGE QUALITY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEOCORTEX; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; THALAMUS; WHITE MATTER;

ALZHEIMER DISEASE; ANIMALS; BRAIN; CONTRAST MEDIA; DISEASE MODELS, ANIMAL; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, TRANSGENIC; PLAQUE, AMYLOID;

EID: 84890952272     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.10.056     Document Type: Article

References (76)

1. Ballard C., Khan Z., Clack H., Corbett A. Nonpharmacological treatment of Alzheimer disease. Can. J. Psychiatry 2011, 56:589-595.
2. Ballatore C., Lee V.M., Trojanowski J.Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 2007, 8:663-672.
3. Barthel H., Luthardt J., Becker G., Patt M., Hammerstein E., Hartwig K., Eggers B., Sattler B., Schildan A., Hesse S., Meyer P.M., Wolf H., Zimmermann T., Reischl J., Rohde B., Gertz H.J., Reininger C., Sabri O. Individualized quantification of brain beta-amyloid burden: results of a proof of mechanism phase 0 florbetaben PET trial in patients with Alzheimer's disease and healthy controls. Eur. J. Nucl. Med. Mol. Imaging 2011, 38:1702-1714.
4. Berry I., Barker G.J., Barkhof F., Campi A., Dousset V., Franconi J.M., Gass A., Schreiber W., Miller D.H., Tofts P.S. A multicenter measurement of magnetization transfer ratio in normal white matter. J. Magn. Reson. Imaging 1999, 9:441-446.
5. Bobinski M., de Leon M.J., Wegiel J., Desanti S., Convit A., Saint Louis L.A., Rusinek H., Wisniewski H.M. The histological validation of post mortem magnetic resonance imaging-determined hippocampal volume in Alzheimer's disease. Neuroscience 2000, 95:721-725.
6. Bozzali M., Franceschi M., Falini A., Pontesilli S., Cercignani M., Magnani G., Scotti G., Comi G., Filippi M. Quantification of tissue damage in AD using diffusion tensor and magnetization transfer MRI. Neurology 2001, 57:1135-1137.
7. Ceckler T.L., Balaban R.S. Tritium proton magnetization transfer as a probe of cross relaxation in aqueous lipid bilayer suspensions. J. Magn. Reson. 1991, 93:572-588.
8. Craig-Schapiro R., Fagan A.M., Holtzman D.M. Biomarkers of Alzheimer's disease. Neurobiol. Dis. 2009, 35:128-140.
9. Dousset V., Grossman R.I., Ramer K.N., Schnall M.D., Young L.H., Gonzalez-Scarano F., Lavi E., Cohen J.A. Experimental allergic encephalomyelitis and multiple sclerosis: lesion characterization with magnetization transfer imaging. Radiology 1992, 182:483-491.
10. Engelborghs S., De Deyn P.P. Biological and genetic markers of sporadic Alzheimer's disease. Acta Med. Okayama 2001, 55:55-63.
11. Engelborghs S., Le Bastard N. The impact of cerebrospinal fluid biomarkers on the diagnosis of Alzheimer's disease. Mol. Diagn. Ther. 2012, 16:135-141.
12. Faber C., Zahneisen B., Tippmann F., Schroeder A., Fahrenholz F. Gradient-echo and CRAZED imaging for minute detection of Alzheimer plaques in an APPV717I×ADAM10-dn mouse model. Magn. Reson. Med. 2007, 57:696-703.
13. 2 changes in mouse models of Alzheimer's disease. NMR Biomed. 2007, 20:343-351.
14. Fornari E., Maeder P., Meuli R., Ghika J., Knyazeva M.G. Demyelination of superficial white matter in early Alzheimer's disease: a magnetization transfer imaging study. Neurobiol. Aging 2012, 33(428):7-19.
15. 2 relaxation measurements with histopathologic correlation in an experimental model of MS. J. Magn. Reson. Imaging 2000, 11:586-595.
