Cholinergic changes in the APP23 transgenic mouse model of cerebral amyloidosis

Journal of Neuroscience

Volumn 22, Issue 8, 2002, Pages 3234-3243

  Boncristiano, Sonia ^a   Calhoun, Michael E ^a,c   Kelly, Peter H ^b   Pfeifer, Michelle ^a   Bondolfi, Luca ^a   Stalder, Martina ^a   Phinney, Amie L ^a,d   Abramowski, Dorothee ^b   Sturchler Pierrat, Christine ^b   Enz, Albert ^b   Sommer, Bernd ^b   Staufenbiel, Matthias ^b   Jucker, Mathias ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NOVARTIS PHARMA AG   (Switzerland)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

ACHE; Aging; Alzheimer's disease; Amyloid; APP; Basal forebrain; CHAT; Cholinergic system; Hippocampus; Lesion; Mouse; Neocortex; Neurodegeneration; Nucleus basalis of Meynert; Stereology

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CHOLINE ACETYLTRANSFERASE;

ADOLESCENT; AGED; AMYLOID NEUROPATHY; AMYLOIDOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEGENERATION; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE MODEL; DISEASE SEVERITY; ENZYME ACTIVITY; FOREBRAIN; MOUSE; NEOCORTEX; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; STEREOMETRY; TRANSGENIC MOUSE; WILD TYPE;

EID: 0037092417     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-08-03234.2002     Document Type: Article

References (87)

