Context-dependent perturbation of neural systems in transgenic mice expressing a cytosolic prion protein

NeuroImage

Volumn 49, Issue 3, 2010, Pages 2607-2617

  Faas, Henryk ^a   Jackson, Walker S ^c   Borkowski, Andrew W ^c   Wang, Xinhe ^d   Ma, Jiyan ^d   Lindquist, Susan ^c   Jasanoff, Alan ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

Magnetic resonance imaging (MRI); Manganese; Neural activity mapping; Neurodegenerative disease; Prion protein (PrP); Transgenic mouse model

Indexed keywords

MANGANESE; PRION PROTEIN; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN SIZE; CEREBELLUM ATROPHY; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE MAPPING; HIPPOCAMPUS; MOUSE; MOUSE MUTANT; NEOCORTEX; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TRANSGENIC MOUSE;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CYTOPLASM; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENES, IMMEDIATE-EARLY; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MICE; MICE, TRANSGENIC; PRION DISEASES; PRIONS;

EID: 72149088444     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.10.009     Document Type: Article

References (51)

1. Aguzzi A., and Polymenidou M. Mammalian prion biology: one century of evolving concepts. Cell 116 (2004) 313-327
2. Anderson S.A., and Frank J.A. MRI of mouse models of neurological disorders. NMR Biomed. 20 (2007) 200-215
3. Angenstein F., Niessen H.G., Goldschmidt J., Lison H., Altrock W.D., Gundelfinger E.D., and Scheich H. Manganese-enhanced MRI reveals structural and functional changes in the cortex of Bassoon mutant mice. Cereb. Cortex 17 (2007) 28-36
4. Aoki I., Wu Y.J., Silva A.C., Lynch R.M., and Koretsky A.P. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 22 (2004) 1046-1059
5. Borchelt D.R., Davis J., Fischer M., Lee M.K., Slunt H.H., Ratovitsky T., Regard J., Copeland N.G., Jenkins N.A., Sisodia S.S., and Price D.L. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet. Anal. 13 (1996) 159-163
6. Bueler H., Fischer M., Lang Y., Bluethmann H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., and Weissmann C. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356 (1992) 577-582
7. Carbon M., Ghilardi M.F., Argyelan M., Dhawan V., Bressman S.B., and Eidelberg D. Increased cerebellar activation during sequence learning in DYT1 carriers: an equiperformance study. Brain 131 (2008) 146-154
8. Castellani R.J., Zhu X., Lee H.G., Moreira P.I., Perry G., and Smith M.A. Neuropathology and treatment of Alzheimer disease: did we lose the forest for the trees?. Expert Rev. Neurother. 7 (2007) 473-485
9. Chiesa R., Piccardo P., Ghetti B., and Harris D.A. Neurological illness in transgenic mice expressing a prion protein with an insertional mutation. Neuron 21 (1998) 1339-1351
10. Chiti Z., Knutsen O.M., Betmouni S., and Greene J.R. An integrated, temporal study of the behavioural, electrophysiological and neuropathological consequences of murine prion disease. Neurobiol. Dis. 22 (2006) 363-373
11. Clayton D.F. The genomic action potential. Neurobiol. Learn. Mem. 74 (2000) 185-216
12. Cunningham C., Deacon R.M., Chan K., Boche D., Rawlins J.N., and Perry V.H. Neuropathologically distinct prion strains give rise to similar temporal profiles of behavioral deficits. Neurobiol. Dis. 18 (2005) 258-269
13. Cunningham C., Deacon R., Wells H., Boche D., Waters S., Diniz C.P., Scott H., Rawlins J.N., and Perry V.H. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur. J. Neurosci. 17 (2003) 2147-2155
14. Dogdas B., Shattuck D.W., and Leahy R.M. Segmentation of skull and scalp in 3-D human MRI using mathematical morphology. Hum. Brain Mapp. 26 (2005) 273-285
15. Engler H., Lundberg P.O., Ekbom K., Nennesmo I., Nilsson A., Bergstrom M., Tsukada H., Hartvig P., and Langstrom B. Multitracer study with positron emission tomography in Creutzfeldt-Jakob disease. Eur. J. Nucl. Med. Mol. Imaging 30 (2003) 85-95
16. Fioriti L., Dossena S., Stewart L.R., Stewart R.S., Harris D.A., Forloni G., and Chiesa R. Cytosolic prion protein (PrP) is not toxic in N2a cells and primary neurons expressing pathogenic PrP mutations. J. Biol. Chem. 280 (2005) 11320-11328
17. Fischer M., Rulicke T., Raeber A., Sailer A., Moser M., Oesch B., Brandner S., Aguzzi A., and Weissmann C. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15 (1996) 1255-1264
18. Gambetti P., Parchi P., Petersen R.B., Chen S.G., and Lugaresi E. Fatal familial insomnia and familial Creutzfeldt-Jakob disease: clinical, pathological and molecular features. Brain Pathol. 5 (1995) 43-51
19. Gambetti P., Kong Q., Zou W., Parchi P., and Chen S.G. Sporadic and familial CJD: classification and characterisation. Br. Med. Bull. 66 (2003) 213-239
20. Henkel K., Zerr I., Hertel A., Gratz K.F., Schroter A., Tschampa H.J., Bihl H., Bull U., Grunwald F., Drzezga A., Spitz J., and Poser S. Positron emission tomography with [(18)F]FDG in the diagnosis of Creutzfeldt-Jakob disease (CJD). J. Neurol. 249 (2002) 699-705
21. Hetz C., Russelakis-Carneiro M., Maundrell K., Castilla J., and Soto C. Caspase-12 and endoplasmic reticulum stress mediate neurotoxicity of pathological prion protein. EMBO J. 22 (2003) 5435-5445