16. Giulietti G., Bozzali M., Figura V., Spano B., Perri R., Marra C., Lacidogna G., Giubilei F., Caltagirone C., Cercignani M. Quantitative magnetization transfer provides information complementary to grey matter atrophy in Alzheimer's disease brains. Neuroimage 2012, 59:1114-1122.
17. Glenner G.G., Wong C.W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 1984, 120:885-890.
18. Gordon M.N., Holcomb L.A., Jantzen P.T., DiCarlo G., Wilcock D., Boyett K.W., Connor K., Melachrino J., O'Callaghan J.P., Morgan D. Time course of the development of Alzheimer-like pathology in the doubly transgenic PS1+APP mouse. Exp. Neurol. 2002, 173:183-195.
19. Gosche K.M., Mortimer J.A., Smith C.D., Markesbery W.R., Snowdon D.A. Hippocampal volume as an index of Alzheimer neuropathology: findings from the Nun Study. Neurology 2002, 58:1476-1482.
20. Graham S.J., Henkelman R.M. Pulsed magnetization transfer imaging: evaluation of technique. Radiology 1999, 212:903-910.
21. Guo S., Getsios D., Hernandez L., Cho K., Lawler E., Altincatal A., Lanes S., Blankenburg M. Florbetaben PET in the early diagnosis of Alzheimer's disease: a discrete event simulation to explore its potential value and key data gaps. Int. J. Alzheimers Dis. 2012, 2012:548157.
22. Hanyu H., Asano T., Sakurai H., Imon Y., Iwamoto T., Takasaki M., Shindo H., Abe K. Diffusion-weighted and magnetization transfer imaging of the corpus callosum in Alzheimer's disease. J. Neurol. Sci. 1999, 167:37-44.
23. Henkelman R.M., Huang X.M., Xiang Q.S., Stanisz G.J., Swanson S.D., Bronskill M.J. Quantitative interpretation of magnetization-transfer. Magn. Reson. Med. 1993, 29:759-766.
24. Henkelman R.M., Stanisz G.J., Graham S.J. Magnetization transfer in MRI: a review. NMR Biomed. 2001, 14:57-64.
25. Hock C., Golombowski S., Naser W., Muller-Spahn F. Increased levels of tau protein in cerebrospinal fluid of patients with Alzheimer's disease-correlation with degree of cognitive impairment. Ann. Neurol. 1995, 37:414-415.
26. Hyman B.T., Van Hoesen G.W., Damasio A.R. Memory-related neural systems in Alzheimer's disease: an anatomic study. Neurology 1990, 40:1721-1730.
27. Ikuta F., Yoshida Y., Ohama E., Oyanagi K., Takeda S., Yamazaki K., Watabe K. Revised pathophysiology on BBB damage: the edema as an ingeniously provided condition for cell motility and lesion repair. Acta Neuropathol. Suppl. 1983, 8:103-110.
28. Imon Y., Hanyu H., Iwamoto T., Takasaki M., Abe K. Atrophy and magnetization transfer ratio of the corpus callosum in patients with Alzheimer's disease. Rinsho Shinkeigaku 1998, 38:1014-1018.
29. Jack C.R., Dickson D.W., Parisi J.E., Xu Y.C., Cha R.H., O'Brien P.C., Edland S.D., Smith G.E., Boeve B.F., Tangalos E.G., Kokmen E., Petersen R.C. Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology 2002, 58:750-757.
30. 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.
31. Jack C.R., Knopman D.S., Jagust W.J., Shaw L.M., Aisen P.S., Weiner M.W., Petersen R.C., Trojanowski J.Q. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 2010, 9:119-128.
32. Jucker M. The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat. Med. 2010, 16:1210-1214.
33. Kabani N.J., Sled J.G., Chertkow H. Magnetization transfer ratio in mild cognitive impairment and dementia of Alzheimer's type. Neuroimage 2002, 15:604-610.
