Neurotrophic effects of Cerebrolysin in the Mecp2308/Y transgenic model of Rett syndrome

Acta Neuropathologica

Volumn 116, Issue 4, 2008, Pages 425-437

  Doppler, Edith ^a   Rockenstein, Edward ^b   Ubhi, Kiren ^b   Inglis, Chandra ^b   Mante, Michael ^b   Adame, Anthony ^b   Crews, Leslie ^b   Hitzl, Monika ^a   Moessler, Herbert ^a   Masliah, Eliezer ^b  

^a Research Initiative Ebewe   (Austria)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Dendrites; Neurodevelopmental disorders; Neurotrophic peptides

Indexed keywords

CEREBROLYSIN; METHYL CPG BINDING PROTEIN 2;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BEHAVIOR DISORDER; CELL LOSS; CONTROLLED STUDY; DENDRITE; DRUG MECHANISM; HIPPOCAMPUS; MALE; MOTOR PERFORMANCE; MOUSE; MOUSE MUTANT; NEOCORTEX; NERVE CELL LESION; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROPATHY; NEUROTROPISM; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RETT SYNDROME; TRANSGENIC MOUSE; TREATMENT DURATION;

ACETYLATION; AGING; AMINO ACIDS; ANIMALS; DENDRITES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; HISTONES; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, TRANSGENIC; MUTATION; NEOCORTEX; NERVE DEGENERATION; NOOTROPIC AGENTS; RETT SYNDROME; SYNAPSES;

EID: 51849145627     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-008-0407-x     Document Type: Article

References (66)