1. Andra K, Abramowski D, Duke M, Probst A, Wiederhold KH, Burki K, Goedert M, Sommer B, Staufenbiel M (1996) Expression of APP in transgenic mice: A comparison of neuron-specific promoters. Neurobiol Aging 17:183-190.
2. Auld DS, Kar S, Quirion R (1998) Beta-amyloid peptides as direct cholinergic neuromodulators: A missing link? Trends Neurosci 21:43-49.
3. Bartus RT, Dean RLD, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414.
4. Beach TG, Kuo YM, Spiegel K, Emmerling MR, Sue LI, Kokjohn K, Roher AE (2000a) The cholinergic deficit coincides with Abeta deposition at the earliest histopathologic stages of Alzheimer disease. J Neuropathol Exp Neurol 59:308-313.
5. Beach TG, Potter PE, Kuo YM, Emmerling MR, Durham RA, Webster SD, Walker DG, Sue LI, Scott S, Layne KJ, Roher AE (2000b) Cholinergic deafferentation of the rabbit cortex: A new animal model of Abeta deposition. Neurosci Lett 283:9-12.
6. Benzing WC, Mufson EJ, Armstrong DM (1993) Immunocytochemical distribution of peptidergic and cholinergic fibers in the human amygdala: Their depletion in Alzheimer's disease and morphologic alteration in non-demented elderly with numerous senile plaques. Brain Res 625:125-138.
7. Bierer LM, Haroutunian V, Gabriel S, Knott PJ, Carlin LS, Purohit DP, Perl DP, Schmeidler J, Kanof P, Davis KL (1995) Neurochemical correlates of dementia severity in Alzheimer's disease: Relative importance of the cholinergic deficits. J Neurochem 64:749-760.
8. Bondolfi L, Calhoun M, Ermini F, Kuhn HG, Wiederhold KH, Walker L, Staufenbiel M, Jucker M (2002) Amyloid-associated neuron loss and gliogenesis in the neocortex of amyloid precursor protein transgenic mice. J Neurosci 22:515-522.
9. Bronfman FC, Moechars D, Van Leuven F (2000) Acetylcholinesterase-positive fiber deafferentation and cell shrinkage in the septohippocampal pathway of aged amyloid precursor protein london mutant transgenic mice. Neurobiol Dis 7:152-168.
10. Buxbaum JD, Oishi M, Chen HI, Pinkas-Kramarski R, Jaffe EA, Gandy SE, Greengard P (1992) Cholinergic agonists and interleukin 1 regulate processing and secretion of the Alzheimer beta/A4 amyloid protein precursor. Proc Natl Acad Sci USA 89:10075-10078.
11. Calhoun ME, Kurth D, Phinney AL, Long JM, Hengemihle J, Mouton PR, Ingram DK, Jucker M (1998a) Hippocampal neuron and synaptophysin-positive bouton number in aging C57BL/6 mice. Neurobiol Aging 19:599-606.
12. Calhoun ME, Wiederhold KH, Abramowski D, Phinney AL, Probst A, Sturchler-Pierrat C, Staufenbiel M, Sommer B, Jucker M (1998b) Neuron loss in APP transgenic mice. Nature 395:755-756.
13. Calhoun ME, Burgermeister P, Phinney AL, Stalder M, Tolnay M, Wiederhold KH, Abramowski D, Sturchler-Pierrat C, Sommer B, Staufenbiel M, Jucker M (1999) Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid. Proc Natl Acad Sci U S A 96:14088-14093.
14. Citron M, Ottersdorf T, Haass C, McConlogue L, Hung AY, Seubert P, Vigo-Pelfrey C, Lieberburg I, Selkoe DJ (1992) Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360:672-674.
15. Collerton D (1986) Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience 19:1-28.
16. Coyle JT, Price DL, DeLong MR (1983) Alzheimer's disease: A disorder of cortical cholinergic innervation. Science 219:1184-1190.
17. Cullen KM, Halliday GM (1998) Neurofibrillary degeneration and cell loss in the nucleus basalis in comparison to cortical Alzheimer pathology. Neurobiol Aging 19:297-306.
18. Cutler NR, Polinsky RJ, Sramek JJ, Enz A, Jhee SS, Mancione L, Hourani J, Zolnouni P (1998) Dose-dependent CSF acetylcholinesterase inhibition by SDZ ENA 713 in Alzheimer's disease. Acta Neurol Scand 97:244-250.
19. DeKosky ST, Harbaugh RE, Schmitt FA, Bakay RA, Chui HC, Knopman DS, Reeder TM, Shetter AG, Senter HJ, Markesbery WR (1992) Cortical biopsy in Alzheimer's disease: Diagnostic accuracy and neurochemical, neuropathological, and cognitive correlations. Intraventricular Bethanecol Study Group. Ann Neurol 32:625-632.
