In vivo MRI identifies cholinergic circuitry deficits in a Down syndrome model

Neurobiology of Aging

Volumn 30, Issue 9, 2009, Pages 1453-1465

  Chen, Yuanxin ^a   Dyakin, Victor V ^a   Branch, Craig A ^a,b   Ardekani, Babak ^a   Yang, Dunsheng ^a   Guilfoyle, David N ^a   Peterson, Jesse ^d   Peterhoff, Corrinne ^a   Ginsberg, Stephen D ^a,c   Cataldo, Anne M ^d,e   Nixon, Ralph A ^a,c  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MCLEAN HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Acetylcholine; Alzheimer's disease; Basal forebrain; Functional imaging; Medial septal nucleus; Ts1Cje trisomic mice; Ts65Dn trisomic mice

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE KINASE A;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRAIN MAPPING; BRAIN REGION; CELL SUBPOPULATION; CHOLINERGIC ACTIVITY; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CINGULATE GYRUS; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC VALUE; DIPLOIDY; DISOMY; DOWN SYNDROME; ENZYME ACTIVITY; FOREBRAIN; HIPPOCAMPUS; IN VIVO STUDY; MALE; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARASYMPATHETIC INNERVATION; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RELAXATION TIME; SEPTUM NUCLEUS; TRISOMY;

ACETYLCHOLINE; ANIMALS; CEREBRAL CORTEX; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; EFFERENT PATHWAYS; GENE DOSAGE; HIPPOCAMPUS; MAGNETIC RESONANCE IMAGING; MICE; PREDICTIVE VALUE OF TESTS; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; SENSITIVITY AND SPECIFICITY; SEPTAL NUCLEI; SYNAPSES; TRISOMY;

EID: 67650590960     PISSN: 01974580     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2007.11.026     Document Type: Article

References (80)

1. Antonarakis S.E., Lyle R., Chrast R., and Scott H.S. Differential gene expression studies to explore the molecular pathophysiology of Down syndrome. Brain Res. Brain Res. Rev. 36 2-3 (2001) 265-274
2. Antonarakis S.E., Lyle R., Dermitzakis E.T., Reymond A., and Deutsch S. Chromosome 21 and Down syndrome: from genomics to pathophysiology. Nat. Rev. Genet. 5 10 (2004) 725-738
3. Apelt J., Kumar A., and Schliebs R. Impairment of cholinergic neurotransmission in adult and aged transgenic Tg2576 mouse brain expressing the Swedish mutation of human beta-amyloid precursor protein. Brain Res. 953 1-2 (2002) 17-30
4. Ardekani B.A., Guckemus S., Bachman A., Hoptman M.J., Wojtaszek M., and Nierenberg J. Quantitative comparison of algorithms for inter-subject registration of 3D volumetric brain MRI scans. J. Neurosci. Methods 142 1 (2005) 67-76
5. Bakshi R., Benedict R.H., Bermel R.A., Caruthers S.D., Puli S.R., Tjoa C.W., Fabiano A.J., and Jacobs L. T2 hypointensity in the deep gray matter of patients with multiple sclerosis: a quantitative magnetic resonance imaging study. Arch. Neurol. 59 1 (2002) 62-68
6. Bakshi R., Dmochowski J., Shaikh Z.A., and Jacobs L. Gray matter T2 hypointensity is related to plaques and atrophy in the brains of multiple sclerosis patients. J. Neurol. Sci. 185 1 (2001) 19-26
7. Bartus R.T. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp. Neurol. 163 2 (2000) 495-529
8. Baxter L.L., Moran T.H., Richtsmeier J.T., Troncoso J., and Reeves R.H. Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse. Hum. Mol. Genet. 9 2 (2000) 195-202
9. Baxter M.G., and Chiba A.A. Cognitive functions of the basal forebrain. Curr. Opin. Neurobiol. 9 2 (1999) 178-183
10. Belichenko P.V., Masliah E., Kleschevnikov A.M., Villar A.J., Epstein C.J., Salehi A., and Mobley W.C. Synaptic structural abnormalities in the Ts65Dn mouse model of Down syndrome. J. Comp. Neurol. 480 3 (2004) 281-298
