The neuroprotective effects of Cerebrolysin™ in a transgenic model of Alzheimer's disease are associated with improved behavioral performance

Journal of Neural Transmission

Volumn 110, Issue 11, 2003, Pages 1313-1327

  Rockenstein, E ^a   Adame, A ^a   Mante, M ^a   Moessler, H ^d   Windisch, M ^c   Masliah, E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JSW Life Sciences GmbH   (Austria)

^d Research Initiative Ebewe   (Austria)

Author keywords

Alzheimer's disease; Amyloid; Apoptosis; Cerebrolysin; Synapses; Transgenic mouse

Indexed keywords

AMYLOID BETA PROTEIN; CEREBROLYSIN; DNA FRAGMENT; SODIUM CHLORIDE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTOSIS; BEHAVIOR; COGNITIVE DEFECT; CONTROLLED STUDY; LEARNING; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE REGENERATION; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TASK PERFORMANCE; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMINO ACIDS; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; APOPTOSIS; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FEMALE; GLIOSIS; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; NEUROPROTECTIVE AGENTS; PRESYNAPTIC TERMINALS; SENILE PLAQUES; TREATMENT OUTCOME;

EID: 0345059236     PISSN: 03009564     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00702-003-0025-7     Document Type: Article

References (52)

1. Alford M, Masliah E, Hansen L, Terry R (1994) A simple dot-immunobinding assay for the quantification of synaptophysin-like immunoreactivity in human brain. J Histochem Cytochem 42: 283-287
2. Arai H, Lee V-Y, Messinger M, Greenberg B, Lowery D, Trojanowski J (1991) Expression patterns of β-amyloid precursor protein (β-APP) in neural and nenneural tissues from Alzheimer's disease and control subjects. Ann Neurol 30: 686-693
3. Bae CY, Cho CY, Cho K, Hoon Oh B, Choi KG, Lee HS, Jung SP, Kim DH, Lee S, Choi GD, Cho H, Lee H (2000) A double-blind, placebo-controlled, multicenter study of Cerebrolysin for Alzheimer's disease. J Am Geriatr Soc 48: 1566-1571
4. Buttini M, Orth M, Bellosta S, Akeefe H, Pitas RE, Wyss-Coray T, Mucke L, Mahley RW (1999) Expression of human apolipoprotein E3 or E4 in the brains of Apoe -/-mice: isoform-specific effects on neurodegeneration. J Neurosci 19: 4867-4880
5. Chartier-Harlin M-C, Crawford F, Houlden H, Warren A, Hughes D, Fidani L, Goate A, Rossor M, Roques P, Hardy J, Mullan M (1991) Early-onset Alzheimer's disease caused by mutations at codon 717 of the β-amyloid precursor protein gene. Nature 353: 844-846
6. Citron M, Diehl T, Capell A, Haass C, Teplow D, Selkoe D (1996) Inhibition of amyloid beta-protein production in neural cells by the serine protease inhibitor AEBSF. Neuron 17: 171-179
7. Clark R, Goate A (1993) Molecular genetics of Alzheimer's disease. Arch Neurol 50: 1164-1172
8. Cole G, Masliah E, Huynh T, DeTeresa R, Terry R, Okudea C, Saitoh T (1989) An antiserum against amyloid β-protein precursor detects a unique peptide in Alzheimer brain. Neurosci Lett 100: 340-346
9. Cras P, Kawai M, Lowery D, Gonzalez-DeWhitt P, Greenberg B, Perry G (1991) Senile plaque neurites in Alzheimer disease accumulate amyloid precursor protein. PNAS USA 88: 7552-7556
10. Eder P, Reinprecht I, Schreiner E, Skofitsch G, Windisch M (2001) Increased density of glutamate receptor subunit 1 due to Cerebrolysin treatment: an immunohistochemical study on aged rats. Histochem J 33: 605-612
11. El-Agnaf O, Mahil D, Patel B, Austen B (2000) Oligomerization and toxicity of beta-amyloid-42 implicated in Alzheimer's disease. Biochem Biophys Res Commun 273: 1003-1007
12. Everall IP, Heaton RK, Marcotte TD, Ellis RJ, McCutchan JA, Atkinson JH, Grant I, Mallory M, Masliah E, Group THNRC (1999) Cortical synaptic density is reduced in mild to moderate human immunodeficiency virus neurocognitive disorder. Brain Pathol 9: 209-217