34. Kalback W., Watson M.D., Kokjohn T.A., Kuo Y.M., Weiss N., Luehrs D.C., Lopez J., Brune D., Sisodia S.S., Staufenbiel M., Emmerling M., Roher A.E. APP transgenic mice Tg2576 accumulate Abeta peptides that are distinct from the chemically modified and insoluble peptides deposited in Alzheimer's disease senile plaques. Biochemistry 2002, 41:922-928.
35. Kiefer C., Brockhaus L., Cattapan-Ludewig K., Ballinari P., Burren Y., Schroth G., Wiest R. Multi-parametric classification of Alzheimer's disease and mild cognitive impairment: the impact of quantitative magnetization transfer MR imaging. Neuroimage 2009, 48:657-667.
36. Klohs J., Deistung A., Schweser F., Grandjean J., Dominietto M., Waschkies C., Nitsch R.M., Knuesel I., Reichenbach J.R., Rudin M. Detection of cerebral microbleeds with quantitative susceptibility mapping in the ArcAbeta mouse model of cerebral amyloidosis. J. Cereb. Blood Flow Metab. 2011, 31:2282-2292.
37. Klunk W.E., Engler H., Nordberg A., Bacskai B.J., Wang Y., Price J.C., Bergstrom M., Hyman B.T., Langstrom B., Mathis C.A. Imaging the pathology of Alzheimer's disease: amyloid-imaging with positron emission tomography. Neuroimaging Clin. N. Am. 2003, 13:781-789. (ix).
38. Klunk W.E., Engler H., Nordberg A., Wang Y.M., Blomqvist G., Holt D.P., Bergstrom M., Savitcheva I., Huang G.F., Estrada S., Ausen B., Debnath M.L., Barletta J., Price J.C., Sandell J., Lopresti B.J., Wall A., Koivisto P., Antoni G., Mathis C.A., Langstrom B. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann. Neurol. 2004, 55:306-319.
39. Kuo Y.M., Kokjohn T.A., Beach T.G., Sue L.I., Brune D., Lopez J.C., Kalback W.M., Abramowski D., Sturchler-Pierrat C., Staufenbiel M., Roher A.E. Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J. Biol. Chem. 2001, 276:12991-12998.
40. Latov N., Nilaver G., Zimmerman E.A., Johnson W.G., Silverman A.J., Defendini R., Cote L. Fibrillary astrocytes proliferate in response to brain injury: a study combining immunoperoxidase technique for glial fibrillary acidic protein and radioautography of tritiated thymidine. Dev. Biol. 1979, 72:381-384.
41. Mann D.M. The pathogenesis and progression of the pathological changes of Alzheimer's disease. Ann. Med. 1989, 21:133-136.
42. Masters C.L., Simms G., Weinman N.A., Multhaup G., McDonald B.L., Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:4245-4249.
43. McConnell H.M., Thompson D.D. Molecular transfer of nonequilibrium nuclear spin magnetization. J. Chem. Phys. 1957, 26:958-959.
44. McGowan E., Pickford F., Kim J., Onstead L., Eriksen J., Yu C., Skipper L., Murphy M.P., Beard J., Das P., Jansen K., Delucia M., Lin W.L., Dolios G., Wang R., Eckman C.B., Dickson D.W., Hutton M., Hardy J., Golde T. Abeta42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron 2005, 47:191-199.
45. Meadowcroft M.D., Herse Z.G., Connor J.R., Yang Q.X. Magnetization transfer imaging of individual beta-amyloid plaques in Alzheimer's disease. Proc. Int. Soc. Magn. Reson. Med. 2011, 19:1.
46. Nagele R.G., Wegiel J., Venkataraman V., Imaki H., Wang K.C., Wegiel J. Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol. Aging 2004, 25:663-674.
47. Nakahara M., Hayashi H., Kumazaki T., Mori O. Value of magnetization transfer contrast as a sensitive technique to reflect histopathological changes in the white matter adjacent to the frontal horns of lateral ventricles. Nihon Ika Daigaku Zasshi 1999, 66:245-252.
48. Pérez-Torres C.J., Reynolds J.O., Pautler R.G. Use of magnetization transfer contrast MRI to detect early molecular pathology in Alzheimer's disease. Magn. Reson. Med 2013, (Electronic publication ahead of print). 10.1002/mrm.24665.