1. Alvarez XA, Cacabelos R, Laredo M, Couceiro V, Sampedro C, Varela M et al (2006) A 24-week, double-blind, placebo-controlled study of three dosages of Cerebrolysin in patients with mild to moderate Alzheimer's disease. Eur J Neurol 13:43-54. doi: 10.1111/j.1468-1331.2006.01222.x
2. Amir RE, Van den Veyver IB, Schultz R, Malicki DM, Tran CQ, Dahle EJ et al (2000) Influence of mutation type and X chromosome inactivation on Rett syndrome phenotypes. Ann Neurol 47:670-679. doi:10.1002/ 1531-8249(200005)47:5<670::AID-ANA20>3.0.CO;2-F
3. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185-188
4. Armstrong D, Dunn JK, Antalffy B, Trivedi R (1995) Selective dendritic alterations in the cortex of Rett syndrome. J Neuropathol Exp Neurol 54:195-201. doi: 10.1097/00005072-199503000-00006
5. Armstrong DD (2005) Neuropathology of Rett syndrome. J Child Neurol 20:747-753
6. Armstrong DD, Dunn K, Antalffy B (1998) Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. J Neuropathol Exp Neurol 57:1013-1017. doi: 10.1097/ 00005072-199811000-00003
7. Belichenko PV, Hagberg B, Dahlstrom A (1997) Morphological study of neocortical areas in Rett syndrome. Acta Neuropathol 93:50-61. doi: 10.1007/s004010050582
8. Bienvenu T, Carrie A, de Roux N, Vinet MC, Jonveaux P, Couvert P et al (2000) MECP2 mutations account for most cases of typical forms of Rett syndrome. Hum Mol Genet 9:1377-1384. doi: 10.1093/hmg/9.9.1377
9. Chen RZ, Akbarian S, Tudor M, Jaenisch R (2001) Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat Genet 27:327-331. doi: 10.1038/85906
10. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ et al (1997) Abnormal dendritic spines in fragile X knockout mice: Maturation and pruning deficits. Proc Natl Acad Sci USA 94:5401-5404. doi: 10.1073/ pnas.94.10.5401
11. Crawley JN (2000) What's wrong with my mouse? Behavioral phenotyping of transgenic and knockout mice. Wiley, New York
12. Fernagut PO, Diguet E, Jaber M, Bioulac B, Tison F (2002) Dopamine transporter knock-out mice are hypersensitive to 3-nitropropionic acid-induced striatal damage. Eur J NeuroSci 15:2053-2056. doi: 10.1046/ j.1460-9568.2002.02047.x
13. Fleming SM, Salcedo J, Fernagut PO, Rockenstein E, Masliah E, Levine MS et al (2004) Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J Neurosci 24:9434-9440. doi: 10.1523/JNEUROSCI.3080-04.2004
14. 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. doi: 10.1016/0304-3940(95)12240-0
15. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 278:4035-4040. doi: 10.1074/jbc.M210256200
16. Gorbachevskaya N, Bashina V, Gratchev V, Iznak A (2001) Cerebrolysin therapy in Rett syndrome: Clinical and EEG mapping study. Brain Dev 23(Suppl. 1):S90-S93. doi: 10.1016/S0387-7604(01)00349-7
17. Grove EA, Tole S (1999) Patterning events and specification signals in the developing hippocampus. Cereb Cortex 9:551-561. doi: 10.1093/cercor/ 9.6.551
18. 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. doi: 10.1016/S0166-4328(98)00127-2
19. Guy J, Hendrich B, Holmes M, Martin JE, Bird A (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27:322-326. doi: 10.1038/85899
20. Hagberg B (2002) Clinical manifestations and stages of Rett syndrome. Ment Retard Dev Disabil Res Rev 8:61-65. doi: 10.1002/mrdd.10020
21. Haninec P, Dubovy P, Samal F, Houstava L, Stejskal L (2004) Reinnervation of the rat musculocutaneous nerve stump after its direct reconnection with the C5 spinal cord segment by the nerve graft following avulsion of the ventral spinal roots: A comparison of intrathecal administration of brain-derived neurotrophic factor and Cerebrolysin. Exp Brain Res 159:425-432. doi: 10.1007/s00221-004-1969-z
22. Haninec P, Houst'ava L, Stejskal L, Dubovy P (2003) Rescue of rat spinal motoneurons from avulsion-induced cell death by intrathecal administration of IGF-I and Cerebrolysin. Ann Anat 185:233-238. doi: 10.1016/S0940-9602(03)80030-4
23. Hartbauer M, Hutter-Paie B, Windisch M (2001) Effects of Cerebrolysin on the outgrowth and protection of processes of cultured brain neurons. J Neural Transm 108:581-592. doi: 10.1007/s007020170058
24. Hartbauer M, Hutter-Paier B, Skofitsch G, Windisch M (2001) Antiapoptotic effects of the peptidergic drug cerebrolysin on primary cultures of embryonic chick cortical neurons. J Neural Transm 108:459-473. doi: 10.1007/s007020170067
25. Hutter-Paier B, Fruhwirth M, Grygar E, Windisch M (1996) Cerebrolysin protects neurons from ischemia-induced loss of microtubule-associated protein 2. J Neural Transm Suppl 47:276
26. Hutter-Paier B, Steiner E, Windisch M (1998) Cerebrolysin protects isolated cortical neurons from neurodegeneration after brief histotoxic hypoxia. J Neural Transm Suppl 53:351-361
27. Hwang DY, Fleming SM, Ardayfio P, Moran-Gates T, Kim H, Tarazi FI et al (2005) 3, 4-dihydroxyphenylalanine reverses the motor deficits in Pitx3-deficient aphakia mice: Behavioral characterization of a novel genetic model of Parkinson's disease. J Neurosci 25:2132-2137. doi: 10.1523/JNEUROSCI.3718-04.2005
28. Jellinger KA (2003) Rett syndrome - an update. J Neural Transm 110:681-701. doi: 10.1007/s00702-003-0822-z
29. Kaufmann WE, Naidu S, Budden S (1995) Abnormal expression of microtubule-associated protein 2 (MAP-2) in neocortex in Rett syndrome. Neuropediatrics 26:109-113
30. Kaufmann WE, Taylor CV, Hohmann CF, Sanwal IB, Naidu S (1997) Abnormalities in neuronal maturation in Rett syndrome neocortex: preliminary molecular correlates. Eur Child Adolesc Psychiatry 6(Suppl. 1):75-77
31. Kerr AM (1995) Early clinical signs in the Rett disorder. Neuropediatrics 26:67-71
32. Kuczenski R, Everall IP, Crews L, Adame A, Grant I, Masliah E (2007) Escalating dose-multiple binge methamphetamine exposure results in degeneration of the neocortex and limbic system in the rat. Exp Neurol 207:42-51. doi: 10.1016/j.expneurol.2007.05.023
33. Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F et al (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69:905-914. doi: 10.1016/0092-8674(92)90610-O