11. Bierer L.M., Haroutunian V., Gabriel S., Knott P.J., Carlin L.S., Purohit D.P., Perl D.P., Schmeidler J., Kanof P., and Davis K.L. Neurochemical correlates of dementia severity in Alzheimer's disease: relative importance of the cholinergic deficits. J. Neurochem. 64 2 (1995) 749-760
12. Bigl V., Woolf N.J., and Butcher L.L. Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res. Bull. 8 6 (1982) 727-749
13. Busciglio J., Pelsman A., Wong C., Pigino G., Yuan M., Mori H., and Yankner B.A. Altered metabolism of the amyloid beta precursor protein is associated with mitochondrial dysfunction in Down's syndrome. Neuron 33 5 (2002) 677-688
14. Capone G.T. Down syndrome: advances in molecular biology and the neurosciences. J. Dev. Behav. Pediatr. 22 1 (2001) 40-59
15. Cataldo A.M., Hamilton D.J., Barnett J.L., Paskevich P.A., and Nixon R.A. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J. Neurosci. 16 (1996) 186-199
16. Cataldo A.M., Petanceska S., Peterhoff C.M., Terio N.B., Epstein C.J., Villar A., Carlson E.J., Staufenbiel M., and Nixon R.A. App gene dosage modulates endosomal abnormalities of Alzheimer's disease in a segmental trisomy 16 mouse model of Down syndrome. J. Neurosci. 23 17 (2003) 6788-6792
17. Contestabile A., Fila T., Bartesaghi R., and Ciani E. Choline acetyltransferase activity at different ages in brain of Ts65Dn mice, an animal model for Down's syndrome and related neurodegenerative diseases. J. Neurochem. 97 2 (2006) 515-526
18. Cooper J.D., Salehi A., Delcroix J.D., Howe C.L., Belichenko P.V., Chua-Couzens J., Kilbridge J.F., Carlson E.J., Epstein C.J., and Mobley W.C. Failed retrograde transport of NGF in a mouse model of Down's syndrome: reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc. Natl. Acad. Sci. U.S.A. 98 18 (2001) 10439-10444
19. Costa A.C., and Grybko M.J. Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: a model of Down syndrome. Neurosci. Lett. 382 3 (2005) 317-322
20. Davies P., and Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 2 8000 (1976) 1403
21. Davisson M.T., Schmidt C., and Akeson E.C. Segmental trisomy of murine chromosome 16: a new model system for studying Down syndrome. Prog. Clin. Biol. Res. 360 (1990) 263-280
22. Davisson M.T., Schmidt C., Reeves R.H., Irving N.G., Akeson E.C., Harris B.S., and Bronson R.T. Segmental trisomy as a mouse model for Down syndrome. Prog. Clin. Biol. Res. 384 (1993) 117-133
23. Dijkhuizen R.M., Ren J., Mandeville J.B., Wu O., Ozdag F.M., Moskowitz M.A., Rosen B.R., and Finklestein S.P. Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc. Natl. Acad. Sci. U.S.A. 98 22 (2001) 12766-12771
24. Eckenstein F.P., Baughman R.W., and Quinn J. An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience 25 2 (1988) 457-474
25. Falangola M.F., Dyakin V.V., Lee S.P., Bogart A., Babb J.S., Duff K., Nixon R., and Helpern J.A. Quantitative MRI reveals aging-associated T2 changes in mouse models of Alzheimer's disease. NMR Biomed. 20 3 (2007) 343-351
26. Ferrer I., and Gullotta F. Down's syndrome and Alzheimer's disease: dendritic spine counts in the hippocampus. Acta Neuropathol. (Berl) 79 6 (1990) 680-685
27. Ginsberg S.D., and Martin L.J. Ultrastructural analysis of the progression of neurodegeneration in the septum following fimbria-fornix transection. Neuroscience 86 (1998) 1259-1272