13. Francis-Turner L, Valouskova V (1996) Nerve growth factor and nootropic drug Cerebrolysin but not fibroblast growth factor can reduce spatial memory impairment elicited by fimbria-fornix transection: short-term study. Neurosci Lett 202: 1-4
14. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemes 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, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyder B, Soriano 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
15. Gavrieli Y, Sherman Y, Ben-Sasson S (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119: 493-501
16. Goate A, Chartier-Harlin M-C, Mullan M, Brown J, Crawford F, Fidani L, Guiffra L, Haynes A, Irving N, James L, Mant R, Newton P, Rooke K, Roques P, Talbot C, Williamson R, Rossor M, Owen M, Hardy J (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349: 704
17. Gschanes A, Windisch M (1999) Early postnatal treatment with peptide preparations influences spatial navigation of young and adult rats. Behav Brain Res 100: 161-166
18. Gschanes A, Boado R, Sametz W, Windisch M (2000) The drug cerebrolysin and its peptide fraction E021 increase the abundance of the blood-brain barrier GLUT1 glucose transporter in brains of young and old rats. Histochem J 32: 71-77
19. Haass C, Lemere CA, Capell A, Citron M, Seubert P, Schenk D, Lannfelt L, Selkoe DJ (1995) The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat Med 1: 1291-1296
20. Hartbauer M, Hutter-Paie B, Windisch M (2001a) Effects of Cerebrolysin on the outgrowth and protection of processes of cultured brain neurons. J Neural Transm 108: 581-592
21. Hartbauer M, Hutter-Paier B, Skofitsch G, Windisch M (2001b) Antiapoptotic effects of the peptidergic drug cerebrolysin on primary cultures of embryonic chick cortical neurons. J Neural Transm 108: 459-473
22. Hsia AY, Masliah E, McConlogue L, Yu G-Q, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96: 3228-3233
23. Klein WL (2002) ADDLs & protofibrils - the missing links? Neurobiol Aging 23: 231-235
24. Knowless RB, Gomez-Isla T, Hyman BT (1998) Abeta associated neuropil changes: correlation with neuronal loss and dementia. JNEN 57: 1122-1130
25. Mallory M, Honer W, Hsu L, Johnson R, Masliah E (1999) In vitro synaptotrophic effects of Cerebrolysin in NT2N cells. Acta Neuropathol 97: 437-446
26. Martin L, Cork L, Koo E, Sisodia S, Weidemann A, Beyreuther K, Masters C, Price D (1989) Localization of amyloid precursor protein (APP) in brains of young and aged monkeys. Soc Neurosci Abstr 15: 23
27. Masliah E, Rockenstein E (2000) Genetically altered transgenic models of Alzheimer's disease. J Neural Transm [Suppl] 59: 175-183
28. Masliah E, Terry R, Alford M, DeTeresa R, Hansen L (1991) Cortical and subcortical patterns of synaptophysin-like immunoreactivity in Alzheimer disease. Am J Pathol 138: 235-246
29. Masliah E, Mallory M, DeTeresa R, Alford M, Hansen L (1993) Differing patterns of aberrant neuronal sprouting in Alzheimer's disease with and without Lewy bodies. Brain Res 617: 258-266
30. Masliah E, Mallory M, Alford M, Tanaka S, Hansen L (1998a) Caspase dependent DNA fragmentation might be associated with excitotoxicity in Alzheimer's disease. J Neuropathol Exp Neurol 57: 1041-1052
31. Masliah E, Raber J, Alford M, Mallory M, Mattson M, Westland C, Mucke L (1998b) Amyloid precursor protein stimulates excitatory amino acid transport: possible involvement in neuroprotective in vivo functions. J Biol Chem 273: 12548-12554
32. Masliah E, Armasolo F, Veinbergs I, Mallory M, Samuel W (1999) Cerebrolysin ameliorates performance deficits and neuronal damage in apolipoprotein E-deficient mice. Pharmacol Biochem Behav 62: 239-245
33. Masliah E, Alford M, Mallory M, Rockenstein E, Moechars D, Van Leuven F (2000) Abnormal glutamate transport function in mutant amyloid precursor protein transgenic mice. Exp Neurol 163: 381-387