49. Petiet A., Santin M., Bertrand A., Wiggins C.J., Petit F., Houitte D., Hantraye P., Benavides J., Debeir T., Rooney T., Dhenain M. Gadolinium-staining reveals amyloid plaques in the brain of Alzheimer's transgenic mice. Neurobiol. Aging 2012, 33:1533-1544.
50. Pike G.B., Glover G.H., Hu B.S., Enzmann D.R. Pulsed magnetization transfer spin-echo MR imaging. J. Magn. Reson. Imaging 1993, 3:531-539.
51. Poduslo J.F., Wengenack T.M., Curran G.L., Wisniewski T., Sigurdsson E.M., Macura S.I., Borowski B.J., Jack C.R. Molecular targeting of Alzheimer's amyloid plaques for contrast-enhanced magnetic resonance imaging. Neurobiol. Dis. 2002, 11:315-329.
52. Praet J., Reekmans K., Lin D., De Vocht N., Bergwerf I., Tambuyzer B., Daans J., Hens N., Goossens H., Pauwels P., Berneman Z., Van der Linden A., Ponsaerts P. Cell type-associated differences in migration, survival, and immunogenicity following grafting in CNS tissue. Cell Transplant. 2012, 21:1867-1881.
53. Radde R., Bolmont T., Kaeser S.A., Coomaraswamy J., Lindau D., Stoltze L., Calhoun M.E., Jaggi F., Wolburg H., Gengler S., Haass C., Ghetti B., Czech C., Holscher C., Mathews P.M., Jucker M. Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep. 2006, 7:940-946.
54. Ramani A., Jensen J.H., Helpern J.A. Quantitative MR imaging in Alzheimer disease. Radiology 2006, 241:26-44.
55. Rausch M., Tofts P., Lervik P., Walmsley A., Mir A., Schubart A., Seabrook T. Characterization of white matter damage in animal models of multiple sclerosis by magnetization transfer ratio and quantitative mapping of the apparent bound proton fraction f. Mult. Scler. 2009, 15:16-27.
56. Ridha B.H., Symms M.R., Tozer D.J., Stockton K.C., Frost C., Siddique M.M., Lewis E.B., MacManus D.G., Boulby P.A., Barker G.J., Rossor M.N., Fox N.C., Tofts P.S. Magnetization transfer ratio in Alzheimer disease: comparison with volumetric measurements. AJNR Am. J. Neuroradiol. 2007, 28:965-970.
57. Ridha B.H., Tozer D.J., Symms M.R., Stockton K.C., Lewis E.B., Siddique M.M., MacManus D.G., Rossor M.N., Fox N.C., Tofts P.S. Quantitative magnetization transfer imaging in Alzheimer disease. Radiology 2007, 244:832-837.
58. Roher A.E., Lowenson J.D., Clarke S., Wolkow C., Wang R., Cotter R.J., Reardon I.M., Zurcher-Neely H.A., Heinrikson R.L., Ball M.J., et al. Structural alterations in the peptide backbone of beta-amyloid core protein may account for its deposition and stability in Alzheimer's disease. J. Biol. Chem. 1993, 268:3072-3083.
59. Ropele S., Schmidt R., Enzinger C., Windisch M., Martinez N.P., Fazekas F. Longitudinal magnetization transfer imaging in mild to severe Alzheimer disease. AJNR Am. J. Neuroradiol. 2012, 33:570-575.
60. Rovira A., Leon A. MR in the diagnosis and monitoring of multiple sclerosis: an overview. Eur. J. Radiol. 2008, 67:409-414.
61. 1-weighted and magnetization-transfer MR images. AJNR Am. J. Neuroradiol. 1999, 20:1939-1945.
62. Serres S., Anthony D.C., Jiang Y., Campbell S.J., Broom K.A., Khrapitchev A., Sibson N.R. Comparison of MRI signatures in pattern I and II multiple sclerosis models. NMR Biomed. 2009, 22:1014-1024.