20. Ellman GL, Courtney KD, Andres VJ, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88-95.
21. Fonnum F (1975) A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407-409.
22. Franklin KBJ, Paxinos G (1997) The Mouse Brain Atlas in Stereotaxic Coordinates. San Diego, CA: Academic.
23. Frautschy SA, Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM (1998) Microglial response to amyloid plaques in APPsw transgene mice. Am J Pathol 152:307-317.
24. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373:523-527.
25. Gaykema RP, Luiten PG, Nyakas C, Traber J (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103-124.
26. Geula C, Mesulam MM, Saroff DM, Wu CK (1998) Relationship between plaques, tangles, and loss of cortical cholinergic fibers in Alzheimer disease. J Neuropathol Exp Neurol 57:63-75.
27. Goedert M (1993) Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci 16:460-465.
28. Gomez-Ramos P, Mufson EJ, Moran MA (1992) Ultrastructural localization of acetylcholinesterase in neurofibrillary tangles, neuropil threads and senile plaques in aged and Alzheimer's brain. Brain Res 569:229-237.
29. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379-394.
30. Haass C, Steiner H (2001) Protofibrils, the unifying toxic molecule of neurodegenerative disorders? Nat Neurosci 4:859-860.
31. Hardy J (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci 20:154-159.
32. Hedreen JC, Bacon SJ, Price DL (1985) A modified histochemical technique to visualize acetylcholinesterase-containing axons. J Histochem Cytochem 33:134-140.
33. Hernandez D, Sugaya K, Qu T, McGowan E, Duff K, McKinney M (2001) Survival and plasticity of basal forebrain cholinergic systems in mice transgenic for presenilin-1 and amyloid precursor protein mutant genes. NeuroReport 12:1377-1384.
34. Howard CV, Cruz-Orive LM, Yaegashi H (1992) Estimating neuron dendritic length in 3D from total vertical projections and from vertical slices. Acta Neurol Scand [Suppl] 137:14-19.
35. Hsiao K, Chapman P, Nilsen S, Eckrnan C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
36. Hung AY, Haass C, Nitsch RM, Qiu WQ, Citron M, Wurtman RJ, Growdon JH, Selkoe DJ (1993) Activation of protein kinase C inhibits cellular production of the amyloid beta-protein. J Biol Chem 268:22959-22962.
37. Inestrosa NC, Alvarez A, Perez CA, Moreno RD, Vicente M, Linker C, Casanueva OI, Soto C, Garrido J (1996) Acetylcholinesterase accelerates assembly of amyloid-beta-peptides into Alzheimer's fibrils: Possible role of the peripheral site of the enzyme. Neuron 16:881-891.
38. Jaffar S, Counts SE, Ma SY, Dadko E, Gordon MN, Morgan D, Mufson EJ (2001) Neuropathology of Mice Carrying Mutant APP(swe) and/or PS1(M146L) transgenes: Alterations in the p75(NTR) cholinergic basal forebrain septohippocampal pathway. Exp Neurol 170:227-243.
39. Jensen EB, Gundersen HLG (1993) The rotator. J Microsc 170:35-44.
40. Jope RS, Song L, Powers RE (1997) Cholinergic activation of phosphoinositide signaling is impaired in Alzheimer's disease brain. Neurobiol Aging 18:111-120.
41. Jucker M, D'Amato F, Mondadori C, Mohajeri H, Magyar J, Bartsch U, Schachner M (1996) Expression of the neural adhesion molecule L1 in the deafferented dentate gyrus. Neuroscience 75:703-715.
42. Jucker M, Calhoun M, Phinney A, Stalder M, Bondolfi L, Winkler D, Herzig M, Pfeifer M, Boncristiano S, Tolnay M, Probst A, Deller T, Abramowski D, Wiederhold K-H, Sturchler-Pierrat C, Sommer B, Staufenbiel M (2001) Pathogenesis and Mechanism of Cerebral Amyloidosis in APP Transgenic Mice. Neurodegenerative Disorders: Loss of Function Through Gain of Function (Beyreuther K, Christen Y, and Masters CL, eds), pp 87-95. Berlin: Springer.
43. Kelly PH, Moore KE (1978) Decrease of neocortical choline acetyltransferase after lesion of the globus pallidus in the rat. Exp Neurol 61:479-484.