28. Ginsberg S.D., and Martin L.J. Axonal transection in adult rat brain induces transsynaptic apoptosis and persistent atrophy of target neurons. J. Neurotrauma 19 (2002) 99-109
29. Ginsberg S.D., Rothstein J.D., Price D.L., and Martin L.J. Fimbria-fornix transections selectively down-regulate subtypes of glutamate transporter and glutamate receptor proteins in septum and hippocampus. J. Neurochem. 67 (1996) 1208-1216
30. Ginsberg S.D., Che S., Wuu J., Counts S.E., and Mufson E.J. Down regulation of trk but not p75 gene expression in single cholinergic basal forebrain neurons mark the progression of Alzheimer's disease. J. Neurochem. 97 2 (2006) 475-487
31. Granholm A.C., Sanders L.A., and Crnic L.S. Loss of cholinergic phenotype in basal forebrain coincides with cognitive decline in a mouse model of Down's syndrome. Exp. Neurol. 161 2 (2000) 647-663
32. Guilfoyle D.N., Dyakin V.V., O'Shea J., Pell G.S., and Helpern J.A. Quantitative measurements of proton spin-lattice (T1) and spin-spin (T2) relaxation times in the mouse brain at 7.0 T. Magn. Reson. Med. 49 3 (2003) 576-580
33. Gyure K.A., Durham R., Stewart W.F., Smialek J.E., and Troncoso J.C. Intraneuronal abeta-amyloid precedes development of amyloid plaques in Down syndrome. Arch. Pathol. Lab. Med. 125 4 (2001) 489-492
34. Haacke E.M., Cheng N.Y., House M.J., Liu Q., Neelavalli J., Ogg R.J., Khan A., Ayaz M., Kirsch W., and Obenaus A. Imaging iron stores in the brain using magnetic resonance imaging. Magn. Reson. Imaging 23 1 (2005) 1-25
35. Harmon K.M., and Wellman C.L. Differential effects of cholinergic lesions on dendritic spines in frontal cortex of young adult and aging rats. Brain Res. 992 1 (2003) 60-68
36. Hebert L.E., Beckett L.A., Scherr P.A., and Evans D.A. Annual incidence of Alzheimer disease in the United States projected to the years 2000 through 2050. Alzheimer Dis. Assoc. Disord. 15 4 (2001) 169-173
37. Hefti F. Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J. Neurosci. 6 (1986) 2155-2162
38. Helpern J.A., Jensen J., Lee S.P., and Falangola M.F. Quantitative MRI assessment of Alzheimer's disease. J. Mol. Neurosci. 24 1 (2004) 45-48
39. Hodgkins P.S., Prasher V., Farrar G., Armstrong R., Sturman S., Corbett J., and Blair J.A. Reduced transferrin binding in Down syndrome: a route to senile plaque formation and dementia. Neuroreport 5 1 (1993) 21-24
40. Holtzman D.M., Li Y.W., DeArmond S.J., McKinley M.P., Gage F.H., Epstein C.J., and Mobley W.C. Mouse model of neurodegeneration: atrophy of basal forebrain cholinergic neurons in trisomy 16 transplants. Proc. Natl. Acad. Sci. U.S.A. 89 4 (1992) 1383-1387
41. Holtzman D.M., Santucci D., Kilbridge J., Chua-Couzens J., Fontana D.J., Daniels S.E., Johnson R.M., Chen K., Sun Y., Carlson E., Alleva E., Epstein C.J., and Mobley W.C. Developmental abnormalities and age-related neurodegeneration in a mouse model of Down syndrome. Proc. Natl. Acad. Sci. U.S.A. 93 23 (1996) 13333-13338
42. Howe C.L., and Mobley W.C. Signaling endosome hypothesis: a cellular mechanism for long distance communication. J. Neurobiol. 58 2 (2004) 207-216
43. Hunter C.L., Bimonte-Nelson H.A., Nelson M., Eckman C.B., and Granholm A.C. Behavioral and neurobiological markers of Alzheimer's disease in Ts65Dn mice: effects of estrogen. Neurobiol. Aging 25 7 (2004) 873-884
44. Iwatsubo T., Mann D.M.A., Odaka A., Suzuki N., and Ihara Y. Amyloid-ß protein (Aß) deposition: Aß42(43) precedes Aß40 in Down's syndrome. Ann. Neurol. 37 (1995) 294-299
45. Kleschevnikov A.M., Belichenko P.V., Villar A.J., Epstein C.J., Malenka R.C., and Mobley W.C. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J. Neurosci. 24 37 (2004) 8153-8160