34. Mucke L, Masliah E, Johnson W, Ruppe M, Rockenstein E, Forss-Petter S, Pietropaolo M, Mallory M, Abraham C (1994) Synaptotrophic effects of human amyloid β protein precursors in the cortex of transgenic mice. Brain Res 666: 151-167
35. Mucke L, Masliah E, Yu G-Q, Mallory M, Rockenstein E, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L (2000) High-level neuronal expression of Abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20: 4050-4058
36. Muresanu DF, Rainer M, Moessler H (2002) Improved global function and activities of daily living in patients with AD: a placebo-controlled clinical study with the neurotrophic agent Cerebrolysin. J Neural Transm [Suppl]: 277-285
37. Reinprecht I, Gschanes A, Windisch M, Fachbach G (1999) Two peptidergic drugs increase the synaptophysin immunoreactivity in brains of 24-month-old rats. Histochem J 31: 395-401
38. Rockenstein E, McConlogue L, Tan H, Power M, Masliah E, Mucke L (1995) Levels and alternative splicing of amyloid β protein precursor (APP) transcripts in brains of APP transgenic mice and humans with Alzheimer's disease. J Biol Chem 270: 28257-28267
39. Rockenstein E, Mallory M, Mante M, Sisk A, Masliah E (2001) Early formation of mature amyloid-b proteins deposits in a mutant APP transgenic model depends on levels of Ab1-42. J Neurosci Res 66: 573-582
40. Rockenstein E, Mallory M, Mante M, Alford M, Windisch M, Moessler H, Masliah E (2002) Effects of Cerebrolysin on amyloid-beta deposition in a transgenic model of Alzheimer's disease. J Neural Transm [Suppl]: 327-336
41. Rossner S, Ueberham U, Schliebs R, Perez-Polo JR, Bigl V (1998) The regulation of amyloid precursor protein metabolism by cholinergic mechanisms and neurotrophin receptor signaling. Prog Neurobiol 56: 541-569
42. Ruether E, Alvarez XA, Rainer M, Moessler H (2002) Sustained improvement of cognition and global function in patients with moderately severe Alzheimer's disease: a double-blind, placebo-controlled study with the neurotrophic agent Cerebrolysin. J Neural Transm [Suppl]: 265-275
43. Ruther E, Ritter R, Apecechea M, Freytag S, Windisch M (1994a) Efficacy of the peptidergic nootropic drug cerebrolysin in patients with senile dementia of the Alzheimer's type (SDAT). Pharmacopsychiatry 27: 32-40
44. Ruther E, Ritter R, Apecechea M, Freitag S, Windisch M (1994b) Efficacy of Cerebrolysin in Alzheimer's disease. In: Jellinger K, Ladurner G, Windisch M (eds) New trends in the diagnosis and therapy of Alzheimer's disease. Springer, Wien New York, pp 131-141
45. Satou T, Itoh T, Tamai Y, Ohde H, Anderson AJ, Hashimoto S (2000) Neurotrophic effects of FPF-1070 (Cerebrolysin) on cultured neurons from chicken embryo dorsal root ganglia, ciliary ganglia, and sympathetic trunks. J Neural Transm 107: 1253-1262
46. Sisodia S, Koo E, Beyreuther K, Unterbeck A, Price D (1990) Evidence that β-amyloid protein in Alzheimer's disease is not derived by normal processing. Science 248: 492-494
47. Toggas S, Masliah E, Rockenstein E, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367: 188-193
48. Veinbergs I, Mante M, Mallory M, Masliah E (2000) Neurotrophic effects of Cerebrolysin in animal models of excitotoxicity. J Neural Transm [Suppl] 59: 273-280
49. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, Benedek GB, Selkoe DJ, Teplow DB (1999) Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274: 25945-25952
50. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539
51. Windholz E, Gschanes A, Windisch M, Fachbach G (2000) Two peptidergic drugs increase the synaptophysin immunoreactivity in brains of 6-week-old rats. Histochem J 32: 79-84
52. Wronski R, Tompa P, Hutter-Paier B, Crailsheim K, Friedrich P, Windisch M (2000) Inhibitory effect of a brain derived peptide preparation on the Ca++-dependent protease, calpain. J Neural Transm 107: 145-157