44. Kelly PH, Hunziker D, Schlecht HP, Carver K, Abramowski D, Wiederhold KH, Sturchler-Pierrat C, Bondolfi L, Jucker M, Staufenbiel M, Sommer B (2002) Progressive Age-related Impairment of Cognitive Behavior in APP23 Transgenic Mice. Submitted.
45. Kitt CA, Hohmann C, Coyle JT, Price DL (1994) Cholinergic innervation of mouse forebrain structures. J Comp Neurol 341:117-129.
46. Klafki HW, Wiltfang J, Staufenbiel M (1996) Electrophoretic separation of betaA4 peptides (1-40) and (1-42). Anal Biochem 237:24-29.
47. Kuo YM, Kokjohn TA, Beach TG, Sue: LI, Brune D, Lopez JC, Kalback WM, Abramowski D, Sturchler-Pierrat C, Staufenbiel M, Roher AE (2001) Comparative analysis of amyloid-beta chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J Biol Chem 276:12991-12998.
48. Ladner CJ, Lee JM (1998) Pharmacological drug treatment of Alzheimer disease: The cholinergic hypothesis revisited. J Neuropathol Exp Neurol 57:719-731.
49. Liberini P, Pioro EP, Maysinger D, Cuello AC (1994) Neocortical infarction in subhuman primates leads to restricted morphological damage of the cholinergic neurons in the nucleus basalis of Meynert. Brain Res 648:1-8.
50. Lin L, Georgievska B, Mattsson A, Isacson O (1999) Cognitive changes and modified processing of amyloid precursor protein in the cortical and hippocampal system after cholinergic synapse loss and muscarinic receptor activation. Proc Natl Acad Sci USA 96:12108-12113.
51. Marsh D, Grassi J, Vigny M, Massoulie J (1984) An immunological study of rat acetylcholinesterase: Comparison with acetylcholinesterases from other vertebrates. J Neurochem 43:204-213.
52. Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D (1996) Comparison of neurodegenerative pathology in transgenic mice over-expressing V717F beta-amyloid precursor protein and Alzheimer's disease. J Neurosci 16:5795-5811.
53. McKinney M, Coyle JT, Hedreen JC (1983) Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 217:103-121.
54. Mesulam MM (1996) The systems-level organization of cholinergic innervation in the human cerebral cortex and its alterations in Alzheimer's disease. Prog Brain Res 109:285-297.
55. Mesulam M, Carson K, Price B, Geula C (1992) Cholinesterases in the amyloid angiopathy of Alzheimer's disease. Ann Neurol 31:565-569.
56. Moran MA, Mufson EJ, Gomez-Ramos P (1993) Colocalization of cholinesterases with beta amyloid protein in aged and Alzheimer's brains. Acta Neuropathol 85:362-369.
57. Mountjoy CQ, Rossor MN, Iversen LL, Roth M (1984) Correlation of cortical cholinergic and GABA deficits with quantitative neuropathological findings in senile dementia. Brain 107:507-518.
58. Nakagawa Y, Reed L, Nakamura M, McIntosh TK, Smith DH, Saatman KE, Raghupathi R, Clemens J, Saido TC, Lee VM, Trojanowski JQ (2000) Brain trauma in aged transgenic mice induces regression of established abeta deposits. Exp Neurol 163:244-252.
59. Nitsch RM, Slack BE, Wurtman RJ, Growdon JH (1992) Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258:304-307.
60. Pedersen WA, Kloczewiak MA, Blusztajn JK (1996) Amyloid beta-protein reduces acetylcholine synthesis in a cell line derived from cholinergic neurons of the basal forebrain. Proc Natl Acad Sci USA 93:8068-8071.
61. Perry EK, Blessed G, Tomlinson BE, Perry RH, Crow TJ, Cross AJ, Dockray GJ, Dimaline R, Arregui A (1981) Neurochemical activities in human temporal lobe related to aging and Alzheimer-type changes. Neurobiol Aging 2:251-256.
62. Perry EK, Johnson M, Kerwin JM, Piggott MA, Court JA, Shaw PJ, Ince PG, Brown A, Perry RH (1992) Convergent cholinergic activities in aging and Alzheimer's disease. Neurobiol Aging 13:393-400.
63. Pettit DL, Shao Z, Yakel JL (2001) Beta-amyloid(1-42) peptide directly modulates nicotinic receptors in the rat hippocampal slice. J Neurosci 21:RC120.
64. Phinney AL, Deller T, Stalder M, Calhoun ME, Frotscher M, Sommer B, Staufenbiel M, Jucker M (1999) Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J Neurosci 19:8552-8559.