46. Köhler C., Chan-Palay V., and Wu J.-Y. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat. Embryol. 169 (1984) 41-44
47. Kromer L.F. Nerve growth factor treatment after brain injury prevents neuronal death. Science 235 (1987) 214-216
48. Mattson M.P. Metal-catalyzed disruption of membrane protein and lipid signaling in the pathogenesis of neurodegenerative disorders. Ann. N.Y. Acad. Sci. 1012 (2004) 37-50
49. Meshorer E., Biton I.E., Ben-Shaul Y., Ben-Ari S., Assaf Y., Soreq H., and Cohen Y. Chronic cholinergic imbalances promote brain diffusion and transport abnormalities. FASEB J. 19 8 (2005) 910-922
50. Mesulam M.M., Mufson E.J., Levey A.I., and Wainer B.H. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp. Neurol. 214 2 (1983) 170-197
51. Mesulam M.M., Mufson E.J., Wainer B.H., and Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10 4 (1983) 1185-1201
52. Mufson E.J., Bothwell M., Hersh L.B., and Kordower J.H. Nerve growth factor receptor immunoreactive profiles in the normal, aged human basal forebrain: colocalization with cholinergic neurons. J. Comp. Neurol. 285 2 (1989) 196-217
53. Mufson E.J., Bothwell M., and Kordower J.H. Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: a quantitative analysis across subregions of the basal forebrain. Exp. Neurol. 105 3 (1989) 221-232
54. Mufson E.J., Ginsberg S.D., Ikonomovic M.D., and DeKosky S.T. Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J. Chem. Neuroanat. 26 4 (2003) 233-242
55. Mufson E.J., Counts S.E., Che S., and Ginsberg S.D. Neuronal gene expression profiling: uncovering the molecular biology of neurodegenerative disease. Prog. Brain Res. 158 2 (2006) 197-222
56. Naumann T., Linke R., and Frotscher M. Fine structure of rat septohippocampal neurons. I. Identification of septohippocampal projections neurons by retrograde tracing combined with electron microscopic immunocytochemistry and intracellular staining. J. Comp. Neurol. 325 (1992) 207-218
57. Nixon R.A. Endosome function and dysfunction in Alzheimer's disease and other neurodegenerative diseases. Neurobiol. Aging 26 3 (2005) 373-382
58. Nixon R.A., and Cataldo A.M. Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J. Alzheimers Dis. 9 3 Suppl. (2006) 277-289
59. Olson L.E., Roper R.J., Baxter L.L., Carlson E.J., Epstein C.J., and Reeves R.H. Down syndrome mouse models Ts65Dn, Ts1Cje, and Ms1Cje/Ts65Dn exhibit variable severity of cerebellar phenotypes. Dev. Dyn. 230 3 (2004) 581-589
60. Paxinos G., and Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates. Second ed. (2001), Academic Press, San Diego
61. Prasher V.P., Farrer M.J., Kessling A.M., Fisher E.M., West R.J., Barber P.C., and Butler A.C. Molecular mapping of Alzheimer-type dementia in Down's syndrome. Ann. Neurol. 43 3 (1998) 380-383
62. Prasher V.P., Gosling P., and Blair J. Role of iron in Alzheimer-type dementia in Down syndrome. Int. J. Geriatr. Psychiatry 13 11 (1998) 818-819
63. Reeves R.H., Irving N.G., Moran T.H., Wohn A., Kitt C., Sisodia S.S., Schmidt C., Bronson R.T., and Davisson M.T. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat. Genet. 11 2 (1995) 177-184
64. Robertson R.T., Gallardo K.A., Claytor K.J., Ha D.H., Ku K.H., Yu B.P., Lauterborn J.C., Wiley R.G., Yu J., Gall C.M., and Leslie F.M. Neonatal treatment with 192 IgG-saporin produces long-term forebrain cholinergic deficits and reduces dendritic branching and spine density of neocortical pyramidal neurons. Cereb. Cortex 8 2 (1998) 142-155
