Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice

Journal of Neuroscience

Volumn 19, Issue 19, 1999, Pages 8552-8559

  Phinney, Amie L ^a   Deller, Thomas ^b   Stalder, Martina ^a   Calhoun, Michael E ^a   Frotscher, Michael ^b   Sommer, Bernd ^c   Staufenbiel, Matthias ^c   Jucker, Mathias ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF FREIBURG   (Germany)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Agi ng; Alzheirner's disease; APP; Axon; CNS; Entorhinal cortex; Hippocampus; Mouse; Neurodegeneration; PHAL; Sprouting; Synapse; Tracing; Vasculature

Indexed keywords

AMYLOID; AMYLOID PRECURSOR PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ENTORHINAL CORTEX; HISTOLOGY; MOUSE; NERVE ENDING; NERVE SPROUTING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SYNAPSE; TRANSGENIC MOUSE;

EID: 0033215972     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-19-08552.1999     Document Type: Article

References (38)

1. Aigner L, Arber S, Kapfhammer JP, Laux T, Schneider C, Botteri F, Brenner HR, Caroni P (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278.
2. Allen PB, Ouimet CC, Greengard P (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci USA 94:9956-9961.
3. Benowitz LI, Rodriguez WR, Neve RL (1990) The pattern of GAP-43 immunostaining changes in the rat hippocampal formation during reactive synaptogenesis. Brain Res Mol Brain Res 8:17-23.
4. Braak H, Braak E (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol (Berl) 82:239-259.
5. Caceres A, Payne MR, Binder LI, Steward O (1983) Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines. Proc Natl Acad Sci USA 80:1738-1742.
6. Calhoun ME, Wiederhold KH, Abramowski D, Phinney AL, Probst A, Sturchler-Pierrat C, Staufenbiel M, Sommer B, Jucker M (1998) Neuron loss in APP transgenic mice. Nature 395:755-756.
7. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276.
8. Deller T, Martinez A, Nitsch R, Frotscher M (1996) A novel entorhinal projection to the rat dentate gyrus: direct innervation of proximal dendrites and cell bodies of granule cells and GABAergic neurons. J Neurosci 16:3322-3333.
9. Deller T, Drakew A, Frotscher M (1999) Different primary target cells are important for fiber lamination in the fascia dentata: a lesson from reeler mutant mice. Exp Neurol 156:239-253.
10. Donahue JE, Berzin TM, Rafii MS, Glass DJ, Yancopoulos GD, Fallon JR, Stopa EG (1999) Agrin in Alzheimer's disease: altered solubility and abnormal distribution within microvasculature and brain parenchyma. Proc Natl Acad Sci USA 96:6468-6472.
11. Frotscher M, Heimrich B, Deller T (1997) Sprouting in the hippocampus is layer-specific. Trends Neurosci 20:218-223.
12. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Hagopian S, Johnson-Wood K, Khan K, Lee M, Liebowitz P, Lieberburg I, Little S, Masliah E, McConglogue L, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyder B, Sorlano F, Tan H, Vitale J, Wadsworth S, Wolozin B, Zhao J (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 373:523-527.
13. Geddes JW, Monaghan DT, Cotman CW, Lott IT, Kim RC, Chui HC (1985) Plasticity of hippocampal circuitry in Alzheimer's disease. Science 230:1179-1181.
14. Geddes JW, Anderson KJ, Cotman CW (1986) Senile plaques as aberrant sprout-stimulating structures. Exp Neurol 94:767-776.
15. Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 290:219-238.
16. Geula C (1998) Abnormalities of neural circuitry in Alzheimer's disease: hippocampus and cortical cholinergic innervation. Neurology 51:818-29.
17. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaqueindependent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
18. Hsiao K, Chapman P, Nilsen S, Eckman 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.
19. Hyman BT, Van Horsen GW, Damasio AR, Barnes CL (1984) Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225:1168-1170.
20. Jucker M, Walker LC, Schwarb P, Hengemihle J, Kuo H, Snow AD, Bamert F, Ingram DK (1994) Age-related deposition of gliaassociated fibrillar material in brains of C57BL/6 mice. Neuroscience 60:875-889.
21. Jucker M, Stalder M, Tolney M, Wiederhold KH, Abramowski D, Sommer B, Staufenbiel M, Calhoun ME (1998) Cerebral amyloid angiopathy in APP transgenic mice with amyloid plaque formation. Soc Neurosci Abstr 24:1502.
22. Knowles RB, Gomez-Isla T, Hyman BT (1998) Abeta associated neuropil changes: correlation with neuronal loss and dementia. J Neuropathol Exp Neurol 57:1122-1130.
23. Koo EH, Park L, Selkoe DJ (1993) Amyloid β-protein as a substrate interacts with extracellular matrix to promote neurite outgrowth. Proc Natl Acad Sci USA 90:4748-4752.
24. Kowall NW, Kosik KS (1987) Axonal disruption and aberrant localization of tau protein characterize the neuropil pathology of Alzheimer's disease. Ann Neurol 22:639-643.
25. Liu Y, Fujise N, Kosaka T (1996) Distribution of calretinin immunore-activity in the mouse dentate gyrus. I. General description. Exp Brain Res 108:389-403.
26. Masliah E, Hansen L, Albright T, Mallory M, Terry RD (1991a) Immunoelectron microscopic study of synaptic pathology in Alzheimer's disease. Acta Neuropathol (Berl) 81:428-433.
27. Masliah E, Mallory M, Hansen L, Alford M, Albright T, DeTeresa R, Terry R, Baudier J, Saitoh T (1991b) Patterns of aberrant sprouting in Alzheimer's disease. Neuron 6:729-739.
28. Perlmutter LS, Barron E, Saperia D, Chui HC (1991) Association between vascular basement membrane components and the lesions of Alzheimer's disease. J Neurosci Res 30:673-681.
29. Peters A, Palay S, Webster H (1991) The fine structure of the nervous system. New York: Oxford UP.
30. Phinney AL, Calhoun ME, Wolfer DP, Lipp HP, Zheng H, Jucker M (1999) No hippocampal neuron or synaptic bouton loss in learning-impaired aged β-amyloid precursor protein-null mice. Neuroscience 90:1207-1216.
31. Selkoe DJ (1991) The molecular pathology of Alzheimer's disease. Neuron 6:487-498.
32. Snow AD, Mar H, Nochlin D, Kimata K, Kato M, Suzuki S, Hassell J, Wight TN (1988) The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease. Am J Pathol 133:456-463.
33. Stalder M, Phinney AL, 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.
34. Stanfield BB, Caviness Jr VS, Cowan WM (1979) The organization of certain afferents to the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:461-483.
35. 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.
36. Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21:317-323.
37. Wisniewski H, Terry D (1973) Reexamination of the pathogenesis of the senile plaque. In: Progress in neuropathology (Zimmerman H, ed), pp 1-26. New York: Grune and Stratton.
38. Yankner BA (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16:921-932.