65. Ransmayr G, Cerrera P, Hirsch EC, Berger W, Fischer W, Agid Y (1992) Alzheimer's disease: Is the decrease of the cholinergic innervation of the hippocampus related to intrinsic hippocampal pathology? Neuroscience 47:843-851.
66. Roberson MR, Harrell LE (1997) Cholinergic activity and amyloid precursor protein metabolism. Brain Res Brain Res Rev 25:50-69.
67. Rossner S, Ueberham U, Yu J, Kirazov L, Schliebs R, Perez-Polo JR, Bigl V (1997) In vivo regulation of amyloid precursor protein secretion in rat neocortex by cholinergic activity. Eur J Neurosci 9:2125-2134.
68. Sassin I, Schultz C, Thal DR, Rub U, Arai K, Braak E, Braak H (2000) Evolution of Alzheimer's disease-related cytoskeletal changes in the basal nucleus of Meynert. Acta Neuropathol (Berl) 100:259-269.
69. Schrader-Fischer G, Paganetti PA (1996) Effect of alkalizing agents on the processing of the beta-amyloid precursor protein. Brain Res 716:91-100.
70. Selkoe DJ (1997) Alzheimer's disease: Genotypes, phenotypes, and treatments. Science 275:630-631.
71. Selkoe DJ (1999) Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399:A23-31.
72. Smith G (1988) Animal models of Alzheimer's disease: Experimental cholinergic denervation. Brain Res 472:103-118.
73. Sofroniew MV, Pearson RC, Eckenstein F, Cuello AC, Powell TP (1983) Retrograde changes in cholinergic neurons in the basal forebrain of the rat following cortical damage. Brain Res 289:370-374.
74. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, Jucker M (1999) Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 154:1673-1684.
75. Stocks EA, McArthur JC, Griffen JW, Mouton PR (1996) An unbiased method for estimation of total epidermal nerve fibre length. J Neurocytol 25:637-644.
76. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Burki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 94:13287-13292.
77. Van Dorpe J, Smeijers L, Dewachter I, Nuyens D, Spittaels K, Van Den Haute C, Mercken M, Moechars D, Laenen I, Kuiperi C, Bruynseels K, Tesseur I, Loos R, Vanderstichele H, Checler F, Sciot R, Van Leuven F (2000) Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the london mutant of human APP in neurons. Am J Pathol 157:1283-1298.
78. Vogels OJ, Broere CA, ter Laak HJ, ten Donkelaar HJ, Nieuwenhuys R, Schulte BP (1990) Cell loss and shrinkage in the nucleus basalis Meynert complex in Alzheimer's disease. Neurobiol Aging 11:3-13.
79. West MJ (1993) New stereological methods for counting neurons. Neurobiol Aging 14:275-285.
80. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
81. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR (1982) Alzheimer's disease and senile dementia: Loss of neurons in the basal forebrain. Science 215:1237-1239.
82. Wilcock GK, Esiri MM, Bowen DM, Smith CC (1982) Alzheimer's disease. Correlation of cortical choline acetyltransferase activity with the severity of dementia and histological abnormalities. J Neurol Sci 57:407-417.
83. Wiltfang J, Smirnov A, Schnierstein B, Kelemen G, Matthies U, Klafki HW, Staufenbiel M, Huther G, Ruther E, Kornhuber J (1997) Improved electrophoretic separation and immunoblotting of beta-amyloid (A beta) peptides 1-40, 1-42, and 1-43. Electrophoresis 18:527-532.
84. Winkler DT, Bondolfi L, Herzig MC, Jann L, Calhoun ME, Wiederhold KH, Tolnay M, Staufenbiel M, Jucker M (2001) Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J Neurosci 21:1619-1627.
85. Winkler J, Suhr ST, Gage FH, Thal LJ, Fisher LJ (1995) Essential role of neocortical acetylcholine in spatial memory. Nature 375:484-487.
86. Wong TP, Debeir T, Duff K, Cuello AC (1999) Reorganization of cholinergic terminals in the cerebral cortex and hippocampus in transgenic mice carrying mutated presenilin-1 and amyloid precursor protein transgenes. J Neurosci 19:2706-2716.
87. Zubenko GS, Moossy J, Martinez AJ, Rao GR, Kopp U, Hanin I (1989) A brain regional analysis of morphologic and cholinergic abnormalities in Alzheimer's disease. Arch Neurol 46:634-638.