22. Hetz C., Castilla J., and Soto C. Perturbation of endoplasmic reticulum homeostasis facilitates prion replication. J. Biol. Chem. 282 (2007) 12725-12733
23. Hockly E., Cordery P.M., Woodman B., Mahal A., van Dellen A., Blakemore C., Lewis C.M., Hannan A.J., and Bates G.P. Environmental enrichment slows disease progression in R6/2 Huntington's disease mice. Ann. Neurol. 51 (2002) 235-242
24. Hsiao K.K., Scott M., Foster D., Groth D.F., DeArmond S.J., and Prusiner S.B. Spontaneous neurodegeneration in transgenic mice with mutant prion protein. Science 250 (1990) 1587-1590
25. Jefferys J.G., Empson R.M., Whittington M.A., and Prusiner S.B. Scrapie infection of transgenic mice leads to network and intrinsic dysfunction of cortical and hippocampal neurones. Neurobiol. Dis. 1 (1994) 25-30
26. Jeffrey M., Halliday W.G., Bell J., Johnston A.R., MacLeod N.K., Ingham C., Sayers A.R., Brown D.A., and Fraser J.R. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol. Appl. Neurobiol. 26 (2000) 41-54
27. Jenkinson M., Bannister P., Brady M., and Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17 (2002) 825-841
28. Kahle P.J. alpha-Synucleinopathy models and human neuropathology: similarities and differences. Acta Neuropathol. 115 (2008) 87-95
29. Kang S.W., Rane N.S., Kim S.J., Garrison J.L., Taunton J., and Hegde R.S. Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell 127 (2006) 999-1013
30. Lasmezas C.I., Deslys J.P., Robain O., Jaegly A., Beringue V., Peyrin J.M., Fournier J.G., Hauw J.J., Rossier J., and Dormont D. Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275 (1997) 402-405
31. Levine M.S., Cepeda C., Hickey M.A., Fleming S.M., and Chesselet M.F. Genetic mouse models of Huntington's and Parkinson's diseases: illuminating but imperfect. Trends Neurosci. 27 (2004) 691-697
32. Lin Y.J., and Koretsky A.P. Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn. Reson. Med. 38 (1997) 378-388
33. Ma J., Wollmann R., and Lindquist S. Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 298 (2002) 1781-1785
34. Mentis M.J., Dhawan V., Nakamura T., Ghilardi M.F., Feigin A., Edwards C., Ghez C., and Eidelberg D. Enhancement of brain activation during trial-and-error sequence learning in early PD. Neurology 60 (2003) 612-619
35. Orr H.T., and Zoghbi H.Y. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30 (2007) 575-621
36. Orsi A., Fioriti L., Chiesa R., and Sitia R. Conditions of endoplasmic reticulum stress favor the accumulation of cytosolic prion protein. J. Biol. Chem. 281 (2006) 30431-30438
37. Palop J.J., Chin J., and Mucke L. A network dysfunction perspective on neurodegenerative diseases. Nature 443 (2006) 768-773
38. Pautler R.G., Silva A.C., and Koretsky A.P. In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 40 (1998) 740-748
39. Paxinos G., and Franklin K. The Mouse Brain in Stereotaxic Coordinates. 2nd Edition (2000), Academic Press, New York
40. Prusiner S.B. Novel proteinaceous infectious particles cause scrapie. Science 216 (1982) 136-144
41. Rane N.S., Yonkovich J.L., and Hegde R.S. Protection from cytosolic prion protein toxicity by modulation of protein translocation. EMBO J. 23 (2004) 4550-4559
42. Rane N.S., Kang S.W., Chakrabarti O., Feigenbaum L., and Hegde R.S. Reduced translocation of nascent prion protein during ER stress contributes to neurodegeneration. Dev. Cell 15 (2008) 359-370
43. Roucou X., Guo Q., Zhang Y., Goodyer C.G., and LeBlanc A.C. Cytosolic prion protein is not toxic and protects against Bax-mediated cell death in human primary neurons. J. Biol. Chem. 278 (2003) 40877-40881
44. Silva A.C., Lee J.H., Aoki I., and Koretsky A.P. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 17 (2004) 532-543
45. Steele A.D., Jackson W.S., King O.D., and Lindquist S. The power of automated high-resolution behavior analysis revealed by its application to mouse models of Huntington's and prion diseases. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 1983-1988
46. Wang X., Wang F., Arterburn L., Wollmann R., and Ma J. The interaction between cytoplasmic prion protein and the hydrophobic lipid core of membrane correlates with neurotoxicity. J. Biol. Chem. 281 (2006) 13559-13565
47. Wang X., Bowers S.L., Wang F., Pu X.A., Nelson R.J., and Ma J. Cytoplasmic prion protein induces forebrain neurotoxicity. Biochim. Biophys. Acta 1792 (2009) 555-563
48. Wirtshafter D. Cholinergic involvement in the cortical and hippocampal Fos expression induced in the rat by placement in a novel environment. Brain Res. 1051 (2005) 57-65
49. Woods R.P., Grafton S.T., Holmes C.J., Cherry S.R., and Mazziotta J.C. Automated image registration: I. General methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. 22 (1998) 139-152
50. Yu J., and Eidelberg E. Recovery of locomotor function in cats after localized cerebellar lesions. Brain Res. 273 (1983) 121-131
51. Yu H., Sternad D., Corcos D.M., and Vaillancourt D.E. Role of hyperactive cerebellum and motor cortex in Parkinson's disease. Neuroimage 35 (2007) 222-233