63. Silbert L.C., Quinn J.F., Moore M.M., Corbridge E., Ball M.J., Murdoch G., Sexton G., Kaye J.A. Changes in premorbid brain volume predict Alzheimer's disease pathology. Neurology 2003, 61:487-492.
64. Sled J.G., Pike G.B. Quantitative imaging of magnetization transfer exchange and relaxation properties in vivo using MRI. Magn. Reson. Med. 2001, 46:923-931.
65. Smith C.J. Diagnostic tests (1) - sensitivity and specificity. Phlebology 2012, 27:250-251.
66. Smith S.A., Farrell J.A., Jones C.K., Reich D.S., Calabresi P.A., van Zijl P.C. Pulsed magnetization transfer imaging with body coil transmission at 3Tesla: feasibility and application. Magn. Reson. Med. 2006, 56:866-875.
67. Sperling R.A., Aisen P.S., Beckett L.A., Bennett D.A., Craft S., Fagan A.M., Iwatsubo T., Jack C.R., Kaye J., Montine T.J., Park D.C., Reiman E.M., Rowe C.C., Siemers E., Stern Y., Yaffe K., Carrillo M.C., Thies B., Morrison-Bogorad M., Wagster M.V., Phelps C.H. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 2011, 7:280-292.
68. Vanhoutte G., Dewachter I., Borghgraef P., Van Leuven F., Van der Linden A. Noninvasive in vivo MRI detection of neuritic plaques associated with iron in APP[V717I] transgenic mice, a model for Alzheimer's disease. Magn. Reson. Med. 2005, 53:607-613.
69. Vemuri P., Gunter J.L., Senjem M.L., Whitwell J.L., Kantarci K., Knopman D.S., Boeve B.F., Petersen R.C., Jack C.R. Alzheimer's disease diagnosis in individual subjects using structural MR images: validation studies. Neuroimage 2008, 39:1186-1197.
70. Wadghiri Y.Z., Sigurdsson E.M., Sadowski M., Elliott J.I., Li Y., Scholtzova H., Tang C.Y., Aguinaldo G., Pappolla M., Duff K., Wisniewski T., Turnbull D.H. Detection of Alzheimer's amyloid in transgenic mice using magnetic resonance microimaging. Magn. Reson. Med. 2003, 50:293-302.
71. Wadghiri Y.Z., Li J., Wang J., Hoang D.M., Sun Y., Xu H., Tsui W., Li Y., Boutajangout A., Wang A., de Leon M., Wisniewski T. Detection of amyloid plaques targeted by bifunctional USPIO in Alzheimer's disease transgenic mice using magnetic resonance microimaging. PLoS One 2013, 8:e57097.
72. Wengenack T.M., Reyes D.A., Curran G.L., Borowski B.J., Lin J., Preboske G.M., Holasek S.S., Gilles E.J., Chamberlain R., Marjanska M., Jack C.R., Garwood M., Poduslo J.F. Regional differences in MRI detection of amyloid plaques in AD transgenic mouse brain. Neuroimage 2011, 54:113-122.
73. Wisniewski H.M., Bancher C., Barcikowska M., Wen G.Y., Currie J. Spectrum of morphological appearance of amyloid deposits in Alzheimer's disease. Acta Neuropathol. 1989, 78:337-347.
74. Wolff S.D., Balaban R.S. Magnetization transfer contrast (Mtc) and tissue water proton relaxation in vivo. Magn. Reson. Med. 1989, 10:135-144.
75. Wolff S.D., Balaban R.S. Magnetization-transfer imaging - practical aspects and clinical-applications. Radiology 1994, 192:593-599.
76. Yang J., Wadghiri Y.Z., Hoang D.M., Tsui W., Sun Y., Chung E., Li Y., Wang A., de Leon M., Wisniewski T. Detection of amyloid plaques targeted by USPIO-Abeta1-42 in Alzheimer's disease transgenic mice using magnetic resonance microimaging. Neuroimage 2011, 55:1600-1609.