34. Mallory M, Honer W, Hsu L, Johnson R, Rockenstein E, Masliah E (1999) In vitro synaptotrophic effects of Cerebrolysin in NT2 N cells. Acta Neuropathol 97:437-446. doi: 10.1007/s004010051012
35. 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. doi: 10.1016/S0091-3057(98)00144-0
36. Matsuura K, Kabuto H, Makino H, Ogawa N (1997) Pole test is a useful method for evaluating the mouse movement disorder caused by striatal dopamine depletion. J Neurosci Methods 73:45-48. doi: 10.1016/ S0165-0270(96)02211-X
37. Miller S, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215. doi: 10.1093/nar/16.3.1215
38. Moretti P, Bouwknecht JA, Teague R, Paylor R, Zoghbi HY (2005) Abnormalities of social interactions and home-cage behavior in a mouse model of Rett syndrome. Hum Mol Genet 14:205-220. doi: 10.1093/hmg/ddi016
39. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B et al (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26:319-327. doi: 10.1523/ JNEUROSCI.2623-05.2006
40. Muresanu DF, Alvarez XA, Moessler H, Buia M, Stan A, Pintea D et al (2008) A pilot study to evaluate the effects of Cerebrolysin on cognition and qEEG in vascular dementia: Cognitive improvement correlates with qEEG acceleration. J Neurol Sci 267:112-119. doi: 10.1016/j.jns.2007.10.016
41. Nan X, Campoy FJ, Bird A (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88:471-481. doi: 10.1016/S0092-8674(00)81887-5
42. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN et al (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389. doi: 10.1038/30764
43. Nan X, Tate P, Li E, Bird A (1996) DNA methylation specifies chromosomal localization of MeCP2. Mol Cell Biol 16:414-421
44. Nomura Y, Segawa M, Higurashi M (1985) Rett syndrome - an early catecholamine and indolamine deficient disorder? Brain Dev 7:334-341
45. Ogawa N, Hirose Y, Ohara S, Ono T, Watanabe Y (1985) A simple quantitative bradykinesia test in MPTP-treated mice. Res Commun Chem Pathol Pharmacol 50:435-441
46. Ogawa N, Mizukawa K, Hirose Y, Kajita S, Ohara S, Watanabe Y (1987) MPTP-induced parkinsonian model in mice: Biochemistry, pharmacology and behavior. Eur Neurol 26(Suppl. 1):16-23. doi: 10.1159/000116351
47. Percy AK, Zoghbi HY, Glaze DG (1987) Rett syndrome: Discrimination of typical and variant forms. Brain Dev 9:458-461
48. Poliakov GI (1961) Some results of research into the development of the neuronal structure of the cortical ends of the analyzers in man. J Comp Neurol 117:197-212. doi: 10.1002/cne.901170206
49. 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. doi: 10.1023/A:1003752208971
50. Rockenstein E, Adame A, Mante M, Moessler H, Windisch M, Masliah E (2003) The neuroprotective effects of Cerebrolysin trade mark in a transgenic model of Alzheimer's disease are associated with improved behavioral performance. J Neural Transm 110:1313-1327. doi: 10.1007/ s00702-003-0025-7
51. Rockenstein E, Mallory M, Mante M, Alford M, Windisch M, Moessler H, et al (2002) Effects of Cerebrolysin on amyloid-beta deposition in a transgenic model of Alzheimer's disease. J Neural Transm Suppl 62:327-336
52. Rockenstein E, Mante M, Adame A, Crews L, Moessler H, Masliah E (2007) Effects of Cerebrolysintrade mark on neurogenesis in an APP transgenic model of Alzheimer's disease. Acta Neuropathol 113:265-275. doi: 10.1007/ s00401-006-0166-5
53. Rockenstein E, Torrance M, Mante M, Adame A, Paulino A, Rose JB et al (2006) Cerebrolysin decreases amyloid-beta production by regulating amyloid protein precursor maturation in a transgenic model of Alzheimer's disease. J Neurosci Res 83:1252-1261. doi: 10.1002/jnr.20818
54. Rockenstein E, Torrance M, Mante M, Adame A, Paulino A, Rose JB, Crews L, Moessler H, Masliah E (2006) Cerebrolysin decreases amyloid-beta production by regulating amyloid protein precursor maturation in a transgenic model of Alzheimer's disease. J Neurosci Res 83(7):1252-61.
55. 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. doi: 10.1007/s007020070015
56. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J et al (2002) Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35:243-254. doi: 10.1016/S0896-6273(02)00768-7
57. Shahbazian MD, Zoghbi HY (2002) Rett syndrome and MeCP2: Linking epigenetics and neuronal function. Am J Hum Genet 71:1259-1272. doi: 10.1086/345360
58. Stearns NA, Schaevitz LR, Bowling H, Nag N, Berger UV, Berger-Sweeney J (2007) Behavioral and anatomical abnormalities in Mecp2 mutant mice: A model for Rett syndrome. Neuroscience 146:907-921. doi: 10.1016/ j.neuroscience.2007.02.009
59. Takashima S, Ieshima A, Nakamura H, Becker LE (1989) Dendrites, dementia and the Down syndrome. Brain Dev 11:131-133
60. Tole S, Christian C, Grove EA (1997) Early specification and autonomous development of cortical fields in the mouse hippocampus. Development 124:4959-4970
61. Villard L, Kpebe A, Cardoso C, Chelly PJ, Tardieu PM, Fontes M (2000) Two affected boys in a Rett syndrome family: Clinical and molecular findings. Neurology 55:1188-1193
62. Wan M, Lee SS, Zhang X, Houwink-Manville I, Song HR, Amir RE et al (1999) Rett syndrome and beyond: Recurrent spontaneous and familial MECP2 mutations at CpG hotspots. Am J Hum Genet 65:1520-1529. doi: 10.1086/302690
63. Wei ZH, He QB, Wang H, Su BH, Chen HZ (2007) Meta-analysis: The efficacy of nootropic agent Cerebrolysin in the treatment of Alzheimer's disease. J Neural Transm 114:629-634. doi: 10.1007/s00702-007-0630-y
64. 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. doi: 10.1023/A:1004053809591
65. Wronski R, Kronawetter S, Hutter-Paier B, Crailsheim K, Windisch M (2000) A brain derived peptide preparation reduces the translation dependent loss of a cytoskeletal protein in primary cultured chicken neurons. J Neural Transm Suppl 59:263-272
66. Young JI, Zoghbi HY (2004) X-chromosome inactivation patterns are unbalanced and affect the phenotypic outcome in a mouse model of rett syndrome. Am J Hum Genet 74:511-520. doi: 10.1086/382228