65. Rovelet-Lecrux A., Hannequin D., Raux G., Meur N.L., Laquerriere A., Vital A., Dumanchin C., Feuillette S., Brice A., Vercelletto M., Dubas F., Frebourg T., and Campion D. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 38 1 (2006) 24-26
66. Rovira A., Alonso J., Cucurella G., Nos C., Tintore M., Pedraza S., Rio J., and Montalban X. Evolution of multiple sclerosis lesions on serial contrast-enhanced T1-weighted and magnetization-transfer MR images. AJNR Am. J. Neuroradiol. 20 10 (1999) 1939-1945
67. Sago H., Carlson E.J., Smith D.J., Kilbridge J., Rubin E.M., Mobley W.C., Epstein C.J., and Huang T.-T. Ts1Cje, a partial trisomy 16 mouse model for Down syndrome, exhibits learning and behavioral abnormalities. PNAS 95 11 (1998) 6256-6261
68. Salehi A., Delcroix J.D., Belichenko P.V., Zhan K., Wu C., Valletta J.S., Takimoto-Kimura R., Kleschevnikov A.M., Sambamurti K., Chung P.P., Xia W., Villar A., Campbell W.A., Kulnane L.S., Nixon R.A., Lamb B.T., Epstein C.J., Stokin G.B., Goldstein L.S., and Mobley W.C. Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 51 1 (2006) 29-42
69. Seo H., and Isacson O. Abnormal APP, cholinergic and cognitive function in Ts65Dn Down's model mice. Exp. Neurol. 193 2 (2005) 469-480
70. Siarey R.J., Stoll J., Rapoport S.I., and Galdzicki Z. Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology 36 11-12 (1997) 1549-1554
71. Siarey R.J., Carlson E.J., Epstein C.J., Balbo A., Rapoport S.I., and Galdzicki Z. Increased synaptic depression in the Ts65Dn mouse, a model for mental retardation in Down syndrome. Neuropharmacology 38 12 (1999) 1917-1920
72. Sofroniew M.V., Galletly N.P., Isacson O., and Svendsen C.N. Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science 247 4940 (1990) 338-342
73. Suetsugu M., and Mehraein P. Spine distribution along the apical dendrites of the pyramidal neurons in Down's syndrome. A quantitative Golgi study. Acta Neuropathol. (Berl) 50 3 (1980) 207-210
74. Swanson L.W., and Cowan W.M. The connections of the septal region in the rat. J. Comp. Neurol. 186 4 (1979) 621-656
75. Tuszynski, M.H., Thal, L., Pay, M., Salmon, D.P., U, H.-S., Bakay, R., Patel, P., Blesch, A., Vahlsing, H.L., Ho, G., Tong, G., Potkin, S.G., Fallon, J., Hansen, L., Mufson, E.J., Kordower, J.H., Gall, C., Conner, J.M., 2005. A Phase I clinical trial of nerve growth factor gene therapy for Alzheimer's disease. Nat. Med. 11 (5), 551-555.
76. Villar A.J., Belichenko P.V., Gillespie A.M., Kozy H.M., Mobley W.C., and Epstein C.J. Identification and characterization of a new Down syndrome model, Ts[Rb(12.1716)]2Cje, resulting from a spontaneous Robertsonian fusion between T(171)65Dn and mouse chromosome 12. Mamm. Genome 16 2 (2005) 79-90
77. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., and Delong M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215 4537 (1982) 1237-1239
78. Wisniewski K.E., Dalton A.J., Crapper McLachlan D.R., Wen G.Y., and Wisniewski H.M. Alzheimer's disease in Down's syndrome: clinicopathologic studies. Neurology 35 7 (1985) 957-961
79. Woolf N.J. Cholinoceptive cells in rat cerebral cortex: somatodendritic immunoreactivity for muscarinic receptor and cytoskeletal proteins. J. Chem. Neuroanat. 6 6 (1993) 375-390
80. Zheng F., and Khanna S. Selective destruction of medial septal cholinergic neurons attenuates pyramidal cell suppression, but not excitation in dorsal hippocampus field CA1 induced by subcutaneous injection of formalin. Neuroscience 103 4 (2001) 985-998